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In mammals, the costs of reproduction are biased towards females. Lactation is particularly energetically expensive, and behavioral and physiological data indicate that maternal effort during lactation induces energetic stress. Another source of stress in females is male aggression directed towards them when they are cycling. Evaluating the costs of reproduction in wild and mobile animals can be a challenging task, and requires detailed information on state-dependent parameters such as hormone levels. Glucocorticoid (GC) levels are indicative of nutritional and social stress, and are widely used to assess the costs of reproduction. We investigated variation in urinary levels of cortisol, the main GC in female bonobos (Pan paniscus), between and within reproductive stages. Female chimpanzees (Pan troglodytes), the closest living relative of the bonobos, are often exposed to intense aggression from males, which causes a significant rise in their cortisol levels during the phase of their maximum fecundity. In bonobos, males compete for access to fertile females, but aggressive male mating strategies are absent in this species. Therefore, we expected that GC levels of cycling female bonobos would be lower than those of lactating females. Due to the long period of offspring care in bonobos, we expected that GC levels would remain elevated into the late stage of lactation, when immatures gain body weight but may still be nursed and carried by their mothers. We found elevated urinary GC levels only during the early stage of lactation. The GC levels of cycling females did not differ from those in the mid or late lactation stage. Behavioral strategies of female bonobos may allow them to compensate for the elevated energetic demands of lactation and prolonged maternal care.

Feces are a treasure trove in the study of animal behavior and ecology. Stable carbon and nitrogen isotope analysis allows to assess the dietary niches of elusive primate species and primate breastfeeding behavior. However, some fecal isotope data may unwillingly be biased toward the isotope ratios of undigested plant matter, requiring more consistent sample preparation protocols. We assess the impact of this potential data skew in 114 fecal samples of wild bonobos (Pan paniscus) by measuring the isotope differences (Δ

Fission–fusion dynamics have evolved in a broad range of animal taxa and are thought to allow individuals to mitigate feeding competition. While this is the principal benefit of fission–fusion, few studies have evaluated its costs. We compared gregariousness, foraging budgets, and social budgets between lactating bonobos and chimpanzees from wild populations to evaluate potential costs. Both species exhibit fission–fusion dynamics, but chimpanzees, particularly in East African populations, appear to experience higher feeding competition than bonobos. We expected lactating chimpanzees to be less gregarious than lactating bonobos; reduced gregariousness should allow lactating chimpanzees to mitigate the costs of higher feeding competition without requiring more foraging effort. However, we expected the reduced gregariousness of lactating chimpanzees to limit their time available for affiliative interactions. Using long-term data from LuiKotale bonobos and Gombe chimpanzees, we found that lactating chimpanzees were indeed less gregarious than lactating bonobos, while feeding and travel time did not differ between species. Contrary to our predictions, lactating females did not differ in social interaction time, and lactating chimpanzees spent proportionately more time interacting with individuals other than their immature offspring. Our results indicate that lactating chimpanzees can maintain social budgets comparable to lactating bonobos despite reduced gregariousness and without incurring additional foraging costs. We discuss potential explanations for why lactating bonobos are more gregarious.

In mammals, allogrooming is prominent in forming and maintaining social and cooperative relationships. Yet an animal's social time is constrained, which may limit its access to a large number of partners. Dunbar (1993, Behavioral and Brain Sciences, 16 (4), 681–694) proposed that human polyadic conversations, which allow access to several social partners simultaneously, evolved as a form of social grooming to circumvent this time constraint. In nonhuman primates, polyadic grooming (PG), in contrast to dyadic grooming, may similarly be a time-efficient way to maintain weak social relationships with many partners which can be important for group level cooperation. It remains unknown whether PG is used to fulfil specific cooperative needs by accessing numerous weakly bonded partners and increasing the number of partners accessed per unit of time. We compared the use and effect of PG between chimpanzees, Pan troglodytes, which are highly territorial and collaborative (especially males), and bonobos, Pan paniscus, which are less territorial and collaborative and in which females are the main co-operators. We carried out focal grooming observations in one bonobo and two chimpanzee communities in the wild. As predicted, chimpanzees engaged in more PG than bonobos. Surprisingly, males engaged in PG more than females in both species. While chimpanzees accessed more partners per minute of grooming than bonobos via dyadic grooming, PG increased the number of partners accessed per minute only in bonobos. Finally, chimpanzees primarily used PG with individuals who were close in rank and frequent grooming partners, whereas bonobos used PG with individuals who were distant in rank, close party associates and frequent grooming partners. We suggest that bonobo males use PG to enhance conspecific social tolerance and mate choice. The overall higher rate of PG in chimpanzees suggests that between-group competition may promote polyadic affiliation, which possibly reinforces group cohesion and coordination. © 2020 The Authors

