The Proboscis Monkey (Nasalis larvatus)

Social Group Structures

July 2012
The Proboscis Monkey (Nasalis larvatus)
Social Group Structures

Iris Mulder
Supervisor: Liesbeth Sterck & Frank Rietkerk
Apenheul Primate Park
Behavioural Ecology
Utrecht University
July 25th, 2012

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Table of Contents

Abstract..................................................................................................................... 4

Background of This Thesis ........................................................................................ 5

Introduction: The Proboscis Monkey ......................................................................... 6

Social Organization ................................................................................................. 10

Colobines: Assessing Phylogenetic Species for Similarity in Social Organization.... 12

Baboons: Judging Similarity in Social Organization ................................................. 15

Discussion............................................................................................................... 18

Proboscis monkey: more similar to colobine or baboon social organization ....................... 18

Captivity ............................................................................................................................... 20

Conclusion ........................................................................................................................... 20

Acknowledgements ................................................................................................. 21

References.............................................................................................................. 22

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Abstract

The proboscis monkey (Nasalis larvatus) is a large old world monkey,

indigenous to Borneo. In the coastal areas of this island, groups of proboscis
monkeys live together without a lot of territorial aggression. Studies conducted on the
social organization of this monkey do not unanimously agree on its group
composition. Phylogenetically it differs a lot from the other Colobines and might
therefore show more resemblance to the Papio genus. Comparing the proboscis
monkey to other Colobines shows that snub-nosed monkeys have a similar social
structure. The multilevel society and fission-fusion behaviour of these monkeys make
it a good example for the possible social structures of the proboscis monkey. While
the baboons also exhibit these behaviours, the levels of its multilevel society are
more extensive than observed for the proboscis monkey. Because of this a lot of
influences on the social organization are added. This draws the conclusion that snub-
nosed monkeys have the most similar social organization to the proboscis monkey.
The combined literature in this thesis gives an overview of the monkey’s social
behaviour in the wild and mentions new insights on how to successfully keep them in
an artificial environment. With the knowledge on maintaining groups of proboscis
monkeys in captivity, zoos can cooperate and work against the extinction of this
species in the wild.

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Background of This Thesis
Presently, several primate species are threatened with extinction, among
them the proboscis monkey (Nasalis larvatus). Threats for this monkey include loss
of habitat, hunting and tourism (Sha et al. 2008). To protect these animals and
ensure their survival in the future, two ways of intervention are available. First and
foremost protecting them in their natural habitat and second, maintaining populations
in captivity. However, maintenance in captivity may be difficult for species when their
natural history is not known. Challenges may include their diet, but also an optimal
social organization is crucial to maintain welfare and species specific behaviour in
captivity.
Proboscis monkeys are highly threatened (IUCN 2008); unfortunately
maintenance in an artificial environment remains difficult as well. Part of this problem
is due to their dietary requirements, yet stress is also often considered to highly affect
their welfare. Improving social circumstances may reduce stress in these animals in
captivity. Studies on the social organization of this monkey suggest that they live in a
multilevel society, but this is not well known for this species. This thesis describes the
available knowledge on the social organization of the proboscis monkey. Since
several aspects are unclear, in particular for males, the two sources that may provide
more insight will be discussed. These are the closest relatives, i.e. Colobines, and
the species with similar social organization, i.e. multilevel baboons. On the basis of
this information, any similarities, differences and gaps in our knowledge will be
described. As a result of this research, recommendations will be given on how the
proboscis monkey can be best housed.

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Introduction: The Proboscis Monkey

Colobus monkeys are part of a group named the old world monkeys, also
known as the Cercopithecidae. This group can be divided into two subfamilies, the
Colobinae and the Cercopithecinae (Oates & Davies 1994). The Colobinae, in which
the proboscis monkey is categorized, contains over 30 species distributed over Africa
and Asia (Oates & Davies 1994). A phylogenetic tree based on DNA polymorphisms
can give more insight on the taxonomy of the monkey (Figure 1). After the distinction
between the Colobinae and the Cercopithecinae, the Colobinae are further separated
into an African clade (Colobus monkeys) and an Asian clade (Langurs) (Xing et al.
2005).
Colobinae are often discussed for their complex gastrointestinal tract. This
gives the animals the ability to neutralize the chemical effects of digesting leaves and
reduces the problems that come with the digestion of inhibitors and toxins. For this
reason it allows them to have their folivorous/frugivorous diet (Chivers 1994).

Figure 1 – A cladogram of the Cercipithecidae phylogenetic tree, based on analysis of

specific DNA polymorphisms. The proboscis monkey (Nasalis larvatus) is located in the
centre of the Colobinae subcategory (Xing et al. 2005).

