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Latest news from the bonobos: Pan paniscus myths and realities1

Dernières nouvelles des bonobos: Les mythes et réalités de Pan paniscus
David Beaune

Résumés

Les bonobos sont nos plus proches parents vivants avec les chimpanzés. Ils attirent beaucoup d'attention de la part des anthropologues qui cherchent à comprendre nos origines simiesques. Plus récemment, ils attirent l'attention du grand public en raison de leur comportement remarquable et de leur système social matriarcal singulier. Les médias et certaines aspirations philosophiques ont rapidement érigé les bonobos comme nos plus proches parents, vivant en société pacifique de végétariens féministes, et gouvernée par le sexe. Mais la barrière entre l'homme et l'animal était sauve pour beaucoup tant que ce lubrique primate ne manifestait aucune capacité à exécuter ce qui fait le propre de l'homme. Or les nouvelles découvertes publiées ces dernières années nous permettent d'en savoir plus sur Pan paniscus. Cette revue décrit les résultats les plus récents : Selon les généticiens, bonobos, chimpanzés et humains appartiennent au même genre (Homo ou Pan) avec plus de 98% de gènes communs et un ancêtre partagé il y à 5 à 6 millions d'années. Il est récemment prouvé que les bonobos possèdent les capacités cognitives pour communiquer mais sans pharynx (langage des signes, lexigramme). Les bonobos peuvent résoudre des problèmes complexes et utiliser des outils. En captivité certains bonobos taillent des pierres, allument du feu avec un briquet ou utilisent une pelle pour creuser. Les femelles ont le statut social le plus élevé du groupe grâce à l'association et à la coalition entre femelles. La société n'est pas vraiment femelles-dominantes, mais plutôt co-dominante. La société n'est pas purement égalitaire, mais non violente et tolérante. Ni les agressions mortelles ni l'infanticide n'ont été observés à ce jour en milieu naturel ou en captivité. Le sexe a un rôle primordial dans cette société pacifique. Il n'y a pas de restriction sexuelle excepté l'inceste. Les bonobos sont une espèce clef dans leur écosystème, grâce au service écologique fournit de dispersion de graines. De plus en plus de découvertes fascinantes naissent au sujet de nos cousins qui sont en danger d'extinction et pourraient disparaître d'ici quelques décennies.

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Historique

Soumis 20 juillet 2012. Accepté 31 octobre 2012.

Texte intégral

1 Introduction

  • 1  I thank the Institut Congolais pour la Conservation de la Nature (ICCN) for granting permission to (...)

1Bonobos are one of the large mammal species most recently discovered by science. First informally described in 1929, they were named Pan paniscus in 1933 (Coolidge, 1933). Since Robert Yerkes in the thirties, bonobos were studied in captivity and more recently in the wild beginning in 1973 with Takayoshi Kano at Wamba field site, DR Congo (Kano, 1980). With Congolese wars and political instability, studies in the field were slowed down but research teams persevered and new exciting discoveries about this great ape allow us to better know our cousins' biology and also allow insights into our own origin. This paper reviews the latest news from the bonobos. Some old views of bonobos are obsolete; some previous questions have been answered while others remain unsolved. This review based on recent literature is also punctuated by my own observations with an habituated free-ranging bonobo community at the LuiKotale field site (Hohmann and Fruth, 2003c). My main research focused on the bonobo ecology. I recorded 1879 hours of behavioral data within this community of 25-35 identifiable bonobos, through 22 months of field work (2008-2011). Other discoveries, I hope, will astonish you with new insights about one of the planet's most fascinating animals and one of our closest living relatives.

2 Our closest living relative

2Within our own family of the Hominidae, great apes of the genus Pan, including bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), are our closest living relatives. Chimpanzees live in four major populations, including those located in western Africa (P. t. verus), equatorial Africa (P. t. troglodytes and P. t. schweinfurthii), and the Gulf of Guinea region (P. t. ellioti); with distinct and full species proposed and still debated today (Gonder et al., 2011). Described as pygmy chimpanzees in literature before the 1980s, bonobos have more gracile limbs than chimpanzees but are similar in many other morphological traits and in body size (Females = approx.33-36kg, Male = approx. 43-46kg; (Coolidge and Shea, 1982; Parish, 1996)) to the other Pan species. However, their frequently bipedal posture (D'Août et al., 2004), their morphology, and neotenic characteristics (Shea, 1983) which they share with us (Homo sapiens sapiens), caused many anthropologists to propose the bonobo as the best model for our closest living relative.

