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 Unpublished Doctoral Dissertation, Mahidol University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
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. Pornchai Matangkasombut, Ph.D.

Dean Dean
Faculty of Graduate Studies Faculty of Science
Mahidol University Mahidol University
i
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]
ii
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
Vithoon Viyanant, Ph.D

Monthree Chulasamaya, M.D., Ph.D Director
Dean Graduate Study Program
Faculty of Graduate Studies Department of Biology, Faculty of Science
iii
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.
iv
FRONTISPIECE
A resting adult male Nasalis larvatus displaying an erect penis in the mangrove forest of the
Lower Kinabatangan
v
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).
vi
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
vii
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
viii
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
ix
4.3 ABAI STUDY AREA.......................................................................................................... 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
4.3.2.1 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
4.5.2 Dispersal ................................................................................................................. 57
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
x
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
Figure 4.3a Percent time different number of individuals were within 5m of subject at
Figure 4.3b Percent time different number of individuals were within 5m of subject at
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
Figure 4.14a Percent time different number of individuals was within 2.5m of subject at
Figure 4.14b Percent time different number of individuals was within 2.5m of subject at
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
xi
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
Figure 5.8 Diurnal variation in time spent feeding by different age/sex class of SU1 at
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
xii
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
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
xiii
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
xiv
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
xv
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
xvi
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.
xvii
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).
1
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
2
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,
3
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
4
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
5
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.
6
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.
7
Figure 1.1a Map of Southeast Asia
Figure 1.1b Map of Sabah
8
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
9
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.
10
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.
11
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
12
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.
13
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;
14
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.
15
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.
16
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.
17
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.
18
Figure 2.1 Sukau and Abai showing natural features
19
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
20
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.
21
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
22
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
23
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.
24
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
25
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%).
26
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).
27
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).
28
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.
29
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.
30
Table 3.1 Population size of N. larvatus in the Lower Kinabatangan area
Location Survey length (km) N
Mumiang to Abai 40 82
Kuala Kinabatangan Besar to Abai 40 82
Abai to Sukau 50 128
Sukau to Bilit 35 154
Merah River 12 84
Resang/Sapasidom River 6 44
Menanggul River 10 146
Tenegang Besar River 12 95
Kelananap Lake 17
Total 832
31
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 0.09 154.72
Anacardiaceae 4.1 2.80 333.49
Annonaceae 0.9 1.24 643.93
Apocynaceae 0.1 0.04 152.19
Bombacaceae 0.1 0.14 477.49
Burseraceae 3.7 3.27 434.94
Clusiaceae 9.0 8.38 457.97
Combretaceae 0.6 1.20 1014.75
Datiscaceae 0.4 0.27 307.10
Dilleniaceae 7.8 2.83 180.63
Dipterocarpaceae 6.7 10.21 742.19
Ebenaceae 2.8 2.46 427.84
Elaeocarpaceae 0.9 0.76 397.08
Euphorbiaceae 13.4 14.32 527.57
Fagaceae 0.1 0.03 231.98
Flacourtiaceae 1.5 2.16 732.21
Irvingiaceae 0.2 0.45 1021.80
Lauraceae 8.2 8.35 500.84
Lecythidaceae 2.2 0.99 215.36
Leguminosae 1.6 2.04 626.28
Melastomaceae 4.0 6.42 791.63
Meliaceae 0.8 0.59 361.93
Moraceae 1.3 2.76 1040.67
Myristicaceae 1.0 0.73 350.94
Myrtaceae 8.8 8.90 498.62
Olacaceae 0.1 0.14 980.19
Polygalaceae 1.3 1.20 451.10
Rhizophoraceae 0.1 0.04 151.79
Rosaceae 0.3 0.23 386.72
Rubiaceae 8.5 9.07 520.68
Rutaceae 0.4 0.07 99.57
Sapindaceae 0.3 0.10 164.00
Sapotaceae 1.3 0.50 187.81
Sonneratiaceae 0.4 0.69 783.90
Sterculiaceae 2.2 2.55 556.75
Tiliaceae 2.1 1.71 398.96
Verbenaceae 2.3 2.27 495.77
32
Table 3.3 Abundance and basal area of fifteen commonest tree species at Sukau
Family Species No. of % Total Basal % Total
Stems Stems Area (cm²) Basal
Area
Myrtaceae Eugenia bankensis 122 8.9 60313.75 8.90
Dilleniaceae Dillenia grandifolia 98 7.1 15680.12 2.31
Rubiaceae Neonauclea bernadoi 90 6.5 36811.30 5.43
Lauraceae Litsea odorifera 81 5.9 28877.22 4.26
Euphorbiaceae Mallotus muticus 76 5.5 74230.78 10.95
Anacardiaceae Buchanania insignis 56 4.1 18801.98 2.77
Melastomaceae Kibessia galeata 55 4.0 43539.54 6.42
Burseraceae Canarium apertum 51 3.7 22182.11 3.27
Clusiaceae Calophyllum borneensis 50 3.6 14084.78 2.08
Clusiaceae Cratoxylum sumatrana 47 3.4 35801.92 5.28
Euphorbiaceae Glochidion borneensis 39 2.8 13417.40 1.98
Ebenaceae Diospyros pendula 38 2.8 16593.65 2.45
Dipterocarpaceae Vatica oblongifolia 38 2.8 12973.86 1.91
Lecythidaceae Barringtonia lanceolata 31 2.3 6676.22 0.99
Rubiaceae Anthocephalus chinensis 27 2.0 24542.31 3.62
Total 899 65.3 424503.87 62.72
33
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 5.48 287.58
Annonaceae 3.0 2.99 400.62
Apocynaceae 3.3 1.50 181.00
Burseraceae 4.0 3.16 318.06
Clusiaceae 4.3 1.90 176.56
Combretaceae 0.7 2.01 1212.17
Dilleniaceae 3.0 0.79 106.46
Dipterocarpaceae 2.3 2.66 458.13
Ebenaceae 2.7 0.85 127.75
Elaeocarpaceae 8.3 6.90 333.23
Euphorbiaceae 3.3 2.03 272.17
Lauraceae 1.3 1.23 372.71
Lecythidaceae 0.3 0.09 108.91
Leguminosae 0.3 0.10 121.00
Melastomaceae 14.0 8.05 231.50
Moraceae 2.7 14.71 2220.57
Myrtaceae 11.3 5.99 212.92
Polygalaceae 4.0 3.61 363.66
Rhizophoraceae 6.3 19.86 1262.33
Rubiaceae 1.7 3.91 943.55
Rutaceae 0.3 0.29 336.12
Sapotaceae 1.7 0.66 132.92
Sterculiaceae 2.3 4.34 748.78
Thymelaeaceae 1.7 0.89 215.24
Verbenaceae 8.3 5.26 254.08
34
Table 3.5 Abundance and basal area of fifteen commonest tree species at Abai
Family Species No. of % Total Basal Area % Total
Stems Stems (cm²) Basal Area
Melastomaceae Kibessia galeata 42 14.0 9723.22 8.05
Myrtaceae Eugenia bankensis 34 11.3 7239.14 5.99
Elaeocarpaceae Elaeocarpus canipes 25 8.3 8330.86 6.90
Verbenaceae Vitex pinnata 24 8.0 5880.19 4.87
Anacardiaceae Buchnania insignis 22 7.4 4752.09 3.93
Rhizophoraceae Bruguiera sexangula 15 5.0 23558.60 19.51
Burseraceae Canarium apertum 12 4.0 3816.70 3.16
Polygalaceae Xanthophyllum rufum 12 4.0 4363.96 3.61
Apocynaceae Alstonia angustifolia 10 3.3 1810.02 1.50
Dilleniaceae Dillenia excelsa 9 3.0 58.15 0.79
Annonaceae Polyalthia glauca 9 3.0 3605.57 2.99
Moraceae Ficus condensa 8 2.3 17189.74 14.23
Euphorbiaceae Baccaurea pubera 6 2.0 1627.68 1.35
Clusiaceae Calophyllum borneensis 6 2.0 855.31 0.71
Ebenaceae Diospyros pendula 6 2.0 797.93 0.66
Total 240 79.6 94509.16 78.25
35
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
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)
36
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
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)
37
Table 3.8 Summary of phytochemical analyses of plant parts at Lower Kinabatangan
Mature Young Flowers Fruits
leaves leaves
% Organic Mean 0.29 0.42 0.28 0.24
Nitrogen Range 0.14-0.73 0.22-0.78 0.16-0.4 0.12-0.41
Std. 0.10 0.14 0.10 0.08
deviation
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. 0.64 0.87 0.62 0.49
deviation
Condensed Mean 3.27 1.05 0.26 1.71
Tannins (mg/g) Range 0-30.34 0-13.41 0.12-0.47 0-6.7
Std. 6.06 2.41 0.15 1.94
deviation
% Neutral Mean 60.58 56.37 57.72 63.02
Detergent Fibres Range 34.6-91.5 30.9-89.6 39.2-74 41.6-88.3
Std. 11.64 15.45 14.5 13.07
deviation
Alkaloids 0 91 30 3 5
1+ 2 1
2+ 1
3+ 2 1
4+
Saponins 0 35 8 1 2
1+ 37 11 2 6
2+ 15 1 1
3+ 3 2
4+ 1
0: absent; 1+, 2+, 3+, & 4+: positive reactions (semi-quantitative analysis)
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)
Mature leaves Young leaves
Mean Std. Mean Std.
deviation 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
35
30
Temperature (in Celsius)
25
20
15
10
0
Feb-90
Apr-90
May-90
Sep-90
Oct-90
May-91
Oct-91
Mar-90
Aug-90
Nov-90
Dec-90
Feb-91
Apr-91
Mar-91
Aug-91
Sep-91
Nov-91
Dec-91
Jan-90
Jun-90
Jul-90
Jan-91
Jun-91
Jul-91
Months
Minimum Maximum
Figure 3.1 Mean monthly maximum and minimum temperatures for 1990 and 1991
39
Total Rainfall (in mm)
10
1
100
1000
Jan-90
0
100
200
300
400
500
600
700
Feb-90
Jan-90
Mar-90
Feb-90
Apr-90 Mar-90
May-90 Apr-90
Jun-90 May-90
Jul-90 Jun-90
Dry period
Aug-90 Jul-90
Sep-90 Aug-90
Oct-90 Sep-90
Transitional period
Figure 3.3 Klimagraph for 1990 and 1991

Oct-90
Temperature (˚C)
Nov-90
Wet period
Nov-90
40
Dec-90
Figure 3.2 Monthly rainfall for 1990 and 1991

Jan-91 Dec-90
Jan-91
Feb-91
Months Feb-91
Mar-91
Mar-91
Apr-91
Rainfall (mm)
Apr-91
May-91
May-91
Jun-91
Jun-91
Jul-91
Jul-91
Aug-91
Aug-91
Sep-91
Sep-91
Oct-91
Oct-91
Nov-91
Nov-91
Dec-91 50
Dec-91
1
Cumulative number of species % trees
(n=1378)
0
0
1
10
100
0
100
120
20
40
60
80
0
30-39
40-49
50-59
60-69
at Sukau (n=1,378)
70-79
80-89
200
90-99
100-109
110-119
120-129
130-139
140-149
400
150-159
160-169
170-179
180-189
190-199
200-209
600
210-219
41
220-229
230-239
240-249
250-259
GBH (cm)
260-269
800
270-279
Number of tree stems

280-289
290-299
300-309
310-319
320-329
1000
330-339
340-349
350-359
360-369
370-379
1200
380-389
390-399
400-409
410-419
420-429
430-439
1400
440-449
Figure 3.4 Frequency distribution of girths at breast height of transect trees at Sukau
Figure 3.5 Number of tree species against the number of trees sampled in the transects
% trees % trees
(n=300)
10
1
100
0.1
1
100
10
30-39 Mar-90
40-49 Apr-90
50-59
60-69 May-90
70-79
80-89 Jun-90
90-99
100-109 Jul-90
110-119
Aug-90
120-129
130-139 Sep-90
140-149
150-159 Oct-90
160-169
170-179 Nov-90
180-189
190-199 Dec-90
42
200-209
Young leaves
Jan-91
210-219
220-229 Feb-91
Figure 3.6 Phenological patterns at Sukau (n=500)

Months
230-239
GBH (cm)
240-249 Mar-91
250-259 Flowers
260-269 Apr-91
270-279
May-91
Fruits
280-289
290-299 Jun-91
300-309
310-319 Jul-91
320-329
330-339 Aug-91
340-349
350-359 Sep-91
360-369 Oct-91
370-379
380-389 Nov-91
390-399
400-409 Dec-91
Figure 3.7 Frequency distribution of girths at breast height of transect trees at Abai
410-419
45
40
35
Cumulatve number of species
30
25
20
15
10
0
0 50 100 150 200 250 300
Number of tree stems
Figure 3.8 Number of tree species against the number of trees sampled in the transects
at Abai (n=300)
100
% trees
10
1
Apr-90
May-90
Sep-90
Oct-90
Dec-90
Apr-91
May-91
Oct-91
Dec-91
Mar-90
Aug-90
Nov-90
Feb-91
Mar-91
Aug-91
Sep-91
Nov-91
Jun-90
Jul-90
Jan-91
Jun-91
Jul-91
Months
Young leaves Flowers Fruits
Figure 3.9 Phenological patterns at Abai (n=300)
43
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
2.5
1.5
%
0.5
0
Mature leaves Young leaves Flowers Fruits
Plant parts
Figure 3.11a Mean levels of crude protein in plant parts analysed
44
3.5
2.5
2
mg/g
1.5
0.5
0
Plant parts
Figure 3.11b Mean levels of condensed tannins in plant parts analysed
64
62
60
58
%
56
54
52
Plant parts
Figure 3.11c Mean levels of neutral detergent fibre in plant parts analysed
45
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-
46
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:
47
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).
48
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.
49
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.
50
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
51
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
4.3.1.1 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.
52
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.
53
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).
4.3.2.1 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
54
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,
55
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

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
56
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.
57
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.
58
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).

