Context and Development of Sexual Behavior of Wild Bonobos (Pan paniscus) at Wamba, Zaire

I studied sexual behavior of immature bonobos (Pan paniscus) in a wild group living at Wamba, Zaire, with special reference to its development. Even immature individuals under 1 year old performed sexual behavior. Sexual behavior occurred in almost all age–sex combinations, except between immature and mature females. Based on analyses of behavioral pattern and context, I classified sexual behavior involving immature individuals into three categories. (1) Genital contact between immature individuals was observed during play, and was performed by males more frequently than by females. This sexual behavior shared many traits with that of other great apes. (2) Copulation-like genital contact was observed between immature males and mature females. Its frequency increased with the immature male's age; it developed into copulation in adulthood. (3) Genital contact used to regulate interindividual relationships. This behavior, which is unique to bonobos, was absent among infants. It developed between late juvenile and early adolescent periods in association with changes in social circumstances.     

Effect of Male Emigration on the Vigilance Behavior of Coresident Males in White-Faced Capuchins (Cebus capucinus)

I examined the vigilance behavior of male Cebus capucinus residing in four groups in Santa Rosa Park, Costa Rica. One male emigrated from each of three study groups, providing ideal experimental conditions for examining the effect of coresident males on male vigilance behavior (social and non-social). Following the predator and conspecific defense theories for the adaptive value of male vigilance behavior and the occurrence of multimale groups, I predicted that male nonsocial vigilance would increase after the emigration of a coresident male. My prediction was supported in only one of the three study groups. Males in two groups decreased their nonsocial vigilance after the emigration of a coresident male, which was probably influenced by seasonal changes and the peripherality of one group's coresident male before his emigration. The social vigilance hypothesis proposes that for species with rigid dominance hierarchies, social vigilance should increase with an increase in same sex competitors. Therefore, I predicted that male social vigilance would decrease after the emigration of a coresident male. The hypothesis is generally supported in my findings, as two of the three groups displayed a decrease in social vigilance after the emigration of a coresident male. Increased social vigilance in the third group is best explained by the change in the alpha male's social behavior after the emigration of his only coresident male.     

Agonistic Interactions and Matrifocal Dominance Rank of Wild Bonobos (Pan paniscus) at Wamba

I studied dominance relations in a wild group of bonobos at Wamba, Democratic Republic of Congo. Although agonistic interactions between males occurred frequently, most of them consisted only of display, and physical attacks were infrequent. Dominance rank order seemed to exist among males, but its linearity is unclear. Dominant males rarely disturbed copulatory behavior by subordinate males. However, high-ranking males usually stayed in the central position of the mixed party and, so, would have more chance of access to estrous females. Among females, older individuals tended to be dominant over younger individuals. However, agonistic interactions between females occurred rather infrequently, and most consisted of displacement without any overt aggressive behavior. Dominance between males and females is unclear, but females tended to have priority of access to food. The close social status between males and females may be related to the prolonged estrus of females and their close aggregation during ranging. Existence of a male's mother in the group and her dominance status among females seemed to influence his dominance rank among males. Young adult males whose mothers were alive in the group tended to have high status. In some cases, change in dominance between high-ranking males was preceded by a corresponding change in dominance between their mothers. As the dominance status of females is similar to that of males, mothers may be able to support their sons to achieve high status, stay in the center of the mixed party, and so have greater access to females, which may maximize the number of descendants of the mothers.     

