Evolutionary Anthropology 20:131–142 (2011)

ARTICLES

Female Contributions to the Peaceful Nature of Bonobo

TAKESHI FURUICHI

Although ( troglodytes)andbonobos(Pan paniscus)areclosely panzees.6,10 However, in a recent related, females of the two show surprisingly large differences in many behav- comparative study using data avail- ioral aspects. While female chimpanzees tend to range alone or in small parties during able from various study sites and non-estrous periods, female bonobos aggregate even more often than do males. groups, I showed that there is con- Female chimpanzees do not have frequent social interactions with other females, siderable within-species variation in whereas female bonobos maintain close social associations with one another. party size and that there is no signifi- Although the ranging patterns of parties are generally led by males, cant difference between the two spe- female bonobos often take the initiative in ranging behavior. While female chimpan- cies.11 On the other hand, this study zees usually do not exhibit estrus during postpartum amenorrhea or pregnancy, also confirmed that there is a signifi- female bonobos exhibit a prolonged pseudo-estrus during such non-conceptive peri- cant difference between these species ods. Studies of these two species have also shown great differences in agonistic in the average number of individuals behaviors performed by males. Male chimpanzees frequently fight with other males to in a party relative to the total num- compete for estrous females, but male bonobos seldom do so. While there are many ber of individuals belonging to the records of infanticide by male chimpanzees, there is no confirmed record of such an group. This proportional measure is event among bonobos. Several cases of within-group killing among adult male chim- called the relative party size12 or the panzees have been reported, but there is no such record for bonobos. While inter- attendance ratio.13 Boesch showed group conflicts among chimpanzees sometimes involve killing members of the other that the relative party size was larger group, intergroup conflicts among bonobos are considerably more moderate. In some for bonobos than for chimpanzees.12 cases, bonobos from two different groups may even range together for several days I showed the same pattern highlight- while engaging in various peaceful interactions. I will address two important questions ing a significant difference in the two that arise from these comparisons, exploring why females of such closely related spe- species’ attendance ratios (27% to cies show such clear differences in behavior and whether or not the behavioral char- 51% for bonobos versus 9% to 30% acteristics of female bonobos contribute to the peaceful nature of bonobo society. for chimpanzees).11 Figure 1 illustrates these differen- The social systems of both chim- social groups, called unit groups or ces by comparing group and party panzees and bonobos are character- communities, are semi-closed and sizes between the E1 group of bono- ized by fission and fusion. Their have fairly stable membership, bos at Wamba, in the Luo Scientific except for the transfer of females Reserve, Democratic Republic of the between unit groups.1–4 Within these , and the M group of chimpan- Takeshi Furuichi’s research interests groups, however, character- zees in Kalinzu, Uganda. In both include the sexual behaviors, life histories, studies, we followed the largest par- and ecological adaptations of great , istically split into smaller subgroups with the ultimate goal of understanding or parties, in which memberships ties that we could observe at the the processes involved in hominoid evolu- flexibly change over time.1,4–9 In this time, using the same 1-hour-party tion. He conducts long-term field research on bonobos at Wamba in the Luo Scien- review, I refer to a unit group or method developed for the compari- tific Reserve, Democratic Republic of the community as a group and to a tem- son of party sizes and compositions 14 Congo, and chimpanzees in the Kalinzu porary association of group members across different species and sites. Forest Central Reserve, Uganda. E-mail: [email protected] as a party. As noted, the total numbers of indi- viduals in 1-hour parties were not significantly different between the Key words: Pan paniscus; prolonged estrus; sex- GROUPING PATTERNS AND two species. However, while almost ual behavior; female dominance; mother-son rela- FEMALE INITIATIVE IN half of the group members were tionship DETERMINING RANGING found in the 1-hour parties of bono- bos, a smaller proportion of mem- VC 2011 Wiley-Liss, Inc. Early studies on the ecology of bers were found in those of chim- DOI 10.1002/evan.20308 Published online in Wiley Online Library bonobos suggested that their party panzees. In particular, there is a (wileyonlinelibrary.com). sizes were larger than those of chim- marked between-species difference in 132 Furuichi ARTICLES

Various hypotheses have been offered to explain the tendency of female chimpanzees to range alone or in small parties.17–21 For example, in a food patch females may be sub- ject to larger costs from contest com- petition than are males due to their lower dominance status. in a larger party may increase the fre- quency of shifts between food patches and thus impose larger costs from scramble competition on females because their lower velocity leads to longer travel times between, and late arrival to, food patches and feeding sites. If these hypotheses are true, then females may avoid large parties in favor of small ones, as was shown for chimpanzees in Kibale, Uganda.19 This prediction, however, Figure 1. Comparisons of party size and composition in the M group of chimpanzees in was not verified in bonobos, among Kalinzu and the E1 group of bonobos at Wamba. We recorded individuals observed in which the attendance ratio of each 1-hour period while following a party, which approximates the number of individu- als ranging and feeding together. The length of bars with solid lines represents the aver- females was always higher than that age number of individuals found in the 1-hour party; the length of bars with dotted lines of males, irrespective of party size represents the number of all individuals belonging to the unit-group. See Hashimoto, Fur- (Fig. 2). This suggests that the rela- uichi, and Tashino14 and Mulavwa and colleagues91 for more details. tionship between social grouping and food supply may differ for bono- bos and chimpanzees. For example, female attendance ratio, with less our study was interrupted by politi- bonobos often forage on the abun- than one-tenth of the female chim- cal instability, we occasionally provi- dant terrestrial herbs, fruits, and panzees, but almost two-thirds of the sioned the bonobos, either at sleep- young leaves of small but widely dis- female bonobos, found in parties. ing sites or at a permanent provi- tributed trees as they travel between Although the term ‘‘fission-fusion’’ sioning site. During this period, we large fruit trees; this may lower the is usually used to describe the group- observed an average of 88.9% of traveling speeds of parties and thus ing patterns of both chimpanzees adult or adolescent females and reduce the costs that females incur and bonobos, the species differ sub- 87.6% of adult or adolescent males.9 by attending large parties. Alterna- stantially in their cohesiveness. As Since 2003, in studies of the same tively, female bonobos may want to seen in an example from Mahale, group under completely natural con- attend large parties for social rea- Tanzania,15 fission and fusion of par- ditions, all group members were sons, regardless of the increased ties occurs frequently among chim- present on many observation days, feeding costs they may incur. As I panzees. Because different parties especially during the high-fruiting will discuss later, females may be may range in distant areas, only season. For example, during the 12 able to increase their social status rarely can a researcher observe all months of 2008, all of the adult relative to males by aggregating with members of the group within the group members were observed on 35 other females or they may want to same day.16 In Kalinzu, where we of the 124 days on which parties of range with their sons to support their have studied chimpanzees since the study group were observed from attempts to acquire higher dominance 1992, several years elapsed between sleeping site to sleeping site. Eighty- rank or reproductive success. observations of certain females that three percent (S.D. ¼ 27%, median ¼ Although it is not yet supported by usually ranged in the periphery of 100%) of adult females, and 79% quantitative data, female bonobos the home range. Most likely these (S.D. ¼ 26%, median ¼ 28%) of adult appear to be able to determine rang- females were not observed during males were observed during each of ing activity, which seems in part re- pregnancy or lactation periods the 124 days (Sakamaki and co- sponsible for the cohesive grouping. because they were primarily ranging workers, unpublished data). Although At Wamba, party movements typi- with their dependent infants and bonobos split into several parties dur- cally occur when members descend juveniles, apart from other members ing the day, group members range in from a tall fruit tree and take a short of the group (Hashimoto and Furui- adjacent areas and travel in a similar break on lower trees, observing one chi, unpublished data). direction, exchanging vocalizations, another. Some of the males climb In contrast, most members of the so that many of them appeared at down and perform branch-dragging bonobo group at Wamba can be least once a day in the party we were behavior while running on the observed daily. Before 1996, when following. ground, seemingly to propose a ARTICLES Female contributions to bonobo 133

