Reviewed Article
Folia Primatol 2002;73:1–20
Received: June 8, 2001
Accepted after revision: November 26, 2001
The Social Organisation of a Population
of Sumatran Orang-Utans
Ian Singleton a
Carel P. van Schaikb
a
Durrell Institute of Conservation and Ecology, University of Kent at Canterbury,
UK; b Department of Biological Anthropology and Anatomy, Duke University,
Durham, N.C., USA
Key Words
Sumatra ` Orang-utan ` Social organisation ` Swamp forests ` Social groups
Abstract
Female orang-utans in a Sumatran swamp forest live in large, but stable,
and widely overlapping home ranges. They preferentially associate with some of
their female neighbours, possibly relatives, to form socially distinct clusters that
also experience reproductive synchrony. Sexually mature males range more
widely than females, but among them the dominant adult male has a relatively
more limited range. His ranging and that of the subadult males reflect the local
abundance of sexually attractive females. The other adult males tend to avoid
these concentrations and focus on areas away from the dominant male. Females
show philopatric tendencies. Male-biased sex ratios at birth give way to heavily
female-biased sex ratios among adults. This suggests a net loss of males as
they mature, due either to excess male mortality (e.g. by male mating competition), excess male dispersal from the population or a combination of both. We
conclude that the orang-utan social organisation is best described as a loose
community, showing neither spatial nor social exclusivity, consisting of one or
more female clusters and the adult male they all prefer as mate.
Copyright © 2002 S. Karger AG, Basel
Introduction
Social organisation generally refers to the spatiotemporal distribution of individuals in a population. Most diurnal primates form social groups that vary considerably in size and cohesiveness and in age and sex composition. In some species
there are also characteristic intergroup associations [1]. Despite this complexity in
Ó2002 S. Karger AG, Basel
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Carel P. van Schaik, Department of
Biological Anthropology and Anatomy, Duke University
Box 90383, Durham, NC 27708-0383 (USA)
Tel. +1 919 660 7390, Fax +1 919 660 7348
E-Mail carel.vanschaik@duke.edu
group sizes and structures, however, some form of social organisation above the
individual level is almost always found. Nevertheless, a possible exception to this
among diurnal species may be the orang-utan, whose social organisation remains an
enigma. Even after several decades of work, it is not clear whether any higher-level
social units, beyond the mother-infant dyad, can be recognised in this species [2, 3].
Indeed, their semi-solitary lifestyle may be most similar to the social organisation
of nocturnal mammals, including many prosimian primates [4].
The apparent absence of social units in orang-utans is remarkable, not only
because all other anthropoids show clear-cut social units, but also because recent
work suggests that some orang-utan populations exhibit fission-fusion behaviour.
Van Schaik [5] proposes that female orang-utans, at least at the swamp site of Suaq
Balimbing in Sumatra, can be regarded as an example of an individual-based fission-fusion system, in that they form travel associations (parties) more often and
for longer periods than would be expected by chance. These parties not only include sexual consortships, but also involve multiple females with offspring
(‘nursery groups’). In other primate species with fission-fusion behaviour, distinct
social units, usually called communities, can be recognised (e.g. chimpanzees [6–
8], spider monkeys [9, 10] and woolly spider monkeys [11]). A community includes all individuals that are regularly seen over months in temporary subgroups
called ‘parties’ and share a common home range. Although no spatially distinct
communities can be recognised within orang-utan populations [12, 13], the possibility remains that socially distinct communities do occur, based on preferential
association.
The aim of this paper is to describe the social organisation of the orang-utans
at Suaq Balimbing, where both high home range overlap [13] and high rates of association [5] relative to other sites [14–17] provide excellent opportunities to detect
social units if they exist. We will follow the socio-ecological paradigm [18, 19] and
begin with a consideration of female distribution and associations. Female orangutans are not territorial. At Suaq Balimbing their home ranges are very large
(approx. 850 ha) and show virtually complete overlap with many other females, as
well as numerous males [13]. We examine the evidence for clustering of female
home ranges and ask whether females of the same cluster show physical similarity
and reproductive synchrony. We also explore the implications of these range sizes
and how they can be used, alongside density estimates, to elucidate valuable information on orang-utan sex ratios.
In animals that are largely solitary, and where territoriality is impossible to
achieve, the nature of male-male competition and female mating preferences are
likely to determine both the mating system and the social structure. We show that
the range use of orang-utan males is dictated by the presence of receptive females,
but that different classes of males have different mating strategies and thus different association tendencies.
We also provide evidence for a net loss of males from the population as it matures and end by discussing the implications of our findings for orang-utan social
organisation and social structure. The role of female mate preferences emerges
once again as pivotal, but its adaptive significance remains unknown.
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Singleton/van Schaik
Fig. 1. Map of the study area. The stippled area denotes hills. The dense trail system to the
north is the Wildlife Conservation Society (WCS) study area. Trails to the south and east of
this were added in late 1996 and represent the ‘expanded’ study area.
