Alloparenting for chimpanzee twins

In April 2009, a female chimpanzee named Sango, living in a captive group at the Noichi Zoo, Japan, gave birth to dizygotic male-female twin chimpanzees (male: Daiya, female: Sakura). The extent to which adult group members cared for the twins was investigated using a focal animal sampling method targeting six adults (one male) when the twin chimpanzees were two years old. Data were collected for an average of 6.78 h (SD = 0.79) per focal participant. An unaffiliated female adult of Sango was engaged in parenting Sakura as much as Sango. Given that Sakura was in lesser proximity to Sango than Daiya, Sakura's departures from her mother and her ability to gesture requests might have enabled non-kin adults to provide her care.


Results
Parenting behavior among adult chimpanzees. Figure 2(a) shows the occurrence rates of parenting behavior of focal adults toward Daiya, the male twin. Sango had the highest parenting behavior rate of all adult chimpanzees and was engaged in all four kinds of parenting behaviors (walking together, infant carriage, grooming, and physical contact). Sango was the only adult who was observed carrying Daiya. Robin, the father of Daiya and one of Sango's affiliated adults, was also engaged in parenting, particularly in physical contact with Daiya. The other four female adults cared for Daiya at a lower rate than did Sango and Robin. Figure 2(b) shows the occurrence rate of parenting behavior of focal adults toward Sakura, the female twin. Unlike in the case of Daiya, Cherry, who was one of Sango's unaffiliated adults, was engaged in parenting Sakura for as much time as did Sango. Additionally, Sango, Cherry, and Koyuki (an adult affiliated to Sango) were engaged in all four kinds of parenting behavior. Moreover, besides Sango, three adult females (Koyuki, Cherry, and Chelsea) were found carrying Sakura.
The effect of proximity between focal adults and Sango, and focal adults and twins on parenting behavior. To determine the effects of the social relationships of the twins with Sango on the parental behavior by focal adults other than Sango, we conducted correlation analyses on proximity rate between twins and focal adults, Sango and focal adults, and the occurrence rate of alloparental behavior by focal adults.
There was no significant correlation between the occurrence rate of parental behavior toward Daiya by focal adults and the proximity rate between Sango and the focal adults. However, there was a positive correlation between the occurrence rates of parental behavior toward Daiya by focal adults and proximity between Daiya and the focal adults ( Table 1). The same was true for Sakura: There was no significant correlation between the occurrence rate of parental behavior toward Sakura by focal adults and the proximity rate between Sango and the focal adults. However, there was a positive correlation between the occurrence rates of parental behavior toward Sakura by   focal adults and proximity between Sakura and the focal adults ( Table 2).
The effect of proximity between Sango and the twins on proximity between focal adults and twins. Table 3 shows the cross-tabulation of the number of scans revealing the relations between whether Daiya and his mother Sango were within the reach of each other and whether each focal adult and Daiya were simultaneously within the reach of each other. In this analysis, we counted the total scans conducted when the adult chimpanzee was in the outside enclosure, and categorized the scans into four conditions that occurred in a combination of whether Daiya and his mother, Sango, were within each other's reach, and whether each focal adult and Daiya were simultaneously within each other's reach. For example, the total number of scans conducted when Robin was in the outside enclosure was 382, and for 32 of these scans, both Sango and Robin were within reach of Daiya, for 114 scans Sango was within reach but Robin was out of reach of Daiya, for 62 scans Sango was out of reach but Robin was within reach of Daiya, and for 174 scans both Sango and Robin were out of reach of Daiya.
Koyuki and Daiya were within the reach of each other at a higher rate when Sango and Daiya were also within the reach of each other than when they were out of reach (x 2 (1) 5 6.12, p 5 0.013). In contrast, Chelsea and Daiya were within the reach of each other at a higher rate when Daiya and Sango were not within the reach of each other (x 2 (1) 5 16.39, p , 0.00006). Table 4 shows the cross-tabulation of the number of scans revealing the relations between whether Sakura and her mother were within the reach of each other and whether each focal adult and Sakura were simultaneously within the reach of each other. All of Sango's affiliated adults (Robin and Koyuki) and Sakura were within the reach of each other at a higher rate when Sango and Sakura were also within the reach of each other (Robin: x 2 (1) 5 8.52, p , 0.004; Koyuki: x 2 (1) 5 4.31, p , 0.038). In contrast, two of Sango's nonaffiliated adults (Cherry and Chelsea) and Sakura were within the reach of each other at a higher rate when Sakura and Sango were not within the reach of each other (Cherry: x 2 (1) 5 22.36, p , 0.000002; Chelsea: x 2 (1) 5 11.95, p , 0.001).
Communication between focal adults and twins before infant carriage. By using the 1-min fixed-interval point sampling method, we recorded infant carriage at 50 sampling points. We observed communications between focal adults and infants before four of these 50 sampling points. All four communications were between Sakura and focal adults. Two were adult-initiated communications between Koyuki and Sakura, and Sango and Sakura. The other two were infant-initiated communications between Cherry and Sakura, and Chelsea and Sakura. Both Cherry and Chelsea were Sango's non-affiliated adults. The details are as follows.      Proximity between Sango and the twins. To determine whether Sango was equally close to each of her twins, we compared the numbers of proximity and non-proximity scans with Sango and each of Daiya and Sakura by using a chi-squared test. Daiya was    close to Sango at a significantly higher rate than was Sakura ( Figure 7; x 2 (1) 5 5.59, n 5 764, p , 0.018).

