Bird Community Structure and Diversity in Peninsular Malaysia

BIRD COMMUNITY STRUCTURE AND

DIVERSITY IN PENINSULAR MALAYSIA

NUR MUNIRA BINTI AZMAN

UNIVERSITI SAINS MALAYSIA

2017

BIRD COMMUNITY STRUCTURE AND

DIVERSITY IN PENINSULAR MALAYSIA

NUR MUNIRA BINTI AZMAN

Thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy

July 2017 DEDICATION

My humble effort I dedicate

Loving parents and grandparents, whose

Utmost efforts and prayers are always with me.

Respected teachers, whose

Kind guidance and encouragement helped me to reach at this stage.

My husband and little son, whose

Became my backbone throughout this journey.

ACKNOWLEDGEMENT

Alhamdulillah, all praises to Allah s.w.t, for giving me the opportunity and strength to complete my fieldwork, analyses and thesis writing. I would like to express my deepest gratitude to my supportive supervisor, Professor Shahrul Anuar Mohd Sah and my dedicated co-supervisor, Dr. Amirrudin Ahmad who have provided guidance and ideas from commencement of this project. Their assistance and thoughts are much appreciated. Thank you to Dr. Nurul Salmi Abdul Latip for her continuous motivation in completion of this project.

I would like to thank the Institute for Post-graduate Studies (IPS), Universiti Sains Malaysia, and the transportation provided by the School of Biological Sciences, Universiti Sains Malaysia (USM). I acknowledge the Ministry of Higher Education (KPT) for awarding MyBrain15 (MyPhd) scholarship to me.

Sincere appreciation to my passionate teachers; Mr. Mohd Abdul Muin Md. Akil and Mr. Mohd Nasir Azizan who successfully trained me in bird identification. I am also indebted to my field assistants; Mr. Yusof Omar, Mr. Nordin Ahmad, Mr. Hafizul, Mr. Abdullah, and Mr. Muthu who made all field data collection possible. My deepest gratitude to my fellow friends, Dr. Nur Juliani Shafie, Nur Adibah Ishadi, Bidarulmunir Ahmad Anas, Norafifah Supardy, Nor Amira Abdul Rahman, Mahfuzah Othman, and Aini Hasanah for their ideas, time and advice.

Thank you to my husband, Mr. Mohd Nasir Azizan, my son Ammar Mifhal Mohd Nasir, my family members; Mak Kelly, Nenek, Mak Yum, Ayah, Wa and Na for their continuous motivation and inspiration in completion of my study. To my late father, Azman Hashim and my late grandmother, Fatimah Hj Ali, thank you for their support and prayers.

And last but not least, I would like to thank everyone who has helped me either directly or indirectly during my field work and thesis writing, whom I cannot mention one by one.

TABLE OF CONTENTS

ACKNOWLEDGEMENT ii

TABLE OF CONTENTS iii

LIST OF TABLES viii

LIST OF FIGURES x

LIST OF ABBREVIATIONS xiv

LIST OF SYMBOLS xvi

ABSTRAK xvii

ABSTRACT xix

CHAPTER 1: INTRODUCTION 1

1.1 Bird diversity in the tropics 1

1.2 Bird diversity in natural habitats of Peninsular Malaysia 3

1.3 The importance of birds 6

1.4 Contribution of rice fields on bird diversity in Peninsular Malaysia 9

1.5 Rationale 10

1.6 Thesis outline 13

1.7 Objectives 15

CHAPTER 2: LITERATURE REVIEW 16

2.1 Birds in natural habitats 16

2.2 Estimating bird species richness 19

2.3 Beta diversity analysis 25

2.4 Patterns of rarity among birds 30

2.4.1 Rarity in birds 30

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2.4.2 Functional diversity measure 32

