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Primates (2013) 54:2731

DOI 10.1007/s10329-012-0334-2

NEWS AND PERSPECTIVES

Identification of individual adult female Javan lutungs


(Trachypithecus auratus sondaicus) by using patterns of dark
pigmentation in the pubic area
Yamato Tsuji Kanthi Arum Widayati
Islamul Hadi Bambang Suryobroto
Kunio Watanabe

Received: 2 October 2012 / Accepted: 5 November 2012 / Published online: 18 November 2012
Japan Monkey Centre and Springer Japan 2012

Abstract In a series of field surveys of wild Javan


lutungs (Trachypithecus auratus sondaicus) conducted at
Pangandaran Nature Reserve in West Java, Indonesia, from
2011 to 2012, we tried to use a method of individual
identification by using individual-specific patterns of dark
pigmentation in the pubic area. During the 2011 dry season, we used a digital SLR camera with a 400-mm telephoto lens to photograph the pubic area of each individual
of a habituated group. These photographs were the basis for
identifying 14 different adult females. During the rainy
season of 2011 and the dry season of 2012, we checked the
presence/absence of each of the identified individuals and
found that these patterns were stable, at least during our
study period. We found that two adult females and one
adult female disappeared from the subject group between
the first and second and between the second and third
surveys, respectively, and that one adult female gave birth
between the first and second surveys, but the infant had
disappeared from the group between the second and third
surveys. We could not confirm the validity of the method
for juvenile females because of the dense white hair in their
pubic areas and the fact that few individuals had clear
patterns. Furthermore, we could not use this method for
Y. Tsuji (&)  K. Watanabe
Department of Ecology and Behavior, Primate Research
Institute, Kyoto University, 41-2 Kanrin, Inuyama,
Aichi 484-8506, Japan
e-mail: ytsuji1002@gmail.com
K. A. Widayati  I. Hadi  B. Suryobroto
Department of Biology, Faculty of Mathematics and Natural
Sciences, Bogor Agricultural University, Bogor, Indonesia
I. Hadi
Biology Study Program, Faculty of Mathematics and Natural
Sciences, Mataram University, Mataram, Indonesia

males because of the lack of pigmentation in the pubic


area. As patterns of pigmentation in the pubic area are
known to be present in other Trachypithecus species, our
method can be useful for identification of individual adult
females of these species, on which few individual-based
behavioral studies have been conducted. Collecting individual-based behavioral data would enable us to track the
presence of individuals in groups or movements between
groups; determine the effects of social rank and age on
within-group competition and copulation; and examine
population data.
Keywords Individual identification  Pangandaran
Nature Reserve  Pubic area  Spot pattern 
Trachypithecus auratus

Introduction
Identification of individuals is essential for documentation
of differences and measurement of behavior that forms the
basis of many lines of inquiry in behavioral ecology
(National Research Council 1981). Many primatologists
have conducted individual-based long-term studies of
many species and study sites, revealing not only fundamental life-history information, for example the timing of
sexual maturation, birth intervals, aging, and movements
between groups but also individual strategies or tactics
based on social and reproductive status (Koenig et al. 1998;
Pazol and Cords 2005; Kappeler and Watts 2012; Tsuji and
Takatsuki 2012).
Among primate species, very few individual-based
studies of colobines have been conducted. Until recently,
researchers have made a-priori assumptions that colobines
are egalitarian and that competition within or between

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groups over food resources rarely occurs because their


folivorous diet is widely available and distributed homogeneously, which would be expected to reduce within-group
competition (van Schaik 1989; Koenig 2002, but see Hladik
1977). However, recent studies have shown that colobines
feed not only on leaves, but also on fruit and flowers
(Matsuda et al. 2009; Dela 2012; Erb et al. 2012), and that
the availability of the latter often affects their feeding and
ranging behavior (Bennett 1986; Matsuda et al. 2009; Li
et al. 2010; Zhou et al. 2011). Indeed, because young leaves
are available in clumps, competition over these food
resources occurs (Koenig and Borries 2001; Harris 2006;
Fashing 2011; Kirkpatrick 2011). Therefore, many
researchers have started to pay attention to the social
composition of colobines to determine whether social
hierarchies exist with regard to the distribution of food
items among group members. These data would provide a
new perspective on the social system of colobine monkeys.
For example, Hrdy and Hrdy (1976) and Koenig et al.
(1998) demonstrated the existence of a social hierarchy
among female Hanuman langurs (Semnopithecus entellus)
and showed that the intensity of within-group competition
changes according to food type. The number of individualbased studies of colobines may be limited because their
dense, monochromatic hair and arboreal nature render discrimination of individuals difficult. Some researchers have
identified individuals by using clear injuries as marks (Wolf
and Fleagle 1977), but such natural signs do not remain on a
long-term basis and thus cannot be used as permanent signs.
Other researchers have used shape; differences in the
thickness, color, and form of tails, and differences in the
color and form of crests and whiskers (Sterck 1997; Matsuda et al. 2009; Minhas et al. 2010). Others have successfully identified several monkeys by color-marking their
tails (Teichroeb et al. 2005), but changes in pelage coloration may have long-term social effects in primate species
relying largely on vision (Teichroeb et al. 2005).
Furuya (1961) and Brotoisworo (1991), who conducted
studies of wild Trachypithecus species from the 1960s to
the 1970s, independently reported the possibility of identifying monkeys by use of individual-specific patterns of
dark pigmentation in the pubic area. Recently, similar
characteristics were also reported for T. phayrei, T. leucocephalus, and T. hatinhensis (Koenig et al. 2004; Jin
et al. 2009; Nadler 2010). This non-invasive method has
the potential to contribute to individual-based behavioral
studies of Trachypithecus monkeys, which is one of the
major groups of Asian colobines (Kirkpatrick 2011) and
about which little information regarding social systems is
available. In this study, we tried to validate the individualidentification method for wild Javan lutungs (Trachypithecus auratus sondaicus) inhabiting Pangandaran Nature
Reserve (PNR) in West Java, Indonesia.