3However, contrary to popular belief, bonobos are not more closely related to us than are chimpanzees. We share a common ancestor with both Pan which dates to 5-6 million years ago, and approximately 98% of our DNA (Wildman et al., 2003; Patterson et al., 2006; Prufer et al., 2012) with both species. Bonobos and chimpanzees diverged from 0.93 (Won and Hey, 2005) to 2 million years ago (Raaum et al., 2005) and are separated by the Congo River, which acts as a biogeographic barrier by splitting the Congo basin. Therefore, both are genetically equidistant to us.

4Pan troglodytes and P. paniscus are so close to us that an increasing number of scientists propose a fusion of the genus of our cousins Pan, with our own genus Homo; with the proposed classification: Homo sapiens (humankind), Homo troglodytes (chimpanzee), and Homo paniscus (bonobo) (Wildman et al., 2003). This little taxonomic revolution could be difficult for the general public to accept, but an extraterrestrial taxonomist would not hesitate. One day we might accept ourselves as the third chimpanzee (Diamond, 1991). Another more philosophical rapprochement is the Great Ape Project (GAP) launched in the 1990s (Cavalieri and Singer, 1993). It is an appeal of 36 scientists from different disciplines aiming at the legal equalization of the non-human great apes with humans. The central point of the initiative is the "Declaration on Great Apes", claiming the inclusion of great apes in the "community of equals" and thus securing three basic rights for all great apes: 1. The Right to Life; 2. Protection of Individual Freedom; 3. The Prohibition of Torture. Furthermore, the project pleads for the idea of conferring the "moral status of person" on great apes. But beyond religion and ethics, rejection of this idea is mainly due to pressure for maintaining the use of living apes as "biological material" for experimentation in industry (Carlsson et al., 2004). We can note that the United States and Gabon are the only remaining countries allowing such research.

3 A tool maker

5Chimpanzees are well recognized as tool makers in the wild, with cultural variation in usage among populations across Africa (Whiten et al., 1999). For bonobos, tool-related behaviors are observed in wild populations but are rare and less sophisticated than those observed in chimpanzees (Kano, 1982; Ingmanson, 1996; Hohmann and Fruth, 2003a). This bonobo difference could be explained by the fact that they inhabit a less challenging environment than chimpanzees with no need for weapons, or may simply the general lack of studies of this species compared to chimpanzees. However, in captivity, tool making and usage by bonobos have both been well described (Jordan, 1982; Toth et al., 1993; Gold, 2002; Mulcahy and Call, 2006; Gruber et al., 2010). Kanzi and Pan-Banisha, a famous male and female who have gained widespread attention for their skills in language and have lived in the stimulating environment of the Great Ape Trust of Iowa since 2005 (Savage-Rumbaugh and Lewin, 1994). They can light a fire with a lighter, cook a meal, roast marshmallows and perform other impressive tasks. They have the basic stone-tool making skills required to produce usable flakes and fragments by hard-hammer percussion (Toth et al., 1993) and their techniques are improving (Schick et al., 1999). Their reported tool production and utilization for food retrieval (digging or breaking wooden logs) exhibits Homo-like technological competencies (Roffman et al., 2012).

6The most recent results appear to describe bonobos as having a similar repertoire in captivity, and equal tool-using capabilities equal as to those of chimpanzees (Herrmann et al., 2008; Gruber et al., 2010). Bonobos as chimpanzees use less dramatic tools for social purposes, games or comfort (cleaning with specific leaves, use of leaves as an umbrella against rain), while chimpanzees use also impressive reported tool techniques in the context of difficult food-acquisition tasks. Another remarkable point is that just like chimpanzees, female bonobos are more willing to use tools than males (Gruber et al., 2010). Because wild and captive bonobos share the same cognitive abilities required for tool use, such behavior is expected to occur in wild bonobos as well.

4 Communication

7Bonobos, like gorillas and chimpanzees, show a human-like asymmetry in language-related brain areas, which has been correlated with language dominance (Cantalupo and Hopkins, 2001). But articulation of speech is physically impossible and language is restricted to vocalizations and gestures (Pika et al., 2005; Pollick and de Waal, 2007). We share several communicative roots like the gestural NO by head shaking (Schneider et al., 2010) and almost all of these are understood by humans. Gestural communications include sexual invitation with body posture and hand raising, begging, embracing, mouth/tongue kissing, kicking, slapping, etc. with facial nuance and context dependence (Pika et al., 2005).

