Primates (2007) 48:117121
DOI 10.1007/s10329-006-0005-2
O R I G I N A L A RT I C L E
Female transfer between one-male groups of proboscis monkey
(Nasalis larvatus)
Tadahiro Murai Maryati Mohamed
Henry Bernard Patrick Andau Mahedi
Rashid Saburi Seigo Higashi
Received: 21 February 2006 / Accepted: 5 June 2006 / Published online: 27 July 2006

Japan Monkey Centre and Springer-Verlag 2006
Abstract Successful or unsuccessful female transfers
were observed seven times during a 32-month field
study of proboscis monkeys (Nasalis larvatus) inhabit-
ing a riverine forest along a tributary of the Kinaba-
tangan River, Sabah, Malaysia. In all cases, the females
voluntarily left their own groups and immediately
joined with another one. When adult females tried to
shift to other groups, adult males called them back to
their own groups, but appeared to be indifferent to
subadult females. When the adult females returned,
the males never attacked the females physically, but
instead often emitted herding sounds to them. One
subadult female was repelled by a resident adult fe-
male. When one adult female transferred into a new
one-male group, she left her behind son in an all-male
group. The number of females often fluctuated in most
study groups, with this fluctuation being more promi-
nent among subadult females than adult females. It is
likely that female transfer in proboscis monkeys is not
a rare occurrence and that it is especially common
among sub-adult females.
T. Murai (&)
Primate Research Institute, Kyoto University,
Kanrin, Inuyama, Aich 484-8506, Japan
e-mail: murai@pri.kyoto-u.ac.jp
M. Mohamed H. Bernard
Institute for Tropical Biology and Conservation,
University of Malaysia Sabah, Sabah, Malaysia
P. A. Mahedi R. Saburi
Sabah Wildlife Department, Sabah, Malaysia
S. Higashi
Graduate School of Environmental Earth Science,
Hokkaido University, Hokkaido, Japan
Keywords All-male group Female transfer
Nasalis larvatus One-male group Proboscis monkey
Introduction
In most primate species that live in groups containing
more than one breeding female, males show a much
greater tendency than females both to emigrate from
the natal group and to transfer between groups (see a
review of Pusey and Packer 1987). However, Moore
(1984) found that 31 out of 59 primate species showed
female transfers either evidently or probably and
suggested that female transfers are not as rare as pre-
viously assumed. Folivorous primates (e.g. Alouatta
and the Colobinae), in particular, appear to have this
tendency for female transfer.
The proboscis monkey (Nasalis larvatus) is endemic
to Borneo Island, inhabiting mangrove, peat swamp or
riverine forests. This species belongs to the sub-family
Colobinae that includes at least 30 species classified
into four to nine genera (Oates and Davies 1994), and
it is characterized by a multi-chambered stomach that
is an adaptation to digest foliage (Bauchop and Mar-
tucci 1968). The typical social unit of proboscis mon-
keys is a one-male group consisting of a single male
and several females with their offspring. Young males
usually emigrate from their natal groups, subsequently
forming all-male groups; solitary males are rare (Ben-
nett and Sebastian 1988; Boonratana 1999, 2002; Murai
2004; Yeager 1990, 1991, 1995). In addition to male
emigration, female transfer has also been confirmed by
observed changes in group composition (Bennett and
Sebastian 1988; Boonratana 1999; Rajanathan and
Bennett 1990; Yeager 1990). However, to date, the
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118 Primates (2007) 48:117121

