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.     

Molar development in common chimpanzees (Pan troglodytes)

Numerous studies have reported on enamel and dentine development in hominoid molars, although little is known about intraspecific incremental feature variation. Furthermore, a recent histological study suggested that there is little or no time between age at chimpanzee crown completion and age at molar eruption, which is unlikely given that root growth is necessary for tooth eruption. The study presented here redefines growth standards for chimpanzee molar teeth and examines variation in incremental features. The periodicity of Retzius lines in a relatively large sample was found to be 6 or 7 days. The number of Retzius lines and cuspal enamel thickness both vary within a cusp type, among cusps, and among molars, resulting in marked variation in formation time. Daily secretion rate is consistent within analogous cuspal zones (inner, middle, and outer enamel) within and among cusp types and among molar types. Significantly increasing trends are found from inner to outer cuspal enamel (3 to 5 microns/day). Cuspal initiation and completion sequences also vary, although sequences for mandibular molar cusps are more consistent. Cusp-specific formation time ranges from approximately 2 to 3 years, increasing from M1 to M2, and often decreasing from M2 to M3. These times are intermediate between radiographic studies and a previous histological study, although both formation time within cusps and overlap between molars vary considerably. Cusp-specific (coronal) extension rates range from approximately 4 to 9 microns/day, and root extension rates in the first 5 mm of roots range from 3 to 9 microns/day. These rates are greater in M1 than in M2 or M3, and they are greater in mandibular molars than in respective maxillary molars. This significant enlargement of comparative data on nonhuman primate incremental development demonstrates that developmental variation among cusp and molar types should be considered during interpretations and comparisons of small samples of fossil hominins and hominoids.     

Imaginary Play in chimpanzees (Pan troglodytes)

Imaginary Play was studied in a group of five signing chimpanzees and it was found that chimpanzees engage in imaginary play similar to that found in human children. Fifteen hours of remote videotapes were analyzed for instances of imaginary play. Behaviors were defined as imaginary play by meeting a predetermined criteria which allowed them to be classified into one of six different categories of imaginary play. Six instances of imaginary play were found and these were classified into the two categories of Animation and Substitution. Observations of imaginary play in other research with chimpanzees were discussed.     

Innovation in wild chimpanzees (Pan troglodytes)

Innovations of behavior have major implications for the concept of culture in animals. Innovation has rarefy been documented in wild animal populations. The chimpanzees of the Taï National Park, Côte d’Ivoire, spontaneously included new patterns of behavior in their repertoire during our study. Some innovations were incorporated into a minority of the group members’ repertoire, whereas others, such as building day nests in trees and on the ground more frequently, became general behaviors. Similarly, new contexts for use of leaf- clipping behavior and novel ways of feeding on some leaves appeared and rapidly became part of the behavior of most group members. The environmental parameters were too stable to explain these new forms of behavior, as most of them took place within 1 month during the same dry season. In a similar way, leaf- grooming acquired a new function in Gombe chimpanzees. A process similar to social conventions could explain the emergence of these new functions for an existing behavior in a way rather similar to human “fashion. ” Three major characteristics of human culture — the absence of individual variations in the performance of the behavior, the general use of the behavior by group members, and the ability to modify the function of a behavior — characterize leaf-clipping in Taï chimpanzees and leaf- grooming in Gombe chimpanzees.     

Twinning and heteropaternity in chimpanzees (Pan troglodytes)

Unlike monozygotic (MZ) twins, dizygotic (DZ) twins develop from separate ova. The resulting twins can have different sires if the fertilizing sperm comes from different males. Routine paternity testing of a pair of same-sexed chimpanzee twins born to a female housed with two males indicated that the twins were sired by two different males. DNA typing of 22 short-tandem repeat (STR) loci demonstrated that these twins were not MZ twins but heteropaternal DZ twins. Reproductive data from 1926-2002 at five domestic chimpanzee colonies, including 52 twins and two triplets in 1,865 maternities, were used to estimate total twinning rates and the MZ and DZ components. The average chimpanzee MZ twinning rate (0.43%) equaled the average human MZ rate (0.48%). However, the chimpanzee DZ twinning rate (2.36%) was over twice the human average, and higher than all but the fertility-enhanced human populations of Nigeria. Similarly high twinning rates among African chimpanzees indicated that these estimates were not artifacts of captivity. Log-linear analyses of maternal and paternal effects on recurrent twinning indicated that females who twinned previously had recurrence risks five times greater than average, while evidence for a paternal twinning effect was weak. Chimpanzee twinning rates appear to be elevated relative to corresponding estimated human rates, making twinning and possibly heteropaternity more important features of chimpanzee reproductive biology than previously recognized.     

