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Solving mammalian riddles.

A reconstruction of the Tertiary and Quaternary distribution of

mammals and their palaeoenvironments in island South-East Asia

VOLUME I: Main text

Erik Meijaard

School of Archaeology and Anthropology

The Australian National University

A thesis submitted for the degree of Doctor of Philosophy of the Australian National University

Canberra, Australia

6 January, 2004

Except where cited in the text, this work is the result of research

carried out by the author

……………………………………………………

Erik Meijaard

School of Archaeology and Anthropology

The Australian National University

Canberra, Australia

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Detail of a Ma’a (ceremonial cloth) from Java, early 19th century; from collection Robert Holmgren and Anita Spartus, with permission from the National Gallery of Australia.

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ACKNOWLEDGEMENTS

I dedicate this thesis to Rona and Emily, whom I thank for the joy and love they gave

me during the many hours that I was working on this thesis.

Although my name appears on the cover of this thesis, my research has very much

been a collective endeavour, which would not have been possible without the

dedicated efforts of many more people than I can possibly name in the limited space

available. I have done my best to remember all of those who have supported me in my

work and I sincerely hope that no one feels unjustly left out of these

acknowledgements.

My foremost gratitude goes to my supervisor Prof. Dr. Colin P. Groves, who has been

an invaluable support and inspiration in my research. Colin is an inexhaustible source

of information, whom I have been able to very regularly consult on a wide variety of

issues. Also, Colin has shown considerable interest in not only my PhD research, but

also other research and conservation issues, support that was often welcome and

which kept me enthusiastic about my activities.

I thank my co-supervisors Prof. Dr. John Chappell and Prof. Dr. Peter Bellwood at the

Australian National University, and the external examiners for providing constructive

input into this thesis. I would like to thank Dr. Herman Rijksen for his support in my

scholarship application, and also thank him for his invaluable lessons in critical

analysis of interactions betweens people and their natural environment. I am grateful

to Dr. Peter van Bree for introducing me to the fascinating subject of biogeography

and mammalian evolution.

I thank the Australian National University and the Australian Government for

providing the financial support that enabled me to conduct three-and-a-half years of

research in this great country. In relation to that I thank Prof. Dr. Carel van Schaik and

Prof. Dr. Steph Menken for their support in obtaining the ANU scholarship. I received

further financial support from the Gibbon Foundation, where I would like to thank Dr.

W. Smits, and WWF-Indonesia. The Field Museum in Chicago provided me with a

travel grant which enabled me to do my morphological research in their collection. I

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am grateful to LIPI (the Indonesian Institute for Sciences), and to the Sarawak

Biodiversity Council for providing research permits.

Among the many other people that have supported my research with their ideas and by

sending me advice and their published and unpublished work, special thanks go to

David Taylor, Don Melnick, Ettore Randi, George Amato, Jonathan Kingdon, Manuel

Ruedi, Walter Erleben, and Yahdi Zaim. I especially thank Elsbeth Zwart of the Artis

library of the University of Amsterdam for her support in tracking down and sending

me literature. I also thank Sue Fraser, Kathleen Callen, David McGregor, Paul Johns

and Marolyn Robson for their help at ANU. I am indepted to the following museum

curators for allowing me to do research in their collections: Dr. Charles Leh at the

Kuching Museum, Mrs. Yang Chang Man at the Singapore Museum, Dr. Peter van

Bree and A. Rol at the Amsterdam Museum, Dr. Paula Jenkins at the British Natural

History Museum, Dr. Chris Smeenk at National Museum of Natural History in Leiden,

Dr. Agus Suyanto at the Zoological Museum in Cibinong, and Dr. Lawrence Heaney

at the Field Museum in Chicago. At the Universitas Indonesia, I thank Dr. Noviar

Andayani and Prof. Dr. Indrawatigandjar for their logistical and technical

collaboration. I am grateful to the staff at Medan Zoo, Bandung Zoo, and Pematang

Siantar Zoo for their help in obtaining blood samples from a variety of mammal

species. I thank the US Geological Survey for allowing me to use their maps of

geology, and oil and gas fields of SE Asia.

