Project Title: Proboscis monkey (Nasalis larvatus) food resources in mangrove

forests in Kalimantan
Introduction
The proboscis monkey (Nasalis larvatus) is an endemic species of the island of Borneo. It can be
found in all provinces of Kalimantan (Indonesia), the states of Sabah and Sarawak (Malaysia) and in
Brunei Darussalam (Meijaard & Nijman 2000). It is classified as Endangered (EN) according to the
IUCN Red List (Meijaard et al. 2008). In conservation, the proboscis monkey represents a flagship
species complementary to orangutans because it often inhabits forests where orangutans are absent,
such as the mangrove forests.
The ecology of the proboscis monkeys is still puzzling. The males of this species belong to the
largest representatives of the colobine subfamily of the Old World monkeys (Grueter 2013). It is
perhaps due to the large body size that the proboscis monkeys feature several peculiarities in their
feeding behavior and physiology, including the recent evidence for rumination, analogous to
rumination known in many ungulate species but so far in no other primates (Matsuda et al. 2014).
Also in terms of habitat selection, the proboscis monkeys differ from most other species, except the
silvered langurs (Trachypithecis cristatus) and, to a lesser degree, the long-tailed macaques (Macaca
fascicularis). These three species (two folivores and one omnivore) often occur together in habitats,
which include riverine forests, swamps and mangroves. On the other hand, they are usually absent
from the extensive dipterocarp forests in Borneos interior, far from shores and major rivers. It is not
yet clear what makes these three species adapted and limited to these particular habitats, and what
makes them ecologicaly distinct from all other primate species in Borneo. It is worth noting that the
habitat selected by proboscis monkeys is the fastest-disappearing habitat in Borneo (Meijaard &
Nijman 2000), which makes the ecology of this particular species an urgent issue also from the
perspective of conservation.
The habitat of proboscis monkeys can be divided into two very distinct types, with a minimal overlap
in vegetation composition freshwater and coastal habitat. There are many important distinctions
between these two habitats. For the proboscis monkey ecology, the most important differences include
very low floral diversity of the mangrove forest, and low availability of food for the large vertebrates,
which is evident from a very low diversity of this guild, in sharp contrast to extremely high vertebrate
diversity of the primary dipterocarp rainforest adjoining the mangroves in Borneo (Chapman 1976).
Most vertebrates that live in mangroves are either highly generalized opportunists (Macaca
fascicularis, Sus barbatus, Callosciurus notatus, Rattus tiomanicus, Cynopterus brachyotis) or, on
contrary, highly specialized. Proboscis monkeys belong to the latter category the highly specialized
inhabitants of the mangroves. The exact nature of their specialization and adaptation to the survival in
this harsh habitat however remains poorly understood.
One possible explanation of the proboscis monkeys survival in mangroves relates to their large
home ranges. Although in some areas, the home ranges were observed to be small (Tarakan: Lhota,
pers. comm.), in many areas they are very large, even around 9 km
2
(Bennett & Sebastian 1988). They
may move 2201734 m in a single day (Matsuda et al. 2009). This may enable them to leave the
mangrove habitat on regular, even daily basis, and forage in other forest types. According to personal
communication with other researchers, it has been observed in many instances that the proboscis
monkeys leave mangrove forest during their daily ranging and feed on leaves, fruits and seeds in the
adjoining non-mangrove habitat. It is therefore possible that even the proboscis monkeys inhabiting
mangroves depend vitally in the non-mangrove forest, which may have important implications for
conservation.
The food selection of proboscis monkeys based on the chemical composition of young leaves has
been studied previously in the riverine forest habitat (Yeager et al. 1997, Matsuda et al. 2013) In
addition, one brief study has been conducted in mangrove forest, which can be classified as degraded
inner mangroves (Agoramoorthy & Hsu 2005). It has been shown in these studies that protein-to-fiber
ratio is the major determinant of leaf choice by the monkeys, but the mineral content also plays a role.
Proboscis monkeys appeared to select the leaves with high contain of phosphorus and potassium, and
avoided food sources with higher concentrations of calcium and manganese (Yeager et al. 1997). In
other line of evidence, it has been suggested that calcium, magnesium, potassium and sodium may
limit distribution of proboscis monkeys because the access to these minerals (in salt licks or mineral
springs) is known to limit distribution of large ungulates (Matsuda et al. 2013) in Kalimantan and
elsewhere. Apparently, most minerals are not limited in the marine environment of the mangrove
forest, which may be significant for the proboscis monkeys ecology. Finally, it is very likely that the
condensed tannins and secondary compounds, produced by plants in order to protect their leaves from
consumption by herbivores, represent a significant and possibly even limiting factor on the proboscis
monkey food choice and habitat selection (Davies & Oates 1995). These compounds are however
most difficult to analyze in laboratory (due to their chemical diversity) and their importance in
proboscis monkey ecology is therefore still poorly understood.