Allogrooming Behavior and Grooming Site Preferences in Captive Bonobos (Pan paniscus): Association with Female Dominance

I tested the utility of Seyfarth's (1977) model of rank-related attractiveness to explain the distribution of allogrooming behavior among captive bonobos (Pan paniscus). Adult female bonobos generally have high social status and may be dominant over males. As predicted by the model, I found that high-ranking adult females received most allogrooming within each of the four investigated groups. Among adult female-adult female dyads, however, allogrooming was not clearly associated with dominance rank. Contradictory to predictions of the model, the highest-ranking females were responsible for most displacements over allogrooming, and grooming competition is positively correlated with dominance rank. In the second part of this study, I investigated the social significance of allogrooming body site preferences. Bonobos direct significantly most allogrooming to the face of conspecifics, and high- and low-ranking individuals, as well as males and females, differ significantly in their preferences for certain allogrooming sites. Subordinates and males tended to avoid facial grooming and preferred the back and anogenital region, while high-ranking individuals and females directed most allogrooming to the face and head of grooming partners. Data from this study support the hypothesis that high-ranking females are the most attractive grooming partners within a female-centered bonobo society. Many other aspects of allogrooming behavior, however, are not consistent with the model of rank-related attractiveness.     

Hand Preference in Free-Ranging White-Throated Capuchins (Cebus capucinus) in Costa Rica

I studied the hand preference patterns of individuals in three troops of white-throated capuchins (C. capucinus) in Palo Verde, Costa Rica, during 11 months from February 1995 to January 1996. I used focal and ad libitum sampling techniques and tested several frameworks that seek to explain and to predict primate hand use patterns via a variety of spontaneous tasks that differ in manipulative difficulty and required postural regulation: reach, tap, grab, carry, and object-use. The monkeys showed symmetrical hand use patterns for the easy tasks, reach and tap; strongly asymmetrical patterns for the highly manipulative task, object-use, at the individual level; and weak population-level biases for tasks requiring a degree of postural regulation, carry. The results for data on grab are inconclusive. These results do not support the available primate hand use frameworks and differ from most of the captive literature on hand preference in Cebus. The findings indicate that postural regulation may influence hand use patterns in nonhuman primates at the population level.     

Urine Washing and Sniffing in Wild White-faced Capuchins (<Emphasis Type=Italic>Cebus capucinus</Emphasis>): Testing Functional Hypotheses

Urine washing (UW) is taxonomically widespread among strepsirhines and platyrrhines, yet its functional significance is still unclear. We used 2274 h of focal follows of 35 adult and subadult wild white-faced capuchins (Cebus capucinus) to test 1) the intergroup signaling, intragroup social signaling, and thermoregulatory hypotheses for UW and 2) the hypothesis that individuals sniff each other's urine and other traces to gather socially significant information. Males engaged in significantly more UW than females. All 5 α-males engaged in more UW than subordinate males did, including 4 α-males that increased their UW rate above that of their male groupmates after their rise to α rank. Males engaged in significantly less UW while in view of other males than at other times. Male-male sniffing rates do not correlate with either aggression rate or dominance rank distance. Urine washing rates did not increase while subjects were in parts of their home range where more intergroup encounters occurred. Urine washing rates were highest early in the morning and late in the afternoon, presumably when temperatures were coolest. The data do not support either the thermoregulatory or social signaling hypothesis. We suggest that experiments with captive capuchins are necessary to resolve the issue of the function of urine washing in the taxon.     

Ant-Gathering with Tools by Captive Tufted Capuchins (Cebus apella)

We examined ant-gathering with tools by captive tufted capuchins (Cebus apella) via two experiments. In Experiment 1, we provided groups of subjects with sticks and small branches and an apparatus that accommodated the use of tools to gather ants. In Experiment 2, we sealed the apparatus with acetate and provided the same subjects with sticks and stones. Seven of 14 subjects used sticks and leaves as probes to extract ants from the apparatus. Six of them modified probes by detaching sticks from larger branches, breaking sticks into two or more pieces, and subtracting leaves and bark. Three subjects later used a stone and stick tool-set to penetrate acetate barriers and to extract ants. These results demonstrate the use of tools by Cebus to capture moving prey and are consistent with the idea that sensorimotor skills associated with the production and use of tools in primates evolved convergently in capuchins and great apes.     

