Boonratana, R. 1993a. The ecology and behaviour of the proboscis monkey (Nasalis larvatus) in the Lower Kinabatangan, Sabah. Unpublished doctoral dissertation, Mahidol University

THE ECOLOGY AND BEHAVIOUR OF THE

PROBOSCIS MONKEY (Nasalis larvatus) IN THE LOWER KINABATANGAN, SABAH

BY

RAMESH BOONRATANA

A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY (BIOLOGY)

IN THE

FACULTY OF GRADUATE STUDIES OF

MAHIDOL UNIVERSITY 1993

i

This thesis entitled

THE ECOLOGY AND BEHAVIOUR OF THE PROBOSCIS MONKEY (Nasalis larvatus) IN THE

LOWER KINABATANGAN, SABAH

was submitted to the Faculty of Graduate Studies, Mahidol University for the degree of Doctor of

Philosophy (Biology)

on

May 16, 1994. [Academic Year 1993-94]

Ramesh Boonratana Candidate

Warren Y. Brockelman, Ph.D. Preceptor

Monthree Chulasamaya, M.D., Ph.D. Dean Faculty of Graduate Studies Mahidol University

Pornchai Matangkasombut, Ph.D. Dean Faculty of Science Mahidol University

ii

EVALUATION OF THE FINAL EXAMINATION THE DEFENSE OF THESIS

.....................

We, the members of the Supervisory Graduate Committee

for

RAMESH BOONRATANA

unanimously approve the thesis entitled

THE ECOLOGY AND BEHAVIOUR OF THE PROBOSCIS MONKEY (Nasalis larvatus) IN THE LOWER KINABATANGAN, SABAH

We further agree that he has satisfactorily defended his thesis at the examination given by the Supervisory Committee

on

May 16, 1994. [Academic Year 1993-94]

iii

We recommend therefore that

RAMESH BOONRATANA

be awarded the degree of

Doctor of Philosophy in Biology

from

Mahidol University

Warren Y. Brockelman, Ph.D Chairman

Visut Baimai, Ph.D Member

Sompoad Srikosamatara, Ph.D Member

Sangvorn Kitthawee, Ph.D Member

Monthree Chulasamaya, M.D., Ph.D Dean Faculty of Graduate Studies

Vithoon Viyanant, Ph.D Director Graduate Study Program Department of Biology, Faculty of Science

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BIOGRAPHY

NAME Ramesh Boonratana

DATE OF BIRTH 25 September B.E. 2503 (1960)

PLACE OF BIRTH Kota Bharu, Malaysia

INSTITUTIONS ATTENDED Kerala University, 1980-1981:

Pre-degree (Medical)

Panjab University, 1981-1985:

Bachelor of Science (Anthropology)

Panjab University, 1985-1987:

Master of Science (Anthropology)

RESEARCH GRANT Wildlife Conservation Society

Bronx, N.Y. 10460-1099

U.S.A.

POSITION HELD & OFFICE Research Fellow

Wildlife Conservation Society

Bronx, N.Y. 10460-1099

U.S.A.

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FRONTISPIECE

A resting adult male Nasalis larvatus displaying an erect penis in the mangrove forest of the Lower Kinabatangan

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DEDICATION

To the memory of “Papa” a primate, extinct and yet extant...

“...and I think it’s going to be a long, long, time before I touch down, and brings me around to find that I’m not the man they think I am at home...” (Sir Elton John).

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CONTENTS

BIOGRAPHY ........................................................................................................................ IV

FRONTISPIECE..................................................................................................................... V

DEDICATION....................................................................................................................... VI

CONTENTS.......................................................................................................................... VII

ACKNOWLEDGMENTS ................................................................................................... XV

ABSTRACT ....................................................................................................................... XVII

CHAPTER 1: INTRODUCTION ........................................................................................... 1 1.1 INTRODUCTION .................................................................................................................. 1

1.2 THE STUDY ANIMAL ......................................................................................................... 1 1.2.1 General Description .................................................................................................. 1 1.2.2 Specific Description .................................................................................................. 2 1.2.3 Distribution ............................................................................................................... 2 1.2.4 Status in Sabah .......................................................................................................... 3 1.2.5 Current Threats ......................................................................................................... 3

1.3 STUDIES OF COLOBINE BEHAVIOUR AND ECOLOGY .......................................................... 3 1.3.1 Studies on Nasalis larvatus ....................................................................................... 5

1.4 AIMS OF STUDY ................................................................................................................. 6

1.5 SUMMARY ......................................................................................................................... 6 Figure 1.1a Map of Southeast Asia ........................................................................................ 8 Figure 1.1b Map of Sabah ..................................................................................................... 8

CHAPTER 2: METHODS ...................................................................................................... 9

2.1 INTRODUCTION .................................................................................................................. 9

2.2 MONTHLY SCHEDULE ....................................................................................................... 9

2.3 FIELD ASSISTANCE .......................................................................................................... 10

2.4 CLIMATE ......................................................................................................................... 10

2.5 BOTANY .......................................................................................................................... 10

2.6 PHYTOCHEMISTRY .......................................................................................................... 11

2.7 FOOD SAMPLES ............................................................................................................... 12

2.8 HABITUATION ................................................................................................................. 12

2.9 SURVEYS ......................................................................................................................... 12 2.9.1 Aerial Survey .......................................................................................................... 12 2.9.2 River Surveys .......................................................................................................... 12 2.9.3 Transect Surveys ..................................................................................................... 14

2.10 FULL DAY FOLLOWS ..................................................................................................... 14

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2.11 DATA ANALYSIS ........................................................................................................... 15

2.12 SUMMARY ..................................................................................................................... 15 Table 2.1 Weather categories (adapted from Bennett, 1983; Davies, 1984) ...................... 17 Table 2.2 Age/sex categories used in this study (adapted from Bennett, 1986a) ................ 17 Table 2.3 Activity categories used in this study (adapted from Bennett, 1983) ................... 18 Figure 2.2 The Menanggul River was frequently blocked by tree falls and Eichhornia crassipes, which require clearing, usually when the tide was low ...................................... 20 Figure 2.3 Abai study area at high tide ............................................................................... 20

CHAPTER 3: STUDY AREA ............................................................................................... 21 3.1 INTRODUCTION ................................................................................................................ 21

3.1.1 The Kinabatangan River ......................................................................................... 21 3.1.2 Soils and Geology ................................................................................................... 21 3.1.3 Climate .................................................................................................................... 21 3.1.4 Logging History ...................................................................................................... 22 3.1.5 Hunting Pressure ..................................................................................................... 22 3.1.6 Population Size of N. larvatus ................................................................................ 22

3.2 SUKAU STUDY AREA ....................................................................................................... 22 3.2.1 Wild Fauna .............................................................................................................. 22

3.2.1.1 Density and Biomass of N. larvatus ................................................................ 23 3.2.2 Flora ........................................................................................................................ 23

3.2.2.1 Botanical Structure ........................................................................................... 23 3.2.2.2 Botanical Composition .................................................................................... 23 3.2.2.3 Phenology ........................................................................................................ 24

3.3 ABAI STUDY AREA .......................................................................................................... 24 3.3.1 Wild Fauna .............................................................................................................. 24

3.3.1.1 Density and Biomass of N. larvatus ................................................................ 25 3.3.2 Flora ........................................................................................................................ 25

3.3.2.1 Botanical Structure ........................................................................................... 25 3.3.2.2 Botanical Composition .................................................................................... 25 3.3.2.3 Phenology ........................................................................................................ 25

3.4 COMPARISON BETWEEN SUKAU AND ABAI ..................................................................... 26 3.4.1 Botanical Structure ................................................................................................. 26 3.4.2 Botanical Composition ........................................................................................... 26 3.4.3 Phenology ............................................................................................................... 27

3.5 FORESTS IN SABAH .......................................................................................................... 27

3.6 PHYTOCHEMISTRY .......................................................................................................... 27 3.6.1 Organic Nitrogen and Crude Protein ...................................................................... 28 3.6.2 Condensed Tannin .................................................................................................. 28 3.6.3 Neutral Detergent Fibre .......................................................................................... 29 3.6.4 Alkaloids ................................................................................................................. 29 3.6.5 Saponins .................................................................................................................. 29

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3.7 SUMMARY ....................................................................................................................... 29 Table 3.1 Population size of N. larvatus in the Lower Kinabatangan area ........................ 31 Table 3.2 Abundance and basal area of tree families in botanical transects at Sukau ....... 32 Table 3.3 Abundance and basal area of fifteen commonest tree species at Sukau .............. 33 Table 3.4 Abundance and basal area of tree families in botanical transects at Abai ......... 34 Table 3.5 Abundance and basal area of fifteen commonest tree species at Abai ................ 35 Table 3.6 Ten commonest families by percent trees in botanical plots and transects in Sabah .................................................................................................................................... 36 Table 3.7 Ten commonest families by percent basal area in botanical plots and transects in Sabah .................................................................................................................................... 37 Table 3.8 Summary of phytochemical analyses of plant parts at Lower Kinabatangan ..... 38 Table 3.9 Comparison of mean levels of nitrogen, protein, condensed tannin and neutral detergent fibre in mature and young leaves of the same species (n=32) ............................. 39 Figure 3.1 Mean monthly maximum and minimum temperatures for 1990 and 1991 ........ 39 Figure 3.2 Monthly rainfall for 1990 and 1991 ................................................................... 40 Figure 3.3 Klimagraph for 1990 and 1991 .......................................................................... 40 Figure 3.4 Frequency distribution of girths at breast height of transect trees at Sukau (n=1378) .............................................................................................................................. 41 Figure 3.5 Number of tree species against the number of trees sampled in the transects at Sukau (n=1,378) .................................................................................................................. 41 Figure 3.6 Phenological patterns at Sukau (n=500) ........................................................... 42 Figure 3.7 Frequency distribution of girths at breast height of transect trees at Abai (n=300) ................................................................................................................................ 42 Figure 3.8 Number of tree species against the number of trees sampled in the transects at Abai (n=300) ........................................................................................................................ 43 Figure 3.9 Phenological patterns at Abai (n=300) ............................................................. 43 Figure 3.10 Location of botanical plots and transects in Sabah ......................................... 44 Figure 3.11a Mean levels of crude protein in plant parts analysed .................................... 44 Figure 3.11b Mean levels of condensed tannins in plant parts analysed ............................ 45 Figure 3.11c Mean levels of neutral detergent fibre in plant parts analysed ...................... 45

CHAPTER 4: SOCIAL ORGANISATION AND BEHAVIOUR ..................................... 46 4.1 INTRODUCTION ................................................................................................................ 46

4.2 SUKAU STUDY AREA ....................................................................................................... 46 4.2.1 Social Organisation ................................................................................................. 46

4.2.1.1 Size and Composition of N. larvatus Groups .................................................. 46 4.2.1.2 Changes in Composition of SU1, the Focal Group .......................................... 47 4.2.1.3 Group Spread ................................................................................................... 47 4.2.1.4 Intra-group Associations .................................................................................. 47 4.2.1.5 Intra-group Spacing ......................................................................................... 48 4.2.1.6 Inter-group Associations .................................................................................. 48

4.2.2 Social Behaviour ..................................................................................................... 49 4.2.2.1 Agonistic Behaviour ........................................................................................ 49 4.2.2.2 Grooming ......................................................................................................... 50 4.2.2.3 Sexual Behaviour ............................................................................................. 50 4.2.2.4 Births ................................................................................................................ 51 4.2.2.5 Allomothering .................................................................................................. 51 4.2.2.6 Play .................................................................................................................. 51 4.2.2.7 Vigilance .......................................................................................................... 51

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4.3 ABAI STUDY AREA .......................................................................................................... 52 4.3.1 Social Organisation ................................................................................................. 52

4.3.1.1 Size and Composition of N. larvatus Groups .................................................. 52 4.3.1.2 Group Spread ................................................................................................... 53 4.3.1.3 Intra-group Associations .................................................................................. 53 4.3.1.4 Intra-group Spacing ......................................................................................... 54 4.3.1.5 Inter-group Associations .................................................................................. 54

4.3.2 Social Behaviour ..................................................................................................... 54 4.3.2.1 Agonistic Behaviour ........................................................................................ 54 4.3.2.2 Grooming ......................................................................................................... 55 4.3.2.3 Sexual Behaviour ............................................................................................. 55 4.3.2.4 Births ................................................................................................................ 55 4.3.2.5 Allomothering .................................................................................................. 55 4.3.2.6 Play .................................................................................................................. 55 4.3.2.7 Vigilance .......................................................................................................... 55

4.4 Comparison between Sites ......................................................................................... 56

4.5 DISCUSSION..................................................................................................................... 56 4.5.1 Social Organisation ................................................................................................. 56 4.5.2 Dispersal ................................................................................................................. 57 4.5.3 Social Behaviour ..................................................................................................... 59 4.5.4 Vigilance ................................................................................................................. 61

4.6 SUMMARY ....................................................................................................................... 61 Table 4.1 Age/sex composition of identified groups at Sukau ............................................. 63 Table 4.2 Demographic changes within SU1 ...................................................................... 64 Table 4.3 Percent time members of SU1 belonging to different age/sex categories were nearest to subject at Sukau study area (n=4966, weighted data). ....................................... 64 Table 4.4 Daily number of SU1’s inter-group associations of ≤50m and ≤100m compared with the predicted number of such associations if groups were ranging randomly with respect to each other (n=93) ................................................................................................ 65 Table 4.5 Percent agonistic interactions within SU1, between SU1 and other N. larvatus groups, and between SU1 and other species (n=34, weighted scans) ................................. 65 Table 4.6 Percent allogrooming occasions within members of SU1 (n=115, weighted scans) ................................................................................................................................... 66 Table 4.7 Summary of copulatory bouts of N. larvatus at Sukau ........................................ 67 Table 4.8 Percent play occasions within members of SU1 (n=180, weighted scans) ......... 68 Table 4.9 Percent time members of harems belonging to different age/sex categories were nearest to subject at Abai study area (n=1023, weighted data). ......................................... 68 Table 4.10 Percent allogrooming occasions within members of harems at Abai (n=16, weighted scans) .................................................................................................................... 69 Table 4.11 Percent play occasions within members of harems at Abai (n=45, weighted scans) ................................................................................................................................... 69 Table 4.12 Summary of N. larvatus social organisation at different sites ........................... 70 Figure 4.1a Percent time nearest neighbour was within cumulative distance from subject at Sukau (n=4966, weighted data) ....................................................................................... 71 Figure 4.1b Percent time nearest neighbour was within cumulative distance from subject at Sukau (n=4966, weighted data) ....................................................................................... 71

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Figure 4.2a Percent time different number of individuals were within 2.5m of subject at Sukau (n=4966, weighted data) ........................................................................................... 72 Figure 4.2b Percent time different number of individuals were within 2.5m of subject at Sukau (n=4966, weighted data) ........................................................................................... 72 Figure 4.3a Percent time different number of individuals were within 5m of subject at Sukau (n=4966, weighted data) ........................................................................................... 73 Figure 4.3b Percent time different number of individuals were within 5m of subject at Sukau (n=4966, weighted data) ........................................................................................... 73 Figure 4.4 Percent nights when other N. larvatus group/groups were close to SU1 at Sukau (n=96) .................................................................................................................................. 74 Figure 4.5 Percent nights when 0, 1, 2, 3 and 4 groups were within 100m of SU1 at Sukau (n=96) .................................................................................................................................. 74 Figure 4.6 Activity budgets of SU1 at Sukau (n=4966, weighted data) .............................. 75 Figure 4.7 An adult female grooming a juvenile-1 .............................................................. 75 Figure 4.8 An adult female watching the observer .............................................................. 76 Figure 4.9 Number of Infant-1s per adult female observed each month at Sukau .............. 76 Figure 4.10 Percent time different age/sex classes spent at vigilance (n=1257, weighted data) ..................................................................................................................................... 77 Figure 4.11 An adult male prior to release (note tattoo on right cheek) ............................. 77 Figure 4.12 A juvenile with an open-mouthed threat towards the observer ....................... 78 Figure 4.13a Percent time nearest neighbour was at cumulative distance from subject at Abai (n=1023, weighted data) ............................................................................................. 78 Figure 4.13b Percent time nearest neighbour was at cumulative distance from subject at Abai (n=1023, weighted data) ............................................................................................. 79 Figure 4.14a Percent time different number of individuals was within 2.5m of subject at Abai (n=1023, weighted data) ............................................................................................. 79 Figure 4.14b Percent time different number of individuals was within 2.5m of subject at Abai (n=1023, weighted data) ............................................................................................. 80 Figure 4.15a Percent time different number of individuals was within 5m of subject at Abai (n=1023, weighted data) ...................................................................................................... 80 Figure 4.15b Percent time different number of individuals was within 5m of subject at Abai (n=1023, weighted data) ...................................................................................................... 81 Figure 4.16 Percent of nights when another N. larvatus group was close to a harem at Abai (n=205) ........................................................................................................................ 81 Figure 4.17 Percent of nights when 0, 1, and 2 groups were within 100m of a harem at Abai (n=205) ........................................................................................................................ 82 Figure 4.18 Activity budgets of harem groups at Abai (n=1023, weighted data) ............... 82 Figure 4.19. Number of infant-1s per adult female observed each month at Abai .............. 83

CHAPTER 5: FEEDING ECOLOGY ................................................................................. 84

5.1 INTRODUCTION ................................................................................................................ 84

5.2 SUKAU STUDY AREA ....................................................................................................... 85 5.2.1 Food Items .............................................................................................................. 85 5.2.2 Monthly Variation ................................................................................................... 85 5.2.3 Diurnal Variation .................................................................................................... 86 5.2.4 Age-Sex Variation .................................................................................................. 86

5.3 ABAI STUDY AREA .......................................................................................................... 87 5.3.1 Food Items .............................................................................................................. 87

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5.3.2 Monthly Variation ................................................................................................... 88 5.3.3 Age/Sex Variation ................................................................................................... 88

5.4 DRINKING BEHAVIOUR.................................................................................................... 88

5.5 FOOD SELECTION AND PHYTOCHEMISTRY ...................................................................... 89 5.5.1 Leaf Selection ......................................................................................................... 89 5.5.2 Flower Selection ..................................................................................................... 90 5.5.3 Fruit Selection ......................................................................................................... 90

5.6 DISCUSSION..................................................................................................................... 90

5.7 SUMMARY ....................................................................................................................... 92 Table 5.1 List of food plants and plant parts eaten by N. larvatus at Sukau ....................... 94 Table 5.2 Percent plant parts of food plants in diet of N. larvatus at Sukau, recorded during scan observations (n=613, unweighted scans) ........................................................ 95 Table 5.3 List of food plants and plant parts eaten by N. larvatus at Abai ......................... 95 Table 5.4 Percent plant parts of food plants in diet of N. larvatus at Abai, recorded during scan observations (n=184, unweighted scans) .................................................................... 96 Table 5.5 Chemical composition of plant parts observed eaten with certainty by N. larvatus (see tables 5.1 & 5.3) ........................................................................................................... 96 Table 5.6 Chemical composition of plant parts not observed eaten by N. larvatus ............ 97 Table 5.7 Comparative proportions of plant parts in some colobines’ diets (expressed as percentages) ......................................................................................................................... 98 Figure 5.1 Percentage of different items in harem groups' diet at Sukau (n=594, unweighted data) .................................................................................................................. 99 Figure 5.2 Percentage of different items in non-harem groups' diet at Sukau (n=72, unweighted data) .................................................................................................................. 99 Figure 5.3 Monthly variation in plant parts eaten by N. larvatus groups at Sukau (n=540, unweighted data) ................................................................................................................ 100 Figure 5.4a Monthly variation in young leaves eaten (n=428, unweighted data), to that in the forest (n=500, phenology data), at Sukau .................................................................... 100 Figure 5.4b Monthly variation in flowers eaten (n=49, unweighted data), to that in the forest (n=500, phenology data), at Sukau ......................................................................... 101 Figure 5.4c Monthly variation in fruits eaten (n=63, unweighted data), to that in the forest (n=500, phenology data), at Sukau .................................................................................... 101 Figure 5.5 Diurnal variation in plant parts eaten by SU1 at Sukau (n=489, unweighted data) ................................................................................................................................... 102 Figure 5.6 Percentage of different items in harem groups' diet by age/sex class at Sukau (n=534, unweighted data) .................................................................................................. 103 Figure 5.7 Monthly variation in time spent feeding by different age/sex class of SU1 at Sukau (n=534, weighted data) ........................................................................................... 104 Figure 5.8 Diurnal variation in time spent feeding by different age/sex class of SU1 at Sukau (n=534, weighted data) ........................................................................................... 104 Figure 5.9 Percentage of different items in harem groups' diet at Abai (n=155, unweighted data) ................................................................................................................................... 105 Figure 5.10 Percentage of different items in all-male groups' diet at Abai (n=33, unweighted data) ................................................................................................................ 105 Figure 5.11 A juvenile-2 male feeding on the inflorescence of Nypa fruticans (Arecaceae) at Abai ................................................................................................................................ 106 Figure 5.12 An adult male drinking water from the Kinabatangan River ......................... 106

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Figure 5.13 Monthly variation in plant parts eaten by N. larvatus groups at Abai (n=155, unweighted data). ............................................................................................................... 107 Figure 5.14a Monthly variation in young leaves eaten (n=101, unweighted data), to that in the forest (n=300, phenology data), at Abai ...................................................................... 107 Figure 5.14b Monthly variation in flowers eaten (n=24, unweighted data), to that in the forest (n=300, phenology data), at Abai ............................................................................ 108 Figure 5.14c Monthly variation in fruits eaten (n=59, unweighted data), to that in the forest (n=300, phenology data), at Abai ............................................................................ 108 Figure 5.15 Percentage of different items in harem groups' diet by age/sex class at Abai (n=154, unweighted data) .................................................................................................. 109 Figure 5.16 Monthly variation in time spent feeding by different age/sex class of harem groups at Abai (n=155, weighted data) ............................................................................. 110 Figure 5.17 Condensed tannin (CT) + neutral detergent fibre (NDF) against protein content of plant samples eaten and not eaten .................................................................... 110

CHAPTER 6: RANGING BEHAVIOUR .......................................................................... 111 6.1 INTRODUCTION .............................................................................................................. 111

6.2 SUKAU STUDY AREA ..................................................................................................... 111 6.2.1 Home Range ......................................................................................................... 112 6.2.2 Day Range Lengths ............................................................................................... 112

6.2.2.1 Rainfall ........................................................................................................... 112 6.2.2.2 Phenology ...................................................................................................... 113 6.2.2.3 Food Resources .............................................................................................. 113

6.2.3 Quadrat Use .......................................................................................................... 113 6.2.3.1 Rainfall ........................................................................................................... 114 6.2.3.2 Phenology ...................................................................................................... 114 6.2.3.3 Food Resources .............................................................................................. 114

6.2.4 Height Use ............................................................................................................ 114 6.2.5 Swimming ............................................................................................................. 115

6.3 ABAI STUDY AREA ........................................................................................................ 115 6.3.1 Home Range ......................................................................................................... 115 6.3.2 Height Use ............................................................................................................ 115 6.3.3 Swimming ............................................................................................................. 116

6.4 COMPARISON BETWEEN SITES ....................................................................................... 116

6.5 DISCUSSION................................................................................................................... 116

6.6 SUMMARY ..................................................................................................................... 119 Table 6.1 Summary of home range size, group size, and population density of N. larvatus at different sites .................................................................................................................. 120 Figure 6.1 All day ranges of SU1 at Sukau, Jan. – Dec. 1991 (n=93) .............................. 120 Figure 6.2 Cumulative number of 1ha quadrats entered by SU1 at Sukau (n=93) ........... 121 Figure 6.3 Frequency distribution of day range lengths of SU1 at Sukau (n=53) ............ 121 Figure 6.4 Mean monthly day range lengths of SU1 at Sukau (n=53) .............................. 122 Figure 6.5 Frequency distribution of 1ha quadrats entered by SU1 each day (n=53) ..... 122 Figure 6.6 Mean monthly number of 1ha quadrats entered by SU1 at Sukau (n=53) ...... 123 Figure 6.7 Monthly total number of 1ha quadrats entered by SU1 at Sukau (n=93) ........ 123

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Figure 6.8 Differential quadrat use by SU1 at Sukau from Jan. – Dec. 1991 (n=4966, weighted data) .................................................................................................................... 124 Figure 6.9 Height of SU1 at Sukau when engaged in major activities .............................. 125 Figure 6.10 Mean height of SU1 at different time of day at Sukau (n=4966, weighted data) ............................................................................................................................................ 125 Figure 6.11 Use of riverside habitat by N. larvatus groups at Abai (Feb. 1990 – Dec. 1991) ............................................................................................................................................ 126 Figure 6.12 Height of N. larvatus groups at Abai when engaged in major activities ....... 127

CHAPTER 7: CONCLUDING DISCUSSION ................................................................. 128 7.1 INTRODUCTION .............................................................................................................. 128

7.2 IMPORTANCE OF THE LOWER KINABATANGAN AREA ................................................... 128

7.3 CONSERVATION RECOMMENDATIONS ........................................................................... 128

7.4 FUTURE RESEARCH ....................................................................................................... 129

7.5 CONCLUSIONS ............................................................................................................... 130

7.6 SUMMARY ..................................................................................................................... 130

LITERATURE CITED ....................................................................................................... 131

APPENDIX I: LIST OF WILD FAUNA RECORDED AT SUKAU .............................. 145

APPENDIX II: LIST OF WILD FAUNA RECORDED AT ABAI ................................ 153

APPENDIX III: TREE SPECIES AND THEIR PROPORTIONS IN THE BOTANICAL TRANSECTS AT SUKAU (N=1378). ....................................................... 156

APPENDIX IV: TREE SPECIES AND THEIR PROPORTIONS IN THE BOTANICAL TRANSECTS AT ABAI (N=300). ............................................................. 159

APPENDIX V: RESULTS OF PHYTOCHEMICAL ANALYSES OF PLANT ITEMS COLLECTED AT SUKAU AND ABAI (ADAPTED FROM LOH, 1991). ................... 161

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ACKNOWLEDGMENTS

The initiation of this study resulted from a predawn conversation (and beers) with Dr. George Schaller on the first day of 1988. Dr. Schaller’s suggestion was set in motion by Dr. Alan R. Rabinowitz, mentor and friend. Dr. Rabinowitz’s faith in me, when others failed, will never be forgotten. My deepest appreciation goes to Dr. Elizabeth L. Bennett, “the white dayak.” This thesis would not have been possible without her supervision from the time this study was formulated until its bound form. Credit also goes to members of my supervisory committee at Mahidol University, Drs. Warren Y. Brockelman, Sompoad Srikosamatara, Visut Baimai and Sangvorn Kitthawee for their feedback and comments. I am particularly indebted to Dr. Brockelman who helped me overcame many obstacles during my early years at Mahidol University, and in Thailand.

I wish to acknowledge Datuk Wilfred Lingham, the Permanent Secretary of the Sabah Ministry of Tourism and Environmental Development, and Mr. Mahedi Andau, the Director of the Sabah Wildlife Department, for permission to conduct this study. Their enthusiastic support was a constant source of encouragement throughout the study. I am grateful to Mr. Laurentius Ambu, the Assistant Director, Ms. Jumrafiah Abd. Shukor, Wildlife Officer, Mr. Sundang Sarim, Senior Wildlife Ranger, of the Sabah Wildlife Department, for seeing me through many difficulties, also for their friendship.

Mr. Jibius Dausip, Wildlife Ranger, accompanied me on my reconnaissance trip to the Lower Kinabatangan. His friendly relations with the villagers of Abai and Sukau were an asset. Mr. Rashid Saburi, Wildlife Officer, and Mr. David Antonius, Wildlife Ranger, helped set up the Abai study area. Their physical efforts greatly matched their appetites. At Sukau, Wildlife Officers Ms. Jumrafiah Abd. Shukor and Mr. Gunik Gunsalam helped set up the study. Mr. Paimim Diun, Senior Wildlife Ranger, an excellent bird-watcher, help compiled the bird list for Sukau study area. Mr. Paul Langgi, Senior Wildlife Ranger, did an excellent job at identifying the transect trees, and is noted for his knowledge of medicinal plants. I also wish to acknowledge the various personnel from the Sabah Wildlife Department who joined the project as trainees. In particular, two very dedicated wildlife rangers, Mr. Richard “Bludder” Jaikim and Mr. Leo “Jaws” Siawa.

Mr. Dionysius S. Sharma, Scientific Officer with World Wide Fund for Nature, Malaysia provided excellent field assistance. His devotion to the project, despite having to endure severe malarial infections twice, will always be appreciated. His musical talent was always a welcome change to the buzzing of mosquitoes. Phytochemical analyses were carried out at Malaysian National University (Sabah), by Dr. Siraj Omar and Ms. Loh Soo Nai. Mr. Lee Ying Fah, Research Officer of the Sabah Forestry Department, allowed the use of facilities at the department’s herbarium. Plant samples were identified by Mr. Leopold Madani, a botanist with the Research Division of Sabah Forestry Department. The Royal Malaysian Air Force, in particular the aircrew, Lt. Khalaiselvan a/l Letchumanan, Lt. Syed Islam b. Shahajam, and Sgt. Sundarajan a/l Rajagopal are acknowledged for an aerial survey carried out in February 1990.

I gained useful advice through discussions with Drs. Junaidi Payne, Clive W. Marsh, Alan R. Rabinowitz, Thomas T. Struhsaker, Rob Stuebing and Volker Sommer. In New York, I am ever indebted to Dr. Mary C. Pearl and Ms. Martha Schwartz for facilitating all my requests. At Cambridge University, Dr. David J. Chivers, Ms. Ruth K. Laidlaw and Mr. Mohammad F. Ahsan, from the Sub-department of Veterinary Anatomy, and Dr. Kaushik S. Bose from the Department of Biological Anthropology extended me the use of facilities at

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their respective departments, and at the University Library. Data analysis and thesis write-up were carried out at the Center for Conservation Biology, Mahidol University.

My colleagues, Ms. Nantiya Aggimarangsee and Mr. Zainuddin Dahaban, and friends, Mr. Max Lawrence, Ms. Leslie Prudente, Mr. Cede Prudente, Dr. Rika Akamatsu, Ms. Sylvia Alsisto and Ms. Christine Chia also contributed to this study. Sunny, Lee and Chong of the “Mile 4 gang” helped me through my stressful and frustrating moments. At Sukau, I am indebted to Mr. Suhaini Md. Kiju, Abang Karim and Pa’ Amirbak, and at Abai, Cikgu Tahir b. Mastar and the late Encik Mastar b. Separi, for making my stay at both the villages pleasant and memorable.

My mother, Mdm. Krishnawanti Moluthra, and my brothers, ASPs. Chowalit and Sukree Boonratana provided constant encouragement and moral support. Struggling through each field day, Choon and Stanley inspired me to achieve my goals. Their love was my tower of strength when the going got tough.

This study was funded by the Wildlife Conservation Society, previously known as Wildlife Conservation International, a conservation research division of the New York Zoological Society. Schooling for the first academic year at Mahidol University was funded by the International Primatological Society under its Conservation Scholarship Programme. World Wildlife Fund, U.S., funded the second and third academic years of schooling under its Asian Fellowship Programme. I received additional subsistence from the Association of Southeast Asia Institute of Higher Learning through Mahidol University.

Lastly, many thanks to nenek of “The Last Resort,” and all the guardian spirits of the Lower Kinabatangan for keeping me safe from malaria, crocodiles, pirates, and fair maidens (although not necessarily in that order).

Ramesh Boonratana

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Thesis Title The Ecology and Behaviour of the Proboscis Monkey (Nasalis larvatus) in the Lower Kinabatangan, Sabah

Name Ramesh Boonratana Degree Doctor of Philosophy (Biology) Thesis Supervisory Committee Warren Y. Brockelman, Ph.D.

Visut Baimai, Ph.D. Sompoad Srikosamatara, Ph.D. Sangvorn Kitthawee, Ph.D.

Date of Graduation 16 May B.E. 2537 (1994)

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. The aims of the study were to assess the ecology and behaviour of N. larvatus in relation to the botany and phytochemistry of the habitat flora. This involved two years fieldwork in the mangrove and riverine forests in the Lower Kinabatangan area.

The basic social unit of N. larvatus is a relatively stable harem, comprising a single adult male, several adult females and their offspring. The social structure of N. larvatus in the Lower Kinabatangan is flexible, and comprised relatively stable harem, all-male and predominantly male non-breeding groups. Different groups frequently selected riverside sleeping sites that were close to one another. Some groups associated more than others did, implying a secondary level of social organisation, the band. Intra-group agonistic and social interactions were rare, implying that intra-group competition was low. This, in turn suggested that food was abundant and available.

All colobines, including N. larvatus, possess specialised digestive physiology and sacculated stomachs with anaerobic, cellulolytic bacteria in their fore-stomachs. This adaptation allows them to break down cell wall constituents and defensive chemicals found in plant foods. N. larvatus is a folivore-frugivore, with a strong preference for seeds. They are highly selective feeders, avoiding items with high levels of digestion inhibitors.

Nasalis larvatus groups in the Lower Kinabatangan were wide-ranging, returning to sleep by the Kinabatangan River or its tributaries every evening. N. larvatus are not territorial, and the ranges of different groups completely overlapped each other. The home range size of the focal harem group, SU1, at Sukau was observed to be 221ha. SU1 increased its day range lengths as high quality foods become scarcer, and the group selected particular quadrats on days when its members ate high quality foods. This suggested that food resources were unevenly distributed and highly clumped.

Differences in home range size, group size, and population density of N. larvatus between sites, and the fact that groups were non-territorial, with completely overlapping ranges and low level of intra-group interactions, strongly implied that these variables were influenced by ecological pressures, particularly by the distribution, size and abundance of food resources.

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CHAPTER 1: INTRODUCTION

1.1 INTRODUCTION This study describes the behaviour and ecology of a colobine, Nasalis larvatus (van

Wurmb), and how these are inter-related to determine its survival and reproduction. The survival and reproduction of a species are influenced by the way it behaves within its habitat. Its behaviour, however, is influenced by the ecological constraints imposed by its habitat. Some species make good ecological models, showing the relationship between the animals and their habitat. Diurnal primates, particularly colobines, are ideal because they allow this relationship to be observed closely, as expressed through their behaviour, social organisation and ranging patterns.

In this chapter, I will describe the study animal, N. larvatus in terms of its taxonomy, distribution, present status, and current threats to its survival. Then, I will briefly review some past studies on the ecology and behaviour of colobines, including N. larvatus, emphasising ecological parameters that influence various aspects of colobine social organisation and behaviour. I will not attempt to review all known studies of colobine ecology, but will draw out examples that are most relevant to the current study. Finally, I will describe the specific aims of the study.

1.2 THE STUDY ANIMAL The subfamilies Colobinae and Cercopithecinae belong to the family Cercopithecidae,

the only family of Old World Monkeys. The family Cercopithecidae is distributed throughout Africa and Asia. There are nine genera in the subfamily Colobinae, seven of which are found in Asia: Semnopithecus, Trachypithecus, Presbytis, Nasalis, Simias, Rhinopithecus and Pygathrix. Two, Colobus and Procolobus, are found in Africa (Napier & Napier, 1967; Kavanagh, 1983; Napier, 1985; Oates, 1985; Eudey, 1987).