As an integral part of the immune response, testosterone secretion is inhibited when an individual is confronted with an immune challenge. Testosterone-mediated physiological, morphological, and behavioral traits are compromised at times of impaired health. Nevertheless, males of some species seem to maintain high levels of testosterone when confronted with an immune challenge, upholding competitive strength but compromising their immune response. It has been argued that this phenomenon will occur only in species living in social systems with high degrees of male-male competition over mating opportunities. Male chimpanzees contest over access to fertile females and dominants sire the majority of offspring. This male mating pattern makes chimpanzees a candidate species where we could expect males to maintain high testosterone levels, compromising their immune response, to ensure immediate reproductive success. We measured blood testosterone levels in male and female chimpanzees, who expressed clinical symptoms (symptomatic) or showed no evidence of clinical disease on assessment (asymptomatic). For females, we expected to find lower testosterone levels in symptomatic individuals than in asymptomatic subjects. In males, we would predict lower testosterone levels in symptomatic individuals than in asymptomatic males, if the immune response leads to a decrease in testosterone secretion. Alternatively, males could have equal levels of testosterone when symptomatic and asymptomatic, upholding competitive strength. Our results show that male chimpanzees exhibit lower levels of testosterone when confronted with an immune challenge than when being asymptomatic. This suggests that male testosterone secretion is suppressed as part of the immune response, which potentially increases survival and lifetime reproductive success. It will, however, negatively impact momentary competitive ability. Also, males may employ different mating strategies, some of which are less testosterone-driven (e.g., affiliative strategies). Consequently, in some individuals, the costs of maintaining high testosterone levels may not outweigh the potential gain in reproductive success.

Quantifying physiological challenges has gained increasing importance in evolutionary biology, behavioral physiology, and conservation. One matrix that is particularly useful for obtaining long-term records of physiological changes in mammals is hair. Potential markers are components of the endocannabinoid (EC) system, which regulates homeostasis of the brain as well as the endocrine and immune systems. Here, we present results from the first study to measure ECs (anandamide [AEA], 2-archidonyl glycerol [2-AG]) and EC-like compounds (N-palmitoylethanolamine [PEA], N-oleoylethanolamine [OEA], N-stearoylethanolamine [SEA]) in the hair of a nonhuman primate. We found that AEA, SEA, PEA, and OEA can be reliably measured in hair samples. When comparing the measurements of hair from different body parts, we found that variations of some analytes suggest that hair location is likely to affect results. For changes in health status, measurements of ECs and EC-like compounds reflected differences at both intra- and interindividual levels. We concluded that the EC system potentially provides novel tools to assess well-being, health status, and metabolic stress-not only in the hair of humans but also in that of domestic and wild animals. Measuring changes in ECs and EC-like compounds may improve the long-term monitoring of health status in captive and wild primates and may serve as a useful measure in animal welfare programs.

Predation is a major cause of mortality in non-human primates, and considered a selective force in the evolution of primate societies. Although larger body size is considered as protection against predation, evidence for predation on great apes by carnivores comes from chimpanzees (Pan troglodytes), gorillas (Gorilla gorilla), and orangutans (Pongospp.). Here, we describe the first encounter between wild bonobos (Pan paniscus) and a leopard (Panthera pardus). A single leopard was confronted by a group of habituated bonobos for three hours. Two adult males and one adolescent female bonobo actively harassed the leopard, which remained still for most of the encounter and reacted only to close approaches by bonobos. While no predation was observed, their behaviours confirm that bonobos perceive leopards as potential predators. Our report adds novel information to descriptions from other African ape species, and sheds light on the behavioural repertoire of bonobos’ anti-predation strategies. For future investigations, we suggest tagging leopards to remotely monitor their movements and allow assessment of encounter rates as one of several factors influencing predation pressure.

The concept of social dominance has been used in a plethora of studies to assess animal behaviour and relationships between individuals for nearly a century. Nevertheless, a standard approach does not yet exist to assess dominance in species that have a nonlinear or weakly linear hierarchical structure. We amassed 316 published data sets and show that 73.7% of the data sets and 90.3% of 103 species that we reviewed do not have a strongly linear structure. Herein, we present a novel method, ADAGIO, for assessing the structure of dominance networks. ADAGIO computes dominance hierarchies, in the form of directed acyclic graphs, to represent the dominance relations of a given group of animals. Thus far, most methods for computing dominance ranks assume implicitly that the dominance relation is a total order of the individuals in a group. ADAGIO does not assume or require this to be always true, and is hence more appropriate for analysing dominance hierarchies that are not strongly linear. We evaluated our approach against other frequently used methods, I&SI, David's score and Elo-rating, on 12 000 simulated data sets and on 279 interaction matrices from published, empirical data. The results from the simulated data show that ADAGIO achieves a significantly smaller error, and hence performs better when assigning ranks than other methods. Additionally, ADAGIO generated accurate dominance hierarchies for empirical data sets with a high index of linearity. Hence, our findings suggest that ADAGIO is currently the most reliable method to assess social dominance in gregarious animals living in groups of any size. Furthermore, since ADAGIO was designed to be generic, its applicability has the potential to extend beyond dominance data. The source code of our algorithm and all simulations used for this paper are publicly available at http://ngonga.github.io/adagio/ .

