OPEN

SUBJECT AREAS:

Alloparenting for chimpanzee twins

Takeshi Kishimoto1, Juko Ando2, Seiki Tatara3, Nobuhiro Yamada3, Katsuya Konishi3, Natsuko Kimura3,
Akira Fukumori4 & Masaki Tomonaga5

HUMAN BEHAVIOUR
ANIMAL BEHAVIOUR
BIOLOGICAL ANTHROPOLOGY

Received
19 May 2014
Accepted
18 August 2014
Published
9 September 2014

Correspondence and
requests for materials
should be addressed to
T.K. (tkishimoto@usacred-heart.ac.jp)

Faculty of Liberal Arts, University of the Sacred Heart, Tokyo, Japan, 2Faculty of Letters, Keio University, Tokyo, Japan, 3Noichi
Zoological Park of Kochi Prefecture, Kochi, Japan, 4Hirakawa Zoological Park, Kagoshima, Japan, 5Primate Research Institute,
Kyoto University, Aichi, Japan.

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 5 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, Sakuras
departures from her mother and her ability to gesture requests might have enabled non-kin adults to provide
her care.

n humans (Homo sapiens), having young twins sometimes has a deleterious effect on the emotional well-being
of mothers. Thorpe, Golding, MacGillivray, and Greenwood1 showed that mothers of twins at 5 years had
significantly higher malaise scores, indicative of depression, than did mothers of singletons at the same age.
Maternal depression is at least in part caused by the heavier burden of parenting on mothers of twins than on
mothers of singletons2,3. This occasionally results in maltreatment of twins4. Diminishing the parental stress of the
mothers of twins might require the involvement of alloparents who share the burden of parenting with mothers
such as fathers, extended families, and community members5.
Chimpanzees (Pan troglodytes), the closest relatives of humans, normally give birth to one infant at a time;
however, they also give birth to twins, albeit infrequently. According to the data from the International Species
Information System (ISIS), one of 59 captive births was multiple6. Some cases of twin births have also been
reported in the wild. For example, Matsumoto-Oda7 reported a case of twin birth among the chimpanzees of the
Mahale Mountain National Park, Tanzania. Additionally, Goodall8 reported a case of twin birth in the Gombe
National Park, Tanzania. However, in both these cases, the twins were unable to reach adulthood, as one or both
the twins died within few years7,8. Even among captives, 64% of individuals born as twins die by the end of the first
year of their birth, whereas only 23% of singletons pass away during the first year of life6.
One of the difficulties in rearing infant twins among chimpanzee mothers might have been the absence of
alloparents. This idea is supported by the single case of successfully raised chimpanzee twins in the wild at Gombe.
The mother, Gremlin, gave birth to female twins (Golden and Glitter) in 19989. The twins are still alive and
surviving well into adulthood10. The Jane Goodall Institute10 has introduced video episodes indicating that the
twins were often taken care of by their older sister Gaia. These episodes suggested that alloparenting by Gaia
reduced the parental burden on Gremlin, and thus allowed for the successful rearing of the twins. Although
reports from the Jane Goodall Institute supported the idea that chimpanzee mothers can rear twins if alloparents
are available, quantitative data remain sparse. In particular, no research has indicated who is more suitable to
become a chimpanzee alloparent or the types of care responsibilities assumed by alloparents.
In April 2009, a female chimpanzee named Sango living in the captive group at the Noichi Zoological Park of
Kochi Prefecture, Japan, gave birth to dizygotic male-female twins (male: Daiya, female: Sakura; Figure 1). To
date, the twins have been successfully reared by their mother. To investigate the hypothesis that alloparents are
necessary for twin rearing, we observed the chimpanzee group at Noichi when the twins were two years old. In
general, the third year of life in chimpanzees is the middle of infancy in their life cycle, and they still depend on
their mothers in diverse ways. For example, infant chimpanzees still depend on their mothers for transport by
riding on their mothers when they travel8,11. In other words, to ensure their infants survival, chimpanzee mothers
must take care of them. We investigated whether and how adult group members (besides the mother) cared for
the twins. Additionally, we explored the causes of alloparenting among chimpanzees, focusing on two primary
factors, namely, the individuals that were most likely to become alloparents and the external triggers for alloparenting behavior.

SCIENTIFIC REPORTS | 4 : 6306 | DOI: 10.1038/srep06306

www.nature.com/scientificreports
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 Sangos 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.

Figure 1 | Sango was holding the twins (left: Daiya, right: Sakura) in her
arms when they were 5 months old. Photo courtesy of Nobuhiro Yamada.

