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.     

Function and distribution of coalitions in captive bonobos (Pan paniscus)

We examined the distribution of support behaviour within a captive group of bonobos. Most support was evoked by inter-sexual conflicts with the two highest ranking females. Within a dyad, the usual winner was most often supported. Individuals that challenged the rank order by aggressions and pestering were aggressed more often by their targets in the company of an ally. The two lowest ranking males served as scapegoats, receiving 80% of the contra-support. In coalitions, inviduals did not aggress victims they would not dare to attack without supporters. However, the victims of coalitions reacted more strongly with fear and rarely counteraggressed than when being attacked alone, indicative of the high impact of aggression in support. The alpha female showed some control behaviour when intervening in conflicts. The data fitted with several functional hypotheses: coalitions functioned to maintain existing ranks, to acquire ranks, to reduce tension, and to test or strengthen the bond. We suggest that support behaviour fulfilled a crucial role in the maintenance of the power of the two highest ranking females over the males. Among the females themselves the dominance relationships were not based on coalitions, but on individual attributes.     

Monitoring hormones in urine and feces of captive bonobos (Pan paniscus)

Urinary and fecal hormones were analyzed on average every other day in 17 female bonobos kept at four US zoos (San Diego Zoo and Wild Animal Park, Milwaukee, Columbus, and Cincinnati). Ovarian cycle activity was monitored throughout the 15-month study period using estrogen and progesterone profiles and swelling charts. Behavioral data on sexual activity were also collected on a daily basis. Fecal and urinary samples were analyzed using high pressure liquid chromatography (HPLC), gas chromatography-mass spectrometry (CG-MS), and nanoelectrospray. Preliminary results indicate that in urine, both conjugated progestin and estrogen metabolites were abundant, while in fecal samples, free progestin metabolites from the 5a-pregnane series were found. Although traces of estrogen metabolites were detected in fecal samples, long-term monitoring of ovarian activity in our study yielded no meaningful estrogen profiles. In contrast, fecal progestin profiles, after adjusting for a one-day delay in excretion, closely matched the corresponding urinary progestin profiles. Using the identical antibody and tracer for both, fecal and urinary progestins, fecal samples yielded approximately ten times the relative amount of progestins compared to urinary progestins. Thus, when converted using a regression formula, fecal progestins may complete the picture obtained from urinary progestins, particularly in cases where the urine sample record is unavailable or incomplete. Evidence of the usefulness of urinary cortisol as a measure of stress is presented.     

Sexual competition in a group of captive bonobos (Pan paniscus)

We describe the occurrence of sexual competition, expressed as harassment of sexual interactions in a captive group of bonobos. We monitored all aggressive and pestering interventions during sexual interactions of three captive adult females, one adolescent, and three adult males. The study period covered two complete menstrual cycles for each female, with continuous daily observations. There was relatively little overt sexual competition by the males, in analogy with other studies. Most male interventions occurred towards interactions with the alfa female. The alfa female performed the most intense and the highest number of interventions towards the sexual interactions of the other females. The data provide evidence for female intra-sexual competition in this female dominant species.     

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.     

圈养黑猩猩血液生理生化指标测定

正动物园作为综合保护、科普宣传与公众教育的重要场所,在濒危物种的迁地保护工作中发挥着十分重要的作用(Kleiman et al.,2010)。然而,不同的濒危物种在生理学及生活史方面存在很大差异;加之部分物种的生物学信息匮乏,使得动物园的饲养繁育和疾病防控工作面临重大挑战。在常规体检及疾病诊断时,血液参数值有助于对动物机体的临床检查与诊断,解读动物的生理、营养和病理状态(胡翊群,2004;Etim et al.,2014),是及时发现动物     

Handedness in captive bonobos (Pan paniscus)

Species level right-handedness is often considered to be unique to humans. Handedness is held to be interrelated to our language ability and has been used as a means of tracing the evolution of language. Here we examine handedness in 3 captive groups of bonobos (Pan paniscus) comprising 22 individuals. We found no evidence for species level handedness. Conclusions that can be drawn from these findings are: (1) species level handedness evolved after the divergence of the Pan and Homo lineages; (2) inconsistent preferences may represent precursors to human handedness, and (3) Pan may have language abilities but these cannot be measured using handedness.     