Very importantly I would like to thank Andi Erman, Vincent Nijman, and Gabriella

Frederiksson for their companionship and their willingness to endure extensive

discussions on SE Asian biogeography and conservation over many glasses of beer

and stronger liquids. I am also thankful to my parents, brother and sister, and to my

friends Marcel, Mark, Leo, and Rudo. And finally, I am most grateful to my fellow

Great Bustards, Hans von Trapp and Macpie Man, for their wise teachings on drivers

and co-drivers, and constant supply of avant-garde musical and poetic expressions.

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TABLE OF CONTENTS

ACKNOWLEDGEMENTS .......................................................................................................................i TABLE OF CONTENTS .........................................................................................................................iv GLOSSARY AND DEFINITIONS .........................................................................................................ix ABSTRACT ..............................................................................................................................................x CHAPTER 1. THE BIOGEOGRAPHIC THEORY OF ISLAND SOUTH-EAST ASIA........................1 CHAPTER 2. OBJECTIVES, HYPOTHESES, AND RESEARCH METHODOLOGY ......................12

2.1 RESEARCH BACKGROUND AND MAMMALIAN RIDDLES ..................................................................13 2.2 FUNDAMENTAL ASSUMPTIONS, GENERAL METHODOLOGY, AND HYPOTHESES..............................21 2.3 DETAILED METHODOLOGY .............................................................................................................26

2.3.1 Geology, Palaeobotany, and Palaeoclimatology ...................................................................26 2.3.2 DNA and the Molecular Clock ...............................................................................................27 2.3.3 Ecological and Morphological Characteristics as Palaeoenvironmental indicators ............30 2.3.4 Species Choice........................................................................................................................30 2.3.5 Testing the Model ...................................................................................................................33 2.3.6 Organizational Details ...........................................................................................................33 2.3.7 Stratigraphy and stage-boundaries ........................................................................................34

CHAPTER 3. THE PALAEOENVIRONMENTAL SCENE BASED ON DATA MINING ................36 3.1 GENERAL GEOLOGY AND TECTONIC FRAMEWORK.........................................................................37 3.2 PALAEOCLIMATE ............................................................................................................................39

General climate patterns of SE Asia ...............................................................................................39 Late Tertiary and Quaternary temperature changes.......................................................................41 Monsoon fluctuations ......................................................................................................................43

3.3 SEA-LEVEL CHANGES .....................................................................................................................45 3.4 PALAEOENVIRONMENTS .................................................................................................................49

General patterns of vegetation changes ..........................................................................................49 Palaeoenvironments of Java............................................................................................................52 Palaeoenvironments of Sumatra......................................................................................................68 Palaeoenvironments of Borneo .......................................................................................................80 Palaeoenvironments of the Malay Peninsula and Malacca Strait ..................................................90 Palaeoenvironments of the South China Sea...................................................................................98 Palaeoenvironments of southern mainland Asia ...........................................................................105 The Palaeogeography of Sulawesi, Nusa Tenggara, and the Philippines.....................................115 Summary of palaeoenvironmental and palaeogeographical reconstructions ...............................119

3.5 PALAEOGEOGRAPHICAL RECONSTRUCTIONS ................................................................................121 Early Miocene (MIO 1) .................................................................................................................121 Middle Miocene (MIO 2)...............................................................................................................122 Middle to early Late Miocene (MIO 3) .........................................................................................123 Late Miocene (MIO 4) ...................................................................................................................124 Early Pliocene lowstand (PLIO 1) ................................................................................................125 Early to Middle Pliocene highstand (PLIO 2)...............................................................................126 Middle Pliocene (PLIO 3) .............................................................................................................127 Late Pliocene (PLIO 4) .................................................................................................................128 Early Pleistocene (PLEI 1)............................................................................................................129 Early–Middle Pleistocene (PLEI 2) ..............................................................................................130 Early–Middle Pleistocene highstand (PLEI 3)..............................................................................131 Middle Pleistocene lowstand (PLEI 4)..........................................................................................132 Late Pleistocene (PLEI 5) .............................................................................................................133