Habitat Use and Ranging of Wild Bonobos (Pan paniscus) at Wamba

The relationship between vegetation and ranging patterns of wild bonobos at Wamba, Democratic Republic of the Congo, was examined. Via Landsat data, we distinguished three types of vegetation—dry forest, swamp forest, and disturbed forest—at Wamba. The home ranges of the study groups changed considerably from year to year, due mainly to intergroup relationships. The population density of each group varied between 1.4 and 2.5 individuals per km ² and was lowest during a period of population increase. Home ranges consisted mainly of dry forest. The bonobos used dry forest more frequently than the other forest types, though they also used swamp and disturbed forest almost every day. The latter types of forest seemed to be important resources for the bonobos, owing to the abundant herbaceous plants that are rich in protein and constantly available. The bonobos tended to use dry forest more frequently in the rainy season than in the relatively dry season, probably because the favored fruits in the dry forest were mostly available in the rainy season. There was no seasonal difference in the size of the daily ranging area.     

Sexual behavior in brown capuchins ( Cebus apella )

We observed sexual behavior patterns in two captive groups of Cebus apella.We obtained data on intersexual solicitations and intersexual competition. The length of proceptivity cycles by females averaged 18.8 ± 1.2 days; this corresponds with published reports of physiological measures of ovulatory cycles. Females initiated sexual interactions with males significantly more than males initiated interactions with females, and female solicitations increased in frequency over the duration of displayed periods of proceptivity. In contrast, male solicitations of females were infrequent and did not change significantly throughout female proceptive phases. Each female solicited the same male throughout a given proceptive phase. We observed no evidence of male-male or female-female competition. Males seem to respond to female sexual behavior directed toward them, rather than initiating sexual interactions themselves. Even so, male sexual interactions with females followed only a small proportion of solicitations.     

Dominance and its Behavioral Measures in a Captive Group of Bonobos (Pan paniscus)

We investigated the existence of a social dominance hierarchy in the captive group of six adult bonobos at the Planckendael Zoo. We quantified the pattern of dyadic exchange of a number of behaviors to examine to what extent each behavior fits a linear rank order model. Following de Waal (1989), we distinguish three types of dominance: agonistic dominance, competitive ability and formal dominance. Fleeing upon aggression is a good measure of agonistic dominance. The agonistic dominance hierarchy in the study group shows significant and strong linearity. The rank order was: 1. female (22 yr), 2. female (15 yr)., 3. male (23 yr.), 4. female (15 yr.), 5. male (9 yr.), 6. male (10 yr.). As in the wild, the females occupy high ranks. There is prominent but nonexclusive female agonistic dominance. Teeth-baring does not fulfil the criteria of a formal submission signal. Peering is a request for tolerance of proximity. Since its direction within dyads is consistent with that of fleeing interactions, it is a useful additional measure to determine agonistic ranks in bonobos. In competitive situations, the females acquire more food than other group members do. The rank obtained from access to food resources differs from the agonistic rank due to female intrasexual social tolerance, expressed in food sharing. We typify the dominance styles in the group as female intrasexual tolerance and male challenging of rank differences. The agonistic rank order correlates significantly with age and has a strong predictive value for other social behaviors.     

Sexual competition in a group of captive bonobos (Pan paniscus)

We describe the occurrence of sexual competition, expressed as harassment of sexual interactions in a captive group of bonobos. We monitored all aggressive and pestering interventions during sexual interactions of three captive adult females, one adolescent, and three adult males. The study period covered two complete menstrual cycles for each female, with continuous daily observations. There was relatively little overt sexual competition by the males, in analogy with other studies. Most male interventions occurred towards interactions with the alfa female. The alfa female performed the most intense and the highest number of interventions towards the sexual interactions of the other females. The data provide evidence for female intra-sexual competition in this female dominant species.     