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
59
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
60
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
61
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.
62
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 3
A♀ 8 7 7 8 8 6
SA♂ 2 2 3
SA♀ 1 1 1 1 1
J2♂ 2 3 2
J2♀ 1 3 2 1 1 2
J2? 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)
63
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
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) 382
A♀ 3.7 (5) 26.2 (35) 0.4 (10) 3.0 (5) 29.5 (25) 25.1 (15) 12.2 (5) 2540
SA♀ 11.4 (5) 78.6 (40) 0 (5) 0 (5) 9.9 (25) 0 (15) 0 (5) 33
J2 4.7 (5) 70.5 (40) 0.9 (10) 3.6 (0) 13.9 (25) 4.3 (15) 1.9 (5) 259
J1 3.1 (5) 76.5 (40) 0 (10) 1.5 (5) 14.6 (20) 2.8 (15) 1.3 (5) 1071
I2 0.4 (5) 89.8 (40) 0.6 (10) 1.1 (5) 3.2 (25) 4.2 (10) 0.6 (5) 491
I1 0 (5) 94.0 (40) 0 (10) 0.6 (5) 1.8 (25) 1.4 (10) 2.3 (5) 190
infant
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)
Distance Observed Predicted
OMGs Non-OMGs SU2 SU7 All Groups
≤50m 0.438 0.375 0.365 0.292 0.604 0.31
≤100m 0.521 0.552 0.385 0.438 0.677 0.59
(same side of river)
≤100m 0.542 0.573 0.396 0.458 0.688 0.59
(opposite sides of
river)
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)
Aggresso Recipient Total
r 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
infant; ♂♀=one male group; ♂♂=non breeding group (all males and predominantly males);
☺=observer; ☻=Macaca nemestrina
65
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
infant
66
Table 4.7 Summary of copulatory bouts of N. larvatus at Sukau
Date Group No. of Duration Harass Comments
mounts (seconds)
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.
67
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
infant
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 0 9.0 9.6 3.7 0 63
(50) (7.1) (7.1) (14.3) (14.3) (7.1)
A♀ 5.9 22.7 0 5.4 27 24.9 6.9 488
(7.1) (42.9) (7.1) (7.1) (14.3) (14.3) (7.1)
SA♀ 0 33.5 0 66.5 0 0 0 3
(7.1) (50) (7.1) (7.1) (14.3) (14.3) (7.1)
J2 2.7 56.5 2.6 10.4 15.4 12.3 0 90
(7.1) (50) (7.1) (0) (14.3) (14.3) (7.1)
J1 1.1 64.5 0 4.5 22.6 5.7 0.8 230
(7.1) (50) (7.1) (7.1) (7.1) (14.3) (7.1)
I2 0 77.7 0 2.8 10.9 7.4 0.6 114
(7.1) (50) (7.1) (7.1) (14.3) (7.1) (7.1)
I1 0 100 0 0 0 0 0 33
(7.1) (50) (7.1) (7.1) (14.3) (14.3) (0)
infant
68
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
infant
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
infant
69
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 Common Uncommon Common Common
within 100m (% (70%) (20%) (70%) (65.5%)
nights)
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.
70
120
100
80
% scans
60
40
20
0
0 >0-1 >1-2 >2-3 >3-4 >4-5
Distance (metres)
Adult Male Adult Female Subadult Female
Figure 4.1a Percent time nearest neighbour was within cumulative distance from
subject at Sukau (n=4966, weighted data)
120
100
80
% scans
60
40
20
0
0 >0-1 >1-2 >2-3 >3-4 >4-5
Distance (metres)
Juvenile-2 Juvenile-1 Infant-2 Infant-1
Figure 4.1b Percent time nearest neighbour was within cumulative distance from
subject at Sukau (n=4966, weighted data)
71
40
35
30
25
% scans
20
15
10
0
0 1 2 3 4 5 6 7 8 9 10 >10
Number of Individuals
Figure 4.2a Percent time different number of individuals were within 2.5m of subject at
Sukau (n=4966, weighted data)
45
40
35
30
% scans
25
20
15
10
0
0 1 2 3 4 5 6 7 8 9 10 >10
Number of individuals
Figure 4.2b Percent time different number of individuals were within 2.5m of subject at
72
35
30
25
20
% scans
15
10
0
1 2 3 4 5 6 7 8 9 10 >10
Figure 4.3a Percent time different number of individuals were within 5m of subject at
35
30
25
20
% scans
15
10
0
1 2 3 4 5 6 7 8 9 10 >10
Figure 4.3b Percent time different number of individuals were within 5m of subject at
73
80
70
60
50
% nights
40
30
20
10
0
<50m (same side) <100m (same side) <100m (both sides)
Distance and riverbank
Harem Non-harem SU2 SU7 All Groups
Figure 4.4 Percent nights when other N. larvatus group/groups were close to SU1 at
Sukau (n=96)
40
35
30
25
% scans
20
15
10
0
0 1 2 3 4
Number of groups
Figure 4.5 Percent nights when 0, 1, 2, 3 and 4 groups were within 100m of SU1 at
Sukau (n=96)
74
100
10
% scans
0.1
0.01
Activities
Figure 4.6 Activity budgets of SU1 at Sukau (n=4966, weighted data)
Figure 4.7 An adult female grooming a juvenile-1
75
Figure 4.8 An adult female watching the observer
0.35
0.3
0.25
Infants/adult female
0.2
0.15
0.1
0.05
0
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
Figure 4.9 Number of Infant-1s per adult female observed each month at Sukau
76
60
50
40
% scans
30
20
10
0
AM AF SAF Juv2 Juv1 Inf2 Inf1
Age/sex classes
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)
77
Figure 4.12 A juvenile with an open-mouthed threat towards the observer
120
100
80
% scans
60
40
20
0
0 >0-1 >1-2 >2-3 >3-4 >4-5
Distance (metres)
Figure 4.13a Percent time nearest neighbour was at cumulative distance from subject at
Abai (n=1023, weighted data)
78
120
100
80
% scans
60
40
20
0
0 >0-1 >1-2 >2-3 >3-4 >4-5
Distance (metres)
Figure 4.13b Percent time nearest neighbour was at cumulative distance from subject at
120
100
80
% scans
60
40
20
0
1 2 3 4 5 6 7 8 9 10 >10
Figure 4.14a Percent time different number of individuals was within 2.5m of subject at
79
35
30
25
20
% scans
15
10
0
1 2 3 4 5 6 7 8 9 10 >10
Figure 4.14b Percent time different number of individuals was within 2.5m of subject at
70
60
50
40
% scans
30
20
10
0
1 2 3 4 5 6 7 8 9 10 >10
Figure 4.15a Percent time different number of individuals was within 5m of subject at
80
35
30
25
20
% scans
15
10
0
1 2 3 4 5 6 7 8 9 10 >10
Figure 4.15b Percent time different number of individuals was within 5m of subject at
16
14
12
10
% nights
0
<50m (same sides) <100m (same sides) <100m (both sides)
Distance and riverbank
Harem All-male
Figure 4.16 Percent of nights when another N. larvatus group was close to a harem at
Abai (n=205)
81
90
80
70
60
50
% scans
40
30
20
10
0
0 1 2
Number of groups
Figure 4.17 Percent of nights when 0, 1, and 2 groups were within 100m of a harem at
Abai (n=205)
100
10
% scans
0.1
0.01
Activities
Figure 4.18 Activity budgets of harem groups at Abai (n=1023, weighted data)
82
0.7
0.6
0.5
Infants/adult female
0.4
0.3
0.2
0.1
0
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
Figure 4.19. Number of infant-1s per adult female observed each month at Abai
83
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 &
84
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
85
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
86
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.
87
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.
88
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
89
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;
90
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).
91
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
92
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.
93
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
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)
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
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)
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 % Neutral
Tannin Detergent
(mg/g) 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
96
Table 5.6 Chemical composition of plant parts not observed eaten by N. larvatus
Species Part Saponin % Protein Condensed % Neutral
Tannin Detergent
(mg/g) 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
97
Table 5.7 Comparative proportions of plant parts in some colobines’ diets (expressed as
percentages)
Species ML ML YL FL FR FR+ SD Source
+YL SD
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.
98
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%)
Figure 5.1 Percentage of different items in harem groups' diet at Sukau (n=594,
unweighted data)
Young leaves (59.7%)

Ripe fruits (1.4%)
Unripe fruits (37.5%)
Unknown items (1.4%)
Figure 5.2 Percentage of different items in non-harem groups' diet at Sukau (n=72,
unweighted data)
99
100
90
80
70
% feeding time
60
50
40
30
20
10
0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
1991
Young leaves Fruits Flowers Seeds
Figure 5.3 Monthly variation in plant parts eaten by N. larvatus groups at Sukau
(n=540, unweighted data)
120
100
80
% feeding time
60
40
20
0
1991
% in diet % in forest
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
35
30
25
% feeding time
20
15
10
0
1991
forest (n=500, phenology data), at Sukau
30
25
20
% feeding time
15
10
0
1991
forest (n=500, phenology data), at Sukau
101
120
100
80
% feeding time
60
40
20
0
600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800
Time of day (in hours)
Leaves Flowers Fruits Seeds
Figure 5.5 Diurnal variation in plant parts eaten by SU1 at Sukau (n=489, unweighted
data)
102
Adult males (n=35) Adult females (n=290)
Young leaves (72.5%) Mature leaves (0.3%)

Young leaves (88.6%) Flowers (5.7%) Unknown items (7%) Seeds (2.8%)
Flowers (0.3%) Flower buds (8.7%)
Unripe fruits (2.9%) Unknown items (2.9%)
Ripe fruits (6.6%) Unripe fruits (1.7%)
Juvenile-2s (n=63) Juvenile-1s (n=121)
Young leaves (74.6%) Unknown items (11.1%) Young leaves (66.7%) Unknown items (8.3%)
Seeds (1.6%) Flowers (4.8%) Seeds (2.5%) Flowers (10%)
Unripe fruits (6.3%) Ripe fruits (1.6%) 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%)
Figure 5.6 Percentage of different items in harem groups' diet by age/sex class at Sukau
103
120
100
80
% time feeding
60
40
20
0
1991
Adult males Adult females Juvenile-2s Juvenile-1s Infant-2s
Figure 5.7 Monthly variation in time spent feeding by different age/sex class of SU1 at
80
70
60
% time feeding
50
40
30
20
10
0
600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800
Time of day
Adult males Adult females Juvenile-2s Juvenile-1s Infant-2s
Figure 5.8 Diurnal variation in time spent feeding by different age/sex class of SU1 at
104
Young leaves (49.7%) Unknown items (2.6%) Seeds (11.6%) Flowers (15.5%) Unripe fruits (20.6%)
Figure 5.9 Percentage of different items in harem groups' diet at Abai (n=155,
unweighted data)
Young leaves (72.7%) Unripe fruits (27.3%)
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
Figure 5.12 An adult male drinking water from the Kinabatangan River
106
120
100
80
% time feeding
60
40
20
0
Mar Apr May Jun Aug Sep Oct Nov
1991
Young leaves Fruits Flowers Seeds
Figure 5.13 Monthly variation in plant parts eaten by N. larvatus groups at Abai (n=155,
unweighted data).
120
100
80
% feeding time
60
40
20
0
1991
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
80
70
60
% feeding time
50
40
30
20
10
0
1991
forest (n=300, phenology data), at Abai
120
100
80
% feeding time
60
40
20
0
1991
forest (n=300, phenology data), at Abai
108
Adult males (n=10) Adult females (n=82)
Young leaves (30%) Seeds (10%) Young leaves (51.2%) Flowers (14.6%)
Unripe fruits (15.9%) Seeds (17.1%)
Flowers (30%) Unripe fruits (30%) Unknown items (1.2%)
Juvenile-2s (n=14) Juvenile-1s (n=42)
Young leaves (45.2%) Flowers (11.9%)

Young leaves (71.4%) Flowers (14.3%)
Unripe fruits (31%) Seeds (7.1%)
Unripe fruits (7.1%) Unknown items (7.1%) Unknown items (4.8%)
Figure 5.15 Percentage of different items in harem groups' diet by age/sex class at Abai
109
80
70
60
% time feeding
50
40
30
20
10
0
1991
Adult males Adult females Older juveniles
Young juveniles Older infants
Figure 5.16 Monthly variation in time spent feeding by different age/sex class of harem
groups at Abai (n=155, weighted data)
100
90
80
70
60
CT+NDF
50
40
30
20
10
0
0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5
Protein
Eaten Not eaten
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
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.