CHAPTER 4: FURTHER DATA MINING ON FAUNAL EVOLUTION IN THE INDO-MALAYAN REGION................................................................................................................................................134

4.1 FOSSIL VERTEBRATES...................................................................................................................135 Fossil vertebrates of Java..............................................................................................................135 Fossil vertebrates of Sumatra, Borneo, Palawan, and the Malay Peninsula................................141 Fossil vertebrates of Thailand and Indochina...............................................................................144

4.2 BACKGROUND INFORMATION ON PHYLOGENY, EVOLUTION AND BIOGEOGRAPHY OF SELECTED SE ASIAN MAMMALS ...............................................................................................................................150

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Insectivora .....................................................................................................................................150 Scandentia .....................................................................................................................................152 Chiroptera .....................................................................................................................................154 Pholidota .......................................................................................................................................155 Primates.........................................................................................................................................155 Rodentia ........................................................................................................................................165 Carnivora ......................................................................................................................................179 Proboscidea...................................................................................................................................193 Perissodactyla ...............................................................................................................................196 Artiodactyla ...................................................................................................................................198 Lagomorphs...................................................................................................................................206

CHAPTER 5: DISCUSSION OF THE NEW MODEL ........................................................................210 Comments on the methodology......................................................................................................211 Phylogenetic patterns and links to palaeogeographies.................................................................213 Late Tertiary and Quaternary stages in the zoogeographic evolution of island SE Asia .............219 Zoogeographic and phylogenetic patterns in the light of the new model......................................242

CHAPTER 6: TESTING AND APPLYING THE MODEL.................................................................246 6.1 MALAYAN SUN BEAR (URSUS (HELARCTOS) MALAYANUS) GENETICS AND MORPHOLOGY ............247 6.2 THE METABOLIC COSTS OF SWIMMING..........................................................................................256 6.3 BANTENG (BOS JAVANICUS) MORPHOLOGY....................................................................................261 6.4 MOUSE-DEER (TRAGULUS SP.) MORPHOLOGY ..............................................................................269 6.5 CERVINE MORPHOLOGY AND GENETICS ........................................................................................272 6.6 SE ASIAN PIGS..............................................................................................................................273 6.7 BORNEO’S PRIMATES: A BIOGEOGRAPHICAL AND EVOLUTIONARY MODEL....................................277 6.8 EVOLUTION OF PRESBYTIS.............................................................................................................278 6.9 LEOPARD (PANTHERA PARDUS) MORPHOLOGY.............................................................................282 6.10 MAMMALIAN ISLAND SPECIES AS PALAEOENVIRONMENTAL INDICATORS...................................283

CHAPTER 7: SOLVING MAMMALIAN RIDDLES .........................................................................284 The Leopard ..................................................................................................................................285 Tiger ..............................................................................................................................................285 The Proboscis Monkey ..................................................................................................................286 Orang-utan ....................................................................................................................................287 Banteng..........................................................................................................................................289 Tragulus javanicus on Java...........................................................................................................289 Elephants .......................................................................................................................................290 Sus barbatus, S. verrucosus, and S. scrofa....................................................................................291

CHAPTER 8: CONCLUSIONS AND IMPLICATIONS OF THE NEW MODEL.............................293 Conservation in Sundaland ...........................................................................................................294 Human dispersal and evolution in Sundaland...............................................................................297

POSTSCRIPT........................................................................................................................................300 REFERENCES......................................................................................................................................302 APPENDICES.......................................................................................................................................348

