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.     

Social behavior of a group of orangutans (Pongo pygmaeus) on an artificial island in Singapore Zoological Gardens

The behavior of 12 orangutans (three adult males, two adult females, two subadult males, three adolescent males, and two infant males) was observed on a 450-m² island at the Singapore Zoological Gardens (SZG). Male orangutans (6–18 years old) showed less social and solitary play as they aged; adults (over 16 years old) were not seen to play. As they grew older males increasingly spent less time making physical contact, but the amount of time they spent in proximity (within arm's length) to others increased. Adult females regularly played with other group members. Contact, allogrooming, and social play showed nonrandom relationships between individuals. Adult females showed the most allogrooming and contact, adolescent and subadult males the most play. There was no obvious dominance hierarchy. One adult male spent about 10% of his time walking around the perimeter of the island. One-year-old infants rarely interacted with other individuals apart from their own and the other infant's mother. While orangutans lead relatively solitary lives in nature, it was concluded that the opportunities for social contact and play provided by the SZG orangutan island were beneficial to this species in captivity. Opportunities for social interaction provided the animals with a means of increasing the stimulus component of their environment, thus compensating for the inevitable restriction of complexity and unpredictability as compared with the wild state.     

Play behaviour and its effects on social development of common chimpanzees (Pan troglodytes)

The aim of the study was to monitor the social development of infant and juvenile common chimpanzees (Pan troglodytes) through their play behaviour at Taronga Zoo in Sydney in order to examine the possible effects of captivity (such as limited opportunities to play) on social development. Play behaviour was observed by focal animal sampling to determine individual differences, and their relationship to age, sex, and relatedness of the subjects. Analysis revealed marked individual variations in social, solitary, and object play behaviours indicative of a relatively well-balanced social and physical environment. Subjects showed a marked preference for play-partners of a different age compared to their own, and initiated interactions with similar frequency with members of both sexes. Many social-play dyads consisted of related individuals, and familiarity with prospective play-mates was the most decisive factor in social interactions.     

Food Neophobia and Social Learning Opportunities in Great Apes

Finding food resources and maintaining a balanced diet are major concerns for all animals. A compromise between neophobia and neophilia is hypothesised to enable animals to enlarge their diet while limiting the risk of poisoning. However, little is known about how primates respond to novel food items and whether their use is socially transmitted. By comparing how four different species of great apes respond to novel food items, we investigated how differences in physiology (digestive tract size and microbial content), habitats (predictability of food availability), and social systems (group size and composition) affect their response toward novelty. We presented two familiar foods, one novel fruit, four novel aromatic plants from herbal medicine, and kaolin to captive chimpanzees (Pan troglodytes), western gorillas (Gorilla gorilla), Bornean orangutans (Pongo pygmaeus) and Sumatran orangutans (Pongo abelii). We recorded smelling, approach-taste delays, ingestion, interindividual observations, and food transfers with continuous sampling. We found that behaviors differed between the apes: chimpanzees were the most cautious species and observed their conspecifics handling the items more frequently than the other apes. Close observations and food transfers were extremely rare in gorillas in comparison to orangutans and chimpanzees. We suggest that a low neophobia level reflects an adaptive response to digestive physiological features in gorillas and to unpredictable food availability in orangutans. Social interactions appeared to be predominant in chimpanzees and in both orangutan species to overcome food neophobia. They reflect higher social tolerance and more opportunities for social learning and cultural transmission in a feeding context.     

