Twin rearing is rare in chimpanzees and thus, very few studies have investigated how twin chimpanzees are reared in their communities. To our knowledge, this is the first study to provide quantitative data on parenting behaviors by a mother chimpanzee and adult group members toward infant twins.

Rearing twins would be difficult for chimpanzees because of the heavier parenting burden on mothers. In fact, reports of successful twin rearing by chimpanzees are scarce. We hypothesized that alloparents, who share the burden of parenting, would be necessary for successful rearing of twins.

In the captive community of chimpanzees at the Noichi Zoological Park, we found that parenting behaviors were observed in not only the mother of the twins, but also the adult group members. In the case of Daiya—the male twin—mother Sango and father Robin were particularly engaged in parenting. The aspects of their parenting behaviors, however, were different. Sango was engaged in all four kinds of parenting behavior, while Robin was primarily engaged in physical contact and walking together. This suggests that parenting responsibilities were divided between Robin and Sango. While Sango provided essential care for Daiya's survival (e.g., infant carriage), Robin and Daiya were often engaged in play. The physical contact and walking together by Robin toward Daiya might have been facilitated by the types of social play common in chimpanzees such as “play bite” and “play run”14. However, the observation of play between the infant male chimpanzee and the adult male was unremarkable. According to Lansdorf et al.15, infant male chimpanzees in the Gombe National Park were engaged in social interaction with adult males to a greater extent than infant female chimpanzees. This suggests that the preference for adult males is a general trait among infant male chimpanzees. Thus, the parenting of Daiya by Sango and Robin would be considered normal chimpanzee behavior.

In the case of Sakura, the female twin, not only Sango, but also Cherry and Koyuki were engaged in parenting. Interestingly, these three adult female chimpanzees provided all four kinds of parenting behavior. This indicates that adult females (Cherry and Koyuki) provided the same care as the mother, suggesting that they were alloparents of Sakura. Perhaps such alloparenting by Cherry and Koyuki reduced the burden of parenting for Sango, thus facilitating successful twin rearing by Sango.

Previous studies have reported cases of alloparenting in chimpanzees. Most were the cases of adoption, in which alloparenting was conducted by adults other than mothers after the mother had died. Boesch, Bole, Eckhardt and Boesch16 reported that not only kin female adults but also non-kin adults adopted orphaned infants and provided essential care for the infants' survival, such as food sharing or infant carriage. On the other hand, Wroblewski17 reported a case of adoption of an infant by his grandmother when the mother was alive. This was the first report of chimpanzee adoption from a living mother. These examples suggest that most alloparenting behaviors toward infants were conducted after the infants' mothers had died. The parenting behaviors of other adults are rare when mothers are still alive. Furthermore, such examples have been limited to care by kindred adults. Unlike the findings of these previous studies, our study represents the first example where an infant was cared for by non-kin adults while the infants' mother was still alive.

Why did female adults, such as Cherry and Koyuki, care for Sakura despite there being no kinship between them? One possibility is that alloparenting toward infants by non-kin adults is altruistic behavior toward the mothers of the infants. Stanford18 reported that female capped langurs (Prebytis pileatus) often provide care for non-kin infants. He suggested that these allomothering behaviors by females might have adaptive altruistic behavior among group females, in that it enables lactating females to increase the feeding time. Our results, however, did not support this idea because of the following points. If the allomothering behaviors in this study represented altruistic behavior from Cherry or Koyuki toward Sango, a long-lasting relationship must have existed between them such that the altruistic behaviors would be rewarded in the form of returned altruistic behavior from the recipient19. However, we found no significant relation between each adult's parenting behavior occurrence rates toward Sakura and the index of intimacy between Sango and each adult as measured by the proximity rate between Sango and each adult. Additionally, the focal adult who provided the most care for Sakura was Cherry, who was one of Sango's non-affiliated adults. These results suggest that the alloparenting behavior toward Sakura by other adult group members was not due to the bonding between Sango and the adults, suggesting that the altruistic rewards from Sango toward the adults were unlikely to occur.

