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The Social Behavior of Chimpanzees and Bonobos: Empirical Evidence and Shifting Assumptions

Author(s): Craig B. Stanford

Source: Current Anthropology , Vol. 39, No. 4 (August/October 1998), pp. 399-420

Published by: The University of Chicago Press on behalf of Wenner-Gren Foundation for Anthropological Research

Stable URL: https://www.jstor.org/stable/10.1086/204757

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https://www.jstor.org/stable/10.1086/204757

Molecular studies indicate that humans, chimpanzees (Pan troglodytes), and bonobos (P. paniscus) are very closely related in a lineage that split into hominid andThe Social Behavior Pan lines approximately 6–7 million years ago, possibly following a divergence from the gorilla lineage about 1–of Chimpanzees 2 million years earlier (Caccone and Powell 1989, Ru- volo et al. 1991). Chimpanzees and bonobos have a more recent common ancestry only some 2–2.5 millionand Bonobos years ago (Caccone and Powell 1989). Although it is now an endangered species, the chimpanzee is an ex- tremely successful species ecologically, occurring in aEmpirical Evidence and Shifting wide range of habitat types across the equatorial portion of the African continent. The bonobo, by contrast, isAssumptions1 found in a much more geographically and ecologically restricted region of lowland rain forest in central Zaı̈re. Until the 1980s, so little was known about the behavior of wild bonobos that detailed comparisons between theby Craig B. Stanford two Pan species were not possible. The number of field observation hours on bonobos is today still a small frac- tion of the database of chimpanzee behavior and ecol- ogy (White 1996a), but cross-species comparisons are

As our closest living relatives, chimpanzees and bonobos have nevertheless commonplace. been widely used as models of the behavior of early hominids. In These two African apes have been reported to differrecent years, as information on the social behavior and ecology

dramatically in patterns of sexuality, dominance, same-of bonobos has come to light, many interspecific comparisons have been made. Chimpanzees have been characterized in terms sex social bonds, and the frequency and intensity of of their intercommunity warfare, meat eating, infanticide, canni- both intragroup and intergroup aggression. Chimpan- balism, male status-striving, and dominance over females. Bo- zees have long been described in terms of male dom- nobos, meanwhile, have been portrayed as the ‘‘Make love, not

inance over females, hunting and meat eating, andwar’’ ape, characterized by female power-sharing, a lack of aggres- intercommunity warfare. According to Wrangham andsion between either individuals or groups, richly elaborated sex-

ual behavior that occurs without the constraint of a narrow win- Peterson (1996:191), ‘‘What most male chimpanzees dow of fertility, and the use of sex for communicative purposes. strive for is being on top, the one position where they This paper evaluates the evidence for this dichotomy and consid- will never have to grovel. It is the difficulty of gettingers the reasons that contrasting portrayals of the two great apes

there that induces aggression.’’ Bonobos have been seenhave developed. While there are marked differences in social be- havior between these two species, I argue that they are more sim- as sharply contrasting with chimpanzees, displaying fe- ilar behaviorally than most accounts have suggested. I discuss male dominance over males, richly elaborated sexual several reasons that current views of bonobo and chimpanzee so- behavior that often occurs in a nonconceptive context, cieties may not accord well with field data. Among these are a

and a general lack of aggressiveness. In de Waal’s (1997:bias toward captive data on bonobos, the tendency to see bo- 22) description, ‘‘Bonobo society, unlike that of chim-nobos as derived because their behavior has been described more

recently than that of chimpanzees, and the possibility that inter- panzees, is best characterized as female centered and pretations of bonobo-chimpanzee differences are reflections of egalitarian, with sex substituting for aggression. Fe- human male-female differences. males occupy prominent, often ruling positions in soci-

ety, and the high points of bonobo intellectual life are craig b. stanford is Associate Professor and Co-Director of found not in cooperative hunting or strategies tothe Jane Goodall Research Center, Department of Anthropology,

achieve dominance but in conflict resolution and sensi-University of Southern California (Los Angeles, Calif. 90089- 0032, U.S.A. [[email protected]]). He was educated at tivity to others.’’ The importance of these closely re- Drew University, Rutgers University, and the University of Cali- lated apes in the ontogeny of theories about the origins fornia, Berkeley (Ph.D., 1990) and has taught at the University of of human behavior cannot be overstated. Our under- Michigan (1989–91) as well as conducting research on nonhuman

standing of the biology of extinct forms representedprimates in Uganda, Tanzania, Peru, and Bangladesh. His publica- tions include ‘‘Chimpanzee Hunting Behavior and Human Evolu- tion’’ (American Scientist 83:256–61), ‘‘Predation and Male Bonds in Primate Societies’’ (Behaviour, in press), and Chimpan- zee and Red Colobus: The Ecology of Predator and Prey (Cam- invitation to participate. I thank the other participants for their bridge: Harvard University Press, 1998). The present paper was constructive comments on an earlier version of the manuscript, es- submitted 12 vi 97 and accepted 11 ix 97. pecially Richard Byrne, Sarah Hrdy, Alison Jolly, Karen Strier, Rob-

ert Sussman, and Hiroyuki Takasaki. Christopher Boehm, William McGrew, Jim Moore, and two anonymous reviewers also read and improved the paper. Research on Gombe chimpanzees was sup- ported from 1990 to 1995 by the National Geographic Society, the Fulbright Foundation, the L. S. B. Leakey Foundation, and the Uni-1. This paper was originally prepared for the Wenner-Gren Founda-

tion Conference ‘‘Changing Images of Primate Societies,’’ June 15– versity of Southern California. Research clearance was granted by the Tanzanian Commission for Science and Technology, Tanzania22, 1996, in Terresopolis, Brazil. I am grateful to the Foundation

and to the organizers, Shirley Strum and Linda Fedigan, for their National Parks, and the Serengeti Wildlife Research Institute.

399

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400 current anthropology Volume 39, Number 4, August–October 1998

only by fossilized skeletal remains would be quite dif- and numerous shorter field studies. The study sites from which data in this paper are drawn are Gombe Na-ferent if we lacked living individuals of Pan for compar-

ison. Chimpanzees and bonobos provide us with exam- tional Park, Tanzania (Goodall 1986), Mahale National Park, also in Tanzania (Nishida 1990), Taı̈ Nationalples of the range of possible adaptations for feeding,

ranging, territoriality, mating, offspring rearing, and a Park in Côte d’Ivoire (Boesch and Boesch 1989, Boesch 1994), and Kibale National Park, Uganda (Wrangham,variety of other behaviors without which there would

be no starting point for reconstructing hominid soci- Clark, and Isabirye-Basuta 1992, Chapman, White, and Wrangham 1994).eties. They are, because of their kinship with humans,

their similar morphology, and their cognitive abilities, Our current view of chimpanzee society has emerged slowly, mainly because of the difficulty of obtaining athe main referential models for early hominids (Tooby

and DeVore 1987). Wrangham and Peterson (1996) have clear portrait of their fission-fusion form of polygyny. Increasing knowledge and changing attitudes aboutrecently argued for an evolutionary continuity of male

violence that extends from our close ancestry with chimpanzee society can be divided into three stages, each corresponding to a decade of field research. Duringchimpanzees. They argue on behavioral and morpholog-

ical grounds that humans have a greater phylogenetic the first stage of modern primate research in the 1960s, chimpanzee behavior first became a subject of system-affinity to chimpanzees than to bonobos.

In this paper I examine behavioral differences be- atic field study. After several years of observation in the wild, Goodall (1968) had made the landmark discoveriestween chimpanzees and bonobos and argue that the so-

cial behavior of these two great apes, while distinct in of meat eating and tool use. Throughout the 1960s Goo- dall believed that chimpanzee society, unlike that ofsome respects, is more similar than is often claimed. I

use data from field studies of the two species to address other group-living primates, had no group structure whatever. Relationships among individuals appeared tointerspecific differences in female dominance, sexual

behavior, and male aggression. be in constant flux. Nishida (1968) was the first to put forward a model of chimpanzee society based on the ‘‘unit-group’’ (later called the ‘‘community’’ by Western primatologists). This large-scale structure has a stableChimpanzee Social Behavior membership but no stable grouping patterns other than mothers and their dependent offspring. Other membersThe difficulty in generalizing about the natural history

of Pan troglodytes is illustrated by the fact that the fol- come together and depart unpredictably, giving rise to the label ‘‘fission-fusion society’’ (taken from Kum-lowing two statements, either of which might be found

in a textbook description of chimpanzee behavior, are mer’s [1968] study of Papio hamadryas). Males tend to be social with each other, and male alliances play a cru-equally accurate: cial role in the maintenance of territorial borders and in attempts to control females.A. Chimpanzee society is characterized by male con-

trol and dominance over females and by male aggres- In the second stage of research, in the 1970s, there were two major advances. The ecological influences onsion and sexual coercion directed at females. Male terri-

toriality and patrolling exclude extracommunity males chimpanzee behavior became clear, and key aspects of their behavior that had previously been unsuspectedand acquire new females for male reproductive benefits.

Females are essentially reproductive commodities over came to light. In both Mahale National Park and Gombe National Park, the negative effects of artificialwhich males compete.

B. Chimpanzee society is characterized by actively provisioning, which had led to heightened intracom- munity aggression, were recognized and curtailed, andmate-soliciting females that incite male competition

during their periovulatory period and that with their in- the collection of data became more systematic and in- cluded more ecological information. At Gombe, obser-fants form the nuclear units of the social system. Fe-

males forage solitarily to optimize food intake in fruit vation of the animals during long follows through the forest began to replace data collection in the feeding sta-patches and become more social when it suits their re-

productive tactics. Males may appear to dictate mating tion. Wrangham (1979) conducted the first thorough study of chimpanzee behavioral ecology, focusing pri-efforts, but the promiscuous, mate-soliciting female is

the driving force in the mating system of the species. marily on the males. It was this study that developed Nishida’s idea of the community as a male-defended structure within which less sociable females traveledFemale chimpanzees are indeed active mate solici-

tors, play important dominance roles in chimpanzee so- alone to optimize their use of food patches. Later obser- vation of intercommunity lethal territoriality rein-ciety, and strongly influence the shape of the social sys-

tem through their frequent sociality and periodic forced the view that chimpanzee society was male-con- trolled from both within and without. This representedmultiple matings. Few observers have observed wild

chimpanzees, however, without concluding that fe- a fundamental change in thinking about chimpanzees and also a revelation for its similarity to the homicidalmales live in a largely male-dominated and male-

controlled social environment. aggression that is a regular feature of many human soci- eties. Meanwhile, life histories of females showed thatChimpanzees have been more intensively studied

than bonobos, with several long-term (ten-plus years) they typically emigrate from their natal communities

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stanford Chimpanzees and Bonobos 401

at or after puberty (Goodall 1986). Female reproductive strategies involve multiple matings with males of their own and other communities. Despite Goodall’s early observations of intensely aggressive competition among males for estrous females, chimpanzee social systems came to be described in terms of casual promiscuity.