Methods
This study was conducted at the Suaq Balimbing Research Station (03º04' N, 97º26' E),
in the Kluet region of the Leuser Ecosystem (formerly Gunung Leuser National Park). Data
on orang-utan movements were amassed during focal animal follows between June 1994 and
September 1998. The majority of follows took place within the basic Wildlife Conservation
Society (WCS) study area (fig. 1), but from February 1997 some individuals were also followed outside it, in the expanded study area. Within the WCS study area, the routes taken by
focal individuals were plotted on maps of the trail system at frequent intervals during all
follows, using compass bearings and distance estimates. The position of the animal and the
time were also noted on these maps every 30 min. Furthermore, the identity and location of
any other individuals encountered within 50 m of the focal animal were also recorded, along
with times of approach and departure. Each time a trail was crossed, the accuracy of these
maps could be verified. During follows outside the WCS study area, similar data were plotted on a grid, with cells measuring 100 m × 100 m, and the orang-utan’s actual location was
Orang-Utan Social Organisation
Folia Primatol 2002;73:1–20
3
recorded at sporadic intervals (when weather and forest cover permitted), using a hand-held
GPS (Global Positioning System) receiver. The GPS positions were then located on a
1:50,000 scale topographic map of the entire study area, and the approximate route taken
between positions was inserted from the grid maps produced in the field. Again, routes could
be verified whenever some of the less common trails outside the main WCS study area were
crossed. Using this procedure, routes plotted between GPS fixes were considered reasonably
accurate.
All follow maps were subsequently stored in ARC/INFO GIS software both as routes
(lines), allowing distances and velocities to be measured, and as 30-min points (i.e. the location of the focal individual every 0 and 30 min past each hour, regardless of the time the
follow began or ended). Subsequent examination of ranges used primarily the 30-min point
data. It was also possible, using GIS, to assign the 30-min point locations of focal individuals to any other individuals that were known to be less than 50 m away at the corresponding
times. Hence the total number of 30-min point locations for an individual includes data from
both when they were themselves the focal individual being followed and data from when
they were not, but were within 50 m of a focal individual. Some individuals were also encountered during other work (i.e. as casual observations), and a small number of these records were included in the analysis, particularly if such encounters were at locations not previously known to lie within their range.
Measuring Range Overlap
Using the data obtained from the above methods, it was possible to discern a polygonal
range area for each female simply by joining all of the points known to be within their home
range with straight lines. For a fuller description of the methods used, see Singleton and van
Schaik [13] and Singleton [20]. Thus, all adult females possess a polygonal range, of which
a portion of measurable area lies within the WCS study area. Furthermore, each female (of
those that were followed on at least 10 separate follows of over 3 h duration) utilised a home
range that overlapped the ranges of all other such females. It is therefore possible to calculate the size of the overlapping area as a crude estimate of the percentage of a female’s true
range that overlaps with that of each other female. This then permits an investigation to
determine if a relationship exists between the degree of range overlap between two females
and the amount of time they spend in association with each other. As an example, an individual A may have a polygonal range that totals 500 ha, of which 300 ha lie within the
boundaries of the WCS study area. Likewise, individual B may have a polygonal range of
600 ha of which 400 ha lie within the WCS study area. In such a scenario, a part of the 300ha portion of A’s range may lie within the 400-ha portion of B’s range. If that part was
200 ha, then it could be inferred that individual A shares two thirds, or 66.6%, of her range
with individual B. Naturally, when calculating percentages in this manner, the values are not
symmetrical between individuals as the percentage of individual A’s range that lies within
individual B’s is not the same as the percentage of B’s lying in A’s. Hence two values are
calculated for each combination.
Estimating Expected Association Rates
The focal animal samples yielded the percentage of time that each focal individual was
in association (<50 m) with other named independent animals. Party sizes can easily be calculated as 1 + the sum of the association values per individual [5, 20]. We can use the ranging information to calculate the expected time of association of one individual with another
using the following equation, which corrects for the observed association tendency:
Aij =
Qij
Σ Qij
× Σ Lij
j
j
where Lij = the proportion of individual i’s total follow time spent with female j, Qij = the
proportion of the target individual’s (i’s) range that is overlapped by that of individual j. NB:
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Singleton/van Schaik
ΣQij (the ‘overlap index’) may be greater than 100% as several individuals are included, and
ΣLij (the ‘association index’) may be greater than 100% as females can associate with several other individuals simultaneously.
As an example, if female B’s range covers 30% of A’s, C’s covers 30% and D’s covers
60%, then A’s overlap index would be 120%. Similarly, if A spent 60% of her time with B,
60% with C and 60% with D, then her association index would be 180%. However, the expected time of association with B, taking into account A’s association tendency, would be
only:
30
× 180 = 45%
Aij =
30 + 30 + 60
Thus, the conclusion would be that A spent a greater proportion of her time in association with B than expected.
Results
Female Home Range Clustering
Singleton and van Schaik [13] found that female home ranges at Suaq Balimbing were stable over several years, overlapped those of many other females and
were large, at least 850 ha in total with core areas of over 500 ha. Indeed, most, if
not all, females clearly had home ranges that were larger than the WCS study area.
Nevertheless, many females did appear to have range boundaries within the WCS
study area and seemed to consistently leave or enter it in the same border zone and
in the same general direction. Thus, we were able to classify the females with respect to the approximate position of their home range.
We also gained the impression that the coincidence of range boundaries among
some ‘subgroups’ of females was more than would be expected by chance or attraction to the same resources, since they remained stable over many years [13]. For
example, the ranges of Pelet, Diana and Becky in the north-west and those of Abby
and Karen in the north-east appeared to share very similar range boundaries. Some
females’ ranges also seemed to be located in the same general area (e.g. Ani, Tevi,
Mega, Una, Novi, all of whose ranges covered most of the central portion of the
WCS study area; figure 10 in Singleton and van Schaik [13]). We adopted the term
‘cluster’ to refer to these apparent ‘groupings’ of females.