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 Like many Colobus monkeys, proboscis monkeys are arboreal, spending their
nights in taller padada trees (Kawabe & Mano 1972). During night time, the proboscis
monkey always tries to find a tree close to a river (Bennett & Davies 1994). During
the day, groups of proboscis monkeys travel further inland, however the distance
they travel is limited by the monkey’s need to return to a river in the evening (Bennett
& Sebastian 1988; Bennett & Davies 1994). As a result, depending on the location of
rivers around the group, they can be restricted to a small part of the forest or range
widely (Bennett & Davies 1994). As reviewed by (Sha et al. 2008), the monkeys can
be found up to 750 km inland, but are often closer to the coastal area, on average 55
km away from the coast. The proboscis monkey is known to be mostly confined to
riverine, mangrove, peat swamp and fresh water swamp forests (Bennett &
Sebastian 1988; Meijaard & Nijman 2000). Populations of this monkey have been
spotted in Kalimantan, Sabah, Sarawak and Brunei, all regions of the island of
Borneo (Kawabe & Mano 1972; Meijaard & Nijman 2000).
As mentioned before, the social organization of the proboscis monkey
remains rather unclear. In the early days of studies on this monkey, there has been a
lot of discussion on whether or not the proboscis monkey lives in multi-male units
(MMUs) or one-male units (OMUs). Mostly older studies mentioned observations of
MMUs, describing the proboscis monkey as living in multi-male groups with a social
organization comparable to the silver-leaf monkey (Kern 1964; Kawabe & Mano
1972; Macdonald 1982; Salter et al. 1985). Later on, the idea of the proboscis
monkey in an OMU-based society was considered (Bennett & Sebastian 1988;
Yeager 1990; Yeager 1991; Boonratana 2000).
Explanations for this large discrepancy between observations can be
intraspecific variation or a discrepancy in methodology between the different studies
could be the case (Yeager 1990). The definition of the term group seems to be one of
the most important aspects. While early studies include individuals in a group when
they are located within 100 meters of each other, more recent research has added
further requirements (Kern 1964; Macdonald 1982). For instance, spatial distribution
of the animals while in a 100 meter radius can help dividing the large multi-male
group into smaller OMUs (Yeager 1990). In addition, observing the group movements
can help deciding on its members. As described earlier, groups of proboscis
monkeys join together during night times, which may have been a cause for the less
apparent group formations. On the other hand, when evaluating the possibility of
intraspecific variation for the proboscis monkey, this would mean that the habitat in
which the observations were done may have an influence on the existence of multi-
male groups (Yeager 1995). The first studies noticing loosely organized MMUs
observed the proboscis monkey in nipa swamp forests (Kern 1964), while the stable
MMUs are described during a study mostly in mangrove swamps and tropical rain
forest (Kawabe & Mano 1972). Studies done in riverine forests mention observations
of all-male units (AMUs) as well as OMUs (Bennett & Sebastian 1988; Boonratana
2000; Matsuda et al. 2009). This is equal to what is found in freshwater peat swamp

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forest by (Yeager 1990). Looking at this, it might be concluded that nipa and
mangrove swamp forests are a habitat preferred by MMUs, while riverine and
freshwater peat swamp forests are inhabited by AMUs and OMUs. However, this
option is severely disputed by studies that performed observations in the same area
in which only MMUs were described earlier (Kern 1964; Macdonald 1982; Yeager
1995). With the use of the broadened methodology, described before, they conclude
no MMUs exist in this area, thereby rejecting the possibility of intraspecific variation
(Yeager 1995). The existence of MMUs was discarded and OMU is now accepted as
the basic unit of the proboscis monkey.
Apart from the OMU, AMUs have been reported for the proboscis monkey as
well. All-male groups for this species consist of around nine individuals, with
members varying frequently and females occasionally joining the group too (Bennett
& Sebastian 1988; Murai 2004). More recently however, larger groups of 29
individuals have been observed (Murai 2004), this suggests that the number of
members within an AMU can vary widely. An interesting feature of AMUs is that they
have a larger range than OMUs. It might be that AMUs come across OMUs more
often this way, creating possibilities for the bachelor males to take over a harem
group (Murai 2004). The AMUs seem to be a temporary option for most of its
members. The group is joined by mostly juvenile or sub-adult males and left by
young adults forming their own OMU (Murai 2004). While AMUs are a rather
common sight, according to some reports the proboscis males are rarely observed
solitary (Yeager 1990). This in contrast to what was thought in other studies on this
monkey, in which males were suggested to be solitary frequently (Bennett &
Sebastian 1988) or occasionally (Yeager 1991). More recent studies claim that young
males can become solitary for a while, until reaching adulthood and joining a bisexual
group to reproduce (Murai 2004).
Not only males can migrate between groups, females have also been
reported to leave their group regularly (Murai et al. 2007). Sub-adult females switch
more between groups than adult females and they spend time in AMUs as well
(Murai 2004). One of the main causes for the females to leave their natal group is to
avoid inbreeding (Clutton-Brock 1989). This is possibly the foremost reason why the
transferring females are generally in a sub-adult status, since they leave their natal
group when reaching sexual maturity (Murai et al. 2007). When an adult female
decides to leave a group the dominant male of the old group might try to call the
transferring female back to their original group. When it is a sub-adult female
however, males might not even show interest in the female leaving (Murai 2004).
When the females depart from their natal group, they often leave their sons to AMUs.
This type of switching between groups is also known as fission-fusion. Fission-fusion
dynamics refer to groups with a highly variable composition as a result of merging
and splitting into subgroups, a social organization used by for instance chimpanzees
or orang-utans (Amici et al. 2008). Fission-fusion activities go hand in hand with
multilevel societies. A multilevel society can be recognized by its stable units, which