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.
111
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
112
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.
113
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.
114
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
115
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).
116
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.
117
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
118
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.
119
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)
120
300
250
200
No. of quadrats
150
100
50
0
1991
Figure 6.2 Cumulative number of 1ha quadrats entered by SU1 at Sukau (n=93)
14
12
10
8
% days
0
100
200
300
400
500
600
700
800
900
1000
1100
1200
1300
1400
1500
1600
1700
1800
Day range length (m)
Figure 6.3 Frequency distribution of day range lengths of SU1 at Sukau (n=53)
121
1400
1200
1000
Day range length (m)
800
600
400
200
0
Feb Mar Apr May Jun Jul Aug Sep Oct Nov
1991
Figure 6.4 Mean monthly day range lengths of SU1 at Sukau (n=53)
14
12
10
8
% days
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
No. of quadrats
Figure 6.5 Frequency distribution of 1ha quadrats entered by SU1 each day (n=53)
122
16
14
12
Mean no. of quadrats
10
0
Feb Mar Apr May Jun Jul Aug Sep Oct Nov
1991
Figure 6.6 Mean monthly number of 1ha quadrats entered by SU1 at Sukau (n=53)
50
45
40
35
No. of quadrats
30
25
20
15
10
0
1991
Figure 6.7 Monthly total number of 1ha quadrats entered by SU1 at Sukau (n=93)
123
Figure 6.8 Differential quadrat use by SU1 at Sukau from Jan. – Dec. 1991 (n=4966,
weighted data)
124
18
16
14
12
10
% time
0
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
Height (m)
Feed Travel Rest
Figure 6.9 Height of SU1 at Sukau when engaged in major activities
16
14
12
Mean height (m)
10
0
10:00
11:00
12:00
13:00
14:00
15:00
16:00
17:00
18:00
5:00
6:00
7:00
8:00
9:00
Time of day (hours)
Figure 6.10 Mean height of SU1 at different time of day at Sukau (n=4966, weighted
data)
125
Mangrove forest
Location of N.
larvatus groups
Freshwater swamps and riverine forest
Lowland dipterocarp forest and