To describe these clusters, the following approach was taken. We first generated clusters based on range use (more specifically the location of their core areas)
and then evaluated their validity by testing the distribution of other features over
these clusters. Home range centroids were calculated for each female, using the
mean x and y coordinates of all points (generally 30-min points; see Methods)
known to lie within their range. Figure 2 shows the location of these weighted centroids for each adult female. Because the station was located in the north-west corner of the WCS study area, far more data were collected in the northern half of it,
and as a result there were fewer follows of females in the south. For this reason,
several females who were known (from party data and other occasional encounters)
to be residents of the southern parts of the WCS study area were not included due
to a lack of ranging (follow) data pertaining to them. Some other individuals may
have been missed altogether. Thus, the lower density of home ranges (and hence
centroids) in the south is simply an artefact of the reduced coverage there.
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Folia Primatol 2002;73:1–20
5
Fig. 2. Map showing the location of range centroids for all adult females.
Figure 3 provides the dendrogram of a cluster analysis based on females with
at least 10 follows of 3 h or more duration. As with the range centroids, it uses the
mean x and y coordinates for each female as its data set. Two clear clusters appear
to be discernible. The first contains the northern females, in two subclusters, corresponding to a north-western (Diana, Becky, Pelet and Una) and north-eastern group
(Karen and Abby). All of these females have clear and stable range boundaries in
the northern half of the study area. The second cluster contains the central and
south-western females (Ani, Tevi, Hanes, Sela, Butet and Mega). As stated, some
other southern females did not enter this analysis because of insufficient follows.
Thus, it appears that there is a real distinction between clusters of females from
different areas, at least between those from the north-west, north-east and south.
The next question, therefore, is whether these clusters are merely a reflection of
home range location, or whether the females at Suaq Balimbing show clear tendencies to associate preferentially with some of their most immediate neighbours.
Female Association Patterns Controlling for Range Overlap
Meaningful association patterns are unlikely if individuals meet others simply
as a result of random movements within and throughout their highly overlapping
home ranges. Thus, the first step in this analysis is to examine whether females
generally show stronger tendencies towards association than expected on the basis
of chance movements alone. Van Schaik [5] has already shown that the mean party
size for this population was far in excess of what would be expected solely on the
basis of chance encounters (using Waser’s gas model [21]) and that associations
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Singleton/van Schaik
Fig. 3. Wards method cluster diagram using females with 10 or more follows of 3 h
duration or more.
were not simply passive aggregations in fruit trees. Instead, they largely represented actively maintained travel parties. Singleton [20] repeated this analysis for
each individual separately (and using a larger sample). He found that all but one of
the 32 individuals of both sexes tested (with at least 10 follows of over 3 h duration) had an encounter rate above that expected by the gas model. Therefore, associations may potentially reflect individual preferences.
Associations between two individuals, if merely reflecting a general tendency
to seek company, should be proportional to the degree to which their home ranges
overlap. For this reason, expected association values (Aij) were calculated based on
the observed degree of (qualitative) home range overlap in the study area (see
Methods). The observed proportion of each female's time that was spent with each
other female (Lij) was then divided by the expected value based on range overlap
(Aij). This therefore produced observed/expected ratios for each pair of females
(table 1). Figure 4 connects all those pairings of females who show reciprocated
ratios of greater than 1 (i.e. the ratio is greater than 1 for each female), suggesting
preferential association between them. This sociogram again shows the two previously noted clusters, indicating that home range overlap alone cannot explain their
associations.
A more formal way of testing whether females preferentially associate with
others within their cluster is to assess whether each female’s top three Lij/Aij ratios,
provided they are greater than 1, are more likely to be with females from their own
cluster than with females from the other cluster. Of 33 top three ratios that were
greater than 1 (out of a possible total of 36; table 1), 24 pairings were with females
from the focal individual’s own cluster and 9 with females from the other cluster.
This difference is highly significant [expected values were 15 and 18, respectively,
because females are slightly more likely by chance to associate with a female from
the other cluster: χ2 (d.f. = 1) = 9.90, p < 0.01]. This analysis confirms the conclusion that females preferentially associated with members of their own cluster.
Orang-Utan Social Organisation
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7
Fig. 4. Sociogram connecting pairs of females whose association tendencies exceeded
chance levels in both directions.
Are Cluster Members Relatives?
If relatives settle in neighbouring ranges and preferentially associate with each
other, then cluster members should be more similar genetically. We were struck by
the remarkable physical similarity between some of the females within clusters.
Indeed, in some cases we could only distinguish them on the basis of subtle characteristics (e.g. scars, injuries, age, sex of infants).
The following pairs or multiples of females were considered to have very
strong physical similarities: Abby – Karen; Andai – Betty; Butet – Hanes – Novi –
Sela; Diana – Pelet; Molly – Rini – Adf49. It is clear that all of these combinations
were members of the same cluster. Andai is Ani’s daughter and Betty is Butet’s
daughter; both mothers are in the same cluster. Not enough ranging data were collected on Novi, but our impression was that she appeared to range in the same general area as the females in the southern cluster (fig. 2) and associated with these
females. Molly, Rini and Adf49 are all south-eastern females. Thus, cluster members are considered likely to be genetically related.
Timing of Reproduction in Female Clusters
There was a tendency for females ranging in the same part of the entire study
area (i.e. the combined area of the WCS and expanded study area) to have infants
of the same size. We therefore compared the observed or estimated birth years of
the youngest infants of all of the known females that could confidently be assigned
to a cluster. In table 2, all of these females were divided into three groups, based
either on the location of their range centroids, if enough ranging data existed, or on
the locations of relatively few encounters with them. The first two correspond with
the two clusters of figure 3, with the addition of two others as central females.
