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, THAILAND E-mail: rbz@loxinfo.co.th
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; Oates et al., 1980; Bennett, 1983; Davies, 1984; Davies et 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 are not 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 vast colonies 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,

Feeding Ecology of Proboscis Monkeys

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 fermentation increases the level of acidity in the fore-stomach, and is harmful to the microflora 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 of N. 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 the forest, 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 observer on 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 quick and noiseless follows impossible. The presence of Crocodylus porosus in the area was also a deterrent. Thus, almost all observations were made from the boat, when the animals were by the river. The observer remained with a group for as long as possible and then searched for another group when the first 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 the group that could be observed during that period. An observation refers to one animal recorded during each scan. During every feeding observation, data that were recorded included time, age, sex, and identity of the individual, plant part 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 monkeys consumed almost an equal amount of whole fruits and flowers, including flower buds. About 20% of the fruits consumed comprised ripe fruits. The fleshy portions of fruit were at times discarded, and only seeds were consumed. Although this was a small portion of the animals diet (2.4%), it probably was an important dietary item. About 8% of the food items eaten could not be observed with certainty. Almost 60% of the non-breeding groups (NBG) diet comprised young leaves. Unripe fruits were also significant food items. The sample size of food items that could not be identified was small (1.4%). Only some plant species that N. larvatus consumed could be identified with certainty (Table 2). Among those, Mallotus muticus (Euphorbiaceae), a common species at Sukau (Boonratana, 1993), was an important food plant. Mature and young leaves, and unripe fruits including seeds of this species were consumed. About 50% of the mature leaves eaten were M. muticus.

Feeding Ecology of Proboscis Monkeys Table 1. Percentage of different items in N. larvatus diet Groups OMG (Sukau; n=594) NBG (Sukau; n=72) OMG (Abai; n=155) NBG (Abai; n=33) ML 0.3 YL 72.7 59.7 49.7 72.7 RF 1.7 1.43 UF 6.6 37.5 20.6 27.3 FL 7.8 15.5 FB 0.5 SD 2.4 11.6 UN 8 1.4 2.6 -

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 of Ficus 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<0.05). There was also a negative correlation between the amounts of young leaves and flowers in the diet (rs=-0.601, n=12, p<0.005). N. larvatus ate more young leaves than they ate fruits and flowers. The amount of young leaves in the diet reached a peak in May and June, which corresponded with low levels of fruits and flowers eaten in those two months respectively. In July, a decrease in young leaves in the diet corresponded with an increase in flowers and fruits intake. Items in the diet were correlated with the phenology of their habitat. A slight negative correlation existed between young leaves in the animals diet and their availability in the forest (rs=-0.486, n=12, p<0.05), but the availability of

Ramesh Boonratana 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 Coeloestegia sp. (Bombacaceae) Unidentified sp. A (Combretaceae) Merrenia borneensis (Convulvulaceae) Dillenia indica (Dilleniaceae) Dipterocarpus sp. A (Dipterocarpaceae) Claoxylon sp. A (Euphorbiaceae) Glochidion borneensis (Euphorbiaceae) Glochidion obscurum (Euphorbiaceae) Macaranga hypoleuca (Euphorbiaceae) Mallotus floribindus (Euphorbiaceae) Mallotus wrayi (Euphorbiaceae) Mallotus muticus (Euphorbiaceae) Mallotus sp. A (Euphorbiaceae) Bridelia stipularis (Euphorbiaceae) Bauhinia sambafida-sambafida (Fabaceae) Spantholobus hirsutus (Fabaceae) Homalium foetidum (Flacourtiaceae) Hydnocarpus woodii (Flacourtiaceae) Dehessia incrassata (Lauraceae) Ficus condensa (Moraceae) Ficus globbosa (Moraceae) Ficus pellucido-punctata (Moraceae) Ficus depressa (Moraceae) Ficus racemosa (Moraceae) Ficus spp. (Moraceae) Knema latifolia (Myristicaceae) Stenochlaena palustris (Polypodiaceae) Parinari oblongifolia (Rosaceae) Nauclea subidita (Rubiaceae) Neonauclea gigantea (Rubiaceae) Neonauclea crytopoda (Rubiaceae) Anthocephalus chinensis (Rubiaceae) Unidentified sp. B (Santalaceae) Microcos antidesmifolia (Tiliaceae) Microcos sp. A (Tiliaceae) Cayratia sp. A (Vitaceae) Part Eaten YL UF(0.7) UF FL(0.2), FB(0.2) YL YL YL YL, UF YL YL ML, YL ML(0.2), YL(5.7), UF(0.8), SD YL SD YL YL YL UF(0.2), SD YL YL YL, UF UF UF UF, RF YL(1.6), UF(0.2) YL YL YL YL YL SD YL YL YL, UF(2.9) YL YL

