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Preliminary vocal repertoire and vocal communication of wild bonobos (Pan paniscus) at Lilungu (Democratic Republic of Congo).

Vocal communication in bonobos, Pan paniscus, has been studied mainly in captive groups. The few studies carried out in the wild are on only specific aspects of their behaviour. The aim of this study is to give a preliminary description of the vocal repertoire and a qualitative account of the contextual use of the vocalizations described. Observations were carried out on three wild communities, with a total of 68 individuals, for 685 h. No artificial feeding was used at any stage of the study. The vocal repertoire is composed of 15 vocal units and 19 sequences. There is great variability both in the sequences and in the vocal units, and the categories are not always completely discrete. The repertoire is compared to that of captive bonobos described by De Waal. Most sequences are used in various contexts, and for each behaviour there is a complete array of sequences and their variation. The behaviour patterns observed and the sequences uttered by the animals in each context are discussed.

Animals↗

What do bonobos (Pan paniscus) understand about physical contact?

The present study aimed to test what bonobos (Pan paniscus) understand about contact. The task consisted of a clear horizontal tube containing a piece of food and a stick with a disk attached. The bonobos chose which side to push or pull the stick for the disk to contact the food and make it accessible. There were 9 variations in tube design, which differed in the positions of the stick, disk, and food. All 5 bonobos passed at least 1 configuration. A recent study (A. E. Helme, N. S. Clayton, & N. J. Emery, 2006) found that rooks could learn only tube configurations that provided an asymmetrical stick cue, whereas bonobos did not demonstrate an understanding of contact but showed more individual variation, attending to the positions of the food, disk, and stick.

Animals↗

Social structures in Pan paniscus: testing the female bonding hypothesis.

Based on previous research in captivity, bonobos, Pan paniscus, have been called a female-bonded species. However, genetic and behavioural data indicate that wild females migrate. Bonding between these unrelated females would then be in contradiction with socio-ecological models. It has been argued that female bonding has been overemphasized in captive bonobos. We examine patterns of proximity, grooming and support behaviour in six well established captive groups of bonobos. We find that female bonding was not a typical characteristic of all captive bonobo groups. In only two groups there was a trend for females to prefer proximity with other females over association with males. We found no evidence that following or grooming between females was more frequent than between males and unrelated females or between males. Only in coalitions, females supported each other more than male-female or male-male dyads. We also investigated five mother-son pairs. Grooming was more frequent among mothers and sons than in any other dyad, but sons did not groom their mothers more than males groomed unrelated females. Mothers groomed their sons, or provided more support to them than females groomed or supported unrelated males. Thus, while bonds between females were clearly present, intersexual relations between males and either unrelated females or their mothers are of more, or equal importance.

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The chimpanzee-specific pericentric inversions that distinguish humans and chimpanzees have identical breakpoints in Pan troglodytes and Pan paniscus.

Seven of nine pericentric inversions that distinguish human (HSA) and chimpanzee karyotypes are chimpanzee-specific. In this study we investigated whether the two extant chimpanzee species, Pan troglodytes (common chimpanzee) and Pan paniscus (bonobo), share exactly the same pericentric inversions. The methods applied were FISH with breakpoint-spanning BAC/PAC clones and PCR analyses of the breakpoint junction sequences. Our findings for the homologues to HSA 4, 5, 9, 12, 16, and 17 confirm for the first time at the sequence level that these pericentric inversions have identical breakpoints in the common chimpanzee and the bonobo. Therefore, these inversions predate the separation of the two chimpanzee species 0.86-2 Mya. Further, the inversions distinguishing human and chimpanzee karyotypes may be regarded as early acquisitions, such that they are likely to have been present at the time of human/chimpanzee divergence. According to the chromosomal speciation theory the inversions themselves could have promoted human speciation.

Animals↗

Chromosomal analysis of the pygmy chimpanzee (Pan paniscus) with a comparison to man.

The karyotype of Pan paniscus is reexamined by G-banding and examined for the first time by C-banding. In addition, examination of the chromosomes by the use of the fluorochromes adreamycine and 33258 Hoechst is undertaken. C-banding showed a surprising pattern with numerous terminal C-bands, as interstitial C-band, and several chromosomes lacking C-bands. Polymorphic conditions for C-bands are also identified involving several pairs. In a comparison to the chromosomes of man, G-banding revealed two pericentric inversions not previously observed. Only chromosome pairs No. 9,11,12 and the X are similar to man's by all techniques employed.