Innovative social behavior in chimpanzees (Pan troglodytes)

We present evidence of agonistic buffering in captive chimpanzees, recorded from 1993 until 2005, mainly from ad libitum sampling in over 2000 hr of observation. A total of 33 agonistic buffering episodes were analyzed for context and effects of this complex social behavior. Agonistic buffering was directed at the whole chimpanzee colony as they supported an individual who initially received aggression from the alpha male, independently of the victim's age, sex or social rank. Chimpanzee agonistic buffering behavior is compared with that in other nonhuman primate species, and we describe some particularities of chimpanzee agonistic buffering: the status of the buffers used-socially important offspring such as those from the alpha female-and the social rank of the adult male responsible for the buffering episode-alpha male. Possible functions for this behavior in chimpanzees are suggested as appeasement of group members in a particularly crowded captive setting, and/or as a "forced reconciliation" mechanism. Chimpanzees exhibit behavioral flexibility by adapting themselves to new social and physical situations and use novel behavior to achieve social benefits.     

Measurement of eye-gaze in chimpanzees (Pan troglodytes)

Gaze cues are used as an index of social cognition in primates, yet the sensitivity to different forms of gaze, and consequently the cues required to test gaze-following abilities remain understudied. Whereas the eye is attributed special signal value in humans, the camouflaged ocular morphology of non-human primates has led to the consensus that head orientation may be a more salient cue. This study presents the first documentation of the surface eye movements of the chimpanzee, Pan troglodytes, in order to determine the behavioral forms of eye-gaze and their saliency as signals, document their functional variation, and address the signal value of the eyes distinct from head orientation. Movements of the eye were identified as Scan (continuous movement), Glance (a single movement <1 sec), or Fixate (no movement). Scans, glances, and fixations were reliably detected by humans during live observation and from video (Cohen's kappa over 0.70) and, therefore, are likely also to be detected by conspecifics. Eye-gaze comprised a nonunitary measure of visual attention, reflecting the attentional task demands of different activities. Specifically, chimpanzees spent significantly more time scanning while feeding and resting, than grooming, F(2,28) = 10.23, P<0.001, and spent significantly more time fixating while grooming, than feeding or resting, F(2,28) = 7.52, P<0.01. Further, eye-gaze was often incongruent with head movement, varying significantly with the form of eye-gaze: incongruence was found during 12-21% of fixations, during 42-49% of scans, and during 70-100% of glances, F(2,16) = 30.17, P<0.001. These findings provide the basis for discrimination of the adaptive significance of gaze-processing abilities with emphasis on sensitivity to eye-gaze distinct from head orientation. If we are to continue exploring gaze-processing abilities in primates, then we need greater consideration of the precise nature of the signals themselves. Here we present evidence for special consideration of the eyes as a salient signal in P. troglodytes.     

Food Preferences Among Captive Western Gorillas (Gorilla gorilla gorilla) and Chimpanzees (Pan troglodytes)