dry land below 70m elevation
Figure 6.11 Use of riverside habitat by N. larvatus groups at Abai (Feb. 1990 – Dec.
1991)
126
18
16
14
12
10
% time
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
Height (m)
Feed Travel Rest
Figure 6.12 Height of N. larvatus groups at Abai when engaged in major activities
127
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:
128
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.
129
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.
130
LITERATURE CITED
Alexander, R.D. 1974. The evolution of social behaviour. Ann. Rev. Ecol. Syst. 5: 325-83.
Altmann, J. 1974. Observational study of behaviour: sampling methods. Behaviour 49: 227-
267.
Altmann, S.A. and J. Altmann. 1970. Baboon Ecology. Chicago: Chicago University Press.
Anderson, C.M. 1981. Intertroop relations of chacma baboons (Papio ursinus). Int. J.
Primatol. 2: 285-310.
Anon. 1981. Gross and net primary production and growth parameters. In Tropical Forests
Ecosystem, 233-248. Paris: UNESCO.
Baranga, D. 1983. Changes in chemical composition of food parts in the diet of colobus
monkeys. Ecology 64: 668-673.
Bauchop, T. 1971. Stomach microbiology of primates. Ann. Rev. Microbiol. 25: 429-436.
Bauchop, T. 1978. Digestion of leaves in vertebrate arboreal folivores. In The Ecology of
Arboreal Folivores, ed. G.G. Montgomery, 193-204. Washington: Smithsonian
Institution Press.
Bauchop, T. and R.W. Martucci. 1968. Ruminant-like digestion of the langur monkey.
Science, New York 161: 698-700.
Bennett, E.L. 1983. The banded langur: ecology of a colobine in West Malaysian rainforest.
Unpublished doctoral dissertation, University of Cambridge.
________. 1986a. Proboscis Monkeys in Sarawak: their Ecology, Status, Conservation and
Management. WWF Malaysia, Kuala Lumpur, and New York Zoological Society,
New York.
________. 1986b. Environmental correlates of ranging behaviour in the banded langur,
Presbytis melalophos. Folia Primatol. 47: 26-38.
________. 1987. Big noses of Borneo. Animal Kingdom March/April: 9-15.
________. 1988a. Cyrano of the Swamps. BBC Wildlife 6(2): 71-75
________. 1988b. Proboscis monkeys and their swamp forests in Sarawak. Oryx 22(2): 69-
74.
________. 1991. Diurnal Primates. In The State of Nature Conservation in Malaysia, ed. R.
Kiew, 150-172. Kuala Lumpur: United Selangor Press Sdn. Bhd.
________. (in press). Proboscis monkey, Nasalis larvatus. Illustrated Monographs of Living
Primates. The institute, Wezep, the Netherlands.
Bennett, E.L. and J.O. Caldecott. 1988. Rain forest primates of Peninsular Malaysia. In
Ecosystems of the World, Volume 14A: Tropical Forests, eds. H. Leith and M.J.A.
Werger. Holland: Elsevier.
Bennett, E.L. and F. Gombek. 1993. Proboscis Monkeys of Borneo. Kota Kinabalu: Borneo
Natural History and Publications, and KOKTAS.
Bennett, E.L. and A.C. Sebastian. 1988. Social organization and ecology of proboscis
monkeys (Nasalis larvatus) in mixed coastal forest in Sarawak. Int. J. Primatol. 9:33-
255.
Bennett, E.L., G.W.H. Davison and M. Kavanagh. 1983. Social changes in a family of
siamang (Hylobates syndactylus). Malay Nat. J. 36: 187-196.
Berman, C.M. 1982. The ontogeny of social relationships with group companions among
free-ranging infant rhesus monkeys, 1: Social networks and differentiation. Anim.
Behav. 30: 149-62.
Bernstein, I.S. 1968. The lutong of Kuala Selangor. Behaviour 32: 1-16.
131
Bertram, B.C.R. 1978. Living in groups: predators and prey. In Behavioural Ecology, eds.
J.R. Krebs and N.B. Davies, 64-96. London: Blackwell Press.
________. 1980. Vigilance and group size in ostritches. Anim. Behav. 28: 278-286.
Bismark, M. 1980. Behaviour and Population Density of Proboscis Monkey (Nasalis
larvatus) at Tanjung Puting Game Reserve, Central Kalimantan. Report No. 357,
Lembaga Penilitan Hutan, Bogor.
________. 1981. Preliminary survey of the proboscis monkey at Tanjung Puting Reserve,
Kalimantan. Tigerpaper 8: 26.
Boelkins, R.C. and A.P. Wilson. 1972. Intergroup social dynamics of the Cayo Santiago
rhesus (Macaca mulatta) with special reference to changes in group membership by
males. Primates 13: 125-40.
Boggess, J.E. 1979. Troop male membership changes and infant-killing in langurs (Presbytis
entellus). Folia Primatol. 32: 65-107.
Boonratana, R. 1993a. Die Pinocchios des Regenwalds. GEO 3: 132-142.
________. 1993b. El pinocho de la selva. GEO 81: 40-50.
Boonratana, R. and D.S. Sharma (in press). Conservation of proboscis monkeys in the Lower
Kinabatangan, Sabah. In Proceedings of the XIVth Congress of International
Primatological Society held at Strasbourg, France, August 16-21, 1992.
Breuggeman, J.A. 1973. Parental care in a group of free-ranging rhesus monkeys (Macaca
mulatta). Folia Primatol. 20: 178-210.
Brockelman, W.Y. and R. Ali. 1987. Methods of surveying and sampling forest primate
populations. In Primate Conservation in the Tropical Rain Forest, eds. C.W. Marsh
and R.A. Mittermeier, 23-62. New York: Alan R. Liss, Inc.
Brown, J.L. and G.H. Orians. 1970. Spacing patterns in mobile animals. Am. Rev. Ecol. Syst.
1: 239-262.
Brown, J.L. 1964. The evolutionary diversity in avian territorial systems. Wilson Bull. 76:
160-169.
Burnham, K.P., D.R. Anderson and J.L. Laake. 1980. Estimation of density from line transect
sampling of biological populations. Wildlife Monographs 72: 1-202.
Burns, R.E. 1971. Method of estimation of tannin in grain Sorghum. Agronomy Journal 63:
511-512.
Busse, C. 1977. Chimpanzee predation as a possible factor in the evolution of red colobus
monkey social organisation. Evolution. 31: 907-911.
Butynski, T.M. 1982. Harem male replacement and infanticide in the blue monkey
(Cercopithecus mitis stuhlamanni) in the Kibale Forest, Uganda. Amer. J. Primat. 3:1-
22.
Caraco, T. 1979a. Time budgeting and group size: a theory. Ecology 60: 611-617.
________. 1979b. Time budgeting and group size: a test of theory. Ecology 60: 618-627.
Caldecott, J.O. 1980. Habitat quality and populations of two sympatric gibbons (Hylobatidae)
on a mountain in Malaya. Folia Primatol. 33: 291-309.
Caldecott, J.O. 1986. An Ecological and Behavioural Study of the Pig-tailed Macaque.
Contributions to Primatology, Volume 21. Basel: Karger.
Calvert, W.H., L.E. Hedrick and L.P. Brower. 1979. Mortality of the monarch butterfly,
Danaus plexxipus: avian predation of five over-wintering sites in Mexico. Science
182: 1272-1275.
Carpenter, C.R. 1942. Sexual behavior of free-ranging rhesus monkeys, M. mulatta. J. Comp.
Psychol. 33: 113-162.
Cheney, D.L. 1978. Interactions of immature male and female baboons with adult females.
Anim. Behav. 26: 389-408.
132
________. 1987. Interactions and relationships between groups. In Primate Societies, ed.
B.B. Smuts, D.L.Cheney, R.M. Seyfarth, R.W. Wrangham and T.T. Struhsaker, 267-
281. Chicago: University of Chicago Press.
Cheney, D.L. and R.M. Seyfarth. 1983. Non-random dispersal in free-ranging vervet
monkeys: Social and genetic consequences. Am. Nat. 122: 392-412.
Chivers, D.J. 1969. On the daily behaviour and spacing of howling monkey groups. Folia
Primatol. 10: 48-102.
________. 1974. The siamang in Malaya Basel: Karger.
________. 1975. The behaviour of siamang in the Krau Game Reserve. Malay. Nat. J. 29: 7-
22.
________. ed. 1980. Malayan Forest Primates. New York: Plenum Press.
Chivers, D.J. and C.M. Hladik. 1980. Morphology of the gastrointestinal tract in primates:
comparisons with other mammals in relation to diet. J. Morphol. 166: 337-386.
Chivers, D.J. and J.J. Raemaekers. 1980. Long-term changes in behaviour. In Malayan Forest
Primates, ed. D.J. Chivers, 209-260. New York: Plenum Press.
Choo, G.M., P.G. Waterman, D.D. McKey, and J.S. Gartlan. 1981. A simple enzyme assay
for dry matter digestibility and its value in studying food selection by generalist
herbivores. Oecologia 49: 170-178.
Church, D.C. and W.G. Pond. 1988. Basic Animal Nutrition and Feeding. 3rd ed. New York:
John Wiley and sons.
Clutton-Brock, T.H. 1972. Feeding and ranging behaviour of the red colobus monkey.
________. 1974. Primate ecology and social organisation. Nature, Lond. 250: 539-542.
________. 1975. Ranging behaviour of red colobus (Colobus badius tephrosceles) in the
Gombe National Park. Anim. Behav. 23: 706-722.
________. ed. 1977a. Primate Ecology: Studies of Feeding and Ranging Behaviour in
Lemurs, Monkey, and Apes. London: Academic Press.
________. 1977b. Some aspects of intraspecific variation in feeding and ranging behaviour in
primates. In Primate Ecology: Studies of Feeding and Ranging Behaviour in Lemurs,
Monkey, and Apes, ed. T.H. Clutton-Brock, 539-556. London: Academic Press.
________. 1988. Female transfer and inbreeding avoidance in social mammals. Nature 337:
70-72.
________. 1989. Mammalian mating systems. Proc. Roy. Soc. Lond. B. 236: 339-372.
Clutton-Brock, T.H. and P.H. Harvey. 1977a. Primate ecology and social organisation. J.
Zool. Lond. 183: 1-39.
________. 1977b. Species differences in feeding and ranging behaviour in primates. In
Primate Ecology, ed. T.H. Clutton-Brock, 557-584. London: Academic Press.
________. 1978. Mammals, resources, and reproductive strategies. Nature 273: 191-195.
Coelho, A.M., S.A. Turner and C.A. Bramblett. 1983. Allogrooming and social status: an
assessment of the contributions of female behaviour to the social organisation of
Hamadryas baboons. Primates 24: 184-197.
Cords, M. 1987. Forest guenons and patas monkeys: male-male competition in one-male
groups. In Primate Societies, eds. B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W.
Wrangham and T.T. Struhsaker, 98-111. Chicago: University of Chicago Press.
Crockett, C.M. 1984. Emigration by female red howler monkeys and the case for female
competition. In Female Primates: Studies by Female Primatologists, ed. M.F. Small.
New York: Alan R. Liss.
Crockett, C.M. and J.F. Eisenberg. 1987. Howlers: Variations in group size and demography.
In Primate Societies, eds. B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham
and T.T. Struhsaker, 54-68. Chicago: University of Chicago Press.
133
Crook, J.H. 1970a. Social organization and environment: Aspects of contemporary social
ethology. Anim. Behav. 18: 197-209.
Crook, J.H. 1972. Sexual selection, dimorphism, and social organization in the primates. In
Sexual Selection and the Descent of Man, ed. B.G. Campbell. Chicago: Aldine.
Crook, J. and F.P.G. Aldrich-Blake, 1968. Ecological and behavioural contrasts between
sympatric ground-dwelling primates in Ethiopia. Folia Primatol. 8: 192-227.
Crook, J.H. and J.S. Gartlan. 1966. Evolution of primate societies. Nature 210: 1200-1203.
Culvenor, C.C.J. and J.S. Fitzgerald. 1963. A field methods for alkaloids screening of plants.
J. Pharm. Sci. 52: 303-304.
Curtin, R.A. 1975. The socioecology of the common langur, Presbytis entellus, in the Nepal
Himalaya. Unpublished doctoral dissertation, University of California.
Curtin, S.H. 1976. Niche separation in sympatric Malaysian colobines (Presbytis obscura and
Presbytis melalophos). Ybk. Phys. Anth. 20: 421-439.
Dalby, A. 1978. Temperature-induced of tannins. Analytical Biochemistry 85: 325-327.
Davidge, C. 1978. Ecology of baboons (Papio ursinus) at Cape Point. Zool. Africana 13:
329-350.
Davies, A.G. 1984. An ecological study of the red leaf monkey (Presbytis rubicunda) in the
dipterocarp forest of northern Borneo. Unpublished doctoral dissertation, University
of Cambridge.
________. 1987. Adult male replacement and group formation in Presbytis rubicunda. Folia
Primatol. 49: 111- 114.
Davies, G. and J. Payne. 1982. A faunal survey of Sabah. IUCN/WWF Project No. 1692.
Kuala Lumpur: World Wildlife Fund - Malaysia.
Davies, A.G., J.O. Caldecott and D.J. Chivers. 1983. Natural foods as a guide to the nutrition
of Old World Primates. In Standards in Laboratory Animal Management, ed. J.
Remfry, 225-244. Potters Bar: U.F.A.W.
Davies, A.G., E.L. Bennett and P.G. Waterman. 1988. Food selection by two South-east
Asian colobine monkeys (Presbytis rubicunda and Presbytis melalophos) in relation
to plant chemistry. Biol. J. of the Linn. Soc. 34: 33-56.
Davies, N.B. and A.I. Houston. 1984. Territory economics. In Behavioural Ecology: An
Evolutionary Approach, eds. J.R. Krebs and N.B. Davies. Sunerland, Mass.: Sinauer
Association.
Davis, D.D. 1962. Mammals of the lowland rain-forest of North Borneo. Bulletin of the
National Museum of Singapore 31: 1-129.
Dawson, G.A. 1979. The use of time and space by the Panamanian tamarin, Saguinus
oedipus. Folia Primatol. 31: 253-284.
Deag, J.M. 1977. The status of the Barbary macaque Macaca sylvanus in captivity and
factors influencing its distribution in the wild. In Primate Conservation, eds. HSH
Rainier III and G.H. Bourne, 267-297. New York: Academic Press.
Dierenfeld, E.S., F.W. Koontz and R.S. Goldstein. 1992. Feed intake, digestion and passage
of the proboscis monkey (Nasalis larvatus) in captivity. Primates 33(3): 399-405.
Dittus, W.P.J. 1979. The evolution of behaviours regulating density and age-sex distribution
in the toque monkey. Behaviour 63: 281-322.
Dolhinow, P. and G. Murphy. 1982. Langur monkey (Presbytis entellus) development: the
first three months of life. Folia Primatol. 39: 305-331.
Dunbar, R.I.M. 1980. Demographic and life history variables of a population of gelada
baboons. Behav. Ecol. Sociobiol. 49: 485-506.
________. 1988. Primate Social Systems. London: Croom Helm.
Dunbar, R.I.M. and E.P. Dunbar. 1974. Ecology and population dynamics of Colobus
guereza in Ethiopia. Folia Primatol. 21: 188-208.
134
Dunbar, R.I.M. and E.P. Dunbar. 1975. Social dynamics of gelada baboons. Contrib.
Primatol. 6.
Eisenberg, J.F., N.A. Muckenhirn and R. Rudran. 1972. The relation between ecology and
social structure in primates. Science 176: 863-74.
Elliot, D.G. 1912. A Review of the Primates. Volume III. Anthropoidea: Miopithecus to Pan.
New York: American Musuem of Natural History.
Eudey, A.A. 1987. Action Plan for Asian Primate Conservation 1987-91. IUCN/UNDP.
Fagen, R. 1981. Animal Play Behavior. Oxford: Oxford University Press.
Fairbanks, L.A. and M.T. McGuire. 1984. Determinants of fecundity and reproductive
success in captive vervet monkeys. Am. J. Primatol. 7: 27-38.
Forbes, H.O. 1897. A Handbook to the Primates. Volume II. London: Edward Lloyd.
Fossey, D. 1974. Observations on the home range of one group of mountain gorillas (Gorilla
gorilla beringei). Anim. Behav. 22: 568-581.
Fossey, D. and A.H. Harcourt. 1977. Feeding ecology of free-ranging mountain gorilla
(Gorilla gorilla beringei). In Primate Ecology, ed. T.H. Clutton-Brock, 415-447.
London: Academic Press.
Foster, W.A. and J.E. Treherne. 1981. Evidence for the dilution effect in the selfish herd from
fish predation on marine insect. Nature. 295: 466-467.
Freeland, W.J. 1976. Pathogens and the evolution of primate sociality. Biotropica 8: 12-24.
________. 1979. Mangabey (Cercocebus albigena). Social organisation and population
density in relation to food use and availability. Folia Primatol. 32: 108-124.
Freeland, W.H. and D.H. Janzen. 1974. Strategies in herbivory by mammals: the role of plant
secondary compounds. Am. Nat. 108: 269-289.
Freeland, W.J., P.H. Calcott and L. Anderson. 1985. Tannins and saponins: interaction in
herbivore diets. Biochemical Systematics and Ecology 13: 189-193.
Froehlich, J.W. and R.W. Thorington. 1982. The genetic structure and socioecology of
howler monkeys (Alouatta paliatta) on Barro Colorad Island. In The Ecology of
Tropical Forests, eds. A.S. Rand and D.M. Windsor, 291-305. Washington D.C.:
Smithsonian Institution Press.
Gartlan, J.S. and C.K. Brain. 1968. Ecology and social variability in Cercopithecus aethiops
and C. mitis. In Primates: Studies in Adaptation and Variability, ed. P. Jay, 253-292.
New York: Holt, Rhinehart and Winston.
Gartlan, J.S., D.B. McKey, P.G. Waterman, C.N. Mbi and T.T. Struhsaker. 1980. A
comparative study of the phytochemistry of two African rain forests. Biochemical
Systematics and Ecology 8: 401-422.
Gautier-Hion, A., J.P. Gautier and R. Quris. 1981. Forest structure and fruit availability as
complementary factors influencing habitat use in a troop of monkeys (Cercopithecus
cepio). Terre et Vie 25: 427-490.
Gittins, S.P. 1979. The behaviour and ecology of the agile gibbon, Hylobates agilis.
________. 1983. Use of forest canopy by the agile gibbon. Folia Primatol. 40: 134-144.
Glander, K.E. 1984. Group composition in mantled howling monkeys. Am. J. Phys.
Anthropol. 63: 163. Goodall, J. 1986. The Chimpanzees of Gombe: Patterns of
Behaviour. Cambridge: Harvard University Press.
Gray, J.P. 1985. Primate sociobiology. New Haven: HRAF Press.
Greenwood, P.J. 1980. Mating systems, philopatry and dispersal in birds and mammals.
Anim. Behav. 28: 1140-1162.
Gurmaya, I. 1986. Ecology and behavior of Presbytis thomasi in Northern Sumatra. Primates
27: 151-172.
135
Hall, K.R.L. 1960. Social vigilance behaviour of the Chacma baboon, Papio ursinus.
Behaviour 16: 261-294.
________. 1963. Variations in the ecology of the chacma baboon, Papio ursinus. Symp. Zool.
Soc. Lond. 10: 1-28.
________. 1965. Behaviour and ecology of wild patas monkey Erythrocebus patas in
Uganda. J. Zool. Lond 148: 15-87.
Hamilton, W.D. 1971. Geometry for the selfish herd. J. Theor. Biol. 31: 295-311.
Harcourt, A.H. 1978. Strategies of emigration and transfer by primates, with particular
reference to gorillas. Z. Tierpsychol. 48: 401-420.
________. 1979. Social relationships among female mountain gorillas. Anim. Behav. 27: 251-
264.
Harcourt, A.H., K.S. Stewart and D. Fossey. 1976. Male emigration and female transfer in
wild mountain gorilla. Nature. 263: 226-227.
Harley, D. 1985. Birth spacing in langur monkeys (Presbytis entellus). Int. J. Primatol. 6:
227-242.
Harrison, M.J.S. 1983. Patterns of range use by the green monkey, Cercopithecus sabaeus, at
Mt. Assirik, Senegal. Folia Primatol. 41: 157-179.
Henzi, S.P. and J.W. Lucas. 1980. Observations on the intertroop movement of adult vervet
monkeys (Cercopithecus aethiops). Folia Primatol. 33: 220-35.
Hinde, R.A. 1974. Mother/infant relations in rhesus monkeys. In Ethology and Psychiatry,
ed. N.F. White. Toronto: University of Toronto Press.
Hiraiwa, M. 1981. Maternal and allopaternal care in a troop of free-ranging Japanese
monkeys. Primates 22: 309-329.
Hladik, A and C.M. Hladik. 1969. Rapports trophiques entre vegetation et primates dans la
foret de Barro Colorado (Panama). Terre et Vie 23: 25-117.
Hladik, C.M. 1977a. A comparative study of the feeding strategies of two sympatric species
of leaf monkeys: Presbytis senex and Presbytis entellus. In Primate Ecology, ed. T.H.
Clutton-Brock, 323-353. London: Academic Press.
________. 1977b. Chimpanzees of Gabon and chimpanzees of Gombe: Some comparative
data on diet. In Primate Ecology, ed. T.H. Clutton-Brock, 481-501. New York:
Academic Press.
Hladik, C.M. and A. Hladik. 1972. Disponibilites alimentaires et domaines vitaux des
primates a Ceylan. Terre et Vie 26: 149-215.
Homewood, K.M. 1976. Ecology and behaviour of the Tana mangabey (Cercocebus galeritus
galeritus). Unpublished doctoral dissertation, University of London.
________. 1978. Feeding strategy of the Tana mangabey (Cercocebus galeritus galeritus)
(Mammalia: Primates). J. Zool. Lond. 186: 375-391.
Horrocks, J. 1986. Life-history characteristics of a wild population of vervets (Cercopithecus
aethiops sabaeus) in Barbados, West Indies. Int. J. Primatol. 7: 31-47.
Hrdy, S.B. 1976. The care and exploitation of nonhuman primate infants by conspecifics
other than the mother. Advances in the Study of Behaviour 6: 101-158.
________. 1977. The Langurs of Abu. Cambridge: Harvard University Press.
Huxley, J.S. 1934. A natural experiment on the territorial instinct. British Birds 27: 270-277.
Isbell, L.A. 1983. Daily ranging behavior of red colobus (Colobus badius tephrosceles) in
Kibale Forest, Uganda. Folia Primatol. 41: 34-48.
Iwamoto, T. 1979. Feeding Ecology. In Ecological and Sociological Studies of Gelada
Baboons, ed. M. Kawai, 280-330. Basel: Karger.
Iwamoto, T. and R. Dunbar. 1983. Thermoregulation, habitat quality and the behavioural
ecology of gelada baboons. J. Anim. Ecol. 52: 357-366.
136
IUCN, 1990. 1990 IUCN Red List of Threatened Animals. Gland, Switzerland and
Cambridge, U.K.: IUCN.
Janis, C. 1976. The evolutionary strategy of the Equidae and the origins of rumen and caecal
digestion. Biotropica 6: 69-103.
Janzen, D.H. 1975. Ecology of Plants in the Tropics. London: Edward Arnold.
Jeffrey, S.M. 1979. The proboscis monkey: some preliminary observations. Tigerpaper 6: 5-
6.
________. 1982. Threats to the proboscis monkey. Oryx 16: 337-339.
Jolly, A. 1972. The Evolution of Primate Behaviour. New York: Macmillan.
Kaufmann, J.H. 1983. On the definitions and functions of dominance and territoriality. Biol.
Rev. 58: 1-20.
Kavanagh, M. 1977. Some inter-population variation in the behavioural ecology of
Cercopithecus aethiops tantalus. Unpublished doctoral dissertation, University of
Sussex.
________. 1978. The diet and feeding behaviour of Cercopithecus aethiops tantalus. Folia
Primatol. 30: 30-63.
________. 1980. Invasion of the forest by an African savannah monkey: behavioural
adaptations. Behaviour 73: 238-260.
________. 1981. Variable territoriality among tantalus monkeys in Cameroon. Folia
Primatol. 36: 76-98.
________. 1983. A Complete Guide to Monkeys, Apes and Other Primates. London: Jonathan
Cape.
Kawabe, M. and Mano, T. 1972. Ecology and behaviour of the wild proboscis monkey,
Nasalis larvatus (Wurmb), in Sabah, Malaysia. Primates 13: 213-228.
Kern, J.A. 1964. Observations on the habits of the proboscis monkey, Nasalis larvatus
(Wurmb), made in the Brunei Bay area, Borneo. Zoologica (New York) 49: 183-192.
Khoo, K.K. 1981. Sabah: History and Society. Kuala Lumpur: Malaysian Historical Society.
Kinzey, W.G. 1977. Diet and feeding behaviour of Callicebus torquatus. In Primate Ecology,
ed. T.H. Clutton-Brock, 127-151. London: Academic Press.
Kleiber, N. 1961. The Fire of Life. New York: John Wiley and sons.
Klein, L.L. and D.J. Klein, 1975. Social and ecological contrasts between four taxa of
neotropical primates (Ateles bezelbuth, Alouatta seniculus, Saimiri sciureus, Cebus
apella). Proc. IX. Int. Congr. Anthrop. Ethnol. Sci. Mouton and Co., Chicago.
________. 1977. Feeding behaviour of the Columbian spider monkey. In Primate Ecology,
ed. T.H. Clutton-Brock, 153-181. New York: Academic Press.
Krebs, J.R. and B.L. Partridge. 1973. The significance of head-tilting in the great blue heron.
Nature, Lond. 242: 534.
Krebs, J.R. and N.B. Davies. 1993. An Introduction to Behavioural Ecology. Oxford:
Blackwell Scientific Publications.
Kuhn, H.J. 1964. Zur Kenntnis von Bau und Funktion des Magens der Schlankaffen
(Colobine). Folia Primatol. 2: 193-211.
Kumar, R. and S. Vaithayathan. 1990. Occurence, nutritional significance and effect on
animal productivity of tannins in tree leaves. Animal Feed Science and Technology
30: 21-38.
Kummer, H. 1968. Social Organisation of Hamadryas Baboons. Chicago: University of
Chicago Press.
Lancaster, J.B. 1972. Play-mothering: The relations between juvenile females and young
infants among free-ranging vervets. In Primate Socialization, ed. F.E. Poirier. New
York: Random House.
137
Lebreton, P. 1982. Tannins and alkaloids: two altenative phytochemical tactics for deterring
herbivores. Terre et Vie 36: 539-572.
Loh, S.N. 1991. Analisis kimia tumbuhan yang dikaitkan dengan pemilihan makanan monyet