The vocal repertoire of nonhuman primates is largely fixed. Individuals produce their species-specific vocalizations from a young age, and do not acquire new call types over their lifetime. Despite these limitations, however, monkeys and apes are able to increase their vocal flexibility in several ways, including subtle acoustic modification, call combinations, turn-taking and call persistence. Although primates have been observed to utilize these communicative features, the extent to which they integrate these abilities is not known. Here we show that certain long-distance calls produced by wild bonobos, Pan paniscus, assimilate several aspects of vocal flexibility in ways not previously documented in nonhuman primates. Communication between foraging parties exhibits context-specific call combinations relating to the movement of caller, call modifications that potentially target particular individuals, call-and-answer exchanges in which the initial caller's behaviour depends on the listener's reply, and possible persistence in call production. The selective pressure exerted by bonobos' fission–fusion social structure has likely favoured the integration of these communicative capabilities.

Background: Throughout life, physiological homeostasis is challenged and the capacity to cope with such challenges declines with increasing age. In many species, sex differences exist in life expectancy. Sex-specific differences have been related to extrinsic factors like mate competition and/or intrinsic proximate mechanisms such as hormonal changes. In humans, an intrinsic factor related to aging is soluble alpha klotho (alpha-Kl). Both sexes show an age-related decline in alpha-Kl, but throughout life women have higher levels than men of the same age. Sex differences in alpha-Kl have been linked to a shorter lifespan, as well as to specific morbidity factors such as atherosclerosis and arteries calcifications. In non-human animals, information on alpha-Kl levels is rare and restricted to experimental work. Our cross-sectional study is the first on alpha-Kl levels in two long-lived species: bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). As in most mammals, female bonobos and chimpanzees have longer life expectancy than males. Methods: We measured serum alpha-Kl levels of 140 subjects from 16 zoos with an ELISA to examine if alpha-Kl levels reflect this difference in life expectancy. Results: In both species and in both sexes, alpha-Kl levels declined with age suggesting that this marker has potential for aging studies beyond humans. We also found species-specific differences. Adult female bonobos had higher alpha-Kl levels than males, a difference that corresponds to the pattern found in humans. In chimpanzees, we found the opposite: males had higher alpha-Kl levels than females. Conclusion: We suggest that contrasting sex differences in adult alpha-Kl levels mirror the dominance relations between females and males of the two Pan species; and that this might be related to corresponding sex differences in their exposure to stress. In humans, higher cortisol levels were found to be related to lower alpha-Kl levels. We conclude that there is great potential for studying aging processes in hominoids, and perhaps also in other non-human primates, by measuring alpha-Kl levels. To better understand the causes for sex differences in this aging marker, consideration of behavioural parameters such as competition and stress exposure will be required as well as other physiological markers.

Humans share an extraordinary degree of sociality with other primates, calling for comparative work into the evolutionary drivers of the variation in social engagement observed between species. Of particular interest is the contrast between the chimpanzee (Pan troglodytes) and bonobo (Pan paniscus), the latter exhibiting increased female gregariousness, more tolerant relationships, and elaborate behavioral adaptations for conflict resolution. Here, we test predictions from 3 socioecological hypotheses regarding the evolution of these traits using data on wild bonobos at LuiKotale, Democratic Republic of Congo. Focusing on the behavior of co-feeding females and controlling for variation in characteristics of the feeding patch, food intake rate moderately increased while feeding effort decreased with female dominance rank, indicating that females engaged in competitive exclusion from high-quality food resources. However, these rank effects did not translate into variation in energy balance, as measured from urinary C-peptide levels. Instead, energy balance varied independent of female rank with the proportion of fruit in the diet. Together with the observation that females join forces in conflicts with males, our results support the hypothesis that predicts that females trade off feeding opportunities for safety against male aggression. The key to a full understanding of variation in social structure may be an integrated view of cooperation and competition over access to the key resources food and mates, both within and between the sexes.

7 pages; International audience; This report describes bonobo (Pan paniscus, Hominidae) behavioral flexibility and inter-community differences with high tannin level fruit processing. In fruiting plants, tannin should discourage certain seed dispersers (direct deterrence hypothesis) such as primates. Based on data deriving from five study sites; LuiKotale, Lomako, Wamba, Malebo and Manzano, we compare consumption and dispersal of fruit species rich in tannins: Parinari and Musanga pulp was chewed across all communities probably for saliva tannin neutralisation. However, consumption of the fruits of Canarium schweinfurthii was observed in few communities only with differences in the food process: While bonobos of Wamba, Lomako and Manzano crunched and swallowed the pulp, bonobos of LuiKotale ingested entire fruits, extracted intact fruits from feces, and re-ingested their pulp, spitting the seed after a retention time of 24h in the digestive tract (i.e. endozoochory). We discuss potential functions of this peculiar feeding technique, likely to be a cultural behavior.