CLOSE SOCIAL ASSOCIATIONS AMONG FEMALES

Female bonobos do not merely ag- gregate, but form close social associa- tions with one another. This is another important difference between female bonobos and female chimpan- zees, which do not frequently have affiliative relationships.24 Bonobos form male-philopatric groups.10,25,26 Throughout our stud- ies at Wamba, immigration of males occurred only during or following a single period of war in D. R. Congo Figure 2. Attendance ratios of males and females of the E1 group of bonobos at between 1996 and 2002, when neigh- Wamba. Each dot shows the daily mean attendance ratio, which is the mean probability boring groups of the main study with which each male or female was observed in a 1-hour party. The x axis is the daily group, E1, disappeared. Presumably, mean 1-hour party size. The attendance ratio of females exceeded 1 on three days the remnants of those groups were because one unknown female temporarily joined the party of the study group. See integrated into the study group.27 Mulavwa and colleagues91 for details. Otherwise, there have been no cases 27–29 direction of movement. However, the instead wait for other group members of immigration by males. Hoh- 30 entire party does not move until the to arrive. When the others do arrive, mann and Fruth also reported a dominant females climb down and they produce a chorus of soft vocal- case of immigration by adult males initiate movement in a direction of izations and climb up the tree to- into the study group in Lomako, but their own choice. Even when males gether (Sakamaki, personal communi- these are the only such cases go off alone to explore distant areas cation). Chimpanzees in Kalinzu reported from any of the sites where of their home range, they usually sometimes give loud calls to attract bonobos have been observed fre- return by the evening and rejoin the other group members to feeding trees, quently enough to permit individual females if the latter did not follow but they never wait for other mem- identification (Wamba, Lomako, and them (Furuichi, personal observa- bers to arrive before climbing them. Lui Kotale in D.R. Congo). tion). By directing a party’s move- The two species also exhibit differ- As for females, all of those con- ment patterns, females can determine ent behavioral tendencies at nightfall. firmedtobeborninthestudygroup the ranging rate, length of each leg, When bonobos prepare to stop for the at Wamba disappeared by the age of and day range. This makes it easier night, parties traveling separately but 10 years. If we exclude those that died for females to attend large mixed-sex in the same vicinity start calling to before reaching 2 years of age, the parties because they may be able to oneanother.Wecallthesevocaliza- others all disappeared between the 6 reduce the feeding costs that result tions ‘‘sunset calls.’’ In Kalinzu, I ages of 6 and 10 years. These females from their lower velocities. rarely hear such calls in the evening were assumed to have emigrated, Several other behaviors typical of among chimpanzees. Bonobo parties rather than to have died, because both male and female bonobos also sometimes approach one another, their health conditions were normal appear to enhance the cohesive group- exchanging sunset calls, and begin to before their disappearance. On the ing observed in this species although, make nests after they join. This hap- other hand, all females from other again, these behaviors have yet to be pens most frequently during the high- groups that joined the study group quantitatively examined. In some fruiting season. Bonobos usually for- did so at estimated ages of between 6 cases, when traveling long distances age in large parties during the day or 7 and 14 years. Interestingly, all and aggregate to form even larger par- between different areas in their home females below the age of 10 years that ties in the evening; the next morning, range, bonobos split into two or more immigrated into the study group dis- they again split into several parties to parties, one going ahead and the appeared after a few days to several forage.22 In Kalinzu, there is no tend- others remaining behind. In such months. In contrast, most females ency for chimpanzees to sleep in par- cases, the parties frequently exchange that immigrated into the study group ties larger than those formed during at estimated ages of 10 years or older vocalizations, and some bonobos in the daytime. In Budongo, Uganda, the lead party will sit on the ground party size tends to drop decisively in eventually had offspring and settled and look back, awaiting the arrival of the evening before nest-building into the group permanently. It seems those left behind (Furuichi, personal time.23 Taken together, such behaviors that young adolescent females who observation). I rarely observed such seem to show that bonobos are highly have left their natal groups move from ‘‘waiting’’ behavior among chimpan- motivated to range together to the group to group before settling into a zees in Kalinzu. Similarly, when bono- extent that circumstances permit, and final group.27–29 bos arrive at a big fruiting tree, rather that females play an influential role in While most female bonobos that than climbing up immediately, they the maintenance of group cohesion. immigrate into new groups during 134 Furuichi ARTICLES

exhibit limited periods of sexual re- ceptivity during the peri-ovulatory phase of the ovarian cycle, which I call the ‘‘estrus period’’.36,38 A female in estrus has a fully tumescent ; periods of sexual attractiv- ity and proceptivity, as well as recep- tivity, generally coincide with maxi- mal tumescence of the sexual skin.39 On the other hand, adult female bonobos perform similar sexual behaviors and show maximal tumes- cence even during nonconceptive periods, which I call ‘‘pseudo-estrus’’. Chimpanzees do not exhibit estrus during their long postpartum amen- orrhea, which here represents the pe- riod between parturition and resumption of cyclic estrus. How- ever, bonobos resume cyclic estrus much earlier, although the time between parturition and next concep- tion does not differ much between the two species.37 Also, although chimpanzees cease to exhibit estrus within a few cycles postconception, bonobos continue to exhibit estrus until the late stages of pregnancy. Although the physiological mecha- nism for this pseudo-estrus is not yet understood, it certainly contributes to a female’s coexistence in the group and to the control of male . Figure 3. Estrus periods among chimpanzees and bonobos. Because there is no informa- Figure 3 diagrams these differen- tion on the timing with which bonobos resume fertile estrus, I assumed that they have the ces in the estrus periods between same interval between resumption of fertile estrus and conception as do chimpanzees. chimpanzees and bonobos using data mainly from Mahale and Wamba, adolescence experience estrus and seem to be aimed at getting food with supplementary data from ani- copulate with males, several years because it occurs even when food is mals in captivity. Female chimpan- typically will elapse before they give available elsewhere. The real intent zees experience estrus for 12.5 days birth at approximately 13 to 15 years appears to be the social interaction before ovulation in a cycle of 31.5 of age.31 These females tend to have gained with these senior females. days.40 Although female bonobos frequent social interactions with Through these various interactions, sometimes show continuous estrus other females that immigrated dur- immigrant females establish social throughout the menstrual cycle, they ing the same period or with senior bonds with senior females and also typically show estrus for 14.6 females already established in the bonobo females on the whole form days in a cycle of 42 days.9 Thus, the group, particularly ‘‘specific senior tight associations. Although many proportion of days spent in estrus females’’ who are old and high in are unrelated, their tight associations during a menstrual cycle does not rank.32,33 Immigrant females are seem to improve their status in a substantially differ between the two selective in their choice of specific male-philopatric group. species. On the other hand, there are females to associate with, following significant differences in estrus peri- them as if following their mothers PROLONGED PSEUDO-ESTRUS ods during an interbirth interval. and frequently soliciting them to Female chimpanzees do not show engage in species-typical ‘‘genito-gen- Another conspicuous characteristic estrus during postpartum amenor- ital rubbing’’ behavior.10 They also of female bonobos is their prolonged rhea and resume cyclic estrus at 55.5 direct ‘‘peering’’ behavior32 toward pseudo-estrus periods.9,10,34–37 Like months after parturition, conceiving these senior females when they are females of many , adult 8.9 months thereafter.41 Visible signs feeding and even beg for food from female chimpanzees, except those of estrus cease 2.6 months postcon- their mouths. This behavior does not during adolescent sterility, usually ception42 during the 7.6 months of ARTICLES Female contributions to bonobo societies 135

