Adult Chimpanzees Research Articles

Effects of sex and early rearing condition on adult behavior, health, and well-being in captive chimpanzees (Pan troglodytes)

Scientific evaluation of management strategies for captive species is part of the establishment of best practices for animal welfare. Here we report the effects of sex, rearing, and a sex-by-rearing interaction on adult, captive chimpanzees’ (Pan troglodytes) behavior, health, well-being, personality, and orientation towards humans based on multiple methods (observation, animal records, and surveys). Chimpanzees raised in three conditions, mother-reared (MR), standard nursery (ST) and an experimental nursery (RC), were assessed approximately 20 years after their differential rearing experiences concluded. Sex had a significant effect on behavior towards conspecifics (aggression [M > F]; affiliation [F > M]), on abnormal behavior (rocking [M > F]), and on likelihood of incurring at least one injury (between ages 6 and 10 [M > F]). Rearing condition had a significant impact on behavior towards humans (negative solicitation [RC = ST > MR = ST]; neutral behavior [RC > ST > MR], yawning (RC = ST > MR = ST), subjective well-being (MR = ST > RC = ST), and on GI illness frequency (RC > ST = MR). Sex interacted with rearing on aggression towards humans (for males, RC > MR = ST), frequency of upper respiratory infection (URI: for males RC > MR = ST)) and likelihood of at least one URI between the ages of 11 and 15 (RC males > ST males). Our findings support the conclusion that there are long-term effects of both early rearing and sex on captive adult chimpanzee welfare.

Adult chimps are less consoling

Adult chimpanzees are less likely than young ones to console companions in times of distress. The finding raises questions about how the capacity for empathy changes with age in people's closest relatives--and them. When a chimpanzee gets upset, companions often sit with them and offer reassurance by kissing, grooming or embracing them. They know chimpanzees have personalities: lasting individual features in their behavior. But it was unclear whether their empathetic tendencies are part of their personality, and whether they change over time. Christine Webb at Emory University in Atlanta, Georgia, and her colleagues studied eight years of observations of a group of 44 chimpanzees at Yerkes National Primate Research Center.

Natural pathology of the captive chimpanzee (Pan troglodytes): A 35-year review.

We present the spontaneous pathological lesions identified as a result of necropsy or biopsy for 245 chimpanzees (Pan troglodytes) over a 35-year period. A review of the pathology database was performed for all diagnoses on chimpanzees from 1980 to 2014. All morphologic diagnoses, associated system, organ, etiology, and demographic information were reviewed and analyzed. Cardiomyopathy was the most frequent lesion observed followed by hemosiderosis, hyperplasia, nematodiasis, edema, and hemorrhage. The most frequently affected systems were the gastrointestinal, cardiovascular, urogenital, respiratory, and lymphatic/hematopoietic systems. The most common etiology was undetermined, followed by degenerative, physiologic, neoplastic, parasitic, and bacterial. Perinatal and infant animals were mostly affected by physiologic etiologies and chimpanzee-induced trauma. Bacterial and physiologic etiologies were more common in juvenile animals. Degenerative and physiologic (and neoplastic in geriatric animals) etiologies predominated in adult, middle aged, and geriatric chimpanzees.

Extraction of honey from underground bee nests by central African chimpanzees (Pan troglodytes troglodytes) in Loango National Park, Gabon: Techniques and individual differences.

A detailed analysis of tool use behaviors can disclose the underlying cognitive traits of the users. We investigated the technique used by wild chimpanzees to extract the underground nests of stingless bees (Meliplebeia lendliana), which represent a hard-to-reach resource given their highly undetectable location. Using remote-sensor camera trap footage, we analyzed 151 visits to 50 different bee nests by 18 adult chimpanzees of both sexes. We quantified the degree of complexity and flexibility of this technique by looking at the behavioral repertoire and at its structural organization. We used Generalized Linear Mixed Models to test whether individuals differed in their action repertoire sizes and in their action sequencing patterns, as well as in their preferences of use of different behavioral elements (namely, actions, and grip types). We found that subjects showed non-randomly organized sequences of actions and that the occurrence of certain actions was predicted by the type of the previous action in the sequences. Subjects did not differ in their repertoire sizes, and all used extractive actions involving tools more often than manual digging. As for the type of grip employed, the grip involving the coordinated use of hands and feet together was most frequently used by all subjects when perforating, and we detected significant individual preferences in this domain. Overall, we describe a highly complex and flexible extractive technique, and propose the existence of inter-individual variation in it. We discuss our results in the light of the evolution of higher cognitive abilities in the human lineage.

