Mandibular Shape, Ontogeny and Dental Development in Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)

The postnatal ontogenetic patterns and processes that underlie species differences in African ape adult mandibular morphology are not well understood and there is ongoing debate about whether African ape faces and mandibles develop via divergent or parallel trajectories of shape change. Using three-dimensional (3D) morphometric data, we first tested when in postnatal development differences in mandibular shape are initially evident between sister species Pan troglodytes and P. paniscus. Next, we tested whether each species has a distinct and non-parallel trajectory of mandibular development. Mandibles sampled across a broad developmental range of wildshot bonobos (n = 44) and chimpanzees (n = 59) were radiographed and aged from their dental development. We then collected 3D landmark surface data from all the mandibles. A geometric morphometric analysis of size-corrected 3D data found that bonobos and chimpanzees had parallel and linear ontogenetic trajectories of mandibular shape change. In contrast, mandibular shape was statistically different between P. paniscus and P. troglodytes as early as infancy, suggesting that species shape differences are already established near or before birth. A linear and stable trajectory of shape change suggests that mandibular ontogeny in these apes is unimpacted by non-linear variation in tooth developmental timing.     

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.     

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

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

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.     

Ecological and Behavioral Aspects of Nest Building in Wild Bonobos (Pan paniscus)

Data on nest building behavior were collected from free ranging bonobos (Pan paniscus). Considering the physical features of both nests and trees used for nest construction, bonobos appeared to show various preferences: (1) Trees with small leaves were chosen more frequently than expected; (2) The majority of nests were constructed in trees of the middle forest layer (15 to 30 m) and at a mean height of 16 m; (3) nests built during the day were located higher than night nests and differed in the general mode of construction (number of trees involved). Comparing nests made by mature males and females it became apparent that females (4) built nests higher, (5) constructed day nests more frequently and (6) used them for a longer time than males. Comparison of data collected at different study sites indicates site-specific differences concerning selection of trees and location of nesting sites. Behavioral observations made clear that nests were not only used for rest but also for other activities like feeding, social grooming and play. Moreover, the study provided the first evidence that bonobos build nests also in order to avoid potential or imminent conflicts with other party members. Field observations indicate that these nests symbolize a taboo zone and show another facet of the social abilities of bonobos for the solution of intra group conflicts. It is suggested that this behavior derives from the spatial intolerance shown by females during the process of weaning.     

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.     

Nest Grouping Patterns of Bonobos (Pan paniscus) in Relation to Fruit Availability in a Forest-Savannah Mosaic

A topic of major interest in socio-ecology is the comparison of chimpanzees and bonobos'' grouping patterns. Numerous studies have highlighted the impact of social and environmental factors on the different evolution in group cohesion seen in these sister species. We are still lacking, however, key information about bonobo social traits across their habitat range, in order to make accurate inter-species comparisons. In this study we investigated bonobo social cohesiveness at nesting sites depending on fruit availability in the forest-savannah mosaic of western Democratic Republic of Congo (DRC), a bonobo habitat which has received little attention from researchers and is characterized by high food resource variation within years. We collected data on two bonobo communities. Nest counts at nesting sites were used as a proxy for night grouping patterns and were analysed with regard to fruit availability. We also modelled bonobo population density at the site in order to investigate yearly variation. We found that one community density varied across the three years of surveys, suggesting that this bonobo community has significant variability in use of its home range. This finding highlights the importance of forest connectivity, a likely prerequisite for the ability of bonobos to adapt their ranging patterns to fruit availability changes. We found no influence of overall fruit availability on bonobo cohesiveness. Only fruit availability at the nesting sites showed a positive influence, indicating that bonobos favour food ‘hot spots’ as sleeping sites. Our findings have confirmed the results obtained from previous studies carried out in the dense tropical forests of DRC. Nevertheless, in order to clarify the impact of environmental variability on bonobo social cohesiveness, we will need to make direct observations of the apes in the forest-savannah mosaic as well as make comparisons across the entirety of the bonobos'' range using systematic methodology.     

