Bonobo

Primatologist Frans de Waal states bonobos are capable of altruism, compassion, empathy, kindness, patience, and sensitivity,[41] and described "bonobo society" as a "gynecocracy".[42][lower-alpha 1] Primatologists who have studied bonobos in the wild have documented a wide range of behaviors, including aggressive behavior and more cyclic sexual behavior similar to chimpanzees, even though bonobos show more sexual behavior in a greater variety of relationships. An analysis of female bonding among wild bonobos by Takeshi Furuichi stresses female sexuality and shows how female bonobos spend much more time in estrus than female chimpanzees.[43]

Some primatologists have argued that de Waal's data reflect only the behavior of captive bonobos, suggesting that wild bonobos show levels of aggression closer to what is found among chimpanzees. De Waal has responded that the contrast in temperament between bonobos and chimpanzees observed in captivity is meaningful, because it controls for the influence of environment. The two species behave quite differently even if kept under identical conditions.[44] A 2014 study also found bonobos to be less aggressive than chimpanzees, particularly eastern chimpanzees. The authors argued that the relative peacefulness of western chimpanzees and bonobos was primarily due to ecological factors.[45] Bonobos warn each other of danger less efficiently than chimpanzees in the same situation.[46]

Bonobos are very social.

Bonobo searching for termites

Bonobos are unusual among apes for their matriarchal social structure (extensive overlap between the male and female hierarchies leads some to refer to them as gender-balanced in their power structure). Bonobos do not have a defined territory and communities will travel over a wide range. Due to the nomadic nature of the females and evenly distributed food in their environment, males do not gain any obvious advantages by forming alliances with other males, or by defending a home range, as chimpanzees do. Female bonobos possess sharper canines than female chimpanzees, further fueling their status in the group.[47] Although a male bonobo is dominant to a female in a dyadic interaction,[48] depending on the community, socially-bonded females may be co-dominant with males[49] or dominant over them, even to the extent that females can coerce reluctant males into mating with them.[50][51]

At the top of the hierarchy is a coalition of high-ranking females and males typically headed by an old, experienced matriarch[52] who acts as the decision-maker and leader of the group. Female bonobos typically earn their rank through experience, age, and ability to forge alliances with other females in their group, rather than physical intimidation, and top-ranking females will protect immigrant females from male harassment.[53] While bonobos are often called matriarchal, and while every community is dominated by a female, some males will still obtain a high rank and act as coalitionary partners to the alpha female,[54] often taking initiative in coordinating the groups movements. These males may outrank not only the other males in the group, but also many females.[55] Certain males alert the group to any possible threats, protecting the group from predators such as pythons and leopards.[56][57]

Aggressive encounters between males and females are rare, and males are tolerant of infants and juveniles. A male derives his status from the status of his mother.[58] The mother–son bond often stays strong and continues throughout life. While social hierarchies do exist, and although the son of a high ranking female may outrank a lower female, rank plays a less prominent role than in other primate societies.[59] Relationships between different communities are often positive and affiliative, and bonobos are not a territorial species.[60] Bonobos will also share food with others, even unrelated strangers.[61] Bonobos exhibit paedomorphism (retaining infantile physical characteristics and behaviours),[62] which greatly inhibits aggression and enables unfamiliar bonobos to freely mingle and cooperate with each other.[63]

Males engage in lengthy friendships with females and, in turn, female bonobos prefer to associate with and mate with males who are respectful and easygoing around them. Because female bonobos can use alliances to rebuff coercive and domineering males and select males at their own leisure, they show preference for males who are not aggressive towards them.[64]

Aging bonobos lose their playful streak and become noticeably more irritable in old age. Both sexes have a similar level of aggressiveness.[65]

Bonobos live in a male philopatric society where the females immigrate to new communities while males remain in their natal troop. However, it is not entirely unheard of for males to occasionally transfer into new groups.[66] Additionally, females with powerful mothers may remain in their natal clan.[67]

