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.     

Variation and context of yawns in captive chimpanzees (Pan troglodytes)

Primate yawns are usually categorized according to context (e.g. as a threat, anxious, or rest yawn), but there has been little consideration of whether these yawns are best regarded as a unitary behavior that only differs with respect to the context in which it is observed. This study examined the context and precise morphology of yawns in a group of 11 captive chimpanzees. Focal video sampling was used to describe the morphology and intensity of 124 yawns using ChimpFACS, a system for coding facial movements. Two distinct forms of yawn were identified, a full yawn and a yawn which is modified by additional actions that reduce the mouth aperture. These modified yawns may indicate some degree of voluntary control over facial movement in chimpanzees and, consequently, multiple functions of yawning according to context. To assess context effects, mean activity levels (resting, locomotion, and grooming) and scratching rates were compared one minute before and after each yawn. Locomotion was significantly increased following both types of yawn, whereas scratching rates significantly increased following modified yawns but decreased following full yawns. In terms of individual differences, males did not yawn more than females, although male yawns were of higher intensity, both in the degree of mouth opening and in the amount of associated head movement. These data indicate that yawning is associated with a change in activity levels in chimpanzees, but only modified yawns may be related to increased arousal. Different types of yawn can therefore be differentiated at the morphological level as well as context level. Am. J. Primatol. 72:262–269, 2010. © 2009 Wiley‐Liss, Inc.     

Diagnosis and prevalence of uterine leiomyomata in female chimpanzees (Pan troglodytes)

Uterine leiomyomata are common, affecting 70-80% of women between 30 and 50 years of age. Leiomyomata have been reported for a variety of primate species, although prevalence rates and treatments have not been widely reported. The prevalence, diagnosis, and treatment of uterine leiomyomata in the Alamogordo Primate Facility and the Keeling Center for Comparative Medicine and Research were examined. Uterine leiomyomata were diagnosed in 28.4% of chimpanzees with an average age at diagnosis of 30.4 ± 8.0 years. Advanced age (>30 years) was related to an increase in leiomyomata and use of hormonal contraception was related to a decrease in leiomyomata. As the captive chimpanzee population ages, the incidence of leiomyomata among female chimpanzees will likely increase. The introduction of progesterone-based contraception for nonbreeding research and zoological chimpanzees may reduce the development of leiomyomata. Finally, all chimpanzee facilities should institute aggressive screening programs and carefully consider treatment plans.     

Bed-building in captive chimpanzees (Pan troglodytes): the importance of early rearing

In the wild, great apes sleep in beds they make by successively bending branches into an interwoven platform. These beds are functionally more closely related to human beds than they are to the nests and tree-holes used by other primate species. The idea that bed-building by great apes is learned behavior that is dependent on appropriate early experiences has been proposed but never fully tested. In the present study this hypothesis was indirectly tested in 73 captive adult chimpanzees (Pan troglodytes; 27 wild-born and 46 captive-born). Bed-building and use were tested experimentally by the introduction of three sets of bedding materials. Over 200 hr of scan-sampling data were collected during 45-min observations following introduction of the bedding material. The wild-born subjects built and used beds significantly more often than the captive-born subjects. Also, wild-born subjects used more complex techniques during construction. Captive-born subjects that were mother-reared through early adolescence spent more time building and using beds than their nursery-reared counterparts. These differences remained consistent even when previous adult experience with bedding (measured as naturalistic vs. traditional housing) was accounted for. These results suggest that bed-building is a learned behavior that requires early experience and practice for acquisition.     

Synchrony of estrous swelling in captive group-living chimpanzees (Pan troglodytes)

Recent findings suggest that menstrual synchrony may occur in humans and is more dependent on factors of close personal association than simple prox imity. Part I of this study analyzed the estrous cycles of 10 captive group living chimpanzees (Pan troglodytes) housed in two separate groups in the same building. Each group contained at least one male. The mean discrepan cies for (1) the approximate day of ovulation (last day of maximum swelling) and (2) the day of onset of estrous swelling were determined for all possible pairs within groups and compared to the mean discrepancies of pairs between groups. With respect to the probable day of ovulation, the mean discrepancy of animals caged together was 8.0 days and that of animals caged separately was 10. 7 days. Comparing the onset of estrous swelling, the mean between groups was 10.4 days, whereas females caged together averaged only 5.7 days. A repeated-measures analysis of variance indicated a significant group effect in the onset of estrous swelling (F = 5.68,p < 0.05), whereas there was no significant difference between the animals caged together and those caged separately with respect to the last day of maximum swelling (F = 1.37, NS). Part II of the study compared the onset of the first postpar tum estrus (PPE) to the onset of estrus in cagemates. During a 6-year period, 13 females exhibited 33 PPEs while in social contact with cycling females. Of 86 paired comparisons, the PPE onset of 43 (50%) occurred with in 6 days of the swelling onset of a cagemate. The results suggest that, as in other species (including humans), the social contact and time spent together influence the synchrony of chimpanzee estrous cycles, especially in terms of swelling onset. The synchrony of estrous swelling and possible mediation by olfactory and/or hormonal cues are discussed as they relate to chimpanzee social structure and female reproductive strategy.     