Monitoring metabolic activity in wild living animals has become of particular interest in the field of ecological research. Methods for the repeated non-invasive sampling of individuals are needed. Thyroid hormones (TH) are involved in the regulation of metabolic activity, and their measurement can be used as a proxy to monitor metabolic changes. During periods of low energy intake, serum TH levels are reduced, leading to a decrease in metabolic activity. Using urine samples collected during a food restriction experiment in captive bonobos we validated a total triiodthyronin (TT3) enzyme immunoassay (EIA) for the monitoring of metabolic changes. We found that the majority of immune reactivity of the assay in the urine samples could be explained through immunoreactivity to T3. Furthermore, urinary T3 was stable through repeated freeze-thaw cycles but prolonged exposure to room temperature lead to degradation. Most importantly, we found that for all animals urinary total T3 levels were higher when more digestible energy was consumed. We concluded that urinary total T3 measurements are a suitable method for monitoring metabolic changes in bonobos and potentially in a wide range of animal species.

A positive interaction is any interaction between individuals of the same or different species (mutualism) that provides a benefit to both partners such as increased fitness. Here we focus on seed dispersal mutualism between an animal (bonobo, Pan paniscus) and a plant (velvet tamarind trees, Dialium spp.). In the LuiKotale rainforest southwest of Salonga National Park, Democratic Republic of Congo, seven species of the genus Dialium account for 29.3% of all trees. Dialium is thus the dominant genus in this forest. Dialium fruits make up a large proportion of the diet of a habituated bonobo community in this forest. During the 6 months of the fruiting season, more than half of the bonobos' feeding time is devoted to Dialium fruits. Furthermore, Dialium fruits contribute a considerable proportion of sugar and protein to bonobos' dietary intake, being among the richest fruits for these nutrients. Bonobos in turn ingest fruits with seeds that are disseminated in their feces (endozoochory) at considerable distances (average: 1.25 km after 24 hr of average transit time). Endozoochory through the gut causes loss of the cuticle protection and tegumentary dormancy, as well as an increase in size by water uptake. Thus, after gut passage, seeds are better able to germinate. We consider other primate species as a potential seed disperser and conclude that Dialium germination is dependent on passage through bonobo guts. This plantanimal interaction highlights positive effects between two major organisms of the Congo basin rainforest, and establishes the role of the bonobo as an efficient disperser of Dialium seeds. Am. J. Primatol. 75:394-403, 2013. (c) 2013 Wiley Periodicals, Inc.

Dominance relationships between females and males are characteristic traits of species and are usually associated with sexual dimorphism. Exploring the social and contextual circumstances in which females win conflicts against males allows one to study the conditions triggering shifting power asymmetries between the sexes. This study investigates dominance relationships in bonobos (Pan paniscus) a species in which females are thought to display social dominance despite male biased sexual dimorphism. To identify dominance relationships among females and males we first explored how intrasexual dominance status affects the outcome of intersexual conflicts. Second by incorporating social and behavioral information about the context of intersexual conflicts we tested to which extent different components of power are relevant to the observed asymmetries in the relationships. Post hoc analyses indicate a sex independent dominance hierarchy with several females occupying the top ranks. Our results also reveal that two factors female leverage and motivation to help offspring had a significant influence on the outcome of intersexual conflicts. The results of our study do not indicate an overall reduction in male aggression against females but do show lower levels of male aggression in the mating context and an absence of male aggression toward those females displaying visual signs of elevated fecundity. This indicates that both female sexuality and male mating strategies are involved in the shifting dominance relationships between the sexes. © 2013 Springer Verlag Berlin Heidelberg.

Data on nest building behavior were collected from free ranging bonobos (Pan paniscus). Considering the physical features of both nests and trees used for nest construction, bonobos appeared to show various preferences: (1) Trees with small leaves were chosen more frequently than expected; (2) The majority of nests were constructed in trees of the middle forest layer (15 to 30 m) and at a mean height of 16 m; (3) nests built during the day were located higher than night nests and differed in the general mode of construction (number of trees involved). Comparing nests made by mature males and females it became apparent that females (4) built nests higher, (5) constructed day nests more frequently and (6) used them for a longer time than males. Comparison of data collected at different study sites indicates site‐specific differences concerning selection of trees and location of nesting sites. Behavioral observations made clear that nests were not only used for rest but also for other activities like feeding, social grooming and play. Moreover, the study provided the first evidence that bonobos build nests also in order to avoid potential or imminent conflicts with other party members. Field observations indicate that these nests symbolize a taboo zone and show another facet of the social abilities of bonobos for the solution of intra group conflicts. It is suggested that this behavior derives from the spatial intolerance shown by females during the process of weaning.

Bonobos are known for their pacifistic behavior and their large repertoire of behaviors that are thought to serve conflict resolution. One is an unusual form of ventro-ventral mounting that facilitates genital contacts (GC). Various hypotheses have been proposed to explain its function. In this study we tested predictions of the tension regulation hypothesis using salivary cortisol as a marker for social stress. The results indicate a temporal relationship between GC and cortisol levels. Compared with baseline data and matched samples of unrestricted food access, rates of GC increased when access to food sources was restricted. Cortisol levels were highest when access to food was constrained. However, because the behavioral and hormonal responses occurred when viewing the stimulus at a distance and preceded the physical presence of the stimulus, we conclude that the anticipation of a competitive situation was sufficient to induce social stress. Contrary to our prediction, targets of aggression did not have higher rates of GC nor did they solicit GC more often than others. Furthermore, higher GC rates did not correlate with a more pronounced decrease in cortisol levels. Not all results obtained in this study supported the predictions concerning the regulatory function of GC on social tension and further research is needed to explore this question. However, the results indicate that the anticipation of competition may be sufficient to induce a costly physiological response, and that high levels of resource competition may have lasting effects on physical stress and stress management. Am. J. Primatol. 71:223–232, 2009. © 2008 Wiley-Liss, Inc.