Structure and use of distance calls in wild bonobos (Pan paniscus)

We report the physical structure and use of a distance call (high-hoot) by wild bonobos (Pan paniscus).Although spectrographic analyses reveal high structural variability, the total sample can be subdivided according to the composition of units—the presence or absence of an initial segment—and the range of the lowest harmonic. Analyses of samples from male—female pairs,vocalizing simultaneously and in close proximity, reveal that both animals utter calls in more or less precise temporal alternation but with different spectral ranges. Whether these differences are gender-specific or related to other factors, such as age or the social relations between particular individuals, is not clear. We suggest that (a) individuals of the same party may coordinate their vocal activity on both the temporal and the spectral level and (b) high hootings stimulate emission of equal vocalizations by members of other parties and may increase cohesion among community members. Comparison of a restricted number of spectrograms from known individuals indicates that bonobos may be able to adjust spectral parameters of one type of distance calls (high- hoot) according to corresponding calls of conspecifics.     

Male dominance rank, mating and reproductive success in captive bonobos (Pan paniscus)

In the recent past, application of DNA genotyping techniques has enabled researchers to more accurately test relationships between dominance rank (DR), mating success (MS) and reproductive success (RS). Paternity studies often reveal that reproductive outcome does not always correlate with male DR and/or MS and thus open room for discussion and interpretation of alternative reproductive tactics of both sexes. In this study, we analysed male DR, MS and RS in a group of bonobos at Twycross Zoo (UK). Genetic relationships were determined using 8 tetrameric microsatellite loci. Despite clear and asymmetric dominance relationships, analysed using normalised David's scores based on a dyadic index of dominance among the group's 3 mature males, we found that the most dominant male did not sire the most offspring. In fact, both infants conceived during the observation period were found to be sired by the lower-ranking males. Although the alpha male had almost exclusive mating access to one of the females during the time she was showing a maximal anogenital swelling, her infant was sired by the lowest-ranking male who mostly mated with her when outside the maximal swelling period. This result suggests that either sperm competition operates and/or ovulation is decoupled from the phase of maximal anogenital swelling which could allow greater female choice.     

Social relationships between immigrant and resident bonobo (Pan paniscus) females at Wamba.

Social relations and behaviours of adolescent female pygmy chimpanzees (Pan paniscus) that migrated between unit groups were studied at Wamba, Za?re. Each immigrant female selected one particular resident female, a 'specific senior female' (SSF) and frequently approached and followed her. Affinitive behaviours (e.g. grooming, genitogenital rubbing) were frequently performed between the immigrant and her SSF. Most affinitive behaviours were more likely to be initiated by the immigrant than by her SSF. The immigrant's relationship with her SSF seemed to facilitate the immigrant's integration into the new unit group. Resident males actively approached and mated with the immigrant females. Copulation also appeared to further the immigrant's stable relationship with the resident males.     

Applying Landscape Metrics to Characterize Potential Habitat of Bonobos (Pan paniscus) in the Maringa-Lopori-Wamba Landscape, Democratic Republic of Congo

To conserve areas and species threatened by immediate landscape change requires that we make planning decisions for large areas in the absence of adequate data. Here we study the utility of broad-scale landscape metrics as predictors of species occurrence, especially for remote areas where there is a need to make the most of limited spatial and biological data. Bonobos (Pan paniscus) are endangered great apes endemic to lowland forests of the Democratic Republic of Congo. They are threatened by bushmeat hunting that is exacerbated by habitat fragmentation through slash-and-burn agriculture and timber harvest. We developed four landscape metrics —edge density (ED), COHESION, CONTAGION, and class area (CA)— that may serve as surrogates for measuring accessibility of areas to hunting in order to predict relative bonobo-habitat suitability. We calculated the metrics for the Maringa-Lopori-Wamba (MLW) landscape and evaluated them for utility in predicting bonobo-nest occupancy based on 2009 field data. Cross-validations showed that all four metrics performed similarly. However, forest ED was arguably the best predictor, with an overall classification accuracy of 72.1% in which 85% of known nest blocks (N = 124) were classified correctly. We demonstrated that for a relatively intact landscape and a mobile forest-dwelling species that is fairly tolerant of forest openings, forest fragmentation can still be an important predictor of species occurrence. We suggest that ED can be helpful when mapping bonobo habitat in MLW and can aid landscape-planning and conservation efforts. Our approach may be applied to other edge-sensitive species, especially where high-resolution data are deficient.     

Mothers stick together: how the death of an infant affects female social relationships in a group of wild bonobos (Pan paniscus)

Primates - Sociality is widespread among group-living primates and is beneficial in many ways. Sociality amongst female bonobos (Pan paniscus) has been proposed to have evolved as a female...     

Low Resistance of Senior Resident Females Toward Female Immigration in Bonobos (Pan paniscus) at Wamba,Democratic Republic of the Congo

International Journal of Primatology - Female aggression against outgroup conspecifics is an important aspect of intergroup relationships among female primates. Intense aggression from resident...     