These were Novi, who gave birth in 1996, and Sara, who was not seen to have
given birth (and hence not assigned a year in the table) but quite possibly did so
around 1996 as her previous infant was of a similar age to Novi’s. Sara is therefore
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Singleton/van Schaik
Table 1. The ratio of observed to expected time each focal female spent in association with each other
female (i.e. Lij/Aij, see Methods)
Focal
female
Abby
Ani
Becky
Butet
Diana
Hanes
Karen
Mega
Pelet
Sela
Tevi
Una
Abby
3.022
3.695
0.07
0.922
0
12.33
0.742
1.088
4.382
0.143
12.01
Ani
Becky
Butet
Diana
Hanes
Karen
Mega
Pelet
Sela
Tevi
Una
1.336
2.219
2.296
0.016
0.327
0
3.347
1.029
3.739
2.746
0
0.3
0
1.386
0
1.515
0.252
0
0
0
0
0.998
2.063
0
4.104
0
3.976
0
0
0.405
0
0
0
0
0
0
0.553
0.306
0.68
0.51
0
0
0
0.936
0
0.061
1.195
0
0.341
1.012
0.497
0
0.078
0
0
1.362
0.556
0.205
0
0.375
0
0
0.42
2.133
0.948
0
2.46
0.261
0.838
0.489
0
2.015
3.204
1.441
4.488
0.926
0
4.183
0
0
0
1.998
3.956
0.099
1.797
2.11
2.507
0
2.413
1.571
0
1.093
0
0.073
0
0
0
0
0.131
1.124
0
1.024
0
1.215
1.895
0
0
0
0
0
0
0
0
0.065
0
0
0
0
0
0.107
0
Table 2. Number of births by year, for females residing in different parts of the study area
Location
1990
North
Central
South
1
1991
1992
1993
1994
1995
1996
1997
1
61
1
1
1
3
7
1
1
North = Cluster 1 in figure 3; Central = cluster 2 in figure 3, plus Novi and Sara (but
Sara was not known to give birth in the 1990s, although she did possibly do so in 1996);
South = all southern females (see fig. 2).
1
Sela was last seen in July 1996, when clearly pregnant.
the only female not known (or inferred) to have given birth in the 1990s. Another
of the central females, Sela, was included despite not actually being seen with a
new infant, as she was confirmed to be pregnant when last seen in July 1996, using
a pregnancy test kit on urine [E.A. Fox, pers. commun.]. The third cluster is composed of the southern females, for whom there were insufficient follow data to warrant inclusion in the previous cluster analysis, but whose ranges showed clear-cut
northern boundaries in the southern part of the WCS study area. Naturally, the age
of the majority of infants could only be estimated, using prior knowledge of the
size and behaviour of infants of known ages. Nonetheless, the timing of birth peaks
was clearly different. If we group the data into 2-year periods, to create high
enough expected values, the overall analysis shows significant heterogeneity in the
timing of births among the three groups [χ2 (d.f. = 6) = 18.66, p < 0.005].
Northern females had a clear birth peak around 1992, the central females were
sexually active throughout 1995, most subsequently giving birth in 1996, and the
southern females clearly underwent a birth peak around 1991. The deviations from
these peaks are in part due to nulliparous females being out of phase with others in
the same areas. Thus, the indications were that this was a long-term phenomenon.
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Folia Primatol 2002;73:1–20
9
The data also allow an estimate to be made of interbirth intervals. For example, the northern females became sexually active again in 1999 and most infants of
the central females had initially (in 1994) been estimated as having been born
around 1988. Furthermore, the southern females were sexually active again during
the second half of 1998 and the dominant adult male, Arno, was spending much
time consorting with them at that time (see below). These observations are therefore consistent with interbirth intervals of approximately 8 years in this population,
as reported elsewhere [22].
Male Home Ranges
Earlier analyses at this site have confirmed the finding of all previous orangutan studies, in that male home ranges tend to be far larger than those of females
[13], with a minimum size of approximately 2,500 ha, but possibly considerably
larger. This pattern holds for both adult (flanged) and subadult (unflanged) males,
although some of the latter may in fact have been truly transient [13]. Obviously,
the large male home range size is not due primarily to ecological factors. Instead it
seems that male home ranges are largely determined by the distribution of mating
opportunities.
Observations from Suaq Balimbing clearly indicate that subadult males search
for females over a large area and attempt to mate with those whose infants are large
enough to suggest a return to ovarian activity [23]. The ranges of subadult males
overlapped widely and were therefore not exclusive. Up to 30 individuals could be
seen in the central part of the WCS study area during the course of this study. All,
except adolescent and sometimes subadult, females attempted to avoid or resisted
matings with subadult males. Subadult males, therefore, often resorted to force in
order to obtain matings [23], and these forced matings were especially successful
when the subadult males were larger than the females they were trying to overwhelm.
Adult males did not defend exclusive home ranges either. Indeed, some 15
different adult males visited the WCS study area, and 9 were known to have passed
through the central part of it. They also had very large home ranges [13]. Not all
adult males followed the same reproductive strategy, however. Females with ovarian activity tend to approach attractive adult males, usually the dominant adult male
[23–25]. As a result, non-dominant adult males obtained virtually no matings at all
with receptive females during the study period [23; C.P. van Schaik, unpubl. data].
The dominant adult male in the study area, Arno, also appeared to cover much less
territory than other adult males [20]. Although he was known to cover the entire
study area and was often absent for brief periods, the frequency of his returns (his
presence was recorded in 83.3% of 48 monthly samples) and the limited number of
encounters with him in the expanded study area suggested that Arno’s range was
relatively limited in extent, most likely around 1,500 ha [13]. Furthermore, during
one of his longer absences, he was observed in active consortships with at least 4
females in the area just to the south of the WCS study area, but adjacent to it, and
hence had not travelled far.