Social behavior and genital swelling in pregnant chimpanzees (Pan troglodytes)

Previous reports of increased sexual activity associated with genital swelling during chimpanzee pregnancy have suggested that the tumescent pregnant female may be regarded as a regularly cycling estrous female. Analysis of additional data from seven pregnant and eight cycling females, however, indicated that tumescent pregnant females differed from cycling females in some social interactions with males. As in earlier reports, pregnant females were more receptive to male-initiated copulatory bouts. In addition, pregnant females initiated grooming bouts with males much less frequently than did cycling females, and males spent less time grooming and less frequently inspected the genitals of pregnant than cycling cagemates. This tendency to decrease social interaction during pregnancy is consistent with field reports that pregnant chimpanzees prefer the company of their offspring and other noncycling females. In addition, the genital swelling patterns of 40 chimpanzee pregnancies were analyzed. Length of gestation averaged 231.5 days. Although a high degree of individual variation existed, females were swollen an average of 41% of the days observed, yet reached maximum swelling only 8.7% of the time. Genital swelling was less frequent during the third trimester, averaging 50.5, 47.9, and 22.6% tumescent days in each trimester. Young pregnant females showed maximum swelling more often than did older females. This finding is discussed with respect to field reports of intercommunity transfer of young, tumescent female chimpanzees.     

Characterization of cerebrospinal fluid monoamine metabolites in peripubertal chimpanzees (Pan troglodytes)

Background  Assessment of cerebrospinal (CSF) monoamine metabolites 5-hydroxyindoeacetic acid (5-HIAA) and homovanillic acid (HVA), and the serotonin precursor tryptophan (TRP), in chimpanzees may help in understanding the neurobiology underlying aggressive, impulsive behavior in humans and non-human primates.
Methods  Two CSF samples were obtained from 11 peripubertal chimpanzees 8 months apart and were assayed for monoamine metabolite and TRP concentrations.
Results  Substantial inter-individual stability was observed for 5-HIAA (n = 11; r = 0.83, P  <   0.001) and HVA (r = 0.91, P  <   0.001). Females had significantly higher concentrations of 5-HIAA compared to males (F_1,8 = 7.31; P  <   0.05). Levels of 5-HIAA (r = −0.62, P  <   0.05), HVA (r = −0.86, P  <   0.001) and TRP levels (r = −0.67; P  <   0.05) decreased with age.
Conclusion  Close parallels were observed between chimpanzees and humans with respect to absolute levels, sex effects, ontogeny, and 5-HIAA-HVA correlations, supporting the potential utility of the measures in understanding relationships between monoamine functioning and behavior in chimpanzees and humans.     

Characterization of 15 single nucleotide polymorphism markers for chimpanzees (Pan troglodytes)

We report the characterization of 15 new single nucleotide polymorphism markers for a threatened species, the chimpanzee (Pan troglodytes), developed using a targeted gene approach. These markers are derived from the Y chromosome and autosomal regions of the genome and show frequency differences between chimpanzee subspecies from central and western Africa. These single nucleotide polymorphism markers are the first to be designed for the genotyping of wild chimpanzee populations and will provide a useful addition to the genetic tools employed for the conservation management of this threatened species.     