In the third stage of chimpanzee field research, from the early 1980s through the 1990s, the diversity of chimpanzee behavior became clear as studies from dif- ferent regions of Africa began comparing research find- ings on tool use (McGrew 1992), hunting styles (Boesch 1994, Stanford et al. 1994b), and feeding ecology (Chap- man, White, and Wrangham 1994). Two further long- term field studies produced new perspectives on tool use, hunting, and social cognition (Boesch and Boesch 1983, 1989; Chapman, White, and Wrangham 1994). Ecological data on food patches and their utilization led to predictions that explained the variation in party size

Fig. 1. Mean number of adult males to adult femalesand cohesiveness between the major study sites. Chim- in foraging parties for chimpanzees and bonobos. P.panzee populations exhibit considerable cultural varia- paniscus: W, Wamba; L, Lomako. P. troglodytes: G,tion (McGrew 1992), with learned group traditions that Gombe; K, Kibale; M, Mahale.parallel traditional human societies technologically.

This emerging realization has made it clear that the ex- termination of a chimpanzee population represents the permanent loss of any traditions that were unique to nity structure; centrally located females were thought

to be core members of the Kasakela community, whilethose animals. Party size in chimpanzees appears to be a function of more peripheral-ranging females might have member-

ship in the neighboring community as well. Goodallboth food-patch size and distribution and the presence of sexually receptive females (Goodall 1986, Wran- (1983) pointed out that females are wary of the males of

neighboring communities, suggesting that they cannotgham, Clark, and Isabirye-Basuta 1994). At Gombe, Goodall (1986) considered females with sexual swell- travel with impunity between adjacent male kin groups

and may suffer severe, even lethal attacks from strangerings to be the primary attractant influencing the forma- tion of large mixed-sex parties. She noted that years in males when ambushed in territorial overlap zones.

Male chimpanzees remain in their natal communitywhich many females were cycling were also the years of largest mean party size. Stanford et al. (1994b) also and join groups of males as they approach maturity

(Goodall 1986). These male groups tend to be highly re-found a significant positive correlation among Gombe chimpanzee party size, the presence and number of lated (Morin et al. 1993). They patrol territorial borders

and attack all extracommunity individuals encounteredswollen females, and the tendency to hunt. Most pub- lished papers suggest that party size is primarily a func- except for reproductively fertile females, whom they at-

tempt to recruit into their own community (Goodalltion of food availability (White and Wrangham 1988, Chapman, White and Wrangham 1994). Data on female 1986, Nishida 1990). Females, meanwhile, transfer be-

tween and may even belong to multiple communities,cycles in relation to fluctuation in party size from vari- ous chimpanzee study sites are critical to testing this being allowed to do so when they possess sexual swell-

ings. Recent data from Taı̈ National Park show that fe-hypothesis. Social relationships between the sexes vary among males may reside in one community but mate and con-

ceive offspring with males from another communitythe best-studied chimpanzee populations, and there has been some disagreement about the nature of chimpan- (Gagneux, Woodruff, and Boesch 1997). This suggests

that chimpanzee mating systems and social systems arezee community structure. Gombe foraging parties are small (fig. 1) relative to those at other sites. At Taı̈, not necessarily the same. Boesch (1991) argued that large party sizes were a re- sponse to the threat of predation by leopards. He also argued that the social system of Taı̈ chimpanzees was Bonobos more of a bisexually bonded community than other chimpanzee populations (Boesch 1996). Recently, For many years bonobos occupied a dimly understood

place in the biology of the great apes because of the lackDoran (1997) has disputed both of these claims, using Taı̈ data from a different period that showed commu- of captive or field studies, and they were necessarily ig-

nored in reviews of great-ape behavior. Even a recent re-nity structure and party sizes essentially the same as for other well-studied chimpanzee populations. At Gombe, view of great-ape reproductive behavior (Nadler 1995)

omitted bonobos, referring repeatedly to the gorilla,Wrangham (1977) considered individual female home ranges as somewhat independent of the male commu- orangutan, and chimpanzee as ‘‘the three great ape spe-

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402 current anthropology Volume 39, Number 4, August–October 1998

cies.’’ Bonobos were known as pygmy chimpanzees in (Malenky and Stiles 1991) or a temporal one (Chapman, White, and Wrangham 1994) is unclear.earlier descriptions, and morphological studies that

compared them with chimpanzees were undertaken de- Female bonobos emigrate from their natal commu- nity at or near sexual maturity and establish themselvescades before any behavioral information became avail-

able. In the 1970s these morphological studies began to in neighboring-community ranges (Idani 1991). Furui- chi (1989) found that immigrant female bonobos estab-focus on shared traits of the bonobo, chimpanzee, and

humans. Zihlmann and Cramer (1978) described mor- lished bonds with one female at a time and slowly be- come central in their new communities. He found thatphological distinctions between bonobos and chimpan-

zees, and Zihlmann et al. (1978) put forward the bonobo the oldest females tended to be the highest-ranking. Idani (1991) and Kano (1992) reported that most trans-as the best model for earliest hominid functional mor-

phology and behavior because of evidence of retention ferring females were nulliparous and that they estab- lished bonds with females that were unrelated to them.of early-hominid-like traits. Zihlmann’s bonobo model

was met with skepticism on the grounds that the bo- Female-female bonds are thus based on patterns of af- filiation but not necessarily on kinship.nobo might be an ecologically and morphologically di-

vergent chimpanzee rather than having traits homolo- Male bonobos are strongly philopatric, but this philo- patry is not accompanied by territorial aggression asgous with earliest hominids (Latimer et al. 1981,

Johnson 1981). consistently intense as in chimpanzees. Both hostile and peaceful intercommunity encounters are seen, andBonobo behavior is well-known only from two field

sites in central Congo, Lomako (Badrian and Badrian copulation between females and extracommunity males has been reported (Kano 1992). It would be wrong,1984; White 1988, 1996a, b; Hohmann and Fruth 1993,

1994) and Wamba (Kano 1983, 1992). In the early 1970s, however, to characterize bonobo communities as coex- isting peaceably, since half of encounters do involveresearchers conducted surveys of bonobo populations in

Congo that led to the establishment of these two sites. aggression of some sort (Kano 1992). Chimpanzees were observed for more than 15 years and thousandsThese sites continue to produce the bulk of field data,

with Wamba, under the direction of Takayoshi Kano, of observer-hours, including many intercommunity encounters, before lethal aggression was seen. Weproducing especially detailed observations of sociosex-

ual behavior and intracommunity social dynamics should therefore not assume that lethal or injurious intercommunity aggression never occurs among bo-(Kano 1983, 1992; Furuichi 1987, 1989; Idani 1991;

Hashimoto and Furuichi 1994). Lomako has produced nobos. Lethal aggression during chimpanzee inter- community encounters has been reported from Gombedetailed studies of social behavior and behavioral ecol-

ogy, with an emphasis on the latter (Thompson-Han- (Goodall 1986), Mahale (Nishida 1990), and Kibale (Wrangham, personal communication). The all-male pa-dler, Malenky, and Badrian 1984; White 1988; White

and Burgman 1990; Malenky and Stiles 1991). The dif- trols that characterize chimpanzees are rarer among bo- nobos (Kano 1992), though as bonobo party sizes in-ference in research foci may be due to differences in ha-

bituation. At Wamba, bonobos have long been habitu- crease the percentage of the party that is male also increases (White 1988).ated to observation in an artificial sugarcane plantation,

while at Lomako no provisioning was used and the ani- mals were less observable for many years. Less inten- sively worked bonobo research sites have been estab- Bonobo-Chimpanzee Comparisons lished at Yalosidi (Kano 1983) and Lilungu (Sabater Pi et al. 1993). A number of stark differences in social behavior be-

tween bonobos and chimpanzees have been reported. ILike chimpanzees, bonobos eat mainly ripe fruit, sup- plemented with herbaceous terrestrial plants. Wran- examine the evidence for these differences below. gham (1986) has suggested that bonobos, lacking food competition with gorillas, have adopted a diet high in reproductive ecology widely available pithy foods to mitigate the risk of fruit patchiness. Bonobos live in fission-fusion polygynous Female-female relationships and sexual behavior are

perhaps the two most-discussed differences betweensocieties, the territories of which are defended by strongly male-philopatric kin groups. Bonobo foraging the societies of bonobos and chimpanzees. Adult and

adolescent females of the genus Pan are characterizedparties form for the apparent purpose of providing fe- males with optimal fruit-foraging opportunities (Kano by the vivid advertisement of their sexual receptivity

with perineal swellings for a portion of their menstrual1992). Bonobo foraging parties tend to be substantially larger than those of chimpanzees, though there is con- cycles. Ovulation in both species occurs at the end of

the period of maximal swelling, just before the swellingsiderable size overlap between the species among differ- ent study sites. The smaller party sizes seen in chim- begins to detumesce (Wallis 1992). Male chimpanzees

are attracted to females with swellings during the entirepanzees appear to be related at least partially to differences in food-patch size and distribution and to duration of their maximal swelling, though there is

great individual and age-related variation among fe-bonobo use of herbaceous groundcover plant foods in addition to fruit. Whether the food-patch sizes that males in the level of interest they receive from males

(Goodall 1986). When female chimpanzees are swollenallow bonobo parties to be larger is a spatial difference

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stanford Chimpanzees and Bonobos 403

they become more sociable, attract males, and join (Goodall 1986). This has been considered in sharp con- trast to the behavior of bonobo females, which are saidmixed-sex parties that may comprise a majority of the

community. These aggregations often stay together for to have been released from the constraints of reproduc- tive sex and remain sexually receptive throughoutdays, the males dispersing once the female detumesces

(Goodall 1986). Swellings are thus an important influ- the menstrual cycle (Nadler et al. 1991; Thompson- Handler, Malenky, and Badrian 1984). This nonconcep-ence on chimpanzee grouping patterns.

While the length of the cycle varies among different tive sex has been considered an evolved mode of social communication (de Waal 1987, Wrangham 1993, Parishpopulations of the two species (table 1), chimpanzees

and bonobos are similar in the percentage of the men- 1994). The most detailed study of sexual receptivity in wild female bonobos, however, does not support thisstrual cycle during which maximal swelling occurs.