Natural mortality and cause of death analysis of the captive chimpanzee (Pan troglodytes): A 35-year review.

We present the spontaneous causes of mortality for 137 chimpanzees (Pan troglodytes) over a 35-year period. A record review of the pathology database was performed and a primary cause of mortality was determined for each chimpanzee. The most common causes of mortality were as follows: cardiomyopathy (40% of all mortalities), stillbirth/abortion, acute myocardial necrosis, chimpanzee-induced trauma, amyloidosis, and pneumonia. Five morphologic diagnoses accounted for 61% of mortalities: cardiomyopathy, hemorrhage, acute myocardial necrosis, amyloidosis, and pneumonia. The most common etiologies were degenerative, undetermined, bacterial, traumatic, and neoplastic. The cardiovascular system was most frequently involved, followed by the gastrointestinal, respiratory, and multisystemic diseases. Degenerative diseases were the primary etiological cause of mortality of the adult captive chimpanzee population. Chimpanzee-induced trauma was the major etiological cause of mortality among the perinatal and infant population. This information should be a useful resource for veterinarians and researchers working with chimpanzees.

Feeding in fear? How adult male western chimpanzees (Pan troglodytes verus) adjust to predation and savanna habitat pressures.

We evaluated risk-sensitive foraging in adult male western chimpanzees (Pan troglodytes verus) occupying a savanna environment at Fongoli, Senegal. The aim of this study was to determine how the risks of predation and heat stress influenced their behavior while feeding on a key food, fruit of the baobab tree (Adansonia digitata). Proximity of fruiting baobab trees to anthropogenic landmarks were compared to food intake, feeding rate, and behavioral indicators of fear in adult males (N = 11) at Fongoli. Additionally, we compared foraging to vegetative habitats, baobab ripe fruit nutritive quality, surface water availability, and foraging party composition. Fruit abundance increased with proximity to anthropogenic landmarks, and chimpanzees exhibited higher frequencies of antipredator behaviors as they approached these risky areas. However, predation risk did not deter adult males from visiting these fruiting trees; instead, risky foraging bouts were associated with higher food intakes and longer feeding times. Additionally, higher feeding rates were observed in open-canopy habitats, and this behavior may have minimized their risk of heat stress. Adaptations that minimize predation risk are widespread in mammalian prey species, but these traits are poorly understood in chimpanzees. Great apes encounter few nonhuman predators capable of successfully capturing and killing them; thus, such events are rarely observed. Although people rarely hunt chimpanzees in Senegal, we found that adult males perceived humans as predators and adjusted their behavior while foraging in risky habitats. From an applied perspective, risk-taking behavior is important for understanding and mitigating the problem of crop-feeding in locations where chimpanzees and humans live in sympatry.

Morphology of the lingual papillae in the chimpanzee.

We microscopically examined the dorsal lingual surface of an adult chimpanzee (Pan troglodytes). The tongue of the chimpanzee was about 13 cm long. Filiform papillae were distributed over the entire dorsal surface of the lingual body. There were many fungiform papillae scattered among the filiform papillae. At the posterior end of the lingual body, a triangular arrangement of the vallate papillae, with the apex of the triangle directed posteriorly, was observed. The filiform papillae on the lingual apex consisted of a main papilla and secondary papillae. The filiform papillae on the lingual body had several pointed processes. There were dome-shaped fungiform papillae scattered among the filiform papillae. The vallate papillae were surrounded by grooves and were flattened-oval shaped. Many foliate papillae were observed on the posterolateral regions of the tongue.