2.5 Birds in rice fields 33

CHAPTER 3: GENERAL MATERIALS AND METHODS 36

3.1 Review of method used 36

3.2 Study areas 39

3.3 Sample collection 41

3.3.1 Point count method 41

3.3.2 Capture technique 42

CHAPTER 4: SPECIES RICHNESS AND COMMUNITY 45 STRUCTURE OF BIRDS IN NATURAL HABITATS OF PENINSULAR MALAYSIA

4.1 Introduction 45

4.2 Materials and methods 47

4.2.1 Data analysis 47

4.2.1(a) Species accumulation curve 47

4.2.1(b) Bird status 48

4.3 Results 51

4.3.1 Species accumulation curve 51

4.3.2 Bird species occurrence across study sites 53

4.4 Discussion 67

4.4.1 Species accumulation curve 67

4.4.2 Bird species occurrence across study sites 68

4.5 Conclusion 71

CHAPTER 5: BIRD SPECIES RICHNESS IN NATURAL 73 HABITATS OF PENINSULAR MALAYSIA

5.1 Introduction 73

5.2 Materials and methods 76

5.2.1 Data analysis 76

5.2.1(a) Species richness estimator 76

5.2.1(b) Performance evaluation of estimators 77

5.2.1(c) Inventory completeness index 80

5.2.1(d) Adjusted estimate range 80

5.3 Results 81

5.3.1 Species accumulation curve and species estimations 81

5.3.2 Performance evaluation of estimators 85

5.4 Discussion 88

5.5 Conclusion 94

CHAPTER 6: BETA DIVERSITY OF BIRD COMMUNITIES IN 96 NATURAL HABITATS, PENINSULAR MALAYSIA

6.1 Introduction 96

6.2 Materials and methods 97

6.2.1 Study areas 98

6.2.2 Data analysis 100

6.3 Results 102

6.3.1 Beta diversity: Variation in community structure 102

6.3.2 Avifauna dissimilarity: Turnover in species assemblages 105

6.3.3 Taxonomic similarity between regions 108

6.4 Discussion 109

6.4.1 Beta diversity: Variation in community structure 110

6.4.2 Avifauna similarity: Turnover in species assemblages 115

6.4.3 Taxonomic similarity within region 117

6.5 Conclusion 119

CHAPTER 7: PATTERNS OF RARITY AMONG BIRDS IN 121 NATURAL HABITATS OF PENINSULAR MALAYSIA

7.1 Introduction 121

7.1.1 Forms of rarity 121

7.1.2 Species classification into forms of rarity 123

7.1.3 Functional diversity for rare species 125

7.2 Materials and methods 125

7.2.1 Study areas 125

7.2.2 Data analysis 126

7.2.2(a) Forms of rarity 126

7.2.2(b) Functional diversity 127

7.3 Results 130

7.3.1 Patterns of rarity 130

7.3.2 Functional diversity of rare species 132

7.4 Discussion 136

7.4.1 Patterns of species rarity 136

7.4.2 Functional diversity of rare species 141

7.5 Conclusion 145

CHAPTER 8: THE CONTRIBUTION OF RICE FIELDS TO THE 147 BIRD DIVERSITY IN PENINSULAR MALAYSIA

8.1 Introduction 147

8.2 Materials and methods 150

8.2.1 Study areas 151

8.2.2 Data analysis 156

8.2.2(a) Species composition 156

8.2.2(b) Species community structure 156

8.3 Results 158

8.3.1 Species accumulation curve and species composition across 158 rice fields 8.3.2 Bird status in rice fields 164

8.3.3 Comparison of species community structure in natural 166 habitats and rice fields 8.4 Discussion 174

8.4.1 Birds in rice fields 174

8.4.2 Contribution of rice fields to bird diversity 176

8.5 Conclusion 180

CHAPTER 9: GENERAL DISCUSSION 182

CHAPTER 10: GENERAL CONCLUSION 187

10.1 Conclusion 187

10.2 Future research 189

REFERENCES 191

APPENDICES

LIST OF PUBLICATIONS AND PROCEEDINGS

vii

LIST OF TABLES

Page

Table 2.1 Various ecological studies that used species richness estimator 22 over the last two decades.

Table 3.1 List of differences between point count and mist-netting 38 methods (Herzoq et al., 2002; Derlindati & Caziani, 2005; Barlow et al., 2007a).