The mitochondrial DNA molecule of sumatran orangutan and a molecular proposal for two (Bornean and Sumatran) species of orangutan

The complete mitochondrial DNA (mtDNA) molecule of Sumatran orangutan, plus the complete mitochondrial control region of another Sumatran specimen and the control regions and five protein-coding genes of two specimens of Bornean orangutan were sequenced and compared with a previously reported complete mtDNA of Bornean orangutan. The two orangutans are presently separated at the subspecies level. Comparison with five different species pairs—namely, harbor seal/grey seal, horse/donkey, fin whale/blue whale, common chimpanzee/pygmy chimpanzee, and Homo/common chimpanzee—showed that the molecular difference between Sumatran and Bornean orangutan is much greater than that between the seals, and greater than that between the two chimpanzees, but similar to that between the horse and the donkey and the fin and blue whales. Considering their limited morphological distinction the comparison revealed unexpectedly great molecular difference between the two orangutans. The nucleotide difference between the orangutans is about 75% of that between Homo and the common chimpanzee, whereas the amino acid difference exceeds that between Homo and the common chimpanzee. On the basis of their molecular distinction we propose that the two orangutans should be recognized as different species, Pongo pygmaeus, Bornean orangutan, and P. abelii, Sumatran orangutan. Received: 15 May 1996 / Accepted: 21 June 1996     

The development of wild immature Sumatran orangutans (Pongo abelii) at Ketambe

Orangutans have the longest immature period and inter-birth interval of all ape species. This may be explained by a slow life history, the need to develop skills or by their relatively solitary lifestyle, which prevents a mother from associating with two offspring. This study of wild immature orangutans at the Ketambe Research Station, Indonesia, describes, with partly cross-sectional, partly longitudinal data, their development to independence. The study subjects ranged from 1 to 11 years of age. Data on their activity budget, diet, mother–offspring proximity and maintenance of proximity, association with conspecifics and play behavior were collected. The results indicate that immature orangutans can provide for their own food and transport, and therefore were independent of direct maternal care, at an age of possibly 3 but more clearly 6 years. This is similar to chimpanzees, and refutes the slow life history hypothesis. Immature orangutans remain within their mother’s vicinity until the age of 8 years, indicating a dependence on indirect maternal care, and this coincides with the period during which the mother does not produce another offspring. A female orangutan seems unable to associate with an older immature while caring for a new infant. This is consistent with the solitary-lifestyle hypothesis and corroborates the results obtained with the Sumatran orangutan population at Suaq Balimbing. However, why an immature depends indirectly on its mother for such a long period remains unclear. It is possible that it needs to develop ecological or social skills or needs the protection of its mother. Unfortunately, no data were available to distinguish between these possibilities.     

The Right Time to Happen: Play Developmental Divergence in the Two Pan Species

Bonobos, compared to chimpanzees, are highly motivated to play as adults. Therefore, it is interesting to compare the two species at earlier developmental stages to determine how and when these differences arise. We measured and compared some play parameters between the two species including frequency, number of partners (solitary, dyadic, and polyadic play), session length, and escalation into overt aggression. Since solitary play has a role in developing cognitive and physical skills, it is not surprising that chimpanzees and bonobos share similar developmental trajectories in the motivation to engage in this activity. The striking divergence in play developmental pathways emerged for social play. Infants of the two species showed comparable social play levels, which began to diverge during the juvenile period, a ‘timing hotspot’ for play development. Compared to chimpanzees, social play sessions in juvenile bonobos escalated less frequently into overt aggression, lasted longer, and frequently involved more than two partners concurrently (polyadic play). In this view, play fighting in juvenile bonobos seems to maintain a cooperative mood, whereas in juvenile chimpanzees it acquires more competitive elements. The retention of juvenile traits into adulthood typical of bonobos can be due to a developmental delay in social inhibition. Our findings show that the divergence of play ontogenetic pathways between the two Pan species and the relative emergence of play neotenic traits in bonobos can be detected before individuals reach sexual maturity. The high play motivation showed by adult bonobos compared to chimpanzees is probably the result of a long developmental process, rooted in the delicate transitional phase, which leads subjects from infancy to juvenility.     

Cyclic development of contact behavior in apes and humans

Nursing and mother-infant distance were observed in three orangutans, two gorillas, one chimpanzee and four humans. All four species showed periods of a recurrence of greater time spent nursing and in contact with the mother. The initial regressive or reattachment period occurred similarly in all four species at between 6–12 months of age. An orangutan observed for two years showed a second period at 19–21 months. Other studies of weight gain in the three ape species coincidently peaked at the same time. When estimated peaks of individuals of each species were summed, the resulting graphs showed a differentiation of species rates of development. Gorillas developed most rapidly, orangutans developed most slowly, while chimpanzees and humans developed within the middle range.     