Permanent tooth mineralization in bonobos (Pan paniscus) and chimpanzees (P. troglodytes)

The timing of tooth mineralization in bonobos (Pan paniscus) is virtually uncharacterized. Analysis of these developmental features in bonobos and the possible differences with its sister species, the chimpanzee (P. troglodytes), is important to properly quantify the normal ranges of dental growth variation in closely related primate species. Understanding this variation among bonobo, chimpanzee and modern human dental development is necessary to better contextualize the life histories of extinct hominins. This study tests whether bonobos and chimpanzees are distinguished from each other by covariance among the relative timing and sequences of tooth crown initiation, mineralization, root extension, and completion. Using multivariate statistical analyses, we compared the relative timing of permanent tooth crypt formation, crown mineralization, and root extension between 34 P. paniscus and 80 P. troglodytes mandibles radiographed in lateral and occlusal views. Covariance among our 12 assigned dental scores failed to statistically distinguish between bonobos and chimpanzees. Rather than clustering by species, individuals clustered by age group (infant, younger or older juvenile, and adult). Dental scores covaried similarly between the incisors, as well as between both premolars. Conversely, covariance among dental scores distinguished the canine and each of the three molars not only from each other, but also from the rest of the anterior teeth. Our study showed no significant differences in the relative timing of permanent tooth crown and root formation between bonobos and chimpanzees. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

Comparing infant and juvenile behavior in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): a preliminary study

The dichotomy between the two Pan species, the bonobo (Pan paniscus) and chimpanzee (Pan troglodytes) has been strongly emphasized until very recently. Given that most studies were primarily based on adult individuals, we shifted the “continuity versus discontinuity” discussion to the infant and juvenile stage. Our aim was to test quantitatively, some conflicting statements made in literature considering species differences between immature bonobos and chimpanzees. On one hand it is suggested that infant bonobos show retardation in motor and social development when compared with chimpanzees. Additionally it is expected that the weaning process is more traumatic to chimpanzee than bonobo infants. But on the other hand the development of behaviors is expected to be very similar in both species. We observed eight mother–infant pairs of each species in several European zoos. Our preliminary research partially confirms that immature chimpanzees seem spatially more independent, spending more time at a larger distance from their mother than immature bonobos. However, the other data do not seem to support the hypothesis that bonobo infants show retardation of motor or social development. The development of solitary play, environmental exploration, social play, non-copulatory mounts and aggressive interactions do not differ between the species. Bonobo infants in general even groom other group members more than chimpanzee infants. We also found that older bonobo infants have more nipple contact than same aged chimpanzees and that the weaning process seems to end later for bonobos than for immature chimpanzee. Additionally, although immature bonobos show in general more signs of distress, our data suggest that the weaning period itself is more traumatic for chimpanzees.     

An advantage for concavities in shape perception by chimpanzees (Pan troglodytes)

The significance of concavity in object shape perception by chimpanzees (Pan troglodytes) was investigated in a matching-to-sample procedure. For the task, chimpanzees were required to choose a polygon stimulus that was identical in shape to a sample. The incorrect alternative was defined by the addition or subtraction of a concave or convex apex. Chimpanzees were more sensitive to the concave deformation than to the convex deformation. This tendency conforms to the theories of human visual perception that have treated concave features as important factors in reconstructing three-dimensional structures from two-dimensional images. Our results suggest that shape representation in chimpanzees is similar to that in humans and that chimpanzees visually process two-dimensional images in the same manner as humans.     

Volumetric and lateralized differences in selected brain regions of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus)

The two species of Pan, bonobos and common chimpanzees, have been reported to have different social organization, cognitive and linguistic abilities and motor skill, despite their close biological relationship. Here, we examined whether bonobos and chimpanzee differ in selected brain regions that may map to these different social and cognitive abilities. Eight chimpanzees and eight bonobos matched on age, sex and rearing experiences were magnetic resonance images scanned and volumetric measures were obtained for the whole brain, cerebellum, striatum, motor‐hand area, hippocampus, inferior frontal gyrus and planum temporale. Chimpanzees had significantly larger cerebellum and borderline significantly larger hippocampus and putamen, after adjusting for brain size, compared with bonobos. Bonobos showed greater leftward asymmetries in the striatum and motor‐hand area compared with chimpanzees. No significant differences in either the volume or lateralization for the so‐called language homologs were found between species. The results suggest that the two species of Pan are quite similar neurologically, though some volumetric and lateralized differences may reflect inherent differences in social organization, cognition and motor skills. Am. J. Primatol. 71:988–997, 2009. © 2009 Wiley‐Liss, Inc.     