We present evidence for the consumption of a diurnal, arboreal, group living primate by bonobos. The digit of an immature black mangabey (Lophocebus aterrimus) was found in the fresh feces of a bonobo (Pan paniscus) at the Lui Kotale study site, Democratic Republic of Congo. In close proximity to the fecal sample containing the remains of the digit, we also found a large part of the pelt of a black mangabey. Evidence suggests that the Lui Kotale bonobos consume more meat than other bonobo populations and have greater variation in the mammalian species exploited than previously thought [Hohmann & Fruth, Folia primatologica 79:103–110]. The current finding supports Stanford’s argument [Current Anthropology 39:399–420] that some differences in the diet and behavior between chimpanzees (P. troglodytes) and bonobos are an artefact of the limited number of bonobo study populations. If bonobos did obtain the monkey by active hunting, this would challenge current evolutionary models relating the intra-specific aggression and violence seen in chimpanzees and humans to hunting and meat consumption [Wrangham, Yearbook of Physical Anthropology 42:1–30]. Am. J. Primatol. 71:171–174, 2009. r 2008 Wiley-Liss, Inc.

Chimpanzees (Pan troglodytes) are well-known to eat invertebrates, especially social insects, across Africa, but allopatric bonobos (P. paniscus) are not. Bonobo insectivory is sparsely documented and apparently sporadic. However, the availability to bonobos of social insect prey and raw materials with which to make tools to exploit them is unknown. Here, we test a set of hypotheses that relates to questions of presence, abundance, density, and distribution of taxa that Pan consume and of vegetation suitable for making extractive foraging tools. We worked at Lui Kotal, Democratic Republic of Congo, where unprovisioned bonobos live in intact forest, far from villages. We collected insect and fecal specimens, transected for prey and assessed raw materials, and monitored mounds of Macrotermes. All but 1 of the major taxa of relevant termites, ants, and (stinging) honey bees were present. The 3 main taxa of insects that chimpanzees elsewhere eat —Macrotermes (fungus-growing termites), Dorylus (Anomma; army or driver ants), and Apis (honey bees)— were abundant and widespread, and usually at densities exceeding those at well-known chimpanzee study-sites. Similarly, woody and nonwoody vegetation suitable for making fishing probes was common at mounds of Macrotermes. There is no obvious ecological reason why bonobos should not use elementary technology in extractive foraging, e.g., termite-fish, ant-fish, ant-dip, honey-dip, to obtain social insects.

Compared to data from chimpanzees, observations on prey capture and meat eating by bonobos (Pan paniscus) are still rare, fragmentary and anecdotal. Here we present new and unpublished information from wild bonobos at Lui Kotale, Salonga National Park, Democratic Republic of Congo. Our observations confirm that solitary and terrestrial ungulates are the major prey. However, bonobos at Lui Kotale also consumed other mammalian prey, including other primates. Evidence from direct observations is complemented with information obtained by macroscopic analyses of fresh faeces. Results suggest that bonobos consume meat with frequencies similar to some chimpanzee populations. The data emphasize differences between the two Pan species in terms of prey species selection and prey capture.

We collected urine samples from seven male bonobos (Pan paniscus) in the Eyengo community, Lomako Forest, Democratic Republic of Congo, and assayed them for testosterone (T). T levels averaged 525 pmol/mg Cr in adult males, and 309 pmol/mg Cr in subadult males. We collected hormonal and behavioral data during a period of relative social instability following the recent arrival of two immigrant males. In concordance with predictions derived from the challenge hypothesis [Wingfield et al., American Naturalist 136:829-846, 1990], which relates T to levels of reproductive aggression, the alpha male had the highest circulating levels of T. When we removed the two recent immigrant males from the analysis, there was a significant positive correlation between T levels and dominance rank for the long-term resident males (n=5, P=0.001, r2=0.98). These are the first data on T levels in wild bonobos, and the results suggest that further study of the relationship between T levels and social context in this species could inform current models relating hormones and aggression in wild apes.

Previous work on bonobos (Pan paniscus) has focused on the role of aggression in the context of conflict resolution in captive groups. This study investigates events of aggressive behaviour of wild bonobos to evaluate its significance in the context of mating. Temporal association (15 minutes) between aggression and mating was used to assume functional relationship. The proportion of events that were found to be related to mating activity was highest for female-female aggression followed by male-male, male-female, and female-male aggression. The results suggest that intrasexual aggression is used to manipulate the mating success of competitors: Males competed for access to oestrus females, aggression between males was high on mating days, and aggressors had higher mating rates than targets. Harassment by females disturbed mating attempts of targets, the rate of aggression increased with the number of oestrous females per party and following harassment, aggressors tended to mate more often with the male partner of the target female. Unlike intrasexual aggression, support for the predicted functions of inter-sexual aggression in the context of mating was weak. Aggression by males against females was rare and was almost never followed by mating between aggressor and target. Female aggression against males occurred frequently but appeared to be independent of mating behaviour. The results did not support the female-defence alliance hypothesis (Parish, 1996). However, when males and females engaged in close association, the rate of aggression tended to be lower and rates of mating were higher than during control periods. We suggest that male intersexual aggression is incompatible with intersexual bonding and propose that the potential benefits that males derive from affiliative long-term association with females prevent males from being aggressive against females.

