Social Behavior of the Bonobo

 

Bonobo Taxonomy

The bonobo (Pan paniscus), or pygmy chimpanzee, is one of the three species of African apes.  Bonobos and chimpanzees (Pan troglodytes), for which they were initially mistaken, are the two living primate species most closely related to human beings.  The other African ape, the gorilla, and the orangutan of Borneo, are more distantly related to the Pan genus, and make up the remainder of the family Pongidae, or great apes.  Members of the superfamily Hominoidea (which includes the great apes, humans, and the gibbons) share several distinctive anatomical features, which set them apart from other primates. 

Bonobos were for a time thought merely to be a subspecies as chimpanzees, but later work has shown them to be distinct species in their own right.  There are significant differences between the Pan species, both in terms of anatomy and in terms of social behavior.  Based on studies of mandibular variation among the African apes, for instance, Andrea Taylor and Colin Groves note that “bonobos…remain clearly differentiated from common chimpanzees, and [are] more distinct than any of the chimpanzee subspecies from each other.” (Taylor p. 550)  Also, as is suggested by the term pygmy chimpanzee, bonobos can tend to be smaller on average than chimpanzees.  As an example of a possible behavioral difference, the bonobo is often presented as more commonly bipedal than the chimpanzee, though that claim is by no means free of controversy.[1]

Conservation

Bonobos live nearly exclusively within the Democratic Republic of the Congo, and though they are protected both by Congolese and international laws, the IUCN Red List includes the bonobo among its endangered species.  Living primarily in tropical and subtropical lowland forests, the biggest threats to bonobos in the wild come from habitat loss through agricultural clearing, commercial lumber extraction, and encroaching human settlements. (Red List)  Elsewhere, erosion of hunting taboos, economic crises, political instability, and deforestation are listed among the reasons for the rapid decline of the overall bonobo population.  A proposal to create a 3800 km2 reserve along the Lomako river was submitted to the Institut Congolais pour la Conservation de la Nature in 1990, but as of 1999 had not yet been approved. (Dupain)  Though Dupain and others note that the proposed reserve might theoretically contain about 8000 of the estimated 15,000 wild bonobos, their 1995 survey of the area suggests that the bonobo population in the area is no longer secure.  They found substantial evidence of human presence within the proposed area, though officially there are no permanent dwellings there.  If the reserve is to have any significant positive impact on the wild bonobo populations therein, it needs to be created as soon as possible.

However, creating the reserve alone would likely be insufficient to really protect bonobos.  Much of the increased hunting pressure in the area results from local human populations driven to move into forested areas and take up subsistence hunting because the deteriorating economy makes them less and less sure they will be able to sell the crops they used to farm.  These people will require some assurance that farming will once again become profitable if they are to return to that way of life.  Furthermore, one of the local groups of people, the Kitiwalists, is a religious sect that does not accept Congolese laws and declared the forest to be theirs. (Dupain)  If the DRC hopes to accomplish more than creating a nature reserve on paper, laws protecting the bonobos and other local species would have to be more fully enforced than they are now.

Feeding and Spacing

            Bonobos, like the other great apes, maintain a varied diet but feed primarily on fruits and leaves.  In addition, bonobos have also been observed to eat pith, invertebrates, and small mammals. (Badrian)  Though the bonobo diet is highly similar to that of the closely related chimpanzee, there has been a certain amount of controversy as to whether bonobos, like gorillas, show a greater preference for leaves and other herbaceous vegetation than the more frugivorous chimpanzees.  If it exists, a preference for this more abundant, nonseasonal food source might help explain the relaxed competition for food among bonobos as compared to chimpanzees. (Horiuchi)  Unsurprisingly, the amount of fruit consumed by bonobos at different times of the year varies somewhat according to the relative abundance of fruit in the environment, and when fruit is scarce, it predictably constitutes a smaller proportion of the total bonobo diet.