Nasalis larvatus belongs to the “odd-nosed colobines,” a small group of bizarre and largely unstudied species. Other monkeys that belong to this group are Simias concolor, Rhinopithecus roxellanae, R. bieti, R. brelichi, R. avunculus and Pygathrix nemaeus (Kavanagh, 1983; Eudey, 1987; Bennett, 1991). N. larvatus was first described by van Wurmb in 1784 (Napier & Napier, 1967) and originally called Cercopithecus larvatus (Forbes, 1897; Elliot, 1912; Napier, 1985). N. larvatus has also been called by other scientific names, which include Simia nasicus, Cercopithecus capistratus, Semnopithecus larvatus and Rhynopithecus nasalis (Forbes, 1897; Elliot, 1912).

1.2.1 GENERAL DESCRIPTION The colobines are mainly arboreal, have a long tail and lack cheek pouches. The

species belonging to this subfamily are characterised by having a reduced first digit on the forelimb (Napier, 1985; Napier & Napier, 1967; 1983). Another distinguishing characteristic of all colobines is that they possess a large, sacculated stomach containing a diverse array of micro flora. Bacteria in the colobines’ multi-chambered stomach convert cellulose, the basic component of leaves, into volatile fatty acids. This enables colobines to obtain energy from leaves. Secondly, the bacteria deactivate toxins in the food, enabling colobines to consume poisonous items (Bauchop & Martucci, 1968; Kuhn, 1964; Hladik, 1977a; Parra, 1978; Chivers & Hladik, 1980; McKey et al., 1981).

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A major disadvantage with the colobine digestive system is that it cannot process readily digestible foods such as sugary fruits. The bacteria would ferment them so rapidly that there would be a sudden build-up of gases and acid in the stomach, termed acidosis, which can lead to the monkey’s death (Davies et al., 1983; 1988). Colobines also avoid foods with excessively high level of protein. These foods lead to an over-production of ammonia and histamine in the stomach, which in turn, can lead to blood and liver disorders (Davies et al., 1988).

1.2.2 SPECIFIC DESCRIPTION Nasalis larvatus is a large, sexually dimorphic, arboreal colobine, endemic to the

island of Borneo in South-east Asia (figure 2.1). Adult males of this monotypic species weigh an average of 20 kg and have been recorded close to 24 kg, with a head-body 75cm long and tail adding another 67cm. The adult females weigh an average of 10 kg (maximum 12 kg), with a head-body length of 62cm and a tail adding a further 57cm (Schultz, 1942; Napier & Napier, 1967; Napier, 1985). Adult males have an enlarged, pendulous nose that overhangs the mouth. The function of the nose may be to regulate body temperature, but most likely, it is a product of sexual selection (Kavanagh, 1983; Bennett, 1987; 1988a).

Nasalis larvatus has orange-brown to reddish-brown fur on the head, shoulders, upper arms and thighs. The under parts are paler. The fur is thicker and darker in the males, and they have a white rump patch and tail, instead of the off-white to pale-grey in the females. Newly born N. larvatus have sparse, blackish fur and have dark blue faces with snubby, upturned noses (Napier & Napier, 1967; Bennett, 1987; in press; Bennett & Gombek, 1993).

The front and hind limbs of N. larvatus are not very different to each other in length, a characteristic associated with ground travelling primates. The hind feet of both sexes have partially webbed toes (Napier & Napier, 1967; Napier, 1985). Presumably, this adaptation aids them in swimming across rivers and walking on soft mangrove mud without sinking (Bennett, 1986a; in press; Bennett & Sebastian, 1988; Bennett & Gombek, 1993).

1.2.3 DISTRIBUTION The subfamily Colobinae ranges from the western Ghats to northern Assam,

spreading northeast to China and southeast through Indochina and the Malay Peninsula to the Indonesian islands of Sumatra, Java, and Borneo. Colobines represent a radiation into a wide range of environments, occupying most habitats from tropical swamps to high mountains (Kavanagh, 1983; Bennett, 1991; Stanford, 1991).

The distribution of N. larvatus is limited to Borneo (figure 1.1) and to two islands, Berhala and Sebatik, on the northeast coast (Davis, 1962; Napier & Napier, 1967; Payne et al., 1985). They are largely restricted to mangrove, riverine and peat swamp forests of the coastal lowlands (Kern, 1964; Kawabe & Mano, 1972; Jeffrey 1979; 1982; Payne et al., 1985; Salter & MacKenzie, 1985; Salter et al., 1985; Bennett, 1986a; 1988a; 1991; in press; Bennett & Sebastian, 1988; Bennett & Gombek, 1993). N. larvatus populations are sometimes found much further inland along major rivers such as the Kinabatangan and Segama in Sabah, and the Barito in Kalimantan (Payne et al., 1985). In addition, there are infrequent reports of seemingly nomadic animals that briefly pass through hill forest areas in the Bornean interior (Bennett, 1986a; 1988b; 1991; in press; Bennett & Gombek, 1993).

In western Sabah, the species’ range is patchy and shrinking (Davies & Payne, 1982; Payne et al., 1985), with small populations on the Klias Peninsula (Kawabe and Mano, 1972; Bennett, 1986a; 1991; Scott, 1989), and at the Rampayan River within the Tempasuk Plain (Davies & Payne, 1982; Scott, 1989). In eastern Sabah, N. larvatus is commonly found in the

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extensive swampy coastal plains, especially around Dewhurst Bay and along the Kinabatangan, Segama and Sugut rivers (Davies & Payne, 1982; Payne et al., 1985; Bennett, 1986a; 1991; Scott, 1989).

1.2.4 STATUS IN SABAH N. larvatus is currently listed as “vulnerable” in the IUCN’s red list of threatened

animals (IUCN, 1990). In Sabah, N. larvatus is listed as a totally protected species under the Fauna Conservation Ordinance of 1963 and its amendments. Presently, however, no viable populations are effectively protected within a Totally Protected Area in Sabah (Bennett, 1986a; 1991; Bennett & Gombek, 1993).

The Kulamba Wildlife Reserve was established in 1984 to protect the wetlands in southeastern Sabah, but most of the population is outside the reserve (Bennett, 1986a; 1991). N. larvatus are also found in the Kabili-Sepilok Virgin Jungle Reserve, but again much of the population is found outside the Reserve (Bennett, 1991). Small populations are protected in the Danum Valley and Gunung Lutong Conservation Areas, but it is likely that they range out of these areas (Bennett, 1991).

A Lower Kinabatangan Wildlife Reserve, covering an area of 35,000ha has been proposed to provide protection to wildlife, particularly populations of N. larvatus, Pongo pygmaeus, Dicerorhinus sumatrensis, Elephas maximus, Anhinga melanogaster and Crocodylus porosus. The proposed reserve would also protect freshwater fisheries of economic importance, besides offering nature tourism and other recreational outlets.

1.2.5 CURRENT THREATS Habitat destruction is the major threat to survival of N. larvatus in the lower

Kinabatangan. Many different areas of the lowland rainforest and the mangrove have been logged at least once (section 3.1.4). The lowland rainforest in the flood-free zone of the lower Kinabatangan region is being clear-felled to make way for cocoa and oil palm plantations measuring hundreds to thousands of hectares, and totalling more than 60,000ha (Boonratana, 1993a & b; Boonratana & Sharma, in press). This threatens not only N. larvatus but also other forms of wildlife. Canals up to 3km long and 5m wide have been dug to drain the swampy areas within the plantations into the rivers. Electric fencing is usually placed around the plantations to deter large mammals from damaging the crops. This fencing and drainage undoubtedly disrupt many of the mammals’ ranging patterns, especially species with large ranges, including N. larvatus, Dicerorhinus sumatrensis, Elephas maximus, Bos javanicus, Cervus unicolor, Muntiacus muntjak and Sus barbatus (Boonratana, 1993a & b; Boonratana & Sharma, in press).

Another serious form of habitat destruction in the lower Kinabatangan is small clearings of forest for agriculture and for villages adjacent to rivers where monkey populations occur. Most clearings are made for government-sponsored farming projects, ranging from 0.5 to 4ha. N. larvatus used these areas before clearance (Boonratana, 1993a & b; Boonratana & Sharma, in press).

1.3 STUDIES OF COLOBINE BEHAVIOUR AND ECOLOGY It was not until the 1970s that primate field studies started looking at ecological

parameters to explain social behaviour and organisation, and to study differences between conspecifics living in different habitats. Initial attempts to look into the influence of ecological parameters started with a comparison between the different primate social organisation within broad “ecological grades” (Crook & Gartlan, 1966). As a result of this,

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variables of ecology and behaviour were inter-related to explain the evolution and adaptive significance of primate societies (Struhsaker, 1969; Crook, 1970a; Eisenberg et al., 1972; Wilson, 1975).

The earliest attempts at detailed ecological study of colobines were on Procolobus badius tephrosceles, (Clutton-Brock, 1975; Struhsaker, 1975) and Colobus guereza (Oates, 1977a). Ecological parameters were examined to explain their influences on the social organisation of the two species. It was observed, for example, that P.b. tephrosceles lived in large groups of 40-80 animals, with wide and overlapping home ranges, but the sympatric C. guereza lived in small groups of about 12 animals, and had home ranges about one-sixth the size of P.b. tephrosceles.

Detailed ecological comparisons of the two sympatric colobines (Clutton-Brock, 1974; Struhsaker & Oates, 1975), determined that the differences in group size and ranging patterns were mainly due to the dietary differences between species, hence the distribution of their food sources. The diet of P.b. tephrosceles, which they obtain from widely scattered food sources, is quite diverse. To maximise their food intake, P.b. tephrosceles travel in large groups, over large areas, and visit large food sources. Likewise, in a later study, Isbell (1983) found that food availability and dietetic requirements strongly influenced ranging patterns of P.b. tephrosceles. Conversely, the diet of C. guereza was not as diverse; therefore, individuals could fulfil their food requirements from a small exclusive area by maintaining a small group size. The different patterns of territoriality among African colobines were suggested to be due to variations in the overall abundance of food, seasonality and diversity of the forests (Struhsaker & Oates, 1975; Struhsaker & Leland; 1979).

Similarly, ecological studies on Semnopithecus entellus and Trachypithecus vetulus drew on the relationship between ecology and social organisation (Hladik & Hladik, 1972; Hladik, 1977a), and showed relationships between diet and group size parallel to those described for the African colobines. S. entellus have wide and overlapping ranges, with a diverse diet. By contrast, T. vetulus live in small groups, have small ranges and its diet comprises leaves from the commonest species. The distribution of food sources was again suggested to influence feeding and ranging patterns (Hladik, 1977a). Comparison between sympatric Presbytis melalophos and Trachypithecus obscurus at Kuala Lompat, showed that P. melalophos ate seeds more, whereas T. obscurus had a less diverse, more folivorous diet, albeit with similar group and range sizes (Curtin, 1976; 1980; MacKinnon & MacKinnon, 1980). The similar distribution of food sources at the site was suggested to account for the similarity in group and range sizes.

In a later study at Kuala Lompat, Bennett (1983; 1986b) found that P. melalophos travelled far and more widely, with different groups coming together to feed in large, rare food sources, when they ate a specialised diet of flowers or fruits plus seeds. When favoured foods were scarce, P. melalophos fed on a greater variety of foods, the groups travelled less far and neighbouring groups met less often. Home range size and overlap varied considerably between sites and was related to the size and number of food sources. The study revealed that the distribution and size of food sources and length of time for which any one food source produces food items were important in influencing the occurrence of territoriality. The pressure for P. melalophos to interact socially was shown to result from low level of competition for any one food item, due to the availability and abundance of food at Kuala Lompat throughout the year (Bennett, 1986b).

Bennett’s (1983, 1986b) study and Davies’s (1984) on Presbytis rubicunda at Sepilok, in northern Borneo examined the distribution and abundance of food plants, and phytochemistry of the habitat flora, and related these to colobine behaviour. The biomass of

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South-east Asian colobines was shown to be influenced by the botanical composition of the forest. Colobines’ biomass was positively correlated with the abundance of legumes, but negatively correlated with that of dipterocarps. The biomass of colobines at five different evergreen forest sites was positively correlated with the digestibility of mature leaves in the forest (Bennett, 1983; Davies, 1984; Davies et al., 1988; Waterman et al., 1988). This was then shown to influence group size, inter-group relations, home range size and ranging patterns. The small group size of P. rubicunda at Sepilok was due to food sources being small and clumped (Davies, 1984), therefore minimising feeding competition (Alexander, 1974; Wilson, 1975; Wrangham, 1975; van Schaik & van Hooff, 1983).

A more recent study on Trachypithecus pileatus (Stanford, 1991), showed that they had overlapping ranges and were non-territorial. Day range lengths of T. pileatus increased during periods of intensive fruit-eating, but ranged less widely when feeding on mature leaves. This again, was strongly indicative of the influence of the distribution of food resources on ranging patterns of T. pileatus.

Another important approach to colobine ecology has been the examination of feeding behaviour in relation to plant chemistry. The earliest studies described the nutrients present in different plant parts eaten by S. entellus and T. vetulus (Hladik & Hladik, 1972). The study strongly suggested that, in addition to nutrient needs, food choice was influenced by the presence of digestion inhibitors. This implied that food was selected so as to maximise nutrient intake and at the same time, minimise the intake of digestion inhibitors (Freeland & Janzen, 1974; Pyke et al., 1977; Davies et al., 1988; Waterman et al 1988). Oates et al. (1980) studied food selection in Trachypithecus johnii as function of forest ecology, and found that there was a preference for young leaves. This supported the observation that food selection in colobines was determined by leaf digestibility, which is largely determined by the fibre, tannin and protein content (Davies et al., 1988). This and other studies of colobine ecology in both Asia (Bennett, 1983; Davies, 1984; Davies et al, 1988; Waterman et al., 1988) and Africa (McKey, 1978; McKey et al., 1981; Oates 1988) have confirmed that food selection is influenced by the ratio of protein to digestion inhibitors.

1.3.1 STUDIES ON NASALIS LARVATUS The behaviour and ecology of N. larvatus in the wild were until recently relatively

unknown. Earlier studies gave conflicting reports on their social organisation. Studies carried out in Brunei Bay (Kern, 1964; Macdonald, 1982) and in East Kalimantan (Jeffrey, 1979) reported N. larvatus living in loosely organised multi-male troops that mixed and separated frequently. Another study in Sabah (Kawabe & Mano, 1972), however, reported that these multi-male groups were highly integrated and cohesive.

Recent long-term studies conducted at Samunsam Wildlife Sanctuary in Sarawak (Bennett, 1986a; 1991; in press; Bennett et al., 1987; Bennett & Sebastian, 1988; Rajanathan & Bennett, 1990), and at Tanjung Puting National Park in Kalimantan (Yeager, 1989; 1990a & b; 1991a; 1992) show that N. larvatus has a flexible social structure. The basic unit is a harem comprising one adult male, several adult females, and their offspring. Furthermore, there seem to be two levels of social organisation, the harem and the band (Yeager, 1991a).

Harems at Samunsam range from five to 19 animals and average nine individuals (Bennett, 1986a; in press; Bennett & Sebastian, 1988; Rajanathan & Bennett, 1990), whereas at Tanjung Puting, they average 12.6 individuals and range from three to 26 animals (Yeager, 1989; 1990a; 1991a). Males leave their natal group as young as one to two years old to join loosely bonded all-male groups. Different groups frequently come together, especially in the evening along the rivers. Adult females also move between harems (Bennett, 1986a; 1991; in

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press; Bennett & Sebastian, 1988; Rajanathan & Bennett, 1990). Harems range widely, occupying an area of 9km² in mixed riverine forest at Samunsam (Bennett, 1986a; in press; Bennett & Sebastian, 1988; Rajanathan & Bennett, 1990). In peat swamp forest at Tanjung Puting, however, their range is much smaller covering an area of 130.3ha (Yeager, 1989; 1992). This difference can partly be attributed to the difference in habitat types, and partly in the different methods of estimation (section 6.5). The ranges of different groups in both study areas completely overlap one another, and although wide-ranging, they return to the river every evening (Bennett, 1986a; 1991; in press; Bennett & Sebastian, 1988; Yeager, 1989; 1991a).

These two studies showed that the differences in monthly ranging patterns are influenced by the differences in the monthly distribution and availability of foods (Bennett, 1986a; Yeager, 1989). Furthermore, these studies found N. larvatus to be selective feeders, mainly limiting their diet to seeds, young leaves and non-succulent fruits of selected plant species (Bennett, 1986a; Bennett & Sebastian, 1988; Yeager, 1989).

1.4 AIMS OF STUDY In spite of recent studies (section 1.4), there are still many gaps in our knowledge

about the behaviour and ecology of N. larvatus. This study has attempted to fill some of these gaps. Furthermore, this is the first attempt to study the ecology and behaviour of N. larvatus in mangrove forest. The aims of the study were as follows:

1. To describe the botany of the mangrove and riverine forests in the Lower Kinabatangan, and compare with other sites in Sabah;

2. To monitor and compare the production of plant parts of trees in the mangrove and riverine forests, and to assess changes in food availability throughout the year;

3. To describe the phytochemical composition of the vegetation in the study areas, comparing plant parts eaten and not eaten;

4. To study the feeding behaviour of N. larvatus in relation to the botany, phenology and phytochemistry of the habitat;

5. To study the ranging behaviour and social organisation of N. larvatus in relation to the pattern of watercourses throughout the area, and the different habitat types at different times of year;

6. To compare the ecology and behaviour of N. larvatus in the mangrove and riverine forests.

1.5 SUMMARY 1. Past ecological studies of colobines have shown that group size and ranging patterns were

related to the distribution, size and availability of food resources.

2. N. larvatus is a large, sexually dimorphic, monotypic species, endemic to the island of Borneo, where it is largely restricted to riverine, peat swamp and mangrove forests of the coastal lowlands.

3. Although N. larvatus is a totally protected species in Sabah, no viable populations are effectively protected within a Totally Protected Area. Threats to N. larvatus in the Lower Kinabatangan area include hunting, habitat destruction through logging, farming and oil palm plantation.

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4. The behaviour and ecology of N. larvatus were relatively unknown until recently. Earlier reports on their social organisation were conflicting. Recent long-term studies showed that the basic social unit of N. larvatus is a harem.

5. The aim of the study was to assess the ecology and behaviour of N. larvatus in relation to the botany and phytochemistry of the habitat flora. A comparison of the ecology and behaviour of N. larvatus in the mangrove and riverine forests was also made. Ranging behaviour and social organisation is also studied in relation to the patterns of watercourses in the area.

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Figure 1.1a Map of Southeast Asia

Figure 1.1b Map of Sabah

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CHAPTER 2: METHODS

2.1 INTRODUCTION Fieldwork was conducted from January 1990 to December 1991 inclusive. Two sites

in the Lower Kinabatangan region, Sukau and Abai, were selected for the study (figure 2.1). The sites, located along the Kinabatangan River, have different forest types (sections 3.2.2 and 3.3.2). The sites were selected for the following reasons:

1. Observations made during a reconnaissance trip in October 1989, showed that the Lower Kinabatangan Region might have the largest population of N. larvatus in Sabah.

2. The region has both mangrove and riverine forests among others. The distribution of N. larvatus is restricted mainly to peat swamp, mangrove and riverine forests of the coastal lowlands (section 1.2.3).

3. This region has many ox-bow lakes, tributaries and interconnecting creeks that would be ideal to observe ranging behaviour of N. larvatus.

4. The riverine forest at Sukau and the mangrove forest at Abai were accessible from each other. Furthermore, both Sukau and Abai were accessible from Sandakan by river and road in the former, and by river in the latter. Sandakan was the nearest major town where supplies could be purchased.

5. Hunting pressure on N. larvatus in the region was apparently negligible. This would be an added advantage at habituation attempts.

6. Any wildlife research conducted in the Lower Kinabatangan region would provide essential information to the management of the proposed Lower Kinabatangan Wildlife Reserve (section 1.2.4).

2.2 MONTHLY SCHEDULE The first month was spent becoming familiar with the region. This was done using a

boat along the Kinabatangan River and its tributaries, and by walking extensively along old logging roads and animal trails. In February 1990, location markers were placed every 25m along the Menanggul River at Sukau and the Merah River at Abai. Botanical transects at Sukau and Abai sites were also prepared during this period. Data collection using boat surveys began from February 1990, and for phenology, from March 1990. Phenology was studied monthly until December 1991. At least ten days a month were spent at each study site. A harem group (see Kavanagh, 1983 for definition), SU1, at Sukau was identified as the focal group (section 4.2.1.2). Then, a 100m grid network of trails to encompass the group’s home range at Sukau was prepared (section 2.10). The monthly schedule for the second year is summarised below:

Principal Investigator: Day Activity 1-5 Boat surveys and phenology at Menanggul River 5-10 Boat surveys and phenology at Merah River 11-15 Full day observations at Sukau study area 16-20 Full day observations at Abai study area 21-22 Maintenance of trails and waterways

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Research Assistant: Day Activity 1-3 Boat surveys at Sapasidom River 3-5 Boat surveys at Tenegang Besar 5-7 Boat surveys at Kelandaun and Kelananap Lakes 7-10 Boat surveys at Menanggul River 11-15 Transect surveys at Sukau study area 16-20 Full day observations at Sukau study area 21-22 Maintenance of trails and waterways

2.3 FIELD ASSISTANCE From January until November 1991, Mr. Dionysius S. Sharma, a trainee Scientific

Officer from World Wide Fund for Nature, Malaysia, provided field assistance. During the study, Sharma assisted in data collection of full day follows, and he also carried out river surveys and transect surveys. For the first three months, Sharma was trained in data collection techniques. From April onwards, his data were used in this thesis, i.e. after his data and mine were comparable. To ensure this, scan observations and river surveys were conducted by Sharma and me simultaneously at the same place and on the same set of animals. This was continued for two months until the same results were obtained, and was done before Sharma’s actual data collection. Throughout the study, the staff of the Sabah Wildlife Department provided logistical assistance, while simultaneously being trained in field techniques and data collection methods.

2.4 CLIMATE Rainfall and temperature data were recorded by the Meteorological Service of

Malaysia at Sandakan Airport, approximately 50km from Sukau and 40km from Abai. Rainfall and temperature data were not collected in the field due to the short duration that I spent at each study site. The airport adjoins a mangrove forest and is part of the coastal wetlands of Sandakan. Thus, although there would be differences on a daily basis the overall climate of Sukau and Abai was expected to show little difference to that recorded at Sandakan airport.

2.5 BOTANY Botanical transects were established at Sukau and Abai study areas to describe the

structure and tree species composition of the forest, and to monitor the phenology of the trees. Every month, the crowns of all transects’ trees were examined for the presence of mature and young leaves, ripe and unripe fruits, and flowers.

Transects were placed perpendicular to the edge of the river. At the Sukau study area, kilometre-long straight line transects were placed on both sides of the Menanggul River at the 1st, 3rd, 5th, 7th and 9th kilometres. The number of trees within the transects totalled 1,378. All trees of at least 30cm girth at breast height (g.b.h) located within a meter on either side of the transect line were measured, tagged and identified. A 30cm g.b.h was used to allow comparison with other plots in Sabah (Davies, 1984). Girths of buttressed trees were measured immediately above the buttresses (Bennett, 1983; Davies, 1984). Trees that were partly within a meter of the transects were included if 50% of their bases or more were within the strip. The basal area of each tree was calculated. The basal area is a good indicator of tree size and foliage biomass (Anon., 1981). Only the first 50 trees from the river at each transect were used for phenology, making a total of 500 trees.

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At Abai study area, straight line transects were similarly placed on both sides of the Merah River, at the 3rd, 6th and 9th kilometres. The 1st, 3rd, 5th, 7th and 9th kilometres were not selected because the 1st and 5th transects had little or no standing trees. The 6th kilometre was selected instead of the 5th and 7th kilometres, being equidistant from the 3rd and 9th kilometre. Nypa fruticans (Arecaceae) was abundant and dominated the study area. About half of the Merah River was lined with extensive stands of N. fruticans. It was neither measured nor tagged for phenology, because it was not a tree, and because of its structure. The number of trees within the transects totalled 300, a good sample size considering that there were not many standing trees in the area. In addition, the floral diversity was very low; therefore, the need for a large sample is reduced.

Transect trees were identified by Mr. Paul Langgi, a senior ranger with the Sabah Wildlife Department. Mr. Langgi was a botanist attached to the Sabah Forestry Department before he moved to the Wildlife Department. Samples from trees that could not be identified in the field were collected and later identified at the herbarium of the Forestry Department.

2.6 PHYTOCHEMISTRY Plant parts were collected from common trees found along the botanical transects and

along the rivers, and from known N. larvatus food trees at Sukau and Abai study areas. Plant parts were collected from at least two trees for each species. This was to investigate the phytochemistry of different plant parts and species (section 3.6), and to examine the factors likely to influence food selection (section 5.5). Samples were analysed by Ms. Loh Soo Nai under Dr. Siraj Omar’s supervision at the Department of Chemistry, Malaysian National University (Universiti Kebangsaan Malaysia), Kota Kinabalu (Loh, 1991).

Samples collected were kept in a cool and dry place away from direct sunlight until transported to the laboratory. At the laboratory, samples were oven-dried at 45 C, and then placed in airtight plastic bags for further analysis. Samples were analysed for the presence of alkaloids, saponins, nitrogen, condensed tannin and neutral detergent fibre (Loh, 1991).

The samples were analysed for alkaloids (Alk) using Mayer’s reagent (Culvenor and Fitzgerald, 1963), and for saponins (Sap) using bubbles test (Simes et al., 1959). Results were semi-qualitatively quantified for absence and from 1+ to 4+ for residual amounts in alkaloids. The presence of saponins based on the height of bubbles was similarly quantified.

The amount of organic nitrogen (N) in plant samples was determined by the micro-Kjeldahl method that has been modified (Ng, 1972), and expressed as % dry weight. Crude protein (%Prot) was calculated by multiplying %N by a factor of 6.25 (Maynard & Loosli, 1969). Condensed tannins were analysed using vanilin-HCl (Burns, 1971; Dalby, 1978) and expressed in mg/g. Analysis for neutral detergent fibre (NDF) used van Soest’s method (van Soest and Wine, 1967; Church and Pond, 1988), and was expressed as % dry weight.

Although the methods for analysing nitrogen and condensed tannins differed from those used in previous colobine studies (Bennett, 1983; Davies, 1984; Davies et al, 1988; Waterman et al, 1988), the results were nevertheless comparable (Loh, 1991). Loh (1991) analysed for NDF instead of acid detergent fibre (ADF), because N. larvatus is a polygastric herbivore, a ruminant with an almost neutral pH value in the forestomach that allows bacteria to thrive (Bauchop, 1978). NDF was analysed as dietary fibre content in diets consumed by captive N. larvatus (Dierenfeld et al., 1992), and results were comparable to this study.

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2.7 FOOD SAMPLES Plant samples (n=52) whose parts were seen to be eaten by N. larvatus were collected

and brought to the Research Division of the Sabah Forestry Department. The samples were identified by Mr. Leopold Madani, a botanist with the division. Plant-food samples were also collected for phytochemical analysis at the Malaysian National University.

2.8 HABITUATION Attempts were made to habituate N. larvatus so as to reduce bias in observations. The

presence of local people and tourists, and the absence of hunting pressure on the animals made habituation easier. The animals, however, were habituated only to observers in a boat. Away from the river and in the forest, they would flee from observers on foot. Habituation of N. larvatus groups, particularly SU1, to Sharma and me, met with little success. Furthermore, other N. larvatus groups and other mammalian species were frequently encountered in the forest. Their reaction to the observers would always cause the focal group, SU1, to flee along with the animals encountered.

Thus, to collect data without bias, dull coloured clothes were worn, so as to remain inconspicuous while on foot in the forest. It was only at the end of the study that we could occasionally approach SU1 to about 50m, with the group being aware of our presence, without it fleeing.

2.9 SURVEYS

2.9.1 AERIAL SURVEY An aerial survey was conducted on March 25, 1991 to assess the availability of N.

larvatus habitats in the Lower Kinabatangan region. Aerial survey routes were chosen to fly mainly over the Kinabatangan River, particularly around the study areas. Routes generally followed the main rivers both for ease of navigation, also because riverbanks are essential to N. larvatus (section 2.9.2). The flight was courtesy of the Royal Malaysian Air Force using a Sea King helicopter.

Flying height varied from 15 to 300m, depending on the terrain and location. The route involved circling round the ox-bow lakes, in areas of extensive damage due to logging and agriculture, and other areas of interest. Information recorded was habitat damage type, extent of damage, condition of rivers and lakes, presence of N. larvatus or any other large animals, and other general observations. Photographic records were also made during the flight.

2.9.2 RIVER SURVEYS Nasalis larvatus sleep in trees next to rivers every night (Kern, 1964; Kawabe &

Mano, 1972; Jeffrey, 1979; Macdonald, 1982; Salter et al., 1985; Bennett, 1986a; Bennett & Sebastian, 1988; Rajanathan & Bennett, 1990; Yeager, 1989; 1991a & b). Thus, by travelling in a boat along the rivers before dusk and just after dawn, it was possible to observe most groups. Surveys were conducted using a small boat fitted with a 25-HP outboard engine. They began at 1630 hours and usually ended at 1830 hours, between the time when animals arrived at the river and when it was too dark to count well. The surveys were repeated the next morning at 0545 hours following the same route taken the previous evening and ending at 0715 hours. This allowed two attempts at group counts, identifications and locations to be

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made for any one night (Bennett, 1986a; Bennett & Sebastian, 1988; Rajanathan & Bennett, 1990).

Groups’ positions were located and mapped by placing plastic tags every 25m along the Menanggul River for 10km, measured from the river-mouth, and along the Merah River for 12km, measured from the river-mouth. The Menanggul River was frequently blocked by fallen trees and by Eichhornia crassipes (Pontederiace) (figure 2.2), so a longer distance could not be surveyed given the time constraints. Furthermore, the river was shallow at some places and was also tidal (section 3.1.1). On the other hand, the Merah River was wide and deep, and could be navigated to a longer distance.

The rivers to be surveyed were divided into two halves. During an evening survey, only one half of the survey length was covered. The other half was surveyed on the next evening. Cruising speed was maintained at not more than 5km/hr, and about ten to fifteen minutes were spent observing each group. Therefore, given the limited amount of time animals were visible by the river, only one-half of the survey length could be covered in one evening.

Opportunistic surveys were also conducted in the estuaries of the Kinabatangan River, along the Kinabatangan River from Mumiang to Bilit, and the various tributaries and ox-bow lakes located between Mumiang to Bilit (figure 2.1). From April to November 1991, Sharma conducted systematic river surveys along Tenegang Besar, Sapasidom and Menanggul Rivers, and at Kelandaun and Kelananap Lakes.

During a river survey, the following information was recorded:

1. date;

2. site;

3. river tide at start of survey;

4. weather at start of survey, recorded in a three number code (table 2.1);

5. start and end time of survey

The above information was recorded once per survey, and following was recorded once per encounter:

6. time when each group/individual was encountered;

7. location of encounter, with reference to markers placed along the rivers;

8. spread of group along the river, i.e. the distance from the first to the last individual in that group, referring to the location markers;

9. observed number of individuals, i.e. the minimum number present;

10. estimated number of individuals, i.e. probably a more accurate assessment of the number present;

11. age/sex composition of the group (table 2.2);

12. food item if seen feeding;

13. bank of river where groups or individuals were encountered;

14. other species of animals, if found within 20m to the group or individual.

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2.9.3 TRANSECT SURVEYS Surveys were conducted at Sukau by Sharma, to document the presence and

abundance of the vertebrate fauna (Sharma, 1992). Transects prepared for collecting botanical data were used for the surveys (section 2.5). Each transect was walked once a month between 0630 to 1130 hours. Animals were recorded through direct observations or from indirect evidence, such as scats, spoor, feeding signs and vocalisations. The line transect method was used to estimate mammal density (Burnham et al., 1980; Brockelman & Ali, 1987). The Fourier Series Estimator (Burnham, et al., 1980) was used to calculate mammal densities, and Simpson’s Index was applied to calculate bird diversity (Sharma, 1992).

2.10 FULL DAY FOLLOWS To obtain information on N. larvatus ranging and social behaviour, full day

observations from dawn to dusk were made, using the scan sampling method (Altmann, 1974). All observations were made using a pair of Zeiss Dialyt 10x40B binoculars. A focal group, SU1 (section 4.2.1.2), was identified and observed by myself for a minimum of five consecutive days a month, for twelve months at the Sukau study area (section 2.2). Additional data on SU1’s ranging and social behaviour were obtained by Sharma, who observed the group for another five consecutive days every month (section 2.2). Whenever SU1 could not be located, then observations were made on other N. larvatus groups.

Observations were made from the boat in the morning before SU1 moved away from the riverside and in the evening after the group returned to the riverside. During the day when SU1 moved into the forest, the group was followed on foot. To enable this, a continuous network of trails based on a grid system measuring 100m x 100m was made. This also allowed SU1’s position to be plotted more accurately. The group’s position (centre of group) was plotted on maps (1:100) every 15 minutes or whenever its’ position changed at least 20m.

At Abai, at least five consecutive days per month, were spent on behavioural observations. It was, however, 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 high tide (figure 2.3). The ground was very soft and muddy during low tide, 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. I remained with a group for as long as possible, and then searched for another group when the first group was not visible anymore.

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. Each observation was recorded three seconds after the individual was sighted; so as to reduce bias towards individuals engaged in eye-catching activities (Kavanagh, 1977; Bennett, 1983).

Data recorded during each scan sample were:

1. date;

2. study area;

3. group, whether harem, all-male or non-breeding, and group identity. A non-breeding group refers to a loosely bonded predominantly male group with at least one female member;

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4. time, referring to Malaysian Standard Time (GMT+8);

5. weather, in a three-number code (table 2.1);

6. location of the group. At Sukau, it was with reference to the grid network of trails. At Abai, the group’s position was referred to the location markers along the river (section 2.9.2);

The following information was recorded once during every observation:

7. age and sex of observed individual (table 2.2);

8. identity of observed individual, if known;

9. behaviour (table 2.3);

10. plant part and species, if known, when feeding was observed;

11. age and sex of the individual nearest to the observed individual (the nearest neighbour);

12. the distance from the observed individual to the nearest neighbour;

13. the number of other group members within 2.5m and 5m of the observed animal (Struhsaker, 1975; Struhsaker & Leland, 1979);

14. height of observed animal above ground.

2.11 DATA ANALYSIS Data collected were analysed by hand and with a Toshiba T1600 laptop computer, and

an IBM AT portable computer. Statistical analysis was performed using the Statistical Package for the Social Sciences (SPSS) packaged program (Nie et al., 1975). Statistical tests and abbreviations in this thesis follow those used by Siegel and Castellan, Jr. (1988). Statistical tests are two-tailed unless stated otherwise.