I used a zoological park setting to address food preferences among gorillas (Gorilla gorilla gorill) and chimpanzees (Pan troglodytes). Gorillas and chimpanzees are different sizes, and consequently, have been traditionally viewed as ecologically distinct. Sympatric western gorillas and chimpanzees have proved difficult to study in the wild. Limited field data have provided conflicting information about whether gorillas are fundamentally different from chimpanzees in diet and behavior. Fruit eating shapes the behavior of most apes, but it is unclear whether the large-bodied gorillas are an exception to this rule, specifically whether they are less selective and more opportunistic fruit eaters than chimpanzees are. My research provides experimental observational data to complement field data and to better characterize the diets and food preferences of the African apes. During laboratory research at the San Francisco Zoological Gardens, I examined individual and specific differences in food preferences of captive gorillas and chimpanzees via experimental paired-choice food trials with foods that varied in nutritional content. During the study, I offered 2500 paired-food choices to 6 individual gorillas and 2000 additional pairs to them as a group. I also proffered 600 food pairs to 4 individual chimpanzees. Despite expectations of the implications of body size differences for diet, gorillas and chimpanzees exhibited similar food preferences. Both species preferred foods high in non-starch sugars and sugar-to-fiber ratios, and low in total dietary fiber. Neither species avoided foods containing tannins. These data support other suggestions of African apes sharing a frugivorous adaptation.     

Electrocardiogram abnormalities in captive chimpanzees (Pan troglodytes)

Although cardiovascular disease is the leading cause of death in the captive chimpanzee population, little is known about the prevalence and etiology of heart disease in this species. We reviewed the physical exam records of 265 common chimpanzees (Pan troglodytes) for electrocardiogram abnormalities. During the 24-mo period reviewed (August 2003 through August 2005), 34 animals were diagnosed with cardiac arrhythmias consisting of ventricular arrhythmias, supraventricular arrhythmias, conduction disturbances, mixed arrhythmias, and bradycardia. The incidence of cardiac arrhythmia was significantly higher in male animals, chimpanzees 20 to 39 y old, and those with structural heart disease. Incidence of cardiac arrhythmia was not significantly higher in animals with hypertension, hyperlipidemia, or chronic viral infections. During the retrospective period, 7 animals with cardiac arrhythmias died or were euthanized. Mortality was significantly higher in animals with ventricular arrhythmias compared with those without ventricular arrhythmias. We conclude that in the common chimpanzee, age, male gender, and structural heart disease are risk factors for developing cardiac arrhythmias and that ventricular arrhythmias are risk factors for mortality.     

Probit and survival analysis of tooth emergence ages in a mixed-longitudinal sample of chimpanzees (Pan troglodytes).

Tooth emergence data from a mixed-longitudinal sample of 58 chimpanzees of known age were analyzed using probit and survival techniques to produce median emergence ages, ranges of variability, and emergence sequences for primary and permanent teeth. Between-group comparisons were made to test for statistically significant differences in emergence ages. No such differences were found between right and left sides, or between maxilla and mandible, for any primary or permanent teeth. Male-female comparisons did demonstrate significant emergence-age differences for some teeth, although they were not always bilaterally symmetrical. More complete data are required to further clarify the nature of sex differences in tooth emergence in chimpanzees. Regression models for age prediction from the number of emerged teeth were generated and indicate that males achieve a given number of emerged teeth at a significantly later age than females. However, when fewer than five teeth have emerged, males are predicted to be younger than females. The sizable root mean square error values for these models suggest that this method of age prediction has limited usefulness owing to the amount of variability in timing of tooth emergence in chimpanzees. The implications of these data for studies on tooth emergence in early hominids are addressed.     

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.     

Not all chimpanzees (Pan troglodytes) show self-recognition

When a chimpanzee is presented with a mirror it initially responds with social behavior directed toward the reflection. After several hours of exposure to the mirror the social behavior decreases and the mirror is used to guide self-directed responses to previously unobservable parts of the body such as the face. When a distinctively colored mark is unobtrousively applied to the chimpanzee's face and the chimpanzee touches the mark while observing itself in the mirror, this behavior is said to indicate self-recognition. Such self-recognition has been considered to be a robust phenomenon in chimpanzees, with self-directed and mark-directed behaviors both appearing in all socially-housed adult chimpanzees tested. In our study 11 chimpanzees were given mirror exposure and tested with the mark test. Only one of the 11 chimpanzees touched the mark during test, although several showed self-directed behavior using the mirror to guide their movements. Such experimental factors as mirror size, position, or temporal spacing of the mirror exposure, and such subject variables as age, sex, previous social experience, and subspecies were insufficient to explain the difference between the present and previous findings. We suggest that there are individual differences in mirror recognition behavior in chimpanzees, and that further consideration of the factors contributing to this phenomenon, including the development of additional tests for self-recognition, is needed.     

