Boonratana, R. 2003b. Feeding Ecology of Proboscis Monkeys (Nasalis larvatus) in the Lower Kinabatangan, Sabah, Malaysia. Sabah Parks Nature Journal. 6: 1-26

8/22/2019 Boonratana, R. 2003b. Feeding Ecology of Proboscis Monkeys (Nasalis larvatus) in the Lower Kinabatangan, Saba

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Sabah Parks Nature Journal Vol. 6 (2003):1-26

Feeding Ecology of Proboscis Monkeys(Nasalis larvatus) in the Lower Kinabatangan,

Sabah, Malaysia

Ramesh Boonratana

Department of Biology, Faculty of Science

Chiang Mai University,

Chiang Mai 50202, THAILANDE-mail: [email protected]

Abstract: Nasalis larvatus is a large, sexually dimorphic, monotypic arboreal colobine,

endemic to the island of Borneo, where it is largely restricted to riverine, peat swamp

and mangrove forests of the coastal lowlands. All colobines, including N. larvatus,

possess specialised digestive physiology and sacculated stomachs with anaerobic,

cellulolytic bacteria in their fore-stomachs. This allows them to break down cell wall

constituents and defensive chemicals found in plant foods. N. larvatus are selective

feeders, consuming large quantities of young foliage, and a significant proportion of

flowers, unripe fruits and seeds. Compared to mature individuals, immature

individuals consumed less foliage, but instead consumed more flowers and fruits,

including seeds. Food items with high levels of digestion inhibitors were avoided.

Food items were selected for their higher protein to digestion inhibitor ratio. Being a

large colobine, N. larvatus need a large total food intake, and since they can afford to

process food slowly, their food items must be abundant, but not necessarily easy to

digest.

Key Words: Borneo, feeding ecology, Nasalis larvatus, Proboscis monkey

INTRODUCTION

Like most primates, Nasalis larvatus depend on plant foods to meet their

dietary requirements, which include acquisition of energy, protein, vitamins,

and trace elements. A primate must also minimise its intake of toxins and

compounds that will inhibit digestion. To meet these demands, primates have

evolved different strategies for food selection, and they do not feed at random,

but are highly selective feeders.


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There are two principal factors underlying the selection of plant foods: the

nutritional and secondary compound content of the plant part, and its relative

availability in time and space (McKey, 1978; Milton, 1979; McKey et al., 1981;

Oateset al

., 1980; Bennett, 1983; Davies, 1984; Davieset al

., 1988;Waterman et al., 1988). Many primate species must choose foods from more

than one dietary category each day to obtain a balance of essential nutrients

and energy. They must also choose from many dietary categories to reduce

potential toxins from any one species (Waterman, 1984). This, however,

limits the amount of food that can be eaten from any one category per unit

time.

In response to grazing, plants employ defences to protect their parts, of which

one is to alter the physical composition of the plant parts. It can also include

the nutritional content of the plant parts, their proportion of indigestible

material, and their content of defensive compounds (Freeland & Janzen,1974; Milton, 1984). Plant parts contain secondary compounds, some of

which may function to deter plant-eating animals, and some are highly toxic

to many animals (Freeland & Janzen, 1974; McKey, 1978; Oates et al., 1980;

McKey et al., 1981; Waterman & Choo, 1981). Some secondary compounds

can be distasteful and malodorous. Some others can interfere with the

digestion of nutrients in the gut or with the metabolic processes of the

animal, sometimes with fatal results (Freeland & Janzen, 1974). Furthermore,

most plant parts are high in indigestible cell wall materials that are made up

of celluloses, hemicelluloses, and lignin. These three cell wall constituents arenot affected by any known digestive enzymes of vertebrates (Parra, 1978).

To counter toxic substances and to break down cell wall constituents,

colobines including N. larvatus have enlarged fore-stomachs that contain vastcolonies of bacteria with cellulolytic properties (Bauchop & Martucci, 1968;

Ohwaki et al., 1974; Bauchop, 1978). Such specialised digestive systems can

also detoxify chemical defences found in the food (McKey et al., 1981). The

gut flora can also break down the celluloses and hemicelluloses of plant cell

walls by fermentation. During fermentation, various end products are

produced, including energy-rich short-chain volatile fatty acids. These volatile

fatty acids can be absorbed by the animal and might make an important

contribution to its energy budget (Bauchop & Martucci, 1968; Parra, 1978).