Feeding Ecology of Proboscis Monkeys All unidentified spp. Liana ML(0.2), YL(67.9), RF(1.6), UF(4.4), FL(7.3), FB(0.3), SD(2.3) YL(0.7), RF(0.2)

ML: mature leaves; YL: young leaves; RF: Ripe fruits; UF: unripe fruits; FL: flowers; FB: flower 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<0.05) between the amount of flowers in the diet and in the forest. This showed that the animals fed on flowers more when there were more flowers available. No correlation existed between the amount of fruits in diet and in the forest. Items in the diet were correlated with monthly variation in time spent resting, travelling and vigilance (Boonratana, 1993). A negative correlation existed between time spent feeding on fruits and time spent resting (rs=0.510, n=12, p<0.05). The amount of seeds in the diet was positively correlated with monthly time spent travelling (rs=0.434, n=12, p<0.05), but negatively correlated with time spent in vigilance (rs=-0.608, n=12, p<0.005). Thus, in the search for edible seeds, N. larvatus spent more time travelling and less time inactive. Monthly variation in rainfall was negatively correlated with the amount of flowers eaten (rs=-0.490, n=12, p<0.05), but showed no correlation with other food items (Boonratana, 1993). Monthly production of flowers was inversely correlated with rainfall (Boonratana, 1993). This meant that

Fig. 1. Monthly variation in plant parts eaten at Sukau (n=540, unweighted data)

Ramesh Boonratana

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<0.005). Diurnal Variation The diet of N. larvatus at different times of day was examined for variation, if any, in particular plant parts (Fig. 2). The animals ate young leaves at start and end of the day. Otherwise, there was a trimodal pattern in young leaves eaten throughout the day with peaks at 0900, 1200 and 1400 hours respectively. The animals fed on young leaves and some flowers soon after waking up. Flowers were consumed at low levels but reached higher levels at 1100 hours and between 1500 and 1600 hours. Fruits were eaten mostly in the morning and in the evening. Seeds were eaten at low levels during the morning, but reached a peak at 1300 hours. Overall, the variation throughout the day was slight, showing no major trends. Age/Sex Variation Different age/sex classes did not spend equal proportions of their time feeding (Table 3). Excluding sub-adult females, the trend was for a reduction in young leaves eaten with decreasing body size. At the other extreme, older infants fed more on ripe fruits than other age/sex classes. Other than young leaves, adult females fed more on plant parts when compared to adult males. Similarly, immature individuals (juveniles and infants) ate more plant parts other than young leaves compared to adults.

Fig. 2. Diurnal variation of plant parts eaten by SU1 at Sukau (n=489, unweighted data)

Feeding Ecology of Proboscis Monkeys Table 3. Percentage of different items in one-male groups diet by age/sex class at Sukau (n=534) and Abai (n=154)
ML SUKAU Adult males (n=35) Adult females (n=290) Older juveniles (n=63) Younger juveniles (n=121) Older infants (n=23) ABAI Adult males (n=10) Adult females (n=82) Older juveniles (n=14) Younger juveniles (n=42) 0.3 YL 88.6 72.5 74.6 66.7 60.9 30 51.2 71.4 45.2 RF 1.7 1.6 17.6 UF 2.9 6.6 6.3 10.8 4.3 30 15.9 7.1 31 FL 5.7 8.7 4.8 10 8.7 30 14.6 14.3 11.9 FB 0.3 1.7 SD 2.8 1.6 2.5 10 17.1 7.1 UN 2.9 7 11.1 8.3 8.7 1.2 7.1 4.8

ML: mature leaves; YL: young leaves; RF: Ripe fruits; UF: unripe fruits; FL: flowers; FB: flower 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<0.05), and between adult males and older infants (T=3, n=12, p<0.01). Older juveniles spent more time feeding than adult males, whereas older infants spent less time feeding than adult males.

Fig. 3. Monthly variation in time spent feeding by different age/sex class of SU1 at Sukau (n=534, weighted data)

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Similarly, adult females spent less time feeding than older juveniles (T=7.78, n=12, p<0.05), but spent significantly more time than older infants (T=0, n=12, p<0.01). There were significant differences in time spent feeding between older juveniles and younger juveniles (T=3, n=12, p<0.05), and between older juveniles and older infants (T=0, n=12, p<0.01). Both young juveniles and older infants spent less time feeding than older juveniles did. Young juveniles spent more time feeding than did older infants (T=3, n=12, p<0.01). There was no significant difference between the amount of time adults and immature individuals spent feeding monthly (T=7, n=12, p>0.01). Daily, there was a strong variation in the food eaten by the different age-sex classes at different times of day (Fig. 4). Throughout most part of the day, members of SU1 normally did not feed on the same plant part on the same trees of the same species simultaneously. It was more usual for them to spread over a few nearby trees while feeding. At certain times of day, they were occasionally seen feeding on the same plant part from the same species either from the same tree or from a few adjoining trees. This was just as they woke up or when they were ready to retire for the day.