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often or permanently associate with other units, creating another level of social
grouping (Grueter & Van Schaik 2010). Thus, the proboscis monkey lives in a
multilevel society with fission-fusion dynamics. In this society, the OMU is the basic
unit, but AMUs are observed as well.
The proboscis monkeys currently have an endangered status on the IUCN
Red List of Threatened Species (IUCN 2008) and there are signs that their numbers
are further declining (Sha et al. 2008). Besides protecting the animals in their natural
environment, zoos are able to help the survival of this animal as well. However, partly
due to the uncertainties of the social organization of the proboscis monkey, they are
not often successfully kept in an artificial environment. Only a small number of
studies has been done regarding their social organization in captivity. The few
studies mentioning the proboscis monkey in captive social units are describing
OMUs, therefore this is most likely the most used social composition in captivity
(Dierenfeld et al. 1992; Yeager et al. 1997; Agoramoorthy et al. 2004; Cui & Xiao
2004). A recent study however, has focussed on the maintenance of an AMU in
captivity at Singapore Zoo (Sha et al. 2012). This idea was created due to the
presence of surplus males, which can be a problem to maintain in captivity. They
cannot remain in the same group as they grew up, since adding adult males to an
OMU causes stress and fights within the group (Sha et al. 2012). For this reason the
surplus males require extra maintenance and space; however it now seems that
AMUs can be formed to solve this.
In sum, the multilevel society with fission-fusion structures is of great
influence on the overall social organization of the proboscis monkey. It can be
concluded that the monkeys may switch between groups during the different phases
of their lives. Solely stating that they live in OMUs and AMUs does not explain the
complete social situation of this monkey in the wild. This should be taken into
consideration when reaching a conclusion after evaluating the resemblances
between the different animal species.

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Social Organization
To find out more about the social organization of Colobine and baboon
species, it is important to be aware of the types of social living, primates exhibit.
Depending on many factors, for instance nocturnal versus diurnal animals, primates
have all developed their own social organization. The external influences on social
organization can be summarized in a scheme (Figure 2). The three main ecological
influences that can cause changes in social behaviour are also three aspects that are
affected by the group formation, namely feeding, predation and reproduction (Van
Schaik & Van Hooff 1983). Competition for food is higher in large groups and lower in
smaller groups. Naturally the availability of food within the group’s range is important
as well (Van Schaik & Van Hooff 1983). On the other hand, predation pressure
triggers an anti-predation response. These two behavioural responses affect group
size, where both large groups and small groups can each have their advantages.
Large groups are easily spotted by a possible predator; however the members of the
group have a larger change of spotting the predator as well and fleeing away in time.
Small groups however, may not be spotted as easily, but they are more likely to be
caught since they might not notice the predator in time (Alexander 1974). Group size
and the group cohesion influence a male’s ability to monopolize females and thereby
affect mating strategies and the resulting group composition. At this point, the
influencing factors start to have an effect on the social organization of the group. The
scheme concludes with patterns in social behaviour, which is affected by the group
composition and relatedness. Migration and emigration within a group influence the
relatedness between members, which has an effect on animals coming to the aid of
one another (Massey 1977).