TABLE 1. Estrus Sex Ratio of Chimpanzees and Bonobos bonobos. In Gombe, where there are Chimpanzee Chimpanzee Bonobo closer numbers of males and (Mahale) (Gombe) (Wamba) females, the estrus sex ratio is much higher than that of Wamba bonobos. Proportion of a cycling period 0.16 0.11 0.77 Although it ignores substantial during an interbirth intervala Proportion of days in estrus during 0.40 0.38 0.35 between-group and temporal varia- a mestrual cycleb tion, Figure 4 illustrates the general Proportion of days in estrus during 0.064 0.042 0.27 differences in the sexual relations of an interbirth interval (a*b)c chimpanzees and bonobos, using the Adult sex ratio (#adult males/#adult 0.27 0.51 0.75 number of adult chimpanzees in females)d Mahale M group in 198441 and the Estrus sex ratio (# adult males/# adult 4.2 12.3 2.8 number of adult bonobos and the females showing estrus) (d/c) number of estrous adult females in the Wamba E1 group in 1987–88.37 If we use the estimated proportion of pregnancy.43 Therefore, female chim- 0.77, or about 5 to 7 times larger. If days in estrus, only 2.2 of 35 female panzees are in estrus for only 12.5 we multiply these figures by the pro- chimpanzees, on average, are days per cycle over the course of portion of days on which females are expected to show estrus at a given 11.5 months during an interbirth in estrus during each menstrual cycle time, while 10 adult males compete interval of 6 years.41 In contrast, (0.4 and 0.38, respectively for Mahale for access to these females (Fig. 4, female bonobos resume estrus 1 year and Gombe chimpanzees, 0.35 for top). Although the proportions vary after parturition.10 Although no in- Wamba bonobos), the proportions of for different groups and study sites, formation about the timing at which days in estrus during interbirth inter- chimpanzee mating behaviors female bonobos resume fertile estrus, vals becomes 0.064 for Mahale chim- include possessive mating by high- judging from the timing of subse- panzees and 0.042 for Gombe chim- ranking males, opportunistic and quent conception they apparently panzees, while the proportion for promiscuous mating, and mating remain infertile during this period. Wamba bonobos is 0.27 days. This during consortships.1,23,36,40,46–53 In Therefore, this is a pseudo-estrus means that female chimpanzees many groups, the alpha males and/or without possibility of conception. show estrus on only about 5% of the males allied with them may have pri- Female bonobos also show pseudo- days in their adult lives, or that, on ority in mating access, so that estrus during pregnancy until about average, only 1 out of 20 females females cannot usually refuse their 1 month before parturition.10 Thus, shows estrus at any given time. In attempts. During oppor- the total time that female bonobos contrast, female bonobos show tunistic mating, females are some- show estrus during an interbirth estrus for as much as 27% of their times severely attacked by males that interval of 57.6 months28 is much adult lives, so that at any given time attempt copulations.51 Thus, copula- longer than that for female chimpan- 1 of every 4 females is in estrus. In tions are, to a large extent, influ- zees. reality, however, the actual differ- enced by power games among males, This difference in female receptiv- ence is somewhat moderated by the with female choice of mating part- ity between species may have impor- lower adult sex ratio in chimpanzee ners being limited. tant implications with regard to the groups. Although this itself may be a Among bonobos, in contrast, intensity of sexual competition result of the severe intermale compe- although there were only 9 females within groups. To test this hypothe- tition and resultant killing of infant in the group, a greater number of sis, I compared the estrus sex ratio or adult males, the ratios of the females (3.1 on average) showed (or operational sex ratio) between numbers of adult male chimpanzees estrus at any given time (Fig. 4, the two species. The estrus sex ratio to that of adult females at Mahale bottom).37 In such situations, it is is defined as the ratio of the number and Gombe were as low as 0.27 and difficult for an alpha male to monop- of adult males to the number of 0.51, respectively, during the study olize all estrous females. Therefore adult females showing estrus at a periods. If we take this adult sex ra- other males may be able to approach given time. We estimated the estrus tio into account, the estimated estrus estrous females and solicit them for sex ratio for chimpanzees in Mahale sex ratio becomes 4.2 for Mahale copulation more freely than can and Gombe, and for bonobos at chimpanzees and 12.3 for Gombe male chimpanzees.10,54,55 Copula- Wamba, using published reproduc- chimpanzees. On the other hand, tions are not frequently disturbed by tive data7,9,10,28,37,40–45 (Table 1; see Wamba bonobos have the highest ra- other males at Wamba, although Furuichi and Hashimoto37 for more tio of adult males to adult females intermale aggression is known to be details). (0.75), but the estrus sex ratio is still more frequently observed in the mat- The proportions of cycling periods estimated to be as low as 2.8. There- ing context at Lomako56 and Lui that occur during interbirth intervals fore, even for the Mahale chimpan- Kotale.57 Under such circumstances, are 0.16 and 0.11 for Mahale and zees, where the number of adult the most important thing for males Gombe chimpanzees, respectively; males is less, the estrus sex ratio is is not to dominate other males, but for Wamba bonobos, this figure is still higher than that among Wamba rather to be preferred by females as 136 Furuichi ARTICLES

Figure 4. Sexual relations among chimpanzees and bonobos. Females are drawn in upper parts, males in lower parts. Dark colors show estrous females and alpha males. Arrows show the solicitation or acceptance of copulations.