Wild female bonobos experience a period of about 14 claim. Furuichi (1987) found that although female bo- nobos at Wamba do copulate when not maximally swol-days of a 42-day cycle during which their anogenital re-

gion is tumescent, pink, and highly visible to others in len, more than 95% of matings were observed during periods of maximal or near-maximal swelling. This isthe community (Furuichi 1987). Longer swelling dura-

tions (up to 23 days) have been reported from captivity approximately the same as for chimpanzees (97% [Goo- dall 1986]). Female bonobos are thus somewhat more(Dahl 1986, Dahl, Nadler, and Collins 1991). Female

chimpanzees are maximally swollen for slightly fewer flexible than other apes in the timing of sexual receptiv- ity, but they are not released from the constraints ofdays (mean 5 13 at Gombe) of a shorter (36-day) men-

strual cycle (Wallis 1997). At Gombe, although births sexual swelling cycles. Female bonobos are frequently portrayed as hyper-are aseasonal (Goodall 1986), swelling cycles are sea-

sonal, peaking in the dry season and influencing party sexual, but mating frequencies in the wild are actually quite comparable for the two species of Pan. De Waalaggregations (Wallis 1995). Whether olfactory cues ac-

company the visual stimulus of the swelling is un- (1987) reported that bonobos in the San Diego Zoo copu- lated five times as frequently as chimpanzees, althoughknown but strongly suspected. Female chimpanzees

and bonobos also swell while they are pregnant or lac- he acknowledged that this rate might be an artifact of captive confinement. Comparisons between a wild andtating, though these anovulatory swellings may be less

regular in frequency and duration (Wallis 1992). Males a captive population may not reflect naturalistic mating patterns. Swollen female chimpanzees copulate withare nevertheless attracted to nonovulating swollen fe-

males. Swellings during pregnancy and in adolescent fe- multiple males during the early stages of their swelling cycle. As many as 50 copulation bouts with eight malesmales thus play a role in nonreproductive sex. in a day have been recorded, and swollen females have copulated with up to eight adult males in several min-bonobo sexuality utes (Goodall 1986). At Wamba, bonobo females ac- tively solicit sex from a range of males and may copu-It has become a fundamental premise of bonobo sexual-

ity and of the bonobo’s link to human behavior that late multiple times per hour while swollen (Kano 1992). However, female chimpanzees at Mahale have higheramong primates only bonobo and human females are

sexually active outside the periovulatory period. In the reported mean copulation rates than Wamba bonobos (Takahata, Ihobe, and Idani 1996). Moreover, male cop-wild, nearly all female chimpanzee sexual behavior is

observed during maximal or near-maximal swelling ulation rates in the wild are higher among chimpanzees than they are among bonobos. Mahale male chimpan- zees copulated at a higher mean rate than male bonobos at Wamba (P. troglodytes 0.20–0.29/hr., P. paniscustable 1 0.10–0.21/hr.). These rates are for adults, but adoles-Anogenital Swelling Durations in Chimpanzees cent male chimpanzees also have higher copulationand Bonobos rates than adolescent male bonobos. Bonobo mating rates are therefore not higher than those among chim-

Mean Maximal panzees if the swelling duration and not the entire in- Swelling Duration terbirth period is used as the time frame. If the entire (days) Species/Site Source interbirth period is included, then bonobos do show

higher copulation rates, because the period of maximal 13 (36.1% of 36- P. troglodytes/Gombe Wallis (1997) swelling occupies a slightly larger percentage of the

day cycle) menstrual cycle in bonobos than it does in chimpanzees 12.5 (39.7% of P. troglodytes/Mahale Hasegawa and (Kano 1996).

31.5-day cycle) Hirai-Hasegawa Female bonobos do not mate more frequently or sig-(1983)

nificantly less cyclically than chimpanzees, but there14.6 (34.8% of 42- P. paniscus/Wamba Furuichi (1987) day cycle) are some fundamental differences between the two spe-

12.9 (39.3% of P. paniscus/Wamba Kano (1996) cies. One difference relates to the presence of swollen 32.8-day cycle) females in foraging parties. At Gombe, at least one es-23.5 (47.9% of 49- P. paniscus/captive Dahl (1986)

trous female chimpanzee is present in the communityday cycle) about half of all days (Tutin 1979). However, only a mi-

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404 current anthropology Volume 39, Number 4, August–October 1998

Female bonobos also transfer to new communities at adolescence and also may receive aggression from the females in the new community (Idani, cited in Furuichi 1989). Bonobo females are by contrast often dominant to males (Kano 1992) and form close relationships with males and especially with other females (Furuichi 1989, Idani 1991). The power base, which in chimpanzee soci- ety rests solidly with adult males, is therefore more female-centered in bonobos, perhaps because of greater bonobo female sociality that enables female coalitions to form and to dominate males (Furuichi 1989; Parish 1994, 1996). However, Wood and White (1996) have shown that at Lomako females are dominant only in the arena of feeding priority. Most sex-for-food exchanges among bonobos at Lomako occur just before males allow females priority of access to feeding patches, and

Fig. 2. Percentage of foraging parties containing one this may be part of a larger pattern of strategic male def- or more estrous females, Wamba (P. paniscus [Kano erence in this species. If social dominance is considered 1992]), Gombe (P. troglodytes [unpublished data]), separately from priority of feeding access, the pattern of Mahale (P. troglodytes [Nishida 1968]). dominance in bonobos more strongly resembles that of

chimpanzees. Genital-genital rubbing is a nonreproduc- tive sexual behavior of female bonobos and is a further example of affiliation among females. The primary goalnority of mixed-sex foraging parties contain a swollen

female (fig. 2; 20–30% for Gombe and Mahale). More- of genital rubbing appears to be easing intracommunity tensions, particularly when competition over foodover, the data presented for Gombe are somewhat in-

flated because the sample of parties used is drawn from threatens to disrupt social harmony (White 1988). Such affiliative encounters between females occur frequentlyhunting parties, which tend to be substantially larger

than foraging parties on the whole (Stanford, unpub- in captivity as well (de Waal 1987; Parish 1994, 1996). It is probably not true that male bonobos are not af-lished). By contrast, nearly every mixed-sex party of bo-

nobos has at least one sexually swollen female (98%, filiative with each other; rather, their bonds may be less apparent and perhaps less strong than female-femaleWamba [Kano 1992]). This is because of the larger mean

size of bonobo parties and the greater number of days and female-male bonds tend to be. Male bonobos engage in territorial defense (Kano 1992), and bonobo society ison which each female is maximally swollen. The im-

portance of this difference is that access to reproduc- strongly male-philopatric. The emphasis on female sex- uality and female power is the result of studies showingtively active females is much greater for bonobo males

than for chimpanzee males, perhaps accounting for the that of female-female, male-female, and male-male af- filiation the last is least frequent.lower levels of intermale aggression that are reported

for bonobos.

meat eating bonobo female dominance

Meat eating by chimpanzees is well documented (Teleki 1973; Takahata, Hasegawa, and Nishida 1984;Another reported difference between bonobos and

chimpanzees involves the web of relationships among Uehara et al. 1992; Boesch and Boesch 1989; Stanford et al. 1994a; Stanford 1998) and is a systematic aspect ofadult females and males. Chimpanzee society is male-

dominated; adult males are typically dominant over all chimpanzee behavior across their geographic range. Chimpanzees incorporate the meat of hunted mammalsadult females, and adolescent males rise in rank by do-

minating each adult female before reaching the bottom in their diet, and at some sites the biomass of the meat captured by a community may approach 1,000 kg perof the male hierarchy (Goodall 1986, Nishida 1990). The

overall level of affiliative behaviors such as grooming or year (Stanford 1996). Red colobus monkeys (Colobus badius) are the main prey item at Gombe, Mahale, Ki-support in conflicts is lower among chimpanzees than

among bonobos, even among females whose infants bale, and Taı̈. The impact that chimpanzees have on red colobus populations at these and other sites may be anmay form play groups in their presence (Goodall 1986).

It may be that female chimpanzees are affiliative with important population regulator (Stanford 1995) as well as an influence on the structure of the red colobus socialeach other but that their bonds are less apparent than

female-male and male-male ones. Eventually, female system (Stanford 1998). Captured meat is often shared among the hunting party and may be shared nepotisti-chimpanzees establish themselves as members of a new

community, though many spend the majority of their cally and strategically. Most kills (approximately 92% at Gombe [Stanford et al. 1994a]) are made by males.time alone. Dominance relationships among female

chimpanzees are often not obvious to an observer and Chimpanzees probably hunt for both nutritional and political reasons in that alliances are cemented by themay be nonlinear (Goodall 1986).

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stanford Chimpanzees and Bonobos 405

giving of meat. They also appear to obtain meat for so- pears to allow female chimpanzees mobility between communities.ciosexual benefits in that males sometimes offer meat

to females and receive matings in the process (Nishida This hypothesis also addresses the object of male- bonded territorial defense in chimpanzees. The numberet al. 1992, Stanford et al. 1994b). Hunting at Gombe,

Mahale, and Taı̈ is seasonal, and at Gombe this season- of males in a community is positively correlated with the size of the territory that is defended against otherality corresponds with periods of the availability of

swollen females that are a robust predictor of party size communities (Stanford 1998). This male-bonded behav- ior may be related to either female defense or food de-(Stanford et al. 1994b). At both Gombe and Taı̈, hunting

success increases with increasing party size. fense; data on territoriality and female transfer are seen as key in modeling the behavior of the common homi-Among bonobos, meat eating is rare. Indeed, forest

monkeys (Cercopithecus ssp. and Colobus ssp.), which noid ancestor (Ghiglieri 1987, Wrangham 1987). If fe- male swellings are related to intense male territorialitywould be relished prey for chimpanzees at Gombe, Ma-

hale, Kibale, and Taı̈, have been used as playthings because they grant the females safe passage between communities, then territoriality may be food-resource-rather than as food items by bonobos at Lilungu (Sabater

Pi et al. 1993). Wamba bonobos rarely hunt even though based. This is because, from a male’s perspective, hav- ing as many females as possible in the communitytheir mean party size is larger than that found in any

chimpanzee population (Kano 1992). If male chimpan- should be a reproductive benefit, and so any immigrat- ing female should be welcomed whether currently cy-zees hunt primarily for political and sociosexual rather

than nutritional reasons, then one might expect male cling or not. To resident females new immigrants repre- sent both food and mating competition. Swellings maybonobos to be less interested in hunting, for two rea-

sons. First, female bonobos do not need to engage in po- therefore allow female chimpanzees to enter communi- ties against the wishes of previous immigrants becauselitical or sexual behavior to obtain a share of the meat;

they may simply take it away. Hohmann and Fruth they do so at a time when their swellings make them highly attractive to males. The same may apply to fe-(1993) reported instances of females’ taking fresh kills

away from male captors, which occurs very rarely in male bonobos, which also face aggression from resident females when immigrating to a new community.chimpanzees. The manipulative use of meat seen in

male chimpanzees would not be effective for male bo- Conversely, Hamilton (1984) and Hrdy and Whitten (1987) have hypothesized that by signaling ovulation,nobos, since they typically defer to females in feeding

situations. These observations point also to a social genital swellings might increase paternity certainty and therefore paternal investment by males. Clutton-Brockrather than nutritional basis for hunting in chimpan-

zees. Given that there is a range of potential prey, in- and Harvey (1976) argued that because a swollen, ovu- lating female becomes a focus of excitement and com-cluding monkeys, at both bonobo study sites, it is hard

to understand why bonobos would show little interest petition among males, the swelling’s function is to in- cite male competitive behavior, allowing her to choosein hunting if meat were the prized nutritional resource

it has been thought to be in chimpanzees. the most fit mate or mates. Harcourt (1981) has sug- gested that the swellings may function simply to extend the time period during which females can locate andsexual swellings stay in proximity to potential male mates. Tutin (1979) reported, however, that most conceptions during herThe sexual swelling is an evolved feature which, be-

cause it is visually obvious and connected to reproduc- study of Gombe chimpanzee reproductive behavior probably occurred during consortships, outside of thetion, has received much attention from primatologists.