Figure 2 – Schematic view of the ecological effects on the social organization of primates,
adjusted from (Van Schaik & Van Hooff 1983)

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 Animal species early in the evolution are generally thought to be solitary and
nocturnal (Eisenberg et al. 1972). With this as a starting point, those species were
affected by external influences to eventually change their social organization and
evolve. Looking at social organization alone, three types of organization can be
described, namely solitary animals or animals with one or multiple group members.
The social structure of solitary primates can be described as a
neighbourhood, in which animals are familiar with other animals in their range, yet
they all are separate social units (Richard 1985; Kappeler & Van Schaik 2002). A
second form of social organization is living in pairs, which is one of the rarest forms
of social organization in primates (Kappeler & Van Schaik 2002; van Schaik &
Kappeler 2003). Living in pairs compared to in a group, does not seem beneficial
most importantly for the reason that it declines reproduction options (Kappeler & Van
Schaik 2002). The third type of social organization, exhibited by the majority of
primates, is group-living.
Group living primates is a very broad type of social organization, in which
many more distinctions are made that are all affecting the social behaviour of the
animals. The ratio of male and female individuals within the group can give rise to
further divisions within this large group, leading to multi-male, multi-female or multi-
male multi-female units (Eisenberg et al. 1972; Kappeler & Van Schaik 2002). A
second important distinction in group living animals is often made, namely between
one-male and multi-male groups. This distinction can highly affect the social
behaviour of the animals in terms of resource and group defence or aggression (Van
Schaik & Van Hooff 1983; Terborgh & Janson 1986; van Schaik & Kappeler 2003). In
groups with multiple males, the males will join together to form a cooperative defence
against possible predators, while in one-male units defending multiple females might
become a problem (Terborgh & Janson 1986). The social organization of group living
primates could become even more complex when units join together and form
multilevel societies and fission-fusion activities occur. A good example of a primate
species living in a extensive multilevel society is the hamadryas baboon, which will
be discussed in further detail later on (Stammbach 1987). In sum, group living
primates can vary widely in social organization, from rather simple multi-male units to
one-male units within multilevel societies.
After considering the types of social organization, it has become clear that all
three types have their advantages as well as their disadvantages (Kappeler & Van
Schaik 2002). Thus, there is no single optimal group structure; depending on
environmental influences a group can find its own balance.

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Colobines: Assessing Phylogenetic Species for
Similarity in Social Organization

To find out whether the social organization of the proboscis monkey and the
role of the males within these groups are comparable to what occurs in other
Colobine species, this section will revolve around the social organization of the Asian
Colobines. When only looking at group sizes of Asian Colobines, large differences
can be found between species, for example the troop size ranges from around four
animals (Mentawai leaf-monkeys) to troops of over 400 animals (snub-nosed
monkeys) (Newton & Dunbar 1994). This and many other aspects affect the type of
social organization per species.
Three types of social organization have been observed in Asian Colobines,
namely separate OMUs also known as non-multilevel societies, multilevel societies
and large multi-male multi-female groups (Grueter & Van Schaik 2009; Grueter &
Van Schaik 2010). A couple of studies mention a monogamous lifestyle for some
Colobine species as well (Bennett & Davies 1994; Newton & Dunbar 1994). In Table
1 an overview of the social organization of frequently studied Asian Colobines is
given, including unit size, unit composition, the presence of AMUs and social
organization. The first column represents unit size, which is for the proboscis monkey
around 13.4 according to this study, however looking at other studies the number of
members in one group often varies (Bennett & Sebastian 1988; Newton & Dunbar
1994; Grueter & Van Schaik 2009). Including the relatively larger AMUs, in which
males can spend several years, the number is a little higher than suggested by
earlier studies (Bennett & Sebastian 1988; Oates & Davies 1994). Secondly, unit
composition is mentioned, described as either a one-male or a multi-male unit. The
standard composition for the Asian Colobines seems to be the OMU, apart from
several species of the genus Semnopithecus who have a clear multi-male multi-
female organization (Grueter & Van Schaik 2010). The third column shows whether
or not the species include AMUs, suggesting that in almost all species AMUs are
present. Finally, the type of social organization is divided into two groups, namely
multilevel or non-multilevel. As mentioned before, multilevel societies can be
explained as stable units often or permanently associating with other units, creating
another level of social grouping (Grueter & Van Schaik 2010). While most Asian
Colobines are non-multilevel, the proboscis monkey and all species of the
Rhinopithecus genus show a multilevel social organization. Table 1 shows that on all
four aspects the Colobine species differ significantly from each other and it is not
possible to form one conclusion about their social systems.