Colobines include large proportions of leaves in their diet and maintain the

proper forestomach environment for plant foods to be digested (Waterman et

al., 1988). This high consumption of leaves led to the belief that the general

trend in colobine diets is towards folivory (Struhsaker, 1975; Clutton-Brock,

1977; Struhsaker & Leland, 1987). Most colobine studies have, however,

found that fruits and seeds are also consumed in significant amounts (Curtin,


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1975; 1980; Hladik, 1977; Oates, 1977; 1988; Oates et al., 1980; Marsh,

1981; McKey et al., 1981; Bennett, 1983; Davies, 1984; Gurmaya, 1986;

Bennett & Sebastian, 1988; Yeager, 1989; Stanford, 1991; Boonratana & Le,

1994). Sugar-rich fruits are normally avoided because their fermentationincreases the level of acidity in the fore-stomach, and is harmful to the micro-

flora present, and can also cause bloat (Bauchop, 1978; Davies et al., 1983;

1988). Although seeds are slower to digest, they are rich in protein,

carbohydrates and lipids (McKey et al., 1981; Waterman, 1984), hence are

important sources of energy.

This paper describes the food of N. larvatus, and the monthly, diurnal, and

age/sex variation of the diet in relation to the availability of foods. The

selection of food items in relation to the animals digestive physiology and

phytochemistry of plant parts is also examined.

STUDY AREA

The study was conducted at Sukau (530N/11817E) and Abai

(541N/11823E), located along the Kinabatangan River in eastern Sabah,

Bornean Malaysia. Much of the Lower Kinabatangan region is forested, albeit

subjected to different degrees of disturbance, and sparsely scattered with

villages and oil palm plantations. The lower part of the Kinabatangan River

meanders through a large flat floodplain, much of which is subject to seasonal

flooding, resulting in low-stature forest with little timber of commercial value.The forest at Sukau is predominantly riverine, whereas at Abai it is

predominantly mangrove (Boonratana, 1993).

Mean temperatures did not vary much between months during the study

period. The mean monthly minimum for 1990 and 1991 was 23.7C, and the

mean monthly maximum for 1990 was 32.9C, and for 1991, it was 33C. The

total rainfall for 1990 was 1,816 mm, and for 1991 it was 2,975 mm

(Boonratana, 1993).

METHODS

To obtain information on N. larvatus feeding ecology, full day observations

from dawn to dusk were made, using the scan sampling method (Altmann,

1974). All observations were made using Zeiss Dialyt 10x40B binoculars. At

the Sukau study area, a focal one-male group (OMG), SU1 was identified and

observed. Whenever SU1 could not be located, then observations were made

on other groups ofN. larvatus. Observations were made from the boat in the

morning before SU1 moved away from the riverside, and in the evening after


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the group returned to the riverside. During the day when SU1 moved into theforest, the group was followed on foot.

At Abai, it was not possible to observe a group continuously throughout the

day. This was partly due to the shyness of the study animals to the observeron foot, but mainly due to the forest being flooded during the high tide.During low tide, however, the ground was very soft and muddy, making quickand noiseless follows impossible. The presence of Crocodylus porosus in thearea was also a deterrent. Thus, almost all observations were made from theboat, when the animals were by the river. The observer remained with agroup for as long as possible and then searched for another group when thefirst group was no longer visible.

Scan samples were recorded during a 2-minute period every 15 minutes from

dawn to dusk on every full day follow, and encompassed all members of thegroup that could be observed during that period. An observation refers toone animal recorded during each scan. During every feeding observation, datathat were recorded included time, age, sex, and identity of the individual, plantpart and species (if identifiable).

RESULTS

Sukau Study Area

Food Items

Young leaves were the major food item for OMGs at Sukau, accounting for

more than 70% of their annual diet (Table 1), while mature leaves (0.3%),made an insignificant proportion of the animals diet. The monkeysconsumed almost an equal amount of whole fruits and flowers, includingflower buds. About 20% of the fruits consumed comprised ripe fruits. Thefleshy portions of fruit were at times discarded, and only seeds wereconsumed. Although this was a small portion of the animals diet (2.4%), itprobably was an important dietary item. About 8% of the food items eatencould not be observed with certainty. Almost 60% of the non-breeding

groups (NBG) diet comprised young leaves. Unripe fruits were alsosignificant food items. The sample size of food items that could not beidentified was small (1.4%).

