Comparing maternal styles in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes)

Studies on Cercopithecine primate maternal styles, using factor analysis on a set of maternal behaviors, commonly render two factors that describe separate dimensions of maternal behavior: protectiveness and rejection. The aims of this study were to 1) investigate whether this method for determining maternal styles in Cercopithecine species can be applied to bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), 2) determine whether they follow the same pattern, and 3) assess whether species differences in maternal style are apparent. We performed a factor analysis on nine maternal behaviors using data on eight mother-infant pairs of each species. This resulted in three factors: protectiveness, distance, and refusal. Protectiveness is positively correlated with time spent in ventral contact, making contact, approaching, and restraining. Distance is positively related with breaking contact and leaving. Refusal is positively correlated with rejecting and nipple-rejecting. The pattern of protectiveness corresponds with the pattern found in Cercopithecine species, suggesting a high consistency of this dimension across species and higher taxa. The retention of the other two factors indicates that in the Pan species, breaking contact and leaving represent another dimension, apart from rejecting and nipple-rejecting, which usually fall under one dimension in Cercopithecine species. An interspecific comparison of the factor scores for each dimension of maternal behavior reveals that, on average, bonobos and chimpanzees score equally on protectiveness. Scores on distance increase positively with infant age in chimpanzees, and negatively in bonobos, and on average bonobos have higher scores on refusal. These interspecies differences in maternal style are discussed in the light of interspecies differences in infant development, infant vulnerability to aggression, interbirth intervals, and female sociality.     

Patterns of microsatellite polymorphism in the range-restricted bonobo (Pan paniscus): considerations for interspecific comparison with chimpanzees (P. troglodytes)

The endangered great ape, Pan paniscus (bonobo) has the smallest range of the African apes. Virtually nothing is known about the genetic diversity or genetic structure of this species, while substantial amounts of polymorphism have been reported for the bonobo’s widespread congener, the chimpanzee (P. troglodytes). Given its restricted range, what is the extent of genetic variation in the bonobo relative to the chimpanzee, and is the bonobo genetically depauperate? To investigate patterns of genetic polymorphism, bonobos of wild origin were genotyped for 28 microsatellite loci. The mean number of alleles per locus (5.2) and the mean observed heterozygosity (0.52) in bonobos were similar to variation observed in a wild chimpanzee community (P. t. schweinfurthii). The rarer bonobo is not genetically depauperate and may have genetic diversity comparable to the eastern chimpanzee subspecies. Bonobos have approximately 55% of the allelic diversity and 66% of the observed heterozygosity exhibited by all three chimpanzee subspecies sampled across equatorial Africa. Resampling techniques were used to quantify the effects of sample size differences and number and choice of loci between bonobos and chimpanzees. The examination of these variables underscores their importance in accurately interpreting interspecific comparisons of diversity estimates.     

Comparing the adoption of protective behaviors: The framing effects of national culture and hazard onset type

On the basis of framing effect and protective action decision model, this study examines the differences in people's response to diverse hazard onset types (sudden or gradual) under different cultural frameworks (China and the United States) and the framing effects of culture and hazard onset type on people's perception and behavioral response. The data are derived from three questionnaire surveys on people's behavioral response to H7N9 and smog emergency in China and H1N1 in the United States. Results indicate that people with different cultures and diverse contexts of hazard onset type present substantial differences in risk perception, protective action perception, stakeholder perception, and behavioral expectations. Furthermore, culture and hazard onset type exert significant framing effects on people's three types of perception, reliance on official information sources, and intention to adopt protective actions. This research empirically verifies the existence of framing effect in culture and decision scenarios, thereby helping in developing different emergency communication strategies.     

Cognitive research in zoo-housed chimpanzees: influence of personality and impact on welfare

We monitored chimpanzee welfare during the introduction of on-exhibit cognitive research training and testing, as measured by behavior and interest in such training, and related individual variation to personality assessments. We observed 11 chimpanzees (six males; five females) over a 16-month period and compared their behavior across three conditions: (1) Baseline (nontraining/research situations) and (2) an on-going, off-exhibit program of Husbandry Training and (3) Research Pod Activities, on-exhibit, group training for cognitive testing. There was considerable individual variation in their interest levels during research sessions; females and those scoring higher for Openness were present more frequently (including those who actively participated and those who observed others participating), but interest did not vary in relation to rates of self-directed behaviors (SDBs), rank, or the level of social disruptions within the group (i.e. large-scale displays or fights). The frequency of SDBs was predicted by the Neuroticism personality factor, but did not differ across baseline and training contexts, indicating that these activities do not negatively impact welfare. We also explored vigilance as an indicator of social uncertainty, but social monitoring did not differ in relation to either social context or rank. Finally, we explored how the specific characteristics of the research context impacted on SDBs; namely, social context, reward contingency, and visual access to keepers. SDBs increased only when visual access to keepers was restricted, suggesting that visual contact reduced uncertainty in novel training contexts. Overall, the introduction of a cognitive research program did not compromise welfare, and the chimpanzees' repeated interest and willingness to participate suggests that the research was enriching.     

