Male Bonobos Research Articles

Disseminated T-cell lymphoma in a bonobo (Pan paniscus)

Disseminated lymphoma was diagnosed in an 8-year-old male bonobo (Pan paniscus). The male bonobo presented with a 4-6 week history of dyspnea and facial swelling around the eyes; thoracic radiographs and computed tomography scan indicated a craniodorsal mediastinal soft tissue mass. Upon gross examination, there was a large, cream to white mass expanding the mediastinum and pericardial sac. The mass extended along the thoracic aorta and cranial vena cava, through the thoracic inlet, along and encircling the trachea, and bilaterally into the thyroid glands. Microscopically, neoplastic lymphocytes were present in the thymus, trachea, lungs, kidney, heart, and numerous other tissues. Immunohistochemical staining of neoplastic lymphocytes revealed diffuse immunoreactivity for cluster of differentiation (CD)3 indicating T-cell lymphoma. Routine viral screening was negative via polymerase chain reaction.

Female contributions to the peaceful nature of bonobo society

Although chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) are closely related, females of the two species show surprisingly large differences in many behavioral aspects. While female chimpanzees tend to range alone or in small parties during non-estrous periods, female bonobos aggregate even more often than do males. Female chimpanzees do not have frequent social interactions with other females, whereas female bonobos maintain close social associations with one another. Although the ranging patterns of chimpanzee parties are generally led by males, female bonobos often take the initiative in ranging behavior. While female chimpanzees usually do not exhibit estrus during postpartum amenorrhea or pregnancy, female bonobos exhibit a prolonged pseudo-estrus during such non-conceptive periods. Studies of these two species have also shown great differences in agonistic behaviors performed by males. Male chimpanzees frequently fight with other males to compete for estrous females, but male bonobos seldom do so. While there are many records of infanticide by male chimpanzees, there is no confirmed record of such an event among bonobos. Several cases of within-group killing among adult male chimpanzees have been reported, but there is no such record for bonobos. While intergroup conflicts among chimpanzees sometimes involve killing members of the other group, intergroup conflicts among bonobos are considerably more moderate. In some cases, bonobos from two different groups may even range together for several days while engaging in various peaceful interactions. I will address two important questions that arise from these comparisons, exploring why females of such closely related species show such clear differences in behavior and whether or not the behavioral characteristics of female bonobos contribute to the peaceful nature of bonobo society.

Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus)

Variation in male mating success is often related to rank differences. Males who are unable to monopolize oestrous females alone may engage in coalitions, thus enhancing their mating success. While studies on chimpanzees and dolphins suggest that coalitions are independent of kinship, information from female philopatric species shows the importance of kin support, especially from mothers, on the reproductive success of females. Therefore, one might expect a similar effect on sons in male philopatric species. We evaluate mating success determinants in male bonobos using data from nine male individuals from a wild population. Results reveal a steep, linear male dominance hierarchy and a positive correlation between dominance status and mating success. In addition to rank, the presence of mothers enhances the mating success of sons and reduces the proportion of matings by the highest ranking male. Mothers and sons have high association rates and mothers provide agonistic aid to sons in conflicts with other males. As bonobos are male-philopatric and adult females occupy high dominance status, maternal support extends into adulthood and females have the leverage to intervene in male conflicts. The absence of female support to unrelated males suggests that mothers gain indirect fitness benefits by supporting their sons.

Bandicoots, Bonobos, and Boys: Papillomavirus and Vaccination Strategies

To better understand strategies for elimination of human papillomavirus (HPV), a brief history may provide insight. Papillomaviruses certainly are much older than humankind. They are relatively simple viruses containing a short double-stranded DNA genome, surrounded by a protein capsid. A single viral protein called L1 is all that is required for the formation of the icosahedral capsid. Papillomaviruses multiply mainly in squamous epithelia of the skin and genital surfaces. The viruses enter through small breaks in the epithelial surface. The virus then produces progeny virus that exit the host as the epithelial cell desquamates. Papillomaviruses are present in many mammals. One dramatic example is the bandicoot, one of many ancient marsupial species found only in Australia (Fig 1). Two closely related primordial papillomaviruses have been isolated from bandicoots.1 The viruses may have arisen 10 million years ago when Australia was physically separated from all other continents on planet earth. They are killing many bandicoots by causing skin infiltrates consisting of extensive epidermal hyperplasia leading to papillomas and carcinomas on the mouth, face, and flanks. Both male and female bandicoots are afflicted. Papillomaviruses also coevolved over 6 million years ago with higher primates such as the bonobo of central Africa, previously called the pygmy chimpanzee. The bonobo has become well known for social and sexual characteristics that more closely resemble humankind than its common chimpanzee cousin. Bonobos develop oral focal epithelial hyperplasia and papillomas caused by a virus strain that closely resembles HPV.2 Both male and female bonobos are afflicted. Lucy and her Australopithicus family members, who lived in eastern Africa 3 million years ago, certainly were infected with papillomaviruses and passed them on to their descendents. As a … Address correspondence to Charles Grose, MD, University of Iowa, Department of Pediatrics, 200 Hawkins Dr, Iowa City, IA 52242. E-mail: charles-grose{at}uiowa.edu