Alliances between males are poorly developed in most bonobo communities, while females will form alliances with each other and alliances between males and females occur, including multisex hunting parties.[68] There is a confirmed case of a grown male bonobo adopting his orphaned infant brother.[69]

A mother bonobo will also support her grown son in conflicts with other males and help him secure better ties with other females, enhancing her chance of gaining grandchildren from him.[70] She will even take measures such as physical intervention to prevent other males from breeding with certain females she wants her son to mate with.[71] Although mothers play a role in aiding their sons, and the hierarchy among males is largely reflected by their mother's social status, some motherless males will still successfully dominate some males who do have mothers.[72]

Female bonobos have also been observed fostering infants from outside their established community.[73][74]

Bonobos are not known to kill each other, and are generally less violent than chimpanzees, yet aggression still manifests itself in this species. Although female bonobos dominate males and selectively mate with males who do not exhibit aggression toward them, competition between the males themselves is intense and high-ranking males secure more matings than low-ranking ones.[75] Indeed, the size difference between male and female bonobos is in fact more pronounced in bonobos than it is in chimpanzees, as male bonobos do not form alliances and therefore have little incentive to hold back when fighting for access to females.[76] Male bonobos are known to attack each other and inflict serious injuries such as missing digits, damaged eyes and torn ears. Some of these injuries may also occur when a male threatens the high ranking females and is injured by them, as the larger male is swarmed and outnumbered by these female mobs.[77]

Due to the promiscuous mating behavior of female bonobos, a male cannot be sure which offspring are his. As a result, the entirety of parental care in bonobos is assumed by the mothers.[78] However, bonobos are not as promiscuous as chimpanzees and slightly polygamous tendencies occur, with high-ranking males enjoying greater reproductive success than low-ranking males. Unlike chimpanzees, where any male can coerce a female into mating with him, female bonobos enjoy greater sexual preferences and can rebuff undesirable males, an advantage of female-female bonding, and actively seek out higher-ranking males.[79]

Bonobo party size tends to vary because the groups exhibit a fission–fusion pattern. A community of approximately 100 will split into small groups during the day while looking for food, and then will come back together to sleep. They sleep in nests that they construct in trees.

Female bonobos more often than not secure feeding privileges and feed before males do, although they are rarely successful in one-on-one confrontations with males, a female bonobo with several allies supporting her has extremely high success in monopolizing food sources.[80] Different communities favour different prey. In some communities females exclusively hunt and have a preference for rodents, in others both sexes hunt, and will target monkeys.[81]

In captive settings, females exhibit extreme food-based aggression towards males, and forge coalitions against them to monopolize specific food items, often going as far as to mutilate any males who fail to heed their warning.[82]

In wild settings, however, female bonobos will quietly ask males for food if they had gotten it first, instead of forcibly confiscating it, suggesting sex-based hierarchy roles are less rigid than in captive colonies.[83]

Female bonobos are known to lead hunts on duikers and successfully defend their bounty from marauding males in the wild. They are more tolerant of younger males pestering them yet exhibit heightened aggression towards older males.[84]

Bonobos mating, Jacksonville Zoo and Gardens.

Sexual activity generally plays a major role in bonobo society, being used as what some scientists perceive as a greeting, a means of forming social bonds, a means of conflict resolution, and postconflict reconciliation.[85][4] Bonobos are the only non-human animal to have been observed engaging in tongue kissing.[86] Bonobos and humans are the only primates to typically engage in face-to-face genital sex, although a pair of western gorillas has also been photographed in this position.[87]

Bonobos do not form permanent monogamous sexual relationships with individual partners. They also do not seem to discriminate in their sexual behavior by sex or age, with the possible exception of abstaining from sexual activity between mothers and their adult sons. When bonobos come upon a new food source or feeding ground, the increased excitement will usually lead to communal sexual activity, presumably decreasing tension and encouraging peaceful feeding.[88]

More often than the males, female bonobos engage in mutual genital-rubbing behavior, possibly to bond socially with each other, thus forming a female nucleus of bonobo society. The bonding among females enables them to dominate most of the males.[88] Adolescent females often leave their native community to join another community. This migration mixes the bonobo gene pools, providing genetic diversity. Sexual bonding with other females establishes these new females as members of the group.