Reconciliation and consolation in captive bonobos (Pan paniscus)

Although reconciliation in bonobos (Pan paniscus) has previously been described, it has not been analyzed heretofore by the postconflict (PC) match-control (MC) method. Furthermore, although reconciliation has been investigated before in this species, consolation has not. In this study we analyzed agonistic and affiliative contacts in all sex-class combinations to clarify and reevaluate the occurrence of reconciliation in bonobos via the PC-MC method. We also investigated the occurrence of consolation by analyzing the victims' triadic contact tendency (TCT), the influence of the sex of victims, and the relative occurrence of consolation and reconciliation. We collected 167 pairs of PC-MC observations in a captive group of bonobos (in Apeldoorn, The Netherlands). The conciliatory tendency (CCT) we obtained was tendentially lower than the mean value previously found for Yerkes captive chimpanzees. Close relationships, which were present in all female-female (FF) and some male-female (MF) dyads, positively affected reconciliation rates. When only adult PC-MC pairs (157) were considered, the mean TCTs and CCTs did not differ significantly. When we focused on types of PC affiliative contact, in the case of consolation we found a striking preference for sociosexual patterns. As to the relative occurrence of consolation and reconciliation, the highest level of the former was found in the absence of the latter. When reconciliation took place, consolation generally preceded it, suggesting that consolation may be a substitutive behavior. Our findings suggest that even if reconciliation remains the best option, consolation may be an alternative substitute for reconciliation that is used to buffer the tension originating from an unresolved conflict. Reconciliation and consolation are complex phenomena that are probably related to the life history of a group. Given that few studies have been conducted on this subject, we can not at this time make any generalizations regarding conflict resolution in certain species by comparing results among studies.     

A geometric morphometric analysis of heterochrony in the cranium of chimpanzees and bonobos

Despite several decades of research, there remains a lack of consensus on the extent to which bonobos are paedomorphic (juvenilized) chimpanzees in terms of cranial morphology. This study reexamines the issue by comparing the ontogeny of cranial shape in cross-sectional samples of bonobos (Pan paniscus) and chimpanzees (Pan troglodytes) using both internal and external 3D landmarks digitized from CT scans. Geometric morphometric methods were used to quantify shape and size; dental-maturation criteria were used to estimate relative dental age. Heterochrony was evaluated using combined size-shape (allometry) and shape-age relationships for the entire cranium, the face, and the braincase. These analyses indicate that the bonobo skull is paedomorphic relative to the chimpanzee for the first principal component of size-related shape variation, most likely via a mechanism of postformation (paedomorphosis due to initial shape underdevelopment). However, the results also indicate that not all aspects of shape differences between the two species, particularly in the face, can be attributed to heterochronic transformation and that additional developmental differences must also have occurred during their evolution.     

Developing classification in action: II. Young chimpanzees (Pan troglodytes)

The development of spontaneous object manipulation in 5 chimpanzees (Pan troglodytes) from ages 15 to 54 months was investigated, focusing on formal properties of subjects’ acts and the objects they manipulated. Young chimpanzees’ manipulation progress from serial one-at-a-time acts on one object to parallel two-at-a-time acts on two or more objects. With age, simultaneous acts become increasingly transformational and identical or reciprocal to each other. Moreover, the class properties of objects manipulated simultaneously change. When presented with objects belonging to two different classes, subjects shift, with age, from manipulating different objects to manipulating identical or similar objects. In all these respects young chimpanzee’ development is similar to human infants’. In others it differs. Most especially, the onset age is later and the development is slower as well as less structurally complex.     

Peering in mature, captive bonobos (Pan paniscus)

“Peering”—close-proximity staring at the mouth of another—was observed in ten (three males and seven females) mature (at least 7 years old) bonobos (Pan paniscus) living in three social groups at the San Diego Zoo and Wild Animal Park. Instantaneous scan samples, taken at 2-min intervals, over a three-and-a-half year period, yielded 617 observations of peering (1.4 per observation hour). Food was exchanged in only 15 of these scans. Peering was most often performed by younger animals and was primarily directed toward older females (“matrons”). In a given dyad, the animal more likely to peer at the other was also more like to both peer and be peered at if they frequently groomed and infrequently displayed aggression at a given female. An adolescent male showed the highest frequency of peering when living with two older females, but dropped to adult male levels when later housed with two younger (albeit mature) females. A reversal in which animal was more likely to peer, follow, and groom occurred in one female dyad, after the birth of the younger animal's first infant. After a similar birth in the other group, no such changes were observed. We discuss how these and related findings, in conjunction with what is known of the social structure of this species, suggest that one possible function of peering in bonobos may be as a signal acknowledging female status.     