The Spearman rank-order correlation coefficient rs was used to measure the association between two variables. Since variables were measured on an ordinal scale, it was possible to rank them into ordered series. When a correlation was observed between two variables, there was always the possibility that the correlation was due to the association between each of the two variables and a third variable. Thus, it was also necessary to use the Kendall partial rank-order correlation coefficient Txyz, which measures the degree of relation between two variables X and Y when a third variable Z is held constant (Siegel & Castellan, Jr., 1988).

In each scan, it was possible to see more animals engaging in conspicuous activities (e.g., travelling) than in other inconspicuous activities (e.g., resting). To reduce this bias, the number of individuals recorded in each scan was weighted, such that each scan contributed one point to the dataset, irrespective of how many animals were seen during the scan. Weighting involves dividing each observation in a scan by the total number of observations made in that scan. Therefore, the combined weighting for each scan is one (Kavanagh, 1977; Bennett, 1983).

2.12 SUMMARY 1. Officers and rangers from the Sabah Wildlife Department provided field assistance

throughout the study. Mr. Dionysius S. Sharma, a scientific officer with World Wide Fund for Nature, Malaysia, provided field assistance for 11 months during the second year.

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2. Botanical transects were located systematically along the Menanggul and Merah Rivers. All trees with a minimum of 30cm g.b.h. found within a metre of the straight line transects were tagged, enumerated and identified.

3. Plant parts collected along the transects and rivers were analysed for their phytochemistry by Ms. Loh Soo Nai and Dr. Siraj Omar at the National University of Malaysia, Kota Kinabalu.

4. An aerial survey courtesy of the Royal Malaysian Air Force, was carried out to assess N. larvatus habitats in the study area. The survey was conducted along the main tributaries and around the ox-bow lakes in the Lower Kinabatangan region.

5. Monthly boat surveys were conducted at both study sites to determine the population, group size and age-sex composition of the N. larvatus population. Opportunistic boat surveys were also carried out along the Kinabatangan River, its tributaries and ox-bow lakes from Mumiang to Bilit.

6. Botanical transects at Sukau were also used by D.S. Sharma to carry out wildlife surveys. These were to determine the presence and abundance of other species of wildlife in the area.

7. At Sukau, a harem group was identified and then habituated for full day observations. The purpose was to determine its ranging, feeding and social behaviour. At Abai, due to shyness of the study animals and difficulty of the terrain, observations were limited to the riverside and were not throughout the daylight hours.

8. During full day follows, observations were made by scan sampling for two minutes every 15 minutes from dawn to dusk. To reduce bias, observations were recorded three seconds after the subject was selected.

9. The SPSS packaged program was used to analyse the data. To reduce bias, each observation was weighted by the reciprocal of the number of observations in that scan. Thus, each scan was weighted equally regardless of the number of observations therein.

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Table 2.1 Weather categories (adapted from Bennett, 1983; Davies, 1984)

Overall weather (1-5) 1: Dry and sunny; 2: Dry and not sunny; 3: Drizzle i.e. fine misty rain and does not penetrate canopy; 4: Rain i.e. rain able to penetrate canopy and reach forest floor; 5: Downpour i.e. heavy rain that impaired visibility.

Cloud cover (0-8) 0: No cloud; 2: 25% cloud cover; 4: 50% cloud cover; 6: 75% cloud cover; 8: 100% cloud cover.

Wind (0-2) 0: Negligible; 1: Leaves move; 2: Branches move.

Table 2.2 Age/sex categories used in this study (adapted from Bennett, 1986a)

Category Criteria Adult male Male of full body size with fully developed nose and mane of hair

across back. He has a flesh coloured face and yellow collar. There is a distinct triangular white patch in the sacral region leading to a long, thick white tail. The rest of the fur is predominantly reddish brown.

Adult female Female of full body size. Compared to the adult male, she has a smaller nose. The rump patch and tail is somewhat darker, and the tail is not as thick.

Sub-adult male Male more than 3/4 full body size but without fully developed nose and/or mane across back. Other basic features are the same as the adult male.

Sub-adult female Female more than 3/4 but not yet fully adult body size. Juvenile-2 male Male with adult coloured face and brown fur coat, but not yet 3/4 full

adult size. Juvenile-2 males can be the same size or larger than adult females.

Juvenile-2 female Female with adult coloured face and brown fur coat, but not yet 3/4 full adult size.

Juvenile-1 male Male with adult coloured face and brown fur coat, but not yet 1/2 full adult size.

Juvenile-1 female Female with adult coloured face and brown fur coat, but not yet 1/2 full adult size.

Infant-2 Male and female with brown fur on head and body but with at least some dark skin on face.

Infant-1 Male and female with dark brown/black fur on body and/or head and dark coloured face.

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Table 2.3 Activity categories used in this study (adapted from Bennett, 1983)

Activity Definition Sit* Subject sitting but not engaged in any other activity, except clinging (see

cling). Stand* Subject standing on two or four limbs but not engaged in any other

activity. Lie* Subject lying down and not engaged in any other activity. Travel Any movement between two points. Sub-divided into: 1. travel within

the same tree; 2. travel between trees; 3. travel on the ground; 4. swimming.

Groom Any scratching or cleaning action using hands, feet or mouth. Sub-divided into 1. autogroom; 2. subject allogroom another; 3. subject being allogroomed.

Feed Subject manipulating, putting into mouth or masticating food items. Suckle Subject with nipple of adult females in mouth. Drink Subject drinking or licking fluids. Cling Subject clinging to another individual with both hands. The subject's

weight may or may not be supported by the other individual. Allomothering Subject assist in the care of the offspring that is not its own; or subject (a

young offspring) being cared for by individuals other than its own parent.

Play Chasing, wrestling, exploratory and other movements that apparently are not goal-directed. Play can be solitary or social i.e. involving two or more individuals.

Mount Subject positions itself behind and above another, with ventral-dorsal contact. Sub-divided into 1. male mounting the female with penile penetration; 2. female being mounted by the male with penile penetration; 3. homosexual mounting without penile penetration; 4. heterosexual mounting without penile penetration.

Agonistic Subject delivers or receives act of aggression. Sub-divided into 1. without physical contact e.g., deliver open-mouth facial threat; 2. with physical contact e.g., grab, lunge or bite.

Vocalise** Any call produced by subject. Includes "honk", grunt, bark, cough, squeal and scream.

Urinate Subject discharges urine. Defecate Subject discharges faeces (from the bowels).

* For sitting, standing and lying, the direction that the subject was apparently looking was also recorded. The categories used were: 1) look at observer; 2) look at other humans or boats; 3) look at other proboscis monkey/group; 4) look at other species; 5) general observation (undirected line of vision); 6) rest/sleep (eyes closed). ** Usually accompanies some of the activities defined above. Note: By the above definitions, no two activities except vocalisation are recorded together. If an animal is travelling along a branch while masticating or manipulating food, the activity was recorded as travelling. If the distance travelled is less than 0.5m, then it was recorded as feeding.

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Figure 2.1 Sukau and Abai showing natural features

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Figure 2.2 The Menanggul River was frequently blocked by tree falls and Eichhornia crassipes, which require clearing, usually when the tide was low

Figure 2.3 Abai study area at high tide

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CHAPTER 3: STUDY AREA

3.1 INTRODUCTION The study of N. larvatus was conducted at Sukau (118° 17’E, 5° 30’N) and Abai

(118° 22’E, 5 41’N), located along the Kinabatangan River in eastern Sabah (figure 2.1). Attempts were made to compare the ecology and behaviour of N. larvatus in the two different areas. The Lower Kinabatangan region is mostly under forest on flat land that had been subjected to different degrees of disturbance. Open water, hills, villages and plantations are sparsely scattered throughout (Payne, 1989). This chapter aims to describe the structure, composition, phenology and phytochemistry of the forests at Sukau and Abai.

3.1.1 THE KINABATANGAN RIVER The Kinabatangan River is Sabah’s largest river, with a length of 560km, and a

catchment area of 16,800km² (Scott, 1989). Its main source of water is run-off from mountains in the south-eastern interior (figure 1.1). The lower 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 Kinabatangan floodplain, measuring approximately 280,000ha, is the largest and possibly the most important wetland in Sabah (Scott, 1989). The river finally empties into a large delta, which is brackish and tidal.

Tidal range in the lower Kinabatangan River averages 1.1m, but the river level can rise to 5m overnight if there is widespread rain upriver. There are many ox-bow lakes in the area from the middle reaches of the river down to the coastal plains. They are at various stages of infilling.

3.1.2 SOILS AND GEOLOGY The soils in the flood-prone area are alluvium, which lies on top of sedimentary rocks,

mainly sandstones with some mudstones and limestones. Raised alluvial terraces and plains are found along the banks of the main river and its larger tributaries. These can vary in extent from tens of metres to more than a kilometre. These areas are very fertile for agriculture but risk periodic high floods. Behind and scattered among these terraces and plains is low-lying freshwater swamp forest. Although the soil is also alluvium and thus fertile in terms of mineral content, it is not suitable for most plants because it is waterlogged. The alluvial soils are only thousands of years old, which is quite recent in geological terms (Payne, 1989).

Scattered throughout the region are small but steep hard sandstone hills, which protruded from massive layers beneath. The remainder of the Kinabatangan landscape is made up of soft sandstones and mudstones. An interesting feature of the floodplain is the limestone outcrops. These sandstone and limestone hills were formed during the Miocene epoch, between 26 and 7 million years ago (Payne, 1989).

3.1.3 CLIMATE Mean temperatures did not vary much between months during study period. The mean

monthly minimum for 1990 and 1991 was 23.7 C (figure 3.1). While the mean monthly maximum for 1990 was 32.9°C, and for 1991, it was 33°C. The total rainfall for 1990 was 1,816mm, and for 1991, it was 2,975mm (figure 3.2). It rained for a total of 159 days in 1990, and for a total of 183 days in 1991. This means that it rained on average once in two days.

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Klimagraphic information showed that there were two dry periods (less than 50mm) in 1990, in February and April, whereas 1991 had only one dry period, in March (figure 3.3).

3.1.4 LOGGING HISTORY The earliest record for timber exports from Sandakan was as early as 1883 (Khoo,

1981). The lower Kinabatangan was subjected to commercial logging since the early 1950s until present (Payne, 1989). Virtually all of the forests of the Kinabatangan area have been logged at least once. In the early 1980s, logging of mangroves in eastern Sabah was widespread, mainly for woodchips. It was banned in early 1987 (Bennett, 1991).

Large quantities of rattan have been collected from the region and they have long been an important local trade item. The long stretches of flat land along the banks of the Kinabatangan and its tributaries have been the principal source of supply. Most of the harvesting was within a kilometre of the waterways (Khoo, 1981). All the rattan harvested from the region until 1989 was wild; after that, most of the rattan harvested was cultivated by the Sabah Forestry Development Authority (Payne, 1989).

3.1.5 HUNTING PRESSURE In the lower Kinabatangan, approximately 98% of the local people are Moslems, so

do not hunt N. larvatus for meat. Occasional visits by pirates discouraged outsiders from hunting around the estuaries. Furthermore, N. larvatus did not raid crops and thus were not considered as pests. Hunting of N. larvatus by outsiders from nearby towns for meat, however, was reported in the mangroves of the Sandakan Peninsula, but never reported in the study areas (Boonratana, 1993a & b; Boonratana & Sharma, in press).

3.1.6 POPULATION SIZE OF N. LARVATUS Systematic and opportunistic river surveys of N. larvatus (section 2.9.2), conducted in

different parts of the Lower Kinabatangan (figure 2.1), showed that there are at least 832 individuals (table 3.1) to be found from Bilit to the estuary (Boonratana & Sharma, in press). The actual figure, however, could be at least twice that, because certain areas in the estuary were not surveyed due to pirate threats, and some tributaries could only be surveyed to a limited distance due to being blocked by fallen trees, cut logs, debris and Eichhornia crassipes (Pontederiace) (Boonratana & Sharma, in press).

3.2 SUKAU STUDY AREA

3.2.1 WILD FAUNA A check-list of mammals, birds and reptiles at Sukau is given in Appendix I. Only

those species whose presence was recorded during the study period are included in the list. At least 51 mammal species including two volant mammals, and 196 bird species are found in the area. It has a high diversity and abundance of wildlife, in particular primates.

Ten primate species are found in the area (Boonratana, 1993a & b; Boonratana & Sharma, in press), four of which are Bornean endemics, namely Nasalis larvatus, Presbytis hosei, two subspecies of P. rubicunda (P.r. rubicunda and P.r. chrysea), and Hylobates muelleri. The other primates are Pongo pygmaeus, Trachypithecus cristatus, Macaca nemestrina, M. fascicularis, Nycticebus coucang, and Tarsius bancanus. This is one of only two known sites in Asia with ten primate species, and one of only two known sites in the world with four sympatric colobines (Boonratana, 1993a & b; Boonratana & Sharma, in

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press). The other site is the Danum Valley Conservation Area in south-east Sabah (Boonratana & Sharma, in press).

Other large mammals found in the Lower Kinabatangan area include Elephas maximus, Dicerorhinus sumatrensis, Bos javanicus, Cervus unicolor, Muntiacus muntjak, Helarctos malayanus, Neofelis nebulosa, Felis planiceps, F. bengalensis and Sus barbatus (Boonratana & Sharma, in press).

All eight species of hornbills found in Borneo have been recorded in the area. Five species of Bornean endemic birds occur here, namely Lonchura fuscans, Pityriasis gymnocephala, Ptilocichla leucogrammica, Cyornis superba and Pitta baudi. The ox-bow lakes are important breeding grounds for Anhinga melanogaster and Crocodylus porosus, both of which are becoming very rare in other parts of northern Borneo (Boonratana & Sharma, in press).

3.2.1.1 DENSITY AND BIOMASS OF N. larvatus The population density of N. larvatus at Sukau was 34.01 individuals/km², which

gives a biomass of 255.35 kg/km². The population density was calculated by dividing the total number of individuals from known groups in association with SU1 (section 4.2.1.6), by the focal (SU1) group’s home range size, as different groups’ ranges overlapped completely (section 6.2.1).

3.2.2 FLORA At Sukau, the principal vegetation types in the flood-prone areas are riverine forest

and freshwater swamp forest. There are also some open reed swamps. In the flood-free zone, there are remnants of pristine lowland dipterocarp forest, logged-over swamp forest and burnt lowland dipterocarp forest, and cocoa and oil palm plantations.

3.2.2.1 BOTANICAL STRUCTURE The 2m wide transects at Sukau covered a total area of 1.96ha. They contained 1,378

trees with a minimum 30cm girth at breast height (g.b.h). Thus, the density of trees of 30cm g.b.h was 703 per hectare. Most of the transect trees at Sukau had girths less than 140cm, with the maximum recorded girth 447cm (figure 3.4). The mean and median girths of trees in transects were 65.4cm and 49cm, respectively.

3.2.2.2 BOTANICAL COMPOSITION The 1378 trees in the botanical transects at Sukau, comprised 109 species from 37

families. The species, number of stems and basal area of each are listed in Appendix III. To assess species richness, the rate at which the number of tree species increased with increasing tree sample size was plotted (figure 3.5). Although the curve is close to being level by the end, there was still an obvious tendency for the number of species to increase if the total sample size is increased. It would probably take several hundred additional trees before the curve reaches a plateau.

The maximum basal area recorded for any one of the transect trees was 15,896cm², and the mean basal area of all trees was 492cm². The transects covered an area of 19,550m² and had a total basal area of 67.77m² for trees with 30cm g.b.h. Therefore, the total basal area per hectare was 34.58m².

Euphorbiaceae was the most abundant tree family in terms of stem-number at Sukau and had the greatest basal area (table 3.2). Although Dipterocarpaceae ranked seventh in terms of abundance, it had the next greatest basal area. Tree families that were also abundant

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in terms of stem-number include Clusiaceae, Myrtaceae, Rubiaceae, Lauraceae and Dilleniaceae.

Eugenia bankensis (Myrtaceae) was the commonest tree species in the transects and made up 8.8% of the total number of trees 30cm g.b.h. (table 3.3). The next commonest tree species was Dillenia grandifolia (Dilleniaceae), followed by Neonauclea bernadoi (Rubiaceae), Litsea odorifera (Lauraceae) and Mallotus muticus (Euphorbiaceae). In terms of basal area however, M. muticus had the highest at 10.95%, followed by E. bankensis at 8.9%.

3.2.2.3 PHENOLOGY A total of 500 trees from the transects was monitored for their phenological cycle

from March 1990 to December 1991 (figure 3.6). The production of young leaves was high throughout most of the study period, being exceptionally high from October 1990 to January 1991, and from March to December 1991. These coincided with mostly wet periods, except March 1991, which was just after the wet period. From March to May 1990, leaf production was moderate. This was during and just after a dry period. There, however, was no correlation between young leaf production and rainfall (rs=0.163, n=22, p>0.05). The minimum recorded leaf production during the study period was 58% of trees in May 1990, just after a dry period.

There was a distinct peak in flower production in April 1990 when 20.6% of transect trees bore flowers, coinciding with a dry period. There were two peaks in flower production for 1991, in April (16.4%), just after a dry period, and in October (16.8%), when rainfall was moderate. No correlation existed between rainfall and flower production (rs=-0.170, n=22, p>0.05). During the study period, flower production was lowest in December 1990 when only 1.4% of trees bore flowers.

There was a distinct fruiting season from June to August 1990 with a peak in June (14.2% of all trees). This was during a wet period. There were two fruiting seasons in 1991, during a wet and dry period, from January to April, and during a wet season, from July to September. There was no correlation between fruit production and rainfall (rs=0.116, n=22, p>0.05). The peak in fruit production for 1991 was in August, when 12% of trees bore fruits. The lowest fruit production was in March 1990 when only 1.4% trees bore fruits.

3.3 ABAI STUDY AREA

3.3.1 WILD FAUNA A check-list of mammals, birds and reptiles in and around Abai study area is given in

Appendix III. Only those species whose presence was recorded during the study period are included in the list. There are at least 17 non-volant mammal species and 75 bird species found in the area.

The primates sighted at Abai were N. larvatus, P. hosei, P.r. rubicunda, P.r. chrysea, T. cristatus, M. nemestrina, M. fascicularis, H. muelleri, and P. pygmaeus. Other large mammals found there include E. maximus, D. sumatrensis, B. javanicus, C. unicolor, H. malayanus and S. barbatus. All eight hornbill species are resident in the area. There are two Bornean endemics, Pityriasis gymnocephala and Lonchura fuscans. Treron fulvicollis, T. olax and Psittacula longicauda are particularly common. It probably is also an important site for Cicona stormi and Leptoptilos javanicus. Crocodylus porosus although not common, is also present.

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3.3.1.1 DENSITY AND BIOMASS OF N. larvatus The population density of N. larvatus at Abai was 10 individuals/km², giving a

biomass of 75.08 kg/km². The density was calculated by dividing the maximum number of individuals observed in a single survey by the estimated home range of a harem group, AB1. This assumed that N. larvatus groups did not travel farther than 350m away from the Merah river (section 6.3.1), and that they use both sides of the river uniformly.

3.3.2 FLORA The principal vegetation at Abai is mangrove forest with extensive stands of Nypa

fruticans (Arecaceae) at the inland edge and the upper tidal limit of the estuaries. Upriver from this, beyond the influence of seawater, riverine forest and lowland swamp forest dominate in the seasonally flood-prone zone. Transitional forest exists where mangrove forest intergrades to riverine forest. There are also some forests on steep hills and flat ground. The trees at Abai are highly clumped. The tree species and their proportions in the botanical transects at Abai are given in Appendix IV.

3.3.2.1 BOTANICAL STRUCTURE The transects covered an area of 0.29ha. Thus, the density of trees with 30cm g.b.h.

was 1034.5 per hectare. Most of the transect trees at Abai had girths lower than 120cm, with the maximum girth being 408cm (figure 3.7). Mean and median girths of the transect trees were 59 and 47cm, respectively.

3.3.2.2 BOTANICAL COMPOSITION The botanical transects at Abai contained 300 trees, comprising a total of 42 species

belonging to 26 families. To assess species richness, the rate at which the number of tree species increased with increasing tree sample size was plotted (figure 3.8). If the total sample size was increased, very little increase in the number of tree species is expected. The maximum basal area of the transect trees was 13,243cm², and the mean basal area was 402.6cm². The transects covered an area of 2,906m² and had a total basal area of 12.08m². Therefore, the basal area per hectare was 41.64m².

Melastomaceae was the most abundant tree family at Abai, followed by Myrtaceae, Elaeocarpaceae, Verbenceae, Anacardiaceae and Rhizophoraceae (table 3.4). Although trees belonging to the family Rhizophoraceae were not very abundant, it had the greatest basal area of all families. Moraceae also was not abundant, but had the next greatest basal area.

The commonest tree species at Abai was Kibessia galeata (Melastomaceae) which made 14.0% of the total trees (table 3.5). This was followed by Eugenia bankensis (Myrtaceae), Elaeocarpus canipes (Elaeocarpaceae), Vitex pinnata (Verbenaceae), and Buchanania insignis (Anacardiaceae). Bruguiera sexangula (Rhizophoraceae) had the greatest basal area, 19.51% of the total.

3.3.2.3 PHENOLOGY A total of 300 trees was monitored monthly for their phenological cycles. This was

from March 1990 to December 1991, except June 1990 when the principal investigator suffered from viral fever (figure 3.9).

Young leaf production was high from December 1990 to January 1991, and from March to December 1991. These peaks coincided with periods of high rainfall, except in March when it was dry. April 1990 was the month with the lowest leaf production, when only 43.3% of transect trees produced young leaves. This coincided with the dry period for that

26

year. There was a positive correlation between young leaf production and rainfall (rs=0.491, n=21, p<0.05).

In 1990, flower production was highest in October, during a wet period, when 29.3% of transect trees bore flowers. 1991 saw two flowering seasons, from March to May, and from July to September. No correlation, however, existed between flower production and rainfall (rs=-0.183, n=21, p>0.05). December 1990 had the lowest flower production, when only 8.4% of transect trees produced flowers, while September 1991 had the highest at 41% of trees.

Fruit production was high from December 1990 to February 1991, in April 1991, and from August to October 1991. All these peaks were during the wet periods. A significant positive correlation existed between fruit production and rainfall (rs=0.513, n=21, p<0.05). Highest fruit production for 1990 was in December at 28.4% and for 1991 it was in January and April, both at 29.7%. The lowest fruit production was in April 1990 at 6%, which was a dry period.

3.4 COMPARISON BETWEEN SUKAU AND ABAI

3.4.1 BOTANICAL STRUCTURE The number of transect trees 30cm g.b.h. at Abai was 300, compared to 1378 at

Sukau. Abai had a total of 1035 trees per hectare, while Sukau had only 703 trees per hectare. The mean g.b.h at Abai (59cm) was less than that at Sukau (65cm). There is a small difference in median girth at breast height between Abai (47cm) and Sukau (49cm).

3.4.2 BOTANICAL COMPOSITION The 300 transect trees at Abai included 42 species from 26 families, whereas the 1378

trees at Sukau included 109 species from 37 families. Abai had 42 species in 300 individuals (figure 3.8); whereas Sukau had 66 species in the first 300 individuals (figure 3.6). Therefore, the forest at Sukau was more species-rich than that at Abai. The Shannon-Weiner diversity index (H’) at the species level was calculated for each study area. This index showed that the forest at Sukau (H’=3.72) was more diverse than that at Abai (H’=3.13).

Twenty-five families were common to both areas. These made up 98.3% of total transect trees at Abai and 90.2% of total transect trees at Sukau. The basal area of species common to both areas was 99.1% of the total for Abai, and 94.8% of the total for Sukau. Melastomataceae (14%) had the highest percent of transect trees at Abai, whereas at Sukau it was Euphorbiaceae (13.4%). The highest percent in terms of basal area at Abai was Rhizophoraceae (19.9%), while at Sukau it was Euphorbiaceae (14.3%).

When the 15 commonest species at Sukau and at Abai were compared, only six species were common to both areas. They were Eugenia bankensis (Myrtaceae), Buchanania insignis (Anacardiaceae), Kibessia galeata (Melastomataceae), Canarium apertum (Burseraceae), Calophyllum borneensis (Clusiaceae) and Diospyros pendula (Ebenaceae). At Abai, the commonest tree in the transects was Kibessia galeata (14%), but the tree with the highest percent of total basal area was Bruguiera sexangula (19.5%). At Sukau, the commonest species was Eugenia bankensis (8.8%), and the tree with the highest percent basal area was Mallotus muticus (11%).

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3.4.3 PHENOLOGY The phenological patterns at Abai and Sukau exhibited both similarities and

differences. The differences, however, were small. Young leaf production at both sites was very similar. There was no significant difference in young leaf production at the two sites (Mann-Whitney U=203.5, n1=21, n2=22, p>0.05). More flowers were produced at Abai than Sukau in most months and the trend was significant (U=38, n1=21, n2=22, p<0.05). The trend throughout the year, however, was similar to that at Sukau. In October 1990, however, there was a peak in flower production at Abai, but not at Sukau.

Except March 1990, the trend in fruit production was similar at both sites, although production was generally less at Sukau. This difference was significant (U=65.5, n1=21, n2=22, p<0.05). Fruit production at Sukau and Abai was much higher than that at Sepilok (Davies, 1984) and Kuala Lompat (Bennett, 1983), which might partly explain the high primate density and diversity in the Lower Kinabatangan.

3.5 FORESTS IN SABAH The ten commonest tree families from botanical plots and transects at different sites in

Sabah (figure 3.10) were compared for their stem abundance (table 3.6) and basal area (table 3.7). Dipterocarpaceae was the most abundant family at most sites except at Sukau and Tabin unlogged, where Euphorbiaceae was the most abundant family, and at Tabin logged-distant, where Rubiaceae was the most abundant. Dipterocarpaceae was not one of the ten commonest species at Abai. Instead, Melastomaceae followed by Myrtaceae, were the most abundant families. At Sepilok, Segaliud-Lokan, Kuamut, Kalabakan and Silabukan, Dipterocarpaceae accounted for about one third of all stems. At Tabin logged-distant, however, Rubiaceae accounted for more than one-third of all stems. Trees from the family Dipterocarpaceae are generally abundant throughout Sabah and the rest of Borneo (Whitmore, 1984).

The families that were common in at least seven sites were Annonaceae, Dipterocarpaceae, Ebenaceae, Euphorbiaceae, Lauraceae, Meliaceae and Myrtaceae. The families that were common in only one site were Alangiaceae at Kalabakan, Dilleniaceae at Sukau, Moraceae at Tabin logged-distant, Apocynaceae, Elaeocarpaceae, Rhizophoraceae and Verbenaceae at Abai. Abai had more families that were not common to other sites. This was presumably because it was a different forest type. It is partially mangrove forest at Abai, while all the rest are dryland forests.

Similarly, Dipterocarpaceae made up more than half of the basal area at most sites except Abai, Sukau, Tabin logged-adjacent, and Tabin logged-distant. At Abai, Rhizophoraceae and Moraceae in total made up not less than one-third of the total basal area there, although Moraceae was not a common family. At Sukau, Euphorbiaceae had the highest biomass reflected by having the most abundant number of stems. Myristicaceae was not common at Tabin logged-adjacent, yet its biomass was more than one-fifth of the total there. At Tabin logged-distant, Rubiaceae was the most common tree family and had the highest biomass.

3.6 PHYTOCHEMISTRY Phytochemical studies in plant communities not only provide a better understanding

of the dynamics of an ecosystem, but also provide a better understanding of the effects of plant chemicals on the feeding ecology of an herbivore (Janzen, 1975; McKey et al., 1981).

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To an herbivore, it is essential to select foods that contain essential nutrients, while at the same time avoiding or reducing the intake of deleterious compounds (Freeland and Janzen, 1974). To understand the criteria by which N. larvatus selects its foods, plant parts from the Lower Kinabatangan region (mainly from Sukau study area) were analysed for their phytochemical contents.

Phytochemical analyses were carried out on a total of 153 samples from 98 species. These included 130 leaf samples, 18 fruit samples and 5 flower samples (table 3.8). The mean values of organic nitrogen content, condensed tannin and neutral detergent fibre for mature leaves, young leaves, flowers and fruits are compared (figures 3.11a, b & c). The chemical composition of plant parts analysed is given in Appendix V.

3.6.1 ORGANIC NITROGEN AND CRUDE PROTEIN Organic nitrogen content (% dry weight) of samples ranged from 0.12 to 0.78%, and

the crude protein content was estimated to range from 0.75 to 4.89%. A major portion (56.2%) of all the plant samples had a crude protein content that ranged from 1 to 2%. Among all plant parts, young leaves had the highest mean crude protein content (2.62%). A comparison with mature leaves showed a significant difference (Student’s t=-4.75, n1=97, n2=33, p<0.05).

A direct comparison of mature and young leaves of 32 species was made for their organic nitrogen and crude protein content (table 3.9). The mean organic nitrogen and crude protein content were higher in young leaves than mature leaves. Two samples, however, had higher organic nitrogen and protein content in mature leaves. These were Phyllanthodendron sp. (Euphorbiaceae), and Rosaceae sp. A (Rosaceae). The difference in crude protein content between young and mature leaves was significant (t=-3.81, n1=32, n2=32, p<0.05).

All flower samples had crude protein content 1%. The mean crude protein content was more than fruits but less than leaves. There was a significant difference in crude protein content between flowers and young leaves (t=2.82, n1=33, n2=5, p<0.05).

Fruits had the lowest mean crude protein content (1.50%). There was a significant difference in crude protein content between young leaves and fruits (t=5.9, n1=33, n2=18, p<0.05). There also was a significant difference between mature leaves and fruits (t=2.59, n1=97, n2=18, p<0.05).

3.6.2 CONDENSED TANNIN Analysis for condensed tannin (CT) in plant parts showed a wide range in values (0 to

30.34mg/g). 92.2% of the samples had CT values lower than 10mg/g, and a majority (61.4%) had less than 1mg/g. 13.1% of the samples did not contain CT. Mature leaves had the highest mean CT value (3.27mg/g). The mean value of CT in young leaves was less than half that of mature leaves. A significant difference in CT values existed between mature and young leaves (t=2.99, n1=97, n2=33, p<0.05).

Thirty-two sets of mature and young leaves from the same species were compared for their CT values (table 3.9). The mean CT value of mature leaves was 3.05mg/g, while that for young leaves was 1.07mg/g. 34.4% of the sets had higher CT in young leaves than mature leaves, while 3.1% had the same value. The difference in CT value between mature and young leaves was not significant (t=1.79, n1=32, n2=32, p>0.05).

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Half of the unripe fruit samples had less than 1mg/g of CT. Only one fruit sample had a value higher than 6mg/g, an unidentified sp. B (Euphorbiaceae). All the flower samples had values below 1mg/g, and furthermore they showed the lowest mean level of CT (0.26mg/g).

3.6.3 NEUTRAL DETERGENT FIBRE Analysis of neutral detergent fibre (NDF) showed a range from 30.9 to 91.5%. A

large portion (76.5%) of all the plant-part samples had NDF values of more than 50%. Mature leaves had higher mean NDF value than young leaves. There was, however, no significant difference (t=1.43, n1=97, n2=33, p>0.05).

NDF values for 32 sets of mature and young leaves from the same species were compared (table 3.9). The mean NDF of mature leaves (57.9%) was higher than young leaves (55.33%). 21.9% of the sets, however, had higher values for young leaves than for mature leaves, and there was no significant difference in NDF values (t=0.79, n1=32, n2=32 p>0.05).

3.6.4 ALKALOIDS From a total of 136 samples, only 5.2% contained alkaloids. Only the leaf samples

contained alkaloids, 5.2% of mature leaves and 6.3% of young leaves.

3.6.5 SAPONINS 63.2% of a total of 125 samples contained saponins. 44.8% of the total, however were

positive at 1+. In terms of plant parts, 61.5% of mature leaves, 60% of young leaves, 66.7% of flowers, and 81.8% of fruits gave positive results when tested for saponins.

3.7 SUMMARY 1. The study was conducted at Sukau and Abai, located along the lower Kinabatangan River

in eastern Sabah. The Kinabatangan River is Sabah’s largest river with a floodplain that measures approximately 280,000ha.

2. The forest at Sukau was predominantly riverine, whereas at Abai it was predominantly mangrove. The soils in the Lower Kinabatangan region are alluvium, derived from sedimentary rocks, which comprise sandstone, mudstone and limestone.

3. The rainfall during the study period averaged 2,395mm per annum. Daily mean temperature varied little between months and ranged from 23.7 C to 33 C.

4. The population density of N. larvatus at Sukau and Abai were 34.01 individuals/km² and 10 individuals/km² respectively. The biomasses in these two areas were estimated to be 255.35 kg/km² and 75.08 kg/km² respectively.

5. Transect trees were all at least 30cm girth at breast-height. The botanical transects at Sukau comprised 1378 trees from 109 species, whereas at Abai comprised 300 trees from 42 species. The forest at Sukau (H’=3.72) was more diverse than at Abai (H’=3.13).

6. There was no significant difference in young leaf production at Sukau and Abai. Flower and fruit productions, however, were more at Abai.

7. Condensed tannin levels were generally highest for mature leaves and lowest for flowers. Fruits had the highest level of neutral detergent fibre, whereas young leaves had the lowest. Statistical tests between young and mature leaves showed no significant difference for either condensed tannin or neutral detergent fibre.

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8. None of the fruit and flower samples that were tested contained alkaloids. Alkaloids were found in 5.2% of mature leaf samples and 6.3% of young leaf samples. At least 60% of the plant parts tested contained saponins.

