Non-antagonistic relations between wild bonobos and two species of guenons

Interspecific relations between wild bonobos (Pan paniscus) and two species of guenons (Cercopithecus wolfi andC. ascanius) were studied at Wamba in the Central Zaire Basin from September 1989 to January 1990. Data on the guenons were collected while following parties of bonobos or when searching for them. The guenons were observed directly 59 times during the study period. In about half of these observations, the guenons were found within 20 m from the bonobo parties. The encounters between the bonobos and the guenons sometimes lasted over an hour. The guenons mainly initiated the encounters by approaching the bonobos. During the encounters, no aggressive interactions were observed between the bonobos and the guenons. Evidence of hunting by wild bonobos has been restricted to small mammals, and there has been no evidence of hunting of primates by wild bonobos. These findings and the results of the present study strongly suggest that wild bonobos do not hunt sympatric primates.     

Do bonobos copulate more frequently and promiscuously than chimpanzees?

The copulatory activities of bonobos (Pan paniscus) of Wamba, Zaire, were compared with those of chimpanzees (P. troglodytes schweinfurthii) of Mahale, Tanzania. The copulation rates of adult male bonobos were equal to or lower than those of adult male chimpanzees. The copulation rates of adult female bonobos were approximately equal to those of adult female chimpanzees who were in maximal genital swelling, but it should be much higher than those of the adult female chimpanzees throughout the birth interval. The copulation rates of adolescent male bonobos were lower than those of adolescent male chimpanzees, whereas the copulation rates of adolescent female bonobos were much higher than those of adolescent female chimpanzees. It was suggested that the bonobos of Wamba did not copulate more promiscuously than did the chimpanzees of Mahale. The female bonobos may show “receptivity”, whereas female chimpanzees may show rather “proceptivity”.     

Function of peering behavior among bonobos (Pan paniscus) at Wamba,Zaire

Peering behavior (prolonged gazing within 30 cm by an animal toward another) in wild bonobos (Pan paniscus) at Wamba, Zaire, was studied. A total of 230 peering episodes were observed in various social contexts. Peering behavior was often directed from younger animals toward older ones. In particular, adult females were most frequently involved in peering, with individuals of all age-sex classes. On the other hand, male bonobos seldom took part in peering behavior. Four types of behavior patterns followed the peering behavior: (1) the peerer left; (2) the peeree left; (3) both peerer and peeree stayed but had no further social interaction; and (4) some other social interaction followed. Type (1) was the most frequent. Peering usually led to tolerance by older (dominant) animals of a younger (subordinate) animal’s subsequent actions directed towards the former. Peering was thus concluded to be a unilateral action for initiating affinitive interactions by the peerer.     

Comparison of behavioral sequence of copulation between chimpanzees and bonobos

We compared sex differences in behaviors leading to copulation of chimpanzees (Pan troglodytes) in the Kalinzu Forest, Uganda with those of bonobos (Pan paniscus) at Wamba, D.R. Congo, using the same definition. Female chimpanzees were more likely to initiate copulation than female bonobos. While most of copulations (96%) were initiated by males in bonobos, among chimpanzees only 63% of copulations were initiated by males. Female bonobos initiated an interaction leading to copulation when males approached them within a short distance. On the other hand, both male and female chimpanzees initiated behavior at a longer distance. Higher proceptivity and a higher copulation rate during the maximal swelling period of female chimpanzees might suggest that they gain greater benefits from a high frequency of copulations than do female bonobos.     

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.     

Male-male relationships among wild bonobos (Pan paniscus) at Wamba,Republic of Zaire

Male-male relationships among wild bonobos (Pan paniscus) in two adjacent unitgroups (E1 and E2 groups), which were formed by division of the E group, were studied at Wamba, in the Central Zaire Basin, by analyzing the proximity and social interactions among males. Dominant-subordinate relationships between a male-male dyad were easily recognized from the directions of individual agonistic interactions. Male bonobos rarely joined forces in aggression. Clear differences in social status existed between adult and adolescent male bonobos in both groups, as reported in the case of chimpanzees (Pan troglodytes). The presence of mothers in the unit-group greatly influenced the dominant-subordinate relationships among males through strong mother-son bonds in both groups. However, the extent of the mother-son bonds differed between the groups. Males in the E2 group participated more frequently in agonistic or affinitive interactions than did males in the E1 group. Males in the E1 group were divided spatially into several clusters, while there were cohesive relationships among the adult males in the E2 group. The difference in intensities of mother-son bonds between the groups may be explained by the distribution of males at the time of the division of the E group. Differences in male-male relationships between bonobos and chimpanzees seem to be related to differences in intra- and inter-unit-group competition among males between the two species. Male chimpanzees may achieve coexistence by manipulating ambivalent relationships that are caused by intra- and inter-unit-group competition among them, while male bonobos may achieve coexistence by decreasing intra- and inter-unit-group competition among them.     