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.     

Inbreeding pattern and reproductive success in a rural community from Galicia (Spain)

The present paper is based on information on marital patterns and reproductive performance (reconstituted families) in the rural community of Los Nogales, Galicia, Spain. Biodemographic data were used to analyse temporal changes and structure of consanguinity in the population, as well as consanguinity versus reproductive success. Of 2347 marriages celebrated between 1871 and 1977, 5.15% were between relatives (up to third degree). The population's inbreeding coefficient was above the Spanish average after 1890, and levels were high during the first part of the 20th century. A possible underestimation of inbreeding coefficients is attributed to the elevated frequency of extramarital births occurring in the Los Nogales population (13.47%). The structures of consanguineous matings, expressed as C22/C33 and C33/C44, turned out to be 0.86 and 0.82 respectively. Regarding migration, before 1920 consanguinity increased, but net migration was negative. In the period 1920-1929 consanguinity began to decrease, prior to maximum emigration. As for reproductive success, information from 1503 reconstituted families shows that complete fertility was slightly higher among consanguineous families despite a greater infant mortality. Lower infertility in consanguineous matings, as well as lower age at marriage and first maternity, could explain the above results.     

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.     

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.     

Evidence for Divergence in Populations of Bonobos (Pan paniscus) in the Lomami-Lualaba and Kasai-Sankuru Regions Based on Preliminary Analysis of Craniodental Variation

Historical climatic events and riverine barriers influence the distribution of primates. The River Congo exerts the most significant influence on primate distribution in equatorial Africa, but the extent to which the inner basin of the Congo provided a refuge against Plio-Pleistocene climatic fluctuation is poorly understood. In this study we use cranial and dental morphometrics to examine how riverine barriers affect population patterns in bonobos (Pan paniscus). Bonobos and chimpanzees (Pan troglodytes) are sister species and share the distinction of being the closest evolutionary relatives of humans, yet comparatively little is known about bonobo morphological diversity. We selected 55 adult bonobo crania with well-preserved postcanine dentitions and divided them into regions separated by the rivers Lukenie, Kasai, Lomami, and Lualaba. We found good discrimination among these regions in cranial and dental metrics, but whereas the discriminant functions from cranial metrics were statistically significant, the discriminant functions from dental metrics were not. Mean classification accuracy was 89% for craniometrics, and ranged between 72% and 93% for dental metrics. On average 84–97% of phenetic variation was encountered within regions. Our results mirror molecular studies in suggesting that bonobos are characterized by a long-term stable demographic history allowing strong gene flow between regions and precluding drift and population differentiation. There are some indications that the bonobos from the Lomami-Lualaba and the Kasai-Sankuru regions are divergent, but modest sample sizes do not allow us to be conclusive. We would welcome the opportunity to work with field researchers to augment our sample sizes and reanalyze our data.     

Evidence of psychological essentialism in a symbol-trained bonobo (Pan paniscus)

International Journal of Primatology - Psychological essentialism is the ability to recognize that the class or kind to which an object belongs remains unaltered despite changes to its superficial...     

Non-invasive sampling and DNA amplification for paternity exclusion,community structure,and phylogeography in wild chimpanzees

Genetic studies of free-ranging primates have been seriously impeded by difficulties of sampling tissues, including the undesirability of bleeding habituated animals, of transporting frozen samples to the laboratory, and of the inherent inadequacies of accessible variation including allozymes, mtDNA RFLP patterns and DNA fingerprints. We have developed methods of non-invasive DNA sampling and DNA-level genotyping which, when combined with a hierarchical analysis of mtDNA sequences and hypervariable nDNA simple sequence repeat (microsatellite) loci size length polymorphisms, facilitate the resolution of most questions at the individual, social group (community), population, and species (phylogenetic) levels. This approach, based on DNA amplified from shed hair, represents an important new tool for the acquisition of genetic information and will facilitate the study and management of both captive and free-ranging chimpanzees (Pan troglodytes). Our hierarchical analysis of population genetics of chimpanzees has revealed high historical levels of gene flow and large effective population sizes, as well as substantial divergence between the West African subspecies and chimpanzees from central and East Africa. At the community level, closer relatedness among philopatric males than among females supports the view that kin selection has been an evolutionary force shaping male-male cooperation in this species. Results from our study of the now relatively isolated Gombe community suggest that habitat fragmentation affects population genetic structure and possibly population viability.