Design complexity in termite-fishing tools of chimpanzees (Pan troglodytes)

Adopting the approach taken with New Caledonian crows (Corvus moneduloides), we present evidence of design complexity in one of the termite-fishing tools of chimpanzees (Pan troglodytes) in the Goualougo Triangle, Republic of Congo. Prior to termite fishing, chimpanzees applied a set of deliberate, distinguishable actions to modify herb stems to fashion a brush-tipped probe, which is different from the form of fishing tools used by chimpanzees in East and West Africa. This means that ‘brush-tipped fishing probes’, unlike ‘brush sticks’, are not a by-product of use but a deliberate design feature absent in other chimpanzee populations. The specialized modifications to prepare the tool for termite fishing, measures taken to repair non-functional brushes and appropriate orientation of the modified end suggest that these wild chimpanzees are attentive to tool modifications. We also conducted experimental trials that showed that a brush-tipped probe is more effective in gathering insects than an unmodified fishing probe. Based on these findings, we suggest that chimpanzees in the Congo Basin have developed an improved fishing probe design.     

Video-task acquisition in rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes): A comparative analysis

This study describes video-task acquisition in two nonhuman primate species. The subjects were seven rhesus monkeys (Macaca mulatta) and seven chimpanzees (Pan troglodytes). All subjects were trained to manipulate a joystick which controlled a cursor displayed on a computer monitor. Two criterion levels were used: one based on conceptual knowledge of the task and one based on motor performance. Chimpanzees and rhesus monkeys attained criterion in a comparable number of trials using a conceptually based criterion. However, using a criterion based on motor performance, chimpanzees reached criterion significantly faster than rhesus monkeys. Analysis of error patterns and latency indicated that the rhesus monkeys had a larger asymmetry in response bias and were significantly slower in responding than the chimpanzees. The results are discussed in terms of the relation between object manipulation skills and video-task acquisition.     

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.     

Comparison of object manipulation among 74 species of non-human primates

Seventy-four primates species (24 genera of six families) were presented with a nylon rope and a wooden cube, and their subsequent manipulations were recorded in detail. Five hundreds and six manipulation patterns were distinguished on the basis of the actions performed, body-parts used and relations to other objects. Inter-specific comparisons revealed three groups: (1) lemurs, marmosets, spider monkeys and leaf-eaters; (2) Old World monkeys except leaf-eaters; and (3) cebus monkeys and apes. The first group had the smallest repertoire of manipulations, in which only a few types of actions and body-parts were involved. The second and third groups had more varied modes of manipulation. Actions such as Roll, Rub and Slide, and use of fingers characterized these groups. Except for the lesser ape, their manipulations were frequently related with other objects. Moreover, actions such as Drape, Drop, Strike, Swing and Throw were typical of the third group. The factors producing such inter-specific differences in manipulations and the relations to tool use are discussed.     

Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): Implications for natural social systems and interindividual relationships

This study compares adult play behavior in the two Pan species in order to test the effects of phylogenetic closeness and the nature of social systems on play distribution. The social play (both with fertile and immature subjects) performed by adults did not differ between the two species. In contrast, in bonobos, play levels among fertile subjects were higher than in chimpanzees. Findings regarding levels of undecided conflicts (more frequent in bonobos) and formal submission displays (lacking in bonobos) confirm, in the two colonies under study, that bonobos exhibit "egalitarianism" more than chimpanzees. Some authors emphasized the importance of play-fighting for social assessment when relationships among individuals are not codified and structured according to rank-rules. Indeed, adult bonobos played more roughly than chimpanzees. Moreover, adult bonobos displayed the full play-face at a high frequency especially during rough play sessions, whereas in chimpanzees, the frequency of play signals was not affected by roughness of play. The frequency of social play among bonobo females was higher than in any other sex combinations, whereas no difference was found for chimpanzees. As a matter of fact, social play can be viewed as a balance between cooperation and competition. Among bonobo females, characterized by social competence and affiliation, social play might enhance their behavioral flexibility and increase their socially symmetrical relationships which, after all, are the basis for their egalitarian society.