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 Sangos

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

Figure 2 | The occurrence rates of parental behaviors by each focal adult toward Daiya (a) and Sakura (b). Sango is the mother of Daiya and Sakura.
Robin and Koyuki were adults affiliated with Sango. Cherry, Chelsea, and Judy were adults unaffiliated with Sango.
SCIENTIFIC REPORTS | 4 : 6306 | DOI: 10.1038/srep06306

www.nature.com/scientificreports

Table 1 | Proximity and Parenting Behavior Occurrece Correlations

for Daiya (n 5 5)

1. Alloparenting toward Daiya

2. Proximity rate with Daiya
3. Proximity rate with Sango

1.

2.

3.

0.90*
-

0.80
0.60
-

Note. Values in the table are Spearmans rank-order correlation coefficients.

*: p , .05.

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 others reach, and whether each focal
adult and Daiya were simultaneously within each others 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 (x2(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 (x2(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
Sangos 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: x2(1) 5 8.52, p , 0.004;
Koyuki: x2(1) 5 4.31, p , 0.038). In contrast, two of Sangos 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: x2(1) 5 22.36, p , 0.000002;
Chelsea: x2(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
Table 2 | Proximity and Parenting Behavior Occurrece Correlations
for Sakura (n 5 5)

1. Alloparenting toward Sakura

2. Proximity rate with Sakura
3. Proximity rate with Sango

1.

2.

3.

0.90*
-

0.60
0.30
-

Note. Values in the table are Spearmans rank-order correlation coefficients.

*: p , .05.

SCIENTIFIC REPORTS | 4 : 6306 | DOI: 10.1038/srep06306

Table 3 | Simultaneous Proximity between Sango and Daiya, and

Daiya and Focal Adults
Sango and Daiya

Robin and Daiya

Within reach
Out of reach
Koyuki and Daiya
Within reach
Out of reach
Cherry and Daiya
Within reach
Out of reach
Chelsea and Daiya
Within reach
Out of reach
Judy and Daiya
Within reach
Out of reach

Within reach

Out of reach

x2(1)

32
114

62
174

0.92

32
101

30
189

6.12*

9
120

26
177

2.84

7
107

45
139

16.39**

13
117

19
199

0.16

*p , .05.
**p , .01.

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 Sangos
non-affiliated adults. The details are as follows.
Adult-initiated communication between Koyuki and Sakura. At
15:32 h on July 23, 2011, Sakura and Koyuki were in the proximity
to Sango. When Koyuki started to move away, Sakura gently touched
Koyuki. Thereafter, Koyuki extended her right hand to Sakura with
her palm facing up (Figure 3a). Next, Sakura approached Koyuki and
climbed onto Koyukis back (Figure 3b).
Adult-initiated communication between Sango and Sakura. At
13:22 h on August 18, 2011, Sango began to move under the tower,
and Daiya and Sakura followed. When Sango reached the lower step,
Sango directed her gaze to Sakura and stretched her hand toward
Sakura (Figure 4a). Thereafter, Sakura fell into Sangos arms and

Table 4 | Simultaneous Proximity between Sango and Sakura, and

Sakura and Focal Adults
Sango and Sakura

Robin and Sakura

Within reach
Out of reach
Koyuki and Sakura
Within reach
Out of reach
Cherry and Sakura
Within reach
Out of reach
Chelsea and Sakura
Within reach
Out of reach
Judy and Sakura
Within reach
Out of reach

x2(1)

Within reach

Out of reach

25
90

28
239

8.52**

29
76

44
203

4.31*

13
78

101
140

22.36**

5
86

45
162

11.95**

12
96

30
210

0.14

*p , .05.
**p , .01.

www.nature.com/scientificreports

Figure 3 | Adult-initiated communication. Koyuki stretched her right

hand toward Sakura (a). Then Sakura climbed on to Koyukis back (b).
Photo courtesy Takeshi Kishimoto.

Figure 5 | Infant-initiated communication. Sakura roughly touched

Cherrys head (a). Then Cherry shifted her posture (b), and Sakura
climbed upon Cherrys back (c). Photo courtesy Takeshi Kishimoto.