copulation partners. This may be over males where feeding is con- riphery of the feeding site until why males rarely attack or attempt cerned. Unfortunately, we have only a females finished eating. When overt to sexually coerce females. Females few reports on the frequency of agonis- conflict occurred at feeding sites, allied can easily ignore solicitations by tic interactions between males and females sometimes chased males, but alpha males, and the occurrence of females in wild bonobo populations. males never formed aggressive alli- copulation largely depends on In a study that I did on the E1 group ances against females. It is interesting whether females accept a male’s so- over a 7–month period (528 hr and 56 to note that even the alpha male might licitation.10,54–56,58 Thus, with pro- min over 97 days), males were domi- retreat when approached by middle- longed estrus, females can reduce nant over females in 27 cases, while or low-ranking females. At Lomako, both excessive sexual competition females were dominant over males in males were dominant over females in among and harassment by males. 25 agonistic interactions, showing all 11 cases of dyadic agonistic interac- that males and females had relatively tions between adults and subadults for equal status.58 Most of the male- which dominance between the partici- HIGH SOCIAL STATUS OF dominant cases involved display be- pants was decided. However, females FEMALES haviors in which males ran around had priority of access to food in terms emitting excited vocalizations, drag- of the order in which individuals If females aggregate in the central ging branches, and dashing toward entered food patches.59 Another study part of a mixed-sex party, form close females. Females fled from these at Lomako showed that the frequency social associations, and are active in males, but such behaviors rarely of female aggression against males mate choice, one naturally assumes involved physical attacks. On the other was more than double that of male that they have high social status. This hand, most of the female-dominant aggression against females, opposite assumption is true, but the question interactions represented retreats by to the study at the same site men- of whether their social status is equal males following approaches by fe- tioned earlier.56 to that of males, or whether they are males. Some of the cases occurred in On the other hand, many reports actually dominant over males, feeding situations. For example, when show that female bonobos are domi- remains. This has been a controver- females approached males who were nant over males in captivity.60–63 In a sial topic for quite some time. feeding in a preferred position at a comparative study of various captive In the wild, dominance between feeding site, males yielded their posi- populations, Stevens and colleagues64 males and females is equal or equivo- tions to late-arriving females. Further- showed that the linearity and steepness cal, but females seem to be dominant more, males usually waited at the pe- of dominance vary among captive pop- ARTICLES Female contributions to bonobo societies 137

TEN behaved as the alpha female and the alpha male. Agonistic inter- actions between these two families became infrequent (Fig. 6). It seemed that this entire series of incidents was triggered by the chal- lenge of TEN, but he could take the alpha position only when his mother overtook the mother of the previous alpha male and became alpha female. Indeed, SEN was very supportive of her sons. After TEN took the alpha-male position, she persistently supported her 7-year-old second-youngest son. He Figure 5. Alpha females and alpha males in each study period. Lines show the mother- sometimes behaved dominantly over son relationships. Asterisks show that those females did not have adult or adolescent sons adults in the group, and SEN threat- during the periods of their alpha-female status. ened them when they resisted. When we resumed our study in ulations, and that female dominance is sons, mothers can behave quite 1994, after a 2-year break caused by not exclusive, which means that not all aggressively, as we observed in the political unrest, SEN had died and females are dominant over all males. changes of the alpha female and the the second-ranking female, HALU, However, they also showed that the alpha male in 1983–84 (Fig. 5).58,72 had become the alpha female. highest ranking individuals were By 1983, when I started my study, Because HALU’s eldest son had died females and the lowest-ranking individ- the oldest female, KAME, was the a few years earlier, she had no adult uals were males in all of the popula- alpha female; her oldest son, IBO, or adolescent son. Thus, TEN contin- tions studied. Thus, there really does was the alpha male. KAME had two ued to be the alpha male. However, appear to be a difference in this respect other younger sons, and they always HALU was apparently dominant over between the social tendencies of wild kept close associations. However, TEN, so that the highest ranking and captive bonobos. TEN, an adolescent son of the second- individual in the E1 group during As noted earlier, females can ranking female, SEN, approached the this period was a female. express dominance in situations age of adulthood and began display- Our research was again interrupted involving competition for food. Even ing at KAME’s three sons. IBO did not by a civil war in 1996. When we when feeding on hunted animals, show submissive behaviors and, at resumed our study in 2002, HALU was which are a rare and valuable food the end of many such interactions, not in the group, and was presumed to resource, females in many cases instead mounted TEN. However, he be dead. Although NAO had become maintained possession of the kill,65–68 sometimes left the area to avoid the the alpha female, she also had no adult although among chimpanzees males persistent provocations of the or adolescent son to become alpha typically monopolize such resour- younger TEN. male.Instead,TAWASHI,thethirdson ces.69–71 Therefore, the higher status When males are involved in ago- of the deceased ex-alpha female, of females in captivity might be nistic interactions, mothers some- KAME, was in the alpha male position. explained by the fact that competition times join to support their sons. In the 2008 study period, we found over food occurs more frequently in However, KAME, who was both that KIKU, who had been the second- captivity. However, this will need to pregnant and aged, rarely intervened. ranking female, was the alpha female, be tested through further study of In contrast, SEN sometimes attacked though we do not know when the wild populations. KAME’s sons to support TEN. On rank reversal occurred. During this one occasion, IBO fled from SEN af- period, a young adult male, NOBITA, ter an intense physical fight. A fight became the alpha male. When we INFLUENCE OF MOTHERS ON THE between the two mothers occurred resumed our study in 2002, we had SOCIAL STATUS OF ADULT MALES five days later, with SEN being the tentatively given all adolescent males victor. After this, fights between new names because it was difficult to Interestingly, female bonobos ag- these females occurred several times, confirm the identity of immature gregate, maintain close social associ- but KAME never defeated SEN. Five males after a 6-year break. However, ations, and control social relation- days later, TEN approached IBO, DNA analyses confirmed that ships in the group, but they usually emitting display vocalizations, as NOBITA was identical to KIKUO, the do not behave politically or forge tac- was usual at the time. At first IBO first son born to KIKU.27 Therefore, it tical alliances in the manner of male stood bipedally to fight TEN, but appears that another mother-son pair chimpanzees. However, there is one then turned his back to present his became the alpha female and male. important exception to this general- rump instead, at which point the two Thus, throughout our study of E1 ization: given the chance to raise the males performed rump-rump con- group, which began in 1976, 5 prime or status of their adult or adolescent tact.73 From that time on, SEN and old adult females took the alpha-female 138 Furuichi ARTICLES

Kotale frequently intervened in the mating attempts of unrelated males or provided their sons with agonistic sup- port when unrelated males tried to interfere with their sons’ mating activ- ities. As a result, middle- or low-rank- ing males had increased mating suc- cess when their mothers were present in the party. This kind of support by mothers seems to be a common feature among wild bonobos.