Belanda (Nasalis larvatus) di kawasan Sukau, Sabah. Ijazah sarjanamuda sains,
Universiti Kebangsaan Malaysia.
Macdonald, D.W. 1982. Notes on the size and composition of groups of proboscis monkey,
Nasalis larvatus. Folia Primatol. 37: 95-98.
MacKinnon, J.R. and K.S. MacKinnon. 1980. Niche differentiation in a primate community.
In Malayan Forest Primates, ed. D.J. Chivers, 167-190. New York: Plenum Press.
McKenna, J.J. 1978. Biosocial functions of grooming behavior among the common Indian
langur monkey (Presbytis entellus). Am. J. Phys. Anthrop. 48: 503-510.
McKenna, J.J. 1981. Primate infant caregiving behaviour: origins, consequences and
variability with emphasis on the common Indian langur monkey. In Parental Care in
Mammals, eds. D.J. Gubernick and P.H. Klopfer, 389-416. New York: Plenum Press.
McKey, D. and P.G. Waterman. 1982. Ranging behaviour of a group of black colobus
(Colobus satanas) in the Douala-Edea Reserve, Cameroon. Folia Primatol. 39: 264-
304.
McKey, D.B., J.S. Gartlan, P.G. Waterman and G.M. Choo. 1981. Food selection by black
colobus monkeys (Colobus satanas) in relation to plant chemistry. Biol. J. Linn. Soc.
16: 115-146.
Makwana, S.C. 1978. Field ecology and behaviour of the rhesus macaque (Macaca mulatta).
Primates 19: 483-492.
Marler, P. 1972. Vocalisations of East African monkeys. II. Black and white colobus.
Marsh, C.W. 1979a. Female transference and mate choice among Tana River red colobus.
Nature, Lond. 281: 568-569.
________. 1979b. Comparative aspects of social organisation in the Tana River red colobus,
Colobus badius rufomitratus. Z. Tierpsychol. 51: 337-362.
________. 1981a. Ranging behaviour and its relation to diet selection in Tana River red
colobus (Colobus badius rufomitratus). J. Zool. Lond. 195: 473-492.
________. 1981b. Time budgets of the Tana River red colobus. Folia Primatol. 35: 30-50.
Maynard, A.B. and J.K. Loosli. 1969. Animal Nutrition. New York: McGraw-Hill.
Mehlman, P.T. 1989. Comparative density, demography, and ranging behavior of Barbary
macaques (Macaca sylvanus) in marginal and prime conifer habitats. Int. J. Primatol.
10(4): 269-292.
Menard, N., D. Vallet and A. Gautier-Hion. 1985. Demographic et reproduction de Macaca
sylvanus dans differents habitats en Algerie. Folia Primatol. 44: 65-81.
Milton, K. 1979. Factors influencing leaf choice by howler monkeys: a test of some
hypotheses of food selection by generalist herbivores. Am. Nat. 114: 362-378.
________. 1980. The Foraging Strategy of Howler Monkeys. New York: Columbia
University Press.
________. 1981. Food choice and digestive strategies of two sympatric primate species. Am.
Nat. 117: 496-505.
________. 1984. Habitat, diet, and activity patterns of free-ranging woolly spider monkeys
(Brachyteles arachnoides E. Geoffrey, 1806). Int. J. Primatol. 5: 491-514.
Milton, K. and M.L. May. 1976. Body weight, diet and home range area in primates. Nature,
Lond. 259: 459-462.
Mitani, J.C. and P.S. Rodman. 1979. Territoriality: The relation of ranging patterns and home
range size to defendability, with an analysis of territoriality among primate species.
Behav. Ecol. Sociobiol. 5: 241-251.
138
Mitchell, A.H. 1993. Ecology of Hose’s langur (Presbytis hosei) in logged dipterocarp forest
in northeast Borneo. Unpublished doctoral dissertation, Yale University.
Moir, R.J. 1968. Ruminant digestion and evolution. In Handbook of Physiology, Section 6-V,
ed. C.F. Code, 2673-2694. Washington D.C.: American Physiological Society.
Moore, J. 1984. Female transfer in primates. Int. J. Primatol. 5: 537-589.
Moore, J. and R. Ali. 1984. Are inbreeding and dispersal related? Anim. Behav. 32:n 94-112.
Napier, J.R. and P.H. Napier. 1967. A Handbook of Living Primates. London: Academic
Press.
________. 1985. The Natural History of the Primates. Cambridge: British Museum (Natural
History).
Napier, P.H. 1985. Catalogue of Primates in the British Museum (Natural History) and
Elsewhere in the British Isles. Part III. Family Cercopithecidae, Subfamily Colobinae.
London: British Museum (Natural History).
Neville, M.K. 1968. Ecology and activity of Himalayan foothill rhesus monkeys (Macaca
mulatta). Ecology 49: 110-123.
________. 1972. The population sructure of red howler monkeys in Trinidad and Venzuela.
Folia Primatol. 17: 56-86.
Neville, M.K., K.E. Glander, F. Braza and A.B. Rylands. 1988. The howling monkeys, genus
Alouatta. In Ecology and Behaviour of Neotropical Primates, Vol. 2, eds. R.A
Mittermeier, A.B. Rylands, A. Coimbra-Filho and G.A.B. Fonseca, 349-453.
Washington D.C.: World Wildlife Fund.
Newton, P.N. 1985. The behavioural ecology of forest hanuman langurs. Tigerpaper 12: 3-7.
________. 1987. The social organization of forest hanuman langurs (Presbytis entellus). Int.
J. Primatol. 8: 199-232.
Nishida, T. 1973. The ant-gathering behaviour by the use of tools among wild chimpanzees
of the Mahale Mountains. J. Hum. Evol. 2: 357-370.
________. 1979. The social structure of chimpanzees of the Mahale Mountains. In The Great
Apes, ed. D.A. Hamburg and E.R. McCown. Menlo Park: Benjamin/Cummings.
________. 1983. Alloparental behavior in wild chimpanzees of the Mahale Mountains,
Tanzania. Folia Primatol. 41: 1-33.
Ng, H.C. 1972. Manual of laboratory methods of leaf analysis. Research Bulletin 8: 2-17.
Nicolson, N.A. 1987. Infants, mothers, and other females. In Primate Societies, eds. B.B.
Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham and T.T. Struhsaker, 330-342.
Chicago: University of Chicago Press.
Nie, N.H., C.H. Hull, J.G. Jenkins, K. Steinbrenner, and D.H. Bent. 1975. S.P.S.S: Statistical
Package for the Social Sciences. 2nd. ed. New York: McGraw Hill.
van Noordwijk, M.A. and C.P. van Schaik. 1985. Male immigration and rank acquisition in
wild long-tailed macaques Macaca fascicularis. Anim. Behav. 33: 849-861.
Oates, J.F. 1977a. The guereza and its food. In Primate Ecology: Studies of Feeding and
Ranging Behaviour in Lemurs, Monkey, and Apes, ed. T.H. Clutton-Brock. London:
Academic Press.
________. 1977b. The social life of a black and white colobus monkey (Colobus guereza). Z.
Tierpsychol 45: 1-60.
________. 1985. Action Plan for African Primate Conservation: 1986-1990. Washington
D.C.: WWF Primate Program and IUCN/SSC Primate Specialist Group.
________. 1987. Food distribution and foraging behavior. In Primate Societies, eds. B.B.
________. 1988. The diet of the olive colobus monkey Procolobus verus, in Sierra Leonne.
Int. J. Primatol. 9(5): 457-478.
139
Oates, J.F., T. Swain and J. Zantovska. 1977. Secondary compounds and food selection by
colobus monkeys. Biochem. System. Ecol. 5: 317-321.
Oates, J.F., P.G. Waterman and G.M. Choo. 1980. Food selection by the South Indian leaf
monkey, Presbytis johnii, in relation to leaf chemistry. Oecologia 45: 45-56.
Ohwaki, H., R.E. Hungate, L. Lotter, R.R. Hofmann and G. Maloiy. 1974. Stomach
fermentation in East African Colobus monkeys in their natural state. Appl. Microbiol.
27: 713-723.
Olupot, W., C.A. Chapman, C.H. Brown and P.M. Waser. 1994. Mangabey (Cercocebus
albigena) population density, group size, and ranging: A twenty year comparison. Am.
J. Primatol. 32: 197-205.
Packer, C. 1979. Inter-troop transfer and inbreeding avoidance in Papio anubis. Anim. Behav.
27: 223-243.
Parra, R. 1978. Comparison of foregut and hindgut fermentation in herbivores. In The
Ecology of Aboreal Folivores, ed. G.G. Montgomery, 205-229. Washington D.C.:
Smithsonian Institution Press.
Payne, J., Francis, C.M. & Phillips, K. 1985. A Field Guide to the Mammals of Borneo. Kuala
Lumpur: WWF Malaysia and The Sabah Society.
Payne, J. 1989. A tourism feasibility study for the proposed Kinabatangan Wildlife
Sanctuary. Kuala Lumpur: WWF Malaysia.
Poirier, F.E. 1968. Nilgiri langur (Presbytis johnii) territorial behavior. In Proceedings of the
Second Congress of the International Primatological Society, vol. 1, ed. C.R.
Carpenter. Basel: S. Karger.
Poole, T. 1985. Social Behaviour in Mammals. Glasgow: Blackie.
Post, D.G., G. Hausfater and S.A. McCuskey. 1980. Feeding behavior of yellow baboons
(Papio cynocephalus): Relationship to age, gender, and dominance rank. Folia
Primatol. 34: 170-195.
Pulliam, H.R. 1973. On the advantages of flocking. J. Theor. Biol. 38: 419-422.
Pulliam, H.R. 1976. The principle of optimal behavior and the theory of communities. In
Perspectives in Ethology, eds. P.H. Klopfer and P.P.G. Bateson, 311-332. New York:
Plenum Press.
Pulliam, H.R. and T. Caraco. 1984. Living in groups: is there an optimal group size? In
Behavioural Ecology: An Evolutionary Approach, eds. J.R. Krebs and N.B. Davies,
122-147. Oxford: Blackwell Scientific Publications.
Pusey, A.E. 1979. Intercommunity transfer of chimpanzees in Gombe National Park. In The
Great Apes, eds. D.A. Hamburg and E.R. McCown. Menlo Park, California:
Benjamin/Cummings.
________. 1980. Inbreeding avoidance in chimpanzees. Anim. Behav. 28: 543-582.
Pusey, A.E. and C. Packer. 1987. Dispersal and Philopatry. In Primate Societies, eds. B.B.
Pyke, G.H., H.R. Pulliam and E.L. Charnov. 1977. Optimal foraging: a selective review of
theory and tests. Quart. Rev. Biol. 52: 137-154.
Raemaekers, J.J. 1978. Changes through the day in the food choice of wild gibbons. Folia
Primatol. 30: 194-205.
________. 1980. Causes of variation between months in the distance travelled daily by
gibbons. Folia Primatol. 34: 46-60.
Rahaman, H. and M.D. Parthasarathy. 1962. Studies of the social behavior of bonnet
monkeys. Primates 10: 149-162.
140
Rajaratnam, R. 1991. Differential habitat use by primates in Samunsam Wildlife Sanctuary,
Sarawak, and its application to conservation management. Unpublished master’s
dissertation, University of Florida.
Rajanathan, R. and Bennett, E.L. 1990. Notes on the social behaviour of proboscis monkeys
(Nasalis larvatus). Malayan Nature Journal 44: 35-44.
Rasmussen, D.R. 1979. Correlates of patterns of range use of a troop of yellow baboons
(Papio cynocephalus). I. Sleeping sites, impregnable females, births and male
emigrations and immigrations. Anim. Behav. 27: 1098-1112.
Richard, A. 1985. Primates in Nature. New York: W.H. Freeman.
Robinson, J.G. and C.H. Janson. 1987. Capuchins, squirrel monkeys, and atelines:
socioecological convergence with old world primates. In Primate Societies, eds. B.B.
Robinson, T. 1979. The evolutionary ecology of alkaloids. In Herbivores, Their Interactions
with Secondary Plant Metabolites, ed. G.A. Rosenthal and D.H. Janzen, 413-448.
New York and London: Academic Press.
Rosenblum, L.A., I.C. Kaufman and A.J. Stynes. 1966. Some characteristics of adult social
and autogrooming patterns in two species of macaque. Folia Primatol. 4: 438-451.
Rosenthal, G.A. and D.H. Janzen, eds. 1979. Herbivores, Their Interactions with Secondary
Plant Metabolites. New York and London: Academic Press.
Rudran, R. 1973. Adult male replacement in one-male troops of purple-faced langurs
(Presbytis senex) and its effect on population structure. Folia Primatol. 19: 41-60.
Sade, D.S. 1965. Some aspects of parent-offspring relations in a group of rhesus monkeys,
with a discussion of grooming. Am. J. Phys. Anthrop. 23: 1-18.
Salter, R.E. and Mackenzie, N.A. 1985. Conservation status of the proboscis monkey in
Sarawak. Biol. Conserv. 33: 119-132.
Salter, R.E., N.A. MacKenzie, N. Nightingale, K.M. Aken, and P.P.K. Chai. 1985. Habitat
use, ranging behaviour and food habitats of the proboscis monkey, Nasalis larvatus
(van Wurmb) in Sarawak. Primates 26: 436-451.
van Schaik, C.P. and J. van Hooff. 1983. On the ultimate causes of primate social systems.
van Schaik, C.P., M.A. van Noordwijk, R.J. de Boer and I. den Tonkelaar. 1983. The effect
of group size on time budgets and social behaviour in wild long-tailed macaques
(Macaca fascicularis). Behav. Ecol. Sociobiol. 13: 173-181.
Schaller, G.B. 1985. China’s golden treasure. International Wildlife 15: 29-31.
Schoener, T.W. 1971. Theory of feeding strategies. Ann. Rev. Ecol. Syst. 2: 369-404.
Schulz, A.H. 1942. Growth and development of the proboscis monkey. Bull. Mus. Comp.
Zool., Harvard. 89: 279-314.
Scott, D.A. ed. 1989. A Directory of Asian Wetlands. Gland, Switzerland/Cambridge, U.K:
IUCN.
Sekulic, R. 1982. Daily and seasonal patterns of roaring and spacing in four red howler
Alouatta seniculus troops. Folia Primatol. 39: 22-48.
Seyfarth, R.M. 1980. A distribution of grooming and related behaviours among adult female
vervet monkeys. Anim. Behav. 28: 798-813.
Sharma, D.S. 1992. A wildlife survey of the proposed Kinabatangan Park, Sabah. Kuala
Lumpur: WWF Malaysia.
Siegel, S. and N.J. Castellan, Jr. 1988. Nonparametric Statistics for the Behavioral Sciences.
2nd ed. Singapore: McGraw Hill.
Sigg, H. and A. Stolba. 1981. Home range and daily march in a hamadryas baboon troop.
Folia Primatol. 36: 40-75.
141
Sigg, H., A. Stolba, J.J. Abegglen and V. Dasser. 1982. Life history of hamadryas baboons:
Physical development, infant mortality, reproductive parameters, and family
relationships. Primates 23: 473-487.
Silk, J.B. 1987. Social behavior in evolutionary perspective. In Primate Societies, eds. B.B.
________. 1980. Kidnapping and female competition among captive bonnet macaques.
Primates 21: 100-110.
Simes, J.J.H., J.G. Tracy, C.J. Wibb and W.J. Duristaon. 1959. Australian phytochemical
survey III: Saponin in eastern Australia flowering plants. CSIRO Bulletin, No. 281.
Smith, E.O. ed. 1978. Social Play in Primates. New York: Academic Press.
Smuts, B.B., D.L. Cheney, R.M. Seyfarth, R.W. Wrangham and T.T. Struhsaker. eds. 1987.
Primate Societies. Chicago: University of Chicago Press.
van Soest, P.J. 1977. Plant fibre and its role in herbivore nutrition. Cornell Vet. 67: 307-326.
________. 1981. Forages, Fiber, and the Rumen. Corvallis: C. and O. Books
________.1982. Nutritional Ecology of the Ruminant.
Corvallis: O. and B. Books. van Soest, P.J. and R.H. Wine. 1967. Use of detergents in the
analysis of fibrous feeds. IV. Determination of plant cell-wall constituents. Journal of
the A.O.A.C. 50(1): 50-55.
van Soest, P.J., P. Uden and K.F. Wrick. 1983. Critique and evaluation of markers for use in
nutrition of humans and farm and laboratory animals. Nutr. Rep. Int. 27: 17-28.
Stanford, C.G. 1991. The Capped Langur in Bangladesh: Behavioral Ecology and
Reproductive Tactics, ed. F.S. Szalay. Vol 26. Contributions to Primatology. Basel:
Karger.
Stewart, K.J. and A.H. Harcourt. 1987. Gorillas: Variations in female relationships. In
Primate Societies, eds. B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham
and T.T. Struhsaker, 155-164. Chicago: University of Chicago Press.
Struhsaker, T.T, 1967. Ecology of vervet monkeys (Cercopithecus aethiops) in the Masai-
Amboseli game reserve, Kenya. Ecology 48: 891-904.
________. 1969. Correlates of ecology and social organization among African
cercopithecines. Folia Primatol. 11: 80-118.
________. 1974. Correlates of ranging behaviour in a group of red colobus monkeys
(Colobus badius tephrosceles). Am. Zool. 14: 177-184.
________. 1975. The Red Colobus Monkey. Chicago: University of Chicago Press.
________. 1978. Inter-relations of red colobus monkeys and rainforest trees in the Kibale
Forest, Uganda. In The Ecology of Arboreal Folivores, ed. G.G. Montgomery, 397-
422. Washington D.C.: Smithsonian Institution Press.
________. 1980. Comparison of the behaviour and ecology of red colobus and redtail
monkeys in the Kibale Forest, Uganda. Afr. J. Ecol. 18: 33-51.
Struhsaker, T.T. and L. Leland. 1979. Socioecology of five sympatric monkey species in the
Kibale Forest, Uganda. In Advances in the Study of Behavior, eds. J.S. Rosenblatt,
R.A. Hinde, C. Beer and M.C. Busnel, 159-228. New York: Academic Press.
________. 1987. Colobines: infanticide by adult males. In Primate Societies. eds. Smuts,
B.B., D.L. Cheney, R.M. Seyfarth, R.W. Wrangham and T.T. Struhsaker, 281-324.
Struhsaker, T.T. and J.F. Oates. 1975. Comparison of the behaviour and ecology of red
colobus and black-and- white colobus monkeys in Uganda: a summary. In Socio-
ecology and Psychology of Primates, ed. R.H. Tuttle, 103-123. Hague: Paris.
Sugiyama, Y. 1967. Social organisation of hanuman langurs. In Social Communication
Among Primates, ed. S.A. Altmann, 221-236. Chicago: University of Chicago Press
142
Sugiyama, Y. 1976. Characteristics of the ecology of the Himalayan langurs. J. Hum. Evol. 5:
249-277.
Supriatna, J., B.O. Manullang and E. Soekara. 1986. Group composition, home range, and
diet of the maroon leaf monkey (Presbytis rubicunda) at Tanjung Puting Reserve,
Central Kalimantan, Indonesia. Primates 27(2): 185-190.
Suzuki, A. 1979. The variation and adaptation of social groups of chimpanzees and black and
white colobus monkeys. In Primate Ecology and Human Origins, eds. I. Bernstein
and E.O. Smith, 153-173. New York: Garland.
Symons, D. 1978. Play and Agression: A Study of Rhesus Monkeys. New York: Columbia
University Press.
Takasaki, H. 1981. Troop size, habitat quality and home range area in Japanese macaques.
Behav. Ecol. Sociobiol. 9: 277-281.
Taub, D.M. 1977. Geographic distribution and habitat diversity of the Barbary macaque
(Macaca sylvanus). Folia Primatol. 27: 108-133.
Teas, J., T. Richie, H. Taylor and C. Southwick. 1980. Population patterns and behavioural
ecology of rhesus monkeys (Macaca mulatta) in Nepal. In The Macaques, ed. D.G.
Lindburg, 247-262. New York: Van Nostrand Reinhold.
Tenaza, R. 1975. Territory and monogamy among Kloss’ gibbons (Hylobates klossi) in
Siberut island, Indonesia. Folia Primatol. 24: 60-80.
Terborgh, J. 1983. Five New World Primates: A Study in Comparative Ecology. Princeton:
Princeton University Press.
Terborgh,J. and C.H. Janson. 1986. The socioecology of primate groups. Ann. Rev. Ecol.
Systemat. 17: 111-135.
Tilson, R.L. 1981. Family formation strategies of Kloss gibbons. Folia Primatol. 35: 259-
287.
Treisman, M. 1975a. Predation and the evolution of gregariousness. I. Models for
concealment and evasion. Anim. Behav. 23: 779-800.
________. 1975b. Predation and the evolution of gregariousness. II. An economic model for
predator-prey interaction. Anim. Behav. 223: 801-825.
Underwood, R. 1982. Vigilance behaviour in grazing African antelopes. Behaviour 79: 81-
107.
Vellayan, S. 1982. Chemistry and digestibility of foods of the lar gibbon (Hylobates lar).
Unpublished master’s dissertation, Universiti Pertanian Malaysia.
Wada, K. and Y. Ichiki. 1980. Seasonal home range use by Japanese monkeys in the snowy
Shinga Heights. Primates 21: 468-483.
Walters, J.R. 1987. Transition to adulthood. In Primate Societies, eds. B.B. Smuts, D.L.
Cheney, R.M. Seyfarth, R.W. Wrangham and T.T. Struhsaker 358-369. Chicago:
University of Chicago Press.
Walters, J.R. and R.M. Seyfarth. 1987. Conflict and cooperation. In Primate Societies, eds.
B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham and T.T. Struhsaker 306-
317. Chicago: University of Chicago Press.
Waser, P.M. 1976. Cercocebus albigena: site attachment, avoidance and intergroup spacing.
Am. Nat. 110: 911-935.
Waterman, P.G. 1984. Food acquisition and processing by primates as a function of plant
chemistry. In Food Acquisition and Processing by Primates, eds. D.J. Chivers, B.A.
Wood and A. Bilsborough, 177-211. New York: Plenum Press.
Waterman, P.G. and G.M. Choo. 1981. The effects of digestibility reducing compounds in
leaves on food selection by some Colobinae. Malaysian Applied Biology 10: 147-162.
Waterman, P.G., J.A.M. Ross, E.L. Bennett and A.G. Davies. 1988. A comparison of the
floristics and leaf chemistry of the tree flora in two Malaysian rain forests and the
143
influence of leaf chemistry on populations of colobine monkeys in the Old World.
Biol, J. of the Linn. Soc. 34: 1-32.
Whitmore, T.C. 1984. Tropical Rain Forests of the Far East. Oxford: Clarendon Press.
Whitten, A.J. 1980. The Kloss gibbon in Siberut rainforest. Unpublished doctoral
dissertation, University of Cambridge.
________. 1982. Home range use by Kloss gibbon (Hylobates klossii) on Siberut island,
Indonesia. Anim. Behav. 30: 182-198.
Whitten, P.L. 1983. Diet and dominance among female vervet monkeys (Cercopithecus
aethiops). Am. J. Primatol. 5: 139-159.
Wilson, E.O. 1975. Sociobiology: The new synthesis. Cambridge: Harvard University Press.
Wrangham, R.W. 1975. The behavioural ecology of chimpanzees in the Gombe National
Park, Tanzania. Unpublished doctoral dissertation, University of Cambridge.
________. 1977. Feeding behaviour of chimpanzees in Gombe National Park, Tanzania. In
Primate Ecology, ed. T.H. Clutton-Brock, 503-538. London: Academic Press.
________. 1979. On the evolution of ape social systems. Social Sciences Information 18:
335-368.
________. 1980. An ecological model of female-bonded primate groups. Behaviour 75: 262-
300.
________. 1981. Drinking competition in vervet monkeys. Anim. Behav. 29: 904-910.
________. 1987. Evolution of social structure. In Primate Societies, eds. B.B. Smuts, D.L.
Cheney, R.M. Seyfarth, R.W. Wrangham and T.T. Struhsaker, 282-296.
Chicago: Chicago University Press.
Yeager, C.P. 1989. Feeding ecology of the proboscis monkey (Nasalis larvatus). Int. J.
Primatol. 10: 497-530.
Yeager, C.P. 1990a. Proboscis monkey (Nasalis larvatus) social organization: group
structure. Am. J. Primatol. 20: 95-106.
________. 1990b. Notes on the sexual behavior of the proboscis monkey (Nasalis larvatus).
Am. J. Primatol. 21: 223-227.
________. 1991a. Proboscis monkey (Nasalis larvatus) social organization: Intergroup
patterns of association. Am. J. Primatol. 23: 73-86.
________. 1991b. Possible antipredator behaviour associated with river crossings by
proboscis monkeys (Nasalis larvatus). Am. J. Primatol. 24: 61-66.
________. 1992. Proboscis monkey (Nasalis larvatus) social organization: Nature and
possible functions of intergroup patterns of association. Am. J. Primatol. 26: 133-137.
Yoshiba, K. 1968. Local and intertroop variability in ecology and social behaviour of
common Indian langurs. In Primates: Studies in Adaptation and Variability, ed. P.C.
Jay, 217-242. New York: Holt, Rhinehart and Winston.
Zucker, E.L. and J.R. Kaplan. 1981. Allomaternal behavior in a group of free-ranging patas
monkeys. Am. J. Primatol. 1(1): 57-64.
144
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
145
Mammals
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
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
146
Birds
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
147
Birds
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
148
Birds
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
149
Birds
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
150
Birds
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
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
151
Reptiles
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
Greater Swamp Frog Rana ingeri
Green Paddy Frog Rana erthraea
Cricket Frog Rana nicobariensis
White-lipped Frog Rana chalconata
152
APPENDIX II: LIST OF WILD FAUNA RECORDED AT ABAI
Mammals
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
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
153
Birds
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
154
Birds
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
Water Monitor Lizard Varanus salvator
Estuarine Crocodile Crocodylus porosus
155
APPENDIX III: TREE SPECIES AND THEIR PROPORTIONS IN THE BOTANICAL
TRANSECTS AT SUKAU (N=1378).
Family Species No. of % Total % Total