Perception of motion trajectories of objects from moving cast shadows in human (Homo sapiens) infants, Japanese macaque (Macaca fuscata) infants, and an adult chimpanzee (Pan troglodytes)(Summary of Awarded Presentations at the 24th Annual Meeting)

Perception of motion trajectories of objects from moving cast shadows in human (Homo sapiens) infants, Japanese macaque (Macaca fuscata) infants, and an adult chimpanzee (Pan troglodytes)(Summary of Awarded Presentations at the 24th Annual Meeting)

Mother–infant interactions in captive and wild chimpanzees

We review studies on mother–infant interactions in chimpanzees, our closest living relatives, in captive and wild environments. Infant cognitive development is formed through mother–infant interactions during the long dependent period, which is approximately 5 years. Patterns of interaction between mothers and infants are different from those observed in adult chimpanzees. Mother–infant interactions are relatively altruistic, although solicitation by infants is almost always required. Active teaching has rarely been reported in chimpanzees; instead, infants socially learn new skills through long-term observation. Case studies describing rearing of a disabled infant by a multiparous but inexperienced chimpanzee, and the carrying of dead infants in the wild chimpanzees of Bossou reveal the strong affectionate bond between mothers and infants. Characteristics of human mother–infant interaction are highlighted through comparisons with chimpanzees.

Feeding Consequences of Hand and Foot Disability in Wild Adult Chimpanzees (Pan troglodytes schweinfurthii)

Many wild primates experience long-term limb disability, and their ability to cope with disability has implications for survival and fitness. We quantified the arboreal feeding and postural behaviors of adult chimpanzees to study the consequences of physical limb disabilities. We collected behavioral data for a total of 8 mo on chimpanzees at Sebitoli, Kibale National Park, Uganda, focusing on the time spent feeding, common feeding tree species, body postures, and substrate use. Of the 51 chimpanzees we observed, 16 (31%) exhibited limb anomalies, which varied in form and severity. Disabled chimpanzees climbed as high as chimpanzees without disabilities and did not differ from nondisabled chimpanzees in the amount they used feeding tree species. Adult chimpanzees with severe hand disability spent significantly more time feeding than nondisabled individuals. In addition, manually disabled adults did not suspend themselves from branches during feeding as frequently as nondisabled adults and used larger substrates for gripping and sitting than nondisabled adults. These results indicate that disabled individuals compensate to carry out feeding activities in trees.

Fecal carbon and nitrogen isotopic analysis as an indicator of diet in Kanyawara chimpanzees, Kibale National Park, Uganda.

The shorter-term overview from feces provides scope to investigate dietary fluctuations. We assess the correlation of stable isotopic fecal values with recorded seasonal diet of 10 adult chimpanzees (P. t. schweinfurthii) of the Kanyawara community (Kibale National Park, Uganda) and whether fecal nitrogen levels (%N) indicate a change in crude protein intake. We recorded food eaten by each ape and collected both concurrent fecal samples (N = 115) and plant foods eaten by this community (N = 64). We compared fecal δ13 C and δ15 N values (also %N) with: (a) plant values; (b) feeding data; and (c) food-items found macroscopically in the fecal samples. Interspecies and intraspecies differences in plant and fecal isotope values (and %N) as well as seasonality in diet were determined using parametric and nonparametric tests. No difference in plant δ13 C and δ15 N values was found at intraspecies or interspecies level. Fecal isotope values reflected a diet of C3 plants from evergreen forest vegetation. Seasonal differences in δ13 C and δ15 N corresponded with aspects of feeding and fecal macroscopic data, but only at community level. A change in crude protein intake was not indicated from %N content. This study further validates the use of staple isotope analyses of primate feces to provide a dietary overview, revealing seasonal differences at community level; however, conclusive results may be limited for individuals when using short sampling periods. Further study of variables that influence fecal %N content is also suggested to interpret crude protein intake.

Sex Differences in Age-Related Decline of Urinary Insulin-Like Growth Factor-Binding Protein-3 Levels in Adult Bonobos and Chimpanzees.