            One interesting behavioral aspect of feeding in bonobos has to do with the sharing of food.  While in chimpanzees food may be shared between mothers and infants, and meat is sometimes shared among males, bonobos “share food items other than meat…and [food sharing] occurs even when food is plentiful and when an individual already has some in his or her possession.” (Blount p. 706)  Furthermore, there is a strong association between the sharing of food and sexual activity.  When females share food with other females, it is most often in the context of soliciting genito-genital rubbing, and the most common co-occurrence of sexual activity and food sharing is when females seek to obtain food from dominant males, in which case they are more often successful if they copulate with the males first. (Blount)

            Bonobos have home ranges of 20-50 km2, and like chimpanzees live in fission-fusion societies, usually traveling in small, constantly changing subgroups instead of the larger, more stable community.  However, unlike many other primate species, interactions between larger bonobo communities are not typically marked by territorial threats or violence, though serious conflict has been witnessed in the field.  Instead, there are many reports of peaceful mingling, which is often marked by mutual sex and grooming among animals from apparently different communities. (de Waal 1995)  There are still a great many questions about why bonobos differ in this way from the very closely related chimpanzees.  One potential explanation relies on the previously mentioned abundance and nonseasonality of food sources bonobos use more frequently than chimpanzees.  While debate continues over whether this is actually true, Horiuchi’s mathematical model predicts that behavior patterns initially caused by the relative abundance or poverty of preferred food sources might remain robust even if members of a species moved into environments with significantly more or less relatively available food. (Horiuchi)

Mating System

            As is the case with chimpanzees, bonobos have a relatively promiscuous mating system, with males and females alike typically mating with multiple partners.  One possible explanation for this is that female promiscuity decreases the risk of infanticide by males.  Under this hypothesis, promiscuity confuses paternity enough so that males would potentially be killing their own offspring if they attacked the infant of a promiscuous female, and so they should thus be less likely to do so.[2]  Bonobos have not been observed committing infanticide, but if males in ancestral bonobo populations practiced infanticide more frequently, which seems fairly plausible, then those females that mated most promiscuously, and thus most confused the paternity of their subsequent offspring, would likely have been most successful in avoiding infanticide.  Bonobo females may be so much better than chimp females at preventing infanticide because, in addition to being promiscuous, they exhibit a sexual swelling throughout a much larger portion of their estrus cycles than chimpanzees do. (de Wall 1995, p. 86)

            The large number of sexually receptive females in a group, together with the fact that bonobo males never know when a female is ovulating (since sexual swelling is prominent nearly two-thirds of the time), mean males have a hard time figuring out when it would be worthwhile to compete with each other for access to particular mate. (Streier pp. 241 and 245)  Bonobos mate “during all phases of a female’s sexual cycle, and about a third of copulations occur during periods when fertilization is unlikely or impossible.” (Bagemihl p. 274)  Furthermore, nearly half of bonobo sexual activity occurs between members of the same sex, with 65-75% of this activity being between females. (Id. p. 273)  A full explanation of their promiscuous mating system might therefore be connected to the nearly two-thirds of bonobo sexual activity that has no potential for producing offspring.  The likeliest account for this seems to be that, in bonobos, sexuality plays a significant role in building social bonds.  For instance, the previously discussed relationship sexual activity and food sharing, which occurs even when both individuals already possess food, suggests that both behaviors might sometimes be closer to socialization rituals than to purely functional behaviors.  Female homosexual behavior in particular seems to serve largely as a sort of social tool, in that it marks the successful immigration of a new female into a group and also takes place “whenever tensions arise over access to food, and as a form of reconciliation after a rare aggressive interaction.” (Streier pp. 224-5)

Grouping Patterns and Kinship

Bonobos live in large groups with multiple males and multiple females, but do most of their daily traveling and foraging in smaller, constantly changing parties.  Due to the relative abundance of food resources, the travel costs and those incurred by within-group food competition among bonobos are far less than they would be in species with more patchily distributed food.  As is the case with many other primates, one significant advantage of group living for bonobos is protection from predation, and increased availability of mates may be another. 

