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The Structure of Bonobo Copulation Calls During Reproductive and Non-Reproductive Sex Zanna Clay* & Klaus Zuberbu¨ Hler*

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The Structure of Bonobo Copulation Calls During Reproductive and Non-Reproductive Sex Zanna Clay* & Klaus Zuberbu¨ Hler* Ethology The Structure of Bonobo Copulation Calls During Reproductive and Non-Reproductive Sex Zanna Clay* & Klaus Zuberbu¨ hler* * School of Psychology, University of St Andrews, St Andrews, UK Living Links, Yerkes Primate Research Center, Emory University, Atlanta, GA, USA Correspondence Abstract Zanna Clay, Living Links, Yerkes Primate Research Center, Emory University, Atlanta, Copulation calls in primates are usually identified as sexually selected GA 30322, USA. signals that promote the reproductive success of the caller. In this study, E-mail: [email protected] we investigated the acoustic structure of copulation calls in bonobos (Pan paniscus), a great ape known for its heightened socio-sexuality. Received: June 10, 2011 Throughout their cycles, females engage in sexual relations with both Initial acceptance: August 25, 2011 males and other females and produce copulation calls with both part- Final acceptance: September 15, 2011 (K. Reinhold) ners. We found that calls produced during sexual interactions with male and female partners could not be reliably distinguished in terms of their doi: 10.1111/j.1439-0310.2011.01975.x acoustic structure, despite major differences in mating behaviour and social context. Call structure was equally unaffected by the size of a female’s sexual swelling and by the rank of her mating partner. Rank of the partner did affect call delivery although only with male, but not female partners. The only strong effect on call structure was because of caller identity, suggesting that these signals primarily function to broad- cast individual identity during sexual interactions. This primarily social use of an evolved reproductive signal is consistent with a broader trend seen in this species, namely a transition of sexual behaviour to social functions. forward (Pradhan et al. 2006). Essentially, all con- Introduction verge on the theme that copulation calls are sexually During mating events, numerous mammals and birds selected signals that promote the caller’s reproductive produce loud and acoustically distinct vocalisations, success (e.g. Maestripieri & Roney 2005). For exam- usually referred to as ‘copulation calls’. In some spe- ple, copulation calls may advertise sexual receptivity cies, males are the main producers (e.g. little brown (e.g. Semple 1998, 2001), allowing a female to accrue bats, Myotis lucifugus, Barclay & Thomas 1979), but mate choice benefits by inciting male–male com- generally they are given by females, sometimes petition, either directly (Cox & Le Boeuf 1977) or accompanied by their male partner (e.g. elephant indirectly via sperm competition (O’Connell & Cowli- seals, Mirounga angustirostris, Cox & Le Boeuf 1977; shaw 1994). Copulation calls may also reduce threats African elephants, Loxodonta africana, Poole et al. of infanticide (Pradhan et al. 2006) by promoting 1988). Copulation calls are widespread among pri- paternity uncertainty or enhancing mate guarding mates, particularly in multi-male multi-female Old (O’Connell & Cowlishaw 1994). In chimpanzees (Pan World species, in which females mate promiscuously troglodytes), females are vulnerable to infanticide by and advertise their receptivity with pronounced sex- both males (e.g. Muller et al. 2007) and other ual swellings (Dixson 1998). females (Townsend et al. 2007). In a recent study, it The prevalence and conspicuous nature of female was found that chimpanzee females called most copulation calls has evoked considerable interest and when mating with high-ranked males, possibly as a a broad array of adaptive hypotheses has been put means to confuse paternity and enlist their future 1158 Ethology 117 (2011) 1158–1169 ª 2011 Blackwell Verlag GmbH Z. Clay & K. Zuberbu¨ hler Structure of Bonobo Copulation Calls support (Townsend et al. 2008). At the same time, tension, facilitating reconciliation, enabling affiliation calling was inhibited in the presence of high-ranked and expressing social status (Thompson-Handler females, who also are the most likely perpetrators of et al. 1984; de Waal 1987; Hohmann & Fruth 2000). female-led infanticides (e.g. Pusey et al. 2008). Over- Sex appears to have particular relevance for newly all, this suggests that copulation calls in primates can arriving immigrant females, who use sexual interac- be part of a strategy used by females to maximise tions to facilitate their integration into a new com- reproductive success while minimising social compe- munity and to allow subsequent peaceful coexistence tition. and affiliation with non-related group members (e.g. Examining the acoustic structure of copulation Furuichi 1989; Idani 1991). The