Stems Stems Basal Area
Alangiaceae Alangium ebenaceum 4 0.3 0.09
Anacardiaceae Buchanania insignis 56 4.1 2.77
Anacardiaceae Dracontomelon mangiferum 1 0.1 0.03
Annonaceae Cananga odorata 3 0.2 0.77
Annonaceae Phaenthus crassipetalus 3 0.2 0.14
Annonaceae Polyalthia glauca 7 0.5 0.33
Apocynaceae Alstonia angustifolia 1 0.1 0.02
Apocynaceae Alstonia angustiloba 1 0.1 0.02
Bombacaceae Coelostegia griffithii 1 0.1 0.02
Bombacaceae Durio grandiflorus 1 0.1 0.12
Burseraceae Canarium apertum 51 3.7 3.27
Clusiaceae Cratoxylum sumatrana 47 3.4 5.28
Clusiaceae Cratoxylum borneensis 1 0.1 0.04
Clusiaceae Calophyllum borneensis 51 3.7 2.08
Clusiaceae Calophyllum canum 12 0.9 0.57
Clusiaceae Garcinia bancana 12 0.9 0.39
Clusiaceae Garcinia forbesii 1 0.1 0.02
Combretaceae Terminalia foetidissima 8 0.6 1.20
Datisaceae Octomeles sumatrana 6 0.5 0.27
Dilleniaceae Dillenia excelsa 1 0.1 0.35
Dilleniaceae Dillenia grandifolia 98 7.1 2.30
Dilleniaceae Dillenia indica 7 0.5 0.18
Dipterocarpaceae Dipterocarpus applanatus 4 0.3 0.46
Dipterocarpaceae Dipterocarpus caudiferus 7 0.5 0.94
Dipterocarpaceae Dipterocarpus stellatus 1 0.1 0.03
Dipterocarpaceae Dryobalanops lanceolata 2 0.1 0.28
Dipterocarpaceae Hopea nervosa 2 0.1 0.63
Dipterocarpaceae Parashorea melaanonan 1 0.1 0.03
Dipterocarpaceae Parashorea tomentalla 2 0.1 0.04
Dipterocarpaceae Shorea beccariana 7 0.5 0.24
Dipterocarpaceae Shorea faguetina 1 0.1 0.01
Dipterocarpaceae Shorea glaucescens 2 0.1 0.04
Dipterocarpaceae Shorea inappendiculata 1 0.1 0.08
Dipterocarpaceae Shorea leprosula 8 0.6 1.64
Dipterocarpaceae Shorea macroptera 4 0.3 0.64
156
Dipterocarpaceae Shorea platyclados 1 0.1 0.16
Dipterocarpaceae Shorea scrobiculata 2 0.1 0.08
Dipterocarpaceae Shorea smithiana 2 0.1 2.40
Dipterocarpaceae Shorea xanthophylla 1 0.1 0.05
Dipterocarpaceae Vatica acrocarpa 7 0.5 0.56
Dipterocarpaceae Vatica oblongifolia 38 2.8 1.91
Ebenaceae Diospyros pendula 38 2.8 2.45
Elaeocarpaceae Elaeocarpus canipes 13 0.9 0.76
Euphorbiaceae Bacaurea bracteata 7 0.5 0.18
Euphorbiaceae Bacaurea parviflora 27 1.9 0.49
Euphorbiaceae Baccaurea pubera 2 0.1 0.05
Euphorbiaceae Erismanthus multonii 2 0.1 0.02
Euphorbiaceae Glochidion borneensis 39 2.8 1.98
Euphorbiaceae Koilodepos leavigatum 2 0.1 0.04
Euphorbiaceae Macaranga conifera 18 1.3 0.38
Euphorbiaceae Macaranga hypoleuca 11 0.8 0.23
Euphorbiaceae Mallotus muticus 76 5.5 10.95
Fagaceae Lithocarpus lucidus 1 0.1 0.03
Flacourtiaceae Homalium foetidum 6 0.4 0.46
Flacourtiaceae Hydnocarpus woodii 14 1.0 1.70
Irvingiaceae Irvingia malayana 3 0.2 0.45
Lauraceae Alseodaphne bancana 1 0.1 0.03
Lauraceae Beilschmiedia micrantha 1 0.1 0.01
Lauraceae Cryptocarya cuneata 1 0.1 0.12
Lauraceae Eusideroxylon zwageri 10 0.8 2.86
Lauraceae Litsea firma 15 1.1 0.83
Lauraceae Litsea odorifera 81 5.9 4.26
Lauraceae Notaphoebe kingiana 3 0.2 0.21
Lauraceae Phoebe macrophylla 1 0.1 0.03
Lecythidaceae Baringtonia lanceolata 31 2.3 0.99
Leguminosae Albizzia chinensis 1 0.1 0.04
Leguminosae Albizzia pedicellata 1 0.1 0.02
Leguminosae Fordia cf. gibbsiae 5 0.4 0.16
Leguminosae Intsia palembica 1 0.1 0.42
Leguminosae Koompassia excelsa 1 0.1 0.24
Leguminosae Parkia speciosa 1 0.1 0.14
Leguminosae Sindora irpicina 5 0.4 0.14
Leguminosae Spatholobus hirsutus 1 0.1 0.02
157
Leguminosae Sympetalandra borneensis 6 0.4 0.56
Melastomaceae Kibessia galeata 55 4.0 6.42
Meliaceae Aglaia ignea 6 0.4 0.14
Meliaceae Amoora malaccensis 3 0.2 0.15
Meliaceae Chisocheton beccariana 2 0.1 0.30
Moraceae Artocarpus dadah 1 0.1 0.02
Moraceae Artocarpus elasticus 1 0.1 0.04
Moraceae Artocarpus tamaran 4 0.3 0.09
Moraceae Ficus condensa 12 0.9 2.60
Myristicaceae Knema latifolia 14 1.0 0.73
Myrtaceae Syzygium bankense 122 8.9 8.90
Olacaceae Scorodocarpus borneensis 1 0.1 0.14
Polygalaceae Xanthophyllum rufum 18 1.3 1.20
Rhizophoraceae Carallia brachiata 2 0.1 0.04
Rosaceae Atuna elata 2 0.1 0.15
Rosaceae Parinari oblongifolia 2 0.1 0.08
Rubiaceae Anthocephalus chinensis 27 2.0 3.62
Rubiaceae Neonauclea bernadoi 90 6.5 5.43
Rutaceae Meliocope confusa 5 0.4 0.07
Sapindaceae Nephelium beccarianum 1 0.1 0.01
Sapindaceae Paranephelium nitidum 3 0.2 0.09
Sapotaceae Palaquium rostratum 6 0.5 0.11
Sapotaceae Payena lucida 12 0.9 0.39
Sonneratiaceae Duabanga moluccana 6 0.4 0.69
Sterculiaceae Heritiera borneensis 3 0.2 0.09
Sterculiaceae Heritiera elata 2 0.1 0.03
Sterculiaceae Heritiera littoralis 1 0.1 0.21
Sterculiaceae Pterospermum elongatum 25 1.8 2.21
Tiliaceae Microcos antidesmifolia 21 1.6 0.99
Tiliaceae Pentace adenophora 1 0.1 0.04
Tiliaceae Pentace borneensis 3 0.2 0.24
Tiliaceae Pentace erectinervia 4 0.3 0.44
Verbenceae Teijsmanniodendron bogoriense 2 0.1 0.13
Verbenceae Teijsmanniodendron sympliciodes 10 0.7 0.25
Verbenceae Vitex pinnata 20 1.5 1.89
158
APPENDIX IV: TREE SPECIES AND THEIR PROPORTIONS IN THE BOTANICAL
TRANSECTS AT ABAI (N=300).