There are several areas in which the behavior of bonobos seems to correlate with kinship relations.  Hohmann, Gerloff, Tautz, and Fruth, for instance, found that close kin (defined as parent-offspring, sibling, or half-sibling relationships) engage in grooming more frequently than unrelated individuals. (Hohmann 1999)  Furthermore, many of “the strong social bonds [observed] between mature males and females were partly related to kinship.” (Id. p. 1231)  In the group they observed, the longest close associations were between two mother-son pairs.  This is consistent with the fact that “maternal assistance appears to be a decisive factor affecting male rank and mating success in…bonobos.” (Streier p. 240)  Unlike the closely related chimpanzee, in which male-male conflicts are often fatal, clashes between bonobo males tend to involve agonistic displays without any severe physical aggression.  This being the case, the alliance of an adult female can be every bit as beneficial to a male as the alliance of an adult male, despite the sexual dimorphism favoring males with typically greater size and strength.  Since there is a positive correlation between rank and mating success in male bonobos, it is also to a mother’s advantage to help her adult son attain high rank, as her own genes thereby have an improved chance of being passed onto grandchildren.

Dispersal Patterns and Non-Kin Social Relationships.

Bonobo dispersal patterns are characterized by female exogamy and male philopatry.  As such, bonobo communities tend to include unrelated females and closely related males.  If the theory of inclusive fitness were sufficient for explaining bonobo social behavior, then, we should expect a higher degree of cooperation among males than is found among females, which is the case for female-dispersing chimpanzees.  However, bonobos have been observed to form close, long-term associations with unrelated individuals, both among males, among females, and between males and females.  In a group studied by Hohmann, et al, the majority (more than two-thirds in each of four field seasons) of close associations occurred between unrelated individuals.  There were eight close associations lasting at least two field seasons, and among these were two mother-son pairs, one pair of brothers, and five associations between unrelated individuals.  One of these five was male-male, one was female-female, and the other three were between males and females that were not believed to produce any offspring together. (Hohmann 1999 pp. 1225 and 1227)

The sociality of female bonobos might suggest that female migration to other groups is not as common as previously believed.  Indeed, the high food availability for bonobos corresponds to reduced intragroup feeding competition and thus may reduce the pressure on females to leave their natal groups.  Whether a particular female emigrates may depend on her or her mother’s social status or the number of potential competitors within her natal group. (Hohmann 1999 p. 1221)  Alternatively, there may be other explanations, apart from or in addition to inclusive fitness theory, for why female bonobos associate with each other to such a high degree.  Consistent with the hypothesis that female bonobos disperse, genetic studies of the Eyengo bonobo community in the Lomako forest have found that most adult and subadult males have a resident mother, whereas most females appear to have come from a different natal group. (Hohmann 1999 and Gerloff)  Though this is just one group of bonobos, and though better-studied chimpanzees have been known to show great variance in dispersal rates between groups, it does appear that the high degree of female association and cooperation among bonobos is not explained by inclusive fitness, but is more likely the result of mutualism and reciprocity. (Gerloff p. 1194) 

Two of the behaviors among female bonobos that most clearly involve reciprocity are food sharing and sexual activity, which often occur together.  Food is shared more frequently between females than it is between males, and female-female sharing occurs “most often in the context of one female approaching another to beg for food and soliciting genito-genital contact and rubbing.” (Blount p. 706)  On the other hand, a fair degree of female-female aggression among bonobos has also been observed, particularly in the context of sexual competition.  Hohmann and Fruth note that “in all cases when aggression was associated with mating [that is, when it was directed against a female who was soliciting mating or actually engaged in a copulation] the pair split up because the female or her male mating partner (or both) fled.” (Hohmann 2003 p. 1401)  The fact that “females had significantly higher mating rates when they were aggressors than when they were targets” suggests that this behavior is reproductively advantageous to aggressive females. (Id. p. 1402)