Although Lovejoy (1981) assumed that humans had polygynous setting for which Clutton-Brock and Har- vey’s ‘‘best-male’’ model predicts that swellingsevolved concealed ovulation as a reproductive adapta-

tion by females, it is also possible that the Pan lineage evolved. She also pointed out that the ‘‘best-male’’ hy- pothesis does not fit chimpanzee society well, since fe-evolved swellings to advertise ovulation from a con-

cealed-ovulator ancestor. Although it exerts a major in- males choose mates on the basis of prior affiliative pat- terns with males who offered grooming and food-fluence on chimpanzee and bonobo society, its function

is not clear. Vividly advertised ovulation has arisen sev- sharing opportunities. Reproductive benefits may ac- crue to them only indirectly through benefits to theireral times in the primate order, including among the an-

cestors of some cercopithecines, some colobines, and offspring. More recently, Wallis (1997) has reviewed two decades of Gombe data on conceptions and foundthe Hominoidea (Sillén-Tullberg and Møller 1993).

Hrdy (1981) and Harcourt (1981) have argued that sexual that the majority occurred in polygynous settings, not in consortships.swellings may serve to confuse paternity and thereby

increase a male’s parental investment. The likelihood Explanations of the nature and origin of chimpanzee and bonobo sexual swellings seem to be based primarilyof aggression toward that female or toward her infant

might also be reduced as a result (Takahata 1985). Since on the premise that of the two species it is the latter that is the derived one. This premise may stem from bo-swollen female chimpanzees and bonobos transfer be-

tween communities and female chimpanzees that are nobos’ more limited geographic range and their elabo- rated sexual behavior. In addition, bonobos may tend toencountered by stranger males are attacked and even

killed if they are not swollen, the sexual swelling ap- be viewed as the divergent form because they have been

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406 current anthropology Volume 39, Number 4, August–October 1998

described and studied more recently. This premise may at different stages of the research history of a topic. However, it is especially the case in field primatologynot, however, be warranted. For instance, implicit in

the literature about bonobos is that females have ex- that the logistics of research, the longevity and ex- tended ontogeny of the subjects, and the importance oftended the duration of the sexual swelling, the result of

which is thought to be increased female cooperation documenting the life histories of many individuals of all age- and sex-classes contribute substantially to aand increased affiliation between males and females.

Highly visible swellings are unique traits in this homi- growth of ideas in the discipline through cumulative normal science. Considering chimpanzees to be entirelynoid clade. However, since the ancestral behavioral pat-

terns of chimpanzees/bonobos are unknown, it is also promiscuous without any definable social system was a result of the difficulty in documenting rare events: fe-unknown whether swellings in bonobos have been elab-

orated and extended in duration through natural selec- male migrations, intercommunity conflicts, hunting and meat sharing, male dominance upheavals. Chang-tion. Alternatively, female chimpanzees may have

shortened swelling cycles as an adaptation to attract ing this view took more than a decade; as data accumu- lated so did the depth of the portrait of chimpanzee soci-multiple mates while minimizing feeding competition.

The latter is a reasonable speculation given the typi- ety. The number of observer-hours spent with bonobos in the wild is still comparable to the time spent watch-cally asocial foraging strategy of female chimpanzees

and the number of food competitors in large mixed-sex ing chimpanzees in the 1960s. Comparisons between chimpanzees and bonobos therefore suffer from theparties alongside whom the swollen females must

forage. scantiness of the data on bonobo behavior, allowing in- terpretations based more on perceived contrasts withGoodall (1983) argued that females in each chimpan-

zee community belonged to one community only; they chimpanzees than on observational evidence from bo- nobos. While the evidence for chimpanzee behaviorwere wary of other community territories and might be

ambushed while foraging in a territorial overlap zone. may be subject to interpretation, there can be no ques- tioning the fact that hunting is a primarily male activ-Wrangham (1979) argued that female home ranges were

relatively fixed and that they might be part of more than ity, that lethal aggression occurs between communities, and that these are characteristic of chimpanzees in theone community over which the males ranged; the idea

that males attempt to maximize territory size as a way wild across the African continent. The history of prima- tology has been composed of a series of new paradigmsto encompass more females’ ranges for male reproduc-

tive advantages follows from this point of view. Data to explain accumulating new data. These often involve dichotomies that are shown later to be false; for exam-from some study sites tend to support Goodall’s view;

Hasegawa (1990) has shown that the concept of females ple, the male-philopatric versus female-philopatric di- chotomy has been called into question (Moore 1984a,and males occupying separate ranges is untenable for

Mahale chimpanzees. Strier 1994). Such models tend to be predictive for a time, but as new, contradictory data accumulate they become obsolete. The dichotomy currently drawn be- tween the social systems of chimpanzees and bonobos

Influences on Our View may not accord well with field data. Second, although many of the most detailed studiesof Great-Ape Societies

of intragroup social dynamics among living primates come from captive colonies, captive behavior fre-It is clear that much of the research on these two inten-

sively studied apes remains fraught with untested as- quently differs from behavior in the wild. In the case of bonobos, early captive studies demonstrated behaviorssumptions. In the search for behavioral patterns that

may be adaptations shared by humans and chimpan- that became the focus of much public and scientific at- tention (e.g., de Waal 1987). Bonobos engage in a richzees, the behavioral traits of chimpanzees and bonobos

discussed here—hunting, reproductive behavior, mat- array of sociosexual behaviors in the wild, but the fre- quency of the behaviors is much lower than in captiv-ing systems—have been the most often mentioned. In

this final section I consider some underlying influences ity. Captivity produces heightened frequencies of many behaviors for a variety of reasons, among them releasethat may help to account for the ways in which both

primatologists and the public understand the societies from the need to forage, greater opportunities for social interaction, and enforced proximity and boredom.of these two apes.

The primary reason for change in our ideas about Orangutans are, for example, highly sociable in captiv- ity relative to their solitary wild counterparts. Whilegreat-ape societies over time is the accumulation of

new data. Research findings and their interpretations there is much to be gained from the captive study of be- haviors that are impossible to record well in the field,are strongly influenced by the simple accumulation of

knowledge about a species until a particular behavioral biases are introduced into our interpretation of species- typical behavior because of the way in which captivitytrend becomes evident or it becomes possible to recon-

cile a set of seemingly unrelated behavioral facts using influences behavior. Third, contextual biases may emerge from the cir-a single paradigm. The paradigm formation may itself

be subject to social influences, because research biases cumstances in which the research is done. They repre- sent the situating of ideas and interpretations of evi-lead one to collect some types of data rather than others

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stanford Chimpanzees and Bonobos 407

dence in terms of the perspective the researcher brings equally close, and equally relevant to an understanding of human evolution. While this has delighted some, itto the research. These influences are pervasive (though

whether they fundamentally change the doing of sci- obviously disturbs others. Two strategies have emerged to keep bonobos at a dis-ence is open to debate). The behaviors at the heart of

the chimpanzee-bonobo interspecific variation—sexu- tance so as to preserve chimpanzee-based scenarios of human evolution, which traditionally emphasize war-ality, power and dominance, aggression—are those that

also lie at the center of the debate about human gender fare, hunting, tool use, and male dominance. The first strategy is to describe the bonobo as an interesting butissues and what molds our own behavior. Ortner’s

(1974) argument that men are to women as culture is to specialized anomaly that can be safely ignored as a pos- sible model of the last common ancestor (see Wrang-nature may be reflected in a more recent version that is

evident in popular-scientific portrayals of these two ham and Peterson 1996). The second strategy, adopted by Stanford, is to minimize the differences between theapes: chimpanzees are to bonobos as men are to women.

A recent account of the evolutionary continuity of hu- two Pan species: if bonobos behave, by and large, like chimpanzees, there is no reason to question the latterman violence from an ape ancestor makes a strong case

for chimpanzees as the referent models for the behavior species’s prominence as a model. Let me review the fac- tual basis of some of Stanford’s similarity claims:of modern human males (Wrangham and Peterson

1996). Murder, sexual coercion, hierarchy, and striving Rate of sexual behavior. In arguing that the rates of sexual behavior in bonobos and chimpanzees are simi-for status are all traits that Wrangham and Peterson as-

cribe to chimpanzees as well as to human males. De lar, Stanford counts only copulations between males and females. This is indeed the bulk of sexual activityWaal’s recent (1997) account of bonobos ascribes to

them characteristics often used to describe women: in the chimpanzee, but the bonobo has sex in virtually all possible partner combinations: male-female sex isnonaggressive, sensual, power-sharing, strong through

alliances rather than individually. He writes, ‘‘The not even the most common pattern. Genital rubbing among females, the most typical pattern of the species,chimpanzee resolves sexual issues with power; the bo-

nobo resolves power issues with sex’’ (p. 32). While is absent in chimpanzees. This pattern is conveniently ignored in the calculations. Including all sexual encoun-these characterizations are based on observational data,

they may also be influenced by views of the two apes ters, I have reported a much higher interaction rate among bonobos than chimpanzees (de Waal 1995 andthat accord with human male and female gender stereo-

types. These stereotypes are influenced by the public’s fig. 1). Effects of captivity. The argument that the high ratedesire for explanations of the roots of human behavior.

This issue has risen to enough prominence that the of sociosexual activity in captive bonobos might be at- tributable to confinement fails to consider that thenewsletter of the American Anthropological Associa-

tion recently devoted a series of columns to the treat- above comparison is not with wild chimpanzees but with captive ones. Why are chimpanzees not similarlyment of biological anthropology by the media. The por-

trayal of humans as at an evolutionary crossroads, able affected by confinement? Only captive studies control for environmental conditions and thereby provide con-to choose the bonobo’s sensuous ‘‘Make love, not war’’

nature or the chimpanzees warring, status-striving na- clusive data on interspecific differences; field studies usually concern different species under different ecolog-ture, finds an eager audience. Whether current images

of chimpanzee and bonobo societies and the dichotomy ical conditions. Peacefulness. Given our current knowledge, it is en-between them accord well with field data remains for

future fieldwork to determine. tirely correct to describe bonobos as relatively peaceful. In captivity, bonobos show less violence and consider- ably higher rates of reconciliation following fights than chimpanzees. Bonobos are by no means lacking in ag- gression, however, and despite their reputation they areComments actually less tolerant in relation to food than chimpan- zees (de Waal 1992). In the field, lethal intercommunity aggression, forced copulation, and infanticide havefrans b. m. de waal

Living Links Center and Psychology Department, never been observed. Stanford is not the first, however, to warn that such behavior may yet be discovered (deEmory University, Atlanta, Ga. 30329, U.S.A.