climbed onto Sangos back (Figure 4b). Daiya went to Sangos and
Sakuras side.
Infant-initiated communication between Cherry and Sakura. At
11:58 h on February 5, 2012, Cherry and Sakura were resting about
2 m apart. After Sakura approached the wall and kicked it, she
approached Cherry and roughly touched Cherrys face with her left
hand (Figure 5a). Thereafter, Cherry shifted her posture and moved
(Figure 5b), and Sakura climbed on Cherrys back (Figure 5c).
Infant-initiated communication between Chelsea and Sakura. At 0:
30 h on February 5, 2012, Chelsea, Sakura, and Cherry were resting
in the cave with about 1 m of distance among them. Sakura
approached Chelsea, touched Chelseas head, and dragged Chelsea
outside the cave (Figure 6a, b). Thereafter, Chelsea moved, and
Sakura climbed on Chelseas back (Figure 6c).
Figure 4 | Adult-initiated communication. At the lower part of the tower,
Sango stretched out her left hand (a). Then Sakura fell into Sangos arms
(b). Photo courtesy Takeshi Kishimoto.
SCIENTIFIC REPORTS | 4 : 6306 | DOI: 10.1038/srep06306

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
4

www.nature.com/scientificreports

Figure 6 | Infant-initiated communication. In the cave, Sakura touched

Chelseas head (a) and dragged Chelsea outside (b). Then Sakura climbed
upon Chelseas back (c). Photo courtesy Takeshi Kishimoto.

close to Sango at a significantly higher rate than was Sakura (Figure 7;

x2(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 Daiyathe male twinmother 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
SCIENTIFIC REPORTS | 4 : 6306 | DOI: 10.1038/srep06306

physical contact and walking together. This suggests that parenting

responsibilities were divided between Robin and Sango. While Sango
provided essential care for Daiyas 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 run14. 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 adults 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 Sangos 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
5

www.nature.com/scientificreports

Figure 7 | The rates of proximity and non-proximity scans between Sango and each twin.

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 Cherryone of her alloparentsat 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. Sangos 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

Table 5 | Profiles of chimpanzees at the Noichi Zoological Park of Kochi prefecture

Name

Sex

Date of birth
d

Agea

Proximity value
(%) with Sangob

Relationship with
Sangoc

Sango
Robin

F
M

1976
Nov.12, 1995

35
15

16.75

Affiliated

Koyuki

Apr. 30, 1993

18

26.70

Affiliated

Cherry
Chelsea
Judy
Daiya
Sakura
Mayae
Goue

F
F
F
M
F
F
M

1978d
Dec. 20, 1987
Jan. 5, 1990
Apr. 18, 2009
Apr. 18, 2009
Jan. 9, 1990
1977

33
23
21
2
2
21
34

6.63
4.03
5.46
-

Unaffiliated
Unaffiliated
Unaffiliated
-

Notes
Wild-born. The mother of twins (Daiya and Sakura)
Captive-born. Introduced to the Noichi group in 2008 with
Sango and Koyuki. The father of the twins.
Captive-born and introduced to the Noichi group in 2008
with Sango and Robin.
Wild-born and introduced to the Noichi group in 1999.
Captive-born and introduced to the Noichi group in 1994.
Captive-born. An original member of the Noichi group.
One of the dizygotic twin children of Sango; father is Robin.
One of the dizygotic twin children of Sango; father is Robin.
Captive-born. An original member of the Noichi group.
Captive-born and introduced to the Noichi group in 2011

As of April 9, 2011, the beginning of this study.

The number of scans in which Sango and the focal adult were within the reach of each other was divided by the total number of scans carried out in the observation days in which both Sango and the focal
adult were in the outside enclosure and multiplied by 100.
c
If the proximity value of an adult and Sango was over the average (11.91%), then the adult was classified as an affiliated adult. On the other hand, if the proximity value of an adult and Sango was under the
average, then the adult was classified as an unaffiliated adult.
d
Estimated.
e
Because these chimpanzees were often kept in the indoor rooms and the opportunities to observe them in the outside enclosure were few, we excluded them from the participants.
b

SCIENTIFIC REPORTS | 4 : 6306 | DOI: 10.1038/srep06306

www.nature.com/scientificreports

Table 6 | Information on the number of focal observation, observation days, observation time (min), and number of scans

Name

Number of days in
which focal
Number of
observations were Number of focal
observation daysa
observations
conductedb

Sango
Robin
Koyuki
Cherry
Chelsea
Judy

24
24
22
21
19
21

24
23
19
21
19
20

Total time of focal

observations
(minutes)c

The average
number of focal
observation per
dayd

The average
length of focal
observation per
day (minutes)e

490
420
410
390
350
380

2.04
1.83
2.16
1.86
1.84
1.90

20.42
18.26
21.58
18.57
18.42
19.00

49
42
41
39
35
38

The average
number of
Number of
scans per
scans
dayf
382
382
352
332
298
348

15.92
15.92
16.00
15.81
15.68
16.57

Since some chimpanzees kept in the indoor rooms on some days while Sango and her twins were in the outside enclosure, Sangos number of observation days differed from other chimpanzees.
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.
c
Since each focal sampling was conducted continuously for 10 minutes, the total time of focal observation was calculated by multiplying the number of focal observations by 10.
d
The average number of focal observations per day was calculated by dividing the total number of focal observations by the number of days in which focal observation were conducted.
e
The average length of focal observation per day was calculated by dividing the total time of focal observation by the number of days in which focal observations were conducted.
f
The average number of scans per day was calculated by dividing the number of scans by the number of observation days.
b

help others when others express their needs by gestures. Sakuras

pulling of Cherry or Chelsea would facilitate their understanding
of Sakuras 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.