Only some plant species that N. larvatus consumed could be identified withcertainty (Table 2). Among those, Mallotus muticus (Euphorbiaceae), acommon species at Sukau (Boonratana, 1993), was an important food plant.Mature and young leaves, and unripe fruits including seeds of this specieswere consumed. About 50% of the mature leaves eaten were M. muticus.


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Table 1. Percentage of different items in N. larvatus diet

Groups ML YL RF UF FL FB SD UN

OMG (Sukau; n=594) 0.3 72.7 1.7 6.6 7.8 0.5 2.4 8

NBG (Sukau; n=72) - 59.7 1.43 37.5 - - - 1.4

OMG (Abai; n=155) - 49.7 - 20.6 15.5 - 11.6 2.6

NBG (Abai; n=33) - 72.7 - 27.3 - - - -

ML: mature leaves; YL: young leaves; RF: Ripe fruits; UF: unripe fruits; FL: flowers; FB: flower

buds; SD: seed; UN: unidentified items; OMG: one-male group; NBG: non-breeding group

(includes all-male group and loosely-bonded predominantly male group with at least one

female member).

The unripe fruits of Microcos antidesmifolia (Tiliaceae) and an unidentified

species of the family Combretaceae comprised significant proportions of the

unripe fruits eaten. About one-third of the flower buds eaten were Dillenia

indica (Dilleniaceae).

Although none of the animals was observed to feed on anything other than

plant materials, they must have inadvertently fed on fig wasps and other fig

parasites when they fed on fruits of Ficus spp. (Moraceae). Once, an adult

male and a sub-adult male were observed feeding on the ripe fruits ofFicus

racemosa. These observations, however, were not part of the scan samples,

hence not included in the analysis.

Monthly Variation

There was considerable variation in the proportion of different plant parts

eaten throughout the year (Fig. 1). The amount of young leaves eaten was

high in most months but lower in July and September. This corresponded

with increased fruit intake in the animals diet. There was a negative

correlation between young leaves and fruits in the diet (Spearman rank

correlation rs=-0.413, n=12, p


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Table 2. List of food plants and plant parts eaten by N. larvatus at Sukau. Figures in

parentheses indicate the percentage in the diet, recorded during scan observations

(n=613)

Species Part EatenCoeloestegia sp. (Bombacaceae) YL

Unidentified sp. A (Combretaceae) UF(0.7)

Merrenia borneensis (Convulvulaceae) UF

Dillenia indica (Dilleniaceae) FL(0.2), FB(0.2)

Dipterocarpus sp. A (Dipterocarpaceae) YL

Claoxylon sp. A (Euphorbiaceae) YL

Glochidion borneensis (Euphorbiaceae) YL

Glochidion obscurum (Euphorbiaceae) YL, UF

Macaranga hypoleuca (Euphorbiaceae) YL

Mallotus floribindus (Euphorbiaceae) YLMallotus wrayi (Euphorbiaceae) ML, YL

Mallotus muticus (Euphorbiaceae) ML(0.2), YL(5.7), UF(0.8), SD

Mallotus sp. A (Euphorbiaceae) YL

Bridelia stipularis (Euphorbiaceae) SD

Bauhinia sambafida-sambafida (Fabaceae) YL

Spantholobus hirsutus (Fabaceae) YL

Homalium foetidum (Flacourtiaceae) YL

Hydnocarpus woodii (Flacourtiaceae) UF(0.2), SD

Dehessia incrassata (Lauraceae) YL

Ficus condensa (Moraceae) YLFicus globbosa (Moraceae) YL, UF

Ficus pellucido-punctata (Moraceae) UF

Ficus depressa (Moraceae) UF

Ficus racemosa (Moraceae) UF, RF

Ficus spp. (Moraceae) YL(1.6), UF(0.2)

Knema latifolia (Myristicaceae) YL

Stenochlaena palustris (Polypodiaceae) YL

Parinari oblongifolia (Rosaceae) YL

Nauclea subidita (Rubiaceae) YL

Neonauclea gigantea (Rubiaceae) YL

Neonauclea crytopoda (Rubiaceae) SD

Anthocephalus chinensis (Rubiaceae) YL

Unidentified sp. B (Santalaceae) YL

Microcos antidesmifolia (Tiliaceae) YL, UF(2.9)