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Species Unit size Unit AMU Social
composition organization
Presbytis comata 6.7 OM No Non-multilevel
Presbytis siamensis 15.1 MM UK Multilevel
Presbytis thomasi 8.9 OM Yes Non-multilevel
Presbytis potenziani 3.8 OM No Non-multilevel
Presbytis rubicunda 6.4 OM Yes Non-multilevel
Presbytis hosei 7.5 OM UK Non-multilevel
Trachypithecus obscurus 17 MM Yes Non-multilevel
Trachypithecus geei 10.7 OM Yes Multilevel
Trachypithecus vetulus 8.9 OM Yes Non-multilevel
Trachypithecus johnii 7 MM Yes Non-multilevel
Trachypithecus phayrei 14.3 MM UK Non-multilevel
Trachypithecus leucocephalus 10.3 OM UK Non-multilevel
Trachypithecus pileatus 8.6 OM Yes Multilevel
Trachypithecus francoisi 9.5 MM UK Non-multilevel
Semnopithecus entellus 21.2 MM Yes MM-MF
Semnopithecus schistaceus 23.7 MM UK MM-MF
Semnopithecus priam 29.4 MM UK MM-MF
Simias concolor 5.2 OM No Non-multilevel
Rhinopithecus bieti 8.3 OM Yes Multilevel
Rhinopithecus roxellana 13 OM Yes Multilevel
Rhinopithecus brelichi 6.2 OM Yes Multilevel
Rhinopithecus avunculus 12.9 OM Yes Multilevel
Pygathrix nigripes 11.3 MM UK Multilevel
Nasalis larvatus 13.4 OM Yes Multilevel
Table 1 – An overview of the unit size (mean # of animals), unit composition (one-male or
multi-male), the presence of AMUs (yes, no or unknown) (Newton & Dunbar 1994) and social
organization of the Asian Colobines for which sufficient data are on hand. Social organization
is described as multilevel, non-multilevel or multi-male multi-female (MM-MF). Table adjusted
from (Grueter & Van Schaik 2009).

In addition to the most basic units in the social organization of Colobines, the
OMU, AMUs play an important role in the system as well. In an AMU, group
members are frequently juvenile, while the middle-aged and old males are more
often found in OMUs. In Colobines, all male groups have been observed in 17
species (Murai 2004). For instance, for the Eastern black-and-white Colobus
(Colobus guereza) the maturation of younger animals and immigration of foreign
males can lead to the formation of these groups (Oates & Davies 1994). Many
Colobine populations, e.g. langur species, banded-leaf monkeys and red-leaf
monkeys, also have extra-troop males, who join other units or bands than their natal
unit and try to get access to its females (Newton & Dunbar 1994).

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 Table 1 gives an overview of the similarities and differences between the
social organization of the proboscis monkey and the other Colobinae. While some
genera, like the Semnopithecus, do not seem to share any social aspects, others are
very similar to the proboscis monkey. The snub-nosed monkey (Rhinopithecus)
comes closest to the proboscis monkey regarding social organization (Kirkpatrick et
al. 1998). Both species are known to have a multilevel society, with large range
overlaps between units (Bennett & Davies 1994). The Yunnan snub-nosed monkey
(Rhinopithecus bieti) society consists of mostly OMUs, but AMUs were observed as
well. Those OMUs and the occasional AMU join together to form a band, in which 15
to 18 units can be found (Kirkpatrick et al. 1998). Sub-adult males of the Yunnan
snub-nosed monkey join AMUs as well and may switch between one-male and all-
male units within the band (Kirkpatrick et al. 1998). Depending on the season,
aggression between males was observed between units within a band, which is
similar to what occurs in other Colobine species (Kirkpatrick et al. 1998; Struhsaker
2000). However, another snub-nosed monkey species with similar social
organization, the Sichuan snub-nosed monkey (Rhinopithecus roxellana), does not
show much inter-unit aggression and there seems to be no clear hierarchy between
the units (Zhang et al. 2008). Within an OMU not much aggression is observed for
most Colobines, including the snub-nosed monkeys (Struhsaker & Leland 1987;
Kirkpatrick et al. 1998; Zhang et al. 2008). Regarding aggression during takeovers,
lack of knowledge makes it impossible to form an opinion on this subject. It is known
that after a takeover, a new resident male snub-nosed monkeys will not receive any
support from its females during fights (Zhang et al. 2008).
In conclusion, it has become clear that it is definitely not possible to consider
all Asian Colobines as one regarding social organization and attention should be
given to all separate species to be able to form a conclusion on their social system.
The multilevel society with fission-fusion structures of the snub-nosed monkeys
suggests that, among the Colobines, they are most similar to the proboscis monkey.