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 malefemale 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, to Sango, a 35-year-old wild-born female. The
father of the twins was Robin, a 15-year-old captive-born male. The birth of the twins
was natural, and there are not any human interventions.
According to the breeding record published on the website of Noichi Zoological
Park of Kochi Prefecture27, Sango and twins appeared in the outdoor enclosure for the
first time on April 27, 2009. After that, other adult group members sometimes
touched the twins in Sangos arms. From around December 2009, after the twins were
8 months old, Koyuki, Robin, and Cherry were sometimes observed holding the twins
in their arms. According to Ichino28 who investigated the social relationship of this
captive social group of chimpanzees, when the twins were aged between 18 and 23
months, Daiya spent significant amounts of time with Sango, Sakura, and Robin,
while Sakura spent much time with Sango, Daiya, and Cherry.
The research protocol was approved by a committee of Noichi Zoological Park of
Kochi Prefecture and by the AnimalWelfare and Animal Care Committee of KUPRI
and by the Animal Research Committee of Kyoto University. All procedures adhered

SCIENTIFIC REPORTS | 4 : 6306 | DOI: 10.1038/srep06306

to the Ethical Guidelines for the Conduct of Research on Animals by Zoos and
Aquariums issued by the World Association of Zoos and Aquariums (WAZA), the
Code of Ethics issued by the Japanese Association of Zoos and Aquariums (JAZA),
and the Japanese Act on Welfare and Management of Animals. This study was carried
out in accordance with these guidelines.
Data collection. In this study, the first author (TK) conducted observation of six adult
chimpanzees by using a 10-min focal animal sampling procedure12 when the group
members were in the outside enclosure (853 m2). 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 sampling12.
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. Adultinfant 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 arousal13, 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 twins12. 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 Sangos
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.
1. Thorpe, K., Golding, J., MacGillivray, I. & Greenwood, R. Comparison of
prevalence of depression in mothers of twins and mothers of singletons. Br. Med.
J. 302, 875878 (1991).

www.nature.com/scientificreports
2. Cinar, N. D., Alvur, T. M., Kose, D. & Nemut, T. Breastfeeding twins: A qualitative
study. J. Health Popul. Nutr. 31, 504 (2013).
3. Robin, M., Corroyer, D. & Casati, I. Childcare patterns of mothers of twins during
the first year. J. Child Psychol. Psychiatry. 37, 453460 (1996).
4. Lang, C. A., Cox, M. J. & Flores, G. Maltreatment in multiple-birth children. Child
Abuse Negl. 37, 11091113 (2013).
5. Salami, K. K., Brieger, W. R. & Olutayo, L. Stress and coping among mothers of
twins in rural southwestern Nigeria. Twin Res. 6, 5561 (2003).
6. Seal, U. S., Flesness, N. & Foose, T. Neonatal and infant mortality in captive-born
great apes. Clinical Management of Infant Great Apes (Graham, C. E. & Bowen,
J. A. (eds.)) 193203 (Alan R. Liss Inc, New York, 1985).
7. Matsumoto-Oda, A. First record of a twin birth in chimpanzees of the Mahale
Mountains National Park, Tanzania. Afr. Study Monogr. 16, 159164 (1995).
8. Goodall, J. The Chimpanzees of Gombe: Patterns of Behavior. (Belknap Press of
Harvard University Press, Cambridge, 1986).
9. Pusey, A., Murray, C., Wallauer, W., Wilson, M., Wroblewski, E. & Goodall, J.
Severe aggression among female Pan troglodytes schweinfurthii at Gombe
National Park, Tanzania. Int. J. Primatol. 29, 949973 (2008).
10. The Jane Goodall Institute, Twins! Golden & Glitter. Date of access: 10/3/2014,
http://www.janegoodall.org/chimp-central-twins (2010).
11. Hirata, S. Communication between mother and infant chimpanzees and its role in
the evolution of social intelligence. Origins of the Social Mind [Itakura, S. & Fujita,
K. (eds.)] [2138] (Springer Verlag, Tokyo, 2008).
12. Martin, P. & Bateson, P. Measuring Behaviour: An Introductory Guide.
(Cambridge University Press, Cambridge, 1990).
13. Tomasello, M. & Call, J. Primate Cognition. (Oxford University Press, New York,
1997).
14. Cordoni, G. & Palagi, E. Ontogenetic trajectories of chimpanzee social play:
Similarities with humans. PLoS One. 6, e27344 (2011).
15. Lonsdorf, E. V. et al. Boys will be boys: Sex differences in wild infant chimpanzee
social interactions. Anim. Behav. 88, 7983 (2014).
16. Boesch, C., Bole, C., Eckhardt, N. & Boesch, H. Altruism in forest chimpanzees:
The case of adoption. PLoS One. 5, e8901 (2010).
17. Wroblewski, E. E. An unusual incident of adoption in a wild chimpanzee (Pan
troglodytes) population at Gombe National Park. Am. J. Primatol. 70, 995998
(2008).
18. Stanford, C. B. Costs and benefits of allomothering in wild capped langurs
(Presbytis pileata). Behav. Ecol. Sociobiol. 30, 2934 (1992).
19. Trivers, R. L. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 3557 (1971).
20. Bardi, M. & Huffman, M. A. Effects of maternal style on infant behavior in
Japanese macaques (Macaca fuscata). Dev. Psychobiol. 41, 364372 (2002).
21. Sukino, Y., Onishi, K. & Nakamichi, M. Effects of maternal style on the social
interactions of their yearlings in a free-ranging group of Japanese macaques.
Primate Res. 27, 1119 (2011). (Written in Japanese with English abstract).
22. Hemelrijk, C. K. & De Kogel, C. H. What chimpanzee mothers have more sociable
infants? Behaviour. 111, 305318 (1989).
23. Silk, J. B. et al. Chimpanzees are indifferent to the welfare of unrelated group
members. Nature. 437, 13571359 (2005).