Microcos sp. A (Tiliaceae) YL

Cayratia sp. A (Vitaceae) YL


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All unidentified spp. ML(0.2), YL(67.9), RF(1.6),

UF(4.4), FL(7.3), FB(0.3), SD(2.3)

Liana YL(0.7), RF(0.2)


buds; SD: seed; UN: unidentified items.

young leaves was high throughout the year (Boonratana, 1993). Conversely,

there was a slight positive correlation (rs=0.524, n=12, p


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flowers available to N. larvatus were influenced by rainfall patterns.

Alternatively, the monthly mean maximum temperature was positively

correlated with the amount of time N. larvatus spent feeding on flowers

(rs

=0.615, n=12, p


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Table 3. Percentage of different items in one-male groups diet by age/sex class at

Sukau (n=534) and Abai (n=154)

ML YL RF UF FL FB SD UN

SUKAUAdult males (n=35) - 88.6 - 2.9 5.7 - - 2.9

Adult females (n=290) 0.3 72.5 1.7 6.6 8.7 0.3 2.8 7

Older juveniles (n=63) - 74.6 1.6 6.3 4.8 - 1.6 11.1

Younger juveniles (n=121) - 66.7 - 10.8 10 1.7 2.5 8.3

Older infants (n=23) - 60.9 17.6 4.3 8.7 - - 8.7

ABAI

Adult males (n=10) - 30 - 30 30 - 10 -

Adult females (n=82) - 51.2 - 15.9 14.6 - 17.1 1.2

Older juveniles (n=14) - 71.4 - 7.1 14.3 - - 7.1

Younger juveniles (n=42) - 45.2 - 31 11.9 - 7.1 4.8


buds; SD: seed; UN: unidentified items.

Different age/sex classes spent different amounts of time feeding from month

to month (Fig. 3). There was no difference between the amount of time adult

males and adult females spent feeding (Wilcoxon T=5.67, n=12, p>0.05).

There was a significant difference between adult males and older juveniles

(T=7.89, n=12, p


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Similarly, adult females spent less time feeding than older juveniles (T=7.78,

n=12, p


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time feeding than young juveniles (T=11, n=13, p


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Table 4. List of food plants and plant parts eaten by N. larvatus at Abai. Figures in

parentheses indicate the percentage in the diet, recorded during scan observations

(n=184)

Species Part EatenNypa fruticans (Arecaceae) FL(6.5)

Polyalthia glauca (Annonaceae) FL

Canarium sp. A (Burseraceae) YL

Santiria laevigata (Burseraceae) YL

Sapium indicum (Euphorbiaceae) YL

Sonneratia alba (Lythraceae) YL(39.7), UF(7.1), FL(1.1), SD(9.8)

Ficus sumatrana (Moraceae) YL, UF

Ficus microcarpa (Moraceae) YL, UF

Ficus spp. (Moraceae) YL(1.6), UF(7.6)

Eugenia crysantha (Myrtaceae) YLEugenia barringtoides (Myrtaceae) SD

Chionanthus cuspidata (Oleaceae) YL

Bruguiera sexangula (Rhizophoraceae) FL

Ganua motleyana (Sapotaceae) YL, UF

Heritiera littoralis (Sterculiaceae) YL

Pterospermum elongatum (Sterculiaceae) YL

Teijsmanniodendron sp. A (Verbenaceae) YL

Avicennia alba (Verbenaceae) YL, UF, SD, FL

All unidentified spp. YL(13), UF(1.6), FL(5.4)

ML: mature leaves; YL: young leaves; RF: Ripe fruits; UF: unripe fruits; FL: flowers; FB: flowerbuds; SD: seed; UN: unidentified items.

The monthly variations for the various items in the diet were correlated with

the monthly variation in time spent in major activities, but not with

availability. A slight positive correlation existed between the amount of young

leaves in the diet with time spent resting (rs=0.637, n=8, p


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Fig. 5. Monthly variation in plant parts eaten at Abai (n=155, unweighted data)

Age/Sex Variation

Annually, different age/sex classes invested different amounts of time feeding

on different plant parts (Table 3). All age/sex classes, however, spent most of

their time feeding on young leaves. Adult females, juveniles, and older infants

fed more on young leaves than did the OMG males. Adult males spent equal

proportions of their time feeding on young leaves, fruits, and flowers.