LIST OF FIGURES

Figure 1.1. Island SE Asia, a highly fragmented part of the world’s land mass. 2 Figure 1.2. Figure 1.2. Map SE Asia, showing the Sundaic and Wallacean Subregions and

country names 3

Figure 2.1. Orang-utan distribution (present and during the Late Pleistocene) 15 Figure 2.2. Organogram of the research inputs and outputs 19 Figure 2.3. Example of data sheet for genetic sampling 32 Figure 3.1. Worldsat Color Shaded Relief Image of SE Asia 37 Figure 3.2a. Isobars and wind direction over Asia in the wet monsoon (November–April) 39 Figure 3.2b. Isobars and wind direction over Asia in the dry monsoon (May–October) 40 Figure 3.3. Original forest cover (before large-scale destruction) of SE Asia 50 Figure 3.4. Main geological features of Java 52 Figure 3.5. Legend to geological maps used in Figs. 3.6–3.11 53 Figure 3.6. Main geological features in the North-West Java Basin 60

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Figure 3.7. Main geological features of north Sumatra 71 Figure 3.8. Map of the South Sumatra Basin 75 Figure 3.9. Lake Toba from space 79 Figure 3.10. Main geological features of Borneo 80 Figure 3.11. Map of the Kapuas River and its hypothesized change from drainage into the

Batang Lupar (top) to its merge with the Melawi (bottom). 85

Figure 3.12. Main geological features of the Malay Peninsula 91 Figure 3.13. Main geological features of Indochina 105 Figure 3.14. Palaeoenvironmental reconstruction for the Early Miocene 121 Figure 3.15. Palaeoenvironmental map for the early Middle Miocene` 122 Figure 3.16. Palaeoenvironmental reconstruction for the late Middle to early Late Miocene 123 Figure 3.17. Palaeoenvironmental reconstruction for the Late Miocene 124 Figure 3.18. Palaeoenvironmental reconstruction for the Early Pliocene lowstand 125 Figure 3.19. Palaeoenvironmental reconstruction for the Early–Middle Pliocene highstand 126 Figure 3.20. Palaeoenvironmental reconstruction for the Middle Pliocene 127 Figure 3.21. Palaeoenvironmental reconstruction for the Late Pliocene 128 Figure 3.22. Palaeoenvironmental reconstruction for the Early Pleistocene 129 Figure 3.23. Palaeoenvironmental reconstruction for the Early–Middle Pleistocene 130 Figure 3.24. Palaeoenvironmental reconstruction for the Early–Middle Pleistocene highstand 131 Figure 3.25. Palaeoenvironmental reconstruction for the Middle Pleistocene lowstand 132 Figure 3.26. Palaeoenvironmental reconstruction for the Late Pleistocene lowstand 133 Figure 4.1. Phylogeny of the Hylomys group 150 Figure 4.2. Phylogenetic relationships (consensus tree) for a selected number of Crocidura

species 151

Figure 4.3. Immunological divergence tree of the Tupaiidae 153 Figure 4.4. Phylogenetic relationships among Cynopterus fruitbats in the Indonesian

archipelago 154

Figure 4.5. Phylogenetic relationships among gibbons 161 Figure 4.6. Phylogenetic relationships among Asian hominids 164 Figure 4.7. A hypothetical phylogeny of the genus Hystrix 166 Figure 4.8. Strict consensus tree of Asian murine genera 168 Figure 4.9. Phylogenetic relationships and divergence time estimates for SE Asian Muridae 170 Figure 4.10. Squirrel phylogeny 175 Figure 4.11. Strict concensus tree of flying squirrel phylogeny with some of the divergence time

estimates 177

Figure 4.12. The composite tree for the higher groups of carnivores 179 Figure 4.13. Phylogenetic relationships among Asian canids 180 Figure 4.14. The phylogenetic relationships between bears species 181 Figure 4.15. Phylogenetic relationships among living cat species 183 Figure 4.16. Tiger evolution 186 Figure 4.17. Phylogenetic relationships among viverrids 192 Figure 4.18. Recontructed heads of some of the elaphantids mentioned in the text 195 Figure 4.19. Hypothetical relationships among some of the living and fossil Tapiroidea 197 Figure 4.20. Consensus tree of the phylogenetic relathionships within the Muntiacinae 202 Figure 4.21. Phylogenetic relationship among the Bovinae 204 Figure 4.22. Generalized phylogeny for Old World leporid genera based on P3 morphology 207 Figure 5.1. Incomplete lineage sorting as a problem in molecular-based phylogenies, especially

where sample sizes are small 211

Figure 5.2. The Middle–Late Miocene palaeogeography and the dispersal of mainland Asian faunal elements into Sundaland and Sulawesi, and possibly vice versa.