Short-Term Benefits of Play Behavior and Conflict Prevention in Pan paniscus

Most theories on the function of play have focused on ultimate rather than proximate benefits. Play peaks during juvenility but, in some species, it is present in adulthood as well. In primates, social play and grooming often show a matched pattern because they bring individuals into close contact and favor social cohesion. In Pan, researchers have widely documented anticipation of competition at feeding time. Chimpanzees limit aggression over food by grooming (celebration), whereas bonobos use sociosexuality as a reassurance mechanism. We examined the function of play in the context of conflict prevention in the Apenheul bonobo colony. We analyzed the distribution of social play, grooming, and sexual contacts in periods around feeding and in a control condition. Adult-adult and adult-immature play frequencies were significantly higher during prefeeding than in any other condition, thus not supporting the commonly held view that social stress suppresses play. Further, there is a significant positive correlation between adult-adult play and rates of cofeeding. During feeding, adults engaged in their highest levels of sociosexual behaviors, whereas an increase in grooming rates occurred in prefeeding, though not significantly compared to the control rates. In conclusion, bonobos apparently cope with competition and social tension via 2 different mechanisms of conflict management: play to prevent tension, e.g., prefeeding, and sociosexual behaviors as appeasement and reassurance mechanisms once a tense situation emerges.     

Spatial Facilitation in a Probing Task in Wedge-Capped Capuchins (Cebus olivaceus)

Activities ordinarily performed by an animal in a given place may influence the way it behaves towards an object newly found there. We examined the use of probing tools in a group of 4 wedge-capped capuchins (Cebus olivaceus), in the home cage into which we simultaneously introduced two identical apparatuses, one at a site ordinarily used to manipulate objects, and the other at a site mainly used for visual monitoring. We expected that spatial facilitation would occur, i.e., the subjects would be more efficient at the site where manipulative behaviors were more frequently performed. Two monkeys used probing tools to extract syrup from the openings of the apparatuses. Tool use efficiency was higher with the apparatus located at the site where they had performed more manipulative and combinative behaviors. These results are consistent with the hypothesis of spatial facilitation and illustrate the fact that spatial context can be an overwhelming variable that should not be neglected in behavioral research dealing with instrumental tasks.     

Vocal Repertoire of Cebus capucinus: Acoustic Structure, Context, and Usage

Researchers studying nonhuman primate vocal repertoires suggest that convergent environmental, social, and motivational factors account for intra- and interspecific vocal variation. We provide a detailed overview of the vocal repertoire of white-faced capuchins, including acoustic analyses and contextual information of vocal production and vocal usage by different age-sex classes in social interactions. The repertoire is a mixture of graded and discrete vocalizations. In addition, there is general support for structural variation in vocalizations with changes in arousal level. We also identified several combined vocalizations, which might represent variable underlying motivations. Lastly, by including data on the social contexts and production of vocalizations by different age-sex classes, we provide preliminary information about the function of vocalizations in social interactions for individuals of different rank, age, and sex. Future studies are necessary to explore the function of combined vocalizations and how the social function of vocalizations relate to their acoustic structure, because social use of vocalizations may play an important role in shaping vocal evolution.     

Inter-menstrual intervals in captive bonobosPan paniscus

In this study we provide new data on the duration of the inter-menstrual intervals of six captive female bonobos (Pan paniscus). We found that the mean duration of the inter-menstrual interval was about 34 days. This lies close to the average value of 37 days that has been reported for common chimpanzees (Pan troglodytes).     

Hand Preferences in Different Tasks by Tufted Capuchins (Cebus apella)

We examined hand preferences in 25 tufted capuchins (Cebus apella) in three tasks. The hole task involved a single action of reaching for food in a hole. The horizontal panel and the vertical panel tasks required the alignment of two apertures, by moving or lifting a panel, to reach for food in a hole. We found a significant group-level right-hand preference for reaching actions in the hole and in the horizontal panel tasks, but not in the vertical panel task, in which the food retrieval implied the complementary use of both hands. No significant hand bias emerged for moving or lifting actions with high visuospatial components. There is a stronger hand preference in more complex manual activity—coordinated bimanual hand use for food retrieval—than in other unimanual measures. We discuss the results in the context of previous reports on primate laterality.     