Interspecific interactions between wild pygmy chimpanzees (Pan paniscus) and red colobus (Colobus badius)

Interspecific interactions accompanied by physical contacts between wild pygmy chimpanzees (Pan paniscus) and red colobus (Colobus badius) were observed on three occasions at Wamba, Republic of Zaire. In all cases, the red colobus initiated the interactions by approaching the pygmy chimpanzees. Most of the pygmy chimpanzees, which were within 5 m of the red colobus, were juveniles or infants but the adult male pygmy chimpanzees never showed any interest in the red colobus. The red colobus groomed the chimpanzees in two cases, but the latter never groomed the former. No true aggressive interactions were observed between the two species. The lack of any evidence of hunting of red colobus through longitudinal studies of the pygmy chimpanzees of Wamba, together with the present observations, suggests that red colobus are probably not targets of hunting by the pygmy chimpanzees.     

Matrilineal kin relationship and social behavior of wild bonobos (Pan paniscus): Sequencing the D-loop region of mitochondrial DNA

Matrilineal kin-relations among wild bonobos (Pan paniscus) were studied by DNA analysis. Subject individuals were the members of E1 group, living at Wamba, Zaire, which has been studied since 1974. DNA samples were extracted from wadges that bonobos spat out when feeding on sugar cane. The D-loop region of mitochondrial DNA was amplified by the PCR method, and a nucleotide sequence of 350 base pairs was determined for 17 individuals. Nucleotide variations were found at 44 positions of the sequence. Based on these variations, 13 matrilineal units were divided into seven groups, and the mother of an orphan male was determined among several females. These genetic analyses, together with behavioral observation to date, revealed the following facts. High sequence variation in the target region indicated that females transfer between groups of bonobos, which is in agreement with supposition from long-term field studies. For females, there was no relationship between genetic closeness and social closeness that is represented by frequencies of proximity or grooming. After immigration into a new group, females form social associations with senior females without regard to kin relationship.     

Cases of maternal cannibalism in wild bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>) from two different field sites,Wamba and Kokolopori,Democratic Republic of the Congo

Maternal cannibalism, whereby a mother consumes her own offspring, occurs in various animal taxa and is commonly explained by nutritional stress or environmental pressures. It is rare in nonhuman primates and is considered an aberrant behavior only observed under high-stress conditions. It was therefore surprising when, in the first reported case of cannibalism in wild bonobos, a mother consumed part of the dead infant at LuiKotale. Here we report two more cases of maternal cannibalism by wild bonobos at two different study sites, Wamba and Kokolopori. The dead infants’ mothers participated in the cannibalism in both cases. At Kokolopori, although the mother did consume part of the carcass, it was held and shared by another dominant female. At Wamba, the mother was a dominant female within the community and was the primary consumer of the carcass. In both cases, cannibalism resembled other meat-eating events, with the dominant female controlling meat consumption. Infanticide was not observed in either case, but its occurrence could not be ruled out. Although rare, the occurrence of maternal cannibalism at three different study sites suggests that this may represent part of the behavioral repertoire of bonobos, rather than an aberrant behavior.     

Population Dynamics of Wild Bonobos (Pan paniscus) at Wamba

We analyzed population dynamics and birth seasonality of wild bonobos at Wamba, Democratic Republic of the Congo, based on 20 years of observations (1976–1996). Wamba Bonobo infant mortality is much lower than that reported for chimpanzees. This seemes to be related to several socioecological characteristics of bonobos: the use of abundant fruit and herbaceous foods, larger food patch size, female feeding priority, and the absence of infanticide. The mean interval between live births of 4.8 years is shorter than those reported for chimpanzees, and some females simultaneously carried and nursed two successive offspring. Mother–offspring conflicts, such as refusal of suckling attempts and interference with mothers' copulation, which are common in chimpanzees, are rare in Wamba bonobos. A birth peak seems to occur during the light rainy season from March to May, just after the season with the least rainfall. This timing of births is similar to those reported for chimpanzee populations, and might benefit both mother and offspring by maximizing the amount of time before the next dry season.     

Predation on giant flying squirrels (Petaurista philippensis) by black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China

Predation on vertebrates is infrequent in gibbons. In a 14-month field study of the central Yunnan black crested gibbon (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China, we observed gibbons attacking, killing and eating giant flying squirrels (Petaurista philippensis). During 845 h of observation on one study group, the gibbons attacked giant flying squirrels 11 times, and succeeded in 4 cases. Although all members of the group attempted to attack the squirrels, all four successful attacks were made by the same adult female. The victims were infants in three cases and a juvenile or sub-adult in one case. Black crested gibbons also attacked adult giant flying squirrels by grabbing their long tails and throwing them from the canopy, but they failed to catch or kill the prey in three cases observed. Passive meat sharing occurred in three out of four successful cases. Besides hunting giant flying squirrels, the black crested gibbons also ate eggs or chicks in two birds’ nests and one lizard.     