Fig. 6. Monthly variation in time spent feeding by different age/sex class at Abai

(n=155, weighted data)


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Monthly, there were variations in time spent feeding by the different age/sex

classes (Fig. 6). There was no significant difference in time spent feeding

between the OMG males and adult females (T=5.67, n=8, p>0.05). There was

also no significant difference when monthly variation for the time spent

feeding was compared between adults and immature individuals (T=3.25,

n=8, p>0.05).

Adult males spent less time feeding than older juveniles (T=7.89, n=8, p


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Adverse effects of CT can be felt only when it is present at a high level, more

than 1% dry weight (Gartlan et al., 1980). Presbytis rubicunda, however, fed

on foods which had relatively high tannin contents, probably because low

levels of tannins can improve protein digestibility (Davies et al., 1988).

The amount of tannin plus fibre was plotted against that of protein for all

food items eaten and not eaten (Figure 7). The food items that formed a

significant part of the diet all had a relatively high ratio of protein to

digestion inhibitors, seen in the lower right portion of the figure. Similar

results were also seen for past studies of colobine feeding ecology (McKey et

al., 1981; Davies, 1984; Bennett, 1983; Davies et al., 1988). The animals all

selected food items which were above a minimum ratio of protein to

digestion inhibitors.

Fig. 7. Condensed tannin (CT) + Neutral detergent fibre (NDF) against Protein

contents of samples eaten and not eaten

Two of the mature leaf samples, Sapium indicum (Euphorbiaceae) and

Spantholobus hirsutus (Leguminosae), were not eaten although they did notcontain any condensed tannin and had higher protein and NDF levels. The

presence of saponins at a higher level may have deterred the animals from

eating those species. Saponins were present in more than 60% of the mature

leaf samples that were not eaten. Although saponins were present in both

mature leaf samples that were eaten, they were low, implying that it was at an

acceptable level. Furthermore, their CT levels were also low.

Young leaves were most preferred plant part at both Sukau and Abai

(Boonratana, 1993). Only seven samples out of the 33 analysed were known


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Table 6. Chemical composition of plant parts not observed eaten by N. larvatus

Species Part Sap %Prot CT %NDF

Polyalthia glauca ML 1.56 9.15 56.5

Dillenia indica ML 1+ 1.75 0.24 64.2YL 1.94 0.24 58.0

Claoxylon sp. A ML 0.88 2.71 61.1

Sapium indicum ML 2+ 2.19 0 63.7

Homalium foetidum ML 1.44 30.34 40.6

Hydnocarpus woodii ML 1+ 1.94 3.65 67

Spantholobus hirsutus ML 2+ 4.56 0 91.5

Sonneratia alba ML 2.06 5.15 52.2

Knema latifolia ML 2+ 2.25 3.41 76

Chionanthus cuspidita ML 1+ 1.38 13.29 72.7

Microcos sp. A ML 1+ 1.06 1.41 64.2ML: mature leaves; YL: young leaves; FR: fruits; FB: flower buds; Sap: saponins; %Prot:

percent protein; CT: condensed tannin (mg/g); %NDF: percent neutral detergent fibre

foods ofN. larvatus (Table 5). Young leaves eaten had a higher mean protein,

CT, and NDF than the one young leaf sample not eaten (Table 6). All the young

leaves eaten, however, had low CT level, less than 0.5 mg/g. Results showed

that on the average, young leaves were selected for their higher protein and

moderately high dietary fibre levels, but lower CT level.

Young leaves of Claoxylon sp. A (Euphorbiaceae), a food plant, have a high

protein content, moderately high NDF content and low CT level. Although the

young leaves of Chionanthus cuspidita (Oleaceae) have low protein content,

they were probably consumed because of their low CT, and possibly for their

higher dietary fibre (NDF) level. Conversely, N. larvatus did not feed on the

young leaves of Dillenia indica (Dilleniaceae), despite its acceptable levels of

protein, CT and NDF.

A comparison between mature leaves and young leaves of three species

whose young leaves were eaten showed that the uneaten mature leaves had

lower protein and higher CT level. This implies that young leaves eaten wereof higher levels of digestible protein. Results suggest thatN. larvatus selected

foliage that had higher protein, lower CT, and moderately high NDF.