Effects of aging on hematology and serum clinical chemistry in chimpanzees (Pan troglodytes)

A number of age-related changes in physiological functions have been identified in macaques and humans. However, few studies have examined physiological aging in chimpanzees, despite the increasing age of the chimpanzee population. We documented age-related changes in seven hematology and 17 clinical chemistry parameters in 49 adult chimpanzees (17 males, 32 females) as a comparative viewpoint with human and macaque aging. Longitudinal data were analyzed using weighted linear and quadratic mixed effects regression models. Male chimpanzees exhibited a significant age-related increase in anemia risk, based on significant decreases in hemoglobin (F(1,49)=12.45, P=0.0009) and hematocrit (F(1,49)=15.42, P=0.0003). Both sexes exhibited significant age-related decreases in both kidney and liver function. Decreases in kidney function were noted by significant increases in blood urea nitrogen (F(1,45)=3.92, P=0.036) and creatinine (F(1,50)=5.63, P=0.022) as well as changes in electrolyte (i.e., sodium, potassium, phosphorous, chloride) balance. Declining liver function was based on significant increases in globulin (F(1,46)=32.34, P<0.0001) and decreases in albumin (F(1,48)=23.42, P<0.0001). These changes were most evident beginning at 25-30 years of age in males and 30-35 years of age in females. We recommend amending chimpanzee age classes to categorize males over 25 years and females over 30 years as aged.     

Maternal age, parity, and reproductive outcome in captive chimpanzees (Pan troglodytes)

As early as the 1970s, it was suggested that nonhuman primates may serve as models of human reproductive senescence. In the present study, the reproductive outcomes of 1,255 pregnancies in captive chimpanzees (Pan troglodytes) were examined in relation to parity and its covariate, maternal age. The results show that the percentage of positive pregnancy outcomes was negatively correlated with increasing parity. In addition, spontaneous abortions, stillbirths, and caesarian sections (C-sections) were positively correlated with increasing parity. Maternal age, rather than parity, was found to be the most important predictor of negative birth outcome. This study supports research demonstrating reproductive decline and termination in nonhuman primates, and is the first to quantitatively account for this phenomenon in captive female chimpanzees.     

The implementation and initial evaluation of a physical therapy program for captive chimpanzees (Pan troglodytes)

Due to advances in captive nonhuman primate (NHP) medical care, the number of geriatric chimpanzees (≥35-years old) is growing. With old age comes a variety of physical conditions, including arthritis, stroke, and mobility impairments. Programs aimed at enhancing the welfare of geriatric chimpanzees are now quite common, but there are few published empirical evaluations of the efficacy of such programs. The current study aimed to create, implement, and evaluate the effects of participation in a physical therapy (PT) program on physical health, mobility, welfare, and behavior. Nine chimpanzees with mobility impairments participated in personalized PT routines (using positive reinforcement training) twice per week for 5 months. Additionally, nine control chimpanzees (non-mobility-impaired, matched with PT chimpanzees on age and gender) participated in body exam behavior sessions (also using positive reinforcement training) twice per week. All chimpanzees were rated on 14 health, well-being, and behavior items, as well as level of mobility throughout the PT program. Chimpanzees that participated in the PT program showed significant increases in ratings of physical health, well-being, and activity levels across phases of the program. Furthermore, compared to control chimpanzees, PT chimpanzees showed significant increases in ratings of ease of movement. Because raters were not blind to physical therapy treatment, our results represent an initial evaluation of the program that may suggest that participation in the PT program has physical, behavioral, and welfare benefits. Assessments of novel geriatric-focused care strategies and programs are essential to further enhance the welfare of the captive chimpanzee population, which is currently comprised of many geriatric animals, whose proportion of the captive population will only increase.     

Validation and utility of a body condition scoring system for chimpanzees (Pan troglodytes)

Obesity is a problem in captive chimpanzee colonies that can lead to increased risk for disease; therefore, implementation of effective weight management strategies is imperative. To properly implement a weight management program, captive managers should be able to noninvasively identify and assess overweight or obese individuals. Traditional means of categorizing obese individuals involve sedating the animals to obtain body weights or skin fold measurements. The current study aimed to validate a noninvasive, subjective body condition score (BCS) system for captive chimpanzees. The system utilizes a 10-point scale, with one rated as “emaciated,” five as “normal,” and 10 as “extremely obese.” Between 2013 and 2014, 158 chimpanzees were weighed and scored using this system (a) while sedated and (b) while awake in their social group within 1–3 days of sedation (“In-group” ratings). We found high inter-rater reliability between In-group raters, as well as between sedated and In-group scores. BCSs, which require observation only, were significantly positively correlated with weight (an objective measure of obesity often requiring anesthetization), supporting the scale's validity. The BCS system identified 36 individuals as “overweight,” while the use of weights alone identified only 26 individuals as “overweight.” Furthermore, the BCS system was able to classify individuals of the same sex and weight as having different BCSs, ranging from normal to overweight. Lastly, using focal animal behavioral observations from 2016 to 2018 (N = 120), we found that In-group BCS predicted individual levels of inactive behavior more than 2 years later, demonstrating the predictive validity of the scale. These results illustrate the utility of the BCS system as a noninvasive, reliable, and valid technique that may be more sensitive than traditional methods in identifying and quantifying obesity in chimpanzees. This system can be a useful tool for captive managers to monitor and manage the weight of chimpanzees and other nonhuman primates.     

