Tool use behavior in three wild bonobo communities at Kokolopori

Comparative studies on tool technologies in extant primates, especially in our closest living relatives, offer a window into the evolutionary foundations of tool use in hominins. Whereas chimpanzee tool technology is well studied across populations, the scarcity of described tool technology in wild populations of our other closest living relative, the bonobo, is a mystery. Here we provide a first report of the tool use repertoire of the Kokolopori bonobos and describe in detail the use of leaf-umbrellas during rainfall, with the aim to improve our knowledge of bonobo tool use capacity in the wild. The tool use repertoire of the Kokolopori bonobos was most similar to that of the nearby population of Wamba and comprised eight behaviors, none in a foraging context. Further, over a 6-month period we documented 44 instances of leaf-umbrella use by 22 individuals from three communities, suggesting that this behavior is habitual. Most leaf-umbrella tool users were adult females, and we observed a nonadult using a leaf-umbrella on only a single occasion. While the study and theory of tool technologies is often based on the use of tools in foraging tasks, tool use in bonobos typically occurs in nonforaging contexts across populations. Therefore, incorporating both foraging and nonforaging contexts into our theoretical framework is essential if we wish to advance our understanding of the evolutionary trajectories of tool technology in humans.     

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.     

Observations on the meat-eating behavior of wild bonobos (Pan paniscus) at Wamba,Republic of Zaire

Meat-eating behavior of wild bonobos (Pan paniscus) was witnessed on two occasions at Wamba, Republic of Zaire. Only flying squirrels were observed to be eaten by the bonobos. Several bonobos gathered around the possessor of the meat and showed interest in the meat on all occasions. Begging behavior was noted on one of the two occasions, but the possessor of the meat ignored it. No sharing of meat was seen on either occasion. The exclusive targets of hunting by bonobos are apparently small mammals, such as flying squirrels and infant duikers, since evidence of meat eating by wild bonobos, which have been studied for more than fifteen years, has been restricted to these mammals. The bonobos at Wamba may have a specialized “prey image”, as in the case of the chimpanzees (Pan troglodytes) of the Tai forest, and certain medium-sized or small mammals may not conform to this image.     

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.     

Coprophagy in wild bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>) at Wamba in the Democratic Republic of the Congo: a possibly adaptive strategy?

Four cases of coprophagy and two cases of fecal inspection were identified during the 1142 h of observing wild bonobos at Wamba in the Luo Scientific Reserve in the Democratic Republic of the Congo. At least 5 females in the study group practiced coprophagy and/or fecal inspection. According to our daily behavioral observations, boredom and stress, insufficient roughage, and the search for essential nutrients could not explain the coprophagy. Several episodes observed in this study indicated that bonobos might have sought and ingested certain valuable food items, such as hard Dialium seeds, in feces during relatively lean seasons. Although coprophagy occurred only rarely among wild bonobos, this practice appeared to represent a possibly adaptive feeding strategy during periods of food scarcity rather than a behavioral abnormality.     

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”.     

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.     

Female feeding priority in bonobos, Pan paniscus, and the question of female dominance

The question of whether bonobos show feeding priority and female dominance has been proposed and examined, both in the wild and in captive studies, with differing results. The relationship between female dominance and female feeding priority has been best studied in prosimian primates. These studies use established criteria of females consistently evoking submissive behavior from males in dyadic encounters for determining female dominance. Although the relationship is complex, female dominance in prosimians is associated with preferential access to food. Data from studies of wild habituated bonobos in the Lomako Forest, Democratic Republic of the Congo, are examined for evidence of both female feeding priority and female social dominance using similar criteria as used for prosimians. Bonobos showed evidence of female feeding priority in small, but not in large, food patches. Male-male competition for mating opportunities at the start of the food bout was related to some, but not all, differences in time spent feeding between the sexes. Female dominance similar to that seen in prosimians was not observed in these bonobos. Males were consistently dominant in dyadic interactions. Female feeding priority with male dyadic social dominance implies that male deference during feeding cannot be excluded as one explanation of interpretations of female dominance in bonobos. Additionally, dominance of male bonobos by females appears to require the presence of female coalition partners. As in other primates with female feeding priority, bonobo females express this trait where food is economically defendable. Unlike prosimians, however, bonobo female feeding priority may result from male deference and the importance of female coalitions in nondyadic interactions.     

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.     

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.     

Reproductive failure,possible maternal infanticide,and cannibalism in wild moustached tamarins, <Emphasis Type="Italic">Saguinus mystax</Emphasis>

Maternal infanticide in wild non-human primates has only been reported twice. In this paper, we report a possible new case of infanticide and cannibalism within a series of four successive reproductive failures in wild moustached tamarins, Saguinus mystax. Necropsy and genetic analyses of the corpses enabled us to rule out any pathology, and to determine paternity. The mother was seen biting and then eating the head of its own infant during a period when another female was pregnant and gave birth just 1 month later. Before that, the perpetrator had given birth to twins three times successfully when four to five adult and subadult males were present in the group. Although we do not know for certain that the infant was alive when the mother started biting it, our field observations preceding the event suggest it probably was. The possible infanticide case and the two cases of births and early death of the infants occurred while only two to three adult males were present in the group. This could be the second case of maternal infanticide reported in the genus Saguinus and the similar circumstances suggest a common pattern. We discuss these events in the light of the different functional explanations of infanticide and conclude that parental manipulation was the most likely: the mother could have terminated the investment in offspring that had low chances of survival in a group with low availability of helpers.     