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Baboons: Judging Similarity in Social Organization
Looking at species with a similar social organization, but without a close
phylogenetic relation, can create another view on the proboscis monkey’s social
organization. The multilevel society and fission-fusion structures, as mentioned
before, have frequently been observed in several species of the tribe Papionini,
namely gelada baboons (Theropithecus gelada), hamadryas baboons (Papio
hamadryas) as well as drills (Mandrillus leucophaeus) and mandrills (Mandrillus
sphinx) (Stammbach 1987). This section will take a closer look at their social
behaviour and group composition to find out more about the similarities and
dissimilarities to the proboscis monkey.
The social organization for most baboon species is generally a large group of
animals, living in single level multi-male groups. In these groups, the females form
the foundation of the group and the males can switch between groups to find mates
for breeding (Barton 2000). Nonetheless, bonds between males and females of the
Papio are of high importance. For the males it is a reproductive certainty and for the
females it ensures protection when necessary (Dunbar 1987). However, the
hamadryas and gelada baboons show a different social organization to other Papio,
which is more similar to the organization of the snub-nosed monkey species.
Hamadryas baboons live in multilevel societies with fission-fusion activities, in
which all animals are members of an OMU. Frequently however, two or three OMUs
join together into a clan, which are often formed during foraging (Stammbach 1987).
Clans can join to form a band, in which they have social interactions. During night
times, bands can come together at a sleeping site and compose a troop (Kummer
1984). In contrast to most baboon species, females of the patrilineal hamadryas
baboon transfer between units instead of the males (Barton 2000). These females do
not share as strong relationships with each other as they do in other baboon species
(Barton 2000). In contrast to the large clans of snub-nosed monkeys, the hamadryas
clan exists of only two to three OMUs, making it easier to evaluate the position of the
males. Within the clan, males can have four possible roles (Figure 3). First there is a
unit leader per unit, most often an adult male. There can be one or more followers of
the clan, who can be divided into two categories, namely leaders of initial units or
bachelors. An initial unit is a pair of a male and a female individual forming a small
unit within an OMU. Initial unit leaders are looking for a takeover opportunity when
they have reached maturity. The other type of follower, the bachelor, is often a sub-
adult male that simply follows the clan. Another male within a clan can be an aged
male, often the former leader of one of the units, who remains with its clan.

15
Figure 3 – The four roles of the males within a hamadryas baboon clan. An old adult within a
clan is often a former group leader. There are prime adults as the current unit leaders. And
there can be several followers, who can be subcategorized into two groups, namely leaders of
the initial unit or bachelors (Kummer 1984).

The unit leader will have control over the females and monopolize them against other
males (Kummer 1984). Group takeovers are mostly done by males returning to their
natal unit when reaching adulthood, where they create a bond with a female of this
group and form its own group. Between males, fights may be elicited to try and take
over a unit as well, during these fights females may separate and new OMUs can be
formed (Abegglen 1984; Stammbach 1987). Furthermore, between units of a clan not
a lot of aggression is reported. On the other hand, within units aggression may take
place, especially herding can be performed in an aggressive manner (Stammbach
1987)
In geladas, OMUs can join together to form a band as well, however
contrasting to hamadryas baboons, their band membership is not as constant
(Stammbach 1987). Males may also join an AMU when they are not in an OMU,
which is similar to what snub-nosed monkeys do, but not often observed for
hamadryas baboons (Stammbach 1987). Joining and leaving an AMU occurs when
the unit associates with an OMU and males can attempt a takeover this or join the
AMU as a follower (Kawai et al. 1983). When food is less available, OMUs and AMUs
can form a herd, comparable to a troop. OMU takeovers can be strategic as well as
aggressive for this species. According to the “follower strategy” gelada males may
join an OMU in the role of a follower, but may take over several of the leader’s
females and begin his own group, which is similar to the behaviour of hamadryas
males. Another way to take over a unit is by simply attacking a weaker unit leader
and become leader of the group after winning the fight (Stammbach 1987).
Aggression between units occurs rarely, similar to hamadryas baboon. For geladas,
aggression within units is uncommon as well, which is in contrast to the hamadryas
baboons (Stammbach 1987) Gelada baboons seem to have a similar set up as
hamadryas with some functional differences, for instance gelada baboons are