Flower Selection

A small sample (n=5) of flowers was analysed (Boonratana, 1993; Loh, 1991),

of which only one sample, the flower bud ofDillenia indica (Dilleniaceae) was

eaten (Table 5). It is of interest thatN. larvatus fed on the flower buds of D.

indica even though its protein level is lower than the uneaten leaves of the


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same species (Table 6). Although, CT level of the flower bud was half that of

the leaves, CT level of the leaves were still within the range of other plant

parts eaten. They, however, might have been eating it for energy.

Fruit Selection

A total of 18 fruit samples was analysed (Boonratana, 1993; Loh, 1991), of

which only two, Mallotus muticus (Euphorbiaceae) and Sonneratia alba

(Lythraceae), were identified with certainty as food plants (Table 5).

Generalisations about their selectivity could not be made, as there were no

known fruit samples that were not eaten to compare with. Moreover, the

sample size was too small. It was, however, seen that the protein content, CT,

and NDF of the fruits eaten were within the range of other plant parts eaten.

It is difficult to assess the influence of plant chemicals in fruits and seeds.

Fruits differ in their size, structure, chemical composition, and availabilityaccording to season. Furthermore, fibre and tannin in fruits are mostly found

in the exocarp. Thus, the effects of both on the animals diet are insignificant

if the seeds are broken and the exocarp removed (Davies et al., 1988).

Moreover, animals might be selecting leaves and fruits for different reasons:

leaves for protein, and fruits/seeds for energy.

DISCUSSION

The feeding behaviour of N. larvatus varied through its active period, often

occurring in distinct bouts separated by periods of travel and inactivity.

Rarely was there absolute synchronisation in feeding, although members of

SU1 and other OMGs generally coordinated their travel. Even at the height of

a feeding bout, almost three-quarters of SU1 were either travelling or

inactive. Similarly, at the height ofP. [badius] tephrosceles feeding bouts, about

half of the group was inactive (Clutton-Brock, 1974). Feeding was highly

synchronised in Cercopithecus aethiops only when the group was exploiting a

preferred food source (Kavanagh, 1978).

Most studies on primate feeding patterns showed feeding bouts to be most

intense and prolonged at the beginning and at the end of the active period. N.larvatus at Sukau, however, had their major feeding bouts between 1100 and

1200 hours and at 1600 hours. Although not intensive, they had a prolonged

feeding bout between 0800 and 1000 hours. A likely explanation for this is

that N. larvatus has a prolonged retention time, estimated at 52 hours

(Dierenfeld et al., 1992). Retention is the interval between recovery of 5 and80% of dosed markers in faeces (van Soest, 1982; van Soest et al., 1983).

Thus, N. larvatus do not have such a need to feed much at the beginning of the


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day to obtain energy as a monogastric primate. For monogastric primates like

Hylobates syndactylus (Chivers, 1974), Hylobates lar(Raemaekers, 1978), and

Callicebus torquatus (Kinzey, 1977), there is a very clear diurnal trend. At the

start of the day H. syndactylus and C. torquatus feed on fruits, but at end of theday they feed on leaves. Fruits are easily and quickly digested, therefore

eating fruits at start of the day may restore the energy deficit of the night

(Chivers, 1975; Wrangham, 1977). Eating leaves at end of the day may keep

the digestive system active for longer periods (Clutton-Brock, 1977), and also

allows the animals to obtain enough energy so as not to cause a deficit during

their inactive period (Bennett, 1983).

Data showing that adult N.larvatus consumed more leaves than immature

individuals imply that adults could digest fibre-rich food parts better than

could immature individuals. Thus, immature individuals supplemented their

dietary intake with easily digestible foods. The lack of differences for the timespent feeding between the adult male and females was probably because of

the strong sexual dimorphism exhibited by N. larvatus. In most mammals,

adult females normally feed more than adult males because of the costs of

pregnancy and lactation (Clutton-Brock, 1977). The adult male N. larvatus is

twice bigger than the adult female, therefore, also requires more food. Older

juveniles probably consumed more than adults did because food was

important for growth. Other immature individuals, young juveniles, and older

infants supplemented their dietary intake needed for growth with breast milk.