Electroejaculation in chimpanzees and gorillas and artificial insemination in chimpanzees

Electroejaculation was performed in 3 chimpanzees, 1 pygmy chimpanzee, and 2 gorillas with an instrument that delivers a modified sine wave current with a frequency of 24 Hz. The current stimuli were applied by a rectal probe with longitudinal electrodes. The electrical parameters varied from 6 to 12 V and from 30 to 40 mA for response of erection and lay between 8 and 18 V and between 40 and 145 mA during semen emission. Eleven chimpanzee semen samples showed the following data (x ± SD): total volume 1.9 ± 1.3 ml, volume of the liquid fraction 0.3 ± 0.2 ml, spermatozoa per ejaculate 743 ± 376 × 10⁶, sperm motility 52.7 ± 9.6%, morphologically abnormal spermatozoa 12.2 ± 7.5%. From an adult gorilla, three semen samples were collected, in each case without spermatozoa. The electrostimulation of a 6-year-old gorilla led to an erection, but not to semen emission. Three female chimpanzees were inseminated with fresh or frozen semen, each of them within three different estrous cycles. None of these inseminations led to a pregnancy.     

Triadic social interactions operate across time: a field experiment with wild chimpanzees

Social animals cooperate with bonding partners to outcompete others. Predicting a competitor''s supporter is likely to be beneficial, regardless of whether the supporting relationship is stable or transient, or whether the support happens immediately or later. Although humans make such predictions frequently, it is unclear to what extent animals have the cognitive abilities to recognize others’ transient bond partners and to predict others'' coalitions that extend beyond the immediate present. We conducted playback experiments with wild chimpanzees to test this. About 2 h after fighting, subjects heard recordings of aggressive barks of a bystander, who was or was not a bond partner of the former opponent. Subjects looked longer and moved away more often from barks of the former opponents’ bond partners than non-bond partners. In an additional experiment, subjects moved away more from barks than socially benign calls of the same bond partner. These effects were present despite differences in genetic relatedness and considerable time delays between the two events. Chimpanzees, it appears, integrate memories of social interactions from different sources to make inferences about current interactions. This ability is crucial for connecting triadic social interactions across time, a requirement for predicting aggressive support even after a time delay.     

A skew in poo: Biases in primate fecal isotope analysis and recommendations for standardized sample preparation

Feces are a treasure trove in the study of animal behavior and ecology. Stable carbon and nitrogen isotope analysis allows to assess the dietary niches of elusive primate species and primate breastfeeding behavior. However, some fecal isotope data may unwillingly be biased toward the isotope ratios of undigested plant matter, requiring more consistent sample preparation protocols. We assess the impact of this potential data skew in 114 fecal samples of wild bonobos (Pan paniscus) by measuring the isotope differences (Δ¹³C, Δ¹⁵N) between bulk fecal samples containing larger particles (>1 mm) and filtered samples containing only small particles (<1 mm). We assess the influence of fecal carbon and nitrogen content (ΔC:N) and sample donor age (subadult, adult) on the resulting Δ¹³C, Δ¹⁵N values (n = 228). Additionally, we measure the isotope ratios in three systematically sieved fecal samples of chimpanzees (Pan troglodytes verus), with particle sizes ranging from 20 μm to 8 mm (n = 30). We found differences in fecal carbon and nitrogen content, with the smaller fecal fraction containing more nitrogen on average. While the Δ¹³C values were small and not affected by age or ΔC:N, the Δ¹⁵N values were significantly influenced by fecal ΔC:N, possibly resulting from the differing proportions of undigested plant macroparticles. Significant relationships between carbon stable isotope ratios (δ¹³C) values and %C in large fecal fractions of both age groups corroborated this assessment. Δ¹⁵N values were significantly larger in adults than subadults, which should be of concern in isotope studies comparing adult females with infants to assess breastfeeding. We found a random variation of up to 3.0‰ in δ¹³C and 2.0‰ in nitrogen stable isotope ratios within the chimpanzee fecal samples separated by particle sizes. We show that particle size influences isotope ratios and propose a simple, cost-effective filtration method for primate feces to exclude larger undigested food particles from the analysis, which can easily be adopted by labs worldwide.     