Fig. 4. Diurnal variation in time spent feeding by different age/sex class of SU1 at Sukau (n=534, weighted data)

Similarly, there was no difference in time spent feeding between adult males and adult females, and between adult males and young juveniles. Older juveniles spent more time feeding than did adult males (T=8, n=13, p<0.01), whereas older infants spent less time (T=3.5, n=13, p<0.05). Similarly, adult females spent less time feeding than did older juveniles (T=7.5, n=13, p<0.01) but more than older infants (T=0, n=13, p<0.01). Older juveniles spent more

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time feeding than young juveniles (T=11, n=13, p<0.05) and older infants (T=0, n=13, p<0.01). Immature individuals spent more time feeding than did adults daily (T=6.11, n=123, p<0.05). Abai Study Area Food Items Almost half of the OMGs diet at Abai comprised young leaves (Table 1). Unripe fruits (20.6%), flowers (15.5%), and seeds (11.6%) also figured prominently in their diet. None of the members was ever observed feeding on mature leaves or ripe fruits. Their dietary items could not be observed with certainty for 2.6% of the time. The diet of NBGs consisted entirely of young leaves and unripe fruits (Table 1), but the sample size was small (n=33). Once, a subadult male and once, an older juvenile male were observed feeding on the inflorescence of Nypa fruticans (Arecaceae). These observations, however, were not during the scan sampling period. Analysis of plant parts eaten by N. larvatus at Abai showed that, among the food-plants that could be identified (Table 4), Sonneratia alba (Lythraceae) was an important component of the animals diet. The animals fed on almost all parts of the species and in large quantities. Nypa fruticans was another important species as it was abundant in the study area (Boonratana, 1993), and its inflorescence made up 50% of the animals annual diet of flowers. Ficus spp. (Moraceae), although not abundant, fruited asynchronously and therefore fruits were available to the animals almost throughout the year (Boonratana, 1993). At least a third of the fruits eaten, mostly unripe, belong to the Ficus spp. Monthly Variation There were large monthly variations in plant parts eaten by N. larvatus OMGs at Abai (Fig. 5). There were, however, no correlations in the proportion of different parts eaten. This was most likely due to the small sample size (n=155). Furthermore, data collection was limited to the riverside and did not cover the whole day. There were no correlations between phenological patterns and the amount of plant parts in the diet. This probably resulted from the fact that all plant parts were available throughout the year. Similarly, there were no correlations between monthly rainfall and the amount of plant parts in the animals diet.

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Ramesh Boonratana 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 Nypa fruticans (Arecaceae) Polyalthia glauca (Annonaceae) Canarium sp. A (Burseraceae) Santiria laevigata (Burseraceae) Sapium indicum (Euphorbiaceae) Sonneratia alba (Lythraceae) Ficus sumatrana (Moraceae) Ficus microcarpa (Moraceae) Ficus spp. (Moraceae) Eugenia crysantha (Myrtaceae) Eugenia barringtoides (Myrtaceae) Chionanthus cuspidata (Oleaceae) Bruguiera sexangula (Rhizophoraceae) Ganua motleyana (Sapotaceae) Heritiera littoralis (Sterculiaceae) Pterospermum elongatum (Sterculiaceae) Teijsmanniodendron sp. A (Verbenaceae) Avicennia alba (Verbenaceae) All unidentified spp. Part Eaten FL(6.5) FL YL YL YL YL(39.7), UF(7.1), FL(1.1), SD(9.8) YL, UF YL, UF YL(1.6), UF(7.6) YL SD YL FL YL, UF YL YL YL YL, UF, SD, FL YL(13), UF(1.6), FL(5.4)

ML: mature leaves; YL: young leaves; RF: Ripe fruits; UF: unripe fruits; FL: flowers; FB: flower buds; 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<0.05). There was also a correlation between the amount of flowers in diet with time spent travelling (rs=0.631, n=8, p<0.05), and between the amount of seeds in diet and feeding (rs=0.597, n=8, p<0.05). There was, however, little variation in plant parts available over the year. The above correlations were more likely due to the non-random distribution or patchiness of food trees available (Boonratana, 1993).