Young infants relied wholly on breast milk.Comparison of the diets ofN. larvatus at four different sites shows that young

leaves are the most important dietary items, particularly in the riverine forest

at Sukau (Table 8). In the mangroves of Abai, flowers, fruits, and seedssignificantly contribute to the animals diet. A likely reason for this difference

is that fruits and flowers are more available at Abai than at Sukau

(Boonratana, 1993). Furthermore, the flower and fruit production at Abai

was higher, although the general trends were similar (Boonratana, 1993). At

Tanjung Puting National Park in Kalimantan (Yeager, 1989), and at

Samunsam Wildlife Sanctuary in Sarawak (Bennett & Sebastian, 1988), fruits

and seeds contribute a significant proportion to the diet ofN. larvatus. The

inflorescences of Nypa fruticans (Arecaceae) are more commonly eaten at

Abai than Samunsam, although it occurred in both sites. This is especially

important in view of often huge areas ofN. fruticans around.

Data and observations suggest that N. larvatus are folivore-frugivores, with

also a strong preference for seeds. Almost all fruits eaten were unripe and

non-succulent. The degree of frugivory is subject to availability. Phenological

data show that fruits were more abundant in the mangrove forests of Abai


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Table 7. Comparative proportions, expressed as percentage, of plant parts in some

colobines diets.

Species ML ML

+YL

YL FL FR FR+

SD

SD Source

N. larvatus 0.3 - 72.7 8.3 8.3 - 2.4 Boonratana,

1993.

N. larvatus - - 49.7 15.5 20.6 - 11.6 Boonratana,

1993.

N. larvatus 3 - 38 3 35 - 15 Bennett &

Sebastian,

1988.

N. larvatus 2.7 - 41.2 3 40.3 - 20.3 Yeager, 1989.

T. pileatus 42 - 11 7 24 - 9 Stanford, 1991.

T. obscurus 22 - 36 7 32 - 2 Curtin, 1980.

T. johnii 27 - 31 12 25 - - Oates et al.,

1980

T. vetulus 40 - 20 12 28 - - Hladik, 1977a.

S. entellus 21 - 27 7 45 - - Hladik, 1977a.

S. entellus 31 - 14 - - 47 - Curtin, 1975

P. rubicunda 1 - 36 11 19 - 30 Davies, 1984.

P. melalophos 7 - 26 17 20 - 26 Bennett, 1983.

P. thomasi - 32 - 8 58 - - Gurmaya, 1986.

P. hosei 1.3 - 70.8 0.2 18.8 - 21.3 Mitchell, 1994.

P. hosei 6.5 - 58.3 2.8 2.8 - 16.7 Mitchell, 1994.C. guereza 12 - 62 2 14 - - Oates, 1977.

C. satanas 18 - 21 3 - - 53 McKey et al.,

1981.

P.b.

rufomitratus

11.

5

- 42.4 6.2 24.1 - 0.9 Marsh, 1981.

P.b. tephrosceles 44 - 35 7 1 - - Clutton-Brock,

1977.

P.b. tephrosceles 21 - 51 12 6 - - Struhsaker,

1975.

P. verus 11 - 59 - 5 - 14 Oates, 1988.

R. avunculus - - 38 - 47 - 15 Boonratana &

Le, 1994.

(Boonratana, 1993) and Samunsam (Rajaratnam, 1991), and the peat swamp

forest of Tanjung Puting (Yeager, 1989), than in the riverine forest of Sukau.

Colobines generally feed on young leaves and fruits. Seed-eating, however, is

integral to the diet of some species. In C. satanas, a little more than half their

diet consists of seeds (McKey et al., 1981). Similarly, 30% of the diet ofP.


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Ramesh Boonratana

rubicunda comprised seeds (Davies, 1984; Davies et al., 1988). Colobines

avoid eating succulent, sweet fruits but select for unripe fruits and seeds.

When, on occasion, sugar-rich foods are eaten, volatile fatty acids are

produced much more quickly than they can be absorbed. This can lead toacidosis, with fatal results (Davies et al., 1988).

All the food plant samples ofN. larvatus contain low levels of CT. Herbivores

generally avoid foods with high amounts of CT because high CT levels can

inhibit food absorption in three ways (Kumar & Vaithiyanathan, 1990). First,

it can reduce the digestive ability in ruminants, reacting with the outer layer

of the gut cells, and reducing the absorption ability of the gut wall. In

ruminants, this serves as an important factor in the control of the intake of

food. Secondly, there is evidence showing that CT can influence hormone

levels. Thirdly, an animal may reduce its food intake just because of distaste.

