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

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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

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Primates (2007) 48:117121 119

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

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

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

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Primates (2007) 48:117121 121

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served, the original group and receiving group were in larvatus) in the Lower Kinabatangan, Northern Borneo.
close proximity. Easier access to the target group might Trop Biodivers 6:179187
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Acknowledgements We would like to express our sincere ioral ecology and reproductive tactics. Contributions to
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