Objectives

Our current understanding of the proboscis monkey feeding ecology is mainly based on the studies in
the riverine forests. The proboscis monkeys inhabiting mangrove forests remain relatively unknown. It
is probably due to inaccessibility of the habitat for human observers, which means that it is nearly
impossible for the observer to follow the monkeys and directly observe their feeding throughout the
day in a natural habitat. Most of previous studies have been conducted from boats, which restricted
observations to riversides where the proboscis monkeys regularly sleep but where they forage only for
a limited time (reviewed in Bennett 1993 and Sha et al. 2011). Feeding data are highly biased in such
studies. Alternative methods such as telemetry (Onuma 2002) or observation from boardwalks in small
tourist parks (Agoramoorthy & Hsu 2005) have been used in a limited extend but they have their own
limitation and therefore also do not provide adequate data on feeding under natural conditions. The
only study, which focusses on food selection in relation to food chemistry in the mangrove forest
(Agoramoorthy & Hsu 2005) occurred in a habitat with specific vegetation composition and is not
applicable for typical coastal mangroves dominated by Rhizophora spp., Sonneratia alba, and
Avicennia spp.
Keeping in mind all the difficulties of studying feeding ecology of proboscis monkeys in mangrove
forests, this unique habitat also offers an interesting opportunity for the researchers. In contrast to
dipterocarp rainforests and riverine forests, the vegetation diversity of the mangrove forest is very low,
which gives the chance to analyze the nutritional value of all available food. This means that the
nutritional value of the food can be estimated in advance, even in the absence of feeding data (we do
not need to select tree species to be analyzed out of several hundred species, which typically grow in
rainforest). We can then use the data on the chemical composition of the available food sources to
formulate testable hypotheses about feeding (and ranging) behavior.
It is interesting per se to know the nutritional value of the leaves available for proboscis monkeys and
other large herbivores in mangrove habitat. The data can be compared with the similar analysis
conducted in dipterocarp forest and riverine forest in Sabah (Matsuda et al. 2013) in order to
understand what makes the mangrove forest distinct and why is the large herbivores guild in
mangroves so different from that of dipterocarp or riverside forest.

Methodology and concept
The aim of our proposed research is to estimate the nutritional value of food available to proboscis
monkeys in various types of mangrove forest in Kalimantan. We will focus on young leaves, which
represent the major food resource for proboscis monkeys in mangroves (Bennett 1993, Sha et al.
2011) and which have been focus of analysis also in previous studies of food choice of proboscis
monkeys in the riverside forest habitat (Yeager et al. 1997, Matsuda et al. 2013). We will analyze
young leaves of all mangrove species in 3 different study sites, including the species, which are not
known to be eaten by proboscis monkeys. Proboscis monkeys are however known to feed on variety
of other food resources, including mature laves, buds, flowers, fruits and seeds Yeager (1989, Matsuda
et al. 2009). For these resources we will only focus on resources known to be eaten by proboscis
monkeys, based on literature, our own observations and information from colleagues. Chemical
components analyzed will include crude protein, crude lipid, crude ash (representing minerals), NDF
(representing fiber), condensed tannins and total tannins.
Plant samples from 400 to 500 g freshweight will be collected, every single kind of those plant parts
will be cut into small pieces, dried on direct sunlight and the drying samples will be stired several
times during the first 24 hours, so that they will reach drymatter weight. No preservatives added will
be added (to accelerate the process of drying, samples can be dry in 50 C to 55 C circulating in hot air
oven for 12 to 18 hours for leaf dan and for 18 to 24 hours for fruit). Dried samples will be put in
paper bag and labeled and the paper bag will be let open during working in reserach location. Dried
sample could be kept in plastic bag which is closed tightly, added silica gel, and labeled. Before
leaving research location, we will put the bags of dried samples in the cartoon box and add silica gel,
then send to laboratory of nutrient testing using overnight service.
Besides that, however, we will use the results to formulate testable hypotheses about feeding and
ranging behavior of the proboscis monkeys in mangrove habitat. In order to formulate hypotheses
about ranging, we will however need to understand the distribution (zonation) of the tree species
within the mangrove forest. In one of the three study sites (Balikpapan Bay), we will therefore
establish vegetation sample plots, replicating the methodology of previous studies on proboscis
monkeys (Boonratana 2000, Matsuda et al. 2009). In the two remaining locations, the leaf sampling
will be opportunistic and the information on the zonation distribution of the plant species within the
forest will not be available; this is due to time limitation. These data can however be collected by
researchers in future studies.
In order to promote international collaboration, a student from Indonesia will participate on this
study. Several candidates have already applied for this position and the selection process is currently
ongoing. The student will have chance to use the data for his/her bachelors or masters thesis, and
will be included as co-author on all publications.

Location and duration of project

The 3 locations selected for the 6-week study, in February and March 2015, are Sulaiman Bay
(Berau District, East Kalimantan), Tarakan City (North Kalimantan) and Balikpapan Bay (Penajam
Paser Utara District, East Kalimantan, Stark et al. 2012). The samples will be analyzed in Jakarta in
collaboration with Laboratory of Nutrition Testing, Zoology Division, Research Center for Biology,
Indonesian Institute of Sciences (LIPI), Cibinong Science Center (Jl. Raya Jakarta-Bogor KM 46,
Cibinong 16911).