Sex Differences in the Steepness of Dominance Hierarchies in Captive Bonobo Groups

Bonobos have a reputation as a female-dominated and egalitarian species. We examined the 2 aspects of dominance in 6 captive bonobo groups. Females do not consistently evoke submission from all males in all contexts. Though females occupy the highest-ranking positions in the dominance hierarchy, there are in each group males that obtain rather high ranks and are able to dominate ≥1 female. Thus female dominance is not complete and hierarchies can be better described as nonexclusive female dominance. We studied egalitarianism by measuring linearity and steepness of dominance hierarchies. The hierarchies of all groups are highly linear. Hierarchies among males are steeper than among females. On average, male bonobos are more despotic than females, but females too can have despotic relations, both with other females and with males. Hence one can call bonobos in captivity semidespotic rather than egalitarian.

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.

Vertical jumping performance of bonobo (Pan paniscus) suggests superior muscle properties

Vertical jumping was used to assess muscle mechanical output in bonobos and comparisons were drawn to human jumping. Jump height, defined as the vertical displacement of the body centre of mass during the airborne phase, was determined for three bonobos of varying age and sex. All bonobos reached jump heights above 0.7 m, which greatly exceeds typical human maximal performance (0.3-0.4m). Jumps by one male bonobo (34 kg) and one human male (61.5 kg) were analysed using an inverse dynamics approach. Despite the difference in size, the mechanical output delivered by the bonobo and the human jumper during the push-off was similar: about 450 J, with a peak power output close to 3000 W. In the bonobo, most of the mechanical output was generated at the hips. To account for the mechanical output, the muscles actuating the bonobo's hips (directly and indirectly) must deliver muscle-mass-specific power and work output of 615 Wkg-1 and 92 Jkg-1, respectively. This was twice the output expected on the basis of muscle mass specific work and power in other jumping animals but seems physiologically possible. We suggest that the difference is due to a higher specific force (force per unit of cross-sectional area) in the bonobo.

Urinary testosterone levels of wild male bonobos (Pan paniscus) in the Lomako Forest, Democratic Republic of Congo

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.

Urinary Testosterone Metabolite Levels in Bonobos: A Comparison with Chimpanzees in Relation to Social System

[Bonobo ( Pan paniscus ) social structure is characterized by partial female dominance, in contrast to the male dominated chimpanzee ( Pan troglodytes ) society. Furthermore, female bonobos exhibit more overt aggressiveness and a prolonged period of proceptivity during menstrual cycle compared to chimpanzees. Since dominance, aggressiveness and proceptivity are suggested to relate to high T levels, we expected T concentrations of bonobo females to be high. To test this, urinary T metabolite concentrations (measured by immunoreactive 5αandrostane-17α-ol-3-one) were determined, which reliably reflect T status in both species. We predicted a larger overlap between T metabolite concentrations of both sexes in bonobos compared to chimpanzees. Our results support this hypothesis. However, interspecific comparison for each sex revealed substantially lower T metabolite concentrations in bonobo males than in chimpanzee males, while female bonobos displayed levels about equal to those of chimpanzee females. It thus appears that low T metabolite levels in bonobo males are responsible for the large overlap instead of high T metabolite levels in bonobo females. In conclusion, this study suggests that quantitative sex differences in T levels may be predictive of social system. However, partial female dominance in bonobos is probably not mediated by high female T levels. Rather it appears that T levels of mainly male bonobos are adapted to social organization. We hope that these preliminary results ignite further research in this novel area., Bonobo ( Pan paniscus ) social structure is characterized by partial female dominance, in contrast to the male dominated chimpanzee ( Pan troglodytes ) society. Furthermore, female bonobos exhibit more overt aggressiveness and a prolonged period of proceptivity during menstrual cycle compared to chimpanzees. Since dominance, aggressiveness and proceptivity are suggested to relate to high T levels, we expected T concentrations of bonobo females to be high. To test this, urinary T metabolite concentrations (measured by immunoreactive 5αandrostane-17α-ol-3-one) were determined, which reliably reflect T status in both species. We predicted a larger overlap between T metabolite concentrations of both sexes in bonobos compared to chimpanzees. Our results support this hypothesis. However, interspecific comparison for each sex revealed substantially lower T metabolite concentrations in bonobo males than in chimpanzee males, while female bonobos displayed levels about equal to those of chimpanzee females. It thus appears that low T metabolite levels in bonobo males are responsible for the large overlap instead of high T metabolite levels in bonobo females. In conclusion, this study suggests that quantitative sex differences in T levels may be predictive of social system. However, partial female dominance in bonobos is probably not mediated by high female T levels. Rather it appears that T levels of mainly male bonobos are adapted to social organization. We hope that these preliminary results ignite further research in this novel area.]