FEMALE ROLE IN PEACEFUL ENCOUNTERS BETWEEN GROUPS

It is well known that intergroup encounters among chimpanzees are aggressive.76 At Mahale, during con- flicts between groups, males of the K group disappeared one by one, seem- ingly killed by males of the M group, which finally took over both the home range and the females of the Figure 6. An ex-alpha female, KAME (left), is groomed by the ex-alpha male, IBO (center), extinct K group.77 A similar incident and other offspring. [Color figure can be viewed in the online issue, which is available at occurred between Kasakela and wileyonlinelibrary.com.] Kamaha groups at Gombe.7,78 After splitting into the two groups, the position. Three of these had adult or ready died, their mothers were at a larger Kasakela group killed the adolescent sons at the time, and those prime age at the time of their ascent males of the Kahama group, which males took the alpha-male position. to alpha male status. In contrast, finally became extinct. During this When the other two females without many prime adult males occupied process, several fatal attacks were adult or adolescent sons took the alpha lower ranks among adult males in observed. Males of the Kahama position, other males maintained the both the E1 and E2 groups of bono- group sometimes patrolled boundary alpha position, but the alpha female bos at Wamba, although there were areas, attacking and killing Kahama was apparently dominant over the some exception (TAWASHI was the males that were ranging alone.7 Male alpha male in one of these cases. Stated alpha male in the E1 group and patrolling behavior and fatal agonistic differently, 3 of 4 males that have occu- KUMA was the alpha male in the E2 interactions have also been observed pied the alpha position had a mother in group for certain periods). This tend- at Kibale79–82 and Kalinzu83 in the alpha position at the time of their ency may be partly explained by the Uganda, and at Taı¨inCoˆ te d’Ivoire.84 rank acquisition. fact that the mothers of those prime Intergroup encounters among It is clear that females do not adult males had already died.58,72 bonobos are also stressful. When they reach the alpha female position We may ask, then, why some female hear vocalizations of other groups, owing to the high status of their sons bonobos intentionally support their bonobos usually climb up trees and because males never support their maturing sons’ bid for alpha status, de- carefully look in the direction of the mothers in agonistic interactions spite the fact that they do not often sounds. They sometimes quietly among females. Rather, females sup- fight with one another or behave politi- change their direction to avoid other port their sons in agonistic interac- cally. I hypothesized that females may groups. In most cases, however, they tions among males. Among chimpan- compete to increase their number of respond to such vocalizations with a zees, males with strong male allies grand-offspring through the support of chorus of loud calls. The two groups tend to achieve high rank, with their sons.58 Although females cannot gradually approach each other, males at a prime adult age usually increase the number of offspring they exchanging vocalizations. When they taking the alpha position.7,23,47,74,75 themselves produce by fighting with finally meet, males often display, but In contrast, male bonobos in E1 other females, they may be able, by do not usually fight. Although males group tend to obtain the alpha posi- raising the social status of their sons, to do not usually merge at the front tion during late adolescence or early increase the number of their sons’ off- lines, after a time females do move adulthood (estimated ages in years: spring. Gerloff and colleagues26 beyond the front lines and begin to IBO ¼ <20, TEN ¼ 13, TAWASHI ¼ reported that at Lomako two males interact with females of the other 22–28, NOBITA ¼ 20). This may have that attained the highest paternity suc- group, engaging in genito-genital rub- occurred because, except the case of cess were sons of high-ranking females. bing or grooming. It seems as if they TAWASHI, whose mother had al- Surbeck57 reported that females at Lui have found old associates or relatives ARTICLES Female contributions to bonobo societies 139

before transferring to their current groups. Bonobos seem to readily establish peaceful relationships with the groups they encounter, though such relationships are not formed for all combinations of the groups. After the study group E split into E1 and E2 in 1983, the two new groups con- tinued to have peaceful encounters. E1 bonobos also had peaceful encounters with another neighboring group, K, but tended to vacate the area when they heard vocalizations of another neighboring group, B. In the 1980s, the E1 group more fre- quently had peaceful encounters with Figure 7. Characteristic features of female bonobos and relationships among them. P group as they extended their range into the south after splitting off from the original group. After we resumed in the other group. After the initial Encounters between two groups of our study in 2003, E1 group excitement has passed, the groups of- bonobos can be intermittently extended its range into the east, and ten start feeding in the same tree. repeated for several days.85 It seems came to have peaceful encounters Although males tend to stay away that such encounters are stressful for with a newly identified group in from the front lines, it becomes diffi- males; they occasionally moved 2010. Peaceful encounters have also cult to identify the boundary between away, vocalizing in an apparent been reported from Lomako.86 the two groups.10,85 attempt to encourage females to ter- Groups at that site did display to one In the 1986–87 study period, Idani minate the encounter. However, if another, and the frequency of ago- observed 25 encounters between P females did not separate from the nistic interactions increased during group and the main study group, E1, other group, males returned to the the encounters. However, members over 3 months.85 In all encounters, encounter. Thus, these peaceful of the different groups also copu- both groups remained together for intergroup encounters apparently lated with and groomed one another. long periods. During such encoun- were led by females. Such encoun- ters, copulations frequently occurred ters appear to hold no risk for between males and females of the females and they gain an opportunity CONCLUSION different groups. Figure 7 shows the to copulate with extra-group males frequency of copulation by adult or socially interact with extra-group This comparison of the social struc- females of the study group. E1 females that they may have known tures of chimpanzees and bonobos females copulated with males of P group with considerable frequency, though less frequently than with males of the same group. Consider- ing only those encounters, E1 females