Table 4.1 List of birds in presence/absence data for 53 sites of natural 54 habitats in Peninsular Malaysia.

Table 4.2 List of common bird species with more than 25 occurrences in 65 natural habitats of Peninsular Malaysia.

Table 5.1 Seven types of estimators that were used in this study 75 (Colwell & Coddington, 1994; Chazdon 1998; Colwell 2015).

Table 5.2 Summary of species richness estimations for natural habitat in 82 Peninsular Malaysia. Hundred randomisations without replacement were chose by using EstimateS. The upper abundance limit for rare species was set at 10.

Table 5.3 Performance of species observed and seven estimators for bird 86 species in natural habitat of Peninsular Malaysia based on bias and precision measures. The boldly printed estimators were the top three least biased and most precise estimators. A bias value near to zero indicates a least bias estimated while a value close to zero indicates high precision of the estimator. MMM was recorded as the least bias and most precise estimator.

Table 6.1 List of sampling sites based on seven regions of Peninsular 99 Malaysia.

Table 6.2 Beta diversity values (1-Jaccard’s similarity, upper diagonal) 104 and distance (lower diagonal) between 53 study sites.

Table 6.3 Statistical summary for taxonomic similarity ( s ) and 109 Whittaker’s β-diversity applied to birds of the order Passeriformes (presence/absence) recorded from natural habitats within seven regions of Peninsular Malaysia.

Table 7.1 Types of rarity (Longino et al., 2002). 122

Table 7.2 The seven forms of rarity proposed by Rabinowitz (1981) 124 with modifications according Gaston (1994).

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Table 7.3 Attributes of life history traits used for bird species (modified 128 from Barbaro & Halder, 2008).

Table 7.4 Forms of rarity of birds in natural habitats in Peninsular 131 Malaysia based on categories developed by Rabinowitz et al. (1986). Rarity was assessed based on occurrence data of bird species since 1993-2014. The cells are comparable to classification as suggested by Rabinowitz et al. (1986) where ‘YES’ = ≥25 sites, ‘yES’ = 20-24 sites, ‘YEs’ = 15-19 sites, ‘yEs’ = 10-14 sites, ‘YeS’ = 5-9 sites, ‘yeS’ = 3-4 sites, ‘Yes’ = 2 sites and ‘yes’ = 1 site.

Table 8.1 Study areas in rice fields of Peninsular Malaysia. The table 153 explained the details information on the study areas according state.

Table 8.2 List of waterbird species recorded in rice fields of Peninsular 162 Malaysia.

Table 8.3 List of least concern birds that have decreasing population 165 trend in rice fields of Peninsular Malaysia.

Table 8.4 List of study areas fell outside the 95% confidence funnel of 173 average taxonomic distinctness (∆+).

LIST OF FIGURES

Page

Figure 1.1 Total number of bird species recorded and field 5 observations according states in Peninsular Malaysia (eBird, 2016).

Figure 1.2 Total numbers of species recorded in 15 birding hotspots in 5 Peninsular Malaysia. Seven hundred and twenty six bird species have been recorded throughout the country to date (eBird, 2016).

Figure 2.1 Schematic diagrams illustrate the two concepts of beta 27 diversity (a) directional turnover in community structure, and (b) variation of community structure within a given area (adapted from Anderson et al., 2011).

Figure 3.1 Location of study areas within Peninsular Malaysia. Red 40 bullets indicate samples from primary data and yellow bullets samples from secondary sources.

Figure 3.2 Methodology of bird census conducted in the study areas. 44

Figure 4.1 Structure of bird categories following IUCN red list 50 categories and criteria (IUCN, 2001). According to IUCN (2012), birtds listed as critically endangered quality for endangered and vulnerable, and all birds listed as endangered qualify for vulnerable. These three categories are called as ‘threatened’.