Tannin causes saliva protein to settle and blood capillaries or tissues toshrink. Such effects along with the capacity to settle protein depend on the

molecular weight of CT (Kumar & Vaithiyanathan, 1990). In colobines, the

tolerance of CT seems variable between species, and low levels might be

beneficial to small species, by slowing down digestion, thereby improving

protein digestibility and reducing the chances of acidosis (Davies et al.,

1988).

Plant parts eaten by N. larvatus had a moderately high NDF content. Plant

parts that had exceedingly high or low NDF were not selected. Exceedingly

high NDF may cause such a slow rate of digestion and that it clogs up thesystem (Parra, 1978). On the other hand, low levels of NDF may cause the

digestion to proceed too fast, causing acid and methane to be released

excessively until they endanger the animal. A balance, therefore, is required(Loh, 1991).

Plant parts eaten by N. larvatus have few or no saponins. Saponins function as

defence agents in plants, and are expected to influence a herbivores dietary

habits, in the same way that does tannins (Freeland et al., 1985).

Nevertheless, a herbivore may overcome the effects of tannin and saponins by

simultaneously consuming foods that contain both classes of chemicals(Ewart, 1979). It is most likely that the effects of tannin and saponins

neutralise each other.

None of the food plant samples analysed contained any alkaloids. Some

colobine species, however, can detoxify alkaloids in their foods (McKey et al.,

1981; Waterman, 1984). Detoxification is believed to be carried out by the

micro-flora found in the fore-stomach. This is one of the major differences

from monogastric primates (Hladik, 1977; Waterman, 1984). Hylobates lar,

for example, eats foods which contain no alkaloids (Vellayan, 1982).


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21


The digestibility of food depends on the amount of time it remains in the

digestive tract. In turn, this is determined by its passage rate (Janis, 1976; van

Soest, 1977; Milton, 1984). Animals like N. larvatus that pass food through

the gut slowly presumably have emphasised the maximal extraction of

nutrients.

Large mammals like N. larvatus have lower energy requirements per unit

body weight than do small ones (Kleiber, 1961). They can afford to process

food more slowly, but their total food requirements must also be great. Thus,

their food items ought to be abundant but not necessarily easy to digest

(Richard, 1985). In the tropical rainforest, leaves are among the most

abundant edible plant parts. They, however, also contain high levels of partially

or completely indigestible carbohydrates. N. larvatus probably has one of the

lowest metabolic rates among colobines (Dierenfeld et al., 1992), and can

therefore process leaves in bulk, meeting its protein needs and part of itsenergy needs by slowly digesting and absorbing the contents of large

quantities of food with lower levels of energy and digestible protein.

Metabolic costs per unit body weight become proportionally lower with an

increase in body size. Larger species, however, are more likely to show gut

modifications and digestive strategies because of a longer retention time of

food. The efficient digestion of plant cell wall material, particularly more

lignified material, is a time consuming process (van Soest, 1977; 1982).

Furthermore, it has been estimated that a body size of 10 kg or greater might

be required for a digestive strategy based entirely on foregut fermentation(van Soest, 1981). Thus, N. larvatus are one of few Asian colobines that can do

this.

Different primate species feed on different subsets of the available plant

resources. Features of digestive morphology might play an important role in

deciding which plant foods a given primate species chooses (Bennett &

Caldecott, 1988). Food choice might be dictated as much by internal

constraints intrinsic to the digestive system of the animal as by extrinsic

factors such as nutrient content or relative availability (Milton, 1984).

ACKNOWLEDGMENTS

Permission to conduct this study was granted by the Sabah Ministry of

Tourism and Environmental Developments Wildlife Department.

Phytochemical analyses were carried out by Loh Soo Nai, and field assistance

was provided by Dionysius S. Sharma. This study was supervised by Dr.

Elizabeth L. Bennett and Prof. Warren Y. Brockelman, and funded by the

Wildlife Conservation Society.


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Documents

Boonratana, R. 2003b. Feeding Ecology of Proboscis Monkeys (Nasalis larvatus) in the Lower Kinabatangan, Sabah, Malaysia. Sabah Parks Nature Journal. 6: 1-26