Onset and early use of gestural communication in nonhuman great apes

The early gesturing of six bonobos, eight chimpanzees, three gorillas, and eight orangutans was systematically documented using focal animal sampling. Apes' were observed during their first 20 months of life in an effort to investigate: (i) the onset of gesturing; (ii) the order in which signals of different sensory modalities appear; (iii) the extent to which infants make use of these modalities in their early signaling; and (iv) the behavioral contexts where signals are employed. Orangutans differed in important gestural characteristics to African ape species. Most notably, they showed the latest gestural onset and were more likely to use their early signals in food-related interactions. Tactile and visual signals appeared similarly early across all four species. In African apes, however, visual signaling gained prominence over time while tactile signaling decreased. These findings suggest that motor ability, which encourages independence from caregivers, is an important antecedent, among others, in gestural onset and development, a finding which warrants further investigation.     

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.     

The date-delay framing effect in temporal discounting depends on substance abuse

In the present study, individuals with substance use disorders (n=30) and non-addicted controls (n=30) were presented with a delay-discounting task with time being described either as dates or as temporal intervals. Three main results were obtained. First, in both groups reward size had a large impact on discounting future rewards, with discount rates becoming larger with smaller reward sizes. Second, participants discounted future rewards less strongly when their time of delivery was presented as a date instead of a temporal distance. Third, whereas discount rates of individuals with substance use disorders varied substantially with regard to the presentation of time in the task, the controls changed their choices depending on time presentation only slightly.     

Neighbor effect: evidence of affiliative and agonistic social contagion in captive chimpanzees (Pan troglodytes)

Previous studies of captive chimpanzees have demonstrated the "neighbor effect," or social contagion, with respect to agonistic vocalizations and behaviors. The present study considers whether there is a relationship between behavior patterns in focal animals and the auditory signals of neighboring social groups. Using focal-group sampling, we collected 172.5 hr of data on 51 subjects (25 females and 26 males) housed in 10 social groups. We performed two-tailed Wilcoxon matched-pairs signed-rank tests to determine whether the relative frequency of the vocalizations (high vs. low) affected the behaviors. In keeping with past research, we found that agonistic noises and vocalizations from neighboring social groups had a significant effect on the rates of focal-group bluff displays, pant-hoots, and aggression (P<0.05). In addition, we also found significant relationships between grooming behavior and vocalizations in focal groups, and grooming vocalizations from neighboring groups (P<0.05). The results suggest that social contagion is not limited to aggressive behaviors, but also occurs for affiliative behavior patterns.     

Reconciliation, consolation and postconflict behavioral specificity in chimpanzees

Conflicts of interest arise regularly in the lives of all group-living animals and may escalate into aggressive conflicts. The costs of aggressive escalation can be reduced through peaceful postconflict interactions. This study investigated the postconflict behavior of 22 adult chimpanzees at Chester Zoo. The occurrence of reconciliation, i.e. the postconflict affiliative reunion between conflict opponents, and consolation, i.e. a postconflict affiliative interaction directed from a third party to the recipient of aggression, were demonstrated. Consolation was more likely to occur in the absence of reconciliation than after reconciliation, and reconciliation was more likely to occur in the absence of consolation than after consolation, supporting the hypothesis that consolation acts as a substitute for reconciliation when the latter fails to occur. Evidence for behavioral specificity, i.e. context-specific use of certain behaviors, was found for both reconciliation and consolation, which, along with high conciliatory tendencies, suggests an explicit style of postconflict behavior in the study subjects.     