Male Presence
The central females in the study had been sexually active from late 1994 onwards, until most of them gave birth in mid to late 1996. After that, virtually no
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Table 3. Summed monthly presence indices of each age-sex class, period I
(June 1994 to May 1996) versus period II (June 1996 to May 1998)
Age-sex class
Period I
Period II
Change of II
relative to I
Adult female
Subadult female
Subadult males
Arno1
Non-dominant adult males
153
55
138
23
27
155
43
114
18
49
+1
–22
–17
–22
+81
Total
396
379
–4
Note: Monthly search and follow effort were similar: mean of 52.2
field unit days in period I versus 46.8 in period II.
1
Locally dominant adult male.
sexual activity took place inside the WCS study area, with the exception of the nulliparous female Becky. Becky conceived in February 1997, when she was seen consorting with the dominant adult male. Thus, if male visits to particular parts of their
range are in response to the presence of fertile females, we should expect to see
clear differences between the period before June 1996 and afterwards (periods I and
II in table 3, respectively). Indeed, a comparison of the monthly presence of the
main age and sex groups in the WCS study area showed some interesting patterns
(table 3), and the relative change between the two periods can be used to examine
the differential range use of males.
As expected, adult females remained approximately constant through both
periods with regard to their presence in the study area. The decline in subadult females can be attributed to one maturing to adulthood (Becky) and a small number
of others which appeared sporadically near the northern edge of the study area during period I. These may well have been temporarily exploring the edges of their
natal ranges before selecting areas to serve as adult home ranges. The high degree
of sexual activity in the study area and the presence of the dominant adult male at
the time may also have temporarily attracted them there. The total orang-utan presence in the study area also remained approximately constant through both periods.
However, the pattern of male presence underwent a dramatic change. Whereas
Arno was present in virtually every month in period I, his presence went down in
period II. Subadult males responded in the same way to the reduction in the availability of fertile females. Other adult males, however, showed an increase in presence, even though there were fewer mating opportunities in the study area.
Sex Ratios and Inferred Mortality
Individual females living in the centre of the study area can expect to encounter at least 9 individual adult males and some 30 individual subadult males in a 5year period, as well as a number of others nearer the peripheries of their ranges.
Some of these subadult males are residents inside a very large home range, whilst
some are likely to be transients, travelling around in search of a range to settle in.
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11
Table 4. Estimated population sex ratio (expressed as the proportion of
animals that are males, i.e. m/m + f), among fully adult males and females
and among sexually mature/active males and females (thus including
subadults of both sexes), based on point estimates of their densities
Age-sex class
Number with
overlapping
ranges
Adult females
Subadult females
Adolescent females
Adult males (minus Arno)
Arno
Subadult males
Adolescent males
Infants
16
6
3
8
1
30
4
14
Total
82
Home
range, ha
0,850
0,950
0,850
2,500
1,500
2,500
0,850
0,850
Overall density
Density
km–2
1.882
0.632
0.353
0.320
0.067
1.200
0.471
1.647
6.571
Sex ratio, fully adult only: 0.17; sex ratio, all sexually active: 0.39.
To obtain an estimate of the potential intensity of mating competition we need
to estimate the adult sex ratio. For this, we cannot simply take the observed numbers of each age-sex class because of appreciable differences in range size and perhaps degree of range overlap too. Hence, we should first estimate the density for
each class and then determine the sex ratios using the density figures. The procedure for this is as follows.
The observed number of named individuals inside a single 4 ha grid cell in the
centre of the WCS study area provides a point estimate of the local population composition. Using our best estimates of home range size [13], we can then calculate
the density in the area for each age-sex class. The resulting, relative female and
male densities provide the best estimate of the population sex ratio, which is expressed here as the proportion of males.
Table 4 shows the results of this exercise. Local sex ratios (expressed as the
proportion of animals that are males) are estimated to be 0.17 (i.e. around 4.9 females per male) for fully adult individuals and 0.39 (i.e. around 1.6 females per
male) if all sexually active individuals are included. Minor changes in the various
estimates of range overlap and home range do not substantially alter these estimates.
Among 25 named females with infants (including infants born during this
study), the infant sex ratio was 0.56, i.e. slightly male-biased. If males and females
reach the subadult phase at approximately the same age, this implies excess male
mortality of 44% [i.e. (0.56/0.39) – 1].
12
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Discussion
Female Clusters
We found evidence for clusters of females, who may well be related, and
whose ranges share similar boundaries with considerable overlap. Within these
clusters they also show a tendency toward reproductive synchrony, as they have
infants of similar ages, and preferential association with each other, even if home
range overlap is taken into account. Furthermore, they also show a tendency toward
simultaneous presence or absence in the study area as a whole [13, 20]. This could
easily be explained by convergence on particular food resources by females whose
ranges grant them access to them [13]. Nevertheless, the results still show that mutual attraction between females exists within clusters and that movements of females within clusters are to some degree coordinated, even when not in close association.
It is important to note here that the measure of range overlap used in weighting
association rates is necessarily crude. This is largely because the location of a female’s range boundaries outside the WCS study area cannot normally be known
with certainty. However, we suggest that the method used will almost always overestimate true range overlap because only females with sufficient follow data (and
hence a high number of encounters within the study area) were used in the analysis.
Any females whose ranges only slightly overlapped the study area were excluded.