Bonobo clitorises are larger and more externalized than in most mammals;[89] while the weight of a young adolescent female bonobo "is maybe half" that of a human teenager, she has a clitoris that is "three times bigger than the human equivalent, and visible enough to waggle unmistakably as she walks".[90] In scientific literature, the female–female behavior of bonobos pressing genitals together is often referred to as genito-genital (GG) rubbing.[88][91] This sexual activity happens within the immediate female bonobo community and sometimes outside of it. Ethologist Jonathan Balcombe stated that female bonobos rub their clitorises together rapidly for ten to twenty seconds, and this behavior, "which may be repeated in rapid succession, is usually accompanied by grinding, shrieking, and clitoral engorgement"; he added that it is estimated that they engage in this practice "about once every two hours" on average.[89] As bonobos occasionally copulate face-to-face, "evolutionary biologist Marlene Zuk has suggested that the position of the clitoris in bonobos and some other primates has evolved to maximize stimulation during sexual intercourse".[89] The position of the clitoris may alternatively permit GG-rubbings, which has been hypothesized to function as a means for female bonobos to evaluate their intrasocial relationships.[92]

Group of bonobos

Bonobo males engage in various forms of male–male genital behavior.[88][93] The most common form of male–male mounting is similar to that of a heterosexual mounting: one of the males sits "passively on his back [with] the other male thrusting on him", with the penises rubbing together due to both males' erections.[41] In another, rarer form of genital rubbing, two bonobo males hang from a tree limb face-to-face while penis fencing.[88][94] This also may occur when two males rub their penises together while in face-to-face position. Another form of genital interaction (rump rubbing) often occurs to express reconciliation between two males after a conflict, when they stand back-to-back and rub their scrotal sacs together, but such behavior also occurs outside agonistic contexts: Kitamura (1989) observed rump–rump contacts between adult males following sexual solicitation behaviors similar to those between female bonobos prior to GG-rubbing.[95] Takayoshi Kano observed similar practices among bonobos in the natural habitat. Tongue kissing, oral sex, and genital massaging have also been recorded among male bonobos.[96][41]

Wild females give birth for the first time at 13 or 14 years of age.[97] Bonobo reproductive rates are no higher than those of the common chimpanzee.[88] However, female bonobo oestrus periods are longer.[98] During oestrus, females undergo a swelling of the perineal tissue lasting 10 to 20 days. The gestation period is on average 240 days. Postpartum amenorrhea (absence of menstruation) lasts less than one year and a female may resume external signs of oestrus within a year of giving birth, though the female is probably not fertile at this point. Female bonobos carry and nurse their young for four years and give birth on average every 4.6 years.[99] Compared to common chimpanzees, bonobo females resume the genital swelling cycle much sooner after giving birth, enabling them to rejoin the sexual activities of their society. Also, bonobo females which are sterile or too young to reproduce still engage in sexual activity. Mothers will help their sons get more matings from females in oestrus.[59]

Adult male bonobos have sex with infants,[100] although without penetration.[101] Adult females also have sex with infants, but less frequently. Infants are not passive participants. They quite often initiate contacts with both adult males and females, as well as with peers.[100] They have also been shown to be sexually active even in the absence of any stimulation or learning from adults.[102]

Infanticide, while well documented in chimpanzees, is apparently absent in bonobo society.[103] Although infanticide has not been directly observed, there have been documented cases of both female[104] and male[105] bonobos kidnapping infants, sometimes resulting in infants dying from dehydration. Although male bonobos have not yet been seen to practice infanticide, there is a documented incident in captivity involving a dominant female abducting an infant from a lower-ranking female, treating the infant roughly and denying it the chance to suckle. During the kidnapping, the infant's mother was clearly distressed and tried to retrieve her infant. Had the zookeepers not intervened, the infant almost certainly would have died from dehydration. This suggests female bonobos can have hostile rivalries with each other and a propensity to carry out infanticide.[106] The highly sexual nature of bonobo society and the fact that there is little competition over mates means that many males and females are mating with each other, in contrast to the one dominant male chimpanzee that fathers most of the offspring in a group.[107] The strategy of bonobo females mating with many males may be a counterstrategy to infanticide because it confuses paternity. If male bonobos cannot distinguish their own offspring from others, the incentive for infanticide essentially disappears.[103] This is a reproductive strategy that seems specific to bonobos; infanticide is observed in all other great apes except orangutans.[108]

