Stable and fluctuating social preferences and implications for cooperation among female bonobos at LuiKotale, Salonga National Park, DRC.

OBJECTIVES: Female bonobos (Pan paniscus) are characterized as highly affiliative and cooperative, but few studies have quantified the strength and stability of female intra-sexual relationships or explored how variation in social relationships influences cooperation. We measure female social preferences, identify causes of variation in preferences, and test whether variation in social preferences predicts food sharing or coalitionary support. METHODS: Data were collected over 3 years from females in the Bompusa community at LuiKotale, DRC. We measured genetic relatedness and constructed social preference indices for party association, proximity, grooming, GG-rubbing and aggression. We identified preferred social partners based on permutation tests and measured stability using Mantel tests. We used factor analysis to identify inter-relationships between preference indices and used LMMs to test whether variation in social preferences was explained by relatedness, rank differences, having dependent young or co-residency time. We used GLMMs to test whether variation in social preferences predicted food sharing or coalitionary support. RESULTS: All females had preferred non-kin partners for proximity, grooming or GG-rubbing, but only grooming preferences were stable across years. Association indices were higher among lactating females, and aggression was lower among females with longer co-residency times. The factor analysis identified one factor, representing proximity and GG-rubbing preferences, labeled behavioral coordination. Dyads with higher levels of behavioral coordination were more likely to share food. CONCLUSIONS: Female bonobos exhibit stable, differentiated grooming relationships outside of kinship and philopatry. Females also exhibit flexible proximity and GG-rubbing preferences that may facilitate cooperation with a wider range of social partners.

Mixed messages: wild female bonobos show high variability in the timing of ovulation in relation to sexual swelling patterns.

BACKGROUND: The evolution of primate sexual swellings and their influence on mating strategies have captivated the interest of biologists for over a century. Across the primate order, variability in the timing of ovulation with respect to females' sexual swelling patterns differs greatly. Since sexual swellings typically function as signals of female fecundity, the temporal relation between ovulation and sexual swellings can impact the ability of males to pinpoint ovulation and thereby affect male mating strategies. Here, we used endocrine parameters to detect ovulation and examined the temporal relation between the maximum swelling phase (MSP) and ovulation in wild female bonobos (Pan paniscus). Data were collected at the Luikotale field site, Democratic Republic of Congo, spanning 36 months. Observational data from 13 females were used to characterise female swelling cycles (N = 70). Furthermore, we measured urinary oestrone and pregnanediol using liquid chromatography-tandem mass spectrometry, and used pregnanediol to determine the timing of ovulation in 34 cycles (N = 9 females). RESULTS: We found that the duration of females' MSP was highly variable, ranging from 1 to 31 days. Timing of ovulation varied considerably in relation to the onset of the MSP, resulting in a very low day-specific probability of ovulation and fecundity across female cycles. Ovulation occurred during the MSP in only 52.9 % of the analysed swelling cycles, and females showed regular sexual swelling patterns in N = 8 swelling cycles where ovulation did not occur. These findings reveal that sexual swellings of bonobos are less reliable indicators of ovulation compared to other species of primates. CONCLUSIONS: Female bonobos show unusual variability in the duration of the MSP and in the timing of ovulation relative to the sexual swelling signal. These data are important for understanding the evolution of sexual signals, how they influence male and female mating strategies, and how decoupling visual signals of fecundity from the periovulatory period may affect intersexual conflict. By prolonging the period during which males would need to mate guard females to ascertain paternity, the temporal variability of this signal may constrain mate-guarding efforts by male bonobos.

The Steady State Great Ape? Long Term Isotopic Records Reveal the Effects of Season, Social Rank and Reproductive Status on Bonobo Feeding Behavior.

Dietary ecology of extant great apes is known to respond to environmental conditions such as climate and food availability, but also to vary depending on social status and life history characteristics. Bonobos (Pan paniscus) live under comparatively steady ecological conditions in the evergreen rainforests of the Congo Basin. Bonobos are an ideal species for investigating influences of sociodemographic and physiological factors, such as female reproductive status, on diet. We investigate the long term dietary pattern in wild but fully habituated bonobos by stable isotope analysis in hair and integrating a variety of long-term sociodemographic information obtained through observations. We analyzed carbon and nitrogen stable isotopes in 432 hair sections obtained from 101 non-invasively collected hair samples. These samples represented the dietary behavior of 23 adult bonobos from 2008 through 2010. By including isotope and crude protein data from plants we could establish an isotope baseline and interpret the results of several general linear mixed models using the predictors climate, sex, social rank, reproductive state of females, adult age and age of infants. We found that low canopy foliage is a useful isotopic tracer for tropical rainforest settings, and consumption of terrestrial herbs best explains the temporal isotope patterns we found in carbon isotope values of bonobo hair. Only the diet of male bonobos was affected by social rank, with lower nitrogen isotope values in low-ranking young males. Female isotope values mainly differed between different stages of reproduction (cycling, pregnancy, lactation). These isotopic differences appear to be related to changes in dietary preference during pregnancy (high protein diet) and lactation (high energy diet), which allow to compensate for different nutritional needs during maternal investment.

Pointing and pantomime in wild apes? Female bonobos use referential and iconic gestures to request genito-genital rubbing.

Referential and iconic gesturing provide a means to flexibly and intentionally share information about specific entities, locations, or goals. The extent to which nonhuman primates use such gestures is therefore of special interest for understanding the evolution of human language. Here, we describe novel observations of wild female bonobos (Pan paniscus) using referential and potentially iconic gestures to initiate genito-genital (GG) rubbing, which serves important functions in reducing social tension and facilitating cooperation. We collected data from a habituated community of bonobos at Luikotale, DRC, and analysed n = 138 independent gesture bouts made by n = 11 females. Gestures were coded in real time or from video. In addition to meeting the criteria for intentionality, in form and function these gestures resemble pointing and pantomime-two hallmarks of human communication-in the ways in which they indicated the relevant body part or action involved in the goal of GG rubbing. Moreover, the gestures led to GG rubbing in 83.3% of gesture bouts, which in turn increased tolerance in feeding contexts between the participants. We discuss how biologically relevant contexts in which individuals are motivated to cooperate may facilitate the emergence of language precursors to enhance communication in wild apes.

Female sociality during the daytime birth of a wild bonobo at Luikotale, Democratic Republic of the Congo.

Parturition is one of the most important yet least observed events in studies of primate life history and reproduction. Here, I report the first documented observation of a bonobo (Pan paniscus) birth event in the wild, at the Luikotale Bonobo Project field site, Democratic Republic of the Congo. The nulliparous mother's behaviour before, during and after parturition is described, along with reactions of other community members to the birth and the neonate. Data were collected through focal-animal observations, and the events postpartum were photo-documented. The behaviour and spatial distribution of party members were recorded using scan samples. Parturition occurred during the late morning in a social context, with parous females in close proximity to the parturient mother. Placentophagia occurred immediately after delivery, and the parturient shared the placenta with two of the attending females. I compare this observation with reports of parturition in captive bonobos, and highlight the observed female sociality and social support during the birth event. Plausible adaptive advantages of parturition occurring in a social context are discussed, and accrued observations of birth events in wild and free-ranging primates suggest that females may give birth within proximity of others more frequently than previously thought. This account contributes rare empirical data for examining the interface between female sociality and parturition, and the evolution of parturitional behaviours in primates.