SCIENTIFIC REPORTS | 4 : 6306 | DOI: 10.1038/srep06306

24. Hirata, S. Chimpanzee social intelligence: selfishness, altruism, and the mother
infant bond. Primates. 50, 311 (2009).
25. Yamamoto, S., Humle, T. & Tanaka, M. Chimpanzees help each other upon
request. PLoS One. 4, e7416 (2009).
26. Kishimoto, T., Shizawa, Y., Yasuda, J., Hinobayashi, T. & Minami, T. Do pointing
gestures by infants provoke comments from adults? Infant Behav. Dev. 30,
562567 (2007).
27. Noichi Zoological Park of Kochi Prefecture, Breeders Diary. Date of access: 27/7/
2014 (Written in Japanese), http://www.noichizoo.or.jp/park/breed_blog/
breed010.html (2010).
28. Ichino, E. The changes of social relationship associated with the development of
twin chimpanzees. Bachelor thesis of Faculty of Applied Biological Sciences, Gifu
University (2012) (Written in Japanese).

Acknowledgments
We would like to thank T. Kinuta, the former director of Noichi Zoological Park, as well as
K. Yoshii, A. Nishiuchi, and all staff and volunteers at Noichi Zoological Park for their
support during observations. We also thank E. Ichino, Y. Fujimori, M. Kimura and F.
Kawakami for providing beneficial information about chimpanzees. The present study was
conducted under the Memorandum of Understanding for academic cooperation between
Wildlife Research Center, Kyoto Univesity and Noichi Zoological Park of Kochi Prefecture.
This study and the preparation of the manuscript were financially supported by the
JSPS-MEXT Grants-in-Aid for Scientific Research (16002001, 19300091, 20002001,
22650053, 23220006, 26540063 to M.T., and 21223002 to J.A.) and the Cooperative
Research Program of the Primate Research Institute (A-9, A-14) to T.K. and J.A.

Author contributions
T.K., J.A. and M.T. contrived the observation. T.K. conducted the observation and analysed
the data. T.K., J.A., S.T., N.Y., K.K., N.K., A.F. and M.T. discussed the results, and T.K. wrote
the paper.

Additional information
Competing financial interests: The authors declare no competing financial interests.
How to cite this article: Kishimoto, T. et al. Alloparenting for chimpanzee twins. Sci. Rep. 4,
6306; DOI:10.1038/srep06306 (2014).
This work is licensed under a Creative Commons Attribution 4.0 International
License. The images or other third party material in this article are included in the
articles Creative Commons license, unless indicated otherwise in the credit line; if
the material is not included under the Creative Commons license, users will need
to obtain permission from the license holder in order to reproduce the material. To
view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/