It is unknown how the bonobo avoids simian immunodeficiency virus (SIV) and its effects.[109]

Bonobo (Pan paniscus) mother and infant at Lola ya Bonobo

Observations in the wild indicate that the males among the related common chimpanzee communities are hostile to males from outside the community. Parties of males 'patrol' for the neighboring males that might be traveling alone, and attack those single males, often killing them.[110] This does not appear to be the behavior of bonobo males or females, which seem to prefer sexual contact over violent confrontation with outsiders.[4]

While bonobos are more peaceful than chimpanzees, it is not true that they are unaggressive.[111] In the wild, among males, bonobos are half as aggressive as chimpanzees, while female bonobos are more aggressive than female chimpanzees.[111] Both bonobos and chimpanzees exhibit physical aggression more than 100 times as often as humans do.[111]

Grooming: reinforcement of social links

Although referred to as peaceful, bonobo aggression is not restricted to each other, and humans have also been attacked by bonobos, and suffered serious, albeit non-fatal, injuries.[105]

Bonobos are far less violent than chimpanzees, though, as lethal aggression is essentially nonexistent among bonobos while being not infrequent among chimpanzees.[45] It has been hypothesized that bonobos are able to live a more peaceful lifestyle in part because of an abundance of nutritious vegetation in their natural habitat, allowing them to travel and forage in large parties.[112]

Recent studies show that there are significant brain differences between bonobos and chimpanzees. Bonobos have more grey matter volume in the right anterior insula, right dorsal amygdala, hypothalamus, and right dorsomedial prefrontal cortex, all of which are regions assumed to be vital for feeling empathy, sensing distress in others and feeling anxiety.[113] They also have a thick connection between the amygdala, an important area that can spark aggression, and the ventral anterior cingulate cortex, which has been shown to help control impulses in humans.[114][115] This thicker connection may make them better at regulating their emotional impulses and behavior.[116]

Bonobo society is dominated by females, and severing the lifelong alliance between mothers and their male offspring may make them vulnerable to female aggression.[4] De Waal has warned of the danger of romanticizing bonobos: "All animals are competitive by nature and cooperative only under specific circumstances" and that "when first writing about their behaviour, I spoke of 'sex for peace' precisely because bonobos had plenty of conflicts. There would obviously be no need for peacemaking if they lived in perfect harmony."[117]

Surbeck and Hohmann showed in 2008 that bonobos sometimes do hunt monkey species. Five incidents were observed in a group of bonobos in Salonga National Park, which seemed to reflect deliberate cooperative hunting. On three occasions, the hunt was successful, and infant monkeys were captured and eaten.[118]

There is one inferred killing in the wild,[119] and a confirmed lethal attack in captivity.[120] In both cases, the attackers were female and the victims were male.

Folivory: bonobos use certain species for self-medication

The bonobo is an omnivorous frugivore; 57% of its diet is fruit, but this is supplemented with leaves, honey, eggs,[121] meat from small vertebrates such as anomalures, flying squirrels and duikers,[122] and invertebrates.[123] The truffle species Hysterangium bonobo is eaten by bonobos.[124] In some instances, bonobos have been shown to consume lower-order primates.[118] Some claim bonobos have also been known to practise cannibalism in captivity, a claim disputed by others.[125][126] However, at least one confirmed report of cannibalism in the wild of a dead infant was described in 2008.[127][128] A 2016 paper reported two more instances of infant cannibalism, although it was not confirmed if infanticide was involved.[129]