Animals↗

Fatal inflammatory heart disease in a bonobo (Pan paniscus).

We report the first probable identification of encephalomyocarditis virus (EMCV) in a bonobo (Pan paniscus) that had been part of a forest re-introduction programme. Clinical presentation was of episodic acute on chronic heart failure and cerebral infarction with end-stage renal failure rather than sudden death which is more commonly associated with EMCV infection. A postmortem diagnosis of probable EMCV was made using gross pathological and histopathological examination. Findings included acute on chronic heart failure combined with the unusual but characteristic histopathological features of non-suppurative necrotizing myocarditis with mononuclear, inflammatory infiltration of the brain.

Animals↗

The other "closest living relative". How bonobos (Pan paniscus) challenge traditional assumptions about females, dominance, intra- and intersexual interactions, and hominid evolution.

Chimpanzee (Pan troglodytes) societies are typically characterized as physically aggressive, male-bonded and male-dominated. Their close relatives, the bonobos (Pan paniscus), differ in startling and significant ways. For instance, female bonobos bond with one another, form coalitions, and dominate males. A pattern of reluctance to consider, let alone acknowledge, female dominance in bonobos exists, however. Because both species are equally "man's" closest relative, the bonobo social system complicates models of human evolution that have historically been based upon referents that are male and chimpanzee-like. The bonobo evidence suggests that models of human evolution must be reformulated such that they also accommodate: real and meaningful female bonds; the possibility of systematic female dominance over males; female mating strategies which encompass extra-group paternities; hunting and meat distribution by females; the importance of the sharing of plant foods; affinitive inter-community interactions; males that do not stalk and attack and are not territorial; and flexible social relationships in which philopatry does not necessarily predict bonding pattern.

Animals↗

Perineal swelling, intermenstrual cycle, and female sexual behavior in bonobos (Pan paniscus).

Many reports have claimed that the duration of the swelling cycle in female bonobos (Pan paniscus) is longer than that of chimpanzees, and that the bonobo maximum swelling phase is markedly prolonged. Field data on intermenstrual intervals (IMIs) in female bonobos are limited and restricted to interswelling intervals (ISIs), which are assumed to reflect the IMI, though a direct comparison between the duration of ISIs and IMIs is still lacking. Reports on bonobo sexual activity as a function of the swelling phase are often contradictory. Moreover, the function of female homosexual interactions (genito-genital (GG) rubbing) is still debated. This study examines the reliability of the ISI as an approximation of the IMI, and the attractivity of female sexual swellings for other individuals. An analysis of 51 ISI-IMI pairs showed that ISIs are a fair representation of the reproductive cycle. The cycle length was 35.6+/-1.1 SE days relying on the ISI, whereas it was 35.0+/-1.1 SE days considering the IMI. This result is similar to the cycle length reported for chimpanzees. Female homosexual interactions and copulatory rates were higher during maximum tumescence, suggesting that the sexual swelling may be attractive for both males and other females. Furthermore, the GG-rubbing was performed free of a hierarchical postural imposition, and was not correlated with affinitive interactions. We suggest that GG-rubbing, which is generally the most frequent female sexual interaction, is a tool for social assessments among females.

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Bipedality in chimpanzee (Pan troglodytes) and bonobo (Pan paniscus): testing hypotheses on the evolution of bipedalism.

A host of ecological, anatomical, and physiological selective pressures are hypothesized to have played a role in the evolution of hominid bipedalism. A referential model, based on the chimpanzee (Pan troglodytes) and bonobo (Pan paniscus), was used to test through experimental manipulation four hypotheses on the evolution of hominid bipedalism. The introduction of food piles (Carry hypothesis) increased locomotor bipedality in both species. Neither the introduction of branches (Display hypothesis) nor the construction of visual barriers (Vigilance hypothesis) altered bipedality in either species. Introduction of raised foraging structures (Forage hypothesis) increased postural bipedality in chimpanzees. These experimental manipulations provided support for carrying of portable objects and foraging on elevated food-items as plausible mechanisms that shaped bipedalism in hominids.

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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.