8Apes cannot 'speak'. They can however communicate a wide range of information and are even able to talk with us with the help of technology. Kanzi understands spoken English and communicates with a lexigram keyboard. He also modulates his vocalization with evident structural differences produced within a specific semantic context (Taglialatela et al., 2003). A similar structural difference was observed in other captive bonobos which use a specific acoustic structure in long and complex call sequences related to a precise type of food. This suggests that bonobo food-calling sequences convey meaningful information to other group members (Clay and Zuberbuhler, 2009).

9In the wild, bonobos exchange long distance calls (high hoot) between groups (Hohmann and Fruth, 1994). What kind of information do they exchange? The study of communication in wild bonobos is promising and may lead to fascinating discoveries.

5 A female dominant society

10Bonobos live in a male-philopatric structure. This means that males are born and die in the same group while females of 6-13 years emigrate to neighboring groups (Furuichi et al., 2012). Males will stay all their lives with their mothers. Females are accepted into new groups weaving future alliance bonds. Female chimpanzees do not have frequent social interactions with other females, whereas female bonobos maintain close social associations with one another (Furuichi, 2011).

11The result is a singular primate society: a matriarchal bonobo society in clear contrast with the patriarchal societies of chimpanzees, other primates and most human societies (Parish, 1996; Sommer et al., 2011). This unique trait attracted feminists, public attention and debate about male-female dominance. In early studies (mainly male) scientists described this behavior as "strategic male deference" or males being chivalrous to females as a strategy to obtain sex. This made it easier to admit female dominance in bonobo groups (Parish et al., 2000). Females most often initiate sexual interactions and ranging behavior (Furuichi, 2011), have priority of access to preferred food (Hohmann and Fruth, 1993; White and Wood, 2007) and will sometimes chase or be aggressive towards males (i.e. the definition of 'dominance'; NB: not within chimpanzees). Females are so influential in the groups that mothers improve the mating success of their sons when present (Surbeck et al., 2011). In male-male aggression, mothers and females can intervene and decide the outcome of the situation, and eventually influence their son's rank in the hierarchy (Furuichi, 2011). Despite modest physical dimorphism (female body size is 82.5% that of males) females gain power by cooperation and coalition formation (Parish, 1996; White and Wood, 2007). However, female dominance over males is not a rule. Males are consistently dominant in dyadic interactions (White and Wood, 2007). To conclude, it is clear that adult females occupy high dominance status in bonobo societies and that females are rather co-dominant to males (Surbeck et al., 2012). Differences in dominance among individuals are slight but measurable (see below) but we should keep in mind that bonobos show nothing that is comparable to the strong dominance with submission enforced by violence that is characteristic of chimpanzee societies. Are we close to an egalitarian society? Not really, but non-violence gives us this impression.

6 A peaceful vegetarian society

12Because they use sexual behavior in several contexts where other species use aggression, bonobos may be viewed as peaceful. However several injuries have been observed in captivity and in the wild, resulting from beatings, or biting on fingers, faces, or genitals (Parish et al., 2000, personal observation). Recently, the public was shocked by a case of cannibalism among wild bonobos where a baby was consumed by a group, including the mother (Fowler and Hohmann, 2010). We should note that the cause of death remains unknown and violence was not observed. Before the carcass was eaten (it was, after all, meat), the mother, with great affection, carried her offspring's body around with her for a whole day. Indeed, bonobos are not the pure vegetarians that we first thought them to be (Fig. 1). Bonobos kill and eat duikers, birds, rodents and monkeys (Hohmann and Fruth, 1993; 2008; Surbeck and Hohmann, 2008; Surbeck et al., 2009). However, although bonobos appreciate and are excited by meat, they are not organized hunters and carnivory thus remains opportunistic and accounts for only a marginal part of their diet (Oelze et al., 2011), i.e., 0.9% ± SE 0.2 of feeding sessions; N = 1879 hrs of observation (Beaune, 2012).

13Although linear dominance can be determined by agonistic interactions, bonobos are non-violent and mainly engage in chasing acts, submissive behaviours and deference (Hohmann and Fruth, 2003b; Surbeck et al., 2011). Bonobos are highly tolerant and cooperative (Hare et al., 2007). While most primate groups have territorial conflicts, bonobos behave peacefully with neighbouring community, with a large inter-group home range overlap (at Wamba 66% of the group's home range overlaps with those of neighbour groups (Kano and Mulavwa, 1984)). When two groups meet, they often engage in inter-group sexual relations (often female-female), grooming, feeding and foraging together, and sometimes sleeping at the same nesting place (Hohmann and Fruth, 2002; Furuichi, 2011). So far, infanticide and lethal aggression have never been observed in Pan paniscus. We can definitively say that the bonobo has a peaceful nature.