copulated with P males more frequently than they did with E1 males, suggesting that females are eager to copulate with males of different groups. As noted, females move beyond the front lines with- out hesitation, but males tend to stay within the range of their own group. Therefore, males cannot do anything to restrict females even if they copulate with males of the other group. On the other hand, males can copulate with females from the other group that come into their range without any distur- bances from the males of that other group. Figure 8. Characteristic features of female bonobos and relationships among them. 140 Furuichi ARTICLES illustrates how the nature of societies Recent genetic studies have shown for Ecology and Forestry, Ministry of may change depending on which sex that chimpanzees and bonobos Scientific Research and Technology, controls behavioral initiatives. Female diverged within the last million years D. R. Congo. I give special thanks for bonobos are highly gregarious despite or so,89,90 more recently than was pre- their great contribution to this work. living in male-philopatric social viously thought. It is not surprising, I also thank Dr. Toshisada Nishida, groups. They form close social associ- therefore, that chimpanzees and bono- Dr. Juichi Yamagiwa, and Dr. Tet- ations and cooperatively defend their bos share many common traits, suro Matsuzawa for their continued high social status against males, including physical attributes and their support of our studies, and members severely competing only for the high male-philopatric residence patterns. of the Laboratory of Evolu- dominance rank of their sons. The However, something changed for tion Studies and Research high social status of females and their bonobos, probably during a bottleneck Institute of Kyoto University for pro- initiative in social, sexual, and ranging period, that altered the sexuality and viding valuable suggestions. This behaviors seem to contribute to the social status of females. Since chim- study was mainly supported by the peaceful nature of the bonobo society. panzees, , and all Japan Society for the Promotion of The characteristic features of share common traits, such as a lim- Science (JSPS) Grants-in-aid for female bonobos appear to be interre- ited estrus period among females and Scientific Research (02041049, lated and together contribute to the male dominance, this change seems to 06041064, 09041160, 10640613 to high attendance of females in mixed- be specific to bonobos. Considering the Kano; 58041025, 60041020, 62041021 sex parties (Fig. 8). First, bonobo recent divergence of bonobos and to Nishida; 10CE2005 to Takenaka; habitats, as compared with those of chimpanzees, we may infer that small 12575017, 17255005, 22255007 to chimpanzees, have higher density of genetic changes occurred in one or a Furuichi; 17570193, 19405015 to food patches, including large fruit few key features and thus invoked de- Hashimoto; 19107007 to Yamagiwa; treesandsmallerfooditemsonwhich velopment of the whole social system 21255006 to Ihobe); the National they forage while traveling between represented in Figure 8, rather than Geographic Fund for Research and larger trees. Such ecological condi- that the various features evolved inde- Exploration (7511-03 to Furuichi); tions may decrease the travel dis- pendently. For example, if genetic JSPS Core-to-Core program (15001 11,19,87,88 tance between food patches, changes occurred in the physiology to Primate Research Institute); thus reducing the cost for the of females, causing them to show Toyota Foundation (D04-B-285 to slower-moving females. Second, if estrus during nonconceptive periods, Furuichi); JSPS International Train- females can exercise an initiative in this whole social system may have ing Program (2009-8 to Primate ranging, they can avoid incurring developed in an environment with Research Institute); JSPS Asia-Africa larger costs associated with travel abundant and dense food resources, Science Platform Program (2009-8 to than males do, which may promote without requiring many other Furuichi); JSPS Institutional Pro- the aggregation of females in mixed- genetic changes, at least in the early gram for Young Researcher Overseas sex parties. Third, with a prolonged stages. I expect that genetic studies will Visits (2009-37 to Primate Research estrus, females mitigate any potential clarify the small but important genetic Institute); Japan Ministry of the for excessive sexual competition differences that can explain the large Environment Global Environment among males and thereby avoid male differences in sexuality and society of Research Fund (F-061 to Nishida); harassment. In addition, the long the two species in the Pan. Charitable Trust Africa Support periods of pseudo-estrus may prevent Fund (2010 to Support for Conserva- infanticide through paternity confu- tion of Bonobos); and Japan Ministry sion. The high social status of ACKNOWLEDGMENTS females may contribute to their of the Environment Research and aggregation in at least two ways. All the research reported here on Technology Development Fund (D- One way is that females can have bonobos at Wamba and chimpanzees 1007 to Furuichi). priority of access to food and, in the Kalinzu Forest was done with because of their high rank, avoid Drs. Takayoshi Kano, Suehisa Kur- both infanticide and harassment by oda, Kohji Kitamura, Akio Mori, REFERENCES Evelyn Ono-Vineberg, Gen’ichi Idani, males. Another way is that through 1 Nishida T. 1979. The social structure of their close association with and dom- Tomoo Enomoto, Hiroshi Ihobe, chimpanzees of the Mahale Mountains. In: inance support for their adult sons, Naobi Okayasu, Chie Hashimoto, Hamburg DA, McCown ER, editors. The great Ellen J. Ingmanson, Yasuko Tashiro, apes. Menlo Park, CA: Benjamin/Cummings they can take the initiative in rang- p 73–121. ing. On the other hand, the high Hiroyuki Takemoto, Tetsuya Saka- 2 Kano T. 1982. The social group of pygmy degree of aggregation displayed by maki, and other researchers who vis- chimpanzees (Pan paniscus) of Wamba. Prima- bonobo females can also contribute ited Wamba for short periods. Others tes 23:171–188. who did research with us were Mr. 3 Goodall J. 1983. Population dynamics during to their high social status, through a 15-year period in one community of free-liv- formation of coalitions. The social Ekam Wina, Dr. Mwanza N. Ndunda, ing chimpanzees in the Gombe National Park, status of females may also be Dr. Mbangi N. Mulavwa, Mr. Tanzania. Z Tierpsychol 61:1–60. enhanced by the extended female Kumugo Yangozene, Mr. Mikwaya 4 Van Elsacker L, Vervaecke H, Verheyen RF. 1995. A review of terminology on aggregation choice in mating partners resulting Yamba-Yamba, and Mr. Balemba patterns in bonobos (Pan paniscus). Int J Pri- from prolonged estrus. Motema-Salo of the Research Center matol 16:37–52. ARTICLES Female contributions to bonobo societies 141