([email protected]). 24 iii 98 Waal 1989:221). Female dominance. If a male chimpanzee chases a fe-

male away from his food, we generally attribute this toIn the same way that paleontologists prefer their fossil finds to belong to a human ancestor rather than to an his dominance. This rule has been followed by etholo-

gists for every species on the planet, but now we learnextinct side-branch, experts on ape behavior like to claim that their subjects are the only or best model of that female bonobos ‘‘are dominant only in the arena of

feeding priority.’’ It is claimed that if we look beyondthe last common ancestor, Chimpanzee researchers are used to this situation, routinely describing the chim- feeding priority the relations between the sexes in bo-

nobos and chimpanzees are more similar. This is basedpanzee as humanity’s closest living relative. There ex- ists another relative, however, that is equally alive, on a study by Wood and White (1996) that failed to iden-

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408 current anthropology Volume 39, Number 4, August–October 1998

unique social features from surfacing and why attempts are still being made to push it to the sidelines. Anyone interested in the reconstruction of our evolutionary past will need to face the implications of having a sexy, female-centered close relative.

barbara fruth Max-Planck-Institut für Verhaltensphysiologie, 82319 Seewiesen, Germany. 20 iii 98

Stanford is to be congratulated for his attempt to focus on the similarities rather than on the differences be- tween chimpanzees and bonobos. I agree that the em- phasis so far put on the behavioral dichotomy between the two Pan species may be due to the relatively briefer study of bonobos from only two major sites compared with the longer-term investigations of many study sites of chimpanzees. Nevertheless, the combined data set of only these few studies, mostly at Wamba and Lomako, allows Stanford to place the bonobo within the behav- ioral range of chimpanzees. He excuses the remainingFig. 1. Mean (1 SEM) number of sociosexual acts behavioral gaps between the Pan species by a lack ofinitiated per hour per individual for the San Diego published data from the wild and ends his comparisonbonobos and an outdoor colony of chimpanzees at with an appeal for future field research to seek data thatthe Yerkes Primate Center’s field station, separately will eventually allow systematic treatment of the ap-for adults and adolescents (black) and younger parent dichotomy. However, published literature is al-individuals (hatched). The adult rate was significantly ready available that would allow some of the gaps to behigher in the bonobo group despite a reduced number filled and would make his point even stronger.of available partners compared with the chimpanzee Discussing the differences in meat eating betweengroup. The juvenile rates of the two species did not the two Pan species, Stanford argues chimpocentrically,differ. From de Waal (1995). as if blinded by the quantity and quality of Pan troglo- dytes’s favourite prey, red colobus monkeys. This is al- most as if a Texan consuming a T-bone steak daily were to consider a Bavarian savoring a pork roast on Sundaystify male and female bonobos individually; possibly

some males in this community were able to chase some a vegetarian because it was pork instead of beef and be- cause it was consumed only occasionally. At Lomako,females and did so frequently, but a pooled analysis

would show the class of males dominating the class of Pan paniscus regularly kills and eats adult duikers, Cephalophus spp. (Hohmann and Fruth 1993, 1996).females. Other investigators of the same community

did achieve individual recognition and claim obvious fe- Admittedly, the amount of animal prey killed and eaten by bonobos at Lomako is not comparable to that re-male dominance (Fruth and Hohmann, cited in de Waal

1997:79–80). Similarly, at another bonobo field site corded for chimpanzees, but whether meat eating has nutritional or social significance has yet to be clarified.Furuichi (1997) noted that the alpha female could chase

high-ranking males and that the alpha male sometimes The smaller the amount of a nonetheless regularly con- sumed food item the more it might be compensation forretreated for low-ranking females. Furthermore, in all

captive groups that I know female bonobos dominate a nutritional deficit (such as trace elements) or self- medication (Huffman 1997).males—an enormous contrast with chimpanzees (e.g.,

Parish 1994). If sharing fulfills a political function, the shared item need not be meat. At Lomako fruits such as TreculiaFinally, when Stanford speculates about the sociocul-

tural context of the current fascination with bonobos, africana or Anonidium mannii, weighing on average 10–15 kg, are regularly shared by bonobos (Hohmannit would be good to include an analysis of why it has

taken so long for scientists to discuss the matrifocal na- and Fruth 1993, 1996)! They are seasonally available and during that time make up much of the daily diet.ture of bonobo society and the species’s rich sexuality.

It is no accident that the first time Frans Lanting and Again, their nutritional value can be disputed but their the social value cannot. Therefore, Stanford’s interpre-I worked together on an illustrated account of bonobo

society we did so for GEO Magazine; U.S. publishers tation of the apparent missing need for social or politi- cal ceremonies in bonobos, drawn from the low fre-panicked at the thought of a full story. Rather than con-

cluding that the bonobo seems a species made for the quency of consumption of animal prey, seems misconceived. Perhaps he takes a typically male viewmedia, the question is really what has hampered its

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stanford Chimpanzees and Bonobos 409

of politics. Is it so hard to imagine that female bonobos ing the past decade or more, researchers at Wamba have consistently conducted observations away from artifi-might hunt, kill, and share for reasons similar to

males’? cial feeding sites, following the bonobos throughout the day in various parts of their range (Hashimoto and Furu-At Lomako, female bonobos hunt, possess, and dis-

tribute meat. Between 1990 and 1997 we saw seven ichi 1994, Ihobe 1992, Ingmanson 1996, Ono-Vineberg 1997). In addition, it has also been possible to observecases of the sharing of a captured duiker, all but one of

which were adult. Each time, females had possession of neighboring unit-groups (K, S, B) for short periods of time, providing comparisons between well-habituatedthe carcass and shared mostly with other females;

males only occasionally got a share. The rate of fruit groups and those that were less so. One clear difference I observed was that poorly habituated groups spent con-sharing was 15 times greater than that of meat, and

again it was almost always females that owned the food siderably more time in the trees, both for traveling and for resting, than did habituated groups, which fre-and controlled its distribution.

Cooperation by unrelated individuals and the re- quently rested, groomed, played, and moved on the ground.sulting control of key resources is not self-evidently

sex-biased in a male-philopatric society. Bonobo fe- Stanford’s statement concerning the defense of terri- tory by bonobos at Wamba also needs examining. Themales cooperate, and the frequent sociosexual interac-

tions that occur during these sessions may reinforce unit-groups there do not have exclusive ranges. For ex- ample, in 1990–91 the E2 group ranged over approxi-their political ties as well as the act of sharing itself.

Instead of asking why bonobos are not avid meat eaters, mately 45 km2 (Ingmanson 1996), about half of which was also utilized by neighboring unit-groups—E1 onperhaps we should ask why chimpanzees share only

meat. the south, K on the east, S on the north, and B on the west. Only a central part of the range was used exclu- sively by the E2 group during that period of observation. Intergroup interactions occur in these regions of over-ellen j. ingmanson

Dickinson College, P.O. Box 1773, Carlisle, Pa. lap. A unit-group may defend a feeding spot on a partic- ular day, using extensive vocalizations and intimida-17013-2896, U.S.A. 30 iii 98 tion displays, but it may also settle down after some time and feed side by side with the neighboring unit-Stanford presents a timely and needed discussion on the

use of chimpanzees and bonobos as referential models group. In October 1990 this occurred almost daily be- tween E2 and K (Ingmanson, unpublished data). The Sfor understanding the evolution of human behavior,

questioning some of the generalizations that have been group could always displace the E2 group, again making generalizations difficult, but this is clearly not territo-made about these species. Perhaps one of the most im-

portant points to take away from this article is the dif- rial defense in the traditional sense used by most prima- tologists.ficulty of generalizing about either chimpanzees or bo-

nobos at all. What has become clear from research over I agree with Stanford that ‘‘it is probably not true that male bonobos are not affiliative with each other.’’ Ithe past few decades is the variability of behavior

within the genus Pan, both geographically and tempo- have, in fact, observed frequent grooming between males, especially in the E2 group. It was possible to rec-rally. As Stanford says, some of this is clearly the result

of the changing focus of research questions, the gradual ognize affiliations between pairs of males based on grooming and proximity that remained the same be-build-up of observations of infrequent behaviors, and

differences in habituation, but it is also important to tween 1987 and 1991. This is the kind of behavior, though, that requires extensive observation away fromkeep in mind the adaptability of chimpanzees and bo-

nobos to changing ecological and demographic condi- feeding sites to elucidate. Stanford notes that hunting by bonobos may be lesstions. The social structure of a community may truly

be different when examined over a long period of time. frequent than hunting by chimpanzees because female bonobos have greater control of food resources. ThisBecause our understanding of chimpanzee and bo-

nobo behavior will change as our information increases, control can clearly be seen in cases where predation has been observed (Ingmanson and Ihobe 1992). When ait is critical that we utilize the most up-to-date and ac-

curate information when attempting to generalize or high-ranking adult female of the E2 group captured a flying squirrel, she proceeded to share it with otherdevelop models. One aspect that is frequently misrepre-

sented has to do with levels of habituation and the ex- adult females and their offspring. None of the carcass went to any of the adult males, however, even thoughtent of artificial feeding at research sites. Stanford says

that ‘‘at Wamba, bonobos have long been habituated to the highest-ranking male of the group had a temper tan- trum on a branch below the feasting females.observation in an artificial sugarcane plantation.’’

While this is true, it suggests that all observations at A great many inaccuracies have crept into the realm of ‘‘common knowledge’’ concerning both bonobos andWamba have been conducted under artificial feeding

conditions, which is not true. Three unit-groups (E1, E2, chimpanzees. These are maintained by referring only to early studies or captive data, both of which may giveand P) are well habituated to human observations

whether in the forest or in an artificial feeding site. Dur- false impressions. The media and popular writings are

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410 current anthropology Volume 39, Number 4, August–October 1998

particularly bad about this, but scientists are not im- chimpanzees. Stanford needs to address the possible ef- fect of differences in group size for this point to be clari-mune, as can clearly be seen in the treatment of bonobo

sexuality. Bonobos do engage in extensive sexual behav- fied. Intergroup relationships. I think the most marked so-ior, though recent field studies suggest that the differ-

ence from chimpanzees in this regard may be less than cial difference between the two Pan species lies in in- tergroup relationships. A variety of intergroup affilia-previously thought. From my own observations of both

chimpanzees and bonobos under both field and captive tive interactions such as copulation, greeting, grooming, and social play are observed during the en-conditions, where a chimpanzee will predictably use ag-

gression in a situation a bonobo will use sex. Bonobos counters of the E1 group with the P, E2, and B groups at Wamba. In contrast, often lethal aggression char-do engage in aggressive behavior, though, and chimpan-

zees do seem to use sexuality to manipulate social situ- acterizes intergroup relationships in chimpanzees. Stanford argues that there may be lethal or injuriousations. The emphasis on the kind of behavior, I believe,

differs between the two species. What bonobos are par- intergroup aggression in bonobos as well, since chim- panzees were observed for more than 15 years andticularly good at is coordinating group activities, from

feeding to travel, and sex, as well as communication, is thousands of observer-hours before lethal aggression was seen. This may indeed be so. I once found a severea part of this. We must keep in mind that what Pan of-

fers us is examples of the range of possible adaptations laceration on the foot of a young adult male of the E1 group on his rejoining the main party after days of sepa-for an intelligent hominoid while we attempt to main-

tain scientific objectivity in our interpretations. ration that might have resulted from intergroup aggres- sion. However, the presence or absence of lethal in- tergroup aggression does not count for much, as the overall peaceful nature of bonobos is much more impor- tant in the social comparison between the two species.takayoshi kano

Primate Research Institute Kyoto University, Are there any comparable observations of intergroup af- filiative interactions in Gombe chimpanzees during theInugama, Aichi 484, Japan. 25 iii 98 thousands of observer-hours before and after the first observation of intergroup killing?Stanford has presented a good review of the behaviors

of wild chimpanzees and bonobos and concludes that Infanticide. Infanticide, on which Stanford makes lit- tle or no comment, is another important issue if socialthey are similar behaviorally. I too have argued that

they have basically similar social systems of fission-fu- characteristics are to be compared between the two spe- cies of Pan. An infrequent but regular behavior in chim-sion multimale polygyny and female dispersal. How-

ever, I disagree with Stanford on several points and still panzees, it has been explained from the viewpoint of male reproductive strategies; male chimpanzees aresee a behavioral dichotomy between the two species of

Pan. said to kill infants to decrease the genes of extragroup males and simultaneously to induce estrus in females.Male-female dominance. At both Wamba and Lo-

mako, females are dominant in the feeding context; fe- There is no observation of infanticide in bonobos. More- over, adult bonobo males at Wamba carry infants formales frequently supplant males while the reverse oc-

curs much less. Stanford argues that the pattern of short times on occasion, and infant carrying and care are exhibited even by adult males of different groups.dominance in bonobos resembles that of chimpanzees

if social dominance is considered separately. Priority of The mothers of such infants do not respond nervously to these males. It is indeed difficult to conclude that in-access to food is, however, an important function of

dominance. Since most dominance interactions and vir- fanticide does not exist in bonobos, but the observa- tions so far indicate that, if it occurs at all, it is muchtually all agonistic episodes between adult females and

males occur in feeding contexts, I find much less mean- less frequent than in chimpanzees. Prolonged mother-son relationships. Bonobo malesing in dominance occurring in the non-feeding context.