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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<0.05), but more than older infants (T=3, n=8, p<0.01). Similarly, adult females spent less time feeding than older juveniles (T=7.78, n=8, p<0.05), but more than older infants (T=0, n=8, p<0.01). Older juveniles spent more time feeding than young juveniles (T=3, n=8, p<0.05), and older infants (T=0, n=8, p<0.01). Similarly, young juveniles spent more time feeding than older infants (T=3, n=8, p<0.01). Food Selection and Phytochemistry Leaf Selection A total of 97 mature leaf samples was analysed (Boonratana, 1993; Loh, 1991), of which only two, Mallotus muticus and M. wrayi (Euphorbiaceae), were identified with certainty as food plants (Table 5). Mature leaves eaten had a higher mean protein level, but lower levels of mean condensed tannin (CT) and mean neutral detergent fibre (NDF) than uneaten mature leaves (Table 6). Although protein in mature leaves was higher than that of flowers and fruits (Boonratana, 1993; Loh, 1991), N. larvatus rarely fed on mature leaves. This was likely because mature leaves had a higher mean level of CT.
Table 5. Chemical composition of plant parts observed eaten by N. larvatus Species Mallotus muticus Part ML YL FR ML YL YL FR FB YL YL YL YL Sap 1+ 1+ 1+ 1+ %Prot 1.69 2.88 1.44 2.69 3 3.44 1.75 1.1 4.19 1.56 2.63 2.69 CT 0 0.35 0.47 0.12 0 0 0.35 0.12 0.47 0.35 0.35 0.47 %NDF 59.6 55.1 62.7 56.2 65.7 69.7 67 62.9 57.2 70.7 89.6 82.2

Mallotus wrayi Mallotus sp. A Sonneratia alba Dillenia indica Claoxylon sp. A Chionanthus cuspidita Microcos antidesmifolia Microcos sp. A

1+

ML: 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

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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 not contain 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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Ramesh Boonratana Table 6. Chemical composition of plant parts not observed eaten by N. larvatus Species Polyalthia glauca Dillenia indica Claoxylon sp. A Sapium indicum Homalium foetidum Hydnocarpus woodii Spantholobus hirsutus Sonneratia alba Knema latifolia Chionanthus cuspidita Microcos sp. A Part ML ML YL ML ML ML ML ML ML ML ML ML Sap 1+ %Prot 1.56 1.75 1.94 0.88 2.19 1.44 1.94 4.56 2.06 2.25 1.38 1.06 CT 9.15 0.24 0.24 2.71 0 30.34 3.65 0 5.15 3.41 13.29 1.41 %NDF 56.5 64.2 58.0 61.1 63.7 40.6 67 91.5 52.2 76 72.7 64.2

2+ 1+ 2+ 2+ 1+ 1+

ML: 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 of N. 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 were of higher levels of digestible protein. Results suggest that N. 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 of Dillenia indica (Dilleniaceae) was eaten (Table 5). It is of interest that N. 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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Feeding Ecology of Proboscis Monkeys

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 availability according 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 of P. [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 and 80% 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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Ramesh Boonratana

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 the day 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 time spent 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 of N. 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 seeds significantly 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 of N. 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 of N. 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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Feeding Ecology of Proboscis Monkeys Table 7. Comparative proportions, expressed as percentage, of plant parts in some colobines diets. Species N. larvatus N. larvatus N. larvatus ML 0.3 3 ML +YL YL 72.7 49.7 38 FL 8.3 15.5 3 FR 8.3 20.6 35 FR+ SD SD 2.4 11.6 15 Source Boonratana, 1993. Boonratana, 1993. Bennett & Sebastian, 1988. Yeager, 1989. Stanford, 1991. Curtin, 1980. Oates et al., 1980 Hladik, 1977a. Hladik, 1977a. Curtin, 1975 Davies, 1984. Bennett, 1983. Gurmaya, 1986. Mitchell, 1994. Mitchell, 1994. Oates, 1977. McKey et al., 1981. Marsh, 1981. Clutton-Brock, 1977. Struhsaker, 1975. Oates, 1988. Boonratana & Le, 1994.

N. larvatus T. pileatus T. obscurus T. johnii T. vetulus S. entellus S. entellus P. rubicunda P. melalophos P. thomasi P. hosei P. hosei C. guereza C. satanas P.b. rufomitratus P.b. tephrosceles P.b. tephrosceles P. verus R. avunculus

2.7 42 22 27 40 21 31 1 7 1.3 6.5 12 18 11. 5 44 21 11 -

32 -

41.2 11 36 31 20 27 14 36 26 70.8 58.3 62 21 42.4 35 51 59 38

3 7 7 12 12 7 11 17 8 0.2 2.8 2 3 6.2 7 12 -

40.3 24 32 25 28 45 19 20 58 18.8 2.8 14 24.1 1 6 5 47

47 -

20.3 9 2 30 26 21.3 16.7 53 0.9 14 15

(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 of P.

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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 to acidosis, with fatal results (Davies et al., 1988). All the food plant samples of N. 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 to shrink. 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 the system (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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Feeding Ecology of Proboscis Monkeys

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 its energy 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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Ramesh Boonratana

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