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Table 3.1 Population size of N. larvatus in the Lower Kinabatangan area

Location Survey length (km) N Mumiang to Abai 40 82Kuala Kinabatangan Besar to Abai 40 82Abai to Sukau 50 128Sukau to Bilit 35 154Merah River 12 84Resang/Sapasidom River 6 44Menanggul River 10 146Tenegang Besar River 12 95Kelananap Lake 17Total 832

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Table 3.2 Abundance and basal area of tree families in botanical transects at Sukau

Family % Total Stems % Total Basal Area Mean Basal Area (cm²) Alangiaceae 0.3 0.09 154.72Anacardiaceae 4.1 2.80 333.49Annonaceae 0.9 1.24 643.93Apocynaceae 0.1 0.04 152.19Bombacaceae 0.1 0.14 477.49Burseraceae 3.7 3.27 434.94Clusiaceae 9.0 8.38 457.97Combretaceae 0.6 1.20 1014.75Datiscaceae 0.4 0.27 307.10Dilleniaceae 7.8 2.83 180.63Dipterocarpaceae 6.7 10.21 742.19Ebenaceae 2.8 2.46 427.84Elaeocarpaceae 0.9 0.76 397.08Euphorbiaceae 13.4 14.32 527.57Fagaceae 0.1 0.03 231.98Flacourtiaceae 1.5 2.16 732.21Irvingiaceae 0.2 0.45 1021.80Lauraceae 8.2 8.35 500.84Lecythidaceae 2.2 0.99 215.36Leguminosae 1.6 2.04 626.28Melastomaceae 4.0 6.42 791.63Meliaceae 0.8 0.59 361.93Moraceae 1.3 2.76 1040.67Myristicaceae 1.0 0.73 350.94Myrtaceae 8.8 8.90 498.62Olacaceae 0.1 0.14 980.19Polygalaceae 1.3 1.20 451.10Rhizophoraceae 0.1 0.04 151.79Rosaceae 0.3 0.23 386.72Rubiaceae 8.5 9.07 520.68Rutaceae 0.4 0.07 99.57Sapindaceae 0.3 0.10 164.00Sapotaceae 1.3 0.50 187.81Sonneratiaceae 0.4 0.69 783.90Sterculiaceae 2.2 2.55 556.75Tiliaceae 2.1 1.71 398.96Verbenaceae 2.3 2.27 495.77

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Table 3.3 Abundance and basal area of fifteen commonest tree species at Sukau

Family Species No. of Stems

% Total Stems

Basal Area (cm²)

% Total Basal Area

Myrtaceae Eugenia bankensis 122 8.9 60313.75 8.90Dilleniaceae Dillenia grandifolia 98 7.1 15680.12 2.31Rubiaceae Neonauclea bernadoi 90 6.5 36811.30 5.43Lauraceae Litsea odorifera 81 5.9 28877.22 4.26Euphorbiaceae Mallotus muticus 76 5.5 74230.78 10.95Anacardiaceae Buchanania insignis 56 4.1 18801.98 2.77Melastomaceae Kibessia galeata 55 4.0 43539.54 6.42Burseraceae Canarium apertum 51 3.7 22182.11 3.27Clusiaceae Calophyllum borneensis 50 3.6 14084.78 2.08Clusiaceae Cratoxylum sumatrana 47 3.4 35801.92 5.28Euphorbiaceae Glochidion borneensis 39 2.8 13417.40 1.98Ebenaceae Diospyros pendula 38 2.8 16593.65 2.45Dipterocarpaceae Vatica oblongifolia 38 2.8 12973.86 1.91Lecythidaceae Barringtonia lanceolata 31 2.3 6676.22 0.99Rubiaceae Anthocephalus chinensis 27 2.0 24542.31 3.62Total 899 65.3 424503.87 62.72

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Table 3.4 Abundance and basal area of tree families in botanical transects at Abai

Family % Tree Stems % Tree Basal Area Mean Basal Area (cm²) Anacardiaceae 7.7 5.48 287.58Annonaceae 3.0 2.99 400.62Apocynaceae 3.3 1.50 181.00Burseraceae 4.0 3.16 318.06Clusiaceae 4.3 1.90 176.56Combretaceae 0.7 2.01 1212.17Dilleniaceae 3.0 0.79 106.46Dipterocarpaceae 2.3 2.66 458.13Ebenaceae 2.7 0.85 127.75Elaeocarpaceae 8.3 6.90 333.23Euphorbiaceae 3.3 2.03 272.17Flacourtiaceae 1.0 0.76 305.62Lauraceae 1.3 1.23 372.71Lecythidaceae 0.3 0.09 108.91Leguminosae 0.3 0.10 121.00Melastomaceae 14.0 8.05 231.50Moraceae 2.7 14.71 2220.57Myrtaceae 11.3 5.99 212.92Polygalaceae 4.0 3.61 363.66Rhizophoraceae 6.3 19.86 1262.33Rubiaceae 1.7 3.91 943.55Rutaceae 0.3 0.29 336.12Sapotaceae 1.7 0.66 132.92Sterculiaceae 2.3 4.34 748.78Thymelaeaceae 1.7 0.89 215.24Verbenaceae 8.3 5.26 254.08

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Table 3.5 Abundance and basal area of fifteen commonest tree species at Abai


% Total Stems

Basal Area (cm²)

% Total Basal Area

Melastomaceae Kibessia galeata 42 14.0 9723.22 8.05Myrtaceae Eugenia bankensis 34 11.3 7239.14 5.99Elaeocarpaceae Elaeocarpus canipes 25 8.3 8330.86 6.90Verbenaceae Vitex pinnata 24 8.0 5880.19 4.87Anacardiaceae Buchnania insignis 22 7.4 4752.09 3.93Rhizophoraceae Bruguiera sexangula 15 5.0 23558.60 19.51Burseraceae Canarium apertum 12 4.0 3816.70 3.16Polygalaceae Xanthophyllum rufum 12 4.0 4363.96 3.61Apocynaceae Alstonia angustifolia 10 3.3 1810.02 1.50Dilleniaceae Dillenia excelsa 9 3.0 58.15 0.79Annonaceae Polyalthia glauca 9 3.0 3605.57 2.99Moraceae Ficus condensa 8 2.3 17189.74 14.23Euphorbiaceae Baccaurea pubera 6 2.0 1627.68 1.35Clusiaceae Calophyllum borneensis 6 2.0 855.31 0.71Ebenaceae Diospyros pendula 6 2.0 797.93 0.66Total 240 79.6 94509.16 78.25

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Table 3.6 Ten commonest families by percent trees in botanical plots and transects in Sabah

Family I II III IV V VI VII VIII IX X Alangiaceae 1.6 Anacardiaceae 7.7 4.1 3.8 4.1 Annonaceae 2.8 5.8 2.3 5.8 2.8 2.7 2.9 Apocynaceae 3.3 Burseraceae 4.0 3.7 1.7 3.3 2.8 2.9 Clusiaceae 4.3 9.0 Datisaceae 1.9 Dilleniaceae 7.7 Dipterocarpaceae 6.7 26.8 23.7 32.5 37.1 26.1 19.6 17.0 4.9 Ebenaceae 3.6 8.8 5.6 1.6 3.1 5.8 7.8 Elaeocarpaceae 8.3 Euphorbiaceae 13.4 9.4 11.7 13.9 12.2 13.2 21.1 16.8 14.8 Fagaceae 1.9 3.8 Flacourtiaceae 7.6 3.1 5.1 Lauraceae 8.2 8.2 10.8 4.8 6.9 4.1 3.9 2.9 Leguminosae 2.1 2.7 Melastomaceae 14.0 4.0 Meliaceae 4.6 5.3 3.6 3.6 9.1 4.4 2.5 Moraceae 2.5 Myrtaceae 11.3 8.8 3.7 5.2 4.4 2.1 4.6 4.1 4.2 Polygalaceae 4.0 5.8 Rhizophoraceae 6.3 Rubiaceae 8.6 6.7 32.6 Rutaceae 4.4 Sapindaceae 4.6 3.9 4.8 4.0 Sonneratiaceae 11.0 Sterculiaceae 10.2 Tiliaceae 2.9 2.8 8.3 6.5 2.1 Verbenaceae 8.3 Total 71.5 74.2 73.4 84.8 75.5 74.6 68.2 82.1 74.7 87.6 I. Abai (this study)

II. Sukau (this study) III. Sepilok (Davies, 1984) IV. Segaliud-Lokan (Davies, 1984, modified from Fox, 1972) V. Kuamut (Davies, 1984, modified from Fox, 1972)

VI. Kalabakan (Davies, 1984, modified from Fox, 1972) VII. Silabukan (Davies, 1984, modified from Fox, 1972)

VIII. Tabin unlogged (Mitchell, 1993) IX. Tabin logged-adjacent (Mitchell, 1993) X. Tabin logged distant (Mitchell, 1993)

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Table 3.7 Ten commonest families by percent basal area in botanical plots and transects in Sabah

Family I II III IV V VI VII VIII IX X Alangiaceae 2.4 Anacardiaceae 5.5 2.8 1.5 4.0 Annonaceae 2.2 1.7 Apocynaceae Burseraceae 3.3 1.5 1.2 1.6 1.4 Clusiaceae 8.4 Datisaceae 2.9 2.8 Dilleniaceae 2.8 Dipterocarpaceae 10.2 62.9 65.0 66.0 66.0 57.0 64.7 23.8 8.5 Ebenaceae 1.2 4.4 2.4 4.2 6.5 Elaeocarpaceae 6.9 Euphorbiaceae 14.3 2.6 3.0 3.9 4.1 2.9 5.2 5.7 18.7 Fagaceae 1.9 1.3 Flacourtiaceae 3.6 1.6 3.5 Lauraceae 8.4 12.4 9.0 2.4 7.4 1.4 1.5 5.0 Leguminosae 1.9 3.3 1.3 4.1 Melastomaceae 8.1 6.4 Meliaceae 1.4 1.6 5.0 Moraceae 14.7 3.3 1.5 Myristacaceae 22.3 Myrtaceae 6.0 8.9 1.7 3.1 1.6 3.3 Polygalaceae 3.6 Rhizophoraceae 19.9 Rubiaceae 3.9 9.1 1.5 8.8 24.2 Sapindaceae 1.1 1.5 1.4 3.0 Sonneratiaceae 12.4 Sterculiaceae 4.3 2.3 4.9 1.2 2.1 14.3 Tiliaceae 1.3 1.9 1.7 1.3 3.1 2.2 2.6 Theaceae 5.4 Verbenaceae 5.3 1.2 Total 78.2 74.6 89.5 91.8 84.9 89.8 84.9 91.6 81.7 93.5 I. Abai (this study)

II. Sukau (this study) III. Sepilok (Davies, 1984) IV. Segaliud-Lokan (Davies, 1984, modified from Fox, 1972) V. Kuamut (Davies, 1984, modified from Fox, 1972)

VI. Kalabakan (Davies, 1984, modified from Fox, 1972) VII. Silabukan (Davies, 1984, modified from Fox, 1972)

VIII. Tabin unlogged (Mitchell, 1993) IX. Tabin logged-adjacent (Mitchell, 1993) X. Tabin logged distant (Mitchell, 1993)

38

Table 3.8 Summary of phytochemical analyses of plant parts at Lower Kinabatangan

Mature leaves

Young leaves

Flowers Fruits

% Organic Nitrogen

Mean 0.29 0.42 0.28 0.24 Range 0.14-0.73 0.22-0.78 0.16-0.4 0.12-0.41 Std. deviation

0.10 0.14 0.10 0.08

Sample size 97 33 5 18 % Crude Protein Mean 1.84 2.62 1.73 1.50

Range 0.88-4.56 1.38-4.88 1.0-2.5 0.75-2.56 Std. deviation

0.64 0.87 0.62 0.49

Sample size 97 33 5 18 Condensed Tannins (mg/g)

Mean 3.27 1.05 0.26 1.71 Range 0-30.34 0-13.41 0.12-0.47 0-6.7 Std. deviation

6.06 2.41 0.15 1.94

Sample size 97 33 5 18 % Neutral Detergent Fibres

Mean 60.58 56.37 57.72 63.02 Range 34.6-91.5 30.9-89.6 39.2-74 41.6-88.3 Std. deviation

11.64 15.45 14.5 13.07

Sample size 97 33 5 18 Alkaloids 0 91 30 3 5

1+ 2 1 2+ 1 3+ 2 1 4+ Sample size 96 32 3 5

Saponins 0 35 8 1 2 1+ 37 11 2 6 2+ 15 1 1 3+ 3 2 4+ 1 Sample size 91 20 3 11

0: absent; 1+, 2+, 3+, & 4+: positive reactions (semi-quantitative analysis)

39

Table 3.9 Comparison of mean levels of nitrogen, protein, condensed tannin and neutral detergent fibre in mature and young leaves of the same species (n=32)

Mature leaves Young leaves Mean Std.

deviation Mean Std.

deviation % Organic Nitrogen 0.30 0.10 0.42 0.14 % Crude Protein 1.90 0.62 2.62 0.88 Condensed Tannins (mg/g) 2.94 5.40 1.07 2.44 % Neutral Detergent Fibres 57.87 11.10 55.33 14.47

Figure 3.1 Mean monthly maximum and minimum temperatures for 1990 and 1991

0

5

10

15

20

25

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Jan-

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91

Oct

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Nov

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Dec

-91

Tem

pera

ture

(in

Cel

sius

)

Months

Minimum Maximum

40

Figure 3.2 Monthly rainfall for 1990 and 1991

Figure 3.3 Klimagraph for 1990 and 1991

0

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Aug

-91

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91

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-91

Tot

al R

ainf

all (

in m

m)

Months

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1000

Jan-

90

Feb-

90

Mar

-90

Apr

-90

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91

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Mar

-91

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May

-91

Jun-

91

Jul-9

1

Aug

-91

Sep-

91

Oct

-91

Nov

-91

Dec

-91

Temperature (˚C) Rainfall (mm)

Transitional period

Wet period

Dry period

50

41

Figure 3.4 Frequency distribution of girths at breast height of transect trees at Sukau (n=1378)

Figure 3.5 Number of tree species against the number of trees sampled in the transects at Sukau (n=1,378)

0

0

1

1030

-39

40-4

950

-59

60-6

970

-79

80-8

990

-99

100-

109

110-

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120-

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130-

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149

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159

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% tr

ees

GBH (cm)

1

100

0

20

40

60

80

100

120

0 200 400 600 800 1000 1200 1400

Cum

ulat

ive

num

ber

of sp

ecie

s

Number of tree stems

42

Figure 3.6 Phenological patterns at Sukau (n=500)

Figure 3.7 Frequency distribution of girths at breast height of transect trees at Abai (n=300)

1

10

100

Mar

-90

Apr

-90

May

-90

Jun-

90

Jul-9

0

Aug

-90

Sep-

90

Oct

-90

Nov

-90

Dec

-90

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91

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91

Mar

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Apr

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91

Jul-9

1

Aug

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Dec

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% tr

ees

Months

Young leaves Flowers Fruits

0.1

1

10

100

30-3

940

-49

50-5

960

-69

70-7

980

-89

90-9

910

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911

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912

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913

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931

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940

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941

0-41

9

% tr

ees

GBH (cm)

43

Figure 3.8 Number of tree species against the number of trees sampled in the transects at Abai (n=300)

Figure 3.9 Phenological patterns at Abai (n=300)

0

5

10

15

20

25

30

35

40

45

0 50 100 150 200 250 300

Cum

ulat

ve n

umbe

r of

spec

ies

Number of tree stems

1

10

100

Mar

-90

Apr

-90

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-90

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0

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1

Aug

-91

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91

Oct

-91

Nov

-91

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% tr

ees

Months

Young leaves Flowers Fruits

44

1 = Abai 2 = Sukau 3 = Sepilok 4 = Segaliud-Lokan 5 = Kuamut 6 = Kalabakan 7 = Silabukan 8 = Tabin

Figure 3.10 Location of botanical plots and transects in Sabah

Figure 3.11a Mean levels of crude protein in plant parts analysed

0

0.5

1

1.5

2

2.5

3

Mature leaves Young leaves Flowers Fruits

%

Plant parts

45

Figure 3.11b Mean levels of condensed tannins in plant parts analysed

Figure 3.11c Mean levels of neutral detergent fibre in plant parts analysed

0

0.5

1

1.5

2

2.5

3

3.5


mg/

g

Plant parts

52

54

56

58

60

62

64


%

Plant parts

46

CHAPTER 4: SOCIAL ORGANISATION AND BEHAVIOUR

4.1 INTRODUCTION It was not until recently that long-term studies made available information concerning

the social behaviour of N. larvatus. Earlier observations gave conflicting reports. Studies conducted in Brunei Bay (Kern, 1964; Macdonald, 1982) and in East Kalimantan (Jeffrey, 1979) reported N. larvatus living in loosely organised multi-male troops that mixed and separated frequently. Another study in Sabah (Kawabe & Mano, 1972), however, reported that multi-male groups were highly integrated and cohesive.

More recent studies carried out at Samunsam Wildlife Sanctuary in Sarawak (Bennett, 1986a; Bennett & Sebastian, 1988; Rajanathan & Bennett, 1990) and at Tanjung Puting National Park in Kalimantan (Yeager, 1989; 1990a & b; 1991a; 1992) showed that N. larvatus has a flexible social structure. The basic social unit is a harem (see Kavanagh, 1983 for definition) comprising one adult male, several adult females, and their offspring (Bennett, 1986a; Bennett & Sebastian, 1988; Yeager, 1989; Rajanathan & Bennett, 1990). Young juvenile males leave their natal group and join loosely bonded all-male groups (Bennett, 1986a; Bennett & Sebastian, 1988; Yeager, 1989; Rajanathan & Bennett, 1990). Furthermore, there seem to be two levels of social organisation, the harem and the band (Yeager, 1989; 1991a).

The aim of this chapter is to describe and compare the social organisation and behaviour of N. larvatus in different habitats in the Lower Kinabatangan region, including any influences of the habitat.


4.2.1 SOCIAL ORGANISATION

4.2.1.1 SIZE AND COMPOSITION OF N. larvatus GROUPS Throughout the study, six harem, one all-male and two non-breeding (section 2.10)

groups were consistently recognised using individually distinctive animals as markers (table 4.1). The harem groups averaged 17 individuals per group, and ranged from 14 to 20 individuals per group. The adult sex ratio of the harem groups was 1:7.3 (see table 2.1 for definitions of age/sex categories). They were relatively stable over time and none were observed with more than one adult male.

The three non-harem groups (all-male and non-breeding groups) averaged nine individuals per group and ranged from eight to ten individuals per group. Non-harem groups frequently changed their membership. There were, however, some groups whose membership was consistent over a long period. Group SU7, for example, remained unchanged throughout the study (15 months). Furthermore, it had two female members, a juvenile-1 and an infant-2. Another non-breeding group, SU9, also had two female members that remained with the group for at least seven months.

Throughout the study, solitary N. larvatus of both sexes were encountered on 22 occasions. This was recorded when an individual was more than 20m from the nearest conspecific. Adult males comprised 73%, adult females 5%, sub-adult males 18% and sub-

47

adult females 5% of all solitary observations. Twice, an adult female and once, a sub-adult female, were also briefly seen associating with all-male groups. These associations normally did not last more than a few days.

4.2.1.2 CHANGES IN COMPOSITION OF SU1, THE FOCAL GROUP SU1 was first identified in August 1990, and was observed every month until

December 1991 (table 4.2). The group size of SU1 averaged 21 and the adult sex ratio was 1:8.4, varying from eight to nine adult females. Changes in group membership occurred during the study, but not all changes were determined because not every member of SU1 was recognised. Most changes in age/sex composition of SU1 can be attributed to the re-classification of younger animals as they grew older. The adult male Tukkae, two adult females Martina and Choon, and their offspring, Lucy and Pe-pex remained with the group throughout the study. All these individuals were observed within SU1 during the author’s visit to the study area in November 1992.

By November 1990, the group size reduced to 19 individuals when a juvenile-1 male, Stanley, left the group. This presumably occurred when he became a juvenile-2. In February 1991, an adult female Martina, was observed with an infant-1 female, Lucy. Martina most likely gave birth to Lucy in either late January or early February. This increased the group size to 20 individuals. In March 1991, there was another newborn in the group, increasing the size to 21 individuals.

By April 1991, another infant was born to the group, and this increased the group size to 22 individuals. Between April and September 1991, SU1 was reduced to 20 individuals when it lost an adult female, two sub-adult females and one juvenile-2 female. It was not known what happened to them. It was possible that a sub-adult female had departed from the group in August (section 4.2.2.1). There were also two newborns to the group.

SU1 again increased to 22 individuals in October 1991 when two sub-adult females from unknown harem/harems joined SU1 (section 4.2.1.6.). This was the only evidence of female transfer between groups at Sukau. There was, however, a possibility that the two sub-adult females could be the same individuals that left SU1 between April and September 1991, as there were distinguishing marks on them. In November 1991, there was another newborn to SU1, increasing the group size to 23 individuals.

4.2.1.3 GROUP SPREAD It was difficult to estimate the spatial distribution of N. larvatus groups in the forest

because of limited visibility. Group spread was estimated only when groups were roosting by the river. The average group spread of harems was 13.2m (n=396, range 3-50m). Non-harem groups had a similar average spread at 13.1m (range 2-35m, n=73). Although average group spread was similar, the average group size of harem was almost double that of the non-harem group (section 4.2.1.1). Thus, non-harem groups were not as cohesive as harems.

4.2.1.4 INTRA-GROUP ASSOCIATIONS Details of social organisation of SU1 were assessed from the percent time an

individual was nearest to the subject (table 4.3). The expected percent time for which an individual would have been nearest to the subject if all members of SU1 were associating randomly was determined from the average composition of SU1 throughout the study. Chi-square tests were not performed because data were not statistically independent. Results can be summarised as follows:

48

1. The adult male spent more time than expected near to the adult females but less time than expected near to all the other age/sex classes;

2. Adult females spent more time than expected near to the juvenile-1s and infants, but less time than expected to all other age/sex classes;

3. Sub-adult females spent more time than expected near to the adult male and adult females, but less time than expected to all other age/sex classes;

4. Juvenile-2s spent more time than expected near to the adult male, adult females and other juvenile-2s, but less time than expected to all other age/sex classes;

5. Juvenile-1s and infants spent more time than expected near to the adult females, but less time than expected to all other age/sex classes.

Thus, observed combinations show that associations between any two members were not at random but specific.

4.2.1.5 INTRA-GROUP SPACING Intra-group spacing was assessed by finding the distance of the subject to its nearest

neighbour (figures 4.1a & b), and recording the number of other individuals within 2.5m (figures 4.2a & b) and 5m (figures 4.3a & b) of the subject (Struhsaker, 1975; 1980; Oates, 1977b; Struhsaker & Leland, 1979; Bennett, 1983). The results are summarised as follows:

1. The adult male was less than 1m from any other individual for more than 50% of the time. Most of that time was spent close to an adult female.

2. Each adult female spent over 90% of her time within 2m of another individual. Excluding adult females with clinging infants, each adult female spent about half her time within 1m of another individual. This was less than the adult male.

3. Each sub-adult female and juvenile-2 spent 62.3% and 58% of the time respectively within 1m of another individual. They were more gregarious than either the adult male or the adult females.

4. Juvenile-1s and infants (infant-1s and infant-2s) spent more than 75% of the time near another individual. Each infant was less than 1m from any other individual more than 95% of the time. This was because they rarely ventured more than 2m from an adult female.

Although SU1 had a large membership, it formed a cohesive group, with small inter-individual distances. The adult male was equally gregarious to adult females.

4.2.1.6 INTER-GROUP ASSOCIATIONS Different groups frequently come together to spend the night next to the rivers

(Bennett & Sebastian, 1988; Rajanathan & Bennett, 1990; Yeager, 1991a & b). SU1 spent 60.4% and 68.8% of its nights within 50m and 100m respectively of another group (figure 4.4). SU1 spent more nights within 100m of a non-harem group (57.3%) than with another harem (54.2%). The non-harem groups probably followed SU1 or other harems that associated with SU1. A non-harem group followed SU1 from their sleeping trees on 77 out of 93 complete and incomplete full-day follows. When neighbouring groups could be identified with certainty, SU1 spent most nights close to harem group SU2 (39.6%) and non-harem group SU7 (45.8%). These associations suggest a secondary level of social organisation, the band, with fission-fusion of stable harems within bands (Yeager, 1989; 1991a; 1992).

49

More than one group frequently slept near SU1 at night (figure 4.5), and twice four groups were recorded near SU1. Once, seven unidentified groups came together along a 150m stretch of the Menanggul River. When SU1 slept by the Kinabatangan River, there were other N. larvatus groups on the opposite bank on almost all nights. Groups on opposing banks frequently displayed to each other.

SU1 frequently met with other groups during the day and occasionally travelled together. Most (62.5%) of the encounters during the day were with a non-harem group (n=16). The non-harem group frequently (82.8%, n=93) followed SU1 from their sleeping sites and occasionally (20%, n=10) upon an encounter in the forest. On four of the 53 complete full-day follows, SU1 travelled together continuously with two harem and two non-harem groups. Each association lasted for two days. During the first association, SU1 travelled with SU2, SU3, SU7 and SU9. During the second association, groups that travelled with SU1 were SU7, two unknown harems, and an unknown all-male group. In both instances, the non-harem groups followed the harems.

To test whether groups were attracting or avoiding each other, the expected number of inter-group encounters by the rivers over the study period was calculated from the density of groups and the mean distance travelled each day, assuming that groups were ranging through the forest at random (Waser, 1976). The expected number of inter-group encounters per day was equal to: 4 / 2 , where p=number of groups per km², v=mean day range length (km), d=distance between groups, and s=group spread.

The observed and expected number (table 4.4) of inter-group encounters, when conspecific groups came within 50m and 100m of SU1, had the groups been moving at random was significantly different (χ²=0.31, df=2, p<0.95), implying that groups were attracting one another. Similarly, there was a significant difference when SU2 only, was within 50m and 100m of SU1 (table 4.4). There however, were no significant differences when harems only, non-harems only and SU7 only, were within 50m and 100m of SU1 (table 4.4).

4.2.2 SOCIAL BEHAVIOUR

4.2.2.1 AGONISTIC BEHAVIOUR Members of SU1 spent only 0.8% (n=34) of their total activity time (figure 4.6) in

agonistic behaviour (see table 2.3 for definition). Almost 30% of this was directed to other groups, mainly towards non-harem groups (table 4.5). SU1 was also more tolerant of other harems compared to non-harem groups (section 4.2.1.6). Most of the adult male’s aggression was directed outside the group, whereas most of adult females’ aggression was directed either inside the group or to the observer.

Agonistic behaviour exhibited by the adult male towards other groups was usually part of a display repertoire. During displays, the adult male stands on all four limbs and gives open-mouth threats usually accompanied by deep short honking sound. Then suddenly, with a loud roar, he leaps through the foliage and lands on a tree branch several meters away. Almost invariably and seemingly deliberately, he lands on a weak or dead tree branch, which then breaks loudly, adding to the general uproar.

Almost all aggression exhibited by the adult male towards members of his group comprised open-mouth threats. Once, in August the adult male was observed chasing a sub-adult female from the roosting tree. The sub-adult female escaped to a nearby tree and roosted there. The only other group nearby was an unidentified all-male group. The sub-adult female was not observed in SU1 after some days.

50

All agonistic interactions during scan observations between adult females were over sleeping sites, with one female displacing the other. The displacer was sometimes seen grabbing the fur on top of the displaced’s head. In all incidences, the sleeping sites were the terminal branches of trees that overhung the river. This implied a dominance hierarchy among the females of a harem, but its establishment and maintenance are not known until the individuals are identified and more observations are made.

4.2.2.2 GROOMING Grooming (see table 2.3 for definition) comprised 6.1% of SU1 total activity time

(figure 4.6), of which 46% (n=115) was allogrooming. All age/sex classes except the adult male were involved in allogrooming (table 4.6). Almost 65% of all allogrooming occasions were by an adult female grooming a juvenile or an infant (figure 4.7). Adult females were also the foci of all allogrooming activities. They did most of the grooming and received a fair amount of grooming themselves.

4.2.2.3 SEXUAL BEHAVIOUR Eight copulatory bouts in different groups were recorded at Sukau throughout the

study (table 4.7). Copulations in SU1 were recorded four times, twice during scan observations. Weighted scans showed that copulations made only 0.1% of SU1 annual activity budgets (figure 4.6). All copulations consisted of a single mount, and averaged 25 seconds (range 10-40 seconds).

Typically, the adult female approached the adult male, presented her hindquarters in a quadrupedal position with slightly flexed legs and arms, and tail to one side. The male mounted the female from the rear, grasped her hips with his hands, and rested his feet on the supporting tree branch. This was followed by repeated thrusting movements by the male. During copulation, the female maintained a pouted face and pursed lips, and occasionally looked back at the male. A brief pause marked the end of the copulatory bout. The pair separated to at least a metre away after the male dismounts. After separation, both the male and female shuddered briefly.

In all five cases when solicitations were observed with certainty, the adult female was the solicitor. Solicitations by the female began with a sexual gesture, which involved looking at the male with a pouted face, eyelids half closed, chin up and out, lips pursed forward, and occasionally shaking her head from side to side. Harassments of the mating pairs were seen five times but none was successful. Infant-2s and juvenile-1s were the only age/sex classes observed harassing the mating pairs. This included agitated movements, usually accompanied with “screech” vocalisations near the mating pairs. Often they would climb the pair and grab the male’s nose or other parts of his body (table 4.7).

A non-sexual mount in N. larvatus was observed once (table 4.7). An adult female from SU5 bounced from one tree branch to another and then started gesturing as described above. Another adult female of the same group, about 4m away, on the same tree, then similarly gestured but did not bounce from branch to branch. The first female proceeded towards the second female and presented her hindquarters. The second female mounted the first and began thrusting movements, which lasted for two seconds. Both the females frequently looked at the harem male on another tree, about 13m away from the moment the first female started gesturing. The first female still gesturing, proceeded towards the adult male and presented her hindquarters to him. He mounted her and began copulation, which lasted for ten seconds.

51

4.2.2.4 BIRTHS Infant-1s were present throughout most of the study (figure 4.9), with apparent birth

seasons from February to April 1990, and from July to October 1990. Although the birth seasons in 1991 were not as apparent, they were from January to March, and from June to December. The birth seasons in 1991 were earlier than in 1990. Furthermore, the second birth season of 1991 was prolonged. Similarly, data for SU1 (section 4.2.1.2) showed obvious birth seasonality in 1991, from February to March and from August to November. There was no correlation between births and rainfall (rs= -0.19, n=23, p>0.05).

The gestation length of N. larvatus is not known. In Semnopithecus entellus, another Asian colobine of similar body weight, it is 200 ± 10 days (Harley, 1985; Newton, 1987). Gestation length in other Asian colobines may be similar (Struhsaker & Leland, 1987). If gestation length of N. larvatus is indeed similar, then matings in 1990 and in March 1991 should result in the presence of newborns in December 1990, March, May and October 1991 respectively. The prediction for December 1990 was earlier than observed. More mating records are needed to estimate the gestation length of N. larvatus.

4.2.2.5 ALLOMOTHERING Allomothering (see table 2.3 for definition) was observed with certainty only in four

instances, of which two were observed during scan observations. Weighted scans showed that it occupied only 0.1% of the total activity budget of SU1 (figure 4.6). In the first instance, an adult female snatched an infant-2 from another female of the same group. The second female did not put up much resistance. The first female with the infant-2 climbed three metres above the second female and sat. About 30 seconds later, the second female climbed to the first female and took the infant back. The infant-2 screeched and whimpered from the moment it was taken away until the second female took it back.

The second instance involved a juvenile-2 female that took an infant-1 from an adult female, and held it for about five minutes. The only resistance was from the infant, who screeched throughout. The adult female ignored the infant’s scream and groomed another adult female. In the third instance, a juvenile-1 was embracing an infant-1 and attempted to carry it. No resistance was put up by the infant. In the fourth instance, an adult female was observed grooming an infant-1 while the infant was clinging to another adult female. In general, the relationship between infants and adult females carrying them could not always be determined. Thus, there could have been more instances of allomothering involving adult females.

4.2.2.6 PLAY Only juveniles and infants were observed to play (see table 2.3 for definition). Of

their total play time, infants spent more than 60% playing alone (table 4.8). Play frequently involved dangling from branches by one arm, spinning around, dropping several feet onto another branch, and clambering up again.

By contrast, juvenile-1s spent more than 50% of that time in social play, mainly with their peer group. During social play, the young animals chased each other through the branches and frequently wrestled among themselves.

4.2.2.7 VIGILANCE Members of SU1 spent 27.8% (n=180, weighted scans) of their annual activity budget

in vigilance (figure 4.6). This activity was recorded when the subject was scanning its surroundings or when it was looking at objects that were more than 5m from the subject, including the observer (figure 4.8). Bennett (1983) and Kavanagh (1977; 1980) scored this

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activity when the subject was scanning a visual field that was more than 5m from the subject but that did not include the observer. In this study, the observer was included because the animals frequently looked at the observer while on the boat. Furthermore, the study animals would flee if the boat was too close to them or when the observer on foot was spotted in the forest (section 2.8).

Different age/sex classes of SU1 spent different proportions of their time in vigilance (figure 4.10). Sub-adult females spent more than half their total activity time being vigilant. It was uncertain whether sub-adult females spent more time at vigilance than other age/sex classes or whether this was due to a low sample size (n=33). The adult male spent more time in vigilance than did adult females. Monthly, there was no significant difference in the time the adult male and adult females spent at vigilance (Wilcoxon T=5.17, n=12, p>0.01).

There was a negative correlation between the percent of time members of SU1 spent monthly in vigilance and in travelling (rs=-0.657, n=12, p<0.05). This was most likely because travelling required a certain amount of alertness from the individuals. A comparison between the monthly pattern of vigilance and phenology showed a negative correlation with flower production (rs=-0.587, n=12, p<0.05). This suggested that members of SU1 spent more time searching for flowers when they were rare. There were no correlations with young leaf and fruit production.

The factors affecting the varying amount of vigilance are not clear when analysed monthly. Thus, a comparison between the percent time spent at vigilance was compared with day range length, the amounts of young leaves, flowers and fruits plus seeds in the diet for that day. A negative correlation existed between vigilance and day range length (rs=-0.213, n=64, p<0.05). Daily, there were no correlations between vigilance and food items in the diet.

Using partial correlations, the percent of time that members of SU1 spent in vigilance each day was compared with the proportion of young leaves, flowers and fruits plus seeds in the diet that day, keeping the day range length constant. There was a significant positive correlation between vigilance and flowers in diet (Txyz=0.304, n=64, p<0.05). This suggested that members of SU1 increased their vigilance to locate rare food items, as different items vary in their rarity (section 3.2.2.3). A significant negative correlation, however, existed between vigilance and fruits plus seeds in diet (Txyz=-0.044, n=64, p<0.05). This suggested that members of SU1 spent less time at vigilance when there were more fruits plus seeds in their diet, probably to maximise feeding on rare food items.

Although potential predators existed in the area (section 4.5.1), it was unlikely that changes in the proximity of predators was a factor affecting the varying amount of time spent by members of SU1 in vigilance from day to day. It was, however, not possible to prove this under the conditions of this study.

4.3 ABAI STUDY AREA

4.3.1 SOCIAL ORGANISATION

4.3.1.1 SIZE AND COMPOSITION OF N. larvatus GROUPS Throughout the study, only one harem, AB1, was consistently recognised over time. It

had 18 members when first identified, comprising an adult male, eight adult females, two juvenile-1 males, two infant-2 males, an infant-2 female and four infant-2s of unknown sex. Repeated observations (n=324) along twelve kilometres of Merah River showed that harems averaged 14.6 individuals (range 8-22). The adult sex ratio was 1:7.1.

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There were three occasions when a sub-adult male was seen with a harem. A similar observation was made at Samunsam Wildlife Sanctuary (Rajanathan & Bennett, 1990). It was likely that those sub-adult males were the harem males’ offspring, which for unknown reasons remained with the harems. A more detailed study, however, is required to confirm this.

All-male groups at Abai averaged 6.4 individuals (n=54, range 4-9). Occasionally, they were observed with two or more fully adult males (n=8). Typically, all-male groups at Abai comprised an adult male, several sub-adult and juvenile males. During the study, solitary N. larvatus were encountered only four times. A solitary adult male was seen twice, a sub-adult female once and a juvenile-2 male once. Once, an adult female with a clinging infant-2 was seen to associate with an all-male group for a day.

In July 1991, an adult male N. larvatus was released by the staff from the Sabah Wildlife Department and me at the mouth of the Merah River. It had been captured wandering in a sawmill in Sandakan Bay. It was retained and quarantined at Sepilok Orang-utan Rehabilitation Centre in Sandakan for three months before release. At time of release, it had been tattooed on its right cheek (figure 4.11) and dyed along its back with a non-permanent black dye. It was not observed again until about four months later close to where it was first released, and near an unknown all-male group. There was a difficulty in determining whether it had joined the non-breeding group, as it was not seen again by the time the study ended. In general, it had a relatively healthy appearance.