In an Afrotropical forest, we tested the hypothesis that fleshy-fruit plants with interspecific differences in fruit quality and quantity affect ranging behaviour of their seed dispersal vector. If fruiting plants could affect their dispersal vector, the plants also affect their seed dispersal distance and eventually their plant population biology. From 2007 to 2011, we measured seed transport by georeference daily bonobo group movements via GPS. Seed dispersal distance was estimated with mechanistic model, using 1200 georeferenced dispersal events and the average seed transit time through bonobo (24.00 h). We compared dissemination for eight plant species that deal with this trade-off: attracting dispersers by means of fruit quality/quantity versus retaining them in the patch because of the same quality/quantity value that attracted them. Because fruit traits of these eight species were different, we expected a difference in seed dispersal distance. Surprisingly, seed dispersal distances induced by bonobos were not affected by fruit traits. Although fruit nutrient contents, abundance and average patch feeding duration differed between plant species, patch feeding time was not related to subsequent dispersal distances. The apes’ dispersal distance survey gave an average dispersal distance estimated of 1332 ± 24 m from the parent plant (97.9% > 100 m). To conclude, feeding time invested in the patch, fruit quality and abundance had no apparent effect on bonobo seed dispersal distance. The possible effects in plant population biology are discussed.

In many Old World primate species, female attractivity increases during the tumescent phase of the sexual swelling for a period that lasts considerably longer than oestrus-related attractivity in other mammals. We examined the reliability of the swelling as an indicator of ovulation in captive bonobos, a species with a long and variable phase of maximum tumescence. Using a combined approach of (1) observations of sexual behaviour, (2) visual scoring of the sexual swelling and (3) analysis of faecal progestin to assess the timing of ovulation during 23 ovulatory cycles of eight adult females, we found that in 30% of these cycles the presumed day of ovulation did not fall within the period of maximum tumescence. When ovulation did occur during maximum swelling, it was more closely related to the end rather than the onset of the maximum swelling period. However, the pattern of sexual swelling was not a reliable indicator of ovulation. In addition, sexual behaviour of both sexes increased in frequency with the degree of the swelling but not around the time of ovulation. We conclude that swellings in bonobos provide honest information on the probability of ovulation, but not its exact timing, and that therefore the ‘obvious ovulation’-hypothesis cannot explain the function of sexual swellings in bonobos.

Coalitions among males during within group conflicts have a strong influence on the competitive and social environment within social groups. To evaluate possible variation in the occurrence of such coalitions in our closest relatives, chimpanzees and bonobos, we compared male aggression and coalitionary behavior in two natural communities, one of each species, with a similar size and composition. Furthermore we compared affiliative behavior that might be related to coalition formation among males. We found higher frequencies of aggression and a greater likelihood to form coalitions during within-group conflicts among wild male chimpanzees at Tai compared to wild male bonobos at LuiKotale. The species differed in the predominant sex of the male coalition partners, with male bonobos forming coalitions more often with females, while male chimpanzees formed coalitions more often with other males. Compared to male bonobos, male chimpanzees showed higher rates of grooming and tended to reconcile more conflicts with other males. Overall our results showed lower frequencies of reconciliation among bonobos than those described in captivity and at artificial feeding sites. These findings add to the evidence that male cooperation and conflict resolution are potentially very different in bonobos and chimpanzees, despite the fact that these two species are closely related, live in multi-male, multi-female communities with a high degree of fission-fusion dynamics and have female-biased migration patterns. Given the correlation between aggressive, cooperative and some affiliative patterns within the species in our study, we hypothesize that the fitness benefits of male relationships are greater in chimpanzees compared to bonobos.

This study reports on close spatial association and repeated behavioural interactions between two strange adult male bonobos with residents of another community. Over a period of 12 months one of the two males developed friendly social relations to some of the females and other residents, which were indistinguishable from those existing between co-residents. Aggression by resident males against the strangers decreased but the former remained intolerant. The strange males appeared at a time when the number of adult resident males was lower as in the years before and when the adult sex ratio (number of adult females per male) was higher as in the years before. Using definitions from studies on dispersal patterns of male gorillas (Harcourt, 1978) and female bonobos (Furuichi, 1989) the spatial association between the two strange males and residents could be described as male transfer.