Discussion
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 Boesch 16 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, Wroblewski 17 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. Stanford 18 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 recipient 19 . 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 protective 20,21 . 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 them 20 . 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 Kogel 22 , 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 Kogel 22 . 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' welfare 23 . 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 Hirata 24 , 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 Tanaka 25 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 staff 26 ). 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.

Methods
Participants. The present study was conducted between April 2011 and March 2012 on a captive social group of chimpanzees at the Noichi Zoological Park of Kochi Prefecture, Japan. In April 2011, the study group consisted of 10 chimpanzees, including two adult males, six adult females, and the dizygotic male-female twin infants (Table 5). Of these, one adult male (Gou) and one adult female (Maya) were often kept in indoor rooms, and there were few opportunities to observe them in the outdoor enclosure. Thus, we excluded them from the participants.
Daiya, the male infant, and Sakura, the female infant, were the two-year-old twins. They were born on April 18, 2009 Data collection. In this study, the first author (TK) conducted observation of six adult chimpanzees by using a 10-min focal animal sampling procedure 12 when the group members were in the outside enclosure (853 m 2 ). Observations were made between 10:00 and 17:00 h on the days when Sango and twins were in the outside enclosure. A video camera (Sony HDR-CX560V) was used to record the behavior of focal participants. The focal observations were conducted in a predetermined order. Observations were not conducted during the feeding time or when it rained.
Parenting behaviors were recorded using 1-min fixed-interval point sampling 12 . Parenting behaviors were categorized into the following four mutually exclusive behaviors: walking together, which included focal adults walking with the twins while maintaining a distance of less than 1 m; infant carriage, which included cases in which the focal adults held the twin infants on their back or in ventral position while moving around; grooming, which included cases in which either focal adults groomed the twins or twins groomed the focal adults; and physical contact, which included cases of breast-feeding, or cases in which the body parts of the focal adults made contact with the body parts of infants, but excluded carriage and grooming instances. If infant carriage was noted, we recorded whether communication between the focal adults and infant twins occurred during the minute preceding the sampling point in which infant carriage was recorded. Adult-infant communication was classified into adult-initiated communication, which included cases in which focal adults outstretched their arm toward the infant; and infant-initiated communication, which included cases in which infants dragged the focal adults. Because there was a possibility that vocalizations of chimpanzees did not occur for communication but were a result of emotional arousal 13 , we did not define the screams or whimper calls by infants as infant-initiated communication. Since these behaviors were distinct, reliability tests were not conducted. Data were collected for an average of 6.78 h (SD 5 0.79) per focal participant.
Besides focal observations, TK conducted scan sampling observations of all chimpanzees, including the six adults and the twins 12 . TK recorded participants who were within the reach of one another by taking notes. The two scan samplings were conducted at intervals of at least 10 min. TK did not conduct scan sampling while he was conducting the focal observation. A total of 382 scan samples were collected. Table 6 shows the details about the information on the number of focal observation, observation days, observation time (min), and number of scans.
Analysis. Proximity values (%) between chimpanzees A and B were calculated as follows: the number of scans in which A and B were within the reach of each other was divided by the total number of scans obtained on the observation days in which both A and B were in the outdoor enclosure and then multiplied by 100. The average proximity value between Sango and other adults was 11.91%. We defined Sango's affiliated and unaffiliated adults on the basis of these proximity scores. Adults with above-average proximity values were considered affiliated, whereas those with belowaverage proximity values were considered unaffiliated ( Table 5).
The occurrence rates (%) of parenting behavior by adults were calculated as follows: the number of sample points in which the focal adults were observed engaging in one of the four kinds of parenting behavior was divided by the number of total sample points for the focal adults and multiplied by 100. For some chimpanzees, the number of days in which focal observations were conducted differed from that of the number of observation days because there were a few days when we could not conduct focal observation but could conduct scan sampling. www.nature.com/scientificreports