Vocal Production by a Language-Competent Pan paniscus

Human spoken language and nonhuman primate vocalization systems have traditionally been regarded as qualitatively different from one another with respect to their semanticity and the way in which individuals acquire and utilize these signals. However, recent studies of the vocal behaviors of both captive and free-ranging monkeys and apes suggest that this dichotomy may not be unequivocal. We examined the vocalizations produced by a linguistically-competent adult male bonobo (Pan paniscus) named Kanzi. We analyzed his vocalizations during communicative interactions with humans in order to determine whether they vary systematically according to the semantic context in which they are produced. We determined semantic contexts based upon a vocalization's co-occurrence with predefined behavioral correlates. Spectrographic and statistical analyses revealed that acoustic structure is similar among the vocalizations that occurred within a specific semantic context and structural differences are evident between the vocalizations produced in different contexts. The results provide evidence that, during communicative interactions with humans, Kanzi modulates his vocal output on both the temporal and spectral levels.

How a Subordinate Male Bonobo Leads Dominant Females up the Garden Path

How a Subordinate Male Bonobo Leads Dominant Females up the Garden Path

Association and social interactions between strangers and residents in bonobos (Pan paniscus)

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.

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”.

Reviewed Article: Leaf-dropping Sexual Display Exhibited by a Male Bonobo at Wamba

Reviewed Article: Leaf-dropping Sexual Display Exhibited by a Male Bonobo at Wamba

Evolution, psychopathology, and sexual offending: Aping our ancestors

Koko at first appears amused by Mbara's approach. The shameless silverback stares at her before exposing his erect penis, while his human scientist cousins make notes at a furious pace; it is not every day observers are privileged to witness such emotionally charged ape behavior. Perhaps their note-taking distracts Koko. She lumbers off into the brush and Mbara does not pursue. Across the continent, Nambuko, a male bonobo, is chased off by several dominant males when he tries to mount Antemba. After an appropriate period of sulking, Nambuko approaches and mounts Tafet, a juvenile bonobo, inexperienced in these matters. She shrieks and tries to fight him off, surprisingly successfully. The troop's ears are alerted and Tafet's mother, Okapa, and her sister Poke, rush in to protect their offspring. Nambuko sulks again.

Evolution, psychopathology, and sexual offending: Aping our ancestors

Koko at first appears amused by Mbara's approach. The shameless silverback stares at her before exposing his erect penis, while his human scientist cousins make notes at a furious pace; it is not every day observes are privileged to witness such emotionally charged ape behavior. Perhaps their note-taking distracts Koko. She lumbers off into the brush and Mbara does not pursue. Across the continent, Nambuko, a male bonobo, is chased off by several dominant males when he tries to mount Antemba. After an appropriate period of sulking, Nambuko approaches and mounts Tafet, a juvenile bonobo, inexperienced in these matters. She shrieks and tries to fight him off, surprisingly successfully. The troop's ears are alerted and Tafet's mother, Okapa, and her sister Poke, rush in to protect their offspring. Nambuko sulks again.

Evolution, Psychopathology, and Sexual Offending: Aping Our Ancestors

Koko at first appears amused by Mbara's approach. The shameless silverback stares at her before exposing his erect penis, while his human scientist cousins make notes at a furious pace; it is not every day observers are privileged to witness such emotionally charged ape behavior. Perhaps their note-taking distracts Koko. She lumbers off into the brush and Mbara does not pursue. Across the continent, Nambuko, a male bonobo, is chased off by several dominant males when he tries to mount Antemba. After an appropriate period of sulking, Nambuko approaches and mounts Tafet, a juvenile bonobo, inexperienced in these matters. She shrieks and tries to fight him off, surprisingly successfully. The troop's ears are alerted and Tafet's mother, Okapa, and her sister Poke, rush in to protect their offspring. Nambuko sulks again.

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.

Species and sex differences in the screams of chimpanzees and bonobos

We examined screams of chimpanzees and bonobos to investigate interspecific and intraspecific variability in call structure. Measurement of 11 acoustic features of screams revealed differences between and within species. One-way analyses of variance and discriminant function analyses show that the calls of chimpanzees and bonobos differ primarily in spectral characteristics. Spectral features also account for acoustic differences between the sexes. These acoustic variations may be attributable to differences in body size and social dispersion between the two species and sexes. The effectiveness with which an acoustic feature could be used to discriminate the two species and female bonobos from male bonobos is negatively associated with its relative variability. These data are consistent with the hypothesis that optimal signals for group identification vary little within groups but differ widely between groups.

Male Ranking Order and Copulation Frequency in the E1 Group of Bonobos, at Wamba, Zaire

1. Among the bonobos in the Wamba forest, central Zaire, male mating frequency was not strongly linked with his dominance rank. However, his mating rate (number of copulations per hour) was positively correlated with his rank.2. Three types of male dominance rank were taken into consideration, namely, rank within the group, party and patch. In bonobos at Wamba, males dramatically increased their temporary ranks (i. e., rank within a patch) by placing themselves opportunistically within the party space, and adult males in particular performed the majority of their copulations when they were the first ranking male within such a patch.3. One case was observed in which there was a “sneaky” sexual solicitation by a male which corresponds to the “leaf clipping” display of Mahale chimpanzees.4. It was concluded from 1, 2, and 3 that sexual competition among male bonobos at Wamba is more intense than has been thought, though other factors, especially the mother-son bond will influence males' mating success as well.