16
matrilineal whereas hamadryas are patrilineal, resulting in a larger role for the males
in the hamadryas society than with geladas (Kawai et al. 1983).
Older reports mention that mandrills and drills live in OMUs as well and meet
in larger groups from time to time (Stammbach 1987; Barton 2000). More recent
reports however, state that there is no evidence of OMUs in the mandrill society
(Abernethy et al. 2002). Older mandrill and drill males could be living solitary.
Additionally, AMUs have not been observed for these species (Stammbach 1987). It
remains difficult to come to a conclusion since not many studies have been done on
these animals. A reason for this is that these monkeys are difficult to follow in the wild
due to low visibility in their habitat (Abernethy et al. 2002). Researchers do state that
females and their infants live together in groups and are joined by males during the
breeding season, which is in agreement to the suggestion that males might live
solitary (Abernethy et al. 2002). Concluding, the social organization of the mandrills
and drills is still unclear on multiple levels and needs more studying to be able to
form a conclusion.
While the discussed baboon species are a lot more similar in their social
organization than the many Colobinae species, it has become clear that they have
more differences than might be expected. Looking at the mandrills and drills, their
social organization may not be as similar to the proboscis monkey as expected. If, as
suggested by later studies, the OMU is not their basic unit, they may only slightly
resemble the social organization of the proboscis monkey. The lack of knowledge of
the social organization makes it impossible to compare to the proboscis monkey
adequately. The hamadryas and gelada baboons however show similarities in social
organization to the proboscis monkey, i.e. multilevel societies with the OMU as a
basic unit. The main difference between those two is the absence of AMUs within the
hamadryas system. Another important difference is the extent of the role of the males
in the groups, since male hamadryas have a lot more influence in the unit than male
geladas, for which the proboscis monkey is similar to the geladas. Table 2 gives an
overview of the several aspects of the social organization of these four baboon
species and the proboscis monkey. This shows most similarities between the
proboscis monkey and the gelada baboons, as concluded before.

Species Unit size Unit AMU Social

composition organization
Theropithecus gelada 10 OM Yes Multilevel
Papio hamadryas 7.3 OM No Multilevel
Mandrillus leucophaeus 15-20 UK No Multilevel
Mandrillus sphinx 20-25 UK No Multilevel
Nasalis larvatus 13.4 OM Yes Multilevel
Table 2 – An overview of the average unit size, unit composition (one-male or multi-male), the
presence of AMUs and social organization of four baboon species (Kummer 1984;
Stammbach 1987; Abernethy et al. 2002). UK stands for unknown.

17
Discussion
Proboscis monkey: more similar to colobine or baboon social
organization

In this thesis a phylogenetic evaluation and an evaluation of species with

similar social structures were done, comparing the two to the social organization of
the proboscis monkey. This created the opportunity to critically discuss its
resemblance to the Colobus species as well as species with similar social societies,
i.e. baboons. The many different social organizations of the Colobinae make it
difficult to form one conclusion on the social organization of the genus. It does
however show that the Sichuan and Yunnan snub-nosed monkeys can be potential
models for the proboscis monkey. The multilevel society that they exhibit is observed
for the proboscis monkey as well (Yeager 1991; Boonratana 2000). Multilevel
societies are also what baboons are known for, especially hamadryas and gelada
baboons. This section will evaluate whether the snub-nosed monkeys or the baboon
species provide a better model for the social organization of the proboscis monkey.
Starting with to the comparison between the proboscis monkey and the snub-
nosed species, their multilevel societies are very similar. The fission-fusion activities
that are observed in the snub-nosed monkey society were not mentioned by earlier
studies on the proboscis monkey. Part of the studies do mention observations of this
type of behaviour (Kawabe & Mano 1972; Macdonald 1982; Newton & Dunbar 1994),
but others state the contrary (Kern 1964; Boonratana 2000). More recently, the social
organization of the proboscis monkey was described in more detail, eliminating this
uncertainty (Boonratana 2000). Researchers of this study state “Nasalis larvatus
have a flexible social structure with a one-male multi-female (or polygynous) group
as the basic social unit. Furthermore, there is a secondary level of social
organization—the band—with ()fission–fusion of stable one-male groups within
bands.” Thus, this type of social organization is similar to the snub-nosed monkeys
as well as hamadryas and(Macdonald 1982) gelada baboons (Kawai et al. 1983;
Yeager 1991).
Another similarity between the two is the amount of aggression observed.
Generally for snub-nosed monkeys, not a lot of aggression has been observed
between individuals that are in a unit together (Kern 1964; Kawabe & Mano 1972;
Salter et al. 1985; Struhsaker & Leland 1987; Kirkpatrick et al. 1998; Zhang et al.
2008). Between units, territorial aggression might take place for the Yunnan snub-
nosed monkey, but is not often recorded for the Sichuan snub-nosed monkey
(Struhsaker 2000; Zhang et al. 2008). Looking at the baboon species, the hamadryas
baboons do exhibit aggressive behaviour within a unit, but are also tolerant to other
units. Regarding another type of aggression, for baboons several studies have been
done on the situation during takeovers, which suggested that the males are known
for their violent attacks against the unit leader of their own or others groups