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Primates (2013) 54:2731

Methods
Pangandaran Nature Reserve is located at 108400 E and
7430 S on the southern coast of West Java, Indonesia, on a
small peninsula about 3 km long and 2 km wide (Sumardja
and Kartawinata 1977). In 2008, eight groups of Javan
lutungs (ca. 140 individuals) lived within the public zone
(Mitani and Watanabe 2009). We followed members of
group A, which ranged throughout the northeastern part of
the public zone (Brotoisworo 1991). Group A comprised
24 individuals as of July 2011 (one adult male, 14 adult
females, eight juveniles, and one infant). The ages of all
individuals except for the infant were determined on the
basis of body size (length from head to rump), which was
measured using a park fence of known size as the reference
(adults, ca. 5070 cm; juveniles, ca. 3050 cm; Tsuji
unpublished data). The infant was easily identified because
of its orange hair. The monkeys in group A were not
provisioned but had been habituated to humans by the
many tourists who visit their home range almost every day.
We could therefore follow the monkeys from a distance of
\10 m without causing any disturbance.
We conducted three field surveys of group A between
2011 and 2012. The first survey was conducted from the
end of July to the middle of August (total observation time:
11 days or 117.5 h), which corresponds to the beginning of
the dry season. The second survey was conducted from
the middle of November to the middle of December of the
same year (20 days or 192.0 h), which corresponds to the
middle of the rainy season. Finally, we conducted a third
survey in April 2012 (10 days or 97.2 h), which corresponds to the early dry season. During each survey, we
continuously followed the monkeys in group A from 06:00
to 18:00 and recorded their activity and the food items
eaten every 10 min by use of scan sampling. We also
recorded the position of the center of the group with a GPS
receiver (GPS Map; Garmin, KS, USA). During each survey, we took photographs of the skin from several directions using a digital SLR camera (EOS Kiss Digital E5;
Canon, Tokyo, Japan) with a 400-mm telephoto lens (EF
100400 mm F 4.55.6 L IS USM; Canon). These photographs were taken when group members were resting on
tree branches or park fences and exposing their pubic areas.
Because the monkeys at PNR spent about half the day
resting (Brotoisworo 1991; Tsuji unpublished data), photographing them was relatively easy. We checked whether
each subject adult female had a neighboring juvenile or
infant, as an approximate evaluation of their kinship situation. At the field station, we checked all photographs and
identified the patterns of dark pigmentation in the pubic
area of each monkey and used these as the basis for reference sheets. We compared photographs taken in different
seasons to check the validity of the patterns. We also

Primates (2013) 54:2731

checked for the presence of each female and juvenile and/


or infant during different seasons for preliminary examination of population data.

Results
Figure 1a shows the pubic areas of different adult females
in group A. Adult females had sparse white hairs in the
pubic area. As Brotoisworo (1991) noted, each adult
female had a unique pattern of dark pigmentation in the
pubic area. During the first survey, in the dry season of
2011, we were able to identify 14 different adult females
on the basis of the shape, size, and location of the dark
pigmentation (Fig. 1a). During the second and the third
surveys, we found 12 and 11, respectively, of the 14 adult
females we had identified in the first survey. Furthermore,
we found one identified adult female who had given birth
during the second survey, but the baby was not in the group
during the third survey. During our surveys, no clear
change in the patterns of dark pigmentation in the pubic
areas of adult females was found.
On the other hand, the pubic areas of most of the
juvenile females were completely covered by dense white
hair, and underlying dark pigmentation could not be confirmed (the skin in the pubic area seemed to be white).
Thus, we could not identify individual juvenile females
during this study (Fig. 1b). Finally, adult and juvenile
males had no white pigmentation in the pubic area, so we
could not use this method for this group (Fig. 1c). We

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could easily discriminate males from adult females based


on the presence of penis and testicles. In the dry season of
2011, only one adult male and one juvenile male were in
group A, but a new, smaller adult male entered the group
during the rainy season of 2011 and stayed in group A
during the 2012 dry season.