Age Factors↗

Gestural communication in subadult bonobos (Pan paniscus): repertoire and use.

This article aims to provide an inventory of the communicative gestures used by bonobos (Pan paniscus), based on observations of subadult bonobos and descriptions of gestural signals and similar behaviors in wild and captive bonobo groups. In addition, we focus on the underlying processes of social cognition, including learning mechanisms and flexibility of gesture use (such as adjustment to the attentional state of the recipient). The subjects were seven bonobos, aged 1-8 years, living in two different groups in captivity. Twenty distinct gestures (one auditory, eight tactile, and 11 visual) were recorded. We found individual differences and similar degrees of concordance of the gestural repertoires between and within groups, which provide evidence that ontogenetic ritualization is the main learning process involved. There is suggestive evidence, however, that some form of social learning may be responsible for the acquisition of special gestures. Overall, the present study establishes that the gestural repertoire of bonobos can be characterized as flexible and adapted to various communicative circumstances, including the attentional state of the recipient. Differences from and similarities to the other African ape species are discussed.

Adaptation, Psychological↗

How the great apes (Pan troglodytes, Pongo pygmaeus, Pan paniscus, and Gorilla gorilla) perform on the reversed contingency task: the effects of food quantity and food visibility.

S. T. Boysen and G. G. Berntson (1995) found that chimpanzees performed poorly on a reversed contingency task in which they had to point to the smaller of 2 food quantities to acquire the larger quantity. The authors compared the performance of 4 great ape species (Pan troglodytes, Pongo pygmaeus, Pan paniscus, and Gorilla gorilla) on the reversed contingency task while manipulating food quantity (0-4 or 1-4) and food visibility (visible pairs or covered pairs). Results showed no systematic species differences but large individual differences. Some individuals of each species were able to solve the reversed contingency task. Both quantity and visibility of the food items had a significant effect on performance. Subjects performed better when the disparity between quantities was smaller and the quantities were not directly visible.

Age Factors↗

Tracking the displacement of objects: a series of tasks with great apes (Pan troglodytes, Pan paniscus, Gorilla gorilla, and Pongo pygmaeus) and young children (Homo sapiens).

The authors administered a series of object displacement tasks to 24 great apes and 24 30-month-old children (Homo sapiens). Objects were placed under 1 or 2 of 3 cups by visible or invisible displacements. The series included 6 tasks: delayed response, inhibition test, A not B, rotations, transpositions, and object permanence. Apes and children solved most tasks performing at comparable levels except in the transposition task, in which apes performed better than children. Ape species performed at comparable levels in all tasks except in single transpositions, in which chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) performed better than gorillas (Gorilla gorilla) and orangutans (Pongo pygmeaus). All species found nonadjacent trials and rotations especially difficult. The number of elements that changed locations, the type of displacement, and having to inhibit predominant reaching responses were factors that negatively affected the subjects' performance.

Animals↗

The simian T-lymphotropic/leukemia virus from Pan paniscus belongs to the type 2 family and infects Asian macaques.

The proviral DNA of the simian T-leukemia/lymphotropic virus (STLV) isolate, originally obtained from a captive colony of pygmy chimpanzees (Pan paniscus) (STLV(pan-p)), was cloned from the DNA of the chronically infected human T-cell line L93-79B. The entire proviral DNA sequence was obtained and compared with sequences of the known genotypes of STLV and human T-leukemia/lymphotropic virus types 1 and 2 (HTLV-1 and -2). Phylogenetic analysis indicates that STLV-2(pan-p) is an early divergence within the type 2 lineage and should be referred to as STLV-2(pan-p). Since STLV-2(pan-p) has been found in African nonhuman primates, we investigated its infectiousness and pathogenicity in Asian monkeys. Pigtailed macaques were inoculated with human cells harboring STLV(pan-p), and infection was assessed by virus isolation, PCR analysis of peripheral blood mononuclear cells, and seroconversion against viral antigens in HTLV-1/HTLV-2 and Western blot assay. Pigtailed macaques became persistently infected by STLV-2(pan-p), and the virus could be transferred by blood transfusion from an infected pigtailed macaque to a rhesus macaque. In addition, like HTLV-1 and HTLV-2, STLV-2(pan-p) was infectious in rabbits. In summary, STLV-2(pan-p) is a novel retrovirus distantly related to HTLV-2 and displays a host range similar to that demonstrated for other HTLV and STLV strains.