Another hypothesis is that Sakura herself built social relationships with Cherry and Koyuki and thus procured parenting behaviors from them. This idea was supported by our results. First, the occurrence rate of parenting behaviors toward Sakura from focal adults besides Sango were positively correlated with the index of intimacy between Sakura and each adult, which was measured by the proximity rate between Sakura and each adult. This suggests that Sakura was provided care by adults who were familiar with her. Second, Sakura was close to Cherry—one of her alloparents—at a higher rate when Sango was not close to them. This suggests that when Sakura was free from Sango, she would move toward Cherry. Thus, Sakura independently built her own altruistic relationships with group adults, including Cherry, who were unfamiliar with Sango. In some primate species, whether infants build their own altruistic relationships or remain close to their mothers depends on their mothers' rearing style (so-called “maternal style”). In Japanese macaques (Macaca fuscata), infants are often handled by adults other than mothers when the mothers of the infants are not protective20,21. Such infants do not make physical contact with their mothers or are not groomed by their mothers; thus, these infants are handled by adults attracted by them20. This relation between maternal style and the frequency of infants being handled by adults other than the mothers was observed in not only macaques but also chimpanzees. According to Hemelrijk and de Kogel22, chimpanzee infants whose mothers often broke contact spent more time in social play with others and less time in contact with their mothers. In our study, Sakura (30.10%) was close to her mother Sango at a slightly lower rate than was Daiya (38.22%). This would be because those infants were twins and could not be cared for equally by Sango and Sango cared for Daiya on a priority basis. Consequently, Sakura would be slightly less close to her mother, leading her to come free, as was observed by Hemelrijk and de Kogel22. Sango's inability to provide equal care might have made Sakura more sociable.

Some questions remain unresolved by the present study. First, we could not entirely reveal why adults other than Sango provided care for Sakura. Previous experimental studies have indicated that chimpanzees do not take care of others' welfare23. Thus, it is puzzling that other adults would have engaged in taxing parenting behaviors (e.g., infant carriage). This question could be answered, at least in part, by the communication between Sakura and alloparents. We observed not only adult-initiated communication, which was also observed by Hirata24, but also infant-initiated communication before infant carriage. We observed that Sakura dragged Cherry or Chelsea before she climbed upon their backs, as if she had requested carriage from them (Figures 5 and 6). Yamamoto, Humle and Tanaka25 revealed that chimpanzees help others when the recipients express their requests by reaching toward what they want. This suggests that chimpanzees help others when others express their needs by gestures. Sakura's pulling of Cherry or Chelsea would facilitate their understanding of Sakura's requests and accordingly, they provided care for her. Interestingly, infant-initiated communication, such as dragging adults, was not observed between Sakura and her mother. Moreover, Daiya was never engaged in such communicative behavior toward Sango. Such infant-initiated gestures are possibly only necessary when infants request parenting from adults other than their mothers. Human infants who are unable to express their requests using speech typically use pointing gestures to not only mothers but also other adults (e.g., nursery staff26). Taken together, the gestural expressions of requests by infants would be important for both species in procuring alloparental care from adults.

Another question that remained unaddressed was the benefit of becoming an alloparent. What benefit would alloparents such as Cherry and Koyuki derive from their altruistic care for Sakura? Perhaps those alloparents would derive benefit as Sakura grows older. Thus, longitudinal observations are necessary to reveal any potential benefits for these alloparents.

In conclusion, this is the first study suggesting that alloparenting from adults other than mothers would contribute to the successful rearing of twins in captive chimpanzees. We also suggested that infants' departing from mothers and gesturing their own requests would make non-kin adults provide care for the infants. Our results provide some insight into why humans give birth in short calving intervals and how institutions of human alloparenting (e.g., nursery school) originated.