Moreover, there is no difference between feeding and maintain close and intimate associations with their mothers throughout their shared lifetimes. The strongnon-feeding dominance relationships among the bo-

nobos of Wamba. For example, approaches of dominant and prolonged mother-son bond is one of the most im- portant social features in bonobos since it influencesfemales often give rise to submissive reactions by

grooming males such as grinning, bending away, etc. male dominance and, to some extent, interrupts the rigid male-male bond that is a major social trait inCopulation rate. Stanford stresses that, according to

Takahata et al. (1996), both adult females and males at chimpanzees. This point also is not addressed by Stan- ford.Mahale copulate at a higher mean rate than do those of

Wamba. For bonobos, Takahata et al. used the data from As I have shown here, bonobos show some marked contrasts in social features with chimpanzees. The in-the E1 group after the fission of the E group into E1 and

E2. The copulation rate for each bonobo in the E1 group terspecific differentiation in social influence by either sex is well reflected in these social differences: femaleshad dropped dramatically after this fission, possibly be-

cause of the decrease in group (community) size from are more influential in bonobo society and males more influential in chimpanzee society. This dichotomy is72 to 30. The Mahale M group consisted of about 100

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stanford Chimpanzees and Bonobos 411

not influenced by popular wishes as Stanford argues but getting to communication (McGrew 1992). This may be the crucial difference between these two sibling species.comes from direct field observations.

w. c. mc grew katharine milton Department of Anthropology, University ofAnthropology and Zoology, Miami University,

Oxford, Ohio 45056, U.S.A. 5 iii 98 California, Berkeley, Calif. 94720-3710, U.S.A. 17 iii 98

Jane Goodall once said that we will not understand the real differences between chimpanzees and humans un- The close genetic relationship between chimpanzees,

bonobos, and humans and, of all extant apes, theirtil we first accept their many similarities. The same ar- gument applies to chimpanzees and bonobos, as admira- unique suitability as possible analogues for some stage

of protohuman evolution (Milton 1987, Milton andbly advanced by Stanford, but the case is even stronger than he states. Demment 1988) make speculations about their social

behavior particularly compelling. Information on eitherEcologically, Pan paniscus is not confined to rain for- est but like P. troglodytes also ranges into woodland sa- species is far more likely to provoke interest and discus-

sion in academic and popular circles than, for example,vanna, as shown by recent field research in Congo (108′ 48″ S, 21′ 20″ E) by Thompson (1995). Further fieldwork comments on the social behavior of the potto. As Stan-

ford points out, there is also a tendency to try to moldwill likely yield even more ecological diversity in the range of bonobos. our perceptions of the behavior of these two apes into

models of what we view as ‘‘most proper’’ for humanReproductively, it is not clear that there are any dif- ferences within or across populations or species of Pan ancestors. Those who prefer a peaceable kingdom lean

toward the image of the female-empowered ‘‘Make lovein length of menstrual cycle or proportion of the cycle taken up by maximal swelling (Takahata et al. 1996). not war’’ bonobo, while those inclined more toward

‘‘Nature red in tooth and claw’’ embrace the image ofAll of the apparent variation in Stanford’s table 1 could be due to sampling error: Kano’s (1996) mean length of the male-bonded, predatory, and aggressive chimpan-

zee. Stanford suggests that some features of the social33 days and Furuichi’s (1987) of 42 days for bonobos at Wamba come from N’s of only 8 and 6 cycles. Other behavior of these two ape species may be more similar

than has been appreciated—the emphasis on one or an-sources of variance include whether cycles of imma- ture, aging, or pregnant females are part of the calcula- other of these postulated interspecific differences hing-

ing, perhaps unconsciously, on the appeal of one or thetions. The only statistically proven species or popula- tion difference in cycle length comes from sample sizes other image as a more satisfactory or politically correct

ancestral model for our own genus and species.of only 4 P. paniscus and 9 P. troglodytes in captivity (Dahl, Nadler, and Collins 1991). In this context, it is worthy of note that a somewhat

similar situation exists in terms of some features of theHierarchically, is there any convincing evidence of fe- male dominance over males in nature outside of the dis- social behavior of wild spider monkeys (Ateles spp.).

Like chimpanzees and bonobos, all spider monkey spe-torting content of the artificial feeding area? (The Wood and White [1996] reference cited is only an abstract, so cies show a fission-fusion pattern of social organization.

However, study of A. paniscus in Surinam showed thatthe data are not available for scrutiny.) Description of the primary goal of genital rubbing as the easing of in- adult males were almost invariably encountered in sub-

groups with adult females and immatures rather than intracommunity tensions seems to be a remarkably pub- lic-spirited interpretation of what is usually thought of all-male associations, which rarely occurred; long calls

(whoops) were given exclusively by males, and foodas a self-serving act. It is hard to know what to make of meat-eating rates long calls at fruiting trees appeared to discourage rather

than encourage other subgroups to join the caller(s) (vanat Wamba if most of the data come from the artificial provisioning area. Until day-long follows of focal sub- Roosmalen 1985). In contrast, on Barro Colorado Island

in Panama, males of A. geoffroyi are most frequentlyjects are reported for bonobos, it is hard to compare their hunting with that of well-habituated chimpanzees found in tightly bonded all-male associations rather

than with females and immatures (Eisenberg and Kuehnat Gombe, Mahale, or Taı̈. If hunting is important to understanding the social 1976, Milton 1993). There are no systematic field data

on long-call initiation by spider monkeys on Barro Colo-behavior of Pan spp., then so too is elementary technol- ogy. Both involve social learning and food sharing. Here rado Island, but observations suggest that males give

most such calls; however, in contrast to the situationa stark difference between P. paniscus and P. troglo- dytes does emerge: Neither behavioral nor archeologi- in Surinam, other spider monkey subgroups may then

join the caller(s). To add complexity, study of anothercal data from wild bonobos show them to be tool users of any note. They show no subsistence technology (Ing- call (whinny) by A. geoffroyi in Costa Rica shows that

it is given more frequently by females than by malesmanson 1996). In contrast, all long-term studies of chimpanzees (including Bossou, not cited by Stanford) and more frequently by dominant than by subordinate

animals and that on hearing such calls other subgroupsshow varied tool kits that range in function from food

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412 current anthropology Volume 39, Number 4, August–October 1998

frequently joined the caller(s) to feed (Chapman and Le- ary tale. For example, in his figure 1, the closest agree- ment occurs between points G and K, representing sitesfebvre 1990).

Why these behavioral differences exist in spider mon- that have a primary investigator in common (Richard Wrangham); the next level of clustering appears to placekeys is not known. Longer study at each site may show

that such differences indicate points on a continuum of K, G, and L (where most researchers have been Euro- pean or American) together, with the predominantlypotential spider monkey social behavior, reflecting per-

haps the particular composition and relationships of in- Japanese sites M and W separate (L and W represent bo- nobos). Do methodological and/or definitional differ-dividuals in the community at the particular time each

study was made or some other factor(s) such as food ences overwhelm taxonomic and ecological ones? Many factors are involved in our attempts to distinguish anddensity and distribution. However, since spider mon-

keys are not generally regarded as possible analogues for define pongid reality, and, as Stanford suggests, our views of apes are subject to strong biases because, insome stage of human evolution, these apparent behav-

ioral differences within and between the sexes in spider part, they reflect biases about ourselves. After that initial surprise, some readers might feelmonkey species and populations have not been inter-

preted in the same light as those of chimpanzees and smug about progress in their own fields, but this would represent a serious misunderstanding. The reason we dobonobos.

By directing our attention to the need for more data not ‘‘understand chimpanzees’’ (or bonobos) is the same as the reason that after about 2,000 years of formal in-on both ape species and particularly bonobos, Stanford

provides a valuable perspective—we do not have to look quiry we still cannot say confidently that we ‘‘under- stand humans.’’ As long as we see tribes, cultures, spe-far into the past to recall how, as more field data

emerged, the sunny image of the playful, fruit-eating cies as categorically unique examples of different essences, we are not likely to get much beyond namingchimpanzee at Gombe was gradually revealed to have a

darker side which included the enthusiastic hunting of the beasts of the field and the birds of the air. For example, there is debate over whether Taı̈ chim-animal prey, savage attacks on chimpanzee neighbors,

and, at times, cannibalism. Who can say what a longer panzees are ‘‘bisexually bonded,’’ unlike the ‘‘male- bonded’’ community described for Gombe (Boeschperiod of time spent studying wild bonobos will reveal?

Perhaps in fact all mammal species, just like us, have 1996, Doran 1997), and a similar though less marked difference has long been noted between Gombe and Ma-both a lighter and a darker side?

Stanford has done a good job both of reviewing the hale (Kawanaka 1984). It also appears that Taı̈ lacks the greater male relatedness observed at Gombe (Gagneux,available information and of directing attention to the

potential biases and preconceptions we may bring to Boesch, and Woodruff n.d.). As Stanford shows (and both Boesch and Doran note), bonobos can be seen inour research and its interpretation. Future fieldwork

should clarify just how different the chimpanzees and some sense as exhibiting an extension of the trend among chimpanzees toward larger, more stable partiesbonobos are in their social behavior and provide some

explanations for differences observed. Regardless of in less seasonal habitats. This trend obscures the cate- gorical meanings of ‘‘male-bonded’’ and ‘‘bisexuallywhat is ultimately concluded about these ape species,

whether the roots of human behavior stem from ances- bonded’’; since average degree of relatedness and aver- age party size/duration can in principle vary continu-tors more closely resembling the present-day image of

the common chimpanzee or that of the bonobo will ously across the full possible range, trying to determine the truth value of the assertion ‘‘chimpanzees are male-likely continue to be fruitlessly debated. However, if

forced to choose between the two current popular im- bonded’’ is like answering yes or no to the question ‘‘Are humans monogamous?’’ Altmann and Altmannages of these two apes, after some 25 years spent in an-

thropology departments I believe I’d have to cast my (1979) pointed out 20 years ago that such subtly differ- ent sociodemographic settings can have profoundly sig-vote for the common chimpanzee! nificant behavioral consequences.