4.3.1.2 GROUP SPREAD Group spread was estimated at dawn and before dusk when the animals were in their

sleeping trees by the river. Harems’ group spread averaged 12.2m (range 4-50m; n=162). Conversely, the group spread of all-male groups averaged 9.8m (range 4-25m; n=48). Although the group spread of all-male groups were smaller, their group sizes were also smaller. Thus, harems were more cohesive than all-male groups.

4.3.1.3 INTRA-GROUP ASSOCIATIONS Details of social organisation of harems at Abai were assessed from the percent time

an individual was nearest to the subject (table 4.9). The expected percent time for which an individual would have been nearest to the subject if all members of harems were associating randomly was determined from the average composition of harems throughout the study (section 4.2.1.4). Results can be summarised as follows:

1. The adult male spent more time than expected near to the adult and sub-adult females but less time than expected near to all the other age/sex classes;

2. Adult females spent more time than expected near to the juvenile-1s and infant-2s, but less time than expected to all other age/sex classes;

3. Sub-adult females spent more time than expected near to the juvenile-2s, but less time than expected to all other age/sex classes;

4. Juvenile-2s spent more time than expected near to the other juvenile-2s and juvenile-1s, but less time than expected to all other age/sex classes;

5. Juvenile-1s spent more time than expected near to the adult females and other juvenile-1s, but less time than expected to all other age/sex classes;

6. Infants spent more time than expected near to the adult females, but less time than expected to all other age/sex classes.

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4.3.1.4 INTRA-GROUP SPACING Intra-group spacing of harems was assessed by finding the distance of the subject to

its nearest neighbour (figures 4.13a & b), and recording the number of other individuals within 2.5m (figures 4.14a & b) and within 5m (figures 4.15a & b) from the subject (section 4.2.1.5). Observations, however, were limited to the riverside (section 2.10). Summarising, the findings were:

1. The adult male was less than 1m away from any other individual for more than 50% of the time. He spent almost 100% of his time within 2m from another individual.

2. Each adult female spent over 90% of her time within 2m of another individual. Each adult female without a clinging infant spent more than 40% of her time within 1m of another individual. This was less than the adult male.

3. Each juvenile-2 spent more than 60% of its time within 1m of another individual. Each juvenile-1 and infant spent most of their time within 1m of another individual.

When harems at Abai were by the river, they were cohesive units. Furthermore, unlike many harem-dwelling species, the adult male was not spatially separated. The inter-individual distance, however, could be erroneous for scarcity of complete daylight observations.

4.3.1.5 INTER-GROUP ASSOCIATIONS Different groups frequently come together to roost by the rivers (section 4.2.1.6).

Each harem at Abai spent most of its nights alone (80%), when there were no other groups within 100m of it (figure 4.16). Once, two harems were observed roosting in a single large tree. Initially, it was difficult to distinguish the two harems when they entered the tree to feed on leaf buds. There was no other foliage on the tree, so visibility was good. The two harem males were at least 1m from each other and no agonistic behaviour was observed between members of the two harems. By dusk, the two harems moved to opposite sides of the tree, separated by about 5m.

More than two groups occasionally slept near each other at night (figure 4.17). This was mainly observed along the Kinabatangan River, where the river bends. There was usually a clumping of standing trees, mainly Sonneratia alba (Lythraceae) at these bends. N. larvatus feeds on young leaves, unripe fruits, seeds and flowers of this species (section 5.3.1). A test (section 4.2.1.6) to see whether groups were avoiding each other could not be carried out because the day range length of N. larvatus groups could not be determined (section 6.3).

4.3.2 SOCIAL BEHAVIOUR

4.3.2.1 AGONISTIC BEHAVIOUR Members of each harem spent 0.7% (n=5, weighted scans) of their total activity time

in agonistic behaviour (figure 4.18). Three of these agonistic interactions were between adult females. All three interactions were over sleeping sites (section 4.2.2.1). In the fourth case, the aggressor was also an adult female but the recipient was a juvenile-2 female. The context of aggression was not known. In the fifth, a juvenile-1 gave an open-mouthed threat towards the observer (figure 4.12).

Once, an adult male from a harem chased an adult female of another harem that was close to his group. The adult male stopped a short distance (approximately 1.5m) before reaching the second harem. He sat for a few seconds and then returned to his own group. On another occasion, an adult male of one harem rushed through a neighbouring harem creating

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uproar in both harems. The adult male from the second harem chased the first male back to his own group. Both males gave short barks and open-mouthed threats that lasted for several seconds. The second male then returned to his own harem. Once, during a display an adult male from one harem suddenly leapt through Nypa fruticans (Arecaceae) and broke two of the fronds, creating uproar in both harems. He, however, fell head first into the water, but quickly clambered up. The two harems were quiet after that.

4.3.2.2 GROOMING Members of each harem spent 5.1% of their total activity time grooming (figure 4.18).

Social grooming, however, occupied only 33.3% (n=16) of this. All age/sex classes except the harem males were involved in social grooming (table 4.10). More than 80% of all grooming occasions were performed by an adult female grooming juvenile-1s or infants. Adult females were also the foci of social grooming, being groomed by other adult females and juvenile-2s.

4.3.2.3 SEXUAL BEHAVIOUR No copulations were recorded during the study. This was mainly due to the observer’s

failure to follow the study animals throughout the daylight hours. Non-sexual mounting was recorded once, when a juvenile-1 of unknown sex mounted an infant-2 male.

4.3.2.4 BIRTHS Infant-1s were present throughout most of the study, with a major peak in September

1990, and minor ones in January, June and December 1991 (figure 4.19). There were no data for July 1990 and February 1991. This was because I was infected with viral fever in the former and in the latter, surveys were not carried out because of thunderstorms. The August to November 1990 birth season was during a wet period (figure 3.4). The peaks in January and December 1991 coincided with peak rains, and the one in June 1991 was also during a wet period. No correlations, however, existed between births and monthly rainfall (rs=-0.17, n=21, p>0.05).

4.3.2.5 ALLOMOTHERING Allomothering was observed only once when a juvenile-1 female carried an infant-1

for a short distance. The infant did not put up any resistance. The juvenile with the clinging infant rushed towards an adult female when some commotion within their group occurred for unknown reasons. The adult female took the infant from the juvenile.

4.3.2.6 PLAY Subjects were seen playing alone for more than 40% of the total play time (table

4.11). Infant-2s played with both juveniles (juvenile-1s and juvenile-2s) and infants (infant-1s and infant-2s). By contrast, juvenile-1s spent almost 70% of play time with their own peer group. Adults were not observed to indulge in play.

4.3.2.7 VIGILANCE Members of each harem spent 30% (n=263) of their total activity time engaged in

vigilance (figure 4.18). Adult females spent more time in vigilance than harem males. Monthly, there was no significant difference in the time the harem males and females spent in vigilance (T=4.50, n=8, p>0.1). No correlations were made for the daily basis due to lack of complete day observations.

Comparison between vigilance and phenological patterns monthly showed a negative correlation with flower production (rs=-0.595, n=8, p<0.05). No conclusions can be made,

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however, due to lack of complete day observations. For similar reasons, partial correlations were not attempted.

4.4 COMPARISON BETWEEN SITES At both Sukau and Abai, the social structure of N. larvatus was flexible, and the basic

social unit was a harem, comprising one adult male, several adult females and their offspring. This was similar to findings at Samunsam (Bennett, 1986a; Bennett & Sebastian, 1988; Rajanathan & Bennett, 1990) and Tanjung Puting (Yeager, 1989; 1990a & b; 1991a; 1992). Along with similarities, there were also differences between sites (table 4.12).

Foremost, compared to the other three sites, the average harem size was greater at Sukau, larger than those previously reported. The adult sex ratio was similar between Sukau and Abai, but both being much higher than at Samunsam and Tanjung Puting. Only at Abai and Samunsam were there observations of sub-adult males with harem groups. In all sites except Abai, it was common to see groups within 100m of each other at sleeping sites.

The average size of non-harem groups at Sukau was similar to that at Tanjung Puting. The group spread, however, was variable. Only at Sukau was there evidence that non-harems were stable over time. One of the major differences between sites was that the non-harem groups at Sukau were relatively stable over time and that they were often seen with more than two adult males. Furthermore, some non-breeding groups had young female members that remained with the group over time. Except at Abai, different groups frequently came together, particularly to sleep next to rivers at night. Data for Sukau and Tanjung Puting showed that some groups associated more than others. Furthermore, groups at Sukau often travelled together throughout the day.

There were many similarities between SU1 at Sukau and harems at Abai in the percent time spent in various social activities. Although this suggests that N. larvatus in different habitats have similar activity budgets, no conclusion can be drawn until data on complete day observations are available.

4.5 DISCUSSION

4.5.1 SOCIAL ORGANISATION The social structure of N. larvatus in the Lower Kinabatangan is flexible and consists

of relatively stable harem, all-male and predominantly male non-breeding groups. Previous recent studies also show harems were relatively stable over time (Bennett, 1986a; 1991; Bennett & Sebastian, 1988; Yeager, 1989; 1990a; 1991a; 1992). N. larvatus groups at Sukau exhibit inter-group associations that show a secondary level of social organisation, the band, with fission-fusion of stable harems within bands. Groups SU1, SU2 and SU7 exhibit preferences in their association patterns, particularly at sleeping sites. Certain groups were never observed in association even though there were large home range overlaps and frequent changes in sleeping site location. The association of N. larvatus groups at sleeping sites at Abai was less than other sites possibly due to scarcer food. It might also be due to the site having lesser big sleeping trees. Much of Merah River is lined with extensive stands of Nypa fruticans (Arecaceae). These inter-group associations were also observed at Tanjung Puting National Park (Yeager, 1989; 1991a; 1992).

This is in contrast with earlier reports of multi-male groups (Kawabe & Mano, 1972; Macdonald, 1982; Salter et al., 1985). These discrepancies are most likely due to the shorter duration of earlier studies. Earlier studies may have mistakenly assumed the association between various groups as a single multi-male group (Yeager, 1990a). Furthermore, the

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presence of two or more adult males, the presence of young females, and the brief association of adult females with clinging infants in non-breeding groups may also have contributed to this mistaken assumption.

The difference in average harem size of N. larvatus between sites could be due to differences in food availability. If so, the larger group size at Sukau suggests greater food availability (Wilson, 1975), larger size of food sources (Clutton-Brock & Harvey, 1978), and large clumped food sources (Struhsaker, 1975; Struhsaker & Leland, 1979). The association of different groups of N. larvatus, indicative of a secondary level of social organisation might be an aggregation to exploit large food sources that are very unpredictable, both in space and time (Homewood, 1976; 1978).

Past hunting pressure may also be another reason for the lower group size at Samunsam (Bennett, 1986a; Bennett & Sebastian, 1988). There was negligible hunting pressure on N. larvatus at the other three sites. As an adaptive response, hunting should lead to larger group sizes through increased vigilance and/or reduce the probability of being captured (see discussion on predation pressure below). In the short term, hunting would reduce group sizes. Hunting at Samunsam, however, largely stopped about six years before Bennett’s (1986a) study was conducted. Thus, other factors could be influencing group size at Samunsam.

It is possible that the presence of predators might also influence group size (Crook & Gartlan, 1966; Eisenberg et al., 1972; Altmann, 1974; van Schaik & van Hooff, 1983). A larger group may reduce the rate of predation by increasing the efficiency with which predators are detected through increased vigilance (Crook, 1970a; 1972; Alexander, 1974; Treisman, 1975a & b; Clutton-Brock & Harvey, 1977a; Bertram, 1980; van Schaik & van Hooff, 1983; van Schaik et al., 1983; Terborgh, 1983; Pulliam & Caraco, 1984; Dunbar, 1988; Krebs & Davies, 1993).

Alternatively, a larger group size may reduce each individual’s chances of being taken by the predator by dilution effect (Hamilton, 1971; Dunbar, 1988; Krebs & Davies, 1993). Data for predation on Danaus plexippus (Calvert et al., 1979) and Halobates robustus (Foster & Treherne, 1981) show that predation rate is inversely related to colony size, so any disadvantage of greater conspicuousness in a large roost is outweighed by the advantage of dilution.

Although predation on N. larvatus was not observed during the study, its potential predators existed in the study areas: Neofelis nebulosa, Crocodylus porosus and Python reticulatus. In mid-1992, a N. nebulosa with a freshly killed adult male at Sukau was seen and photographed (J.C. Prudente, pers. comm.). Once during the study, also at Sukau, a low-flying Spilornis cheela visibly disturbed a harem, causing its members to scramble to the lower tree branches and give distress vocalisations. The influence of predators on the group size of N. larvatus can only be assumed until quantified data on predation pressure are made available. Compared to African forests (Busse, 1977; Struhsaker & Leland, 1979), predation rates on South-east Asian primates are extremely low (Bennett, 1983).

The presence of two or more adult males in all-male and non-breeding groups reflects a high degree of tolerance between individuals. It also reflects a low male mortality rate, suggesting food abundance and/or lack of predation and hunting pressures.

4.5.2 DISPERSAL Male emigration from natal groups is common and well-documented in many primate

species: Macaca mulatta (Boelkins & Wilson, 1972), M. fuscata (Sugiyama, 1976), M.

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fascicularis (van Noordwijk & van Schaik, 1985), M. nemestrina (Caldecott, 1986), M. sinica (Dittus, 1979), Papio anubis (Packer, 1979), Theropithecus gelada (Dunbar, 1980), Cercopithecus aethiops (Henzi & Lucas, 1980; Cheney & Seyfarth, 1983; Horrocks, 1986), Procolobus [badius] rufomitratus (Marsh, 1979b), P. [badius] tephrosceles (Struhsaker & Leland, 1987), Presbytis melalophos (Bennett, 1983), N. larvatus (Bennett & Sebastian, 1988; Yeager, 1990a), Hylobates klossii (Tilson, 1981), H. lar (Chivers & Raemaekers, 1980), H. syndactylus (Chivers & Raemaekers, 1980), and Gorilla gorilla (Harcourt, 1978; Stewart & Harcourt, 1987). Almost all males from these species emigrate by the time they attain physical maturity (Greenwood, 1980; Pusey & Packer, 1987).

Absence of sub-adult and juvenile-2 males in all the known harems at Sukau, and the presence of males in non-harem groups or as solitaries show a departure from their natal groups. Male departures from their natal group in most primate species typically coincide with sexual maturity (Pusey & Packer, 1987). In N. larvatus however, departures occur long before they attain sexual and physical maturity (Bennett & Sebastian, 1988; Yeager 1990a). Avoidance of inbreeding and close intra-sexual competition are the most likely reasons for male departures (Pusey & Packer, 1987).

In addition to male emigrations, female N. larvatus also transfer between groups (Bennett, 1986a; Bennett & Sebastian, 1988; Rajanathan & Bennett, 1990). Female transference in primates is less common than male (see Moore, 1984 for review) but has been recorded for T. gelada (Dunbar & Dunbar, 1975), Papio hamadryas (Kummer, 1968; Sigg et al., 1982), P. [badius] tephrosceles (Struhsaker, 1975; Struhsaker & Leland, 1979), P. [badius] rufomitratus (Marsh, 1979a & b), Presbytis melalophos (Bennett, 1983), P. rubicunda (Davies, 1984; 1987), Trachypithecus vetulus (Rudran, 1973), T. pileatus (Stanford, 1991), H. klossii (Tilson, 1981), H. lar (Chivers & Raemaekers, 1980), H. syndactylus (Chivers & Raemaekers, 1980; Bennett et al., 1983), Pan troglodytes (Nishida, 1979; Pusey, 1979; 1980; Goodall, 1986), G. gorilla (Harcourt, 1978; Stewart & Harcourt, 1987), Alouatta seniculus (Crockett, 1984; Crockett & Eisenberg, 1987), and A. palliata (Glander, 1984).

Maturing females might depart from their natal groups to avoid inbreeding (Harcourt, 1978; Greenwood, 1980; Pusey, 1980; Clutton-Brock, 1988; 1989). This is true only if the males do not emigrate, but in N. larvatus, males also emigrate from their natal groups. Emigration by both sexes does not support this argument (Moore & Ali, 1984). Thus, the advantages of emigration to avoid inbreeding will be reduced.

A possible explanation is that in some harems, the tenure of the adult male is longer than it takes for the females to become sexually mature (Clutton-Brock, 1988). Thus, female emigration is necessary to avoid inbreeding in such cases. Maturing and adult females may also transfer to improve their dominance status and to reduce feeding competition (Greenwood, 1980; Pusey & Packer, 1987).

In N. larvatus, both immature and mature females transfer between groups (this study; Bennett, 1986a; Bennett & Sebastian, 1988; Rajanathan & Bennett, 1990). Evidence suggests a transfer of two sub-adult females into group SU1 at Sukau, unless they were the same ones that left SU1 the previous month. Furthermore, the occasional presence of solitary females, and females briefly associating with non-breeding groups, suggests the transfer of females between groups.

Young females may depart from their natal group as a means to avoid infanticide, which usually accompanies harem takeovers (Hrdy, 1977; Marsh, 1979a & b; Pusey & Packer, 1987). The presence of an infant-2 female in group SU7 at Sukau substantiates this.

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Furthermore, the sighting of an adult female with a clinging infant in an all-male group at Abai suggests that females may depart from harems to avoid infanticide by new resident males. Females may also transfer between groups to improve their dominance status and/or avoid feeding competition (Pusey & Packer, 1987). There is, however, no evidence in this study to support the last two conclusions.

Unfamiliarity with the distribution of food sources in a new area is probably the major reason for female philopatry in most species of primates (Greenwood, 1980; Pusey & Packer, 1987). N. larvatus groups have very large and overlapping ranges. Thus, the transfer of females between groups will not affect them, as they are already familiar with the distribution of food sources (Bennett & Sebastian, 1988). This is as long as they transfer to a group occupying at least part of the same range. There is also partial to complete overlap of home ranges in other primate species, where female transfers between groups have been reported (Fossey, 1974; Struhsaker, 1975; Fossey & Harcourt, 1977; Marsh, 1981a; Sigg & Stolba, 1981; Goodall, 1986; Crockett & Eisenberg, 1987).

Alternatively, a female might remain in her natal group if she benefits from cooperation with kin in the defence of food sources (Wrangham 1980; 1987). This results in female-bonded groups and territorial defence by the females. Furthermore, under this hypothesis, resource distribution simultaneously affects both territoriality and social system. Conversely, it is also possible that resource distribution first affects the degree of territoriality, which in turn influences the costs of transfer between groups to a female (Bennett & Sebastian, 1988).

4.5.3 SOCIAL BEHAVIOUR Living in a social group has its benefits, but its members must also compete for

resources such as food and mates. This results in aggressive behaviour. Agonistic interactions within N. larvatus harems occur at very low levels, suggesting that competition among members is low. This in turn reflects the abundance of resources. Conversely, competition may have been present at higher levels but its manifestation is subtle, possibly because of an already established dominance hierarchy.

At both Sukau and Abai, all agonistic interactions between adult females were over sleeping sites, which were terminal branches of trees that overhung the river. This preference for terminal branches as sleeping sites may be an anti-predator adaptation. Individuals on terminal branches can feel any slight tremor caused by movements within its sleeping tree, such as caused by an animal climbing the tree. Alternatively, the chances of individuals on terminal branches being captured by a predator are less compared to those on the main branches. Whatever the reason the act of one animal displacing another strongly suggests a dominance hierarchy among the adult females.

Although the presence of dominance in N. larvatus could not be confirmed in this study, it is possible that intra-group aggression involves the establishment and maintenance of dominance relationships. As dominance is often related to access to resources, such aggression is an indirect form of resource competition (Post et al., 1980; Wrangham, 1981; Whitten, 1983; Fairbanks & McGuire, 1984; Silk, 1987; Walters & Seyfarth, 1987).

Harem males exhibit aggression mainly towards other groups, primarily against other males. It is in a harem male’s interest to defend his females from other males (Cheney, 1987). Females from other harems might also be acquired through male displays associated with inter-group aggression. The reproductive success of the harem male depends on his ability to compete successfully for and monopolise mates. These displays (section 4.2.2.1) presumably allow females from different harems to assess the displaying male. Inter-group aggression

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exhibited by N. larvatus males are most likely related to the acquisition and defence of females, since home ranges overlap totally, therefore, it is not for food and/or space.

Social grooming is probably the most common form of affiliative behaviour within primate groups. Colobines generally allogroom at low frequency, and rarely involve the adult male (Struhsaker & Leland, 1987). At Sukau and Abai, allogrooming involving an adult male N. larvatus was never seen and that between adult females was rare. Similar observations were made at Tanjung Puting (Yeager, 1990b), and Samunsam (Rajanathan & Bennett, 1990).

In primates, grooming functions to keep the animal’s fur clean (Rosenblum et al., 1966; Freeland, 1976), and to maintain social bonding within groups (Carpenter, 1942; Sade, 1965; Jolly, 1972; McKenna, 1978; Seyfarth, 1980; Coehlo et al., 1983). In N. larvatus, bonding between adult females and young animals is probably also maintained through clinging and suckling. The proximity between members of a harem might similarly serve the same purpose. These reasons might explain the low frequency of social grooming in N. larvatus. Alternatively, it was possible that there was no or little competition for food sources.

Allomothering has been reported for many primate species: Macaca fuscata (Hiraiwa, 1981), M. mulatta (Breuggeman, 1973; Berman, 1982), M. radiata (Rahaman & Parthasarathy, 1962; Silk, 1980), M. arctoides (Rhine & Hendy-Neely, 1978), Erythrocebus patas (Zucker & Kaplan, 1981), Semnopithecus entellus (Hrdy, 1977; McKenna, 1981; Dolhinow & Murphy, 1982), Presbytis melalophos (Bennett, 1983), P. rubicunda (Davies, 1984), Trachypithecus johnii (Poirier, 1968), T. pileatus (Stanford, 1991), N. larvatus (Rajanathan & Bennett, 1990), Papio ursinus (Cheney, 1978), and Pan troglodytes (Nishida, 1983). Patterns of allomothering vary from species to species and are more extensive among some species than others.

By allomothering, a nulliparous female may benefit from maternal experience that will be valuable when it gives birth to its own young (Lancaster, 1972; Hinde, 1974; Hrdy, 1976; 1977; Nishida, 1983; Poole, 1985). A parous and/or low ranking allomother can gain better access to resources through alliances with a higher ranking female by caring for the latter’s offspring (Nishida, 1983; Gray, 1985). The rank and parous state of the two adult females described in section 4.2.2.5 could not be determined. More quantitative data and information on female hierarchy are required before any conclusions can be drawn. Whatever the reasons may be, the primary benefit to the mother appears to be that of mother relief (Gray, 1985; Nicolson, 1987).

Although occurring at low levels, play is an important feature of the behaviour of immature N. larvatus. Both social and solitary play provides an opportunity for the young animals to develop physical and locomotor skills essential during adulthood (Symons, 1978; Smith, 1978; Fagen, 1981). This is particularly true for infants as they spend a significant proportion of their time being carried by their mothers. Furthermore, play allows the training of motor skills that are risky to practice in their usual functional context (Walters, 1987). In contrast to most group-living primates, immature N. larvatus spends much time in solitary play. This presumably reduces the risk of injury associated with social play, while simultaneously acquiring locomotor skills. Furthermore, since they are less social as adults, there is less need for social play.

Although N. larvatus harems are cohesive, there is very little interaction between members of a group. This may be partly because both males and females transfer between groups. Thus, it is possible that adults within harems are not close relatives. There are likely

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to be fewer interactions between females of a group if they are not related (Harcourt, 1979; Wrangham, 1979; Stewart & Harcourt, 1987). If however, the animals are closely related, there are likely to be more interactions between them (Dunbar, 1988; Stewart & Harcourt, 1987).

Another possible explanation for low levels of social interactions within N. larvatus harems is the lack of competition for food resources. High levels of aggression and social grooming in primate species have been shown to relate to frugivory. Fruits are often rare and widely scattered, and therefore likely to produce competition among frugivores. This competition then produces high levels of aggressive and appeasement behaviours (Deag, 1977; Caldecott, 1986).

Conversely, primate species that feed more on leaves show low levels of social interactions (Harcourt et al., 1976; Fossey & Harcourt, 1977; Wrangham, 1979; Bennett, 1983; Davies, 1984; Neville et al., 1988; Struhsaker & Leland, 1979; Stanford, 1991). Folivorous primates need not compete for food resources that are highly abundant and available throughout the year. Thus, competition for food is presumably less (Fossey & Harcourt, 1977; Wrangham, 1979; Bennett, 1983), resulting in a lower need for aggressive and affiliative behaviour between adult females of a harem (Wrangham, 1980; Stewart & Harcourt, 1987). At both Sukau and Abai, N. larvatus consumed large quantities of young leaves that were abundant and available throughout the year. This ultimately reduces the need for affiliative and aggressive behaviour within the group.

4.5.4 VIGILANCE In N. larvatus, the adult male and females of a harem spent almost equal amounts of

time being vigilant. The presence of a known predator and other potential predators (section 4.5.1) is a possible cause for this. The importance of vigilance for detecting predators is well-documented (Hall, 1960; 1965; Pulliam, 1973; 1976; Bertram, 1978; Caraco, 1979). Another explanation is that vigilance increases the likelihood of locating food (Krebs & Partridge, 1973; Underwood, 1982), in particular highly selected food items that are rare. Furthermore, vigilance does not require much energy, and in some ways, it is also a form of rest, allowing the animal to relax its tired muscles and digest its food.

A harem male needs to be particularly vigilant for other males. The costs in lost of gene production are very high for him if another male mated with his females (Underwood, 1982; Bennett, 1983). Conversely, the presence of other harem and extra-group males may benefit the females by allowing them to assess potential mates or harems into which they can transfer.

4.6 SUMMARY 1. The basic social unit of N. larvatus in the Lower Kinabatangan was a harem, and

comprised one adult male, several adult females and their offspring.

2. Three non-harem groups were relatively stable over time, and they had more than one adult male. Furthermore, two non-harem groups had young female members that associated with the group throughout the study.

3. Group spread, inter-individual spacing and nearest neighbour distances showed that harems were spatially cohesive.

4. Different groups frequently associated with each other at roosting sites, and occasionally travelled together throughout the day, albeit lesser at Abai. There were two levels of

62

social organisation, the harem and the band. Analysis of inter-group associations at sleeping sites, however, showed some groups were attracting each other.

5. Aggressive interactions between adult females over sleeping sites, with one displacing the other, implied the existence of a dominance hierarchy among females within a harem.

6. Allogrooming within a harem did not involve the adult male. Social grooming was mainly directed by the adult females towards the young members of the group.

7. Social interactions within groups were rare, implying a low level of intra-group competition. This presumably resulted from a high abundance and availability of key food resources for most of the year.

8. The adult male and females of a harem spent almost an equal amount of time in vigilance. Both sexes possibly performed vigilance for rare food items and potential predators. The harem male was also presumably vigilant for other males. Females might also be assessing other harems for a possible transfer.

63

Table 4.1 Age/sex composition of identified groups at Sukau

♂♀ ♂♂ SU1 SU2 SU3 SU4 SU5 SU6 SU7 SU8 SU9

A♂ 1 1 1 1 1 1 3 3 3A♀ 8 7 7 8 8 6 SA♂ 2 2 3SA♀ 1 1 1 1 1 J2♂ 2 3 2J2♀ 1 3 2 1 1 2J2? 3 1 J1♂ 3 J1♀ 2 1 1 J1? 3 2 1 2 1 I2♂ 1 2 I2♀ 1 2 1 1 I2? 1 2 3 3 1 I1♂ I1♀ I1? 1 1 1 Size 20 19 17 17 15 14 9 8 10

A=adult; SA=subadult; J2=older juvenile; J1=young juvenile; I2=older infant; I1=young infant; ?=sex unknown; ♂♀=one male group; ♂♂=non breeding group (all males and predominantly males)

64

Table 4.2 Demographic changes within SU1

1990 1991 Aug. Sep. Nov. Feb. Mar. Apr. Sep. Oct. Nov. Dec.

A♂ 1 1 1 1 1 1 1 1 1 1 A♀ 8 8 9 9 9 9 8 8 8 8 SA♂ SA♀ 1 1 2 2 2 2 2 2 2 J2♂ J2♀ 1 1 1 2 2 2 1 1 1 2 J1♂ 3 3 2 2 3 3 1 1 1 1 J1♀ 2 2 1 1 1 1 2 2 1 J1? 3 3 3 3 I2♂ 1 1 1 1 I2♀ 1 1 2 1 1 2 1 I2? 1 1 1 2 2 3 4 I1♂ I1♀ 1 1 1 1 I1? 1 2 2 2 2 1 Size 20 20 19 20 21 22 20 22 23 23

A=adult; SA=subadult; J2=older juvenile; J1=young juvenile; I2=older infant; I1=young infant; ?=sex unknown

Table 4.3 Percent time members of SU1 belonging to different age/sex categories were nearest to subject at Sukau study area (n=4966, weighted data). [Values in parentheses show the percent time that the subject would spend nearest to an individual of that age/sex category if all individuals were associating randomly.] Subject Nearest Neighbour n

A♂ A♀ SA♀ J2 J1 I2 I1 A♂ - 78.9 (40) 0.2 (10) 4.3 (5) 15.5 (25) 1.1 (15) 0 (5) 382A♀ 3.7 (5) 26.2 (35) 0.4 (10) 3.0 (5) 29.5 (25) 25.1 (15) 12.2 (5) 2540SA♀ 11.4 (5) 78.6 (40) 0 (5) 0 (5) 9.9 (25) 0 (15) 0 (5) 33J2 4.7 (5) 70.5 (40) 0.9 (10) 3.6 (0) 13.9 (25) 4.3 (15) 1.9 (5) 259J1 3.1 (5) 76.5 (40) 0 (10) 1.5 (5) 14.6 (20) 2.8 (15) 1.3 (5) 1071I2 0.4 (5) 89.8 (40) 0.6 (10) 1.1 (5) 3.2 (25) 4.2 (10) 0.6 (5) 491I1 0 (5) 94.0 (40) 0 (10) 0.6 (5) 1.8 (25) 1.4 (10) 2.3 (5) 190

A=adult; SA=subadult; J2=older juvenile; J1=young juvenile; I2=older infant; I1=young infant

65

Table 4.4 Daily number of SU1’s inter-group associations of ≤50m and ≤100m compared with the predicted number of such associations if groups were ranging randomly with respect to each other (n=93)

Distance Observed PredictedOMGs Non-OMGs SU2 SU7 All Groups

≤50m 0.438 0.375 0.365 0.292 0.604 0.31 ≤100m (same side of river)

0.521 0.552 0.385 0.438 0.677 0.59

≤100m (opposite sides of river)

0.542 0.573 0.396 0.458 0.688 0.59

X² 0.06 0.02 0.14 0.07 0.31 p >0.95 >0.95 <0.95 >0.95 <0.95

Table 4.5 Percent agonistic interactions within SU1, between SU1 and other N. larvatus groups, and between SU1 and other species (n=34, weighted scans)

Aggressor

Recipient Total Within SU1 With others

A♀ SA♀ J2 J1 I2 I1 ♀♂ ♂♂ ☺ ☻ A♂ 3.5 3.5 3.4 6.7 19.4 3.3 39.8 A♀ 13.7 13.9 6.7 3.5 17.7 55.5 SA♀ J2 1.4 1.4 J1 I2 I1 ☻ 3.3 3.3 Total 17.2 3.5 17.3 10 6.7 22.9 19.1 3.3 100

A=adult; SA=subadult; J2=older juvenile; J1=young juvenile; I2=older infant; I1=young infant; ♂♀=one male group; ♂♂=non breeding group (all males and predominantly males); ☺=observer; ☻=Macaca nemestrina

66

Table 4.6 Percent allogrooming occasions within members of SU1 (n=115, weighted scans)

Groomee Groomer Total A♂ A♀ SA♀ J2 J1 I2 I1

A♂ A♀ 19.9 0.8 5.1 8.4 1.2 35.4 SA♀ J2 6.4 6.4 J1 31.8 31.8 I2 15.7 15.7 I1 10.7 10.7 Total 84.5 0.8 5.1 8.4 1.2 100


67

Table 4.7 Summary of copulatory bouts of N. larvatus at Sukau

Date Group No. of mounts

Duration (seconds)

Harass Comments

21/05/90 ? 1 15 I2 Agitated older infant bounced around the mating pair, then grabbed adult male’s fur and screeched. Adult male barked at older infant but did not stop copulating

31/08/90 SU1 1 35 J1 Young juvenile male pulled adult male’s legs and rump, but did not succeed in interfering with the copulation.

28/10/90 ? 1 12 I2 Older infant pulled the nose of the adult male, but did not stop the copulation.

14/03/91 SU1 1 12 none Agitated older infant whimpered near the mating pair, but did not harass. Another adult female and older juvenile sat nearby and watched.

10/09/91 SU1 1 40 J1 Young juvenile pulled the nose of the adult male, but did not stop the copulation.

12/09/91 SU1 1 38 2 I2 Two screeching older infants came towards the copulating pair. One climbed on the adult male’s back, grabbed the adult male’s chest and nose, but failed to stop the copulation. After copulation, the mating pair separated to about 0.5m apart, and shuddered briefly.

18/09/91 ? 1 40 none About four minutes before copulation, adult males of a nearby predominantly male non-breeding group displayed by leaping from branch to branch.

10/11/91 SU5 1 10 none The adult female of the mating pair was non-sexually mounted by another adult female for about two seconds before being sexually mounted by the adult male of the mating pair. See section 4.2.2.3 for details.