Figure 1

Figure 1

Female Olga and her daughter Opale eating a red colobus (Procolobus tholloni), opportunistically killed by the group, LuiKotale, DRC. David Beaune/MPI.
Femelle Olga et sa fille Opale mangeant un colobe rouge (Procolobus tholloni), tué de façon opportuniste par le groupe, LuiKotale, RDC. David Beaune/MPI.

7 The most lascivious hominid

14For the public, the bonobo is our lubricous cousin, performing Kama Sutra positions all day long (de Waal, 1997). Actually, the frequency with which bonobos engage in sex is less than an average of 0.3 copulation/hour (Furuichi and Hashimoto, 2002), with intercourse lasting less than a minute (usually a few seconds). Compared to us, bonobos' frequency of intercourse is definitely higher, with humans averaging 1 to 3 marital coitus per week, the freqeuncy declining with age (Kinsey Institute, 2012). The length of coitus for humans is generally longer than a minute with an average of 5 min for humans (Kinsey Institute, 2012). Bonobos do not have more sex than chimpanzees, nevertheless females of this species do have more sex and start earlier in life than male bonobos (Takahata et al., 1999; Hashimoto and Furuichi, 2006). Most importantly females have sex during non-fertile periods or in non-swelling episodes (Furuichi and Hashimoto, 2004). And when fully tumescent, sexual swelling signals occur even during non-conceptive periods. This is called "pseudo-estrus" (Furuichi, 2011). Thus females with true and confusing estrus signals are proportionally more numerous than females displaying no estrus signals so they are less monopolizable by an alpha male (preventing sexual harassment and infanticide) (Furuichi, 2011). See Fig. 2 for sexual swellings. Male bonobos do not sexually coerce females (Hohmann and Fruth, 2003b) and therefore, their sexual solicitation has to be accepted by the female for intercourse to occur. This strategy, contrasting with chimpanzees, is evolutionarily stable and quite similar to behaviour in most human societies (except that our species lost the receptive signals potentially as a result of similar selective pressures).

15Sex is routinely used for non-reproductive goals (tension-reduction, reconciliation, bartering for social favors, and sex for food exchanges). Behavioral observations support the hypothesis that sex reduces tension and is the basis of this largely peaceful society (Hohmann and Fruth, 2000; Palagi et al., 2004; Hare et al., 2007) and now scientists are trying to test this hypothesis through hormonal experimentation (Hohmann et al., 2009; Wobber et al., 2010).

Figure 2

Figure 2

Female bonobos' sexual swellings David Beaune/MPI.
Gonflements sexuels chez les femelles bonobos. David Beaune/MPI.

8 Sexual taboos? Homosexuality does not matter

16Bonobos practice public sex (Clay and Zuberbühler, 2012) rather than the more secretive sexuality of humans and chimpanzees. Bonobos are bisexual apes and homosexual encounters are common, especially among females (Fruth and Hohmann, 2006). Female bonobos engage in a unique sexual behavior also found in humans (tribadism) termed genito-genital (GG) rubbing in which they embrace ventro-ventrally and rub their genital swellings together with rapid sideways movements (Hohmann and Fruth, 2000) (Fig. 3). Sex seems to be the cement for social bonds. This is why females use it predominantly for their alliance. Sex with high-ranking females could be strategic for subordinates, who can call loudly an audience to acknowledge the scene (Clay and Zuberbühler, 2012). Bonobos can have oral, manual and foot sex. They perform multiple positions not found in other non-human primates (such as ventro-ventral or missionary position in humans). Males can be observed mounting other males without intromission, dorso-dorsally rubbing their scrota with sideways movements, or performing face to face ersatz fencing with erect penises. Juveniles can also be involved (de Waal, 1997; personal observation). Bonobos seem to have no limits to the choice of sexual partners with the exception of incest.

9 Gardener of the forest

17The ecological role of the bonobos has been recently studied at LuiKotale (Beaune et al., in press; Beaune, 2012). Bonobos are efficient seed dispersers; they spend approx. 3.5 hrs/day swallowing the seeds of trees, lianas and herbs of more than 91 species and disperse them at very long distances (0-4.5km). In its entire lifespan, a bonobo should disperse almost 12 million seeds (or 9 tons; excluding seeds <2 mm such as Ficus spp). The great majority of the seeds passed through the gut is viable (34/35 tested species). Compared with seeds not passed through the gut, bonobos' seeds germinate faster and at a higher rate. Furthermore, seeds disseminated by endozoochory with bonobos are better able to escape seed predators, thank to dung beetles attracted by bonobos' faeces (Beaune et al., 2012). For certain species such as the velvet tamarind, bonobos are germination activator (Beaune, 2012). In a Congo forest we estimate that 65% of the individual trees in the forest community are disseminated by bonobos. The great majority of the tree species does not recruit and self-replace without seed dispersal (18/19 plant species). Bonobos seem to be tree planters of the Congo forest.