Focal epithelial hyperplasia of the oral mucosa in two chimpanzees (Pan troglodytes)

Papillomas in the oral mucosa compatible with focal epithelial hyperplasia are reported in two chimpanzees. The lesions were studied by light and electron microscopy. Virus particles were not observed. The literature dealing with focal epithelial hyperplasia in humans and other animals is reviewed.     

The influence of AVPR1A genotype on individual differences in behaviors during a mirror self‐recognition task in chimpanzees (Pan troglodytes)

The mark/rouge test has been used to assess mirror self‐recognition (MSR) in many species. Despite consistent evidence of MSR in great apes, genetic or non‐genetic factors may account for the individual differences in behavioral responses that have been reported. We examined whether vasopressin receptor gene (AVPR1A) polymorphisms are associated with MSR‐related behaviors in chimpanzees since vasopressin has been implicated in the development and evolution of complex social relations and cognition and chimpanzees are polymorphic for the presence of the RS3‐containing DupB region. We compared a sample of DupB+/? and DupB?/? chimpanzees on a mark test to assess its role on social behavior toward a mirror. Chimpanzees were administered two, 10‐min sessions where frequencies of mirror‐guided self‐directed behaviors, contingent actions and other social behaviors were recorded. Approximately one‐third showed evidence of MSR and these individuals exhibited more mirror‐guided self‐exploratory behaviors and mouth contingent actions than chimpanzees not classified as passers. Moreover, DupB+/? males exhibited more scratching and agonistic behaviors than other male and female cohorts. Our findings support previous studies demonstrating individual differences in MSR abilities in chimpanzees and suggest that AVPR1A partly explains individual differences in MSR by influencing the behavioral reactions of chimpanzees in front of a mirror.     

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.     

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.     

Army ant prey availability and consumption by chimpanzees (Pan troglodytes vellerosus) at Gashaka (Nigeria)

Army ant predation by chimpanzees has been studied as an intriguing example of tool use and a possible case of cultural variation. However, the importance of army ant prey in chimpanzee diet and feeding ecology is still only poorly understood. We studied the availability and consumption of army ants in a population of the chimpanzee subspecies Pan troglodytes vellerosus in Nigeria. Army ants were collected from nests and trails (workers) and near artificial light sources (males). Three potential prey species were found: Dorylus rufescens, Dorylus gerstaeckeri and Dorylus kohli . Dorylus rufescens was by far more abundant than the other two species. Only remains from D. rufescens were present in chimpanzee faeces. This is the first report of consumption of this ant species by chimpanzees. However, because of the low availability of the other two species, it is unclear whether this pattern reflects a preference for D. rufescens . Although D. rufescens ' availability varied with weather conditions, the occurrence as well as the absolute and relative numbers of Dorylus fragments in faeces did not. This finding, together with the considerable difficulties encountered by human observers in their efforts to locate nests by following trails, suggests that the chimpanzees in this population do not harvest army ants from trails and do not use trails to locate nests. The overall occurrence of army ant fragments in 42.3% of all faecal samples is the highest ever recorded in any chimpanzee population. This indicates that in this chimpanzee population, army ant prey is not a fallback during periods of sparse availability of plant food, but quantitatively important throughout the year. Future studies will be needed to clarify which cues and strategies chimpanzees use to locate army ant nests and to assess the role of myrmecophagy with respect to macro- or micronutrient demands.     

Acute appendicitis in a chimpanzee (Pan troglodytes)

BACKGROUND: A 7-year old, female chimpanzee (Pan troglodytes) developed acute abdominal pain and anorexia. An irregular, mineral opacity was identified in the caudal right quadrant of the abdomen on radiographs and computed tomography scan, which appeared to be in the region of the cecal appendage. RESULTS AND CONCLUSIONS: A diagnosis of acute appendicitis was made based on clinical signs, abnormal haematology findings, and consultation with a human radiologist. Exploratory laparotomy was performed and the cecal appendage was removed. On histologic examination, the mucosal epithelium contained eosinophilic and neutrophilic inflammation. The inflammation extended through the tunica muscularis to the serosal surface and adjacent mesentery. The histologic findings were consistent with acute appendicitis in humans. The chimpanzee recovered well from surgery with immediate improvement in clinical signs and no post-operative complications.     

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.