Discovering the degree to which taxonomic catego- ries (and, by implication, genes) constrain sociodemo-j im moore

Anthropology Department, University of California, graphic continua is a central goal of primatology. Only by recognizing the underlying conceptual continuitySan Diego, La Jolla, Calif. 92093-0532, U.S.A.

([email protected]). 30 iii 98 can the meaning of local perturbations due to phylog- eny be understood; only by recognizing the nonphyloge- netic forces promoting categorical essentializing can weAfter decades of research at multiple sites, it is perhaps

surprising that we do not yet understand chimpanzees understand and compensate for them. This paper is a real contribution to this effort.and bonobos well enough to tell them apart with confi-

dence. Because of their utility as referential models of However, Stanford does not escape essentializing. A minor example: ‘‘eventually, female chimpanzees es-human ancestors and the ease with which such models

become conflated with those ancestors (Moore 1996), it tablish themselves as members of a new community’’ implies that this is universal; it is not (Moore 1993).is especially important to understand what we know

and do not know about these apes (see, e.g., Moore Sweeping the up to 50% of females who remain in their natal communities (Pusey, Williams, and Goodall 1997)1992). Stanford’s paper represents an important caution-

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stanford Chimpanzees and Bonobos 413

under the archetypal rug can only obscure the reasons and chimpanzees are behaviorally more similar than they are commonly portrayed is unconvincing. For in-most of them emigrate. A more significant example:

Stanford points out that our extravagant view of bonobo stance, until intensive study of the bonobo began there was no evidence that either female bonding or femalesexuality is based largely on captive studies and implic-

itly dismisses these as ‘‘not reflect[ing] naturalistic mat- dominance over males occurred routinely within any of the living Hominoidea. Recent captive studies of bo-ing patterns.’’ Perhaps not, but if bonobos use sex to

‘‘cope’’ with social stress in ways that chimpanzees do nobos, however, reveal that females are remarkably skillful in establishing and maintaining strong affilia-not, then elevated sexuality in captivity for one but not

the other is perfectly understandable and provides in- tive bonds with one another. In grooming, body contact, playing, following each other, and staying in proximity,sight into how these apes work. ‘‘Captive artifacts’’ are

only scientifically misleading if one assumes that there females preferentially select other female rather than male partners (Parish 1996). Moreover, females controlis one species essence best revealed in one type of set-

ting. access to highly desirable food, share it with each other more often than with males, engage in same-sex sexualFinally, Stanford states that ‘‘males sometimes offer

meat to females and receive matings in the process’’; interactions to reduce tension, and form alliances in which they cooperatively attack males and inflict‘‘in the process’’ is ambiguous but implies temporal

proximity and a causal connection. The sources cited do blood-drawing injuries (Parish 1996). Females preferentially associate with each other innot support this statement. Females in estrus are more

successful at begging for meat from males (Teleki 1973), the wild too: 20% of party compositions in Lomako contained only females (average 2.48 females/partyand males are more likely to hunt in the presence of

swollen females (Stanford et al. 1994). Males appear to [Fruth 1995]). Fruth (1995: vii) asserts that ‘‘females show a high degree of association, form coalitions, anduse meat tactically amongst themselves in status poli-

tics (Moore 1984b, Nishida et al. 1992). Females are dominate the society’’ (on the basis of 4,400 field hours and 1,200 hours of direct observation in Lomako frommore likely to engage in restrictive (i.e., temporarily ex-

clusive) mating with males who, on average, share meat 1990 to 1994). Like their captive counterparts, bonobo females inmore frequently with females (Tutin 1979). Finally, fe-

males who receive meat more frequently tend to have the wild control highly valued food resources such as duikers (Hohmann and Fruth 1993), displace males (ex-greater reproductive success (McGrew 1992).1 None of

these studies directly address the ‘‘process’’ responsible cept for sons of dominant females) from key feeding sites, aggressively chase and attack males, and inter-for the patterns. It would be surprising if chimpanzee

meat sharing were not involved in complex feedback vene in (and apparently sometimes decide the outcome of) male-male disputes involving their sons. Even theprocesses contributing to long-term male-female rela-

tionships, sexual and other (analogous to male-male re- social status of a fully adult male is greatly influenced by his mother’s rank. A formerly high-ranking male be-lationships [Moore 1984b]). However, the only attempt

to test this notion found no support for it (Hemelrijk, comes peripheralized upon his mother’s death—thus son’s rank is influenced by mother’s rank rather thanvan Laere, and van Hoof 1992). Stanford may be correct,

but aside from this one study of captive chimpanzees vice versa (Furuichi 1989, Idani 1991, Ihobe 1992). Stan- ford’s suggestion that males defer to females rather thanthe problem simply has not yet been formally been ex-

amined. As Stanford et al. (1994) point out, there are no females’ dominating males is unparsimonious to say the least: how often has dominance behavior in maledata showing that the sharing male receives extra copu-

lations from swollen female recipients as a result of his chimpanzees been ascribed instead to female deference? The assessment that the bonobo pattern is mere malesharing. ‘‘deference’’ or ‘‘female feeding priority’’ is based upon one abstract reporting chasing and fleeing interactions involving unhabituated, unidentified individuals overamy r. parish

Department of Anthropology, University College an unspecified observation period (Wood and White 1996). Yet observations of female aggression coupledLondon, Gower Street, London WC1E 6BT, U.K.

(A. [email protected]). 31 iii 98 with male submission are available for identified habit- uated individuals from both the Lomako and the Wamba research site (e.g., Fruth, cited in de Waal 1997;The most unusual and striking aspects of bonobo soci-

ety are either ignored or inadequately addressed in Stan- Furuichi 1989, 1997; Kano 1987, 1990; references in Ihobe 1992). Although males in the wild are not se-ford’s article, and therefore the argument that bonobos verely injured by females (perhaps because escape op- portunities are enhanced in an unconfined environ-1. McGrew failed to correct for female ages; when this is done, the ment), they certainly cower and flee when females acteffect is nonsignificant for survival to 1 year (U 5 6, p 5 0.222, two-

tailed) but becomes marginally significant for infants surviving to aggressively. 5 years (U 5 3, p 5 0.056). That the effect increases with infant age Intergroup interactions (characterized here as aggres- is intriguing in light of nutritional arguments; given a relationship sive and territorial in both species) in fact illuminatebetween female rank and meat access (Boesch 1994), one wonders

another striking difference between bonobo and chim-what might be the relationship among meat access, rank, and fe- male reproductive success (cf. Pusey, Williams, and Goodall 1997). panzee social systems. Bonobo intergroup encounters

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414 current anthropology Volume 39, Number 4, August–October 1998

very rarely involve any contact aggression and instead Given the behavioral flexibility of both species, com- bined with the often profound intraspecific differencesrely upon vocal exchange (Idani 1990, Ihobe 1992). Even

more remarkable, females freely mate with males from between study populations, it is difficult to identify spe- cies-typical social behaviors that reliably separate theother groups in the presence of males from their own

communities (e.g., Idani 1990), a nearly unimaginable two chimpanzees. In many respects there is a contin- uum between the two species, often depending on eco-scenario for chimpanzees.

Territoriality in bonobos is much relaxed relative to logical conditions. For example, when female chimpan- zees are in large food trees, they groom each other atthat in their congener. More than 66% of the home

range of one Wamba community overlaps with those of frequencies comparable to bonobos (Ghiglieri 1986). Male affiliation is more difficult to compare becauseother groups (Kano and Mulavwa 1984). Bonobo males

travel alone more often than would be expected from grooming may reflect tension reduction among compet- itors (de Waal 1987). Male P. troglodytes frequentlythe socionomic sex ratio (Fruth 1995), which would not

be predicted if males were in danger from males in other groom one another, as do male P. paniscus at Wamba. Affiliative behavior is considerably less frequent amongcommunities. Chimpanzee males found traveling alone

by males from other communities, in contrast, are often male P. paniscus at Lomako (White 1992), where parties are small and unprovisioned. However, at Wamba par-killed.

Finally, the most obvious chimpanzee/bonobo differ- ties are considerably larger, to the extent that one com- munity is considered to be in contact for the entire dayence in sexual behavior is ignored: sexual behavior in

bonobos encompasses all possible age and sex combina- (Furuichi 1989). At Lomako, large groups with multiple males are rarely observed for extended periods of time,tions (e.g., de Waal 1990). Moreover, sexual interaction

is routinely used for nonreproductive goals (tension re- but when they do occur males that are normally intoler- ant of each other may engage in long and intense groom-duction, bartering for social favors, sex-for-food ex-

changes). ing bouts. However, these exchanges appear to be tense interactions rather than the relaxed grooming sessionsOne major similarity ignored in this review is that fe-

males of both species mate with males outside their more commonly observed between females. Therefore, males in groups that cannot or do not split may groomcommunities. Bonobo females mate openly during in-

tergroup encounters. Chimpanzee females in at least one another extensively as a component of competition over access to females. Clearly, the characterization ofone community manage to circumvent extensive male

mate-guarding strategies to conceive with males out- social bonding is complicated by the multiple functions of affiliative behavior reflected by the occurrence ofside of their own communities (Gagneux, Woodruff,

and Boesch 1997). grooming in both friendly and unfriendly contexts. Intraspecific variation in P. paniscus behavior mayWe expect similarities in two closely related species

within the same genus. Equally, we expect that varia- also complicate comparisons of reproductive ecology. For example, the reduced fission and fusion in thetion in ecological opportunity and constraint will have

led to diverse selective pressures and consequent differ- Wamba study communities may influence calculations of the number of estrous females in parties. When theences in behavior after speciation. An exclusive focus

on similarities does more than obfuscate half of the pic- whole community is together all parties will be scored as containing estrous females even if only one female isture: it is impossible to weight the importance of shared

traits without comparison with the species’ differences. in estrus. In contrast, because the communities at Lo- mako are commonly split into several smaller parties,A comparison/contrast (as well as an examination of

causal factors other than a rather postmodernist decons- the percentage of parties containing estrous females is usually low. In the 1984–85 field season, only 22% oftruction of the researchers) would be more likely to pro-

duce a strong contribution to our understanding of the parties contained fully tumescent females on the basis of simple counts of the number of parties containing re-behavioral ecology of the two Pan species. productive females in the two study communities (White, unpublished data). This is very different from the figure of 100% cited for Wamba in Stanford’s figurefrances j. white, kimberley d. wood, and

michelle y. merrill 1 and more comparable to the data on P. troglodytes at Gombe and Mahale. When all females are present in aDepartment of Biological Anthropology and