Female Dominance

            Unique among ape species, in bonobos females tend to be socially dominant to males.  In a Belgian animal park, bonobo females have been observed chasing and harassing unrelated males who have food until that food is dropped. (Van Elsacker p. 34).  At Stuttgart Zoo, a wild-born male had his penis bitten off by a female (though it was successfully sewn back on and he went on to breed successfully), and one male at a zoo in Frankfurt “has had eight fingers and toes bitten off by high-ranking females; his testicles are also badly scarred where they have been bitten many times,” (Jahme p. 299).  While these incidents took place in captivity, wild females have been observed to threaten and chase males in the same way, but a wild male can usually run away and “remain on the periphery of the group until he feels safe enough to come back” (Id. p. 300), whereas in the confines of a zoo enclosure, escape is not an option, and the male must remain to face the aggression of one or more angry females.  In one study of the Eyengo bonobo community in the Lomako forest, female-male aggression was the second most often observed type, after male-male aggression, and occurred more than twice as often as male-female aggression (during the study period in question, female-male aggression occurred 105 times, while male-female aggression occurred only 45 times). (Hohmann 2003 p. 1399).

            In species such as chimpanzees, where similar behaviors are observed with the sexes reversed, the social system is almost invariably described as “male dominant”.  Yet for bonobos,

Females are variously described as “co-dominant”, “almost co-dominant”, “about the same rank” as males, or having “close to” male status, and “appropriate[ly] respect[ful]” of males.  More than a few researchers conclude that dominance relationships are “not clear and invariable” in this species or that a “narrowing status gap” exists.  Apparent female dominance is explained away as “female feeding priority coupled with male social dominance” and females are described pejoratively as “irritable”, “troublesome” or “daring.”  Males, in contrast are “tolerant” of females, “allow” females to have the upper hand, or are “henpecked.” Because males remain in control and defer by choice, their puzzling behavior (rather than their plight) can be comfortably explained as “strategic male deference” or even “chivalry.” (Parish p. 99)

 

Yet the fact that female behavior suggesting dominance has been seen in contexts outside of feeding indicates that the situation is not simply “female feeding priority coupled with male social dominance”.  The fact that males are chased and injured by females strongly suggests that they are not merely “deferring” to females, but actually being dominated by them, at least occasionally.

            In prosimians, where female social dominance is much more common, it correlates with such things as small, monomorphic body size, short breeding season, large infant size, and fast infant growth.  But when compared to the decidedly more male dominant chimpanzees, bonobos are nearly as large, spend more time sexually receptive, and have infants of roughly the same size that grow at about the same rate.  Consequently, the cost-of-reproduction hypothesis that might explain female dominance in prosimians cannot fully account for it in bonobos.  This is especially true given that bonobo food sources tend to be more abundant and readily available than those of chimps, so bonobos need only spend 75% as much time foraging per day as chimps. (Jahme p. 282)  If female dominance is not a result of female energy needs, how else might we be able to explain why female bonobos, who are not typically related to others in their group, are able to dominate males?

            One possible hypothesis is that female solidarity and the strong tendency for bonobo females to cooperate with each other leads to female dominance.  The fact that chimpanzee females are both subordinate to males and cooperate with each other far more rarely than do bonobo females gives some support to this hypothesis.  There have observations that a female bonobo’s ability to dominate a male increases with her age.  (Vervaecke p. 438)  This is likely due, at least in part, to the greater strength of intrasexual bonds among older females compared to those among adolescents who have only recently joined the group.  In addition, “aggressive coalitions of female bonobos have been observed to gang up and attack lone males”, whereas males do not gang up to attack females and competitive skirmishes between members of the same sex “are usually worked out between the two individuals”, (Jahme p. 299).  This suggests that female-female bonds play an important role in the exertion of female bonobo dominance over males.  Female bonding in most other primate species where it is observed tends to depend significantly on kinship relations, which are absent among the females in most bonobo groups.  “Female bonobos have evolved a cultural solution to help them through their isolation from their kin,” (Jahme p. 200), so the question is why they have done so.  That is, why do female bonobos form such strong bonds with each other when other female-dispersing apes, such as chimpanzees, do not?