Hence, whenever there are two females whose ranges both overlap the WCS study
area to a large degree, they also tend to overlap each other’s ranges to a large degree within it, regardless of the location of their range boundaries and the orientation of their ranges outside it. To test this, for three of the females (Ani, Mega and
Butet, whose ranges are well known even outside the WCS study area), we calculated the size of the overlapping area using polygon and circle estimates of entire
ranges (see Singleton and van Schaik [13] for a description of these methods). In all
cases (12 possible permutations), the estimates of overlap using the previous
method were higher than those obtained using the larger ranges. For this reason, we
can state with some confidence that if two individuals associate with each other
more than expected it is even more likely that this is a genuine phenomenon, since
the method is highly conservative.
The female clusters that can be distinguished are not real in the spatial sense
(as with groups of other primates), but they are real in the social sense, as in many
strepsirhines [4]. Thus, the female cluster can be regarded as the basic social unit in
orang-utans. In the absence of formal analyses, evidence for female clusters based
on preferential association cannot yet be claimed for other sites, where female
range overlaps and association rates tend to be much lower. It is considered likely,
however, that Suaq Balimbing is not atypical and that the higher densities that occur there are a direct result of more optimal conditions. Indeed, the results of Suaq
Balimbing may be entirely consistent with observations at other sites.
This female ranging pattern supports the notion of a tendency toward female
philopatry in orang-utans [12], unlike the pattern observed in African apes and
unlike what is often reported in reviews [26, 27]. Several authors have noted that as
adolescent (or subadult) females mature into adults, they settle in ranges that are
overlapping or adjacent to their natal range [16, 18]. The observations at Suaq
Balimbing support these records. They also concur with previous reports on wild
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13
orang-utans in a number of other ways: males are much more wide-ranging than
females, subadult males are more likely to be transients that pass through the area
only once during a period of dispersal, adolescent females are often seen associating with their mothers whilst adolescent males return less and less, and birth sex
ratios are slightly male biased (see below). Given the consistency of these findings
across study sites, female philopatric tendencies are increasingly likely to be the
norm in orang-utans but still need to be confirmed by the results of ongoing genetic
studies.
The benefits derived by females from forming preferential associations with
particular females, presumably relatives, are not clear. Despite many years of fieldwork, not a single case of coalition formation has been observed. Food sharing
among adult females on the other hand, whilst rare, does seem to be concentrated
among members of the same cluster [C.P. van Schaik, unpubl. data]. Also, the acquisition of new skills, especially those related to foraging, requires socially tolerant gregariousness [29], and tolerance is probably increased in parties containing
relatives.
The reproductive synchrony observed may largely be a passive consequence of
shared local phenology [30], i.e. if the timing of conception reflects the nutritional
status of each female, and hence the productivity of the forest within her home
range, then, by default, those that possess overlapping home ranges would be expected to be receptive during similar periods. Nevertheless, synchrony would almost certainly increase the ability of the local dominant male to sire most of the
cluster’s infants because the presence of multiple sexually attractive females keeps
him in the local area. It is therefore also conceivable that reproductive synchrony
increases protection from the male during the early development of infants (see
below).
Male Mating Strategies and Ranging
Differences in male range use and their response to the local abundance of
fertile females shows that three categories of males exist: (i) the dominant adult
male; (ii) the subadult males, and (iii) the other adult males. Each of these categories adopts a different mating strategy. This pattern is compatible with the emerging
consensus of alternative mating strategies, in which adult males are able to monopolise voluntary matings with sexually receptive females, and subadult males
search widely for females and attempt to mate with them, if necessary by force [2,
23, 25, 31, 32]. However, it also indicates an unexpected differentiation among the
adult males.
The dominant male, being preferred by females, should always go to where
fertile females are present within his range. He is sought out by peri-ovulatory females as are dominant adult males at other sites [15, 16, 24, 31, 33] and forms
long-term voluntary consortships with them. Arno has a high rate of matings, all of
which are voluntary or even initiated by the female [23]. His range is limited to a
fairly small area in which the females know him well enough to prefer him immediately (without having to await proof from conflicts with other males), and in which
he is least likely to miss receptive periods amongst the females. By limiting his
range, he also minimises the risks of injury from conflicts with unknown powerful
males whose ranges are centred elsewhere.
14
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Singleton/van Schaik
In contrast, other non-dominant, but fully adult, males stand very little chance
of obtaining matings in the area in which the dominant adult male is actively guarding fertile females [23; C.P. van Schaik, unpubl. data]. Subadult males are agile
enough both to force matings and to avoid being chased off by the dominant male,
but the larger adult males must rely on being selected by the females. However, the
dominant adult male relentlessly chases any long-calling (adult) male from the vicinity of fertile females, if they approach. Thus, all the non-dominant adult males
achieved no matings in 426 h of focal sampling (data cover 1994–1996, when rates
were last analysed), whereas both the dominant male Arno and Tomi (a newly
flanged adult male who remained unchallenged by Arno) had rates of around 0.028
matings per hour (in 1,194 and 212 h, respectively), and the subadult males had a
mean rate of 0.045 (in 979 h). It is therefore understandable that these other adult
males tend to actively avoid the dominant adult male. Instead they appear to concentrate their efforts on areas where the dominant adult male is absent (either because he is elsewhere or has died) and range more widely in doing so. Nondominant adult males may possibly still gain occasional matings with females that
are asynchronously receptive, especially subadult females.
Subadult males are highly mobile and track the availability of fertile females
throughout a large range. As stated, because they are not preferred by females they
attempt to mate whenever they can. They therefore exhibit high rates of mating,
even though attempts to mate are usually resisted by the females [23]. When the
females are receptive, however, the locally dominant male is in a voluntary consortship with her, and subadult males, while closely following the pair, can achieve few
matings with receptive females [23]. Hence, we expect relatively few infants sired
by subadult males. Indeed, data from Ketambe suggest that all observed conceptions take place in voluntary consortships [24], although some of these were with
subadult males.