Abstract Studies of captive populations of bonobos suggest that females are more gregarious than males. This seems to contradict assumed sex-differences in kinship deriving from a species-typical dispersal pattern of female exogamy and male philopatry. Here we present data on spatial associations and affiliative relations among members of one wild community (Eyengo) for which genetic relationships were identified by analysing mitochondrial and nuclear DNA. Our data from Lomako confirm the existence of spatial associations among resident females. In addition, they reveal strong social bonds between males and females. While most female-female associations did not last longer than one field season, long-term associations occurred predominantly between mixed-sex dyads and involved both close kin and unrelated individuals. Differences in social grooming appeared to be related to patterns of spatial association rather than to kinship. It is suggested that under natural conditions social organisation of bonobos is characterised by strong inter-sexual bonds. Males may benefit from bonding with females by increased reproductive success via rank acquisition. For females benefits may derive from inclusive fitness and reduced food competition. Preliminary evidence suggests that females also may benefit from protection by resident males against male intruders.

We describe the cannibalization of an infant bonobo (circa 2.5 years old) at Lui Kotale, in the Democratic Republic of Congo. The infant died of unknown causes and was consumed by several community members including its mother and an older sibling one day after death. Certain features concerning the pattern of consumption fit in with previously observed episodes of cannibalism in Pan, whereas others, such as the mother's participation in consuming the body, are notable. The incident suggests that filial cannibalism among apes need not be the result of nutritional or social stress and does not support the idea that filial cannibalism is a behavioral aberration. Am. J. Primatol. 72:509–514, 2010. © 2010 Wiley-Liss, Inc.

Adult male Nilgiri langurs (Presbytis johnii) utter loud call bouts consisting of one or more phrases. Phrases are made up of several units showing similar or different structural features. The units involved differ with respect to not only their physical structure but also their overall utilization: three vocal patterns are uttered exclusively by mature males living in bisexual groups or all-male bands and, in addition to being part of loud call bouts, are given during encounters with terrestrial predators; two vocal patterns are uttered by males and females, again not just as constituents of loud calls; and one vocal pattern is given exclusively by mature males living in bisexual groups. Within a given bout, phrases differ not only with respect to their composition but also in their temporal organization. In addition to the acoustic components, loud calls are regularly accompanied by stereotyped motoric displays. The motoric and acoustic components of loud call displays appear independently of each other and at different times during ontogeny. The development of the display is characterized by combination of units with different structural features and synchronization of vocal and motoric components. Although more evidence is needed, our observations suggest that the development of loud call displays coincides with the aquisitation of social maturation and competence and requires not only social experience but also a certain amount of motoric training. In spite of the high degree of ritualization, loud call displays are not completely fixed in form, but instead are open to individual- and population-specific variation.

Urinary metabolites of androgens and cortisol were measured in free-living male and female bonobos. Sex differences and correlations between adrenal and gonadal steroid excretion were investigated. The immunoreactive concentrations of androgens were measured with two different androgen assays. One assay used a testosterone (T) antibody raised with a 17beta-hydroxy group, and the other employed an antibody raised against a reduced form, 5alpha-androstane-17alpha-ol-3-one-CM (17alpha) with cross reactivity for epitestosterone and 5alpha-androstanedione. Both assays have been used in bonobo and chimpanzee studies where non-invasive techniques were employed. The levels of 17alpha-androgen metabolites were 1.7- and 3-fold higher than those of T-metabolites in males and females. The two androgen assay results correlated in males but not females. There was a sex difference in the T-metabolites measured. Male levels were significantly higher. Levels of 17alpha in the two sexes were similar. Cortisol metabolite levels (CORT) were similar between the sexes. The T-metabolites were significantly correlated with CORT in males but not in females. In females, the 17alpha-androgen metabolites correlated with CORT. This suggests that either androgen secretion or metabolism differs between the sexes. A parsimonious interpretation of the androgen assay cortisol/androgen correlation differences would be that larger components of dehydroepiandrosterone (DHEA), androstenedione or epitestosterone from the adrenal androgens were being excreted and measured in the females. The CORT/T metabolite interactions in males may reflect male-specific social or metabolic endocrine conditions.

Current models of social organization assume that predation is one of the major forces that promotes group living in diurnal primates. As large body size renders some protection against predators, gregariousness of great apes and other large primate species is usually related to other parameters. The low frequency of observed cases of nonhuman predation on great apes seems to support this assumption. However, recent efforts to study potential predator species have increasingly accumulated direct and indirect evidence of predation by leopards (Panthera pardus) on chimpanzees and gorillas. The following report provides the first evidence of predation by a leopard on bonobos (Pan paniscus) .

Female bonobos, Pan paniscus, show a mounting behaviour that differs physically from that in other primate species. They embrace each other ventroventrally and rub their genital swellings against each other. We investigated five hypotheses on the function of ventroventral mounting (genital contacts) that derive from previous studies of both primate and nonprimate species: (1) reconciliation; (2) mate attraction; (3) tension regulation; (4) expression of social status; and (5) social bonding. We collected data in six field seasons (1993-1998) from members of a habituated, unprovisioned community of wild bonobos at Lomako, Democratic Republic of Congo. No single hypothesis could account for the use of genital contacts, which appeared to be multifunctional. We found support for hypotheses 1 and 3. Rates of postconflict genital contacts exceeded preconflict rates suggesting that the display is used in the context of reconciliation. Rates of genital contacts were high when food could be monopolized and tension was high. However, genital contacts also occurred independently of agonistic encounters. Our study shows rank-related asymmetries in initiation and performance of genital contacts supporting the social status hypothesis: low-ranking females solicited genital contacts more often than high-ranking females while the latter were more often mounter than mountee. Although subordinates took more initiative to achieve genital contact, dominants mostly responded to the solicitation (ventral presentation) with mounting, indicating that the performance benefits both individuals. We suggest that genital contacts can be used to investigate both quality and dynamics of dyadic social relationships among female bonobos. Copyright 2000 The Association for the Study of Animal Behaviour.