5 Wrangham RW. 1986. Ecology and social 23 Reynolds V. 2005. The chimpanzees of the 40 Hasegawa T, Hiraiwa-Hasegawa M. 1983. relationships in two species of chimpanzee. In: Budongo Forest: ecology, behaviour, and con- Opportunistic and restrictive matings among Rubenstein DI, Wrangham RW, editors. Ecolog- servation. New York: Oxford University Press. wild chimpanzees in the Mahale Mountains, ical aspects of social evolution on birds and 24 Muroyama Y, Sugiyama Y. 1994. Grooming Tanzania. J Ethol 1:75–85. mammals. Princeton: Princeton University relationships in two species of chimpanzees. In: 41 Nishida T, Takasaki H, Takahata Y. 1990. Press. p 352–378. Wrangham RW, McGrew WC, de Waal FBM, Demography and reproductive profiles. In: 6 Kuroda S. 1979. Grouping of the pygmy Heltne PG, editors. Chimpanzee cultures. Cam- Nishida T, editor. The chimpanzees of the chimpanzees. 20:161–183. bridge, MA: Harvard University Press. p 169–180. Mahale Mountains: sexual and life history strat- 7 Goodall J. 1986. The chimpanzees of Gombe: 25 Hashimoto C, Furuichi T, Takenaka O. egies. Tokyo: University of Tokyo Press. p 63– patterns of behavior. Cambridge: Harvard Uni- 1996. Matrilineal kin relationship and social 97. versity Press. behavior of wild bonobos (Pan paniscus): 42 Takahata Y, Ihobe H, Idani G. 1996. Com- 8 White FJ. 1988. Party composition and dy- sequencing the D-loop region of mitochondrial paring copulations of chimpanzees and bono- namics in Pan paniscus. Int J Primatol 9:179– DNA. Primates 37:305–318. bos: do females exhibit proceptivity or receptiv- 193. 26 Gerloff U, Hartung B, Fruth B, Hohmann G, ity? In: McGrew WC, Marchant LF, Nishida T, Tautz D. 1999. Intracommunity relationships, editors. Great societies. Cambridge: Cam- 9 Furuichi T. 1987. Sexual swelling, receptivity, dispersal pattern and paternity success in a bridge University Press. p 146–155. and grouping of wild pygmy chimpanzee 43 Martin DR, Graham CE, Gould KG. 1978. females at Wamba, Zaı¨re. Primates 28:309–318. wild living community of bonobos (Pan panis- cus) determined from DNA analysis of faecal Successful artificial insemination in the chim- 10 Kano T. 1992. The last ape: pygmy chimpan- samples. Proc R Soc Lond 266:1189–1195. panzee. Symp Zool Soc Lond 47:197–207. zee behavior and ecology. Stanford, CA: Stan- 27 Hashimoto C, Tashiro Y, Hibino E, Mulavwa 44 Wallis J. 1997. A survey of reproductive pa- ford University Press. M, Yangozene K, Furuichi T, Idani G, Takenaka rameters in the free-ranging chimpanzees of 11 Furuichi T. 2009. Factors underlying party O. 2008. Longitudinal structure of a unit-group of Gombe National Park. J Reprod Fertil 109:297– size differences between chimpanzees and bonobos: male philopatry and possible fusion of 307. bonobos: a review and hypotheses for future unit-groups. In: Furuichi T, Thompson J, editors. 45 Tutin CEG, McGinnis PR. 1981. Chimpanzee study. Primates 50:197–209. The bonobos: behavior, ecology, and conserva- reproduction in the wild. In: Graham CE, edi- 12 Boesch C. 1996. Social grouping in Taı¨ tion.NewYork:Springer.p107–119. tor. Reproductive biology of the great apes: chimpanzees. In: McGrew WC, Marchant LF, 28 Furuichi T, Idani G, Ihobe H, Kuroda S, comparative and biomedical perspectives. New Nishida T, editors. Great ape societies. Cam- Kitamura K, Mori A, Enomoto T, Okayasu N, York: Academic Press. p 239–264. bridge: Cambridge University Press. p 101–113. Hashimoto C, Kano T. 1998. Population dy- 46 Tutin CEG. 1979. Mating patterns and 13 Furuichi T, Mulavwa M, Yangozene K, namics of wild bonobos (Pan paniscus)at reproductive strategies in a community of wild Yamba-Yamba M, Motema-Salo B, Idani G, Wamba. Int J Primatol 19:1029–1043. chimpanzees (Pan troglodytes schweinfurthii). Ihobe H, Hashimoto C, Tashiro Y, Mwanza N. 29 Furuichi T, Idani G, Ihobe H, Hashimoto H, Behav Ecol Sociobiol 6:29–38. 2008. Relationships among fruit abundance, Tashiro Y, Sakamaki T, Mulavwa MN, Yangozene 47 de Waal FBM. 1982. Chimpanzee politics: ranging rate, and party size and composition of K, Kuroda S. n.d. Long-term studies on wild power and sex among apes. London: Jonathan bonobos at Wamba. In: Furuichi T, Thompson bonobos at Wamba, Luo Scientific Reserve, D.R. Cape. J, editors. The bonobos: behavior, ecology, and Congo: towards the understanding of female life 48 Boesch C, Boesch-Achermann H. 2000. The conservation. New York: Springer. p 135–149. history in a male-philopatric species. In: Kappeler chimpanzees of the Taı¨ Forest: behavioral ecol- 14 Hashimoto C, Furuichi T, Tashiro Y. 2001. PM, Watts DP, editors. Long-term field studies of ogy and evolution. New York: Oxford University What factors affect the size of chimpanzee par- primates. Dordrecht: Springer. In press. Press. ties in the Kalinzu Forest, Uganda? Examina- 30 Hohmann G. 2001. Association and social 49 Watts DP. 1998. Coalitionary mate guarding tion of fruit abundance and number of estrous interactions between strangers and residents in by male chimpanzees at Ngogo, Kibale National females. Int J Primatol 22:947–959. bonobos (Pan paniscus). Primates 42:91–99. Park, Uganda. Behav Ecol Sociobiol 44:43–55. 15 31 Nishida T. 1968. The social group of wild Kuroda S. 1989. Developmental retardation 50 Hashimoto C, Furuichi T. 2006. Frequent chimpanzees in the Mahali Mountains. Prima- and behavioral characteristics of pygmy chim- copulations by females and high in tes 9:167–224. panzees. In: Heltne PG, Marquardt L, editors. chimpanzees in the Kalinzu Forest, Uganda. In: 16 Itoh N, Nishida T. 2007. Chimpanzee group- Understanding chimpanzees. Cambridge, MA: Newton-Fisher NE, Notman H, Paterson JD, ing patterns and food availability in Mahale Harvard University Press. p 184–193. Reynolds V, editors. Primates of western Mountains National Park, Tanzania. Primates 32 Furuichi T. 1989. Social interactions and the Uganda. New York: Springer. p 247–257. 48:87–96. life history of female Pan paniscus in Wamba, 51 Muller MN, Kahlenberg SM, Thompson ME, 17 Chapman CA, Wrangham RW, Chapman LJ. Zaire. Int J Primatol 10:173–197. Wrangham RW. 2007. Male coercion and the 1995. Ecological constraints on group size: an 33 Idani G. 1991. Social relationships between costs of promiscuous mating for female chim- analysis of spider monkey and chimpanzee sub- immigrant and resident bonobo (Pan paniscus) panzees. Proc R Soc Lond B Biol Sci 274:1009– groups. Behav Ecol Sociobiol 36:59–70. females at Wamba. Folia Primatol 57:83–95. 1014. 18 Wrangham RW. 1979. Sex differences in 34 Savage-Rumbaugh ES, Wilkerson BJ. 1978. 52 Boesch C, Kohou G, Nene H, Vigilant L. chimpanzee dispersion. In: Hamburg DA, Socio-sexual behavior in Pan paniscus and Pan 2006. Male competition and paternity in wild McCown ER, editors. The great apes. Menlo troglodytes: a comparative study. J Hum Evol chimpanzees of the Taı¨ Forest. Am J Phys Park, CA: Benjamin/Cummings. p 481–489. 7:327–344. Anthropol 130:103–115. 19 Wrangham RW. 2000. Why are male chim- 35 Thompson-Handler N, Malenky RK, Badrian 53 Stumpf RM, Boesch C. 2005. Does promis- panzees more gregarious than mothers? A N. 1984. Sexual behavior of Pan paniscus under cuous mating preclude female choice? Female scramble competition hypothesis. In: Kappeler natural conditions in the Lomako Forest, Equa- sexual strategies in chimpanzees (Pan troglo- PM, editor. Primate males: causes and conse- teur, Zaire. In: Susman RL, editor. The pygmy dytes verus) of the Taı¨ National Park, Cote quences of variation in group composition. chimpanzee: evolutionary biology and behavior. d’Ivoire. Behav Ecol Sociobiol 57:511–524. Cambridge: Cambridge University Press. p 248– New York: Prenum. p 347–368. 54 Furuichi T, Hashimoto C. 2004. Sex differ- 258. 36 Wrangham RW. 1993. The evolution of sex- ences in copulation attempts in wild bonobos 20 Pusey AE, Packer C. 1987. Dispersal and uality in chimpanzees and bonobos. Hum Nat at Wamba. Primates 45:59–62. philopatry. In: Smuts BB, Cheney DL, Seyfarth 4:47–79. 55 Furuichi T. 1992. The prolonged estrus of RM, Wrangham RW, Struhsaker TT, editors. 37 Furuichi T, Hashimoto C. 2002. Why female females and factors influencing mating in a Primate societies. Chicago: University of Chi- bonobos have a lower copulation rate during wild unit-group of bonobos (Pan paniscus)in cago Press. p 250–266. estrus than chimpanzees. In: Boesch C, Hoh- Wamba, Zaire. In: Itoigawa N, Sugiyama Y, 21 Janson CH, Goldsmith ML. 1995. Predicting mann G, Marchant LF, editors. Behavioural di- Sackett G, Thompson R, editors. Topics in pri- group size in primates: Foraging costs and pre- versity in chimpanzees and bonobos. New York: matology, vol. 2: Behavior, ecology, and conser- dation risks. Behav Ecol 6:526–536. Cambridge University Press. p 156–167. vation. Tokyo: University of Tokyo Press. p 38 179–190. 22 Mulavwa MN, Yangozene K, Yamba-Yamba Dixson AF. 1998. Primate sexuality: compara- 56 M, Motema-Salo B, Mwanza NN, Furuichi T. tive studies of the prosimians, monkeys, apes, and Hohmann G, Fruth B. 2003. Intra- and 2010. Nest groups of wild bonobos at Wamba: human beings. Oxford: Oxford University Press. inter-sexual aggression by bonobos in the con- selection of vegetation and tree species and 39 Beach FA. 1976. Sexual attractivity, procep- text of mating. Behaviour 140:1389–1413. relationships between nest group size and party tivity, and receptivity in female mammals. 57 Surbeck M, Mundry R, Hohmann G. 2010. size. Am J Primatol 72:575–586. Horm Behav 7:105–138. Mothers matter! Maternal support, dominance 142 Furuichi ARTICLES