There is increasing interest in the characterization of normative senescence in humans. To assess to what extent aging patterns in humans are unique, comparative data from closely related species, such as non-human primates, can be very useful. Here, we use data from bonobos and chimpanzees, two closely related species that share a common ancestor with humans, to explore physiological markers that are indicative of aging processes. Many studies on aging in humans focus on the somatotropic axis, consisting of growth hormone (GH), insulin-like growth factors (IGFs), and IGF binding proteins (IGFBPs). In humans, IGFBP-3 levels decline steadily with increasing age. We used urinary IGFBP-3 levels as an alternative endocrine marker for IGF-I to identify the temporal pattern known to be related with age-related changes in cell proliferation, growth, and apoptosis. We measured urinary IGFBP-3 levels in samples from 71 bonobos and 102 chimpanzees. Focusing on samples from individuals aged 10 years or older, we found that urinary IGFBP-3 levels decline in both ape species with increasing age. However, in both species, females start with higher urinary IGFBP-3 levels than males, experience a steeper decline with increasing age, and converge with male levels around the age of 30–35 years. Our measurements of urinary IGFBP-3 levels indicate that bonobos and chimpanzees mirror human patterns of age-related decline in IGFBP-3 in older individuals (<10 years) of both sexes. Moreover, such as humans, both ape species show sex-specific differences in IGFBP-3 levels with females having higher levels than males, a result that correlates with sex differences in life expectancy. Using changes in urinary IGFBP-3 levels as a proxy for changes in GH and IGF-I levels that mark age-related changes in cell proliferation, this approach provides an opportunity to investigate trade-offs in life-history strategies in cross-sectional and in longitudinal studies, both in captivity and in the wild.

Introducing tool-based feeders to zoo-housed chimpanzees as a cognitive challenge: spontaneous acquisition of new types of tool use and effects on behaviours and use of space

Cognitively challenging environments are vital to the welfare of captive animals. However, practical enrichment devices that can facilitate animals’ natural behaviours and accommodate individual variation are still limited. We created two types of feeders to facilitate tool-using behaviour in captive chimpanzees: pounding and dipping feeders. The pounding feeder was inspired by pestle-pounding behaviour observed in wild chimpanzees, and we expected that chimpanzees would pound soft foods. The dipping feeder was designed to stimulate actions similar to ant-dipping behaviours observed in wild chimpanzees. We investigated (1) how chimpanzees acquire tool-using behaviours and (2) the effects of the feeders on chimpanzee behaviour and use of space. The subjects were five chimpanzees housed in the Kyoto City Zoo, Japan. In study 1, conducted between March and May 2014, we introduced the feeders and examined the chimpanzees’ behaviours and the characteristics (length, width, etc.) of any tools they used. In study 2, conducted between September and October 2014, random days were designated when feeders were available (enriched condition) and not available (control condition). In study 1, all adult chimpanzees could use the dipping feeder, and two females could obtain foods from the pounding feeder by hitting the foods several times. The ability to acquire new tool-using behaviours was consistent with ability in existing tool-use behaviours. One infant started to use tools by trial and error. Study 2 showed that under the enriched condition, tool-using behaviours increased, stress-related behaviours decreased, and the use of space changed. These results suggest that these tool-based feeders provided an appropriate challenge for the chimpanzees.

Adolescent male chimpanzees do not form a dominance hierarchy with their peers.

Dominance hierarchies are a prominent feature of the lives of many primate species. These hierarchies have important fitness consequences, as high rank is often positively correlated with reproduction. Although adult male chimpanzees strive for status to gain fitness benefits, the development of dominance relationships is not well understood. While two prior studies found that adolescent males do not display dominance relationships with peers, additional research at Ngogo in Kibale National Park, Uganda, indicates that adolescents there form a linear dominance hierarchy. These conflicting findings could reflect different patterns of rank acquisition across sites. An alternate possibility arises from a recent re-evaluation of age estimates at Ngogo and suggests that the report describing decided dominance relationships between adolescent males may have been due to the accidental inclusion of young adult males in the sample. To investigate these issues, we conducted a study of 23 adolescent male chimpanzees of known age during 12months at Ngogo. Adolescent male chimpanzees exchanged pant grunts, a formal signal of submission, only 21 times. Recipients of pant grunts were late adolescent males, ranging between 14 and 16years old. In contrast, younger adolescent males never received pant grunts from other males. Aggression between adolescent males was also rare. Analysis of pant grunts and aggressive interactions did not produce a linear dominance hierarchy among adolescent males. These data indicate that adolescent male chimpanzees do not form decided dominance relationships with their peers and are consistent with the hypothesis that the hierarchy described previously at Ngogo resulted from inaccurate age estimates of male chimpanzees. Because dominance relationships develop before adulthood in other primates, our finding that adolescent male chimpanzees do not do so is surprising. We offer possible explanations for why this is the case and suggest future studies that may help clarify the matter.