Figure 3

Figure 3

Female-female genito-genital (GG) rubbing. David Beaune/MPI.
Frottements génito-génital (GG) entre femelles. David Beaune/MPI.

10 Threatened by extinction

18Bonobos are limited to areas south of the Congo River. Their survival depends on the conservation policies and decisions of the one country were they live: the Democratic Republic of Congo. The species' range covers 500,000 km² of the Cuvette Centrale (Thompson et al., 2003). Deforestation in DRC occurs at an average rate of311,000 ha/year (FAO, 2010) and in the past two decades, bonobos have suffered a 29% loss in their habitat (Junker et al., 2012). However, human hunting and bush meat trafficking is the main cause of bonobo extinction (Hart et al., 2008). Bonobo numbers are hard to estimate. They could number between 10,000 and 50,000 but it is also possible that there are fewer than 10,000 (Thompson et al., 2003). Bonobo populations are decreasing and the species is in danger of extinction (IUCN, 2012).

11 Conclusion. Myths... and realities

19- Bonobos are our closest living relatives...No more than chimpanzees.

20- Bonobos do not use tools...They do. Sophisticated tools (such as chimpanzees') were not observed in wild populations but bonobos do use and built tools.

21- Girls' power is within bonobos...Not really. Females' alliance in this matriarchal society allows dominance towards males. But bonobos are rather co-dominant.

22- Bonobos are peacefull...Yes. Lethal aggression was never reported, although aggressions exist.

23- Bonobos are the primate sex-champion....No. Bonobos use sex for social issues in various ways and without taboos but no more often than chimpanzees in frequency.

24- Homosexuality is common in bonobos...Yes. Especially female-female.

25- Bonobos can disappear...Yes.

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Notes

1  I thank the Institut Congolais pour la Conservation de la Nature (ICCN) for granting permission to conduct research at Salonga National Park, and Lompole villagers for granting permission to access the forest of their ancestors. The methods used to collect data in the field are in compliance with the requirements and guidelines of the ICCN, and adhere to the legal requirements of the host country, the Democratic Republic of Congo. The studied apes are free ranging bonobos observed without invasive method, constraint, contact and any interaction from the researchers. I aslo thank Drs. L. Bollache, F. Bretagnolle, B. Fruth and G. Hohmann for continuous support. Funding sources: the Max-Planck-Society (Germany), the SFDP and the Conseil Régional de Bourgogne (France). Thanks to Pr. D. McKey for the English improvement.

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Table des illustrations

Titre Figure 1
Légende Female Olga and her daughter Opale eating a red colobus (Procolobus tholloni), opportunistically killed by the group, LuiKotale, DRC. David Beaune/MPI.Femelle Olga et sa fille Opale mangeant un colobe rouge (Procolobus tholloni), tué de façon opportuniste par le groupe, LuiKotale, RDC. David Beaune/MPI.
URL http://journals.openedition.org/primatologie/docannexe/image/1090/img-1.jpg
Fichier image/jpeg, 76k
Titre Figure 2
Légende Female bonobos' sexual swellings David Beaune/MPI.Gonflements sexuels chez les femelles bonobos. David Beaune/MPI.
URL http://journals.openedition.org/primatologie/docannexe/image/1090/img-2.jpg
Fichier image/jpeg, 40k
Titre Figure 3
Légende Female-female genito-genital (GG) rubbing. David Beaune/MPI.Frottements génito-génital (GG) entre femelles. David Beaune/MPI.
URL http://journals.openedition.org/primatologie/docannexe/image/1090/img-3.jpg
Fichier image/jpeg, 73k
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Pour citer cet article

Référence électronique

David Beaune, « Latest news from the bonobos: Pan paniscus myths and realities », Revue de primatologie [En ligne], 4 | 2012, document 11, mis en ligne le 15 décembre 2012, consulté le 26 avril 2018. URL : http://journals.openedition.org/primatologie/1090 ; DOI : 10.4000/primatologie.1090

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Auteur

David Beaune

Max Planck Institute for Evolutionary Anthropology, Department of primatology, Deutscher Platz 6, Germany and Laboratoire Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 6 boulevard Gabriel, 21000 Dijon, France
Author for correspondence: david.beaune@gmail.com

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