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Figure 5.3. The palaeogeography during the Early–Middle Pliocene highstand and the possible effects on mammalian evolution.

222

Figure 5.4. The land area that would remain of the present-day topography if sea levels were 100 m higher than today

223

Figure 5.5. West Kalimantan Province, showing the location of heath forest in relation to altitude

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Figure 5.6. The palaeogeography during the Late Pliocene lowstand and the possible effects on mammalian evolution

230

Figure 5.7. The palaeogeography during the Early–Middle Pleistocene and the possible effects 231

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on mammalian evolution Figure 5.8. An alternative scenario for the land bridge between Malaya and Java 234 Figure 5.9. The palaeogeography during the Middle Pleistocene and the possible effects on

mammalian evolution 235

Figure 5.10. The palaeogeography during the late Middle Pleistocene and the possible effects on mammalian evolution

236

Figure 5.11. The palaeogeography during the Late Pleistocene glacial and the possible effects on mammalian evolution

238

Figure 5.12. The locations of hypothetical refugia of evergreen tropical forest during the Last Glacial Maximum

239

Figure 5.13. A recurrent phylogenetic pattern in SE Asia 244 Figure 6.1. A PCA of adult Sun Bear specimens 249 Figure 6.2. A discriminant analysis of adult, female Sun Bear skulls, and the corresponding

correlation matrix 250

Figure 6.3. Means, standard deviations, range, and outliers of the greatest skull length for 8 subregions of the Sun Bear distribution range

251

Figure 6.4. Means, standard deviations, range, and outliers of the ratio between the length of the upper tooth row and the condylo-basal length of adult Bornean and Sumatra Sun Bear specimens

252

Figure 6.5. Graph of the condylo-basal length vs. length of upper tooth row for adult Sun Bear specimens

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Figure 6.6. Phylogenetic neighbourjoining tree based on mtDNA sequence differences in Sun Bear samples

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Figure 6.7. Log body weights frequencies of mammalian genera from Sulawesi, Borneo, Thailand, and Java

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Figure 6.8. Principal component analysis for banteng skulls from Borneo (open circles with cross), Java (open squares), and mainland Asia (closed circles)

262

Figure 6.9. Bi-variate diagram of Banteng horn span (SPAN) vs. horn length (BASE) 263 Figure 6.10. Cave drawings, presumably of banteng, from Ilas Kenceng on the Mangkalihat

Peninsula, East Kalimantan 266

Figure 8.1. The number of mammal species (excluding bats) on small islands in SE Asia. 296

LIST OF TABLES

Table 2.1. Boundaries between stages as used in this research 35 Table 3.1. Global and regional sea-level estimates from literature 45-44 Table 3.2. Nusa Tenggara islands and the time when they became last emergent 117 Table 4.1. Faunal list of Java’s fossil sites 139-141 Table 4.2. Fossil mammals of Indochina and Thailand 144-146 Table 4.3. Fossil murids and sciurids from Thailand 148-149 Table 4.4. Estimates of branching times within the family Cercopithecidae 158 Table 4.5. Comparison of some divergence dates (in Mya) within the Muridae, calibrated

against two proposed times for the separation of the Mus and Rattus lineages 168

Table 4.6. SE Asian mongoose species 193 Table 5.1a. The main divergence events and palaeoenvironmental changes from the Middle

Miocene to Middle Pliocene 213

Table 5.1b. The main divergence events and palaeoenvironmental changes during the Pliocene 214 Table 5.1c. The main divergence events and palaeoenvironmental changes between the Late