Taï chimpanzees change their travel direction for rare feeding trees providing fatty fruits

The production of edible rainforest fruits is characterized by fluctuating and seasonal patterns that require frugivores to flexibly adjust their ranging behaviour. We investigated whether significant changes in a forager's travel direction can inform us about the importance of the nutritional and energetic aspects of different food sources for a wild animal's diet. We recorded the ranging patterns of five adult female chimpanzees, Pan troglodytes verus, for a total of 275 full days in the Tai National Park in Cote d’Ivoire and designed two models that predicted their directional changes at, and on the way to, fruit-bearing feeding trees. In both models, directional change was significantly influenced by the density of the feeding tree species and the crude fat content of that species' fruit. Female chimpanzees were more likely to change their travel direction for rarer trees, at which they fed on fruits that contained higher amounts of fat. In addition, directional changes tended to be positively influenced by the content of nonstructural (‘easy energy’) and structural carbohydrates (NDF) in that species' fruit. We did not detect any effect of sensory cues or social factors on the directional changes, in either model. The amount of fruit available and the time since the start of the fruiting season positively influenced directional change in the second model, which suggests that chimpanzees were updating their knowledge of the fruit availability in individual trees over time. Our results indicate that the nutrient content of fruit and its abundance exerted a significant impact on the shape of chimpanzee female travel paths, which opens up a new avenue for investigation of food preferences in wild animals through analyses of their ranging patterns.

A new method of walking rehabilitation using cognitive tasks in an adult chimpanzee (Pan troglodytes) with a disability: a case study

There are few studies of long-term care and rehabilitation of animals which acquired physical disabilities in captivity, despite their importance for welfare. An adult male chimpanzee named Reo at the Primate Research Institute of Kyoto University, developed acute myelitis, inflammation of the spinal cord, which resulted in impaired leg function. This report describes a walking rehabilitation system set up in a rehabilitation room where he lives. The rehabilitation apparatus consisted of a touch monitor presenting cognitive tasks and a feeder presenting food rewards at a distance of two meters from the monitor, to encourage him to walk between the monitor and the feeder repeatedly. Initially, Reo did not touch the monitor, therefore we needed adjustment of the apparatus and procedure. After the habituation to the monitor and cognitive tasks, he started to show behaviors of saving food rewards without walking, or stopping participation to the rehabilitation. Finally it took seven phases of the adjustment to determine the final setting; when the monitor automatically displayed trials in 4-h, AM (1000-1200hours) and PM (1400-1600hours) sessions through a day, Reo spontaneously walked from the monitor to the feeder to receive rewards, and returned to the monitor to perform the next trial. Comparison of Reo's locomotion in a no-task period and under the final setting revealed that the total travel distance increased from 136.7 to 506.3m, movement patterns became multiple, and the percentage of walking increased from 1.2 to 27.2% in PM session. The findings of this case study suggest that cognitive tasks may be a useful way to rehabilitate physically disabled chimpanzees, and thus improve their welfare in captivity.

Within arm's reach: Measuring forearm length to assess growth patterns in captive bonobos and chimpanzees.

Bonobos and chimpanzees are known to differ in various morphological traits, a dichotomy that is sometimes used as an analogy for evolutionary splits during human evolution. The aim of our study was to measure the forearm length of immature and adult bonobos and adult chimpanzees to assess the extent of age-related changes of forearm length in bonobos and sex-dimorphism in bonobos and chimpanzees. As a proxy of somatic growth we measured forearm length of captive bonobos and chimpanzees ranging in age from 1 to 55 years. Measures were taken from subjects inserting their arms into a transparent Plexiglas® tube, a novel technique facilitating repeated measures of nonanesthetized apes in captivity. Measures from adult females (>12 years) showed that bonobos exceed chimpanzees in terms of forearm length and that sexual dimorphism in forearm length is pronounced in chimpanzees, but not in bonobos. Forearm length increased significantly with chronological age in bonobos. Validation tests revealed that the device generates useful data on morphometric dimensions. In most primates, sexual dimorphism in body size is male-biased and the differences in forearm length in chimpanzees follow this trend. Given that males of the two species did not differ in forearm length, the absence/presence of sexual dimorphism of this trait must be due to differences in somatic growth in females. Our novel method offers an alternative to obtain morphometric measures and facilitates longitudinal studies on somatic growth. Am J Phys Anthropol 161:37-43, 2016. © 2016 Wiley Periodicals, Inc.