Testosterone and energetics in wild chimpanzees (Pan troglodytes schweinfurthii)

Ovarian function in female hominoids is sensitive to both energy flux and energy balance, resulting in a reduced probability of conception during periods when a successful reproductive outcome is less likely. However, the extent to which energetic factors constrain gonadal function in male hominoids is not clear. We examined the effects of both acute and chronic variation in energy availability on urinary testosterone (T) levels in adult male chimpanzees. Acute changes in energy availability, which were assayed by means of observational data on feeding behavior, did not result in decreased T production for 11 individuals at Kibale National Park, Uganda. Chronic energy shortages, on the other hand, may be associated with lower T levels in this population. Adult males in Kibale (n=11), who maintain suboptimal access to energy, exhibit significantly lower urinary T levels than males in captivity (n=11), who are more sedentary and better fed. These results suggest that data on hormonal function in captive chimpanzees should be interpreted with caution because individuals may produce T at levels well above those that are typical in the wild. They also suggest that short-term variations in T levels in male hominoids are more likely to be explained by social factors than by energetic ones.     

The perception of self-agency in chimpanzees (Pan troglodytes)

The ability to distinguish actions and effects caused by oneself from events occurring in the external environment is a fundamental aspect of human cognition. Underlying such distinctions, self-monitoring processes are often assumed, in which predicted events accompanied by one's own volitional action are compared with actual events observed in the external environment. Although many studies have examined the absence or presence of a certain type of self-recognition (i.e. mirror self-recognition) in non-human animals, the underlying cognitive mechanisms remain unclear. Here, we provide, to our knowledge, the first behavioural evidence that chimpanzees can perform self/other distinction for external events on the basis of self-monitoring processes. Three chimpanzees were presented with two cursors on a computer display. One cursor was manipulated by a chimpanzee using a trackball, while the other displayed motion that had been produced previously by the same chimpanzee. Chimpanzees successfully identified which cursor they were able to control. A follow-up experiment revealed that their performance could not be explained by simple associative responses. A further experiment with one chimpanzee showed that the monitoring process occurred in both temporal and spatial dimensions. These findings indicate that chimpanzees and humans share the fundamental cognitive processes underlying the sense of being an independent agent.     

Kinship and social bonds in female chimpanzees (Pan troglodytes)

A large body of theoretical and empirical research suggests that kinship influences the development and maintenance of social bonds among group‐living female mammals, and that human females may be unusual in the extent to which individuals form differentiated social relationships with nonrelatives. Here we combine behavioral observations of party association, spatial proximity, grooming, and space use with extensive molecular genetic analyses to determine whether female chimpanzees form strong social bonds with unrelated individuals of the same sex. We compare our results with those obtained from male chimpanzees who live in the same community and have been shown to form strong social bonds with each other. We demonstrate that party association is as good a predictor of spatial proximity and grooming in females as it is in males, that the highest party association indices are consistently found between female dyads, that the sexes do not differ in the long‐term stability of their party association patterns, and that these results cannot be explained as a by‐product of the tendency of females to selectively range in particular areas of the territory. We also show that close kin (i.e. mother–daughter and sibling dyads) are very rare, indicating that the vast majority of female dyads that form strong social bonds are not closely related. Additional analyses reveal that “subgroups” of females, consisting of individuals who frequently associate with one another in similar areas of the territory, do not consist of relatives. This suggests that a passive form of kin‐biased dispersal, involving the differential migration of females from neighboring communities into subgroups, was also unlikely to be occurring. These results show that, as in males, kinship plays a limited role in structuring the intrasexual social relationships of female chimpanzees. Am. J. Primatol. 71:840–851, 2009. © 2009 Wiley‐Liss, 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.