Knuckle-walking and the evolution of hominoid hands

Knuckle-walking is a pattern of digitigrade locomotion unique to African apes among Primates. Only chimpanzees and gorillas are specially adapted for supporting weight on the dorsal aspects of middle phalanges of flexed hand digits II–V. When forced to the ground, most orangutans assume one of a variety of flexed hand postures, but they cannot knuckle-walk. Some orangutans place their hands in palmigrade postures which are impossible to African apes. The knuckle-walking hands and plantigrade feet of African apes are both morphologically and adaptively distinct from those of Pongo, their nearest relative among extant apes. These features are associated with a common adaptive shift to terrestrial locomotion and support placing chimpanzees and gorillas in the same genus Pan. It is further suggested than Pan comprises the subgenera (a) Pan, including P. troglodytes and pygmy chimpanzees, and (b) Gorilla, including mountain and lowland populations of P. gorilla. African apes probably diverged from ancestral pongids that were specially adapted for distributing their weight in terminal branches of the forest canopy. Early adjustments to terrestrial locomotion may have involved fist-walking which later evolved into knuckle-walking. Orangutans continued to adapt to feeding and locomotion in the forest canopy and their hands and feet became highly specialized for four-digit prehension. Although chimpanzees retained arboreal feeding and nesting habits, they moved from tree to tree by terrestrial routes and became less restricted in habitat. While adapting to a diet of ground plants gorillas increased in size to the point that arboreal nesting is less frequent among them than among chimpanzees and orangutans. Early hominids probably diverged from pongids that had not developed prospective adaptations to knuckle-walking, and therefore did not evolve through a knuckle-walking stage. Initial adjustments to terrestrial quadrupedal locomotion and resting stance probably included palmigrade hand posturing. Their thumbs may have been already well developed as an adaptation for grasping during arboreal climbing. A combination of selection pressures for efficient terrestrial locomotor support and for object manipulation further advanced early hominid hands toward modern human configuration.     

Sexual Differences in Chimpanzee Sociality

Scientists usually attribute sexual differences in sociality to sex-specific dispersal patterns and the availability of kin within the social group. In most primates, the dispersing sex, which has fewer kin around, is the less social sex. Chimpanzees fit well into the pattern, with highly social philopatric males and generally solitary dispersing females. However, researchers in West Africa have long suggested that female chimpanzees can be highly social. We investigated whether chimpanzees in the Taï Forest (Côte d’Ivoire) exhibit the expected sexual differences in 3 social parameters: dyadic association, party composition, and grooming interactions. Though we found a significant sexual difference in each of the 3 parameters, with males being more social than females, the actual values do not reveal striking differences between the sexes and do not support the notion of female chimpanzees as asocial: females had dyadic association indices comparable to mixed-sex dyads, spent ca. 82% of their time together with other adult chimpanzees, and had a comparable number of grooming partners. Further, female associations can be among the strongest bonds within the community, indicating that both sexes can have strongly favored association partners. The findings are in contrast to reports on East African chimpanzees, the females of which are mainly solitary and rarely interact with other females. Our results suggest that researchers cannot generally regard chimpanzee females as asocial and need to redefine models deriving patterns of sociality from dispersal patterns to integrate the possibility of high female sociality in male philopatric systems.     