Delgado and van Schaik [3] note three major differences in sexual behaviour
and demography between Bornean and Sumatran sites. First, consortships with
adult males can last weeks in Sumatra but only a few days at most in Borneo. Second, the great majority of observed matings in Borneo are forced, whereas forced
matings account for less than half of the observed matings in Sumatra. Finally, the
number of adult males recorded for study sites in Borneo exceeds that of subadult
males, whilst in Sumatran study sites the opposite is true. They explain these differences by suggesting that the dominant adult male in Sumatra can maintain long
consortships and thus monopolise matings, reducing the time during which the female is exposed to other males and hence forced matings. In response, subadult
males at the Sumatran sites may opt to slow down their development into full adulthood until a time when they may have a good chance of becoming dominant themselves.
Van Schaik and van Hooff [12] concluded that only two plausible models for
the orang-utan mating system exist, both of which are partly consistent with the
published evidence. The first of these is a roving male promiscuity system [19] in
which males cannot defend access to female ranges and females do not congregate
at predictable areas. Thus all males have large and widely overlapping ranges
within which they search for receptive females. The second is a spatially dispersed
but socially distinct community organised around one dominant adult male. If the
pattern of interisland differences noted here and its interpretation stand up to fur-
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15
ther scrutiny, the first mating system may apply more to the Bornean sites and the
second more to sites in Sumatra. If so, we can predict that the locally dominant
Bornean adult male should show less difference in his range size and range use,
when compared to other adult males, than do those in Sumatra. However, Galdikas
[31] also noted that adult males appeared to have relatively restricted ranges during
periods of ‘residence’ (and presumably of dominance too) at Tanjung Puting, but
these periods may be rather brief compared to Arno’s residence.
A major unsolved question in orang-utan socio-ecology is what benefits females derive from their strong mating preferences against some males, but in favour
of the dominant adult male in an area. Delgado and van Schaik [3], after reviewing
several possible functions, suggest that the available data are most consistent with
the speculative idea that the advantage to females of their mating preferences is protection against infanticide by the dominant adult male, at least in Sumatra.
Sex Ratios and Mortality
As at Suaq Balimbing, birth sex ratios at other study sites have also been
found to be male biased. The sex ratio among wild births at Ketambe was strongly
male biased (proportion of males 0.78; n = 9 [22]), as was the birth sex ratio among
infants born to rehabilitants at Bohorok, at 0.63 (n = 16 births [Riswan, pers. commun.]). If all the data on infants from Suaq Balimbing are combined (i.e. including
the offspring of the 25 named females; see earlier), we obtain a proportion of males
at birth of 0.62 (n = 50), which is significantly different from 0.50 (binomial test, z
= 2.16, p < 0.05). This gives a weighted mean birth sex ratio of 0.64 for wild females.
The strong male bias in birth sex ratios is not apparent in zoos despite a much
larger sample (all births since 1980: 0.512, n = 755 [L. Perkins, pers. commun.]),
suggesting that ecological conditions affect its value. Nonetheless, this persistent
male bias among neonates in the wild is yet another indication that females show a
tendency toward philopatry [34, 35] and contrasts with the female-biased sex ratios
found amongst chimpanzees, in which males are the philopatric sex [36].
Despite the male-biased birth sex ratios, those among sexually mature individuals are highly female biased (table 4). The estimates of the ratios for mature
individuals do depend, however, on the degree of range overlap and home range
sizes used. Home range sizes have been discussed extensively by Singleton and van
Schaik [13] and are considered relatively reliable. Singleton [20] also used several
varying estimates for range sizes and still consistently produced female-biased sex
ratios in the sexually active portion of the population. There are two ways in which
these estimates could be wrong. First, it might conceivably be argued that the measures of range overlap, which are based on all individuals known to have used the
same grid cells over the period from 1994 to 1998, could include some individuals
that have since died and could thus be too high. However, suspected deaths during
the study were few and this is not considered to represent a significant problem.
Second, a potentially serious source of uncertainty in overlap is the number of
subadult males in the central study area. We were not consistently able to recognise
and name new (unhabituated) subadult males in the area and decided that 30 was
the best estimate. This number may seem large, but reducing it results in even
lower estimated sex ratios [20]. In order to eliminate excess male mortality, we
need some 53 subadult males in the area to reach a male proportion of 0.5 and over
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Singleton/van Schaik
70 to maintain it at the observed value among infants of 0.56. As discussed, the
figure of 30 initially used in this process already includes an allowance for unidentified or ‘missed’ subadult males. Thus, the discrepancy between birth sex ratio and
adult sex ratio is large, suggesting an excess male mortality or disappearance of
anywhere up to 50% of males after birth. It is highly unlikely that such a large excess is entirely due to necessarily small differences in the age at which males and
females become sexually mature or at least classified as subadults.
One plausible cause for this shift in sex ratio is differential mortality. Agonistic encounters between adult males are usually violent [16] and may result in injuries and subsequent death [30; C.D. Knott, pers. commun.]. Subadult males usually
escape when chased by adult males, but if they do not, for instance if injured or
diseased, they are likely to be subjected to uncompromising attacks. Many adult,
and some subadult, males do indeed bear scars that are often attributed to fights
[30, 37; pers. observation]. On the other hand, no serious injuries have ever been
observed as a result of forced matings or of female-female conflict. Thus, although
only few deaths of mature wild orang-utans have been witnessed [16, 30; S. Wich,
pers. commun.; C.P. van Schaik, unpubl. data], differential mortality is a plausible
source for the increasingly female-biased sex ratio as a cohort matures. Interestingly, these findings also concur with those of Cocks [38], who reported a similar
sex difference in mortality among sexually mature orang-utans in captivity, though
the underlying causes in this case may well be very different. A tendency towards
excess male mortality is, of course, fully expected in polygynous mammals such as
orang-utans [39].