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Table 4.8 Percent play occasions within members of SU1 (n=180, weighted scans)

Subject Partner Total A♂ A♀ SA♀ J2 J1 I2 I1 Alone

A♂ A♀ SA♀ J2 0.7 0.7 1.4 J1 0.2 16.1 4.2 0.8 15.2 36.5 I2 0.7 5.7 4.9 1.4 22.2 34.9 I1 1.8 1.4 2.3 21.7 27.2 Total 0.9 24.3 10.5 4.5 59.8 100


Table 4.9 Percent time members of harems belonging to different age/sex categories were nearest to subject at Abai study area (n=1023, weighted data). [Values in parentheses show the percent time that the subject would spend nearest to an individual of that age/sex category if all individuals were associating randomly.] Subject Nearest Neighbour n

A♂ A♀ SA♀ J2 J1 I2 I1 A♂ - 77.7

(50) 0 (7.1)

9.0 (7.1)

9.6 (14.3)

3.7 (14.3)

0 (7.1)

63

A♀ 5.9 (7.1)

22.7 (42.9)

0 (7.1)

5.4 (7.1)

27 (14.3)

24.9 (14.3)

6.9 (7.1)

488

SA♀ 0 (7.1)

33.5 (50)

0 (7.1)

66.5 (7.1)

0 (14.3)

0 (14.3)

0 (7.1)

3

J2 2.7 (7.1)

56.5 (50)

2.6 (7.1)

10.4 (0)

15.4 (14.3)

12.3 (14.3)

0 (7.1)

90

J1 1.1 (7.1)

64.5 (50)

0 (7.1)

4.5 (7.1)

22.6 (7.1)

5.7 (14.3)

0.8 (7.1)

230

I2 0 (7.1)

77.7 (50)

0 (7.1)

2.8 (7.1)

10.9 (14.3)

7.4 (7.1)

0.6 (7.1)

114

I1 0 (7.1)

100 (50)

0 (7.1)

0 (7.1)

0 (14.3)

0 (14.3)

0 (0)

33


69

Table 4.10 Percent allogrooming occasions within members of harems at Abai (n=16, weighted scans)

Groomee Groomer Total A♂ A♀ SA♀ J2 J1 I2 I1

A♂ A♀ 7.0 8.2 15.2 SA♀ J2 J1 32.4 32.4 I2 46.3 46.3 I1 6.1 6.1 Total 91.8 8.2 100


Table 4.11 Percent play occasions within members of harems at Abai (n=45, weighted scans)

Subject Partner Total A♂ A♀ SA♀ J2 J1 I2 I1 Alone

A♂ A♀ SA♀ J2 3.4 J1 17.9 3.6 4.8 I2 3.3 17.7 11.6 1.3 18.6 I1 17.8 Total 3.3 35.6 18.6 1.3 41.2 100


70

Table 4.12 Summary of N. larvatus social organisation at different sites

OMGs Sukau Abai Samunsam Tanjung Puting

Size 17 14.6 9 12.6 Sex ratio 1:7.3 1:7.1 1:3.8 1:5 SaM present no yes yes ? Group spread (m) 13.2 12.2 13.7 11.1 Another group within 100m (% nights)

Common (70%)

Uncommon (20%)

Common (70%)

Common (65.5%)

Non-OMGs Size 9 6.4 variable 9.5 Group spread (m) 13.1 9.8 22.3 ? Relative stability yes ? no ? More than one AM yes yes no yes Females present yes possible yes no

Sukau and Abai: Boonratana, 1993.

Samunsam: Bennett, 1986; Bennett and Sebastian, 1988; Rajanathan and Bennett, 1991.

Tanjung Puting: Yeager, 1989; 1990a and b; 1991a; 1992.

71

Figure 4.1a Percent time nearest neighbour was within cumulative distance from subject at Sukau (n=4966, weighted data)

Figure 4.1b Percent time nearest neighbour was within cumulative distance from subject at Sukau (n=4966, weighted data)

0

20

40

60

80

100

120

0 >0-1 >1-2 >2-3 >3-4 >4-5

% sc

ans

Distance (metres)

Adult Male Adult Female Subadult Female

0

20

40

60

80

100

120

0 >0-1 >1-2 >2-3 >3-4 >4-5

% sc

ans

Distance (metres)

Juvenile-2 Juvenile-1 Infant-2 Infant-1

72

Figure 4.2a Percent time different number of individuals were within 2.5m of subject at Sukau (n=4966, weighted data)

Figure 4.2b Percent time different number of individuals were within 2.5m of subject at Sukau (n=4966, weighted data)

0

5

10

15

20

25

30

35

40

0 1 2 3 4 5 6 7 8 9 10 >10

% sc

ans

Number of Individuals


0

5

10

15

20

25

30

35

40

45

0 1 2 3 4 5 6 7 8 9 10 >10

% sc

ans

Number of individuals


73

Figure 4.3a Percent time different number of individuals were within 5m of subject at Sukau (n=4966, weighted data)

Figure 4.3b Percent time different number of individuals were within 5m of subject at Sukau (n=4966, weighted data)

0

5

10

15

20

25

30

35

1 2 3 4 5 6 7 8 9 10 >10

% sc

ans



0

5

10

15

20

25

30

35

1 2 3 4 5 6 7 8 9 10 >10

% sc

ans



74

Figure 4.4 Percent nights when other N. larvatus group/groups were close to SU1 at Sukau (n=96)

Figure 4.5 Percent nights when 0, 1, 2, 3 and 4 groups were within 100m of SU1 at Sukau (n=96)

0

10

20

30

40

50

60

70

80

<50m (same side) <100m (same side) <100m (both sides)

% n

ight

s

Distance and riverbank

Harem Non-harem SU2 SU7 All Groups

0

5

10

15

20

25

30

35

40

0 1 2 3 4

% sc

ans

Number of groups

75

Figure 4.6 Activity budgets of SU1 at Sukau (n=4966, weighted data)

Figure 4.7 An adult female grooming a juvenile-1

0.01

0.1

1

10

100%

scan

s

Activities

76

Figure 4.8 An adult female watching the observer

Figure 4.9 Number of Infant-1s per adult female observed each month at Sukau

0

0.05

0.1

0.15

0.2

0.25

0.3

0.35

F M A M J J A S O N D J F M A M J J A S O N D

1990 1991

Infa

nts/

adul

t fem

ale

77

Figure 4.10 Percent time different age/sex classes spent at vigilance (n=1257, weighted data)

Figure 4.11 An adult male prior to release (note tattoo on right cheek)

0

10

20

30

40

50

60

AM AF SAF Juv2 Juv1 Inf2 Inf1

% sc

ans

Age/sex classes

78

Figure 4.12 A juvenile with an open-mouthed threat towards the observer

Figure 4.13a Percent time nearest neighbour was at cumulative distance from subject at Abai (n=1023, weighted data)

0

20

40

60

80

100

120

0 >0-1 >1-2 >2-3 >3-4 >4-5

% sc

ans

Distance (metres)


79

Figure 4.13b Percent time nearest neighbour was at cumulative distance from subject at Abai (n=1023, weighted data)

Figure 4.14a Percent time different number of individuals was within 2.5m of subject at Abai (n=1023, weighted data)

0

20

40

60

80

100

120

0 >0-1 >1-2 >2-3 >3-4 >4-5

% sc

ans

Distance (metres)


0

20

40

60

80

100

120

1 2 3 4 5 6 7 8 9 10 >10

% sc

ans



80

Figure 4.14b Percent time different number of individuals was within 2.5m of subject at Abai (n=1023, weighted data)

Figure 4.15a Percent time different number of individuals was within 5m of subject at Abai (n=1023, weighted data)

0

5

10

15

20

25

30

35

1 2 3 4 5 6 7 8 9 10 >10

% sc

ans



0

10

20

30

40

50

60

70

1 2 3 4 5 6 7 8 9 10 >10

% sc

ans



81

Figure 4.15b Percent time different number of individuals was within 5m of subject at Abai (n=1023, weighted data)

Figure 4.16 Percent of nights when another N. larvatus group was close to a harem at Abai (n=205)

0

5

10

15

20

25

30

35

1 2 3 4 5 6 7 8 9 10 >10

% sc

ans



0

2

4

6

8

10

12

14

16

<50m (same sides) <100m (same sides) <100m (both sides)

% n

ight

s

Distance and riverbank

Harem All-male

82

Figure 4.17 Percent of nights when 0, 1, and 2 groups were within 100m of a harem at Abai (n=205)

Figure 4.18 Activity budgets of harem groups at Abai (n=1023, weighted data)

0

10

20

30

40

50

60

70

80

90

0 1 2

% sc

ans

Number of groups

0.01

0.1

1

10

100

% sc

ans

Activities

83

Figure 4.19. Number of infant-1s per adult female observed each month at Abai

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

F M A M J J A S O N D J F M A M J J A S O N D

1990 1991

Infa

nts/

adul

t fem

ale

84

CHAPTER 5: FEEDING ECOLOGY

5.1 INTRODUCTION Nasalis larvatus and most other primates depend for their survival on plant foods to

meet their dietary requirements. These requirements 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.

Primates do not feed at random, but are highly selective (e.g., Hladik, 1977a; Oates et al., 1977; 1980; Davies et al., 1988). Two principal factors underlying the selection of plant foods are the nutritional and secondary compound content of the plant part, and its relative availability in time and space (Hladik & Hladik, 1969; 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. The monkeys 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 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). 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, N. larvatus and other colobines have enlarged fore-stomachs that contain vast colonies of bacteria with cellulolytic properties (Kuhn, 1964; Bauchop & Martucci, 1968; Moir, 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, 1977b; Struhsaker & Leland, 1987). Most colobine studies, however, have found that fruits and seeds are also consumed in significant amounts (Curtin, 1975; 1980; Hladik, 1977; Oates, 1977a; 1988; Oates et al., 1980; Marsh, 1981a; McKey et al., 1981; Bennett, 1983; Davies, 1984; Gurmaya, 1986; Bennett &

85

Sebastian, 1988; Yeager, 1989; Stanford, 1991). Sugar-rich fruits are normally avoided because their fermentation increases 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), and are thus important sources of energy.

The aims of this chapter are to describe the diet of N. larvatus throughout the year, and monthly and age/sex variation in relation to the availability of foods. The selection of food items in relation to the animal’s digestive physiology and phytochemistry of plant parts is also examined.


5.2.1 FOOD ITEMS Young leaves were the major food item for N. larvatus harem groups at Sukau,

accounting for more than 70% of their annual diet (figure 5.1), while mature leaves (0.3%), made an insignificant proportion of the animals’ diet. The monkeys consumed an almost equal amount of whole fruits and flowers, including flower buds. About 20% of the fruits consumed consisted of 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 were not observed with certainty.

Almost 60% of the all-male groups’ diet consisted of young leaves (figure 5.2). 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 (table 5.1). Among those, Mallotus muticus (Euphorbiaceae), a common species at Sukau (section 3.2.2.2) was an important food plant (table 5.2). Mature and young leaves, and unripe fruits including seeds were consumed. About 50% of the mature leaves eaten were M. muticus. 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 were observed to feed on anything other than plant materials, they must have fed inadvertently 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.

5.2.2 MONTHLY VARIATION There was considerable variation in the proportion of different plant parts eaten

throughout the year (figure 5.3). The amount of young leaves eaten was high in most months but lower in July and September. This corresponded with increased fruits in the animals’ diet. There was a negative correlation between young leaves and fruits in the diet (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 July, a decrease in young leaves

86

in the diet corresponded with an increase in flowers. 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 young leaves was high throughout the year (figure 5.4a). On the other hand, 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 (figure 5.4b). This shows that the animals fed on flowers more when there were more flowers available. There was no correlation between the amount of fruits in diet and in the forest (figure 5.4c).

Items in the diet were correlated with monthly variation in time spent resting, travelling and vigilance. 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 had no correlation with other food items. Monthly production of flowers was inversely correlated with rainfall (section 3.2.2.3). This meant that 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).

5.2.3 DIURNAL VARIATION The diet of N. larvatus at different times of day was examined for variation, if any, in

particular plant parts (figure 5.5). 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. When the animals awoke, they fed on young leaves and some flowers. 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 fairly slight, showing no major trends.

5.2.4 AGE-SEX VARIATION Different age/sex classes did not spend equal proportions of their time feeding (figure

5.6). Excluding sub-adult females, the trend was for a reduction in young leaves eaten with decreasing body size. At the other extreme, infant-2s fed more on ripe fruits than other age/sex classes. Adult females fed more on plant parts other than young leaves compared to adult males. Similarly, immature individuals (juveniles and infants) ate more plant parts other than young leaves compared to adults. This implied that adults could digest fibre-rich food parts better than could immature individuals. Thus, immature individuals supplemented their dietary intake with easily digestible foods.

Different age/sex classes spent different amounts of time feeding from month to month (figure 5.7). 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 juvenile-2s (T=7.89, n=12, p<0.05), and between adult males and infant-2s (T=3, n=12, p<0.01). Juvenile-2s fed for more time than adult males, whereas infant-2s fed for less time than adult males.

Similarly, adult females fed for less time than juvenile-2s (T=7.78, n=12, p<0.05), but for significantly more time than infant-2s (T=0, n=12, p<0.01). There were significant

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differences in time spent feeding between juvenile-2s and juvenile-1s (T=3, n=12, p<0.05), and between juvenile-2s and infant-2s (T=0, n=12, p<0.01). Both juvenile-1s and infant-2s spent less time feeding than juvenile-2s. Juvenile-1s spent more time feeding than did infant-2s (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 (figure 5.8). 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 a few adjoining trees. This was just as they woke up or when they were ready to retire for the day.

Similarly, there was no difference in time spent feeding between adult males and adult females, and between adult males and juvenile-1s. Juvenile-2s spent more time feeding than did adult males (T=8, n=13, p<0.01), whereas infant-2s spent less time (T=3.5, n=13, p<0.05). Similarly, adult females spent less time feeding than did juvenile-2s (T=7.5, n=13, p<0.01) but more than infant-2s (T=0, n=13, p<0.01). Juvenile-2s spent more time feeding than juvenile-1s (T=11, n=13, p<0.05) and infant-2s (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).

The lack of differences for the time spent feeding between the adult male and females were 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, 1977b). The adult male N. larvatus is twice bigger than the adult female, therefore, also requires more food. Juvenile-2s probably consumed more than adults because food was important for growth. Other immature individuals, juvenile-1s and infant-2s supplemented their dietary intake needed for growth with breast milk. Infant-1s relied wholly on breast milk.

5.3 ABAI STUDY AREA

5.3.1 FOOD ITEMS Almost half of the harem groups’ diet at Abai comprised young leaves (figure 5.9).

Unripe fruits (20.6%), flowers (15.5%) and seeds (11.6%) also figured prominently in their diet. None of the members were ever observed feeding on mature leaves or ripe fruits. Their dietary items could not be observed with certainty 2.6% of the time.

The diet of all-male groups consisted entirely of young leaves and unripe fruits (figure 5.10), but the sample size was small (n=33). Once, a sub-adult male and once, a juvenile-2 male were observed feeding on the inflorescence of Nypa fruticans (Arecaceae) (figure 5.11). 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 5.3), Sonneratia alba (Lythraceae) was an important component of the animals’ diet (table 5.4). 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 (section 3.3.2), and its inflorescence made up 50% of the animals’ annual diet of flowers. Ficus spp. (Moraceae), although not abundant (section 3.3.2.2), fruited asynchronously and therefore fruits were available to the animals almost throughout the year. At least a third of the fruits eaten, mostly unripe, belong to the Ficus spp.

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5.3.2 MONTHLY VARIATION There were large monthly variations in plant parts eaten by N. larvatus harems at

Abai (figure 5.13). There were 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 (figures 5.14a, b & c). 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.

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). In addition, there was 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 in food trees available (section 3.3.2).

5.3.3 AGE/SEX VARIATION Annually, different age/sex classes invested different amounts of time feeding on

different plant parts (figure 5.15). All age/sex classes, however, spent most of their time feeding on young leaves. Adult females, juveniles and infant-2s fed more young leaves than did the harem males. Adult males spent equal proportions of their time feeding on young leaves, fruits and flowers.

Monthly, there were variations in time spent feeding by the different age/sex classes (figure 5.16). There was no significant difference in time spent feeding between the harem 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 fed less than juvenile-2s (T=7.89, n=8, p<0.05), but more than infant-2s (T=3, n=8, p<0.01). Similarly, adult females spent less time feeding than juvenile-2s (T=7.78, n=8, p<0.05), but more than infant-2s (T=0, n=8, p<0.01). Juvenile-2s spent more time feeding than juvenile-1s (T=3, n=8, p<0.05), and infant-2s (T=0, n=8, p<0.01). Similarly, juvenile-1s spent more time feeding than infant-2s (T=3, n=8, p<0.01).

5.4 DRINKING BEHAVIOUR Throughout the study, N. larvatus was observed to drink water on only two occasions.

On September 12, 1991 at 1725 hours, an adult female from group SU1 descended from its night tree to a fallen tree that was partly submerged in the river. It knelt on all four limbs and drank water by putting its mouth to the river. The second drinking occasion occurred on September 14, 1991 at 1657 hours. An adult male from an unknown non-breeding group descended to the riverbank and drank water in the same posture as described for the adult female (figure 5.12).

Both drinking occasions occurred by the Kinabatangan River. The female drank for about seven seconds, and the adult male for about 18 seconds. No N. larvatus were ever observed to drink water on any other occasion.

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At 1748 hours on September 12, 1991, an adult female from SU1 pointed her nose towards the sky and sniffed the air. This was the first time I observed this behaviour. I later learnt that there was a massive forest fire in Kalimantan that started about a week earlier. It was uncertain whether the forest fires, the sniffing of the air and water-drinking were related or not. The sky was hazy and full of smoke particles until the onset of the rainy season in late October.

5.5 FOOD SELECTION AND PHYTOCHEMISTRY

5.5.1 LEAF SELECTION A total of 97 mature leaf samples was analysed (appendix V), of which only two,

Mallotus muticus and M. wrayi (Euphorbiaceae), were identified with certainty as food plants (table 5.5). 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 5.6). Although protein in mature leaves was higher than that of flowers and fruits (section 3.6.1), N. larvatus rarely fed on mature leaves. This was likely because mature leaves had a higher mean level of CT. 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 that 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 5.17). 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 graph. 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 that were above a minimum ratio of protein to digestion inhibitors.

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 (sections 5.2.1 & 5.3.1). Only seven samples out of the 33 analysed were known foods of N. larvatus (table 5.5). Young leaves eaten had a higher mean protein, CT, NDF than the one young leaf sample not eaten (table 5.6). 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 level, but lower CT levels.

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. On the other hand, 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

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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.

5.5.2 FLOWER SELECTION A small sample (n=5, appendix V) of flowers was analysed, of which only one

sample, the flower bud of Dillenia indica (Dilleniaceae) was eaten (table 5.5). 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 same species (table 5.6). 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.

5.5.3 FRUIT SELECTION A total of 18 fruit samples was analysed (appendix V), of which only two, Mallotus

muticus (Euphorbiaceae) and Sonneratia alba (Lythraceae), were identified with certainty as food plants (table 5.5). 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.

5.6 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 harem groups 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 show 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 (section 5.2.3). 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 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;

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Wrangham, 1977). Eating leaves at end of the day may keep the digestive system active for longer periods (Clutton-Brock, 1977b), and also allows the animals to obtain enough energy so as not to cause a deficit during their inactive period (Bennett, 1983).

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. Therefore, 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).

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 5.7). 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 (section 3.4.2). Furthermore, the flower and fruit production at Abai was higher, even though the general trends were similar (section 3.4.2). 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 inflorescence 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.

These data 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 (section 3.3.2.3) 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. 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).

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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 an herbivore’s dietary habits, in the same way that does tannins (Freeland et al., 1985). Nevertheless, an 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, 1977a & b; Waterman, 1984). Hylobates lar, for example, eats foods that contain no alkaloids (Vellayan, 1982).

The digestibility of food depends on its digestibility and 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.

5.7 SUMMARY 1. 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.

2. N. larvatus are selective feeders, consuming large quantities of young foliage, and significant proportions of flowers, unripe fruits and seeds. The description “folivore-frugivore” is more apt for N. larvatus than “folivore.”

3. Peaks in feeding occurred before noon and at dusk. There was little synchronisation in feeding among members of SU1. Furthermore, members did not feed on the same plant parts and species simultaneously. 4. There was variation in percent plant parts eaten by

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different age/sex classes of harems. Immature individuals consumed less foliage and more flowers and fruits, including seeds, compared to mature individuals.

4. Food items with high levels of digestion inhibitors were avoided. Food items were selected for their higher protein to digestion inhibitor ratio.

5. N. larvatus, being a large colobine, needs a large total food intake. Since they can afford to process food slowly, their food items must be abundant but not necessarily easy to digest.

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Table 5.1 List of food plants and plant parts eaten by N. larvatus at Sukau

Family Species Part Eaten Bombacaceae Coeloestegia sp. YL Combretaceae Unidentified sp. A UF Convulvulaceae Merrenia borneensis UF Dilleniaceae Dillenia indica FL, FB Dipterocarpaceae Dipterocarpus sp. A YL Euphorbiaceae Claoxylon sp. A YL

Glochidion borneensis YL Glochidion obscurum YL, UF Macaranga hypoleuca YL Mallotus floribindus YL Mallotus wrayi ML, YL Mallotus muticus ML, YL, UF, SD Mallotus sp. A YL Bridelia stipularis SD

Fabaceae Bauhinia sambafida-sambafida YL Spantholobus hirsutus YL

Flacourtiaceae Homalium foetidum YL Hydnocarpus woodii UF, SD

Lauraceae Dehessia incrassata YL Moraceae Ficus condensa YL

Ficus globbosa YL, UF Ficus pellucido-punctata UF Ficus depressa UF Ficus racemosa UF, RF Ficus spp. YL, UF

Myristicaceae Knema latifolia YL Polypodiaceae Stenochlaena palustris YL Rosaceae Parinari oblongifolia YL Rubiaceae Nauclea subidita YL

Neonauclea gigantea YL Neonauclea crytopoda SD Anthocephalus chinensis YL

Santalaceae Unidentified sp. B YL Tiliaceae Microcos antidesmifolia YL, UF

Microcos sp. A YL Vitaceae Cayratia sp. A YL

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

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Table 5.2 Percent plant parts of food plants in diet of N. larvatus at Sukau, recorded during scan observations (n=613, unweighted scans)

Species ML YL RF UF FL FB SD Unidentified sp. A (Combretaceae) 0.7 Dillenia indica (Dilleniaceae) 0.2 0.2 Mallotus muticus (Euphorbiaceae) 0.2 5.7 0.8 Hydnocarpus woodii (Flacourtiaceae) 0.2 Ficus spp. (Moraceae) 1.6 0.2 Microcos antidesmifolia (Tiliaceae) 29 All unidentified spp. 0.2 67.9 1.6 4.4 7.3 0.3 2.3 Liana 0.7 0.2


Table 5.3 List of food plants and plant parts eaten by N. larvatus at Abai

Family Species Part Eaten Arecaceae Nypa fruticans FL Annonaceae Polyalthia glauca FL Burseraceae Canarium sp. A YL

Santiria laevigata YL Euphorbiaceae Sapium indicum YL Lythraceae Sonneratia alba YL, UF, FL, SD Moraceae Ficus sumatrana YL, UF

Ficus microcarpa YL, UF Ficus spp. YL, UF

Myrtaceae Eugenia crysantha YL Eugenia barringtoides SD

Oleaceae Chionanthus cuspidata YL Rhizophoraceae Bruguiera sexangula FL Sapotaceae Ganua motleyana YL, UF Sterculiaceae Heritiera littoralis YL

Pterospermum elongatum YL Verbenaceae Teijsmanniodendron sp. A YL

Avicennia alba YL, UF, SD, FL ML: mature leaves; YL: young leaves; RF: Ripe fruits; UF: unripe fruits; FL: flowers; FB: flower buds; SD: seeds

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Table 5.4 Percent plant parts of food plants in diet of N. larvatus at Abai, recorded during scan observations (n=184, unweighted scans)

Species ML YL RF UF FL FB SD Ficus spp. 1.6 7.6 Nypa fruticans (Arecaceae) 6.5 Sapium indicum (Euphorbiaceae) 0.5 Sonneratia alba (Lythraceae) 39.7 7.1 1.1 9.8 All unidentified spp. 13 1.6 5.4


Table 5.5 Chemical composition of plant parts observed eaten with certainty by N. larvatus (see tables 5.1 & 5.3)

Species Part Saponin % Protein Condensed Tannin (mg/g)

% Neutral Detergent Fibre

Mallotus muticus ML 1+ 1.69 0 59.6 YL 2.88 0.35 55.1 FR 1+ 1.44 0.47 62.7

Mallotus wrayi ML 1+ 2.69 0.12 56.2 YL 1+ 3 0 65.7

Mallotus sp. A YL 3.44 0 69.7 Sonneratia alba FR 1.75 0.35 67 Dillenia indica FB 1.1 0.12 62.9 Claoxylon sp. A YL 4.19 0.47 57.2 Chionanthus cuspidita YL 1.56 0.35 70.7 Microcos antidesmifolia YL 1+ 2.63 0.35 89.6 Microcos sp. A YL 2.69 0.47 82.2

ML: mature leaves; YL: young leaves; FR: fruits; FB: flower buds

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Table 5.6 Chemical composition of plant parts not observed eaten by N. larvatus

Species Part Saponin % Protein Condensed Tannin (mg/g)

% Neutral Detergent Fibre

Polyalthia glauca ML 1.56 9.15 56.5 Dillenia indica ML 1+ 1.75 0.24 64.2

YL 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 latfolia 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 64.2

ML: mature leaves; YL: young leaves

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Table 5.7 Comparative proportions of plant parts in some colobines’ diets (expressed as percentages)

Species ML ML+YL

YL FL FR FR+SD

SD Source

N. larvatus Sukau 0.3 - 72.7 8.3 8.3 - 2.4 Boonratana, 1993. N. larvatus Abai - - 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 Site 1 1.3 - 70.8 0.2 18.8 - 21.3 Mitchell, 1994. P. hosei Site 2 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. ML: mature leaves; YL: young leaves; RF: Ripe fruits; UF: unripe fruits; FL: flowers; FB: flower buds; SD: seeds

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Figure 5.1 Percentage of different items in harem groups' diet at Sukau (n=594, unweighted data)

Figure 5.2 Percentage of different items in non-harem groups' diet at Sukau (n=72, unweighted data)

Mature leaves (0.3%)

Young leaves (72.7%)

Flowers (7.8%)

Flower buds (0.5%)

Ripe fruits (1.7%)

Unripe fruits (6.6%)

Seeds (2.4%)

Unknown items (8%)

Young leaves (59.7%)

Ripe fruits (1.4%)

Unripe fruits (37.5%)

Unknown items (1.4%)

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Figure 5.3 Monthly variation in plant parts eaten by N. larvatus groups at Sukau (n=540, unweighted data)

Figure 5.4a Monthly variation in young leaves eaten (n=428, unweighted data), to that in the forest (n=500, phenology data), at Sukau

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Figure 5.4b Monthly variation in flowers eaten (n=49, unweighted data), to that in the forest (n=500, phenology data), at Sukau

Figure 5.4c Monthly variation in fruits eaten (n=63, unweighted data), to that in the forest (n=500, phenology data), at Sukau

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Figure 5.5 Diurnal variation in plant parts eaten by SU1 at Sukau (n=489, unweighted data)

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Figure 5.6 Percentage of different items in harem groups' diet by age/sex class at Sukau (n=534, unweighted data)

Adult males (n=35)

Young leaves (88.6%) Flowers (5.7%)Unripe fruits (2.9%) Unknown items (2.9%)

Adult females (n=290)

Young leaves (72.5%) Mature leaves (0.3%)Unknown items (7%) Seeds (2.8%)Flowers (0.3%) Flower buds (8.7%)Ripe fruits (6.6%) Unripe fruits (1.7%)

Juvenile-2s (n=63)

Young leaves (74.6%) Unknown items (11.1%)Seeds (1.6%) Flowers (4.8%)Unripe fruits (6.3%) Ripe fruits (1.6%)

Juvenile-1s (n=121)

Young leaves (66.7%) Unknown items (8.3%)Seeds (2.5%) Flowers (10%)Flower buds (1.7%) Unripe fruits (10.8%)

Infant-2s (n=23)

Young leaves (60.9%) Unknown items (8.7%)Flowers (8.7%) Unripe fruits (4.3%)Ripe fruits (17.6%)

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Figure 5.7 Monthly variation in time spent feeding by different age/sex class of SU1 at Sukau (n=534, weighted data)

Figure 5.8 Diurnal variation in time spent feeding by different age/sex class of SU1 at Sukau (n=534, weighted data)

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Figure 5.9 Percentage of different items in harem groups' diet at Abai (n=155, unweighted data)

Figure 5.10 Percentage of different items in all-male groups' diet at Abai (n=33, unweighted data)

Young leaves (49.7%) Unknown items (2.6%) Seeds (11.6%) Flowers (15.5%) Unripe fruits (20.6%)

Young leaves (72.7%) Unripe fruits (27.3%)

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Figure 5.11 A juvenile-2 male feeding on the inflorescence of Nypa fruticans (Arecaceae) at Abai

Figure 5.12 An adult male drinking water from the Kinabatangan River

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Figure 5.13 Monthly variation in plant parts eaten by N. larvatus groups at Abai (n=155, unweighted data).

Figure 5.14a Monthly variation in young leaves eaten (n=101, unweighted data), to that in the forest (n=300, phenology data), at Abai

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Figure 5.14b Monthly variation in flowers eaten (n=24, unweighted data), to that in the forest (n=300, phenology data), at Abai

Figure 5.14c Monthly variation in fruits eaten (n=59, unweighted data), to that in the forest (n=300, phenology data), at Abai

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Figure 5.15 Percentage of different items in harem groups' diet by age/sex class at Abai (n=154, unweighted data)

Adult males (n=10)

Young leaves (30%) Seeds (10%)

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Adult females (n=82)

Young leaves (51.2%) Flowers (14.6%)Unripe fruits (15.9%) Seeds (17.1%)Unknown items (1.2%)

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Young leaves (71.4%) Flowers (14.3%)

Unripe fruits (7.1%) Unknown items (7.1%)

Juvenile-1s (n=42)

Young leaves (45.2%) Flowers (11.9%)Unripe fruits (31%) Seeds (7.1%)Unknown items (4.8%)

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Figure 5.16 Monthly variation in time spent feeding by different age/sex class of harem groups at Abai (n=155, weighted data)

Figure 5.17 Condensed tannin (CT) + neutral detergent fibre (NDF) against protein content of plant samples eaten and not eaten

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CHAPTER 6: RANGING BEHAVIOUR

6.1 INTRODUCTION Like most animals, primates show a strong attachment to a particular area, known as

the home range. Many definitions of home range exist. In this thesis, home range refers to the entire area occupied by a social group during an entire year, over which the group travels in pursuit of its activities (Jewell, 1966). Furthermore, different investigators have used different methods to estimate or measure primate home ranges. Implicit to all, however, is the measurement of the area occupied by an individual or a group within a specified period.

There are several advantages for species to remain in a circumscribed area. Animals can become familiar with the distribution and phenological cycles of food plants, location of safe refuges and waterholes, and the shortest routes between resource patches (Dunbar, 1988).

There is rarely any uniformity in the way primates use their home range. Patterns of ranging behaviour have been found to be influenced by the distribution and abundance of food trees (Crook & Gartlan, 1966; Altmann, 1974; Chivers, 1974; Clutton-Brock, 1974; 1977b; Klein & Klein, 1975; 1977; Struhsaker, 1975; Homewood, 1976; Milton & May, 1976; Clutton-Brock & Harvey, 1977a & b; Struhsaker & Leland, 1979; Milton, 1980; Whitten, 1980; Marsh, 1981a; Raemaekers, 1980; 1981; Wrangham, 1981; McKey & Waterman, 1982; Harrison, 1983; Davies, 1984; Bennett, 1986b), phenology (Raemaekers, 1980; Marsh, 1981a; Stanford, 1991), body size (Milton & May, 1976; Clutton-Brock & Harvey, 1977b; Terborgh, 1983), group size (Chivers, 1969; Clutton-Brock & Harvey, 1977b; Terborgh & Janson, 1986; Supriatna et al., 1986; Crockett & Eisenberg, 1987; Olupot et al., 1994), groups’ movements on previous days (Fossey & Harcourt, 1977), location of night trees (Crook & Aldrich-Blake, 1968; Tenaza, 1975; Rasmussen, 1979; Gittins, 1979; 1983; Harrison, 1983; Davies, 1984), interaction between conspecific groups (Chivers, 1969; Fossey, 1974; Struhsaker, 1974; 1975; Waser, 1976; Sekulic, 1982), the need to patrol territorial boundaries (Whitten, 1982), and weather conditions (Chivers, 1974; Raemaekers, 1980; McKey and Waterman, 1982; Isbell, 1983). Moreover, the use of different vertical strata has been shown to vary with activity (Gautier-Hion et al., 1981; Whitten, 1982; Davies, 1984) and time of day (Chivers, 1974; Clutton-Brock, 1975).

The aim of this chapter is to describe the ranging patterns of N. larvatus groups in the Sukau and Abai study areas and their use of habitats in both areas. The factors that influence the patterns of home range use will be examined, particularly for SU1 at Sukau.

6.2 SUKAU STUDY AREA Ranging patterns and use of habitat at Sukau will be described for SU1 (section

4.2.1.2). Ninety-three out of 104 attempts at full-day follows at Sukau study area between January and December 1991 were on SU1. Only 53 of the full-day follows on SU1, however, were complete. A complete full-day follow was one when SU1 was followed without losing it from dawn, when the group left its sleeping trees, until dusk, when the group finally settled in its sleeping trees (section 2.10). This usually began at 0530 hours and ended at 1830 hours, approximately 13 hours of observations.

Daily ranging patterns of N. larvatus groups at Sukau were influenced by their habit of returning to the rivers every night. Groups generally moved inland, away from the river in the early morning, returning to trees next to the rivers before dusk.

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6.2.1 HOME RANGE SU1 used a large area. From January to December 1991, SU1 at Sukau entered 251

quadrats. This was derived from 93 days of observation. Each quadrat measured 100m x 100m, thus the home range of SU1, between January and December 1991 was 251ha. The one-hectare quadrat method of assessment, however, may give an overestimation of the home range size because it includes some quadrats that were only partially used by SU1. A grid map representing 0.25ha quadrats (50m x 50m) was superimposed over an aggregate map of the daily maps (figure 6.1). The area occupied by SU1 from January to December 1991 was then 220.5ha.

The cumulative number of one-hectare quadrats entered with time suggests that the total area occupied by SU1 had probably been recorded by the end of the study (figure 6.2). The graph shows an almost steady increase until September, when it levels out slightly, and then reaches a plateau by December. There was no indication that SU1 shifted its range over time. Furthermore, all quadrats entered at the beginning of the study were still being entered by the end of the study. The number of quadrats entered by SU1 in the months of January and December 1991 might have been more than observed; I could not observe SU1 throughout the day during those months due to severe rains and floods.

The home ranges of SU1 and other N. larvatus groups at Sukau completely overlapped one another. Many different groups frequently used the same food sources, night trees and travel routes (section 4.2.1.6). SU1 was never observed to use an area exclusive of other groups.

SU1 predominantly used the riverine forest. It infrequently travelled into lowland dipterocarp forest and into freshwater swamp forest. Neither SU1 nor any other N. larvatus group was seen to enter agricultural lands during the study period. There have been no reports to suggest otherwise. N. larvatus were also never seen to enter large areas by the Kinabatangan River that were lacking natural riverine vegetation, and comprised mainly tall grass and scrub. Similarly, the area on the northern bank by the river-mouth and the area a kilometre from the river-mouth of the Menanggul River were without natural riverside vegetation. These areas were intermittently used as log dumps for logging operations carried out in the area before and during this study. N. larvatus groups were never seen to use these areas.

6.2.2 DAY RANGE LENGTHS Members of SU1 spent 18.2% of their active period travelling (figure 4.6). The

distance travelled on any one day by SU1 was extremely variable (figure 6.3). The mean daily distance travelled in a sample of 53 complete full-day follows was 910m. The shortest day range length was recorded in September 1991 (370m) and the longest was recorded in August 1991 (1810m). The mean day range length varied between months (figure 6.4). SU1 had longer mean monthly day range lengths from April to August 1991, and in November 1991. The peaks were in May, August and November, and the lowest in October.