Behavioral, Ecological, and Evolutionary Aspects of Meat-Eating by Sumatran Orangutans (Pongo abelii)

Meat-eating is an important aspect of human evolution, but how meat became a substantial component of the human diet is still poorly understood. Meat-eating in our closest relatives, the great apes, may provide insight into the emergence of this trait, but most existing data are for chimpanzees. We report 3 rare cases of meat-eating of slow lorises, Nycticebus coucang, by 1 Sumatran orangutan mother–infant dyad in Ketambe, Indonesia, to examine how orangutans find slow lorises and share meat. We combine these 3 cases with 2 previous ones to test the hypothesis that slow loris captures by orangutans are seasonal and dependent on fruit availability. We also provide the first (to our knowledge) quantitative data and high-definition video recordings of meat chewing rates by great apes, which we use to estimate the minimum time necessary for a female Australopithecus africanus to reach its daily energy requirements when feeding partially on raw meat. Captures seemed to be opportunistic but orangutans may have used olfactory cues to detect the prey. The mother often rejected meat sharing requests and only the infant initiated meat sharing. Slow loris captures occurred only during low ripe fruit availability, suggesting that meat may represent a filler fallback food for orangutans. Orangutans ate meat more than twice as slowly as chimpanzees (Pan troglodytes), suggesting that group living may function as a meat intake accelerator in hominoids. Using orangutan data as a model, time spent chewing per day would not require an excessive amount of time for our social ancestors (australopithecines and hominids), as long as meat represented no more than a quarter of their diet.     

Development of ecological competence in Sumatran orangutans

Data on orangutans (Pongo pygmaeus abelii) living in a Sumatran swamp forest yield an estimated median interbirth interval of at least 8 years, concurring with findings from other sites. This longest known mammalian interbirth interval appears due to maternal amenorrhea during the long exclusive dependence of the offspring. We describe the development of various components of offspring independence. In this arboreal ape, 3‐year‐olds had largely reached locomotor independence. Nest‐building skills were also well‐developed in 3‐year‐olds, but immatures shared their mother's nest until weaned at around age 7. At time of birth of the new sibling, association with the mother had begun to decline for both male and female offspring, suggesting that the immatures had mastered all the necessary skills, including basic tool use, to feed themselves. By about 11 years of age, they also ranged independently from the mother. These results show that orangutans do not develop independence more slowly than chimpanzees. Why, then, is weaning 2 years later in orangutans? In chimpanzees, mothers are often accompanied by two or even three consecutive offspring, unlike in orangutans. This contrast suggests that an orangutan mother cannot give birth until the previous offspring is ecologically competent enough to begin to range independently of her, probably due to the high energy costs of association. Thus, the exceptionally long interbirth intervals of orangutans may be a consequence of their solitary lifestyle. Am J Phys Anthropol, 2004. © 2004 Wiley‐Liss, Inc.     

Chimpanzees Cope with Temporary Reduction of Escape Opportunities

Many studies have focused on the responses of primates to changes in population density, but little is known about the responses to more subtle changes in the physical environment. Studies on primate responses to high density supported the use of various coping strategies depending on the circumstances. We investigated which strategy was adopted by a large group of captive chimpanzees in response to a special case of space restriction: the temporary reduction of escape opportunities. Due to work on the outdoor enclosure, the chimpanzees at Chester Zoological Gardens were confined to their indoor quarters for 1 mo. As it was winter, the chimpanzees spent most of their time indoors also during the 7-week control period, but had the option to go outside. Therefore, there was no major difference in the actual density between the two conditions, but by being confined indoors the chimpanzees had reduced escape opportunities. Under this condition they would be expected not to alter their behavior dramatically but to adjust it in ways to avoid conflict and to reduce tension. The chimpanzees did not change their overall aggression rates during the period with a reduction of escape opportunities versus the control period. The patterns of allogrooming and submissive greetings also did not differ between the two periods. However, they appeared to refrain from joining ongoing aggressive interactions during the period with reduced escape opportunities, whereas no change in counteraggression occurred between the two periods. Our findings suggest that the chimpanzees may adopt a selective inhibition strategy when escape opportunities are limited. Further support for such selectivity comes from the analysis of different types of aggressor-target dyads. During the period with reduced escape opportunities, aggression rates decreased in dyads characterized by high aggression rates at baseline, i.e., high aggressor-target dyads, whereas the same individuals did not change their aggressive tendencies in low aggressor-target dyads. Ours is among the few studies showing a decrease, albeit selective, in aggressive behavior during a situation of space restriction. The ability to rapidly adopt an appropriate strategy and to inhibit aggression during such restriction seems to confirm findings of chimpanzees under high density conditions. The inhibition of aggressive tendency may be especially developed in chimpanzees and may be related to the natural challenges posed by the routine changes in subgroup membership characteristic of their fission-fusion social organization.     