performance of calls can provide information relating to their adap- homosexual socio-sexual behaviours is thought to tive significance and communicative potential. In assist in facilitating affiliations between unrelated yellow baboons (Papio cynocephalus), female copula- females (e.g. Fruth & Hohmann 2006). tion calls convey a range of information, including Sexual interactions between females are known as caller identity, partner rank and swelling size (Sem- ‘genital contacts’, whereby two females embrace ple 2001; Semple et al. 2002). In chimpanzees, copu- ventro-ventrally, swinging their hips laterally while lation call structure is a reliable indicator of female keeping their vulvae in contact (Hohmann & Fruth identity (Townsend et al. 2011). In Barbary maca- 2000). Intriguingly, during genital contacts, females ques (Macaca sylvanus), copulation calls co-varied sometimes give calls that sound identical to the ones acoustically with the occurrence of ejaculation (Pfef- they produce when copulating with males (Thomp- ferle et al. 2008a), and this variation was perceived son-Handler et al. 1984; Kano 1992), something that by listeners (Pfefferle et al. 2008b). Providing infor- is not explained by current functional hypotheses mation about identity, receptivity and ejaculations (e.g. Pradhan et al. 2006). Owing to this acoustic may enable females to influence the behavioural similarity and to remain consistent with the estab- decisions of potential mating partners in ways that lished terminology, we term these vocalisations ‘cop- are beneficial to them (Semple & McComb 2000; ulation calls’. Pfefferle et al. 2008b). In a previous study on call use, we found that call Bonobo females (Pan paniscus) also produce copu- production was less common during homo- than lation calls during mating events (Thompson-Handler heterosexual interactions. In particular, when mat- et al. 1984; Kano 1992). This is consistent with Dix- ing with a male partner the average likelihood of a son’s (1998) predictions that emphasise multi-male, female giving copulation calls was about twice as multi-female social structure, fission–fusion dynam- high as when mating with a female partner (32.9% ics and the presence of promiscuous females, who vs. 16.4%; Clay et al. 2011). Despite this difference, exhibit pronounced sexual swellings (Furuichi 1989; the general patterns of call production were very Kano 1992). For a number of reasons, bonobos rep- similar, regardless of the partner’s sex, which sug- resent an intriguing species to study copulation calls. gested that these calls have a broader social function Females are the sex more likely to emigrate (e.g. (Clay et al. 2011). In particular, the average call Kano 1992) but, despite a relatively low degree of production was highly dependent on partner rank genetic relatedness among them (e.g. Gerloff et al. with females most likely to call during sexual inter- 1999), they form strong intra-sexual affiliations and actions with high-ranked partners, regardless of their are highly gregarious (e.g. Furuichi 1989; Kano sex (high-ranked male partners = 59.9%, high- 1992; Hohmann et al. 1999). By developing endur- ranked female partners = 28.2%; low-ranked male ing intra-sexual affiliations and coalitions, bonobo partners = 9.2%, low-ranked female partners = 3.0%; females can exert considerable social power by domi- Clay et al. 2011). These results thus suggest that, nating males, defending resources and avoiding although this signal may have originally evolved infanticide (e.g. Furuichi 1989; Parish 1994; White & within the reproductive context, it has become ritua- Wood 2007). lised to function as a more general social signal, with In bonobos, sex is incorporated into daily life, with the potential of being used in flexible and strategic individuals engaging in sexual interactions in all age ways. and sex combinations, across their sexual cycles, and The aim of the current study was to conduct an in a multitude of positions (e.g. Thompson-Handler acoustic analysis of female bonobo copulation calls et al. 1984; de Waal 1987; Paoli et al. 2006). Partly to investigate the kinds of information conveyed by divorced from reproduction, sex is thought to have these signals. If sexual behaviour in bonobos has a numerous social functions, such as reducing social social function, as suggested by previous research, Ethology 117 (2011) 1158–1169 ª 2011 Blackwell Verlag GmbH 1159 Structure of Bonobo Copulation Calls Z. Clay & K. Zuberbu¨ hler then call morphology should be less affected by part- Table S1). To maximise sample size, we pooled data ner’s sex and more affected by the partner’s social sets from across the three groups and combined data status, a factor that has been shown to influence call for dyads that met each other again in the second rates (Clay et al. 2011). We investigated whether year (n = 9 female–female dyads and n = 19 male– information
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