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.     

Maternal manipulation of hatching asynchrony limits sibling cannibalism in the predatory mite Phytoseiulus persimilis

1. Sibling cannibalism is a common phenomenon in the animal kingdom but entails a high risk of direct and inclusive fitness loss for the mother and her offspring. Therefore, mechanisms limiting sibling cannibalism are expected to be selected for. One way of maternal manipulation of sibling cannibalism is to influence hatching asynchrony between nearby laid eggs. This has rarely been tested experimentally. 2. We examined the ability of ovipositing females of the cannibalistic predatory mite Phytoseiulus persimilis to influence the occurrence of sibling cannibalism among offspring by manipulating hatching asynchrony of nearby laid eggs. 3. In the first experiment, we assessed the occurrence of sibling cannibalism in relation to the hatching interval (24 h and 48 h) between nearby laid eggs. In the second experiment, we tested whether ovipositing females discriminate sites containing young (24-h old) and old (48-h old) eggs, fresh and old traces (metabolic waste products and possibly pheromones) left by the same female (24 h and 48 h ago), or young eggs plus fresh female traces and old eggs plus old female traces. Both experiments were conducted with and without prey. 4. Without prey, siblings were more likely to cannibalize each other if the hatching interval between nearby laid eggs was short (24 h). Cannibalism occurred less often when senior siblings (protonymphs) experienced a delay in the opportunity to cannibalize junior siblings (larvae). 5. Independent of prey availability, females preferentially added new eggs to sites containing old eggs plus old female traces but did neither distinguish between young and old eggs presented without own traces nor between fresh and old traces presented without eggs. 6. We discuss cue perception and use by P. persimilis females and contrast the outcome of our experiments and theoretical predictions of sibling cannibalism. We conclude that P. persimilis mothers increase hatching asynchrony of nearby laid eggs to prevent sibling cannibalism on the last produced offspring. Such a behaviour may be considered a simple form of maternal care increasing the survival prospects of offspring.     

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.     

Infant cannibalism in wild white‐faced capuchin monkeys

Cannibalism has been observed in a variety of animal taxa; however, it is relatively uncommon in primates. Thus, we rely heavily on case reports of this behavior to advance our understanding of the contexts under which it occurs. Here, we report the first observation of cannibalism in a group of wild white‐faced capuchin monkeys (Cebus imitator). The subject was a dead infant, estimated to be 10 days old, and the probable victim of infanticide. Consumption of the corpse was initiated by a 2‐year‐old male (second cousin of the infant), though it was eventually taken over and monopolized by the group''s alpha female (grandaunt of the infant). Although most group members expressed interest in the corpse (sniffing, touching, and threatening it), no others made an attempt to consume it. Given that this is the only observation of cannibalism recorded in over 37 years of study on this population, we consider it to be a rare behavior in this species. This detailed record contributes new data, which, when combined with other reports within and across species and contexts, enables the evaluation of adaptive explanations of cannibalism.     

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.     

Within-group cannibalism by adult male chimpanzees

In the Mahale Mountains National Park, Tanzania, a young adult male chimpanzee was observed to feed on a 3-month-old male infant of the same unit-group. Four other adult males and an adult female shared the carcass. The mother of the victim had immigrated from a neighboring unit-group four years previously. Circumstantial evidence strongly suggests that the first-observed cannibal male also killed the infant. The adult male and the mother of the victim had been familiar socially and sexually with each other since the female immigrated. Since the mother of the victim had usually been ranging in the peripheral part of the unit-group's range, i.e., the overlapping area of the two unit-group's ranges during pregnancy and soon after birth, the infanticidal male might have had reason to suspect the paternity of her infant. Four such cases of within-group cannibalism by adult males suggest that the female range and association pattern before and after parturition are key factors allowing an infant to survive. The possibility of male-biased infanticide is also discussed.     

Sex differences in copulation attempts in wild bonobos at Wamba

We examined sex differences in copulation attempts in a group of wild bonobos at Wamba, Congo, by analyzing the behavioral sequence. Most copulation attempts were initiated by approach or courtship behaviors by males. Males showed these behaviors when they were more than 5 m from females, whereas females did so only when males solicited them from within 5 m. Most copulations involved females showing perineal swelling, because males solicited those females more frequently and those females accepted copulation more frequently than did females in the non-swelling phase. Nevertheless, males solicited females in the non-swelling phase in one-third of copulation attempts, and those females accepted copulation in half of those attempts. This is markedly different from chimpanzees, in which sexual behaviors almost exclusively involve females in the swelling phase. The perineum of female bonobos during the non-swelling phase is soft and wrinkled but fairly large, which may attract males to some extent. The low, but existing, attractiveness and receptivity of female bonobos during the non-swelling phase might have evolved to control sexual competition among males and provide higher social status for females.