Chimpanzee and bonobo males

A comparison of chimpanzees' and bonobos' performance on various cognitive tests[130]

In 2020 the first whole-genome comparison between chimpanzees and bonobos was published and showed genomic aspects that may underlie or have resulted from their divergence and behavioral differences, including selection for genes related to diet and hormones.[131] A 2010 study found that "female bonobos displayed a larger range of tool use behaviours than males, a pattern previously described for chimpanzees but not for other great apes".[132] This finding was affirmed by the results of another 2010 study which also found that "bonobos were more skilled at solving tasks related to theory of mind or an understanding of social causality, while chimpanzees were more skilled at tasks requiring the use of tools and an understanding of physical causality".[130] Bonobos have been found to be more risk-averse compared to chimpanzees, preferring immediate rather than delayed rewards when it comes to foraging. Bonobos also have a weaker spatial memory compared to chimpanzees, with adult bonobos performing comparably to juvenile chimpanzees.[133]

Bonobos are capable of passing the mirror-recognition test for self-awareness, as are all great apes.[134][135] They communicate primarily through vocal means, although the meanings of their vocalizations are not currently known. However, most humans do understand their facial expressions[136] and some of their natural hand gestures, such as their invitation to play. The communication system of wild bonobos includes a characteristic that was earlier only known in humans: bonobos use the same call to mean different things in different situations, and the other bonobos have to take the context into account when determining the meaning.[137]

Two bonobos at the Great Ape Trust, Kanzi and Panbanisha, have been taught how to communicate using a keyboard labeled with lexigrams (geometric symbols) and they can respond to spoken sentences. Kanzi's vocabulary consists of more than 500 English words,[138] and he has comprehension of around 3,000 spoken English words.[139]

Kanzi is also known for learning by observing people trying to teach his mother; Kanzi started doing the tasks that his mother was taught just by watching, some of which his mother had failed to learn. Some, such as philosopher and bioethicist Peter Singer, argue that these results qualify them for "rights to survival and life"—rights which humans theoretically accord to all persons (See great ape personhood).

In the 1990s, Kanzi was taught to make and use simple stone tools. This resulted from a study undertaken by researchers Kathy Schick and Nicholas Toth, and later Gary Garufi. The researchers wanted to know if Kanzi possessed the cognitive and biomechanical abilities required to make and use stone tools. Though Kanzi was able to form flakes, he did not create them in the same way as humans, who hold the core in one hand and knap it with the other, Kanzi threw the cobble against a hard surface or against another cobble. This allowed him to produce a larger force to initiate a fracture as opposed to knapping it in his hands.[140]

As in other great apes and humans, third party affiliation toward the victim—the affinitive contact made toward the recipient of an aggression by a group member other than the aggressor—is present in bonobos.[141] A 2013 study[142] found that both the affiliation spontaneously offered by a bystander to the victim and the affiliation requested by the victim (solicited affiliation) can reduce the probability of further aggression by group members on the victim (this fact supporting the Victim-Protection Hypothesis). Yet, only spontaneous affiliation reduced victim anxiety—measured via self-scratching rates—thus suggesting not only that non-solicited affiliation has a consolatory function but also that the spontaneous gesture—more than the protection itself—works in calming the distressed subject. The authors hypothesize that the victim may perceive the motivational autonomy of the bystander, who does not require an invitation to provide post-conflict affinitive contact. Moreover, spontaneous—but not solicited—third party affiliation was affected by the bond between consoler and victim (this supporting the Consolation Hypothesis). Importantly, spontaneous affiliation followed the empathic gradient described for humans, being mostly offered to kin, then friends, then acquaintances (these categories having been determined using affiliation rates between individuals). Hence, consolation in the bonobo may be an empathy-based phenomenon.

Instances in which bonobos have expressed joy have been reported. One study analyzed and recorded sounds made by human infants and bonobos when they were tickled.[143] Although the bonobos' laugh was at a higher frequency, the laugh was found to follow a spectrographic pattern similar to that of human babies.[143]

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