Animals and mushrooms consumed by bonobos ( Pan paniscus ): New records from lilungu (Ikela), Zaire

We list the animal species, mushrooms and honey, which are consumed by bonobos (Pan paniscus)in the Ikela region (Lilungu), Republic of Zaire, and compare these data with those obtained from other populations of bonobos: Lomako, Yalosidi, and Wamba. Lilungu bonobos consume earthworms more regularly than bonobos do at other localities. They also eat larvae, termites, and ants, but they probably do not consume invertebrates as regularly as chimpanzees do. Lilungu bonobos ate a squirrel and a chiropteran. We report our detailed observations of bonobo foraging, feeding and manipulating foods, including washing some items and complicated handling operations. We note intra- and intergroup differences in the consumption of specific foods and in the way they are handled by the females.     

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.     

Nonconceptive Sexual Behavior in Bonobos and Capuchins

Sexual behavior by infecundable females, and by same-sex and adult-immature dyads, occurs in wild and captive bonobos (Pan paniscus). Proposed functions of these behaviors, in social primates generally, include practice, paternity confusion, exchange, and communication as well as appeasement. We used this framework to interpret and to compare observations of sexual behavior in a captive bonobo group and a wild white-faced capuchin (Cebus capucinus) group. In both species, (a) sexual behavior was no more frequent in cycling females than in pregnant or lactating females and (b) same-sex and adult-immature dyads engaged in as much mounting or genitogenital contact as adult heterosexual dyads did. The species differed in that (a) bonobos engaged in sexual behavior 65 times as frequently as capuchins, (b) only bonobos engaged in sexual contact other than ventrodorsal mounting during focal observation, and (c) bonobo sexual contact was concentrated most heavily in socially tense situations in adult female–female dyads, whereas capuchin sexual contact was concentrated most heavily in socially tense situations in adult male–male dyads. These data and published literature indicate that (a) practice sex occurs in both species, (b) paternity confusion may be a current function of C. capucinus nonconceptive sex, (c) exchange sex remains undemonstrated in capuchins, and (d) communication sex is more important to members of the transferring sex—female bonobos and male capuchins—than to members of the philopatric sex.     

New records on prey capture and meat eating by bonobos at Lui Kotale, Salonga National Park, Democratic Republic of Congo

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.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

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.     

Comparing infant and juvenile behavior in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): a preliminary study

The dichotomy between the two Pan species, the bonobo (Pan paniscus) and chimpanzee (Pan troglodytes) has been strongly emphasized until very recently. Given that most studies were primarily based on adult individuals, we shifted the “continuity versus discontinuity” discussion to the infant and juvenile stage. Our aim was to test quantitatively, some conflicting statements made in literature considering species differences between immature bonobos and chimpanzees. On one hand it is suggested that infant bonobos show retardation in motor and social development when compared with chimpanzees. Additionally it is expected that the weaning process is more traumatic to chimpanzee than bonobo infants. But on the other hand the development of behaviors is expected to be very similar in both species. We observed eight mother–infant pairs of each species in several European zoos. Our preliminary research partially confirms that immature chimpanzees seem spatially more independent, spending more time at a larger distance from their mother than immature bonobos. However, the other data do not seem to support the hypothesis that bonobo infants show retardation of motor or social development. The development of solitary play, environmental exploration, social play, non-copulatory mounts and aggressive interactions do not differ between the species. Bonobo infants in general even groom other group members more than chimpanzee infants. We also found that older bonobo infants have more nipple contact than same aged chimpanzees and that the weaning process seems to end later for bonobos than for immature chimpanzee. Additionally, although immature bonobos show in general more signs of distress, our data suggest that the weaning period itself is more traumatic for chimpanzees.     

Observations of physical abnormalities among the wild bonobos (Pan paniscus) of Wamba,Zaire

The wild bonobos (Pan paniscus) of Wamba, Zaire have an extremely high frequency of external abnormal traits. Out of 96 animals in a sample comprising all age and sex classes from two different natural groups, 46 individuals had at least one limb defect. The frequency of abnormalities was greater in males than in females, and increased directly with age. Almost all infants and juveniles had completely normal limbs, but virtually all males and over half the females which had reached their prime were found to have one or more limb defects. These findings indicate that congenital factors contribute little to the frequency of abnormalities in this sample. Survival rate is the same in individuals with defects as in those without defects. It appears that individual social status is far more important in procuring foods than locomotor ability. Thus, the operation of such abnormalities as a selective factor in intraspecific competition is minimized in the network of their social relations.