18
(Abegglen 1984; Stammbach 1987). Unfortunately, lacking information on aggression
during snub-nosed and proboscis monkey takeovers inhibits the possibility to
compare them to the baboons on this subject.
In literature, when snub-nosed monkeys are discussed for their social
organization, often a reference to baboon species is made as well (Barton 2000;
Zhang et al. 2008). When looking at the mandrill and drill species though, there are
too many unclear parts of the social organization to form a conclusion and make a
reliable comparison to the proboscis monkey. The hamadryas and gelada baboons
are more frequently studied and show many similarities to the proboscis monkey in
social organization. The extensive multilevel societies that the hamadryas baboons
have and the resulting large troops are not necessarily mentioned in studies on the
proboscis monkey. The hamadryas baboon’s multilevel society consists of more
levels (Stammbach 1987; Barton 2000) than the described two levels (OMUs within
bands) of the proboscis monkey (Boonratana 2000).
Both the gelada and the hamadryas baboons have comparable parts of social
organization to the proboscis monkey, but the gelada may be the best comparison to
the proboscis monkey for the Papio genus. Very important for this decision is the
presence of AMUs in the gelada baboon society, which is not mentioned in studies
on the hamadryas baboon. This however is reported for the proboscis monkey and
plays a great role in the maturation of the males (Stammbach 1987). Adding that the
hamadryas baboons are patrilineal, this is not the case for the proboscis monkey. In
this monkey’s social system, switching between units is often performed by the males
and only occasionally by a female animal, which is also described for the gelada
baboon (Stammbach 1987; Murai et al. 2007). Looking at these similarities, it seems
that out of the four Papio the gelada baboon comes closest to the proboscis monkey
regarding social organization.
To sum up, the snub-nosed monkey and the gelada baboons show many
resemblances to the proboscis monkey in social organization. Both primate species
rarely show aggression within and between units. The relatively higher number of
levels to the society of the geladas compared to the two-level organization of the
snub-nosed monkeys makes the snub-nosed monkey more similar to the society of
the proboscis monkey regarding social organization (Stammbach 1987; Kirkpatrick et
al. 1998). This leads to the conclusion that the proboscis monkey in captivity should
be adjusted to the situation of the snub-nosed monkeys in captivity.

19
Captivity

In captivity it is understandable that fission-fusion structures cannot take

place. Surplus males are most often single housed, since it has become obvious that
keeping more than one adult male in a group, creating a multi-male multi-female
group, would lead to an aggressive and stressful environment for the animals.
Housing animals alone however, increases the care and space needed. The
formation of captive AMUs seems to be a successful answer to this problem,
especially since this is a natural solution. As mentioned before, only a small number
of studies has been done regarding the social organization of the proboscis monkey
in captivity, all describing OMUs. Recently however, Singapore Zoo has successfully
created an AMU in captivity, which solves many of the problems, e.g. surplus males
and housing space (Fàbregas & Guillén & Salazar 2007; Sha et al. 2012). Another
species that was studied on the formation of an AMU in captivity is the white crowned
mangabeys (Cercocebus atys lunulatus) at Valencia Zoo. This study concluded that
when the males are socially compatible, this is a very feasible solution to surplus
males. A group of male lion-tailed macaques (Macaca silenus) was successfully kept
in an AMU, with fewer disadvantages than experienced with males housed solitary or
in a multi-male multi-female group (Manns 2000). Proboscis monkeys were observed
when a group of six males were joined together forming an AMU (Sha et al. 2012).
This study noted all aggressive and affiliative behaviours and showed that after six
weeks of introduction, the aggressive behaviour showed a decline while affiliative
behaviour then increased and a hierarchy appeared (Sha et al. 2012).

Conclusion

Coming back to the original comparison, the best model for the social
organization of the proboscis monkey is the snub-nosed monkey. With its two-
layered multilevel society and low aggression levels within and between units, its
social organization is similar to the proboscis monkey. Combining this information
with knowledge of the proboscis monkey in captivity, results in a recommendation to
keep the proboscis monkey in artificial AMUs. The formation of an OMU in captivity
results in a much higher stress levels, as parts of their natural behaviour, e.g. fission-
fusion activities to control the number of males within a group, are suppressed.
Broadening the understanding of the social group structures of the proboscis
monkey in the wild can help optimizing the situation for their counterparts in captivity.
When this Colobine can be kept in an artificial environment without much difficulty,
zoos can maintain breeding programs and cooperate against the extinction of this
species in the wild.

20
Acknowledgements

In this section I would like to take the opportunity to thank Frank Rietkerk and
Apenheul primate park for letting me into their world and helping with me to find a
suitable subject to write about. Furthermore I would like to thank Liesbeth Sterck for
all the necessary encouragement and helping me get things back on track when I lost
myself in all of the available information.

21
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25