process of female transfer had never been observed group Po which at the time was at a distance of about
directly in this species. This paper describes the feature 40 m from group Be. On this occasion, all members of
of female transfer in proboscis monkeys and discusses both groups quietly settled in their sleeping trees, and
the factors influencing this behavior as well as the her behavior did not cause any response. The adult
behavior of adult males and other group members male of Be did not impede her and appeared to be
when female transfer occurred. indifferent to her action. This female sat on the branch
quietly without interaction with the Po group mem-
bers. After 10 min, the adult male of Po suddenly ap-
Methods
proached her from behind and mounted her twice.
Solicitation was not observed in either individual.
The behavior of proboscis monkeys was observed in a
During this event, the other group members of Po
riverine forest along a tributary of the Kinabatangan
showed no reaction to the newcomer. The subadult
River, Sabah, Malaysia (530N/11830E), by the event
female stayed with this new group for at least
sampling method (Lehner 1979) using binoculars and a
8 months.
video camera (DCR-TRV 900, Sony) with a field scope
On the morning of 13 August 2000, a subadult fe-
(VCL-FS 2K, Sony). The video scene could be zoomed
male of group Ts gently solicited the resident adult
in situ up to 120.
male, but he did not response to her. She then ran
Observations were conducted from February 1999 to
directly to group Po, which at the time was at a dis-
October 2001, and in May and June 2002 (in total
tance of about 15 m, and sat in front of the adult male
560 days). By late June 1999, we had identified eight
of the relevant group. She solicited him with a pouting
one-male groups (mean group size: 18 individuals;
face and turned her back to show her genital area. He
range: 834) and one all-male group (about 30 individ-
immediately mounted her twice, grasping her around
uals) by distinguishing all adult males and a few adult
the midsection. During the copulation, no disturbances
females based on their physiognomic external features,
occurred. The transferred female stayed with the new
such as scars and nose shapes. The relative age of each
group for at least 2 months.
individual was determined following Bennett and
On the evening of 11 November 2000, a subadult
Sebastian (1988), who categorized age classes of proboscis
female of group Ts suddenly ran towards group KiBa,
monkeys. The composition of each one-male group was
which was at a distance of about 30 m. She solicited
continuously monitored over the study period.
and leaned toward the adult male of KiBa. He imme-
One-male groups of proboscis monkeys often rested
diately approached and mounted this female. The adult
at night in trees along the riverside with a distance of
male of Ts did not demonstrate any preventing
less than 100 m between each group, but only rarely
behavior. The transferred female was still in group
did more than one group rest in the same tree. Addi-
KiBa at the end of this study.
tionally, group members remained together throughout
The last observed case of successful female transfer
the day, never merging with members of other groups.
was that of an adult female who had an infant male and
No conflicts, except for cases of inter-group transfers,
initially belonged to the one-male group PoBu. Her
were observed between members of different groups.
participation in the PoBu group was confirmed on 20
When it was confirmed that a female had left her own
May 2002. She and her son were found together with a
group and joined with another group for more than
previously all-male group during the evening of 22 May
several days, we considered this act to be a complete
2002. At this time, the PoBu group was situated at a
female transfer. We judged an unsuccessful female
distance of 200 m from this all-male group. The next
transfer to have occurred when a female left her own
morning, she nursed her son for 6 min, suddenly left
group, evidently intermingled with another group, but
her son in the all-male group, jumped into the river and
did not stay in that group, and ultimately moved back
swam the river to join with the one-male group Ts that
to her original group after a short time interval.
had remained on the opposite riverbank since the
previous evening. When she joined with the Ts group,
no members of Ts, including the adult male, showed
Results any special response. This group moved slowly inland
and she followed. On the other hand, her son screamed
Successful female transfers repeatedly but did not follow her, although he was
about 1 year in age and could probably cross the river
On the evening of 9 January 2000, a subadult female of by himself. A subadult male of the all-male group also
group Be suddenly left her own group, and joined with uttered Aoh Aoh for 10 min. The all-male group