Long bone cross-sectional properties reflect changes in locomotor behavior in developing chimpanzees.

Recent studies indicate that the locomotor behavior of wild chimpanzees changes during development. Before transitioning to quadrupedal knuckle-walking in adulthood, young chimpanzees engage in a significant amount of upper limb loading suspensory behavior. We investigated whether these dramatic changes in locomotion influence the strength and shape of chimpanzee long bones. We examined changes in chimpanzee arboreal locomotion over the course of development using behavioral data collected on wild chimpanzees. We measured the midshaft geometric properties of femora and humeri of wild-caught individuals housed in museum collections using micro computed tomographic scans. Chimpanzees spent less time moving arboreally as they aged. Femoral/humeral strength ratios also increased with age, as predicted by the changing loading environment during development. Additional analyses revealed that femoral shape, but not humeral shape, varied across chimpanzee age classes. Adult femora were more elliptical compared with those of infants. This change in adult femora is consistent with the observation that adult chimpanzees spend most of their time moving terrestrially and consequently experience a less variable loading environment than do infants. Taken together, these findings contribute to our understanding of how ontogenetic changes in function affect form. As similar changes may have characterized the behavioral and skeletal ontogeny of extinct hominoids including hominins, these findings furnish a potential means to make inferences about the behavior of fossil taxa based on the structural properties of their bones.

Feeding habitat quality and behavioral trade-offs in chimpanzees: a case for species distribution models.

The distribution and abundance of food resources are among the most important factors that influence animal behavioral strategies. Yet, spatial variation in feeding habitat quality is often difficult to assess with traditional methods that rely on extrapolation from plot survey data or remote sensing. Here, we show that maximum entropy species distribution modeling can be used to successfully predict small-scale variation in the distribution of 24 important plant food species for chimpanzees at Gombe National Park, Tanzania. We combined model predictions with behavioral observations to quantify feeding habitat quality as the cumulative dietary proportion of the species predicted to occur in a given location. This measure exhibited considerable spatial heterogeneity with elevation and latitude, both within and across main habitat types. We used model results to assess individual variation in habitat selection among adult chimpanzees during a 10-year period, testing predictions about trade-offs between foraging and reproductive effort. We found that nonswollen females selected the highest-quality habitats compared with swollen females or males, in line with predictions based on their energetic needs. Swollen females appeared to compromise feeding in favor of mating opportunities, suggesting that females rather than males change their ranging patterns in search of mates. Males generally occupied feeding habitats of lower quality, which may exacerbate energetic challenges of aggression and territory defense. Finally, we documented an increase in feeding habitat quality with community residence time in both sexes during the dry season, suggesting an influence of familiarity on foraging decisions in a highly heterogeneous landscape.

Molecular identification of Oesophagostomum spp. from 'village' chimpanzees in Uganda and their phylogenetic relationship with those of other primates.

Oesophagostomum spp. are parasitic nematodes of mammals, including humans and other primates. To identify species and determine phylogeny, we analysed DNA sequences of adult and larval Oesophagostomum from wild chimpanzees in Bulindi, Uganda, which inhabit degraded forest fragments amid villages. Oesophagostome larvae and/or eggs from baboons in Tanzania and South Africa and from a Japanese macaque were also sequenced. Based on the internal transcribed spacer 2 (ITS2) of nuclear ribosomal DNA and partial cytochrome c oxidase subunit 1 gene (Cox1) of mtDNA, O. stephanostomum and O. bifurcum were identified from chimpanzees. Bulindi is the second locality where molecular detection of O. bifurcum in wild chimpanzees has been made. While most O. stephanostomum had ITS2 genotypes recorded previously, three new genotypes were detected. Among four ITS2 genotypes of O. bifurcum from chimpanzees, one was identical to that from various monkey species in Kibale, Uganda, and baboons from Tanzania and South Africa; another was shared by a baboon from Tanzania. No genotype was identical with that of the cryptic species reported from humans and monkeys in Kibale. Phylogeny based on Cox1 sequences of O. stephanostomum showed locality-dependent clades, whereas those of O. bifurcum formed clades composed of worms from different hosts and localities.