Anacardiaceae Buchanania insignis 22 7.4 3.93
Anacardiaceae Mangifera pajang 1 0.3 1.55
Annonaceae Polyalthia glauca 9 3.0 2.99
Apocynaceae Alstonia angustifolia 10 3.3 1.50
Burseraceae Canarium apertum 12 4.0 3.16
Clusiaceae Calophyllum borneensis 6 2.0 0.71
Clusiaceae Calophyllum canum 4 1.3 0.85
Clusiaceae Cratoxylum sumatrana 2 0.7 0.21
Clusiaceae Garcinia bancana 1 0.3 0.13
Combretaceae Terminalia foetidissima 2 0.7 2.01
Dilleniaceae Dillenia excelsa 9 3.0 0.79
Dipterocarpaceae Shorea leprosula 3 1.0 0.68
Dipterocarpaceae Vatica oblongifolia 3 1.0 0.21
Dipterocarpaceae Vatica papuana 1 0.3 0.13
Ebenaceae Diospyros evana 2 0.7 0.19
Ebenaceae Diospyros pendula 6 2.0 0.66
Elaeocarpaceae Elaeocarpus canipes 25 8.3 6.90
Euphorbiaceae Baccaurea pubera 6 2.0 1.35
Euphorbiaceae Glochidion borneensis 2 0.7 0.58
Euphorbiaceae Macaranga conifera 2 0.7 0.10
Flacourtiaceae Homalium foetidum 3 1.0 0.76
Lauraceae Litsea odorifera 4 1.3 1.23
Lecythidaceae Barringtonia lanceolata 1 0.3 0.09
Leguminosae Sindora irpicina 1 0.3 0.10
Melastomaceae Kibessia galeata 42 14.0 8.05
Moraceae Artocarpus dadah 1 0.3 0.48
Moraceae Ficus condensa 7 2.3 14.23
Myrtaceae Syzygium bankense 34 11.3 5.99
Polygalaceae Xanthophyllum rufum 12 4.0 3.61
Rhizophoraceae Bruguiera sexangula 16 5.3 19.51
Rhizophoraceae Ceriops tagal 3 1.0 0.35
Rubiaceae Neonauclea bernadoi 5 1.7 3.91
Rutaceae Evoida confusa 1 0.3 0.29
Sapotaceae Ganua motleyana 1 0.3 0.08
Sapotaceae Madhuca burkiana 1 0.3 0.12
159
Sapotaceae Palaquium rostratum 2 0.7 0.35
Sapotaceae Planchonella obovata 1 0.3 0.11
Sterculiaceae Heritieria littoralis 7 2.3 4.34
Thymelaeaceae Gonystylus keithii 5 1.7 0.89
Verbenceae Teijsmanniodendron 1 0.3 0.39
sympliociodes
Verbenceae Vitex pinnata 24 8.0 4.87
160
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 56.8
Annonaceae
Goniothalamus roseus ML - 1+ 0.34 2.13 0.30 82.6
Polyalthia insignis ML - - 0.29 1.81 0.35 80.5
Polyalthia glauca ML - - 0.25 1.56 9.15 56.5
Apocynaceae
Willughbeia aff. coriacea ML - 1+ 0.19 1.19 4.47 52.6
Burseraceae
Dacroyodes aff. rugosa ML - - 0.24 1.50 0.94 62.7
Clusiaceae
Garcinia aff. parviflora ML 3+ 1+ 0.20 1.25 2.35 41.7
Garcinia aff. parviflora YL 3+ ? 0.27 1.69 2.47 36.2
Garcinia aff. parviflora FR ? 1+ 0.21 1.31 1.30 50.4
Dipterocarpaceae
Dipterocarpus aff. caudiferus ML - - 0.20 1.25 0.94 62.6
Vatica sp. A ML - - 0.31 1.94 2.59 52.9
Vatica sp. A YL - - 0.35 2.19 2.82 47.8
Vatica sp.B ML - - 0.34 2.13 2.23 65.1
Dilleniaceae
Dillenia indica ML - 1+ 0.28 1.75 0.24 64.2
Dillenia indica YL - - 0.31 1.94 0.24 62.3
Dillenia indica FL - - 0.19 1.19 0.12 62.9
Ebenaceae
Diospyros lanceifolia ML - 2+ 0.31 1.94 0.47 58.0
Diospyros frutescens ML - 2+ 0.27 1.69 0.00 69.6
Diospyros levigata ML - 1+ 0.39 2.44 13.52 70.8
Diospyros levigata YL - ? 0.78 4.88 1.53 66.0
Diospyros pendula ML - - 0.26 1.63 0.12 56.0
Diospyros pendula FR ? 3+ 0.27 1.69 3.65 53.2
Diospyros sp. B ML - - 0.36 2.25 1.88 72.4
Elaeocarpaceae
Elaeocarpus canipes ML - - 0.27 1.68 0.82 52.5
Euphorbiaceae
Aporusa sp. ML - - 0.27 1.68 0.12 41.8
161
Aporusa sp YL - 1+ 0.39 2.44 0.24 52.6
Aporusa elmeri ML - 2+ 0.25 1.56 1.53 61.8
Aporusa elmeri FR ? ? 0.25 1.56 5.53 52.3
Aporusa frutescens ML - 1+ 0.28 1.75 1.06 45.5
Aporusa frutescens FR ? 3+ 0.22 1.38 1.30 62.1
Antidesma neurocarpus ML - 1+ 0.18 1.13 1.06 54.0
Antidesma neurocarpus YL - ? 0.28 1.75 0.00 47.8
Baccaurea parviflora ML - 3+ 0.28 1.75 0.00 65.7
Baccaurea parviflora YL - ? 0.37 2.31 0.24 55.3
Baccaurea parviflora FR - ? 0.21 1.31 3.18 72.9
Baccaurea sp. ML - 2+ 0.25 1.56 0.47 57.7
Baccaurea sp. FR - ? 0.26 1.63 2.00 48.8
Chaetocarpus aff. castanocarpus ML - 1+ 0.29 1.81 0.47 67.4
Claoxylon sp. A ML - - 0.14 0.88 2.71 61.1
Claoxylon sp. A YL - - 0.67 4.19 0.47 57.2
Cleistanthus sp. ML - 1+ 0.28 1.75 1.05 47.6
Croton argyratus ML - - 0.39 2.44 0.35 62.9
Croton oblongifolius ML - 2+ 0.46 2.88 0.94 63.8
Croton oblongifolius YL - ? 0.54 3.38 0.94 71.4
Croton sp ML - 1+ 0.36 2.25 0.47 57.9
Croton sp YL - 1+ 0.43 2.69 0.00 68.0
Croton sp FL ? 1+ 0.16 1.00 0.35 74.0
Drypetes sp. ML - 2+ 0.15 0.94 12.60 62.0
Macaranga beccariana ML - - 0.25 1.56 1.88 63.7
Mallotus penangensis ML 3+ 1+ 0.53 3.31 5.29 58.4
Mallotus penangensis FR ? - 0.15 0.94 0.00 82.5
Mallotus wrayi ML - 1+ 0.43 2.69 0.12 56.2
Mallotus wrayi YL - 1+ 0.48 3.00 0.00 65.7
Mallotus sp. A ML - - 0.35 2.19 0.47 76.8
Mallotus sp. A YL - - 0.55 3.44 0.00 69.7
Mallotus muticus ML - 1+ 0.27 1.69 0.00 59.6
Mallotus muticus YL - ? 0.46 2.88 0.35 55.1
Mallotus muticus FR ? 1+ 0.23 1.44 0.47 62.7
Mallotus sp. B ML - - 0.34 2.13 2.58 61.9
Mallotus sp. B YL - ? 0.69 4.31 0.00 45.7
Mallotus sp. C ML - 2+ 0.59 3.69 0.00 39.9
Mallotus sp. C YL - - 0.67 4.19 0.00 30.9
Phyllanthodendron sp. ML - 2+ 0.46 2.88 0.35 45.3
Phyllanthodendron sp. YL - 1+ 0.36 2.25 0.58 39.1
Sapium aff. indicum ML - 2+ 0.35 2.19 0.00 63.7
162
Vatica sp. B FR ? 1+ 0.12 0.75 2.23 59.2
Euphorbiaceae sp. B FR ? 2+ 0.21 1.31 6.70 54.6
Euphorbiaceae sp. C FR ? ? 0.15 0.94 0.35 67.5
Fagaceae
Lithocarpus lucidus ML - 1+ 0.43 2.68 1.06 60.5
Lithocarpus lucidus YL - ? 0.46 2.88 0.00 50.8
Flacourtiaceae
Homalium foetidum ML - - 0.23 1.44 30.34 40.6
Hydnocarpus woodii ML - 1+ 0.31 1.94 3.65 67.0
Flacortiaceae sp. ML 1+ - 0.25 1.56 12.11 75.3
Gnetaceae
Gnetum gnemon ML - 1+ 0.26 1.63 0.47 34.6
Gnetum gnemon FR - 1+ 0.13 0.81 2.12 41.6
Hyporicaceae
Cratoxylum aff. formosum ML - - 0.30 1.88 1.29 47.8
Lauraceae
Cinnamomum griffithi ML - 1+ 0.23 1.44 0.35 49.6
Litsea odorifera ML 1+ 3+ 0.22 1.38 16.11 73.9
YL 1+ ? 0.41 2.56 13.41 56.3
Lauraceae sp. ML - - 0.29 1.81 12.94 72.1
Lecythidaceae
Barringtonia aff. macrostachys ML - - 0.27 1.69 0.82 58.2
YL - - 0.27 1.69 0.58 45.8
Barringtonia sp. A ML - 1+ 0.23 1.44 1.88 51.2
Barringtonia sp. A YL - 1+ 0.26 1.63 0.58 47.4
Barringtonia lanceolata ML - - 0.28 1.77 0.24 56.3
Barringtonia lanceolata YL - 2+ 0.48 3.00 0.00 55.2
Barringtonia sp. B FL ? ? 0.40 2.50 0.12 39.2
Fabaceae
Fabaceae sp. ML - - 0.34 2.13 18.94 69.5
Spantholobus hirsutus ML - 2+ 0.73 4.56 0.00 91.5
Loganiceae
Fagraea aff. racemosa ML - 1+ 0.24 1.50 0.00 83.0
Lythraceae
Sonneratia alba ML - - 0.33 2.06 5.15 52.2
Sonneratia alba FR - - 0.28 1.75 0.35 67.0
Melastomataceae
Kibbesia azurea ML - ? 0.27 1.69 1.88 53.7
Kibessia sp. A ML - - 0.36 2.25 0.35 45.3
Kibessia galeata ML - - 0.23 1.44 0.00 41.4
163
Meliaceae
Aglaia sp. ML - 2+ 0.72 4.50 0.25 62.5
Sapindaceae
Pometia aff. pinnata ML - 1+ 0.22 1.38 2.94 45.9
Pometia aff. pinnata YL - 1+ 0.50 3.13 0.47 42.2
Moraceae
Ficus sp. A ML - 1+ 0.20 1.25 0.35 62.9
Poikilospermum aff. cordifolium ML - 1+ 0.29 1.81 0.00 61.9
Poikilospermum aff. cordifolium YL - 1+ 0.36 2.25 1.53 55.9
Poikilospermum aff. cordifolium FR ? 1+ 0.29 1.81 0.47 51.8
Poikilospermum aff. cordifolium FL - 1+ 0.33 2.06 0.23 66.3
Myristicaceae
Knema aff. laurina ML - - 0.18 1.13 6.35 68.6
Knema latifolia ML - 2+ 0.36 2.25 3.41 76.0
Myrisnaceae
Ardisia polyactis ML - 2+ 0.14 0.88 5.70 37.9
Myrtaceae
Eugenia sp. A ML - 1+ 0.24 1.50 0.35 66.2
Eugenia sp. B ML - 3+ 0.32 2.00 0.47 48.6
Eugenia sp. C ML 2+ - 0.21 1.31 0.71 67.9
Eugenia sp. E ML - 1+ 0.37 2.31 0.71 59.0
Eugenia sp. F ML - 2+ 0.26 1.63 0.94 57.8
Eugenia sp. G ML - 1+ 0.22 1.38 0.94 60.3
Eugenia sp. J ML - 1+ 0.18 1.13 0.71 74.6
Eugenia sp. M ML - - 0.28 1.75 2.94 69.9
Syzygium sp. ML - 4+ 0.19 1.19 0.25 55.3
Myrtaceae sp. ML - ? 0.24 1.50 4.23 78.9
Oleaceae
Chionanthus cuspidita ML - 1+ 0.22 1.38 13.29 72.7
Chionanthus cuspidita YL - - 0.25 1.56 0.35 70.7
Polygalaceae
Xanthophyllum affine ML - 1+ 0.27 1.69 0.35 65.6
FR ? ? 0.33 2.06 0.12 70.9
Xanthophyllum aff. affine ML - - 0.34 2.13 0.24 78.7
Xanthophyllum aff. affine YL - ? 0.36 2.25 0.35 84.2
Xanthophyllum aff. affine FR ? ? 0.41 2.56 0.35 84.1
Xanthophyllum cordatum ML - 1+ 0.42 2.63 0.71 72.9
Xanthophyllum cordatum FR - ? 0.37 2.31 0.35 88.3
Xanthophyllum rufun ML - 1+ 0.25 1.56 0.00 69.1
Xanthophyllum rufun ML - 1+ 0.34 2.13 0.00 66.4
164
Xanthophyllum rufun YL - ? 0.48 3.00 0.24 87.7
Xanthophyllum sp. C ML - 1+ 0.38 2.38 0.35 83.3
Xanthophyllum sp. M ML - ? 0.23 1.44 0.24 73.1
Rhizophoraceae
Carallia brachiata ML - - 0.24 1.50 1.18 43.7
Rhamnaceae
Zizyphus horsifieldii ML - 1+ 0.24 1.50 27.15 59.8
Zizyphus horsifieldii FR ? 1+ 0.22 1.37 0.35 64.0
Rosaceae
Rosaceae sp. A ML ? ? 0.31 1.94 0.12 39.0
Rosaceae sp. A YL - - 0.23 1.44 0.35 35.2
Rubiaceae
Neonauclea bernardoi ML - 1+ 0.32 2.00 2.82 52.6
Neonauclea bernardoi YL - 1+ 0.38 2.38 0.47 42.4
Pleiocarpidia aff. capitata ML - - 0.30 1.88 0.47 48.9
Pleiocarpidia aff. capitata FL - ? 0.30 1.88 0.47 46.2
Sapotaceae
Madhuca sp. ML - 2+ 0.23 1.44 1.88 51.1
Payena sp ML - - 0.32 2.00 1.77 67.2
Styracaceae
Styracaceae sp. ML - - 0.24 1.50 0.95 62.5
Theaceae
Pyrenaria parviflora ML - ? 0.17 1.06 22.34 40.7
Pyrenaria parviflora YL - 1+ 0.22 1.38 4.35 37.7
Tiliaceae
Microcos antidesmofolia YL - 1+ 0.42 2.63 0.35 89.6
Microcos sp. A ML - 1+ 0.17 1.06 1.41 64.2
Microcos sp. A YL - ? 0.43 2.69 0.47 82.2
Microcos sp. B ML - 1+ 0.27 1.69 2.82 67.2
Microcos sp. B YL - 1+ 0.37 2.31 0.60 59.3
Pentace laxiflora ML - - 0.25 1.56 23.76 69.5
Verbenaceae
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)
165