Pliocene and Middle Pleistocene 215

Table 5.1d. The main divergence events and palaeoenvironmental changes between the Middle and Late Pleistocene

216

Table 6.1. The means and standard deviations (SD) of each of the measured variables for Sun Bears from Borneo, Sumatra, and Malaya/mainland Asia

250

Table 6.2. Indigenous mammalian genera of Sulawesi, their body weight and ecology 257 Table 6.3. Correlation matrix between the principal components in Fig. 6.8 and the variables 263 Table 8.1. Counts of size classes of contiguous Bornean Orangutan habitat areas; a comparison

between the early 1990s and 2002 295

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GLOSSARY AND DEFINITIONS

ANOVA = analysis of variance (a statistical technique)

centrifugal evolution = a recurring pattern in the distribution of taxa: a more evolved

(derived) taxon is often central, surrounded or flanked by more primitive relatives

Cytochrome b gene = part of the mitochondrial DNA

Discriminant Analysis = A statistical technique for situations where one wants to build

a predictive model of group membership based on observed characteristics of each

case. The procedure generates a set of discriminant functions based on linear

combinations of the predictor variables that provide the best discrimination

between the groups.

Holocene = 11 Kya to present

Kya = thousand years ago

Kyr = thousand years

Late Pleistocene = period between 128 and 11 Kya (Jablonksi & Whitfort 1999)

LGM = Last Glacial Maximum

m = metre

monophyletic = groups derived from an exclusive common ancestor

mtDNA = mitochondrial DNA

Mya = million years ago

Myr = million years

neretic zone = that part of the ocean which includes both the estuarine zone and the

continental shelf; thus neretic deposits are of shallow-water origin.

paraphyletic = groups that have evolved from and include a single ancestral species,

but which do not contain all the descendants of that ancestor

PDL = present day level

Principal Components Analysis = A statistical method used in data reduction to

identify a small number of factors that explain most of the variance observed in a

much larger number of variables

RNA = ribonucleic acid, present in all cells

unconformity = a geological tern referring to a hiatus or break in a sequence

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ABSTRACT

Since the mid 19th century, the biogeography of island South-East Asia has been the

subject of much study. Early researchers explained many of the species distribution

patterns by the rise and fall of sea levels and land. This and the work of other

researchers culminated in a theory that emphasized the role of Pleistocene sea level

low stands in species evolution. With the advent of newly developed molecular

techniques, however, it became clear that many species divergence events had taken

place before the Pleistocene and a biogeographical theory focusing on Pleistocene sea

level changes was inadequate. In this research, I have developed a new biogeographic

model that explains present-day distribution patterns and evolutionary relationships

between species. I use this new model to explain 10 ‘mammalian riddles’, i.e.

evolutionary or distribution patterns in selected mammal species groups that could not

be explained with the existing theories. I developed the new model by analyzing the

geological literature for this region, and by mapping palaeogeographical and

palaeoenvironmental changes for the last 20 million years. In addition I compiled

information on the palaeontological record for the region and on divergence times

between taxa using a molecular clock assumption. These phylogenetic data were

compared with the palaeomaps to assess whether particular divergence events could

be correlated with certain palaeogeographical or palaeoenvironmental changes. The

combination of these two information sources has resulted in a much-improved

understanding of mammalian evolution in island SE Asia. Using this model it is now

possible to relate important palaeoenvironmental events, such as the Late Miocene

cooling, an Early–Middle Pliocene highstand, or the emergence and submergence of a

land bridge between the Malay Peninsula and Java to evolutionary changes in species.

I test the accuracy of the new model by analysing the relationships within several

mammal groups using craniometric and molecular analysis. The observed

relationships and deduced timing of divergence between taxa could in many cases be

explained by the model, which indicates that it is relatively accurate. In addition, with

the new model I have been able to find solutions to most mammalian riddles, although

these results require further testing. Overall, I therefore believe I have made a

significant contribution to the biogeographical understanding of island SE Asia.