Sound recordings and behavioural data were collected from four primate species of two genera (Macaca, Presbytis). Comparative analyses of structural and behavioural aspects of vocal communication revealed a high degree of intrageneric similarity but striking intergeneric differences. In the two macaque species (Macaca silenus, Macaca radiata), males and females shared the major part of the repertoire. In contrast, in the two langurs (Presbytis johnii, Presbytis entellus), many calls were exclusive to adult males. Striking differences between both species groups occurred with respect to age-specific patterns of vocal behaviour. The diversity of vocal behaviour was assessed from the number of different calls used and the proportion of each call in relation to total vocal output for a given age/sex class. In Macaca, diversity decreases with the age of the vocalizer, whereas in Presbytis the age of the vocalizer and the diversity of vocal behaviour are positively correlated. A comparison of the data of the two genera does not suggest any causal relationship between group composition (e.g. multi-male vs. one-male group) and communication system. Within each genus, interspecific differences in vocal behaviour can be explained by differences in social behaviour (e.g. group cohesion, intergroup relation, mating behaviour) and functional disparities. Possible factors responsible for the pronounced intergeneric differences in vocal behaviour between Macaca and Presbytis are discussed.

During a field study on habituated groups of wild Nilgiri langurs (Presbytis johnii),four cases of group fission were observed which differed markedly from group changes reported in other species of the same genus. All fissions occurred in groups with more than one mature male and roughly coincided with the onset of loud call vocalization by the second mature male group member. As a result of the fission the founder group factions acquired the structure of a onemale group. The filial factions consisted of both mature males and females and occupied, at least temporarily, a part of, or an area adjacent to, the founder group. During fission, the amount of aggressive interactions between the two mature males increased. However, the majority of agonistic interactions involved ritualized threat and intimidation behavior without physical aggression. In at least three cases the two mature males involved in the fission had not joined recently but had lived in these groups for three years or more. Although the presence of all male bands and single males in the two study populations indicate that male replacement by invasive takeovers may occur, it is suggested that in Nilgiri langurs, noninvasive fissions are probably another common mechanism for the foundation and maintenance of bisexual one-male groups.

Investigations of vocal communication in captive groups of lion-tailed macaques (Macaca silenus) revealed a repertoire of 17 basic patterns. Sixteen of them were recorded and their physical parameters analysed by sonagrams. During a field study these results were verified and complemented, and additional data on the vocal behaviour of this species were gathered. The vocal repertoire of lion-tailed macaques is characterized by discretely structured, mostly interaction- and situation-specific sound patterns. The fundamental characteristics of vocal communication seem to be adjusted to the acoustic conditions of the rain forest habitat as well as to the social organization in 1-male groups. In contrast to other species of the macaque genus, lion-tailed macaques are highly adapted to a strictly arboreal life in the rain forests of the Western Ghats (South India). Due to the dense vegetation in this habitat, propagation of visual signals is restricted to short distances. Vocal signals are therefore of great importance. The vocal repertoire of lion-tailed macaques differs from that of more terrestrial macaques insofar as the basic patterns show comparatively insignificant structural variations. Also, patterns were recorded which have not yet been found in any other member of the genus.

BackgroundExpansion of brain tissue and development of advanced cognitive skills are characteristic traits of human evolution. Their emergence has been causally linked to the intake of nutrients that promote brain development and iodine is considered a critical resource. Rich sources of iodine exist in coastal areas and evolutionary scenarios associate the progressive development of brain size and cognitive skills to such landscapes. This raises the question of how early hominins living in continental areas could have met their iodine requirements. One way to explore this question is to use information from hominoid primates as a proxy for the nutritional ecology of early hominins. Bonobos are particularly interesting in this context as they are restricted to the central part of the Congo basin, an area considered to be iodine deficient based on human standards.MethodsPooled samples of fruit, terrestrial and aquatic herbs were used to assess mineral content with an inductively coupled plasma optical emission spectrometer. Iodine content was measured with the catalytic technique of Sandell-Kolthoff and two separate inductively coupled plasma mass spectrometry methods.ResultsNutritional analyses revealed that the mineral content of aquatic herbs is higher than in other plant foods. Moreover, two species of aquatic herbs consumed by bonobos contain iodine concentrations that are almost equivalent to marine algae.ConclusionsThese data challenge the general notion that the Congo basin is iodine deficient and demonstrate that its lowland forest offers natural sources of iodine in concentrations high enough to prevent iodine deficiency in hominoids and humans. published