Anatomy, Duke University, Durham, N.C. 27708, group, males will presumably prefer to mate with the most swollen females. In contrast, in small parties lack-U.S.A. ([email protected]). 30 iii 98 ing a tumescent female, which are more common at Lomako, male mating choices may show more varia-Bonobos and chimpanzees are clearly closely related

and display many behavioral and ecological similarities. tion. Differences in methodology also complicate compari-The tendency to emphasize their differences is rein-

forced by the resistance of many to retaining the name sons of mating frequency at the Lomako and Wamba field sites. At Wamba, most observations are not fromof ‘‘pygmy chimpanzee’’ for Pan paniscus, on the

ground that Pan troglodytes must then be called ‘‘com- follows of focal animals (Furuichi 1987). At Lomako, fo- cal-animal sampling is used so that mating frequenciesmon.’’ Yet whatever the colloquial name, both are

clearly chimpanzees. can be calculated for individual females at different

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stanford Chimpanzees and Bonobos 415

table 1 and Wood n.d.). However, coalitions of P. paniscus fe- males can dominate males in provisioned and captiveFrequency of Mating by Females at

Lomako populations (Vervaecke, Van Elsacker, and Verheyan 1992, Parish 1994, Furuichi 1989). Coalitions at Lo- mako, while important, are rarer given the greater de-

Observed gree of fission and fusion and the smaller overall partySexual Matings Expected sizes. Female P. paniscus exhibit feeding priority with-Swelling While Focal Frequency

Size-Classa Animalb of Matingsc out female social dominance, implying that there is some form of male deference during feeding in this spe- cies. Males may use deferent behaviors to influence fe-0 2 2.9 male mate choice during the highly fertile period ofI 5 3.9

II 0 14.7 maximal tumescence. The seasonal paucity of econom- III 2 4.5 ically defensible, large food sources in P. troglodytes re- IV 0 0.4 stricts females from having large core areas and forming V 7 4.5

strong associations with potential female allies, thusVI 21 4.8 limiting the degree of female choice that can be ex-VII 0 1.3 pressed. The commonly cited dichotomy of ‘‘sex for power’’ in female P. paniscus versus ‘‘power for sex’’ in

source: White (1986). male P. troglodytes may be oversimplified; instead, fe-note: Observed and expected distributions are sig- male friendships may force P. paniscus males to use in-nificantly different (G 5 35.42, p , 0.001).

aSwelling classes increase in size, with class VII be- dividual chivalry rather than group power to obtain ing maximally tumescent. mating opportunities. bA frequency of zero does not mean that a female was not seen to mate but indicates that she did not mate while she was the focal animal. cBased on the proportion of focal sampling spent on a female with a swelling of that size-class. Reply

craig stanford Los Angeles, Calif., U.S.A. 24 iv 98stages of their sexual swelling (White 1986: table 1). The

results (table 1) show that although females mate at all stages of the cycle, they actually mate less than ex- I began working on this article on the social behavior of

chimpanzees and bonobos in a fit of devil’s advocacy. Ipected at full tumescence given the number of observa- tions for that size-class. In contrast, they mate fre- welcome the diverse views of my colleagues presented

here and remind both reader and commentator that I amquently during the stage just prior to full tumescence. This suggests that, although there is an important so- arguing not that bonobos and chimpanzees are behav-

iorally indistinguishable but only that reported differ-cial function to mating, females become choosier about mates when most likely to conceive. ences have been inflated in the scientific and public

imagination for a variety of both empirical and nonem-Despite clear continuities between the two chimpan- zees, there are also fundamental differences between pirical reasons.

It is important to note one very interesting and sig-them. Female P. troglodytes are less social, as evidenced by the small and independent core areas of the females. nificant pattern in the commentaries at the outset.

With one exception, all the commentators who haveThe distribution of females in these separate but over- lapping core areas provides a major incentive for male studied either bonobos or chimpanzees in the wild

agree strongly with my central assertion—that reportedsociality: a male can cooperate with others to cover the range of more females than he could do alone. In con- differences in social behavior between these two apes

are less striking than commonly reported. The twotrast, from the limited data we have available, female P. paniscus core areas appear to be as large as, if not commentators who disagree strongly have studied these

apes primarily in captivity. This partially reflects a dif-larger than, those of the males (White and Lanjouw 1992). These large core areas, which females usually ference in perspective that derives from the behaviors

one tends to see in conditions of enforced proximity andshare with their regular female associates, clearly re- move one of the main advantages of the cooperative observability versus the natural state, but it is also

a strong statement about research findings and theirmale group. Instead, a situation arises in which a single male can potentially monopolize the mating opportuni- ‘‘reality’’ that goes beyond the data and into issues of

research context. Every field researcher I know wouldties within a foraging party (White and Burgman 1990). P. troglodytes males are characterized as using power vehemently disagree with de Waal’s assertion that

‘‘only captive studies control for environmental condi-for sex, whereas female P. paniscus use sex for power. In wild, unprovisioned populations of both species tions and thereby provide conclusive data on interspe-

cific differences [emphasis mine]; field studies usuallymales are socially dominant to females, largely because of sexual dimorphism (Wood and White 1996, White concern different species under different ecological con-

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416 current anthropology Volume 39, Number 4, August–October 1998

ditions.’’ In fact, since evolutionary processes have literature on female bonobo sociosexual and dominance behavior, nearly all of which was also reviewed in mymolded the social behavior of chimpanzees and bonobos

in response to the ecologies of African forests, de Waal’s article. Unfortunately, all of the key points that she claims I have ignored are in fact discussed there, inassertion is wrong by definition. I therefore find it ironic

that the captive researchers (de Waal and Parish) are the some cases at length. She incorrectly states that I do not mention intercommunity mating by bonobos in my ar-two who are critical of my (apparently heretical) depar-

ture from a purely empirical analysis to ask whether ticle. In fact, I point out that ‘‘both hostile and peaceful intercommunity encounters are seen, and copulationthere are contextual biases that influence research in-

terpretations. The answer, drawn directly from the pat- between females and extracommunity males has been reported’’ (p. x, citing Kano 1992). I stick to my originaltern of the responses as well as from their content, ap-

pears to be yes. That contextual bias consists of (1) point about territoriality. The number of intercommun- ity territorial encounters that involve injury even ininfluences on social behavior itself created by the set-

ting in which the research is conducted (i.e., field or chimpanzee studies is quite low if one excepts the two ‘‘warfares’’ of the 1970s in Gombe and Mahale Nationalcaptivity) and (2) the intellectual biases and the sorts of

questions that the researcher brings to great ape re- Parks. The rate of intercommunity encounters in bo- nobo society that include aggressive chasing is 50%,search depending on where the study is to be conducted.

I firmly believe that these two contextual biases com- and we have spent only a tiny fraction of observation hours watching wild bonobos compared with chimpan-bine to produce some of the divergent views arising

from captive versus field research on chimpanzees and zees. Kano and White et al. both offer their own reviews ofbonobos.

The following are my responses to specific com- bonobo socioecology. Kano agrees with my cross-spe- cies comparison but points out two issues that I ne-ments, discussed in order of the vehemence of their dis-

agreement with me: glected to mention that differ between the two apes— infanticide and prolonged mother-son relationships—De Waal and Parish both cite data from captive stud-

ies of bonobos and chimpanzees showing that copula- and offers the same view as Parish and de Waal that bo- nobo intercommunity encounter behavior is in strikingtion rates are markedly higher for bonobos. De Waal

chastises me for failing to ask why, if bonobo hypersex- contrast to that of chimpanzees. I should have discussed infanticide in chimpanzees, but the explanations foruality is an artifact of confinement, it has not led to

oversexed chimpanzees as well. This point is well those episodes reported so far (mainly from Mahale) have been enigmatic in that in some cases males maytaken, but again it points out how futile it can be to

apply captive data to wild animals. Captivity affects dif- be killing their own offspring. Bonobos have not been reported to kill offspring. White et al. make the very im-ferent species in different ways. You will not see 20

orangutans living amicably in a mixed-sex group in an portant point that there is intraspecific variation among known bonobo populations that we must take into ac-Indonesian forest, nor will you find many zoos in which

the chimpanzee community includes a dozen or more count when comparing the two species of chimpanzee. White et al. point out that the data I present showingfully adult males. I acknowledge that chimpanzees and

bonobos differ in sexuality, in particular with respect to that nearly all parties at Wamba have at least one swol- len female do not agree with Lomako data. At Lomako,bonobo sociosexuality such as genital rubbing. The ob-

servation remains, however, that in their natural habi- smaller party sizes mean that the percentage of parties containing a swollen female is low (about 22%, verytats chimpanzee and bonobo copulation rates and sex-

ual swelling durations are extremely similar. similar to the Gombe data for chimpanzees). They sug- gest that this interpopulational variation may produceDe Waal’s other main criticism strikes me as setting

up a ‘‘straw ape.’’ He claims that both scientists and the differences in male-female behavior between the two best-known bonobo sites, and I fully agree.public have been slow to accept the true extent of bo-

nobo hypersexuality because of our squeamishness The other commentators—Fruth, Ingmanson, McGrew, Milton, and Moore—are in more or lessabout depictions of ape sex. This is presumably because

the photographs thereof are the nonhuman equivalent strong agreement with my main points. In fact, each strengthens my argument about chimpanzee-bonoboof pornography. He suggests that North Americans are

simply too puritanical to handle the notion of a sex- differences by adding evidence that I overlooked. McGrew feels that I have not gone far enough in my cri-crazed, sensuous ape. As I write this piece, Americans

are spending many of their waking hours discussing the tique, pointing out that Pan paniscus occurs not only in rain forest but in other habitats as well. This suggestsdetails of presidential sexual behavior in all its forms,

and when not doing so they are listening to the media that future research in other areas of Congo will yield a wider range of socioecology than has been observed(the same media that are reluctant to portray bonobo

sexuality?) describing it. I therefore do not accept the so far. He also points out that the interspecific data on swelling durations as percentages of the menstrual cy-notion that anyone is reluctant to listen to accounts of

bonobo sexual behavior, in either scientific or tabloid cle that I present in table 1 may be due only to sampling error based on small N’s—in other words, that bonoboforums.

Parish argues with my contentions by reviewing the swellings may not be extended at all compared with

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stanford Chimpanzees and Bonobos 417

those in chimpanzees, except in the raw number of days to ensure that they will have a future on Earth alongside their vastly more abundant human kin.that a female is partially tumescent.

Moore argues that currently accepted differences be- tween chimpanzees and bonobos based on field data could be due as much to methodological differences be- tween research teams as to actual differences in the ani- References Cited mals. If so, it would not be the first time that divergent data collection techniques produced divergent results in altmann, s. a ., and j. altmann. 1979. ‘‘Demographic the practice of equally sound science. One criticism by constraints on behavior and social organization,’’ in Primate

ecology and human origins. Edited by I. S. Bernstein and E. O.Moore—claiming that my statement that chimpanzees Smith, pp. 47–64. New York: Garland Press. [jm].offer meat to females and receive sex in exchange is un-

badrian, a., and n. badrian. 1984. ‘‘Social organizationsupported—is addressed by my work in press (Stanford of Pan paniscus in the Lomako Forest, Zaı̈re,’’ in The pygmy 1998) documenting cases at Gombe in which sex and chimpanzee: Evolutionary biology and behavior. Edited by

R. L. Susman, pp. 275–79. New York: Plenum Press.meat do indeed appear to be exchanged directly. boesch, c. 1991. The effects of leopard predation on groupingFruth points out that I missed published literature on

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