Infant handling in bonobos (Pan paniscus): Exploring functional hypotheses and the relationship to oxytocin.

Infant handling describes interactions between infants and non-maternal group members and is widespread across mammalian taxa. The expression of infant handling behaviors, defined as any affiliative or agonistic interaction between a group member and an infant, varies considerably among primate species. Several functional hypotheses may explain the adaptive value of infant handling including the Kin Selection hypothesis, which describes handling as a mechanism through which indirect fitness is increased and predicts a bias in handling behaviors directed toward related (genetic) infants; the Alliance Formation hypothesis, which describes handling as a social commodity and predicts females with infants will support handlers during conflict; and the Learning-to-Mother hypothesis, which describes handling as a mechanism through which handlers learn species-specific maternal behaviors and predicts that handling will occur most frequently in immature and nulliparous females. Using behavioral observation and data on urinary oxytocin, a neuropeptide hormone known to modulate maternal care and social bonds in mammals, the purpose of this study was to describe the pattern of infant handling in bonobos (Pan paniscus) and to explore proposed functional hypotheses. Data show that related infant-handler dyads occurred significantly more frequently than unrelated infant-handler dyads during some of the study period and that handling was positively correlated with support during conflict. Data also showed that immature and nulliparous females handled infants significantly more than other age-sex categories and exhibited higher post handling oxytocin values than other age-sex class. The trends identified in this data set provide insight into the role oxytocin may play in facilitating care-giving behaviors in young female bonobos and help to narrow the focus of future research efforts, particularly those associated with the Kin Selection, Alliance Formation, and Learning-to-Mother functional hypotheses.

Laterality of Grooming and Tool Use in a Group of Captive Bonobos (Pan paniscus).

Humans exhibit population level handedness for the right hand; however, the evolution of this behavioral phenotype is poorly understood. Here, we compared the laterality of a simple task (grooming) and a complex task (tool use) to investigate whether increasing task difficulty elicited individual hand preference among a group of captive bonobos (Pan paniscus). Subjects were 17 bonobos housed at the Columbus Zoo and Aquarium. Laterality of grooming was recorded using group scans; tool use was recorded using all-occurrence sampling. Grooming was characterized as unimanual or bimanual, and both tasks were scored as right-handed or left-handed. Most individuals did not exhibit significant hand preference for unimanual or bimanual (asymmetrical hand use) grooming, although 1 individual was lateralized for each. For the 8 subjects who engaged in termite fishing enough for statistical testing, 7 individuals exhibited significant laterality and strong individual hand preference. Four subjects preferred their left hand, 3 preferred their right, and 1 had no preference. Grooming, a simple behavior, was not lateralized in this group, yet a more complex behavior revealed a strong individual hand preference, and these results are congruent with other recent findings that demonstrate complex tasks elicit hand preference in bonobos.

Hair plucking, stress, and urinary cortisol among captive bonobos (Pan paniscus).

Hair plucking has been observed in many captive primate species, including the great apes; however, the etiology of this behavioral pattern is poorly understood. While this behavior has not been reported in wild apes, an ethologically identical behavior in humans, known as trichotillomania, is linked to chronic psychosocial stress and is a predominantly female disorder. This study examines hair plucking (defined here as a rapid jerking away of the hair shaft and follicle by the hand or mouth, often accompanied by inspection and consumption of the hair shaft and follicle) in a captive group of bonobos (N = 13) at the Columbus Zoo and Aquarium in Columbus, Ohio. Plucking data were collected using behavior and all-occurrence sampling; 1,450 social and self-directed grooming bouts were recorded during 128 hr of observation. Twenty-one percent of all grooming bouts involved at least one instance of plucking. Urine samples (N = 55) were collected and analyzed for the stress hormone cortisol. Analyses of urinary cortisol levels showed a significant positive correlation between mean cortisol and self-directed plucking for females (r = 0.88, P < 0.05) but not for males (r = -0.73, P = 0.09). These results demonstrate an association between relative self-directed hair plucking and cortisol among female bonobos. This is the first study to investigate the relationship between hair plucking and cortisol among apes. Overall, these data add to our knowledge of a contemporary issue in captive ape management. Zoo Biol. 35:415-422, 2016. © Wiley Periodicals, Inc.

A survey of bonobo (Pan paniscus) oral contraceptive pill use in North American zoos.

Contraception is an essential tool in reproductive management of captive species. The Association of Zoos and Aquariums (AZA) Reproductive Management Center (RMC) gathers data on contraception use and provides recommendations. Although apes have been given oral contraceptive pills (OCPs) for at least 30 years, there have been no published reports with basic information on why the pill is administered, formulations and brands used, and effects on physiology and behavior. Here, we report survey results characterizing OCP use in bonobos (Pan paniscus) housed in North American zoos, as well as information accumulated in the RMC's Contraception Database. Of 26 females treated, there have been no failures and nine reversals. The most commonly administered OCP formulation in bonobos contained ethinyl estradiol (EE) 35 µg/norethindrone 1 mg. Few females on combined oral contraceptives (COCs) were given a continuous active pill regimen; a hormone-free interval of at least 5 days was allowed in most. Crushing the pill and mixing with juice or food was common. Females on COCs seldom experienced breakthrough estrus or bleeding, while these conditions were sometimes observed for females on continuous COCs. All females on COCs exhibited some degree of perineal swelling, with a mean score of 3 or 3+ most commonly reported. Behavioral changes included less sexual behavior, dominant females becoming subordinate, and a negative effect on mood. No appreciable change in weight was noted. Taken together, these results indicate that OCPs are an effective and reversible contraceptive option for bonobos that can be used by zoos and sanctuaries to limit reproduction. Zoo Biol. 35:444-453, 2016. © Wiley Periodicals, Inc.

Sex differences in tool use acquisition in bonobos (Pan paniscus).

All the great ape species are known tool users in both the wild and captivity, although there is great variation in ability and behavioral repertoire. Differences in tool use acquisition between chimpanzees and gorillas have been attributed to differing levels of social tolerance as a result of differences in social structure. Chimpanzees also show sex differences in acquisition and both chimpanzees and bonobos demonstrate a female bias in tool use behaviors. Studies of acquisition are limited in the wild and between species comparisons are complicated in captivity by contexts that often do not reflect natural conditions. Here we investigated tool use acquisition in a captive group of naïve bonobos by simulating naturalistic conditions. We constructed an artificial termite mound fashioned after those that occur in the wild and tested individuals within a social group context. We found sex differences in latencies to attempt and to succeed where females attempted to fish, were successful more quickly, and fished more frequently than males. We compared our results to those reported for chimpanzees and gorillas. Males across all three species did not differ in latency to attempt or to succeed. In contrast, bonobo and chimpanzee females succeeded more quickly than did female gorillas. Female bonobos and female chimpanzees did not differ in either latency to attempt or to succeed. We tested the social tolerance hypothesis by investigating the relationship between tool behaviors and number of neighbors present. We also compared these results to those reported for chimpanzees and gorillas and found that bonobos had the fewest numbers of neighbors present. The results of this study do not support the association between number of neighbors and tool behavior reported for chimpanzees. However, bonobos demonstrated a similar sex difference in tool use acquisition, supporting the hypothesis of a female bias in tool use in Pan.