Boonratana, R. 1993a. The Ecology and Behaviour of The Proboscis Monkey (Nasalis Larvatus) in The Lower Kinabatangan, Sabah. Unpublished Doctoral Dissertation, Mahidol University

Diunggah oleh

Informasi Dokumen

Deskripsi Asli:

Judul Asli

Hak Cipta

Format Tersedia

Bagikan dokumen Ini

Bagikan atau Tanam Dokumen

Opsi Berbagi

Apakah menurut Anda dokumen ini bermanfaat?

Apakah konten ini tidak pantas?

Hak Cipta:

Format Tersedia

Boonratana, R. 1993a. The Ecology and Behaviour of The Proboscis Monkey (Nasalis Larvatus) in The Lower Kinabatangan, Sabah. Unpublished Doctoral Dissertation, Mahidol University

Diunggah oleh

Hak Cipta:

Format Tersedia

THE ECOLOGY AND BEHAVIOUR OF THE

PROBOSCIS MONKEY (Nasalis larvatus) IN THE

A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE

FACULTY OF GRADUATE STUDIES

THE ECOLOGY AND BEHAVIOUR OF THE

was submitted to the Faculty of Graduate Studies,

May 16, 1994.

Warren Y. Brockelman, Ph.D.

Monthree Chulasamaya, M.D., Ph.D. Pornchai Matangkasombut, Ph.D.

We, the members of the Supervisory Graduate Committee

unanimously approve the thesis entitled

THE ECOLOGY AND BEHAVIOUR OF THE PROBOSCIS MONKEY

We further agree that he has satisfactorily defended his

May 16, 1994.

be awarded the degree of

Doctor of Philosophy in Biology

Warren Y. Brockelman, Ph.D

Visut Baimai, Ph.D

Sompoad Srikosamatara, Ph.D

Sangvorn Kitthawee, Ph.D

Vithoon Viyanant, Ph.D

NAME Ramesh Boonratana

To the memory of “Papa”

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

Nasalis larvatus is a large, sexually dimorphic, monotypic arboreal colobine, endemic

1.2 THE STUDY ANIMAL

1.2.1 GENERAL DESCRIPTION

1.2.2 SPECIFIC DESCRIPTION

1.2.4 STATUS IN SABAH

1.2.5 CURRENT THREATS

1.3 STUDIES OF COLOBINE BEHAVIOUR AND ECOLOGY

1.3.1 STUDIES ON NASALIS LARVATUS

1.4 AIMS OF STUDY

Figure 1.1b Map of Sabah

2.2 MONTHLY SCHEDULE

2.3 FIELD ASSISTANCE

2.9.1 AERIAL SURVEY

2.9.2 RIVER SURVEYS

2.10 FULL DAY FOLLOWS

2.11 DATA ANALYSIS

Figure 2.3 Abai study area at high tide

3.1.1 THE KINABATANGAN RIVER

3.1.2 SOILS AND GEOLOGY

3.1.4 LOGGING HISTORY

3.1.5 HUNTING PRESSURE

3.1.6 POPULATION SIZE OF N. LARVATUS

3.2 SUKAU STUDY AREA

3.2.1 WILD FAUNA

3.2.1.1 DENSITY AND BIOMASS OF N. larvatus

3.2.2.1 BOTANICAL STRUCTURE

3.2.2.2 BOTANICAL COMPOSITION

3.3 ABAI STUDY AREA

3.3.1 WILD FAUNA

3.3.2.1 BOTANICAL STRUCTURE

3.3.2.2 BOTANICAL COMPOSITION

3.4 COMPARISON BETWEEN SUKAU AND ABAI

3.4.1 BOTANICAL STRUCTURE

3.4.2 BOTANICAL COMPOSITION

3.5 FORESTS IN SABAH

3.6.1 ORGANIC NITROGEN AND CRUDE PROTEIN

3.6.2 CONDENSED TANNIN

3.6.3 NEUTRAL DETERGENT FIBRE