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.     

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.     

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.     

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.     

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.     

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.     

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.     

Behavioral responsiveness to strangers in young chimpanzees (Pan troglodytes)

Earlier studies of responses of primate infants to strangers were frequently confounded with separation from the attachment figure and/or removal to an unfamiliar setting. In the present study, young chimpanzees were tested in a familiar setting with a human female caretaker who served as an attachment figure. Two strangers were introduced: a human female, approximately the size of the caretaker, who refrained from initiating interactions and a larger human male, who repeatedly approached and initiated contact with the subjects. A somewhat more intense response was elicited by the larger, more assertive male stranger, but neither stranger elicited severe distress. The behavior of the chimpanzees is better described as wary, rather than fearful. These results may be attributable to the continued presence of the caretaker in contrast to previous studies reporting severe distress to strangers when chimpanzees are tested alone. A wariness of strangers in nursery-reared chimpanzees may develop by 6 months of age and may diminish somewhat by 2 years of age under the conditions of this study.     

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.     

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.     

Videotapes as enrichment for captive chimpanzees (Pan troglodytes)

The effectiveness of showing videotapes to captive chimpanzees as an environmental enrichment was quantitatively tested. The responses of 10 subjects (3 adult males and 7 adult females) to videotapes of chimpanzees engaging in a variety of behaviors, to videotapes of other animals and humans, and to television programs were compared. Data collection consisted of 20-minute, continuous sampling tests while various videotapes were shown. A total of 400 tests were conducted. Multivariate analysis of variance was applied to measure differences in the duration of eight categories of behavior across videotapes of varying content. No general behavioral differences in response to the tapes based on sex or housing were revealed. However, with the behavior of monitor-watching analyzed alone, we found that individually housed subjects watched the videotapes more than socially housed subjects. When viewing time was averaged across all videotapes, the chimpanzees watched the monitor a mean of 38.4% of the time available. The chimpanzees' behavior varied significantly only when they were watching the videotapes of various human and chimpanzee activities and not when watching a blank screen. A Pearson's correlation indicated that subjects habituated to repeated presentations of the videotapes, although the effect was small numerically. Although this type of enrichment did not extensively alter behavior, it did occupy a significant portion of the subjects' activity budget; thus, the amount of time spent watching the video stimuli indicated that videotapes may be a useful enrichment for captive chimpanzees. Zoo Biol 19:541-551, 2000. Copyright 2000 Wiley-Liss, Inc.     

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.     

Skeletal differences between pygmy (Pan paniscus) and common chimpanzees (Pan troglodytes)

Skeletal dimensions of pygmy (Pan paniscus) and common (Pan troglodytes) chimpanzees were compared. Significant differences were found in the clavicles, scapulae, pelvises, and in the humerus/femur and femur head/length ratios. No significant differences were observed in long bone lengths or talar breadths. There is extensive overlap in body weights, so that the observed differences cannot be accounted for by body size alone. We conclude that pygmy and common chimpanzees are morphologically distinct. Implications for hominoid evolution are discussed.     

Behavioral responsiveness of young chimpanzees (Pan troglodytes) to a novel environment

Behavioral responsiveness to a novel environment was documented in 22 chimpanzees grouped according to age; 6-months, 1-year, 2-years and 5-years. An attachment figure, a human caretaker, accompanied each subject during the 15-min test sessions so as to preclude confounding of responses to novelty with separation responses. Extreme distress reported previously for chimpanzees and human children when tested alone in a novel situation was rarely observed in these tests when an attachment figure was present. Stereotyped rocking, an indication of mild distress occurred more frequently in the younger animals. Younger animals engaged in distal visual exploration of the environment while remaining close to the attachment figure, whereas the older animals locomoted more frequently and explored the environment directly with their hands. Repeated exposure to the environment reduced the differences among the 6-month, 1-year and 2-year groups. The 6-month group, however, continued to locomote least and least frequently engaged in tactile exploration. These data on chimpanzees resemble data on human children which suggest that an attachment figure: attenuates the distress exhibited by young individuals of these species when exposed to novel stimuli, and thereby provides a secure base which supports the exploration of novel stimuli, a prerequisite to behavioral adaptation.     

Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes)

This study examined whether fecal cortisol could be used as an index of stress responses. The stress responsiveness of fecal cortisol was tested with a stressor known to stimulate adrenal activity, the stress of anesthesia. Daily fecal and urine samples were collected from four captive chimpanzees (Pan troglodytes) before and after anesthetizations with Telazol^®/Ketasat^®. Tests of assay validity indicated that cortisol was measurable in chimpanzee fecal extracts. Fecal cortisol concentrations were significantly elevated 2 days after anesthetization, with elevations in seven of the eight treatments. The posttreatment peak was significantly greater than baseline values in three of the four subjects. Both fecal concentrations and proportionate increases in response to stress were significantly correlated with the corresponding values in urinary cortisol, confirming the stressfulness of these procedures and the stress responsiveness of fecal cortisol. These findings provide evidence for the application of fecal cortisol as a noninvasive index of physiologic stress in nonhuman primates. Am. J. Primatol. 44:57–69, 1998. © 1998 Wiley-Liss, Inc.     

Genetic diversity of Y-specific STRs in chimpanzees (Pan troglodytes)

Using the primers described for humans, sequences for 11 Y-specific microsatellites (DYS434, DYS435, DYS436, DYS437, DYS438, DYS439, GATA A10, A7.1, A7.2, C4, and H4 [Gusm?o et al., in press]), previously described in 10 male chimpanzees (Pan troglodytes), were confirmed in nine additional male chimpanzees. Sequences for nine additional microsatellites (DYS19, DYS385I and II, DYS389I and II, DYS390, DYS391, DYS392, and DYS393) were determined in all 19 male chimpanzees; homology to human Y-Short Tandem Repeat (STRs) was confirmed by sequencing. Good amplification results were not obtained for DYS19 and DYS385I/II. Two amplicons were obtained for DYS389I/II, but in contrast to humans, the larger fragment was not Y-specific. Moreover, no polymorphism was observed for DYS434, DYS435, or GATA A10. Consequently, these eight STRs were eliminated from further analyses, and haplotype and allele frequencies were estimated for the remaining 12 STRs. A high haplotype diversity value was found (1.000 +/- 0.017), demonstrating the usefulness and informative power of these Y-STRs for future studies on chimpanzee population genetics.     

Possible roles of consolation in captive chimpanzees (Pan troglodytes)

Empathy is a necessary prerequisite for the occurrence of consolation. The term "consolation" contains a hypothesis about function, which is distress alleviation. The present study aims to confirm the occurrence of consolation in captive chimpanzees via the post-conflict/matched-control method (PC-MC) and to suggest its possible roles. We collected 273 PC-MC pairs in the group of Pan troglodytes housed in the ZooParc de Beauval (France). We confirmed the presence of consolatory contacts (mean level of consolation, 49.5% +/- 22.3% SEM) in the colony. Consolation rates were significantly higher than reconciliation levels (mean level of reconciliation, 28.9% +/- 16.8% SEM). The level of consolation was greater in the absence of reconciliation than in the presence of it, suggesting that consolation might be an alternative behavior. As friendship and relatedness did not influence the occurrence of consolation, they did not seem to be the best prerequisites for this behavioral mechanism, at least in this chimpanzee colony. Affinitive contacts with third parties were significantly more frequent when the victim called attention to itself during severe aggressions by screaming. These high-pitched sounds seem to be useful in eliciting aid from conspecifics, as occurs in young humans. The occurrence of consolation reduced the likelihood of further attacks among group-members. From this perspective, both victims and consolers most likely gain potential advantages by interacting with each other when aggression is particularly severe, reconciliation is not immediate, and consequently social stress reaches high levels.     

Morphometric variables related to metabolic profile in captive chimpanzees (Pan troglodytes)

Obesity is a risk factor for several diseases including type 2 diabetes and cardiovascular disease. The aim of this study was to compare the relationships of waist circumference and body weight with circulating markers of metabolic, cardiovascular, and hepatic function in chimpanzees (Pan troglodytes). After a 12-h fast, blood was collected from 39 adult captive chimpanzees for measurement of serum glucose, BUN, creatinine, albumin, cholesterol, ALT, AST, ALP, total and direct bilirubin, triglyceride, and insulin, and waist circumference and body weight were measured. Waist circumference was positively correlated with systolic and diastolic blood pressure, glucose, insulin resistance as estimated by the homeostatic model assessment method, and albumin in female chimpanzees and with triglyceride in female and male chimpanzees. Body weight was correlated significantly with systolic and diastolic blood pressure in female chimpanzees and triglyceride in male chimpanzees. Male chimpanzees were heavier and had lower diastolic blood pressure, greater creatinine, albumin, AST, ALP, total bilirubin, and direct bilirubin values than did female chimpanzees. The relationships between waist circumference and blood pressure and triglyceride are consistent with those reported in humans and other primate species. In conclusion, our study is the first work to demonstrate a relationship between waist circumference and metabolic risk factors in chimpanzees. Results demonstrated that waist circumference was associated with more metabolic risk factors than was body weight, particularly in female chimpanzees.