Preliminary bonobo and chimpanzee nesting by habitat type in the northern Lac Tumba Landscape,Democratic Republic of Congo

Knowing how habitat determines the distribution of great apes is essential for understanding their ecology and conservation requirements. Habitats in the northern Lac Tumba Landscape where this study was conducted are mostly swamp and flooded forests, which types have been overlooked in many great ape surveys. This study describes and discusses patterns of bonobo and chimpanzee nesting sites across these habitat types in the general scope of habitat use by great apes. Considerable efforts were deployed to survey forests of the Ngiri Triangle (186 km), Bomongo‐Lubengo (126 km) and Bolombo‐Losombo (112 km). Great ape nesting site encounter rates (r) were calculated for Bonobos (r = 0.21 nesting sites km^?1; Bolombo‐Losombo), chimpanzees (r = 0.11 nesting sites km^?1; Ngiri Triangle) and (r = 0.02 nesting sites km^?1; Bomongo‐Lubengo). Swamps and flooded forests dominated the three zones. Nesting sites were at the highest encounter rates in flooded forests; both great ape species were significantly associated with swampy and flood forests. Human signs did not influence the occurrence of nesting sites in these forests. These results confirm findings from other sites where great apes were observed using swamps; they suggest that future surveys include these types of habitat to avoid under‐estimating population sizes.     

Bonobos have a more human-like second-to-fourth finger length ratio (2D:4D) than chimpanzees: a hypothesized indication of lower prenatal androgens

The ratio of the second-to-fourth finger lengths (2D:4D) has been proposed as an indicator of prenatal sex differentiation. However, 2D:4D has not been studied in the closest living human relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). We report the results from 79 chimpanzees and 39 bonobos of both sexes, including infants, juveniles, and adults. We observed the expected sex difference in 2D:4D, and substantially higher, more human-like, 2D:4D in bonobos than chimpanzees. Previous research indicates that sex differences in 2D:4D result from differences in prenatal sex hormone levels. We hypothesize that the species difference in 2D:4D between bonobos and chimpanzees suggests a possible role for early exposure to sex hormones in the development of behavioral differences between the two species.     

Polymorphisms and gross structure of glycophorin genes in common chimpanzees

Using human α glycophorin cDNA probe and six restriction enzymes, we examined the homologues of human glycophorin genes in genomic DNA of 11 unrelated chimpanzees. We show that, in contrast to the human, the chimpanzee exhibits an unusual array of nonrandomly distributed restriction fragment length polymorphisms (RFLP). No clear correlation was found between the RFLP and the V-A-B-D blood-group phenotypes of the subjects, with one possible exception. However, pairs of allelic RFLP occurring at a relatively high frequency were identified. In addition, the homology of chimpanzee glycophorin genes to the human genes was examined using as probes synthetic oligonucleotides specifying distinct regions of human glycophorin genes. We show that the glycophorin gene family in the chimpanzee consists of at least three members that are homologous to the human α, δ, and E genes (glycophorins A, B, and E) and may share a similar gross structure and overall organization. This research was supported by National Institutes of Health Grant GM 16389.     

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.     

Mother-infant relations and infant development in captive chimpanzees and orang-utans

Four chimpanzee (Pan troglodytes)mother—infant dyads and four orangutan (Pongo pygmaeus)motherinfant dyads were studied for the first 11 months of the infants’ lives. For both species, ventroventral contact and nipple contact decreased over time at a similar rate, but total contact decreased earlier in the orangutans and was 50% lower than for the chimpanzees at the end of the study. Social play between the mothers and the infants did not differ in frequency between the species, but orangutans played above the ground and chimpanzees on the ground. Solitary play differed in form between the species and, like social play, reflected their differences in arboreal and terrestrial proclivities. In addition, the orangutans engaged in solitary play considerably more frequently than the chimpanzees during the second half-year of life. The developmental differences in mother-infant contact and solitary play of these apes are consistent with the differences in their speciestypical social organization. The data may reflect, therefore, early development of species differences in the social and relatively solitary natures of chimpanzees and orangutans, respectively. An erratum to this article is available at .     

Housing conditions and breeding success of chimpanzees at the primate center TNO

Results of rearing and breeding chimpanzees at the Primate Center TNO are presented. The colony was built up from 1964 to 1971 by the acquisition of mostly young chimpanzees; thereafter, it was increased by local breeding. The ages at which the animals became reproductive were between 6 and 11 years for the males and between 7 and 15 years for the females. Seventy-six percent of the pregnancies (N = 132) were carried to full term and 87% of these were live births. Fifty-five percent of the babies were nursed by their mothers for 2–10 months. The next pregnancy after an abortion occurred on the average after 7 months; after a carriage to term, this occurred after 11.9 months. The difference was not influenced by the duration of the weaning period. Animals of 2 years or more that had been weaned within a month were more likely to show body rocking than animals weaned later. Cases of disturbed social or reproductive behavior were rare; the first locally bred animals have become reproductively active.