123
Primates (2007) 48:117121
subsequently moved slowly along the river and the
infant male followed them. The transferred female was
still in group Ts at the end of this study.
The mean size of the groups to which the emigrant
female originally belonged and the mean number of
adult and subadult females of those groups were 13.7
(range: 1115; n=3) and 7.0 (range: 58; n=3) individ-
uals, respectively. The mean size of the groups
receiving the emigrants and the mean number of adult
and subadult females of those groups were 16.3
(range:1617; n=3) and 8.3 (89; n=3) individuals,
respectively. In all cases, the size and number of adult
and subadult females of groups receiving emigrants
were similar or larger than those of the original groups.
Unsuccessful female transfers
During the evening of 12 March 1999, one-male groups
A and B settled themselves, resting quietly in their
sleeping trees. The distance between groups A and B
was about 30 m. An adult female of group A suddenly
left her own group and entered the center of group B
members without any disturbance. She sat quietly on a
branch just below the adult male of group B. The
distance between them was less than 5 m. After 3 min,
the male of group A slowly came over and sat close to
the female. He stared at her and intensively uttered
Aoh Aoh calls for about 10 min without any inter-
actions with the members of group B. The female did
not show any response to him at first, but finally stood
up and slowly returned to her original group. The adult
male of group A followed her. The two stayed in the
same sleeping tree during the night. During this event,
members of group B, including the adult male, did not
show any interests in the invaders.
A similar event was observed in the evening of 9
November 2000 between one-male groups BoWa and
Be. This incident occurred closely following a male
replacement in group BoWa. An adult female and her
infant belonging to group BoWa were found in a tree
in which group Be was resting. They stayed quiet as if
members of group Be, although no interaction was
observed between them. The distance between the
female and the Be adult male was about 7 m. The adult
male of BoWa, Wale, loudly uttered Aoh Aoh calls. males (Fishers exact probability test: p=0.013).
The BoWa group stayed about 40 m apart from group
Be. The BoWa adult male gradually approached and
came to the tree where the group Be members stayed
and sat near this female. He continued to utter Aoh
Aoh calls toward the female for about 10 min. She
finally left this group carrying her infant in her arms,
and returned to the tree where the members of BoWa
stayed. The male followed this female and sat near her.
119
During this event, as in the previous case, the members
of group Be, including the adult male Bera, did not
show any response to the invaders.
On the evening of 10 July 2001, a subadult female of
BoWa gradually approached group KiBa, situated at
the time about 65 m distant from group BoWa. She
stopped and sat down at about 10 m apart from the
adult male of KiBa and gently solicited him with a
pouting face. He also responded by pouting his face.
Both, however, did not approach each other more
closely, keeping their distance and repeating the ex-
change of pouting faces twice during a 10-min period.
The female then started feeding on young leaves. An
adult female of KiBa came near the incoming female
and frequently showed an open mouth display toward
the newcomer. The newcomer stayed and fed on leaves
for about 30 min in the proximity of the group and
subsequently returned to BoWa. During this event, the
adult male of BoWa sometimes uttered gentle Aoh
Aoh calls, but did not approach the trees where the
KiBa group had settled.
The mean size and number of adult and subadult
females of the original groups were 13.5 (range: 1116;
n=2) and 5.5 (mean: 56; n=2) individuals, respectively.
Comparable figures of the groups into which the fe-
males moved were 14.5 (range: 1118; n=2) and 7.0
(range: 59; n=2) individuals, respectively.
Fluctuating the numbers of females
The number of females fluctuated in most groups
during the study period (Fig. 1). Overall, 18 cases of
female transfer were confirmed (eight adult and ten
subadult) (including the direct observations reported
above), while 20 (ten adult and ten subadult) females
disappeared from the study groups on an individual
basis (excluding the case of a confirmed dead adult
female) during the course of the observations. The
mean number of adult females and subadult females
was 58 and 19, respectively, in the study site. The ratio
of transferring adult and subadult females to mean
number of adult and subadult females was 13.8 and
52.6%, respectively. Transfers occurred significantly
more frequently in subadult females than in adult fe-
Discussion
The number of females in most of the study groups
fluctuated during the course of the study period. This
fluctuation was more pronounced in sub-adult females
than in adult females and, moreover, subadult females
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120 Primates (2007) 48:117121

Year 1999 2000 2001 2002

Month 6 7 8 9 10 11 12 1 2 4 5 6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 5 6
Group

Yo
A S S A

Be
S S A

Ts
b b
S A A AS S 3S

Ki
(KiBa) a MR e
A S S S S 2A A
S
Bo
(BoWa) MR c
A S A A 4A A

d
Po X
(PoBu) MD MJ
S S S S A

Pu

De

Fig. 1 The fluctuation of females of study groups. Solid lines
indicate all females present were counted. Dotted lines indicate
not all female were counted in the groups. Arrows indicate
transfers in and out of a group. A Adult female, S subadult
female, MR male replacement occurred, MD resident male
disappeared, MJ a new male joined. Superscripts: a Death of an
adult female (confirmed), b adult female with infant was found in
the all-male group and returned when the male replacement
occurred, c, d four adult females disappeared between 23
October 2001 and 5 May 2002 and two adult females disappeared
one by one until 23 May 2002, when the group finally collapsed, e
an adult female with an infant joined with the all-male group,
and she transferred to Ts leaving her infant with the all male
group (see text)