status and mating success in male bonobos 70 Stanford CB, Wallis J, Matama H, Goodall J. 83 Hashimoto C, Furuichi T. 2005. Possible (Pan paniscus). Proc R Soc B doi:10.1098/ 1994. Patterns of predation by chimpanzees on intergroup killing in chimpanzees in the rspb.2010.1572. red colobus monkeys in Gombe National Park, Kalinzu Forest, Uganda. Pan Afr News 12:3–5. 58 1982–1991. Am J Phys Anthropol 94:213–228. Furuichi T. 1997. Agonistic interactions and 84 Boesch C, Crockford C, Herbinger I, Wittig 71 matrifocal dominance rank of wild bonobos Takahata Y, Hasegawa T, Nishida T. 1984. R, Moebius Y, Normand E. 2008. Intergroup (Pan paniscus) at Wamba. Int J Primatol Chimpanzee predation in the Mahale Moun- conflicts among chimpanzees in Taı¨ National 18:855–875. tains from August 1979 to May 1982. Int J Pri- Park: lethal violence and the female perspective. 59 White FJ, Wood KD. 2007. Female feeding matol 5:213–233. Am J Primatol 70:519–532. priority in bonobos, Pan paniscus, and the 72 Furuichi T, Ihobe H. 1994. Variation in male 85 question of female dominance. Am J Primatol relationships in bonobos and chimpanzees. Idani G. 1990. Relations between unit-groups 69:837–850. Behaviour 130:211–228. of bonobos at Wamba, Zaire: encounters and temporary fusions. Afr Study Monogr 11:153–186. 60 Parish AR. 1996. Female relationships in 73 Kuroda S. 1980. Social behavior of the bonobos (Pan paniscus): evidence for bonding, pygmy chimpanzees. Primates 21:181–197. 86 Hohmann G, Fruth B. 2002. Dynamics in cooperation, and female dominance in a male- 74 Nishida T. 1983. Alpha status and agonistic social organization of bonobos (Pan paniscus). philopatric species. Hum Nat 7:61–96. alliance in wild chimpanzees (Pan troglodytes In: Boesch C, Hohmann G, Marchant LF, edi- 61 Vervaecke H, de Vries H, van Elsacker L. schweinfurthii). Primates 24:318–336. tors. Behavioural diversity in chimpanzees and bonobos. New York: Cambridge University 2000. Dominance and its behavioral measures 75 Nishida T, Hosaka K. 1996. Coalition strat- Press. p 138–150. in a captive group of bonobos (Pan paniscus). egies among adult male chimpanzees of the Int J Primatol 21:47–68. Mahale Mountains, Tanzania. In: McGrew W, 87 Malenky RK, Stiles EW. 1991. Distribution 62 Parish AR. 1994. Sex and food control in the Marchant L, Nishida T, editors. Great ape soci- of terrestrial herbaceous vegetation and its con- uncommon chimpanzee: how bonobo females eties. Cambridge: Cambridge University Press. sumption by Pan paniscus in the Lomako For- overcome a phylogenetic legacy of male domi- p 114–134. est, Zaire. Am J Primatol 23:153–169. nance. Ethol Sociobiol 15:157–179. 76 Wrangham R, Peterson D. 1996. Demonic 88 White FJ, Wrangham RW. 1988. Feeding 63 de Waal FBM. 1995. Bonobo sex and soci- males: apes and the origins of human violence. competition and patch size in the chimpanzee ety. Sci Am Library Series 272:82–88. Boston: Houghton Mifflin. species Pan paniscus and Pan troglodytes. 64 77 Stevens JMG, Vervaecke H, de Vries H, van Nishida T, Hiraiwa-Hasegawa M, Hasegawa T, Behaviour 105:148–164. Elsacker L. 2007. Sex differences in the steep- Takahata Y. 1985. Group extinction and female ness of dominance hierarchies in captive transfer in wild chimpanzees in the Mahale 89 Becquet C, Przeworski M. 2007. A new bonobo groups. Int J Primatol 28:1417–1430. National Park, Tanzania. Z Tierpsychol 67:284–301. approach to estimate parameters of 65 Hohmann G, Fruth B. 1993. Field observa- 78 Williams JM, Oehlert GW, Carlis JV, Pusey models with application to apes. Res tion on meat sharing among bonobos (Pan pan- AE. 2004. Why do male chimpanzees defend a 17:1505–1519. iscus). Folia Primatol 60:225–229. group range? Anim Behav 68:523–532. 90 Hey J. 2010. The divergence of chimpanzee 66 Ihobe H. 1992. Observations on the meat-eat- 79 Watts DP, Muller M, Amsler SJ, Mbabazi G, species and subspecies as revealed in multi- ing behavior of wild bonobos (Pan paniscus)at Mitani JC. 2006. Lethal intergroup aggression population isolation-with-migration analyses. Wamba, Republic of Zaire. Primates 33:247–250. by chimpanzees in Kibale National Park, Mol Biol Evol 27:921–933. 67 Uganda. Am J Primatol 68:161–180. Surbeck M, Hohmann G. 2008. Primate 91 Mulavwa M, Furuichi T, Yangozene K, 80 by bonobos at LuiKotale, Salonga Wrangham R. 1999. Evolution of coalitio- Yamba-Yamba M, Motema-Salo B, Idani G, National Park. Curr Biol 18:R906–907. nary killing. Yearbook Phys Anthropol 42:1–30. Ihobe H, Hashimoto C, Tashiro Y, Mwanza N. 68 Hohmann G, Fruth B. 2007. New records on 81 Wilson M, Wrangham R. 2003. Intergroup 2008. Seasonal changes in fruit production and prey capture and meat eating by bonobos at relations in chimpanzees. Annu Rev Anthropol party size of bonobos at Wamba. In: Furuichi Lui Kotale, , Democratic 32:363–392. T, Thompson J, editors. The bonobos: behavior, Republic of Congo. Folia Primatol 79:103–110. 82 Mitani JC, Watts DP, Amsler SJ. 2010. Le- ecology, and conservation. New York: Springer. 69 Boesch C, Boesch H. 1989. Hunting behav- thal intergroup aggression leads to territorial p 121–134. ior of wild chimpanzees in the Taı¨ National expansion in wild chimpanzees. Curr Biol Park. Am J Phys Anthropol 78:547–573. 20:R507–R508. VC 2011 Wiley-Liss, Inc.

Articles in Forthcoming Issues

• ‘‘An ape’s view of the Oldowan’’ revisited Thomas Wynn, R. Adriana Hernandez-Aguilar, Linda Marchant, and William McGrew • Geochronology of the Turkana Depression Francis Brown and Ian McDougall • Stable isotope ecology in the Omo-Turkana Basin Thure Cerling, Naomi Levin, and Benjamin Passey • Turkana Basin paleoecology: the fossil evidence Rene´ Bobe