Orangutan use of vertical space in an innovative habitat

This study measured use of vertical space in an innovative habitat for three adolescent orangutans (Pongo pygmaeus). The indoor habitat was innovative in two main ways: a flooded floor and retractable skylights. It included four large molded trees and interwoven vines throughout 1,620 m³ of space. The exhibit was divided into four vertical levels: skylights, upper canopy, lower canopy, and flooded floor. Five trained observers made instantaneous scans of the exhibit every 5 minutes, in 1‐hour blocks of time over a 10‐month period, logging 180 hours of observations. One location (of 55) and one behavior (of 53) were noted at each interval. Behaviors were collapsed to form five categories: solitary inactivity, solitary activity, social inactivity, social activity, and eating/drinking. Results showed the orangutans favored the upper canopy, which contained many tree limbs for sitting and reclining. The orangutans next favored the lower canopy and the skylights, especially those skylights that were out of public view. The habitat’s flooded floor was avoided (they used it just 1% of the time), as planned by the exhibit designers who intended to showcase these arboreal primates in trees, not on the ground. When compared with wild orangutans, we considered few of their behaviors to be atypical: foraging/eating plastic (vines) and stereotyped behaviors. Overall, the unique design of the habitat provided opportunities for a range of species‐typical behaviors, varying by vertical level, demonstrating the importance of providing sufficient vertical space for orangutans. Zoo Biol 19:239–251, 2000. © 2000 Wiley‐Liss, Inc.     

Play behavior in immature moor macaques (Macaca maura) and Japanese macaques (Macaca fuscata)

Play is widespread across mammalian taxa, but species strongly vary in the ways they play. In less despotic primate species (i.e., with less steep dominance hierarchies, less severe conflicts, and more reconciliation), play has been described as being more frequent, cooperative, and freely expressed. To study the link between social play and dominance style, we compared play behavior in free-ranging infants, juveniles and subadults of more despotic Japanese macaques (Macaca fuscata, N = 24) and less despotic moor macaques (Macaca maura, N = 17). We found interspecific differences in play behavior that corresponded with the contrasting dominance styles of the study species, largely confirming our predictions. In particular, moor macaques spent a larger proportion of time in solitary and social play than Japanese macaques, while Japanese macaques spent a larger proportion of time in grooming interactions. In moor macaques, play sessions included more players, a larger variety of play behaviors, greater play face rates, a greater proportion of time in contact play, and a higher rate of reciprocal play-biting than in Japanese macaques. Aggressive escalations were not common, but more frequent in Japanese macaques. Finally, a higher frequency of play faces during play sessions predicted the occurrence of more reciprocal play-bites, but not the proportion of time spent in contact play behaviors. Additional studies on other groups and species will allow a better understanding of the link between dominance style and social play.     

Orangutans (Pongo pygmaeus) do not form expectations based on their partner's outcomes

Several primate species form expectations based on others' outcomes, responding negatively when their outcomes differ from their partners'. The function and evolutionary pathway of this behavior are unknown, in part because all of the species which have been tested thus far share traits related to a gregarious lifestyle, intelligence, and cooperativeness. Our goal was to test whether inequity is a homology among primates or a convergence by comparing one species known to show social comparisons, the chimpanzee, to another great ape which differs on several of these life history characteristics. Using a protocol identical to one used previously with chimpanzees, we tested whether orangutans, an intelligent but predominantly solitary species with few opportunities to cooperate, responded similarly. To allow for a strong comparison with chimpanzees (and other species), we used socially housed adults of both sexes, tested with members of their social group. Orangutans did not respond negatively to inequity, supporting previous findings and indicating that inequity responses in apes are likely a convergence based on either sociality or cooperative tendency. These results in such closely related species highlight the need for additional comparative studies to understand better the function and evolution of social behaviors.     