Discussion
In this study, we confirmed that this method of identification of individuals is applicable to adult female Javan
lutungs in PNR. The patterns of dark pigmentation in the
pubic areas of adult females can be identified reliably,
serving to distinguish individuals. We also confirmed that
the patterns of dark pigmentation in the pubic area were
stable for at least 9 months (i.e., from July to the following
April), which implies that the long-term use of this method
is possible. In subsequent research, we need to confirm
whether these patterns are permanent.
Furuya (1961), Koenig et al. (2004), Jin et al. (2009),
and Nadler (2010) have reported similar unique patterns of
pigmentation in the pubic areas of other female Trachypithecus species. For example, the pubic areas of T. hatinhensis show clinal variation in the size of depigmented skin
regions, ranging from small to large patches (Nadler 2010).
On the other hand, the shapes of depigmented skin areas
below the navel vary in T. phayrei (Koenig et al. 2004).
Thus, our method may be applicable to other Trachypithecus species. Few researchers have yet successfully

Fig. 1 Patterns of dark


pigmentation in the pubic areas
of wild Javan lutungs in Group
A in the Pangandaran Nature
Reserve in central Java,
Indonesia: a 14 different adult
females, b one juvenile, and
c one adult male

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collected individual-based behavioral information about


Trachypithecus species because of difficulties with identification that are attributable to their dense, monochromatic
hair and their habitats (i.e., deep forests or rocky areas),
which are difficult to access. Although distinguishing the
patterns of dark pigmentation requires much time, our
method can be useful for identifying individuals (especially
adult females) even at relatively great distances. Similarly
to those conducting research on cetaceans and carnivores,
who have reliably identified and tracked the movements of
individual animals by photographing patterns of black and
white pigmentation on the ventral sides of tail flukes and/or
chests (Baker et al. 1987; Higashide et al. 2012), accumulating individual-based behavioral data would enable us
to track individuals presence in groups or movements
between groups; determine the effects of social rank and
age on within or between-group competition over dietary
resources, copulation, and reproductive strategies; and
examine population data, for example birth and survival,
all of which are important aspects of ecology and evolutionary biology (Clutton-Brock and Sheldon 2010).
Individual identification of adult females in PNR
becomes difficult when their pubic areas are covered by
leaves, tree branches, or other animals. Thus, to facilitate
identification, other physical markers, for example the
shapes of crests and muzzles, must be identified, as pointed
out by Koenig et al. (2004) for T. phayrei. Furthermore,
patterns of pigmentation are known to vary within a single
species: Hanuman langurs in Jodhpur had black perinea that
were not covered by fur, but individuals were nevertheless
reliably identified and observed successfully for several
decades (Mohnot et al. 1981), whereas female Hanuman
langurs in Kanha had spots that were used for identification
(Newton 1987). Detailed behavioral studies would enable
us to obtain additional reliable visual identification markers
applicable to all populations of a given species.
For T. auratus, the unique patterns of dark pigmentation
in the pubic area were clear among all adult females, but
they were unclear in juvenile females (Fig. 1). This age
difference has also been reported for T. hatinhensis (Nadler
2010). The reason for the presence of individually distinctive patterns of pigmentation in adult females only is
unclear. We speculate that these patterns reflect sexual
maturity; that is, dark pigmentation appears when juveniles
become adults and seems to have been selected during
evolution as a reproduction-related trait. In contrast with
macaques and chimpanzees, no obvious swelling of the
sexual organs is observed for Trachypithecus females; thus,
dark pigmentation may be an important visual cue. Longterm or comparative studies could answer these questions.
During our study, two adult females and one adult
female disappeared from group A in the 2011 rainy season
and the 2012 dry season, respectively. Two possible

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explanations for this can be proposed: they may have died


or they may have entered a neighboring group, as Thomas
langurs (Presbytis thomasi) do (Sterck 1997). Because we
did not conduct behavioral observations of neighboring
groups, we could not investigate the latter possibility. If the
females had emigrated after the original dispersal, we
would be forced to view their social system as more
complex than we had originally thought. Further data are
needed to evaluate this possibility. From this perspective,
our method may be applied to other populations and/or
species.
Acknowledgments We would like to thank the forest rangers of
PNR, especially Mr Yana Hendrayana, for access to their facilities,
and Mr Bambang Prayitno, for his assistance during our fieldwork.
We also thank the staff of the Department of Biology of Bogor
Agricultural University, Drs F. Bercovitch, A.F. Dixson, K. Wada,
and C.M. Huang, and an anonymous reviewer for their constructive
comments on an earlier version of this manuscript. This study was
funded by a grant from the AS-HOPE of the Japan Society of Promotion of Science to Y. Tsuji (20102011) and by a Grant-in-Aid
from the Department of Academy and Technology of Japan (nos
23780160 and 24405018).

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