An alternative source of the shifting sex ratios might be differential male dispersal (rather than excess male mortality). It is possible that at least some males
disperse through emigration, most probably during the subadult phase, from highdensity areas such as Suaq Balimbing into areas where densities may be lower.
There need not necessarily be compensatory levels of immigration from these areas. Such areas may resemble most Bornean sites, in that the preferred adult male
may be unable to maintain long consortships, and hence also unable to monopolise
matings with fertile females. Thus, both subadult and non-dominant adult males
might show a tendency to gravitate towards such areas, which would result in
stronger female bias amongst mature individuals in source areas such as Suaq
Balimbing. Without additional data to support this, however, or closer examination
of existing data, this possibility can be only speculative.
Unfortunately, it is impossible to compare these adult sex ratios with those
found elsewhere, since other studies have simply presented the numbers of each agesex class encountered within study areas. Thus, they do not provide an unbiased
estimate of the population sex ratio, because that requires correction for sex differences in home range size or range overlap. The numbers presented here are therefore
the first attempt at producing unbiased estimates of adult sex ratios among orangutans and hence also the first estimates of sex differences in mortality.
The highly female-biased sex ratio observed among fully adult (flanged) males
and females is consistent with the notion of long delays in subadult male development to full adulthood [25, 40]. It is also consistent with the speculative notion that
only a small proportion of subadult males mature into full adults at any one time,
the remainder being suppressed by the presence (or quality) of the dominant adult
male. At Suaq Balimbing, it would seem to be to a male’s advantage to remain
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Folia Primatol 2002;73:1–20
17
subadult until an opportunity to compete for dominant status arises. Naturally, this
argument requires that dominant adult males sire sufficiently more infants than any
individual subadult males. Only then will the potential benefits, through increased
reproductive opportunities, outweigh the potential risks of becoming a nondominant adult male, with very few reproductive opportunities (as observed at Suaq
Balimbing).
We further speculate that the number of subadult males, at least in Sumatra,
developing into adult males is not constant over time. In the presence of a particularly successful dominant adult male, any subadult male that develops secondary
sexual characteristics would either have to compete with this male if he wishes to
sire infants or leave the area. However, if the dominant adult male were to show
signs of weakening or die, it would seem reasonable to expect a number of subadult
males to rapidly mature (a process that can take as little as a few months [41]) and
compete for the new vacancy. Males that are already fully adult but non-dominant,
might also compete, but it could be argued that many would be past their prime and
unlikely to succeed as a result. Such a scenario would mean that development of
secondary sexual characteristics would be a huge gamble to subadult males, as the
majority would fail to accede to the dominant position in the immediate area. Obviously, the differences between study sites suggest that developing into an adult
male is much less risky at the Bornean sites studied so far.
More long-term field data are needed to test this speculation. Unfortunately,
such tests are becoming increasingly difficult as long-term field studies have to be
discontinued. Thus, all fieldwork at Suaq Balimbing had to be stopped in September 1999, due to serious civil unrest. Subsequent illegal logging has destroyed
much of the study site.
Conclusion
The high spatial overlap of the individuals in this swamp population of orangutans shows that spatially discrete social units do not exist. However, there is evidence for non-random association among females and between females and males,
and hence some form of socially distinct social units. Neighbouring, and possibly
related, adult females preferentially associate with each other and show striking
convergence in mate choice on the same (dominant) adult male in the area. Other
sexually mature males are not preferred and must therefore roam more widely in
search of fertile females that are not guarded by their preferred males. Thus, the
‘community’ can be considered to consist of one or more female clusters and the
adult male they all prefer as mate, who has a more limited home range than those of
the other males found in the area. However, it is important to point out that this
‘community’ is not nearly as discrete as that of other fission-fusion primate species,
showing neither spatial nor social exclusivity.
Acknowledgments
For permission to work in Indonesia we are grateful to the Indonesian Institute of Sciences (LIPI). I.S. thanks its biological division Puslitbang Biologi for sponsoring him; C.v.S.
thanks Universitas Indonesia and Universitas Syiah Kuala for this. We thank the Department
18
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Singleton/van Schaik
of Forestry and Nature Conservation (PHPA/PKA) for permission to work at Suaq Balimbing. Long-term financial support for the Suaq Balimbing project was provided by the Wildlife Conservation Society of New York, with additional support from the L.S.B. Leakey
Foundation. The first author also wishes to thank the Durrell Wildlife Conservation Trust for
its support, and Richard Griffiths and John MacKinnon for their advice and assistance. Additional funding was provided by the Wenner-Gren Foundation for Anthropological Research,
the Orangutan Foundation UK, Wildlife Preservation Trust International, the Lindeth Charitable Trust, the American Society of Primatologists and Dom Wormell. We thank Abdussamad, Asril, Azhar, Bahlias, Fahrulrazi, Beth Fox, Ibrahim, the late Idrusman, Ishak, Mukadis, Samsuar, Arnold Sitompul and Zulkifli for help in data collection. We are also grateful to Perry van Duijnhoven, Kathryn Monk, Mike Griffiths and Yarrow Robertson for considerable logistical support and hospitality. Beth Fox, Cheryl Knott, Lori Perkins, Riswan,
Herman Rijksen and Serge Wich kindly provided personal communications. Thanks also to
the European Commission and the Government of Indonesia as the funding agencies for the
Leuser Development Programme. This is Leuser Management Unit Publication No.
024/2000.
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