Social behavior of captive,group-living Orangutans

The behavior of orang-utans (Pongo pygmaeus)was observed in two captive groups (one adult group, one juvenile group). Activity profiles,animal interactions, and compartmental spatial use for both adult-group and juvenile-group individuals were recorded over a 9-month period. Behavioral repertoires for both groups included large amounts of social activity. Equivalent amounts of social activity were found for each group. The social behavior of juvenile animals involved more active behavior such as play. The social behavior of the adult animals was more subtle, involving social monitoring and allogrooming. These results indicate that orangutans, at least when group-living in captivity, exhibit the potential to display social behavior which is apparently of greater frequency and complexity than that which has been observed in the wild. These findings suggest that the solitary behavior of wild orangutans is not a necessary characteristic of orangutan behavior. Under different environmental conditions orangutans appear to readily adapt socially, and, like other nonhuman primates,they have the capacity to exhibit complex and subtle social behavior. This report is based on part of a senior thesis submitted by Sara D. Edwards     

Calculated reciprocity? A comparative test with six primate species

Little evidence of calculated reciprocity has been found in non-human primates so far. In this study, we used a simple experimental set-up to test whether partners pulled a sliding table to altruistically provide food to each other in short-term interactions. We tested 46 dyads of chimpanzees, bonobos, gorillas, orangutans, brown capuchin monkeys and spider monkeys to examine whether a subject’s tendency to provide food to a partner was directly affected by the partner’s previous behaviour, by the species, by the condition (i.e., whether the partner could access the food provided by the subject) and by the social tolerance levels within each dyad. Chimpanzees and orangutans were the only species pulling significantly more when the partner could retrieve the food altruistically provided. However, no species reciprocated food exchanges, as subjects’ probability to pull was not affected by the previous number of the partner’s pulls, with the possible exception of one orangutan dyad. Although subjects clearly knew how the apparatus worked and easily obtained food for themselves, individuals did not usually take the opportunity to provide food to their partners, suggesting that calculated reciprocity is not a common behaviour and that food exchanges are usually not reciprocated in the short-term within dyads.     

Insect-eating by sympatric Lowland gorillas (Gorilla g. gorilla) and chimpanzees (Pan t. troglodytes) in the Lopé Reserve,Gabon

Sympatric populations of lowland gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes troglodytes) in the Lopé Reserve in central Gabon consumed insects at similar average frequencies over a 7-year period (30% versus 31% feces contained insect remains). Data came mostly from fecal analysis supplemented by observation and trail evidence. The weaver ant (Oecophylla longinoda) was the species eaten most frequently by both gorillas and chimpanzees. Other species of insects wore eaten but there was virtually no overlap: Chimpanzees used tools to eat Apis bees (and their honey) and two large species of ants; gorillas ate three species of small ants. Thus, despite their shared habitat, the esources utilized were not identical as gorillas do not show the tool-use “technology” of chimpanzees. The frequency of insect-eating by both species of ape varied seasonally and between years but in different ways. This variation did not seem to be related to the ratio of fruit to foliage in their diets. Gorillas of all age-classes ate insects at similar rates. Comparisons with insectivory by other populations of gorillas indicate differences exist. Mountain gorillas (Gorilla g. beringei) in the Virunga Volcanoes, Rwanda, consume thousands of invertebrates daily, eating them inadvertently with handfuls of herbaceous foods but they deliberately ingest insect-foods only rarely. Lowland gorillas at Lopé habitually ate social insects, and their selective processing of herbaceous foods probably minimizes inadvertent consumption of other invertebrates. Gorillas at Belinga in northeastern Gabon, 250 km from Lop6, ate social insects at similar rates but ignored weaver ants in favor of Cubitermes sulcifrons, a small species of termite that occurs at Lopé but was not eaten by gorillas. This indicates that local traditions similar to those reported for chimpanzees also exist amongst populations of gorillas. © 1992 Wiley-Liss, Inc.