            The chimpanzee food patch is generally thought to be small and seasonal, which means intragroup competition for food resources prohibits females from associating with each other. The bonobo food patch, on the other hand, is generally thought to be large and not seasonal, and so females can always associate with one another. (Horiuchi p. 65)  Horiuchi argues that certain social behaviors (namely modes of competition within groups and between groups), which evolved in the more clearly distinct food availability conditions of ancestral chimpanzee and bonobo populations, are evolutionarily stable and thus resistant to change.  If this is true, then it is to be expected that the two species would continue competing in the same ways as their ancestors, despite the fact that some chimpanzees currently live in areas where food is more abundant than it is in some bonobo habitats.  So perhaps there is a natural inclination for unrelated females in fission-fusion societies to bond with each other (maybe to help them cope with kin isolation, as Jahme suggests), and it is simply the case that in chimpanzees, higher levels of food competition, or the behaviors evolved to deal with more competition, prevent them from doing so.

            But Charlotte Hemelrijk states that “female coalitions against males also occur among common chimpanzees, and a statistical difference in coalition behavior has so far not been shown to exist,” (Hemelrijk p. 91).  This claim may seem odd given the number of accounts of female bonding in bonobos and its absence in chimps, but even if the statement itself is false, it is worth noting that Hemelrijk has developed a computer model that suggests how female dominance might occur independent of any pre-existing tendency for female bonding.  Bonobo groups are significantly more cohesive overall than those of chimpanzees, she argues, and this alone can lead to female dominance over males without increasing the tendency for females to ally against males.  This cohesiveness among both sexes may still be the result of differences in food distribution, since “chimpanzees, for instance, group more cohesively in less seasonally varying areas.” (Id. p. 94)  In any case, members of a highly cohesive group will interact with each other more frequently than in a less cohesive group, and closer physical proximity means more of these interactions will be between individuals with significantly different social rank positions.  Because of this, dominance ranks for all individuals change more over time in highly cohesive groups than in less cohesive groups.  “This automatically increases the probability that some females become dominant over males as a consequence,” (Id. p. 93) even when females start out with collectively lower rank than males.

            As it has so far only been tested in a computer model, the hypothesis that female dominance can arise purely as a consequence of group cohesion (and that female coalition formation may then be an effect of female dominance, rather than a cause) clearly cannot be accepted without a great deal more data collection.  But because the hypothesis exists and has some initial evidence in its favor in the form of a simple computer model, it shouldn’t be too difficult to find relevant data.  One question that could be asked is whether females in more cohesive chimpanzee groups are dominant over more males, on average, than females in less cohesive groups.  If this is the case, and those females are also found to be no more likely to form close bonds with other females in their groups, then we should reject the female solidarity hypothesis in favor of the group cohesion hypothesis.  If female chimpanzees are instead found to remain largely subordinate to the majority of males, regardless of group cohesiveness, then we should reject the group cohesion hypothesis.  Finally, if females in more cohesive chimp groups are found to be more dominant and to be more likely to form close bonds with other females in their groups, then perhaps some combination of the two hypotheses is actually the best explanation for female dominance in bonobos.

 

 

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[1] See, for instance, Videan, Elaine N. and McGrew, W.C. “Are bonobos (Pan paniscus) really more bipedal than chimpanzees (Pan troglodytes)?” American Journal of Primatology. 54(4). July 2001. pp. 233-239.

[2] See, for instance, Matt Ridley’s The Red Queen: Sex and the Evolution of Human Nature. January 1994.  Macmillan Publishing. pp. 205-207.