Amino Acid Sequence↗

Behavioral laterality in captive bonobos (Pan paniscus).

Behavioral laterality was studied in a captive group of 11 bonobos (Pan paniscus). In an observational method a significant left lateral bias in carrying and a right lateral bias in leading limb were found. Direction of lateral bias in carrying and leading limb was enhanced when subjects maintained a bipedal posture. Analysis of bimanual feeding behavior revealed a significant right-hand bias for eating when subjects were holding food with their left hand. In an experimental method a significant shift toward greater right-hand use was found when subjects were required to maintain a bipedal, rather than a quadrupedal, posture. There was no evidence of lateral bias for measures of face touching, self-touching, or gestures. The results are discussed in the context of previous reports of primate laterality.

Animals↗

[Capillaria brochieri n. sp. (Nematoda: Capillariinae) intestinal parasite of the chimpanzee (Pan paniscus) in Zaire].

Capillaria brochieri n. sp. is described in a chimpanzee (Pan paniscus Schwartz, 1929) deceased from diarrhea. The male shows a unique structure of the caudal extremity: two flat paddles, with distal insertion, extend forward on each side of the ventral genital opening. The spicule (1,750 microns in length) shows a flattened anterior extremity and a tapered, curved posterior extremity. The cirrus is non-spiny and very long. Two narrow and very long lateral alae are present. The female bears a vulvar appendage. The egg shell shows an internal dense layer and an external layer of irregular width, showing pores and striations. The paper includes a study of the literature on Capillaria and Anatrichosoma from Primates and Man. C. brochieri is the first species of Capillaria described from the intestine of the chimpanzee. Because of the close analogies between chimpanzee's and man's helminthes, it is possible that C. brochieri has to be considered in human pathology.

Animals↗

Trisomy 17 in a bonobo (Pan paniscus) and deletion of 3q in a lowland gorilla (Gorilla gorilla gorilla): comparison with human trisomy 18 and human deletion 4q syndrome.

A female bonobo (Pan paniscus) born at the San Diego Zoo exhibited inability to nurse and progressive weakness plus multiple congenital abnormalities including aural canal atresia and stenosis, malformed auricles, clenched hands, lordosis, agenesis of the caudal vertebra and cardiac abnormalities. Chromosome analysis identified the bonobo as being trisomic for chromosome 17, the homolog of human chromosome 18. Genotyping with human microsatellites suggested the extra chromosome was maternal in origin. In addition, a male lowland gorilla (Gorilla gorilla gorilla), also born at the zoo, exhibited postnatal growth retardation, facial dysmorphisms and small hands with short fingers. Karyotype analysis revealed the gorilla carried a deletion of the distal q arm of chromosome 3, the homolog of human chromosome 4. The phenotypic and karyotypic abnormalities found in the bonobo and gorilla were consistent with the characteristics of human trisomy 18 and human deletion 4q syndrome, respectively.

Animals↗

Spatio-temporal gait characteristics of the hind-limb cycles during voluntary bipedal and quadrupedal walking in bonobos (Pan paniscus).

Spatio-temporal gait characteristics (step and stride length, stride frequency, duty factor) were determined for the hind-limb cycles of nine bonobos (Pan paniscus) walking quadrupedally and bipedally at a range of speeds. The data were recalculated to dimensionless quantities according to the principle of dynamic similarity. Lower leg length was used as the reference length. Interindividual variability in speed modulation strategy of bonobos appears to be low. Compared to quadrupedal walking, bipedal bonobos use smaller steps to attain a given speed (differences increase with speed), resulting in shorter strides at a higher frequency. In the context of the ("hybrid") dynamic pattern approach to locomotion (Latach, 1998) we argue that, despite these absolute differences, intended walking speed is the basic control variable which elicits both quadrupedal and bipedal walking kinematics in a similar way. Differences in the initial status of the dynamic system may be responsible for the differences in step length between both gaits. Comparison with data deduced from the literature shows that the effects of walking speed on stride length and frequency are similar in bonobos, common chimpanzees, and humans. This suggests that (at least) within extant homininae, spatio-temporal gait characteristics are highly comparable, and this in spite of obvious differences in mass distribution and bipedal posture.

Animals↗