and juvenile females were often found temporarily in
otherwise all-male groups (Murai 2004). Consequently,
based on our observations, female transfer among
groups of proboscis monkeys can be considered to be a
common occurrence, especially among subadult fe-
males. Previous studies also reported female transfer
among proboscis monkeys (Bennett and Sebastian
1988; Boonratana 1999; Rajanathan and Bennett 1990;
Yeager 1990), with between-group transfer also being
more often observed in young females than in adult
females. However only adult female transfers were
reported in some studies, as those study groups did not
contain subadult females (Bennett and Sebastian 1988;
Rajanathan and Bennett 1990).
Resident adult males were observed to be relatively
indifferent to transfers of the subadult females; on the
other hand, they called out to adult females who had
moved from their groups to another one. In the study
population, the estimated mean tenure period for an
adult male was about 6 years (T. Murai, in prepara-
tion), while females take about 5 years to maturate
(Napier and Napier 1985). This suggests that females
need to disperse from their natal groups before
reaching full maturation in order to avoid inbreeding
with their fathers (Clutton-Brock 1988). In the present
study, many subadult females transferred; it is quite
likely that these females had recently reached sexual
maturity and may have been daughters of the adult
male of their current group.
When an adult female tried to shift to another
group, the resident adult male calmly called the female
back to his own group, and physical attacks were never
observed. While vigorous attacks by males on females
can occur in some species (capped langur, Presbytis
pileata, Stanford 1991; hamadryas baboon, Papio
hamadryas, Stammbach 1987), the recouping behavior
of the proboscis monkey is not aggressive, but similar
to the herding-by-sound behavior observed in the gel-
ada baboon (Theropithecus gelada) (Dunbar and
Dunbar 1975).

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Primates (2007) 48:117121
The home range of various proboscis monkey
groups extensively overlaps (Bennett and Sebastian
1988; Boonratana 2000; Yeager 1991). Ali (1981) sug-
gested that females are more likely to transfer between
groups when the home range overlap is extensive due
to a greater familiarity with both the neighbors and the
neighbors ranges. Whenever female transfer was ob-
served, the original group and receiving group were in
close proximity. Easier access to the target group might
assure the safety of the monkeys concerned.
Female transfer may occur most readily in folivor-
ous species (Wrangham 1980). Folivorous food sources
are relatively abundant, evenly distributed and easy to
exploit. If feeding competition in a group is severe,
female may transfer to a smaller group (e.g. Crockett
1984). The result of this study indicated that females
have a tendency to transfer to a larger group, indicat-
ing that intra-group feeding competition is weak and
has no bearing on female transfer in proboscis mon-
keys. Consequently, females of this species are not
constrained in their transfer behavior by food re-
sources.
Sterck (1997) suggested that females transfer to re-
duce the risk of infanticide. Indeed, in Thomass lan-
gurs (Presbytis thomasi), female transfer was observed
mostly when their group was harassed by extra-group
males (Sterck 1997). Although infanticide has been
reported in proboscis monkey in Labuk Bay Sanctuary,
Sabah, Malaysia (Agoramoorthy and Hsu 2004), we
never observed infanticide in our study site, whereas
male replacements were observed three times. Prior to
female transfer, no agonistic interactions were ob-
served between groups. Furthermore, females with
their infants could move together to other groups (this
study; Bennett and Sebastian 1988; Rajanathan and
Bennett 1990). It would therefore appear that the
avoidance of infanticide may not be an important
factor in female transfer in proboscis monkeys.
Acknowledgements We would like to express our sincere
thanks to Dr. K. Watanabe for his valuable advice in preparing
this manuscript, and to Dr. M. Mitani for his encouragement and
field support. Cordial thanks are also due to staff members of the
Kota Kinabatangan Wildlife Department for their help in the
fieldwork, and to Ms. T. Murai for her field assistance throughout
the study. We also thank anonymous reviewers for their valuable
comments on this manuscript.
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