SU1 exhibited a wide variation in the distance travelled through the forest from one day to the next. Various factors contribute to ranging patterns in different primate species. Some of these factors were examined to gain an insight into the determinants of N. larvatus ranging patterns.

6.2.2.1 RAINFALL There was no correlation between monthly mean day range lengths of SU1 and

monthly total rainfall (rs=0.406, n=10, p>0.05). Correlations might suggest otherwise if there

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had been enough observations in December and January. A mean monthly figure, however, was not necessarily representative of what was happening each day. Thus, day range length was correlated with rainfall for those days. Even then, there was no correlation between day range length and rainfall on days with complete full-day follows (rs=0.210, n=53, p>0.05). There was no evidence to show that rainfall influences daily ranging patterns of SU1.

6.2.2.2 PHENOLOGY Day range lengths of SU1 were correlated with phenological patterns at Sukau to

examine the influence of plant part production, if any. There were no significant correlations between monthly mean day range lengths and the production of young leaves (rs=0.042, n=10, p>0.05). Neither were there any correlations between day range lengths and flower production (rs=0.079, n=10, p>0.05), and nor between day range lengths and fruit production (rs=0.055, n=10, p>0.05) for those months. Phenological patterns did not appear to influence the monthly mean day range lengths of SU1.

6.2.2.3 FOOD RESOURCES The proportions of different items in the diet were correlated with day range lengths

of SU1 on days when full-day follows were complete (n=53). This was to examine the influences of seasonally available food resources on day range lengths. There was no correlation in day range lengths with fruits plus seeds in the diet (rs=0.132, n=53, p>0.05). Similarly, there was no correlation between day range lengths and flowers in the diet (rs=0.230, n=53, p>0.05). With young leaves in the diet, however, there was a positive correlation (rs=0.34, n=53, p<0.05). This implied that SU1 travelled farther on days when there were higher proportions of young leaves in their diet. SU1 might have been feeding on young leaves of different plant species located in different areas, to reduce potential toxins from any one species (section 5.1). There were, however, no quantitative data to examine this. It was also possible that fruiting and flowering species were clumped. Thus, SU1 did not need to travel far to feed on fruits, seeds and flowers. Alternatively, it was possible that sources of young leaves were smaller than fruit sources.

6.2.3 QUADRAT USE SU1 did not use the quadrats evenly throughout the area. The mean number of one-

hectare quadrats used each day by SU1 was 10.38, i.e. 10.38ha (4.14% of the home range). The number of one-hectare quadrats used each day varied between four and 22 (figure 6.5). The mean number of quadrats used by SU1 each day varied from month to month (figure 6.6). The mean monthly number of quadrats used each day showed a similar trend to the mean monthly day range lengths. More quadrats were used each day from April to August 1991, and in November 1991. Thus, SU1 did not use its home range evenly in each month.

There was also variation in the total number of quadrats used each month by SU1 (figure 6.7). More quadrats were used in May and August, whereas January and December showed the least use of quadrats. Quadrat use by SU1 in the months of January and December may have been limited by the rains and floods. Conversely, data on quadrat use in those months were small (section 6.2.1).

Except four one-hectare quadrats, quadrats that were used for one percent of the time or more were located by the Menanggul River and the Kinabatangan River (figure 6.8). This strongly shows the dependency of N. larvatus on habitats that adjoined rivers. The west bank of the Kinabatangan River, and in particular both the north and south banks of the Menanggul River, where the two rivers meet were used intensively by SU1, except where there are cleared areas and houses.

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6.2.3.1 RAINFALL There was no correlation between monthly mean number of quadrats used by SU1

and monthly total rainfall (rs=0.212, n=10, p>0.05). Data were derived from complete full-day follows only (n=53). Thus, there was no indication that quadrat use by SU1 was influenced by rainfall each month.

6.2.3.2 PHENOLOGY The number of quadrats used each month by SU1 was tested against phenology at

Sukau to examine the influence of plant part production. There were no correlations between the number of quadrats used each month and the production of young leaves (rs=0.079, n=10, p>0.05). Neither was there any correlation between quadrats used and flower production (rs=0.171, n=10, p>0.05), nor between quadrats used and fruit production (rs=0.024, n=10, p>0.05). Data were derived from complete full-day follows (n=53). Thus, plant part production did not influence monthly mean number of quadrats used by SU1.

6.2.3.3 FOOD RESOURCES The number of quadrats used each month was correlated with the percent of various

food types in the diet of SU1 for that month. This was to see if SU1 used areas in relation to their dietary items. No correlation existed between quadrats used and young leaves in the diet (rs=0.154, n=12, p>0.05). There was a correlation, however, between the number of quadrats used and the percent of diet comprising fruits (rs=0.266, n=11, p<0.05). Similarly, there was a highly significant correlation between the number of quadrats used and the percent of diet comprising flowers (rs=0.857, n=8, p<0.005). Thus, SU1 used particular quadrats when feeding on fruits and flowers.

6.2.4 HEIGHT USE Most activities of SU1 were limited to a maximum height of 21m. The estimated

average and maximum canopy height at Sukau was 20m and 30m respectively. The mean feeding height was 11.2m with a range from one metre to 21m (figure 6.9). SU1 spent more than 50% its feeding time at heights between 10m and 16m. Similarly, SU1 spent more than 60% of its travelling time at heights between 10m and 17m. The mean height for travelling was 12.25m and ranged from ground level to 21m. The group occasionally travelled on the ground between tree patches (recorded at not more than 20m).

The mean height for resting was 12.48m and ranged from three to 21m. SU1 generally rested at heights greater than eight metres but less than 18m (84.2%). SU1 spent most of its time at heights of 14m and 15m, while engaging in feeding, travelling, and resting. This reflected the use of different parts of trees of the same general height for different major activities.

There was a slight variation in heights used by SU1 at different times of day (figure 6.10). The maximum mean height used was 14m at 0900 hours. The mean height used slowly declined to 10.5m at 1700 hours, then increased to nearly 12m at 1800 hours. There was, however, no correlation between height used and time of day (rs=0.160, n=14, p>0.05). This lack of correlation cannot be taken as an implication that N. larvatus were not influenced by diurnal variation in temperature. N. larvatus might have used trees that offered more shade during the hotter parts of the day. There are no quantitative data to look into this. Individuals, however, were observed to turn their backs toward the sun when resting during the mid-day hours.

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6.2.5 SWIMMING N. larvatus groups swam across the Menanggul River, almost daily. The river is about

20m wide. During initial attempts at habituation, a harem group swam across the river five times in a single day, all within a three-hour period, when my presence was detected. Between January to December 1991, SU1 swam across the Menanggul River on at least 31.2% of days (n=93). SU1 swam across the Kinabatangan River at least twice between January and December 1991. The river was about 150m wide at one point of crossing.

To cross the rivers at Sukau, N. larvatus individuals usually selected a tree branch that protruded into the river. From the tree branch, individuals leapt out, landing in the river with a great splash. Once they surfaced, the individuals swam across the remainder portion. They usually leapt from heights ranging from 5 to 15m.

6.3 ABAI STUDY AREA It was not possible to determine the home range sizes and day range lengths of N.

larvatus groups by full-day follows at Abai study area. This was mainly due to the nature of the habitat in that area. It was very muddy during low-tide, making silent and quick follows impossible. At high tide, the mangrove forest was under at least one metre of water and at some places it was 1.5m deep (section 2.10). Furthermore, identified groups were rarely seen with certainty. Thus, almost all observations were recorded along the river. Daily ranging patterns of N. larvatus groups at Abai were similar to that Sukau, in that they returned to the rivers every night.

6.3.1 HOME RANGE Nasalis larvatus groups were observed at a maximum perpendicular distance of 350m

away from the river. The maximum distance between sightings along the Merah River of an identified group, AB1 (section 4.3.1.1), was 4.5km. Assuming that the group used both sides of the river uniformly, therefore the home range of AB1 was expected to be 315ha. Over time, different N. larvatus groups were frequently seen using the same area, sleeping in the same night trees, using the same food sources and travelling along the same routes. This strongly suggests that the ranges of different groups overlap one another completely.

Nasalis larvatus groups at Abai were never seen using the riverside forest evenly throughout the area (figure 6.11). Groups were seen more often in the lower half of Merah River towards the Kinabatangan River. The riverside forest where the Kinabatangan River bends were the most favoured locations for night trees, particularly the bends east and opposite the river-mouth of Merah River. These bends usually have tree patches mainly of Sonneratia alba (Lythraceae) and Bruguiera spp. (Rhizophoraceae)

Although N. larvatus groups were observed to spend more nights in the mangrove forest, there were no data to determine whether they use the mangrove more than other habitat types.

6.3.2 HEIGHT USE Most activities of all N. larvatus groups at Abai study area were limited to a

maximum height of 20m. The estimated average and maximum canopy height at Abai was 15m and 25m. The mean feeding height was nine metres with a range from one metre to 20m (figure 6.12). Groups spent more than 70% feeding at heights between six metres and 15m. Similarly, they spent more than 80% travelling at heights between one metre and 11m. The mean height for travelling was 6.91m, ranging between one and 20m. More than 13% of travelling time was at one metre height. N. larvatus generally travelled along the bases of

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Nypa fruticans (Arecaceae). Although, N. larvatus groups often swam across the river, swimming was never recorded during the scan observations.

The mean height for resting was 9.10m and ranged from one metre to 20m. Groups generally rested at heights between four and 12m (83.6%). N. larvatus groups at Abai used similar heights for feeding and resting. Travelling, however, was generally at lower heights. This was probably because the bases of N. fruticans were easier to travel along than their fronds. This observation could be biased because animals can rarely be seen when they were in the fronds, but could easily be seen at the bases.

6.3.3 SWIMMING N. larvatus groups swam across the Merah River almost daily, which is at least 20m

wide at its widest point. The frequency of river crossings for each group could not be ascertained because the only known group AB1 was rarely identified with certainty (section 6.3.1). Once, a harem group and once a solitary adult male were observed swimming across the Kinabatangan River. Villagers occasionally reported seeing N. larvatus groups swimming across the Kinabatangan River at Abai, but it was never recorded during this study.

6.4 COMPARISON BETWEEN SITES The observed home range size of SU1 in riverine forest at Sukau (section 6.2.1) was

smaller than the estimated home range size of AB1 in mangrove forest at Abai (section 6.3.1). This difference was because the population density at Sukau was higher. When compared to Samunsam and Tanjung Puting (table 6.1), no two sites showed any similarity in terms of mean home range size, group size and population density. N. larvatus at Samunsam had the smallest group sizes, lowest population density, and largest home range sizes. Conversely, N. larvatus at Tanjung Puting had the smallest home range sizes and the highest population density. The group size of N. larvatus, however, was highest at Sukau.

These differences in range size might reflect the difference in habitat types and population density between sites. At all sites, however, ranges of different groups overlapped completely and groups returned to sleep by the rivers every evening.

6.5 DISCUSSION Nasalis larvatus groups in the Lower Kinabatangan area are wide-ranging, with

completely overlapping home ranges. This implies a high degree of inter-group tolerance and the absence of territorial behaviour. Davies and Houston (1984) defined territoriality as the defence of an area that is fixed in space, whereas Brown and Orians (1970) defined territoriality as the exclusion of one group by another from a resource, although the area itself was not defended. N. larvatus groups did not exhibit territorial behaviour by either definition, but can possibly be included in Kaufmann’s (1983) concept of territoriality as space-related dominance.

Theoretically, when animals exclude competitors by defending all or part of home range, they can maximise their access to resources. To predict whether primate species would be territorial, Mitani and Rodman (1979) devised an index of defendability. This index related day range length to the size of the home range, assuming its shape was approximately circular. The index was given as /√ 4 /π , where D=index of defendability, d=day range length (km), and A=home range area (km²). If D is at least one, the primate group is expected to be territorial, and if D is less than one, the primate group is expected to be non-territorial (Mitani & Rodman, 1979).

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The index of defendability of SU1 was calculated to be 0.54, implying that it was not possible for SU1 to be territorial, because it was not economical for it to defend its home range. Territorial behaviour should occur if the benefits of defending an area outweigh the costs (Brown, 1964). Furthermore, SU1 used only 4.14% of its home range daily (section 6.3.3), suggesting that its range was too large to be covered in a single day, and therefore defended.

Comparison of N. larvatus ranging patterns between sites showed variation in home range sizes between sites (section 6.4). The difference in home range sizes between sites is most likely due to the difference in habitat types, which in turn determine the distribution, size and availability of food sources for N. larvatus. The distribution, size and availability of food sources in turn influence group size, population density, and home range size. There are, however, other inter-related variables that influence home range size, such as the degree of overlap by different conspecific groups, and position of night trees.

The wide-ranging behaviour of N. larvatus groups at Samunsam implies a scarcity of food in the mixed riverine-mangrove forest there (Bennett, 1986a; Bennett & Sebastian, 1988). Scarce and unpredictable food supplies require individuals to move over considerable distances and these results in a large range size (Clutton-Brock & Harvey, 1977b). The forest at Samunsam is very heterogeneous, implying a seasonal availability of food. In the mangrove forest at Samunsam, food is always available to N. larvatus groups, but preferred food items in the riverine forest are more seasonal and scarce, and farther upriver. Thus, N. larvatus groups at Samunsam use different habitats at different seasons, migrating in and out of the mangroves (Bennett, 1986a; in press; Bennett & Sebastian, 1988). Seasonally impoverished habitats cause some primate species to migrate between distant seasonal ranges (Kummer, 1968; Dunbar & Dunbar, 1974; Wada & Ichiki, 1980; Terborgh, 1983; Schaller, 1985).

To maintain a high quality diet, some primates might increase day range length as high quality foods become scarcer (Clutton-Brock, 1977b; Bennett & Sebastian, 1988; Bennett, in press). Most primate species, however, are expected to decrease their day range lengths as high quality foods become scarce. Conforming to optimal foraging theories, these animals will then exploit low-quality food sources that are common (Schoener, 1971; Clutton-Brock, 1977b). Conversely, they will travel farther when their preferred food items are available (Clutton-Brock, 1975; McKey & Waterman, 1982; Bennett, 1983; 1986b).

Home range sizes of N. larvatus groups at Abai are much smaller than those at Samunsam, but larger than at Sukau and Tanjung Puting (section 6.4). The mangrove forest at Abai with extensive stands of Nypa fruticans (Arecaceae) (section 3.3.2), provide very little food for N. larvatus. The food trees, however, are highly clumped with large gaps between clumps. Although distances between tree clumps were not measured, the minimum distance was estimated to be about 200m. Thus, compared to Samunsam, N. larvatus at Abai did not need to travel far between food sources, therefore their smaller home range size.

By contrast, although there is some degree of clumping of food trees at Sukau, food is always available and abundant. Preferred food items might be scattered and seasonal. The day range lengths of SU1 increased on days when the group fed more young leaves, but the group did not travel far on days when their diet included a high proportion of fruits and seeds (section 6.3.2.2). Similarly, C. satanas (McKey & Waterman, 1982), P. [badius] rufomitratus (Marsh, 1981a) and S. entellus (Sugiyama, 1976) travel farther each day when feeding on low quality foods.

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In addition, SU1 entered particular quadrats when the group fed on flowers and fruits plus seeds, but did not select particular quadrats when feeding on young leaves (section 6.2.3.3). This probably resulted from an uneven distribution of high quality food sources. Some food sources, although common, were highly clumped. Mallotus muticus (Euphorbiaceae), for example, are commonly found along the Menanggul River (section 3.2.2.2 and 5.2.1).

At Tanjung Puting, the home range sizes of N. larvatus groups are small compared to Samunsam, Sukau and Abai (section 6.4), implying that food sources are highly abundant and available throughout the year (Yeager, 1989). Furthermore, the habitat at Tanjung Puting is not as heterogeneous, therefore could partly explain smaller home range sizes there.

Differences in the distribution, size and abundance of food resources between habitats are known to cause differential range size and patterns in primates (Struhsaker, 1967; Altmann, 1974; Clutton-Brock, 1977b; Oates, 1977a; Dawson, 1979; Freeland, 1979; Struhsaker & Leland, 1979; Kavanagh, 1981; Marsh, 1981a; McKey & Waterman, 1982; Bennett, 1983; 1986a & b; Davies, 1984). Some primate studies have shown that home range size decreases as food sources become more abundant (Struhsaker, 1967; 1978; Sugiyama, 1976; Freeland, 1979; McKey & Waterman, 1982; Terborgh, 1983).

Conversely, the wider an area over which a primate population’s food resources are spread, the greater is a group’s daily range length and annual home range size (Oates, 1987). Several studies have shown a negative correlation between habitat quality and home range size (Hall, 1963; Neville, 1968; Yoshiba, 1968; Gartlan & Brain, 1968; Altmann & Altmann, 1970; Clutton-Brock, 1972; Caldecott, 1986; Cords, 1987).

There is a possibility that home range sizes of N. larvatus groups at Tanjung Putting were underestimated. The method used to estimate home range size at Samunsam (Bennett, 1986a; Bennett & Sebastian, 1988), was similar to that used at Abai (section 6.3.1). Likewise, Yeager (1989) calculated N. larvatus groups’ home range size based on each group’s farthest sighting along a 2km stretch of river, and assuming that groups rarely travelled more than 500m away from the river, and that groups used both sides of the river. She, however, deducted known unused area from this estimate, and failed to consider that groups are known to travel much farther than 2km along a stretch of river.

Groups are, however, known to travel much farther than 2km along a stretch of river (Bennett, 1986a; Bennett and Sebastian, 1988; sections 6.2.1 & 6.3.1). This is also evidenced by the fact that known groups were encountered outside her study area (Yeager, 1991a & b). Furthermore, her follows of known groups ended at 1200 hours (Yeager, 1989; 1990a). This meant that beyond 1200 hours, groups could easily and frequently travel more than 500m away from the river.

Population density, however, is highest at Tanjung Puting (section 6.4), suggesting that food sources are highly abundant and available. The difference in population densities of N. larvatus at the four sites (section 6.4) is most likely due to differences in the distribution, size and availability of food sources. Some studies have shown that population density declines as habitats become increasingly impoverished (Gartlan & Brain, 1968; Yoshiba, 1968; Altmann & Altmann, 1970; Clutton-Brock, 1972; Struhsaker, 1975; Taub, 1977; Iwamoto, 1979; Freeland, 1979; Caldecott, 1980; 1986; Anderson, 1981; Menard et al., 1985; Mehlman, 1989).

Some studies have shown that patterns of ranging behaviour are also influenced by inter-group encounters (Chivers, 1969; Fossey, 1974; Struhsaker, 1974; 1975; Waser, 1976; Sekulic, 1982). The chance of a group meeting another is greater when the group has a longer

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day range length, unless groups avoid each other. N. larvatus groups frequently meet and travel together. It was, however, not possible to test whether inter-group encounters in the forest would influence daily ranging patterns of N. larvatus due to scarcity of data. Inter-group associations by the river were, however, tested (sections 4.2.1.6 and 4.3.1.5). Some groups actively associated with each other, implying that inter-group associations by the river might influence ranging patterns of N. larvatus.

6.6 SUMMARY 1. The home range size of SU1 at Sukau was 220.5ha, and AB1 at Abai was estimated to be

315ha. N. larvatus groups in both areas had ranges that overlapped each other completely.

2. Ranging patterns of SU1 were influenced by diet. Day range lengths increased when SU1 ate more young leaves. SU1 selected particular quadrats when they fed on flowers and fruits.

3. N. larvatus groups at Sukau and Abai frequently swam across the tributaries, and occasionally across the Kinabatangan River.

4. Comparison between four sites in Borneo where N. larvatus populations occur suggests that the small group size, low population density and large home range at Samunsam were due scarcity and seasonality of food resources.

5. Territorial behaviour was not observed in N. larvatus groups at Sukau and Abai. The index of defendability for SU1 at Sukau implied that it was not economical to defend its home range.

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Table 6.1 Summary of home range size, group size, and population density of N. larvatus at different sites Sukau Abai Samunsam Tanjung

Puting Home range size (ha) 220.5 315 900 137 Average group size (all group types) 14.3 10.5 9* 12.1 Population density (individuals/km²) 34.01 10 5.93 62.6 Biomass (kg/km²) 255.35 75.88 45 499.5

* harems only Sukau and Abai: Boonratana, 1993. Samunsam: Bennett, 1986a; Bennett and Sebastian, 1988. Tanjung Puting: Yeager, 1989.

Figure 6.1 All day ranges of SU1 at Sukau, Jan. – Dec. 1991 (n=93)

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Figure 6.2 Cumulative number of 1ha quadrats entered by SU1 at Sukau (n=93)

Figure 6.3 Frequency distribution of day range lengths of SU1 at Sukau (n=53)

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Figure 6.4 Mean monthly day range lengths of SU1 at Sukau (n=53)

Figure 6.5 Frequency distribution of 1ha quadrats entered by SU1 each day (n=53)

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Figure 6.7 Monthly total number of 1ha quadrats entered by SU1 at Sukau (n=93)

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Figure 6.8 Differential quadrat use by SU1 at Sukau from Jan. – Dec. 1991 (n=4966, weighted data)

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Figure 6.9 Height of SU1 at Sukau when engaged in major activities

Figure 6.10 Mean height of SU1 at different time of day at Sukau (n=4966, weighted data)

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Figure 6.11 Use of riverside habitat by N. larvatus groups at Abai (Feb. 1990 – Dec. 1991)

Freshwater swamps and riverine forest

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Figure 6.12 Height of N. larvatus groups at Abai when engaged in major activities

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CHAPTER 7: CONCLUDING DISCUSSION

7.1 INTRODUCTION The primary aims of this study were to assess the ecology and behaviour of N.

larvatus in relation to the botany and phytochemistry of the habitat flora and, more specifically, to compare their ecology and behaviour with N. larvatus groups at other sites. In this final chapter, I will describe the importance of the Lower Kinabatangan region, and then discuss broad recommendations for the conservation of N. larvatus in the Lower Kinabatangan, also topics for future research relevant to this study.

7.2 IMPORTANCE OF THE LOWER KINABATANGAN AREA The Kinabatangan floodplain is the largest and possibly the most important wetland in

Sabah (section 3.1.1). In addition, the area has the largest intact mangrove in the state measuring approximately 40,500ha (Scott, 1989). Furthermore, the ox-bow lakes, which are at various stages of infilling (section 3.1.1), add diversity and uniqueness to the different habitat types found in the area.

Most importantly, the Lower Kinabatangan area has a high diversity and abundance of wildlife, in particular primates, of which ten species are found in the area (section 3.2.1). Four are also Bornean endemics, namely Nasalis larvatus, Presbytis rubicunda, P. hosei and Hylobates muelleri. The Lower Kinabatangan is one of the only two known sites in Asia with ten primate species and one of only two known sites in the world with four sympatric colobines (section 3.2.1).

All eight species of hornbills found in Borneo have been recorded in the area. Five species of Bornean endemic birds occur here, namely Lonchura fuscans, Pityriasis gymnocephala, Ptilocichla leucogrammica, Cyornis superba and Pitta baudi. The ox-bow lakes are important breeding grounds for Anhinga melanogaster and Crocodylus porosus, both of which are becoming very rare in other parts of northern Borneo.

Furthermore, the Lower Kinabatangan region probably is the best site in the whole country for nature enthusiasts to see easily this highly diversified wild fauna, especially the amazing and unique “odd-nosed” colobine, N. larvatus. Spectacular evening riverside displays by harem and non-harem males, and river crossings by N. larvatus groups are common, particularly along the Menanggul River at Sukau.

7.3 CONSERVATION RECOMMENDATIONS The proposed Lower Kinabatangan Wildlife Reserve needs to be gazetted

immediately, to protect a significant proportion of the State’s largest population of N. larvatus (section 3.1.6). This would also protect its highly diversified and abundant wild fauna (sections 3.2.1, 3.3.1 and 7.2), different habitat types (sections 3.2.2, 3.3.2 and 7.2), fisheries and the livelihood of the local residents. It is also an important venue for the tourism industry, with N. larvatus being the major attraction.

Extensions of the proposed reserve need be made, however, to ensure long term conservation of a viable N. larvatus population. This would not only protect a larger forested area and other wildlife but also provide land corridors for the migratory routes to many larger mammals. Some required extensions are:

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1. a minimum of a 1km wide strip of all forested land in the Lower Kinabatangan region on both sides of the Kinabatangan River, its tributaries and ox-bow lake;

2. the vast mangrove forest in the deltaic region of the Kinabatangan River, therefore protecting the largest intact mangrove in the state.

Although hunting of N. larvatus in the Lower Kinabatangan area has never been reported (section 3.1.5), hunting for other wildlife frequently occurs (Boonratana, 1993a & b). Furthermore, with increasing number of immigrants working on oil palm plantations in the area, the demand for wild meat is expected to increase. The gazetting of a Lower Kinabatangan Wildlife Reserve alone does not guarantee that its wildlife is protected. Measures needed to ensure that hunting remains minimal should include regular patrolling and strict law enforcement. Regular patrolling and strict law enforcement would also deter encroachment and illegal felling of trees. Honorary guards comprising local residents can make up for the shortage of staff in the Sabah Wildlife Department.

In addition to protection and law enforcement, there is a need to increase people’s awareness of the value of forests and their wildlife, and the need to conserve them. This is particularly important for the local residents, who practice subsistence agriculture by clearing riverside forest, the prime habitat for N. larvatus (section 1.2.5).

One way to increase conservation awareness is by distributing posters depicting the animals and the penalties for hunting them. Another, probably more important, is by having dialogue sessions with villagers and plantation workers living near the forested areas. Conservation efforts would not be as effective without the support of local people.

7.4 FUTURE RESEARCH Although this study attempted to answer many questions about N. larvatus, there are

still many gaps in our knowledge about its ecology and behaviour. Indeed, many more questions arose from observations made. Thus, this study can be viewed as a foundation stone laid in the Lower Kinabatangan for other researchers to gather more information about N. larvatus and other species in the area. Suggested topics for future research on the ecology and behaviour of colobines in the Lower Kinabatangan include:

1. to re-study certain aspects of the ecology and behaviour of N. larvatus in pure mangrove forest at Abai, which this study was not able to determine, particularly in terms of ranging patterns. It might have been possible to habituate the animals had I spent more time at Abai, but this was not feasible, due to the nature of this study. Any researcher undertaking this venture would need to focus his/her attention only at Abai. Furthermore, since identified animals could rarely be seen with certainty due to the foliage, when the animals were in the fronds of Nypa fruticans (Arecaceae), a few mature individuals of different groups should be marked with colour dyes using marker pistols;

2. a continuation of the study on SU1 at Sukau is recommended, to look deeper into the ecology and behaviour of N. larvatus groups in riverine forest. This would not only extend the findings of this study, but also allow changes in group composition over time be observed, and ultimately the mechanisms involved in male and female dispersal. Furthermore, there is a need to identify food trees and their location as this information probably can ascertain the influence of food resources on the behaviour and social organisation of N. larvatus groups. More food samples should be collected and analysed for their phytochemistry, therefore providing insight into the mechanism underlying the selection of food items.

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3. to study differential habitat use by four sympatric colobines at Sukau. This can even be extended to include all ten primate species found there. A study comparing different species within the same habitat will reveal many aspects about their phylogeny, physiological and morphological adaptations, habitat use, ecology and behaviour. This ultimately will help clarify the mechanisms underlying species coexistence and their proximate factors at the community level, and the possible consequences of these mechanisms affecting population dynamics of these sympatric primates.

7.5 CONCLUSIONS It is unlikely that any single factor influences the behaviour, social structure and

population density of N. larvatus. Many variables are inter-related, although the size, availability and abundance of food resources might be the ultimate influence. This is clear when comparing the ecology and behaviour of N. larvatus between habitats. N. larvatus makes a very good ecological model, allowing us to gain knowledge into the relationship between animals and their habitat flora. Studies of primates and wildlife should include some conservation aspects, because species might become extinct before we can understand their ecology and behaviour.

7.6 SUMMARY 1. The Lower Kinabatangan region has the largest floodplain and the largest intact

mangrove in Sabah, with many ox-bow lakes. It also has a high diversity and abundance of wildlife, particularly primates.

2. Protection of the area by gazetting the Lower Kinabatangan Wildlife Reserve should receive the highest priority, to protect a significant proportion of the state’s largest population. With necessary extensions, the area will also protect a diversity of flora and fauna.

3. Other activities needed to ensure effective protection and management of the reserve include regular patrolling and strict law enforcement to ensure that hunting and land encroachment remains minimal, also an awareness of the importance of conservation.

4. A continuation of N. larvatus studies in the mangrove forest at Abai and on the focal group, SU1, in the riverine forest at Sukau are needed to fill many gaps about N. larvatus ecology and behaviour. Furthermore, a continued monitoring of SU1 is likely to provide insight into N. larvatus social organisation, particularly the mechanisms underlying male and female dispersal.

5. A study comparing different species within the same habitat will help clarify the mechanisms underlying species coexistence and their proximate factors at the community level, and the possible consequences of these mechanisms affecting population dynamics of these sympatric primates.

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APPENDIX I: LIST OF WILD FAUNA RECORDED AT SUKAU

Mammals Common name Scientific name Common Treeshrew Tupaia glis Slender Treeshrew Tupaia gracilis Striped Treeshrew Tupaia dorsalis Large Treeshrew Tupaia tana Dusky Roundleaf Bat Hipposideros ater Large Flying Fox Pteropus vampyrus Slow Loris Nycticebus coucang Western Tarsier Tarsius bancanus Hose's Langur Presbytis hosei Maroon Langur Presbytis rubicunda rubicunda

P.r. chrysea Silvered Langur Trachypithecus cristatus Proboscis Monkey Nasalis larvatus Long-tailed Macaque Macaca fascicularis Pig-tailed Macaque Macaca nemestrina Bornean Gibbon Hylobates muelleri Orangutan Pongo pygmaeus Pangolin Manis javanica Giant Squirrel Ratufa affinis Prevost's Squirrel Callosciurus prevostii Plantain Squirrel Callosciurus notatus Ear-spot Squirrel Callosciurus adamsi Horse-tailed Squirrel Sundasciurus hippurus Slender Squirrel Sundasciurus tenuis Plain Pigmy Squirrel Exilisciurus exilis Low's Squirrel Sundasciurus lowii House Rat Rattus rattus Sun Bear Helarctos malayanus Yellow-throated Marten Martes flavigula Malay Weasel Mustela nudipes Ferret Badger Melogale personata Malay Badger Mydaus javanicus Smooth Otter Lutra perspiciallata Oriental Small-clawed Otter Aonyx cinerea Malay Civet Viverra tangalunga Common Palm Civet Paradoxurus hermaphroditus Banded Civet Hemigalus derbyanus

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Mammals Common name Scientific name Small-toothed Palm Civet Arctogalidia trivirgata Short-tailed Mongoose Herpestes brachyurus Collared Mongoose Herpestes semitorquatus Clouded Leopard Neofelis nebulosa Marbled Cat Felis marmorata Flat-headed Cat Felis planiceps Leopard Cat Felis bengalensis Asian Elephant Elephas maximus Sumatran Rhinoceros Dicerorhinus sumatrensis Bearded Pig Sus barbatus Lesser Mouse-Deer Tragulus javanicus Greater Mouse-Deer Tragulus napu Sambar Deer Cervus unicolor Banteng Bos javanicus Common Barking Deer Muntiacus muntjak

Birds Common name Scientific name Oriental Darter Anhinga melanogaster Great-billed Heron Ardea sumatrana Purple Heron Ardea purpurea Great Egret Egretta alba Intermediate Egret Egretta intermedia Little Egret Egretta garzetta Chinese Egret Egretta eulopholes Cattle Egret Bubulcus ibis Little Heron Butorides striatus Yellow Bittern Ixobrychus sinensis Cinnamon bittern Ixobrychus cinnamomeus Black Bittern Ixobrychus flavicollis Storm's Stork Cicona stormi Jerdon's Baza Aviceda jerdoni Crested Honey-Buzzard Pernis ptilorhynchus Brahminy Kite Haliastur indus Crested Goshawk Accipiter trivirgatus White-bellied Sea-Eagle Haliaeetus leucogaster Grey-headed Fish-Eagle Ichthyophaga ichthyaetus Lesser Fish-Eagle Ichthyophaga humilis Crested Serpent-Eagle Spifornis cheela

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Birds Common name Scientific name Osprey Pandion haliaetus Chestnut-necklaced Partridge Arborophila charltonii Crested Partridge Rollulus rouloul Crested Fireback Lophura ignita Great Argus Argusianus argus White-breasted Waterhen Amaurornis phoenicurus Common Sandpiper Actitis hypoleucos Large Green Pigeon Treron capellei Thick-billed Pigeon Treron curvirostra Cinnamon-headed Pigeon Treron fulvicollis Little Green Pigeon Treron olax Pink-necked Pigeon Treron vernans Jambu Fruit-Dove Ptilinopus jambu Green Imperial Pigeon Ducula aenea Grey Imperial Pigeon Ducula pickeringi Zebra Dove Geopilea striata Emerald Dove Chalcophaps indica Long-tailed Parakeet Psittacula longicauda Blue-crowned Hanging-Parrot Loriculus galgulus Hodgson's Hawk-Cuckoo Cuculus fugax Moustached Hawk-Cuckoo Cuculus vagans Plaintive Cuckoo Cuculus merulinus Violet Cuckoo Chrysococcyx xanthorhynchus Drongo Cuckoo Surniculus lugubris Raffle's Malkoha Phaenicophaeus chlorophaeus Red-billed Malkoha Phaenicophaeus javanicus Chestnut-breasted Malkoha Phaenicophaeus curvirostris Greater Coucal Centropus sinensis Short-toed Coucal Centropus rectunguis Lesser Coucal Centropus bengalensis Sunda Ground-Cuckoo Carpococcyx radiceus Reddish Scops-Owl Otus rufescens Buffy Fish-Owl Ketupa ketupu Brown Wood-Owl Strix leptogrammica Gould's Frogmouth Batrachostomus stellatus Malaysian Eared Nightjar Eurostopodus temminckii Glossy Swiftlet Collocalia esculenta Asian Palm-Swift Cypsiurus balasiensis Whiskered Treeswift Hemiprocne comata

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Birds Common name Scientific name Diard's Trogon Harpactes diardii Red-naped Trogon Harpactes kasumba Scarlet-rumped Trogon Harpactes duvaucelii Banded Kingfisher Lacedo pulchella Rufous-collared Kingfisher Actenoides concreta Ruddy Kingfisher Halcyon coromanda Stork-billed Kingfisher Halcyon capensis Common Kingfisher Alcedo atthis Blue-eared Kingfisher Alcedo meninting Black-backed Kingfisher Ceyx erithacus Rufous-backed Kingfisher Ceyx rufidorsus Blue-throated Bee-eater Merops viridis Blue-tailed Bee-eater Merops philippinus Dollarbird Eurystomus orientalis White-crowned Hornbill Berenicornis comatus Bushy-crested Hornbill Anorrhinus galeritus Wrinkled Hornbill Rhyticeros corrugatus Wreathed Hornbill Rhyticeros undulatus Black Hornbill Anthracoceros malayanus Pied Hornbill Anthracoceros coronatus Rhinoceros Hornbill Buceros rhinoceros Helmeted Hornbill Rhinoplax vigil Brown Barbet Calorhamphus fulignosus Red-crowned Barbet Megalaima rafflesii Red-throated Barbet Megalaima mystacophanos Blue-eared Barbet Megalaima australis Rufous Piculet Sasia abnomis Crimson-winged Woodpecker Picus puniceus Banded Woodpecker Picus miniaceus Rufous Woodpecker Celeus brachyurus Brown-capped Woodpecker Picoldes moluccensis Buff-necked Woodpecker Meiglyptes tukki Grey-and-Buff Woodpecker Hemicircus concretus Common Goldenback Dinoplum javaense Olive-backed Woodpecker Dinoplum rafflesii White-bellied Woodpecker Dryocopus javensis Great Slaty Woodpecker Mulleripicus pulverulentus Orange-backed Woodpecker Reinwardtipicus validus Black-and-Red Broadbill Cymbirhynchus macrorhynchus