Violent coalitionary attacks and intraspecific killing in wild white-faced capuchin monkeys (<Emphasis Type="Italic">Cebus capucinus</Emphasis>)

During 12 years of observation, we have observed three confirmed and two inferred lethal coalitionary attacks on adult male white-faced capuchins (Cebus capucinus) by members of two habituated social groups at Lomas Barbudal Biological Reserve, Costa Rica. In one case, an alpha male was badly wounded and evicted from his group, and when later found by his former groupmates he was attacked by several of them and died less than 24 h later. In two other cases, lone extra-group males were mobbed by adult and immature males of a bisexual group. One victim's abdomen was torn open and he died less than 24 h later. A second victim was quite badly bitten but may have escaped. The fourth and fifth cases resulted from intergroup encounters. One victim lost the use of both arms but may have survived, whereas the other died of unknown causes within an hour of the attack. The observed death rate from coalitionary aggression at our site is approximately the same as that reported for eastern chimpanzees. Because at least three of the five observed incidents involved large coalitions attacking lone victims, they support the general hypothesis that imbalances of power contribute to intraspecific killing in primates. However, the occurrence of lethal coalitional attacks in a species lacking fission–fusion social organization poses a challenge to the more specific version of the imbalance-of-power hypothesis proposed by Manson and Wrangham in 1991 to explain chimpanzee and human intergroup aggression.     

Sexual and Cleaning Behavior and Related Morphology in the Genus Cerocoma (Coleoptera: Meloidae)

The study of sexual behavior has been largely utilized in phylogenetic analyses of Meloidae beetles. Sexual behavior of the tribe Cerocomini is almost unknown, even though the genus Cerocoma shows the most striking sexual dimorphism in the family. In this paper, the sexual behavior of five species, C. (Cerocoma) adamovichiana, C. (C.) graeca, C. (C.) schaefferi, C. (Metacerocoma) schreberi, and C. (M.) prevezaensis, is described. The cleaning behavior of this genus, previously unknown, is also discussed. A morphological analysis by scanning electron microscopy of sexually dimorphic anatomical features of antennae, maxillary palpi, and forelegs, involved in cleaning and sexual activities, is carried out.     

Vertebrate Predation and Food-Sharing in Cebus and Pan

Capuchins and chimpanzees are the only nonhuman primates apart from baboons known to prey systematically upon relatively large vertebrates. Vertebrate predation is common and well documented in Pan troglodytes, rare in Pan paniscus, and commonly reported but infrequently studied in Cebus. Food-sharing is common in both Pan species but rarely reported for wild capuchins. I present data on vertebrate predation and food-sharing by white-faced capuchins (Cebus capucinus) from ongoing field studies at Santa Rosa National Park, Costa Rica. We have observed 106 successful predation events resulting in the capture of 156 prey items during 2929 observation hr (5.35 prey per 100 hr). Squirrels and nestling coatis comprised half of the prey taken; the remainder were mainly nestling birds and eggs. Adult males took 52% of all prey and 67% of squirrels. Squirrels are actively hunted and about 65% of them are adults. I estimated that the average capuchin group kills 43–50 squirrels annually, mostly during the dry season. Capuchins hunt squirrels in groups 81% of the time, and 17% of hunts are successful. There is no evidence for cooperative hunting, but occasional collaboration is suggested. Rates of food-sharing were low (1.7 per 100 hr), and meat was the only food shared between adults. I compare predation and food-sharing in C. capucinus with published data for Pan troglodytes, primarily in Gombe and Taï National Parks. I discuss sex differences, hunting strategies, the relationship between hunting and food-sharing, and various ecological and social factors that may promote vertebrate predation in Pan and Cebus.