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Birds Common name Scientific name Black-and-Yellow Broadbill Eurylaimus ochromalus Banded Broadbill Eurylaimus javanicus Garnet Pitta Pitta granetina Blue-headed Pitta Pitta baudi Banded Pitta Pitta guajana Hooded Pitta Pitta sordida Pacific Swallow Hirundo tahitica Barn Swallow Hirundo rustica Black-winged Flycatcher-shrike Hemipus hirundinaceus Bar-winged Flycatcher-shrike Hemipus picatus Ashy Minivet Pericrocotus divaricatus White-breasted Wood-swallow Artamus leucorhynchus Common Iora Aegithina tiphia Lesser Green Leafbird Chloropsis cyanopogon Greater Green Leafbird Chloropsis sonnerati Asian Fairy-Bluebird Irena puella Puff-backed Bulbul Pycnonotus eutilotus Black-and-White Bulbul Pycnonotus melanoleucos Black-headed Bulbul Pycnonotus atriceps Straw-headed Bulbul Pycnonotus zeylanicus Yellow-vented Bulbul Pycnonotus goiavier Cream-vented Bulbul Pycnonotus simplex Spectacled Bulbul Pycnonotus erythropthalmos Grey-cheeked Bulbul Criniger bres Yellow-bellied Bulbul Criniger phaeocephalus Finsch's Bulbul Criniger finschii Hairy-backed Bulbul Hypsipetes criniger Streaked Bulbul Hypsipetes malaccensis Buff-vented Bulbul Hypsipetes charlotte Rufous-tailed Shama Copsychus pyrropygus Magpie Robin Copsychus saularis White-rumped Shama Copsychus malabaricus White-crowned Forktail Enicurus leschenaulti Malaysian Rail-Babbler Eupetes macrocerus Black-capped Babbler Pellorneum capistratum Short-tailed Babbler Trichastoma malaccense White-chested Babbler Trichastoma rostratum Ferruginous Babbler Trichastoma bicolor Horsefield's Babbler Trichastoma sepiarium

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Birds Common name Scientific name Abbott's Babbler Trichastoma abbotti Rufous-crowned Babbler Melacopteron magnum Scaly-crowned Babbler Melacopteron cinereum Sooty-capped Babbler Melacopterum affine Grey-breasted Babbler Melacopterum albogulare Bornean Wren-Babbler Ptilocichla leucogrammica Striped Wren-Babbler Kenopia striata Striped Tit-Babbler Macronous gularis Fluffy-backed Tit-Babbler Macronous ptilosus Grey-headed Babbler Stachyris poliocephala Black-throated Babbler Stachyris nigricollis Chestnut-rumped Babbler Stachyris maculata Chestnut-winged Babbler Stachyris erythroptera Rufous-fronted Babbler Stachyris rufifrons Brown Fulvetta Alcippe brunneicauda White-bellied Yuhina Yuhina zantholeuca Flyeater Gerygone sulphurea Yellow-bellied Prinia Prinia flaviventris Dark-necked Tailorbird Orthotomus atrogularis Rufous-tailed Tailorbird Orthotomus sericeus Ashy Tailorbird Orthotomus ruficeps Pied Fantail Rhipidura javanica Blue-and-White Flycatcher Cyanoptila cyanomelana White-tailed Flycatcher Cyornis concreta Malaysian Blue Flycatcher Cyornis turcosa Sunda Blue Flycatcher Cyornis caerulata Bornean Blue Flycatcher Cyornis superba Rufous-chested Flycatcher Ficedula dumetoria Rufous-winged Flycatcher Philentoma pyrhopterum Maroon-breasted Flycatcher Philentoma velatum Black-naped Monarch Hypothymis azurea Asian Paradise-Flycatcher Terpsiphone paradisi Yellow-breasted Flowerpecker Prionochilus maculatus Scarlet-backed Flowerpecker Dicaeum cruentatum Orange-bellied Flowerpecker Dicaeum trigonostigma Plain Sunbird Anthreptes simplex Brown-throated Sunbird Anthreptes malacensis Ruby-cheeked Sunbird Anthreptes singalensis Purple-naped Sunbird Hypogramma hypogrammicum

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Birds Common name Scientific name Crimson Sunbird Aethopyga siparaja Scarlet Sunbird Aethopyga mystacalis Little Spiderhunter Arachnothera longirostra Thick-billed Spiderhunter Arachnothera crassirostris Long-billed Spiderhunter Arachnothera robusta Hill Myna Gracula religiosa Bornean Bristle-head Pityriasis gymnocephala Eurasian Tree Sparrow Passer montanus Pin-tailed Parrotfinch Erythrura prasina Tawny breasted Parrotfinch Erythrura hyperythra Dusky Munia Lonchura fuscans Chestnut Munia Lonchura malacca Crow-billed Drongo Dicrurus annectans Bronzed Drongo Dicrurus aeneus Greater Racket-tailed Drongo Dicrurus paradiseus Black-hooded Oriole Oriolus xanthornus Dark-throated Oriole Oriolus xanthonotus Crested Jay Platylophus galericulatus Slender-billed Crow Corvus enca

Reptiles Common name Scientific name Dog-toothed Cat Snake Boiga cynodon Mangrove Snake Boiga dendrophila Puff-faced Water Snake Homalopsis buccata Yellow Racer Gonyosoma sp. Indo-chinese Rat Snake Pytas korros Reticulated Python Python reticulatus Wagler's Pit Viper Trimeresurus wagleri Blue-necked Keelback Macropisthodon rhodomelas Crested Green Lizard Calotes cristatellus Common Skink Mabuya multifasciata Blue-eyed Crested Lizard Goniocephalus sp. Flying Lizard Draco sp. Common House Gecko Hemidactylus frenatus Flying Gecko Ptychozoon homalocephalum Giant Forest Gecko Gekko stentor Striped Tree Skink Lamprolepis vittatus Monitor Lizard Varanus varanus

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Reptiles Common name Scientific name Water Monitor Lizard Varanus salvator Estuarine Crocodile Crocodylus porosus Malaysian Giant Turtle Orlitia borneensis Malayan Box Turtle Cuora amboinensis Malayan Flat-shelled Turtle Notochelys platynota

Amphibians Common name Scientific name Greater Swamp Frog Rana ingeri Green Paddy Frog Rana erthraea Cricket Frog Rana nicobariensis White-lipped Frog Rana chalconata

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APPENDIX II: LIST OF WILD FAUNA RECORDED AT ABAI

Mammals Common name Scientific name Hose's Langur Presbytis hosei Maroon Langur Presbytis rubicunda rubicunda

P.r. chrysea Silvered Langur Trachypithecus cristatus Proboscis Monkey Nasalis larvatus Long-tailed Macaque Macaca fascicularis Pig-tailed Macaque Macaca nemestrina Bornean Gibbon Hylobates muelleri Orangutan Pongo pygmaeus House Rat Rattus rattus Smooth Otter Lutra perspicilliata Binturong Arctictis binturong Asian Elephant Elephas maximus Sumatran Rhinoceros Dicerorhinus sumatrensis Bearded Pig Sus barbatus Greater Mouse-Deer Tragulus napu Sambar Deer Cervus unicolor Banteng Bos javanicus

Birds Common name Scientific name Oriental Darter Anhinga melanogaster Purple Heron Ardea purpurea Great Egret Egretta alba Intermediate Egret Egretta intermedia Chinese Egret Egretta eulophotes Cattle Egret Bubulcus ibis Little Heron Butorides striatus Storm's Stork Ciconia stormi Lesser Adjutant Leptoptilos javanicus Bat Hawk Macherhamphus alcinus Brahminy Kite Haliastur indus White-bellied Sea-Eagle Haliacetus leucogaster Crested Serpent-Eagle Spifornis cheela Crested Fireback Lophura ignita Great Argus Argusianus argus White-breasted Waterhen Amaurornis phoenicurus

154

Birds Common name Scientific name Malaysian Plover Charadrius peronii Common Sandpiper Actitis hypoleucos Cinnamon-headed Pigeon Treron fulvicollis Little Green Pigeon Treron olax Jambu Fruit-Dove Ptilinopus jambu Green Imperial Pigeon Ducula aenea Grey Imperial Pigeon Ducula pickeringi Long-tailed Parakeet Psittacula longicauda Chestnut-breasted Malkoha Phaenicophaeus curvirostris Greater Coucal Centropus sinensis Silver-rumped Swift Raphidura leucopygialis Asian Palm-Swift Cypsiurus balasiensis Whiskered Treeswift Hemiprocne comata Collared Kingfisher Halcyon chloris Black-capped Kingfisher Halcyon pileata Stork-billed Kingfisher Halcyon capensis Blue-eared Kingfisher Alcedo meninting Blue-throated Bee-eater Merops viridis Dollarbird Eurystomus orientalis White-crowned Hornbill Berenicornis comatus Bushy-crested Hornbill Anorrhinus galeritus Wrinkled Hornbill Rhyticeros corrugatus Wreathed Hornbill Rhyticeros undulatus Black Hornbill Anthracoceros malayanus Pied Hornbill Anthracoceros coronatus Rhinoceros Hornbill Buceros rhinoceros Helmeted Hornbill Rhinoplax vigil Red-throated Barbet Megalaima mystacophanos Yellow-crowned Barbet Megalaima henricii Blue-eared Barbet Megalaima australis Rufous Piculet Sasia abnormis Brown-capped Woodpecker Picoldes moluccensis Common Goldenback Dinopium javanense White-bellied Woodpecker Dryocopus javensis Greater Goldenback Chrysocolaptes lucidus Black-and-Red Broadbill Cymbirhynchus macrorhynchus Pacific Swallow Hirundo tahitica Green Iora Aegithina viridissima Common Iora Aegithina tiphia

155

Birds Common name Scientific name Lesser Green Leafbird Chloropsis cyanopogon Black-headed Bulbul Pycnonotus atriceps Magpie Robin Copsychus saularis White-rumped Shama Copsychus malabaricus Abbott's Babbler Trichastoma abbotti Chestnut-rumped Babbler Stachyris maculata Ashy Tailorbird Orthotomus ruficeps Pied Fantail Rhipidura javanica Malaysian Blue Flycatcher Cyornis turcosa Asian Paradise Flycatcher Terpsiphone paradisi Velvet-fronted Nuthatch Sitta frontalis Copper-throated Sunbird Nectarina calcostetha Hill Myna Gracula religiosa Bornean Bristle-head Pityriasis gymnocephala Dusky Munia Lonchura fuscans Crow-billed Drongo Dicrurus annectans Greater Racket-tailed Drongo Dicrurus paradiseus Black-hooded Oriole Oriolus xanthornus Slender-billed Crow Corvus enca

Reptiles Common name Scientific name Water Monitor Lizard Varanus salvator Estuarine Crocodile Crocodylus porosus

156

APPENDIX III: TREE SPECIES AND THEIR PROPORTIONS IN THE BOTANICAL TRANSECTS AT SUKAU (N=1378).


% Total Stems

% Total Basal Area

Alangiaceae Alangium ebenaceum 4 0.3 0.09Anacardiaceae Buchanania insignis 56 4.1 2.77Anacardiaceae Dracontomelon mangiferum 1 0.1 0.03Annonaceae Cananga odorata 3 0.2 0.77Annonaceae Phaenthus crassipetalus 3 0.2 0.14Annonaceae Polyalthia glauca 7 0.5 0.33Apocynaceae Alstonia angustifolia 1 0.1 0.02Apocynaceae Alstonia angustiloba 1 0.1 0.02Bombacaceae Coelostegia griffithii 1 0.1 0.02Bombacaceae Durio grandiflorus 1 0.1 0.12Burseraceae Canarium apertum 51 3.7 3.27Clusiaceae Cratoxylum sumatrana 47 3.4 5.28Clusiaceae Cratoxylum borneensis 1 0.1 0.04Clusiaceae Calophyllum borneensis 51 3.7 2.08Clusiaceae Calophyllum canum 12 0.9 0.57Clusiaceae Garcinia bancana 12 0.9 0.39Clusiaceae Garcinia forbesii 1 0.1 0.02Combretaceae Terminalia foetidissima 8 0.6 1.20Datisaceae Octomeles sumatrana 6 0.5 0.27Dilleniaceae Dillenia excelsa 1 0.1 0.35Dilleniaceae Dillenia grandifolia 98 7.1 2.30Dilleniaceae Dillenia indica 7 0.5 0.18Dipterocarpaceae Dipterocarpus applanatus 4 0.3 0.46Dipterocarpaceae Dipterocarpus caudiferus 7 0.5 0.94Dipterocarpaceae Dipterocarpus stellatus 1 0.1 0.03Dipterocarpaceae Dryobalanops lanceolata 2 0.1 0.28Dipterocarpaceae Hopea nervosa 2 0.1 0.63Dipterocarpaceae Parashorea melaanonan 1 0.1 0.03Dipterocarpaceae Parashorea tomentalla 2 0.1 0.04Dipterocarpaceae Shorea beccariana 7 0.5 0.24Dipterocarpaceae Shorea faguetina 1 0.1 0.01Dipterocarpaceae Shorea glaucescens 2 0.1 0.04Dipterocarpaceae Shorea inappendiculata 1 0.1 0.08Dipterocarpaceae Shorea leprosula 8 0.6 1.64Dipterocarpaceae Shorea macroptera 4 0.3 0.64

157


% Total Stems

% Total Basal Area

Dipterocarpaceae Shorea platyclados 1 0.1 0.16Dipterocarpaceae Shorea scrobiculata 2 0.1 0.08Dipterocarpaceae Shorea smithiana 2 0.1 2.40Dipterocarpaceae Shorea xanthophylla 1 0.1 0.05Dipterocarpaceae Vatica acrocarpa 7 0.5 0.56Dipterocarpaceae Vatica oblongifolia 38 2.8 1.91Ebenaceae Diospyros pendula 38 2.8 2.45Elaeocarpaceae Elaeocarpus canipes 13 0.9 0.76Euphorbiaceae Bacaurea bracteata 7 0.5 0.18Euphorbiaceae Bacaurea parviflora 27 1.9 0.49Euphorbiaceae Baccaurea pubera 2 0.1 0.05Euphorbiaceae Erismanthus multonii 2 0.1 0.02Euphorbiaceae Glochidion borneensis 39 2.8 1.98Euphorbiaceae Koilodepos leavigatum 2 0.1 0.04Euphorbiaceae Macaranga conifera 18 1.3 0.38Euphorbiaceae Macaranga hypoleuca 11 0.8 0.23Euphorbiaceae Mallotus muticus 76 5.5 10.95Fagaceae Lithocarpus lucidus 1 0.1 0.03Flacourtiaceae Homalium foetidum 6 0.4 0.46Flacourtiaceae Hydnocarpus woodii 14 1.0 1.70Irvingiaceae Irvingia malayana 3 0.2 0.45Lauraceae Alseodaphne bancana 1 0.1 0.03Lauraceae Beilschmiedia micrantha 1 0.1 0.01Lauraceae Cryptocarya cuneata 1 0.1 0.12Lauraceae Eusideroxylon zwageri 10 0.8 2.86Lauraceae Litsea firma 15 1.1 0.83Lauraceae Litsea odorifera 81 5.9 4.26Lauraceae Notaphoebe kingiana 3 0.2 0.21Lauraceae Phoebe macrophylla 1 0.1 0.03Lecythidaceae Baringtonia lanceolata 31 2.3 0.99Leguminosae Albizzia chinensis 1 0.1 0.04Leguminosae Albizzia pedicellata 1 0.1 0.02Leguminosae Fordia cf. gibbsiae 5 0.4 0.16Leguminosae Intsia palembica 1 0.1 0.42Leguminosae Koompassia excelsa 1 0.1 0.24Leguminosae Parkia speciosa 1 0.1 0.14Leguminosae Sindora irpicina 5 0.4 0.14Leguminosae Spatholobus hirsutus 1 0.1 0.02

158


% Total Stems

% Total Basal Area

Leguminosae Sympetalandra borneensis 6 0.4 0.56Melastomaceae Kibessia galeata 55 4.0 6.42Meliaceae Aglaia ignea 6 0.4 0.14Meliaceae Amoora malaccensis 3 0.2 0.15Meliaceae Chisocheton beccariana 2 0.1 0.30Moraceae Artocarpus dadah 1 0.1 0.02Moraceae Artocarpus elasticus 1 0.1 0.04Moraceae Artocarpus tamaran 4 0.3 0.09Moraceae Ficus condensa 12 0.9 2.60Myristicaceae Knema latifolia 14 1.0 0.73Myrtaceae Syzygium bankense 122 8.9 8.90Olacaceae Scorodocarpus borneensis 1 0.1 0.14Polygalaceae Xanthophyllum rufum 18 1.3 1.20Rhizophoraceae Carallia brachiata 2 0.1 0.04Rosaceae Atuna elata 2 0.1 0.15Rosaceae Parinari oblongifolia 2 0.1 0.08Rubiaceae Anthocephalus chinensis 27 2.0 3.62Rubiaceae Neonauclea bernadoi 90 6.5 5.43Rutaceae Meliocope confusa 5 0.4 0.07Sapindaceae Nephelium beccarianum 1 0.1 0.01Sapindaceae Paranephelium nitidum 3 0.2 0.09Sapotaceae Palaquium rostratum 6 0.5 0.11Sapotaceae Payena lucida 12 0.9 0.39Sonneratiaceae Duabanga moluccana 6 0.4 0.69Sterculiaceae Heritiera borneensis 3 0.2 0.09Sterculiaceae Heritiera elata 2 0.1 0.03Sterculiaceae Heritiera littoralis 1 0.1 0.21Sterculiaceae Pterospermum elongatum 25 1.8 2.21Tiliaceae Microcos antidesmifolia 21 1.6 0.99Tiliaceae Pentace adenophora 1 0.1 0.04Tiliaceae Pentace borneensis 3 0.2 0.24Tiliaceae Pentace erectinervia 4 0.3 0.44Verbenceae Teijsmanniodendron bogoriense 2 0.1 0.13Verbenceae Teijsmanniodendron sympliciodes 10 0.7 0.25Verbenceae Vitex pinnata 20 1.5 1.89

159

APPENDIX IV: TREE SPECIES AND THEIR PROPORTIONS IN THE BOTANICAL TRANSECTS AT ABAI (N=300).


% Total Stems

% Total Basal Area

Anacardiaceae Buchanania insignis 22 7.4 3.93Anacardiaceae Mangifera pajang 1 0.3 1.55Annonaceae Polyalthia glauca 9 3.0 2.99Apocynaceae Alstonia angustifolia 10 3.3 1.50Burseraceae Canarium apertum 12 4.0 3.16Clusiaceae Calophyllum borneensis 6 2.0 0.71Clusiaceae Calophyllum canum 4 1.3 0.85Clusiaceae Cratoxylum sumatrana 2 0.7 0.21Clusiaceae Garcinia bancana 1 0.3 0.13Combretaceae Terminalia foetidissima 2 0.7 2.01Dilleniaceae Dillenia excelsa 9 3.0 0.79Dipterocarpaceae Shorea leprosula 3 1.0 0.68Dipterocarpaceae Vatica oblongifolia 3 1.0 0.21Dipterocarpaceae Vatica papuana 1 0.3 0.13Ebenaceae Diospyros evana 2 0.7 0.19Ebenaceae Diospyros pendula 6 2.0 0.66Elaeocarpaceae Elaeocarpus canipes 25 8.3 6.90Euphorbiaceae Baccaurea pubera 6 2.0 1.35Euphorbiaceae Glochidion borneensis 2 0.7 0.58Euphorbiaceae Macaranga conifera 2 0.7 0.10Flacourtiaceae Homalium foetidum 3 1.0 0.76Lauraceae Litsea odorifera 4 1.3 1.23Lecythidaceae Barringtonia lanceolata 1 0.3 0.09Leguminosae Sindora irpicina 1 0.3 0.10Melastomaceae Kibessia galeata 42 14.0 8.05Moraceae Artocarpus dadah 1 0.3 0.48Moraceae Ficus condensa 7 2.3 14.23Myrtaceae Syzygium bankense 34 11.3 5.99Polygalaceae Xanthophyllum rufum 12 4.0 3.61Rhizophoraceae Bruguiera sexangula 16 5.3 19.51Rhizophoraceae Ceriops tagal 3 1.0 0.35Rubiaceae Neonauclea bernadoi 5 1.7 3.91Rutaceae Evoida confusa 1 0.3 0.29Sapotaceae Ganua motleyana 1 0.3 0.08Sapotaceae Madhuca burkiana 1 0.3 0.12

160


% Total Stems

% Total Basal Area

Sapotaceae Palaquium rostratum 2 0.7 0.35Sapotaceae Planchonella obovata 1 0.3 0.11Sterculiaceae Heritieria littoralis 7 2.3 4.34Thymelaeaceae Gonystylus keithii 5 1.7 0.89Verbenceae Teijsmanniodendron

sympliociodes 1 0.3 0.39

Verbenceae Vitex pinnata 24 8.0 4.87

161

APPENDIX V: RESULTS OF PHYTOCHEMICAL ANALYSES OF PLANT ITEMS COLLECTED AT SUKAU AND ABAI (ADAPTED FROM LOH, 1991).

Family/Species Part ALK SAP %N %P %CT %NDF Anacardiaceae Melanochyla sp. ML - - 0.23 1.44 1.76 56.8 Anisophylleaceae Anisophyllea sp. ML - 1+ 0.30 1.88 0.35 56.8Annonaceae Goniothalamus roseus ML - 1+ 0.34 2.13 0.30 82.6Polyalthia insignis ML - - 0.29 1.81 0.35 80.5Polyalthia glauca ML - - 0.25 1.56 9.15 56.5Apocynaceae Willughbeia aff. coriacea ML - 1+ 0.19 1.19 4.47 52.6Burseraceae Dacroyodes aff. rugosa ML - - 0.24 1.50 0.94 62.7Clusiaceae Garcinia aff. parviflora ML 3+ 1+ 0.20 1.25 2.35 41.7Garcinia aff. parviflora YL 3+ ? 0.27 1.69 2.47 36.2Garcinia aff. parviflora FR ? 1+ 0.21 1.31 1.30 50.4Dipterocarpaceae Dipterocarpus aff. caudiferus ML - - 0.20 1.25 0.94 62.6Vatica sp. A ML - - 0.31 1.94 2.59 52.9Vatica sp. A YL - - 0.35 2.19 2.82 47.8Vatica sp.B ML - - 0.34 2.13 2.23 65.1Dilleniaceae Dillenia indica ML - 1+ 0.28 1.75 0.24 64.2Dillenia indica YL - - 0.31 1.94 0.24 62.3Dillenia indica FL - - 0.19 1.19 0.12 62.9Ebenaceae Diospyros lanceifolia ML - 2+ 0.31 1.94 0.47 58.0Diospyros frutescens ML - 2+ 0.27 1.69 0.00 69.6Diospyros levigata ML - 1+ 0.39 2.44 13.52 70.8Diospyros levigata YL - ? 0.78 4.88 1.53 66.0Diospyros pendula ML - - 0.26 1.63 0.12 56.0Diospyros pendula FR ? 3+ 0.27 1.69 3.65 53.2Diospyros sp. B ML - - 0.36 2.25 1.88 72.4Elaeocarpaceae Elaeocarpus canipes ML - - 0.27 1.68 0.82 52.5Euphorbiaceae Aporusa sp. ML - - 0.27 1.68 0.12 41.8

162

Family/Species Part ALK SAP %N %P %CT %NDF Aporusa sp YL - 1+ 0.39 2.44 0.24 52.6Aporusa elmeri ML - 2+ 0.25 1.56 1.53 61.8 Aporusa elmeri FR ? ? 0.25 1.56 5.53 52.3Aporusa frutescens ML - 1+ 0.28 1.75 1.06 45.5Aporusa frutescens FR ? 3+ 0.22 1.38 1.30 62.1Antidesma neurocarpus ML - 1+ 0.18 1.13 1.06 54.0Antidesma neurocarpus YL - ? 0.28 1.75 0.00 47.8Baccaurea parviflora ML - 3+ 0.28 1.75 0.00 65.7Baccaurea parviflora YL - ? 0.37 2.31 0.24 55.3Baccaurea parviflora FR - ? 0.21 1.31 3.18 72.9Baccaurea sp. ML - 2+ 0.25 1.56 0.47 57.7Baccaurea sp. FR - ? 0.26 1.63 2.00 48.8Chaetocarpus aff. castanocarpus ML - 1+ 0.29 1.81 0.47 67.4Claoxylon sp. A ML - - 0.14 0.88 2.71 61.1Claoxylon sp. A YL - - 0.67 4.19 0.47 57.2Cleistanthus sp. ML - 1+ 0.28 1.75 1.05 47.6Croton argyratus ML - - 0.39 2.44 0.35 62.9Croton oblongifolius ML - 2+ 0.46 2.88 0.94 63.8Croton oblongifolius YL - ? 0.54 3.38 0.94 71.4Croton sp ML - 1+ 0.36 2.25 0.47 57.9Croton sp YL - 1+ 0.43 2.69 0.00 68.0Croton sp FL ? 1+ 0.16 1.00 0.35 74.0Drypetes sp. ML - 2+ 0.15 0.94 12.60 62.0Macaranga beccariana ML - - 0.25 1.56 1.88 63.7Mallotus penangensis ML 3+ 1+ 0.53 3.31 5.29 58.4Mallotus penangensis FR ? - 0.15 0.94 0.00 82.5Mallotus wrayi ML - 1+ 0.43 2.69 0.12 56.2Mallotus wrayi YL - 1+ 0.48 3.00 0.00 65.7Mallotus sp. A ML - - 0.35 2.19 0.47 76.8Mallotus sp. A YL - - 0.55 3.44 0.00 69.7Mallotus muticus ML - 1+ 0.27 1.69 0.00 59.6Mallotus muticus YL - ? 0.46 2.88 0.35 55.1Mallotus muticus FR ? 1+ 0.23 1.44 0.47 62.7Mallotus sp. B ML - - 0.34 2.13 2.58 61.9Mallotus sp. B YL - ? 0.69 4.31 0.00 45.7Mallotus sp. C ML - 2+ 0.59 3.69 0.00 39.9Mallotus sp. C YL - - 0.67 4.19 0.00 30.9Phyllanthodendron sp. ML - 2+ 0.46 2.88 0.35 45.3Phyllanthodendron sp. YL - 1+ 0.36 2.25 0.58 39.1Sapium aff. indicum ML - 2+ 0.35 2.19 0.00 63.7

163

Family/Species Part ALK SAP %N %P %CT %NDF Vatica sp. B FR ? 1+ 0.12 0.75 2.23 59.2Euphorbiaceae sp. B FR ? 2+ 0.21 1.31 6.70 54.6Euphorbiaceae sp. C FR ? ? 0.15 0.94 0.35 67.5Fagaceae Lithocarpus lucidus ML - 1+ 0.43 2.68 1.06 60.5Lithocarpus lucidus YL - ? 0.46 2.88 0.00 50.8Flacourtiaceae Homalium foetidum ML - - 0.23 1.44 30.34 40.6Hydnocarpus woodii ML - 1+ 0.31 1.94 3.65 67.0Flacortiaceae sp. ML 1+ - 0.25 1.56 12.11 75.3Gnetaceae Gnetum gnemon ML - 1+ 0.26 1.63 0.47 34.6Gnetum gnemon FR - 1+ 0.13 0.81 2.12 41.6Hyporicaceae Cratoxylum aff. formosum ML - - 0.30 1.88 1.29 47.8Lauraceae Cinnamomum griffithi ML - 1+ 0.23 1.44 0.35 49.6Litsea odorifera ML 1+ 3+ 0.22 1.38 16.11 73.9 YL 1+ ? 0.41 2.56 13.41 56.3Lauraceae sp. ML - - 0.29 1.81 12.94 72.1Lecythidaceae Barringtonia aff. macrostachys ML - - 0.27 1.69 0.82 58.2 YL - - 0.27 1.69 0.58 45.8Barringtonia sp. A ML - 1+ 0.23 1.44 1.88 51.2Barringtonia sp. A YL - 1+ 0.26 1.63 0.58 47.4Barringtonia lanceolata ML - - 0.28 1.77 0.24 56.3Barringtonia lanceolata YL - 2+ 0.48 3.00 0.00 55.2Barringtonia sp. B FL ? ? 0.40 2.50 0.12 39.2Fabaceae Fabaceae sp. ML - - 0.34 2.13 18.94 69.5Spantholobus hirsutus ML - 2+ 0.73 4.56 0.00 91.5Loganiceae Fagraea aff. racemosa ML - 1+ 0.24 1.50 0.00 83.0Lythraceae Sonneratia alba ML - - 0.33 2.06 5.15 52.2Sonneratia alba FR - - 0.28 1.75 0.35 67.0Melastomataceae Kibbesia azurea ML - ? 0.27 1.69 1.88 53.7Kibessia sp. A ML - - 0.36 2.25 0.35 45.3Kibessia galeata ML - - 0.23 1.44 0.00 41.4

164

Family/Species Part ALK SAP %N %P %CT %NDF Meliaceae Aglaia sp. ML - 2+ 0.72 4.50 0.25 62.5Sapindaceae Pometia aff. pinnata ML - 1+ 0.22 1.38 2.94 45.9Pometia aff. pinnata YL - 1+ 0.50 3.13 0.47 42.2Moraceae Ficus sp. A ML - 1+ 0.20 1.25 0.35 62.9Poikilospermum aff. cordifolium ML - 1+ 0.29 1.81 0.00 61.9Poikilospermum aff. cordifolium YL - 1+ 0.36 2.25 1.53 55.9Poikilospermum aff. cordifolium FR ? 1+ 0.29 1.81 0.47 51.8Poikilospermum aff. cordifolium FL - 1+ 0.33 2.06 0.23 66.3Myristicaceae Knema aff. laurina ML - - 0.18 1.13 6.35 68.6Knema latifolia ML - 2+ 0.36 2.25 3.41 76.0Myrisnaceae Ardisia polyactis ML - 2+ 0.14 0.88 5.70 37.9Myrtaceae Eugenia sp. A ML - 1+ 0.24 1.50 0.35 66.2Eugenia sp. B ML - 3+ 0.32 2.00 0.47 48.6Eugenia sp. C ML 2+ - 0.21 1.31 0.71 67.9Eugenia sp. E ML - 1+ 0.37 2.31 0.71 59.0Eugenia sp. F ML - 2+ 0.26 1.63 0.94 57.8Eugenia sp. G ML - 1+ 0.22 1.38 0.94 60.3Eugenia sp. J ML - 1+ 0.18 1.13 0.71 74.6Eugenia sp. M ML - - 0.28 1.75 2.94 69.9Syzygium sp. ML - 4+ 0.19 1.19 0.25 55.3Myrtaceae sp. ML - ? 0.24 1.50 4.23 78.9Oleaceae Chionanthus cuspidita ML - 1+ 0.22 1.38 13.29 72.7Chionanthus cuspidita YL - - 0.25 1.56 0.35 70.7Polygalaceae Xanthophyllum affine ML - 1+ 0.27 1.69 0.35 65.6 FR ? ? 0.33 2.06 0.12 70.9Xanthophyllum aff. affine ML - - 0.34 2.13 0.24 78.7Xanthophyllum aff. affine YL - ? 0.36 2.25 0.35 84.2Xanthophyllum aff. affine FR ? ? 0.41 2.56 0.35 84.1Xanthophyllum cordatum ML - 1+ 0.42 2.63 0.71 72.9Xanthophyllum cordatum FR - ? 0.37 2.31 0.35 88.3Xanthophyllum rufun ML - 1+ 0.25 1.56 0.00 69.1Xanthophyllum rufun ML - 1+ 0.34 2.13 0.00 66.4

165

Family/Species Part ALK SAP %N %P %CT %NDF Xanthophyllum rufun YL - ? 0.48 3.00 0.24 87.7Xanthophyllum sp. C ML - 1+ 0.38 2.38 0.35 83.3Xanthophyllum sp. M ML - ? 0.23 1.44 0.24 73.1Rhizophoraceae Carallia brachiata ML - - 0.24 1.50 1.18 43.7Rhamnaceae Zizyphus horsifieldii ML - 1+ 0.24 1.50 27.15 59.8Zizyphus horsifieldii FR ? 1+ 0.22 1.37 0.35 64.0Rosaceae Rosaceae sp. A ML ? ? 0.31 1.94 0.12 39.0Rosaceae sp. A YL - - 0.23 1.44 0.35 35.2Rubiaceae Neonauclea bernardoi ML - 1+ 0.32 2.00 2.82 52.6Neonauclea bernardoi YL - 1+ 0.38 2.38 0.47 42.4Pleiocarpidia aff. capitata ML - - 0.30 1.88 0.47 48.9Pleiocarpidia aff. capitata FL - ? 0.30 1.88 0.47 46.2 Sapotaceae Madhuca sp. ML - 2+ 0.23 1.44 1.88 51.1Payena sp ML - - 0.32 2.00 1.77 67.2Styracaceae Styracaceae sp. ML - - 0.24 1.50 0.95 62.5Theaceae Pyrenaria parviflora ML - ? 0.17 1.06 22.34 40.7Pyrenaria parviflora YL - 1+ 0.22 1.38 4.35 37.7Tiliaceae Microcos antidesmofolia YL - 1+ 0.42 2.63 0.35 89.6Microcos sp. A ML - 1+ 0.17 1.06 1.41 64.2Microcos sp. A YL - ? 0.43 2.69 0.47 82.2Microcos sp. B ML - 1+ 0.27 1.69 2.82 67.2Microcos sp. B YL - 1+ 0.37 2.31 0.60 59.3Pentace laxiflora ML - - 0.25 1.56 23.76 69.5Verbenaceae Vitex pinnata ML - ? 0.42 2.63 0.47 61.4

ALK: Alkaloid SAP: Saponins %N: Percent nitrogen %P: Percent protein

%CT: Percent condensed tannin %NDF: Percent neutral detergent fibre ML: Mature leaves YL: Young leaves FR: Fruits FL: Flowers

0: Absent ?: Indeterminate 1+, 2+, 3+ & 4+: Positive reactions (semi -quantitative analysis)

Documents

Boonratana, R. 1993a. The ecology and behaviour of the proboscis monkey (Nasalis larvatus) in the Lower Kinabatangan, Sabah. Unpublished doctoral dissertation, Mahidol University