Figure 4.2 Species accumulation and rarefaction curve for bird species 52 richness and their unique and duplicate occurrence from 53 natural habitats of Peninsular Malaysia. The jagged line is the species accumulation curve for one of many possible orderings of 53 sites yielding a total 438 bird species richness, from primary and secondary data of natural habitats in Peninsular Malaysia. The smooth solid line is the sample-based rarefaction curve for the same data set, showing the mean number of species for all possible combinations of 1,2,…,53 actual samples from the data set -this curves plots the species expected of the (sample- based) species accumulation curve. The black hole indicates the total richness (438) for all samples pooled. Red and green bullets indicate the number of unique and duplicate occurrence of bird species in every sample from the data.

Figure 4.3 Number of least concern (LC) bird according to population 64 trends and residential status.

Figure 4.4 Number of unique and duplicate species according to 66 residential status; migrant (M), resident (R), resident and migrant (R&M), and vagrant (V).

Figure 4.5 Number of unique and duplicate species according to 66 IUCN red list; least concern (LC), near-threatened (NT), vulnerable (VU), and unknown (UN).

Figure 5.1 Species observe (Sobs) within 5% of asymptote were 78 excluded from the evaluation. The rest of the points were divided into four parts of equal sampling effort. Only second and third parts were evaluated. See above paragraph for details. Figure was adapted from Walther & Morand (1998) that used an example from parasite species richness.

Figure 5.2 Plots comparing the performance of seven estimators of 84 species richness with the observed species accumulation curve, using data from all 53 samples of bird species from the natural habitats of Peninsular Malaysia. At the low number of samples, the Michaelis-Menten Runs appear to estimate high number of species, (hence removed from the graph in order to improve the clarity) and the number predicted is not stable.

Figure 5.3 Observed and estimated number of bird species in natural 87 habitats of Peninsular Malaysia from the most three least bias and precise estimators

Figure 6.1 Relationship between beta diversity values (1-Jaccard’s 103 Similarity) and site distance based on bird presence/absence data with respective linear regression lines. Distance generally has negative influence on beta diversity of birds

Figure 6.2 Dendogram derived from Ward’s method for sites of 106 natural habitats in Peninsular Malaysia.

Figure 7.1 Distribution of rare species with respect to functional trait 133 variables, identified by principle component analyses (PCA) for component 1 and component 2. Several traits were removed for clarity of the figure. The rare species were represented by S1-S46.

Figure 8.1 Total areas of rice fields according to states in Peninsular 148 Malaysia for year 2013 (DOS, 2013).

Figure 8.2 Map of Peninsular Malaysia; the study areas of rice fields 152 are shown with the grey box. Most of the study areas are located in the granary areas (except ML, JH, and TR) namely MADA, IADA Penang, IADA KSM, IADA Seberang Perak, IADA BLS, KADA, and IADA KETARA. Granary areas refer to major irrigation schemes (areas greater than 4,000 hectares) and recognised as the main paddy producing areas. KD: Kedah, PL: Perlis, PP: Penang, PK: Perak, SL:Selangor, KL: Kelantan, TR: Terengganu, ML: Melaka, and JH: Johor Bharu. Note: Bullets for Terengganu and Johor not all appear because they are close to each other.

Figure 8.3 Species accumulation and rarefaction curve for bird species 159 richness and their unique and duplicate occurrence from 83 rice fields of Peninsular Malaysia. The jagged line is the species accumulation curve for one of many possible orderings of 83 sites yielding a total of 129 bird species in rice field habitats. The smooth line is the sample-based rarefaction curve for the same data set, showing the mean number of species for all possible combinations of 1,2,…,83 actual samples from the data set- this curve plots the species expected of the (sample-based) species accumulation curve. The black hole indicates the total richness for all samples pooled. Red square and green triangles indicate the number of unique and duplicate occurrence of bird species in every sample from the data.

Figure 8.4 Number of species overlap among the two habitat types 167 illustrated by Venn diagram. Rice fields contributed 55 species richness to the total checklist of natural habitats and rice fields (493).

Figure 8.5 Tree diagram resulted from average linkage clustering 168 using the unweighted pair-group method (UPMGA) on bird communities at natural habitats and rice fields of Peninsular Malaysia. Only one study area of rice fields (PK6) were group within natural habitats.

Figure 8.6 Three-dimensional nMDS configuration (Jaccard similarity 169 measure) with stress value = 0.12 showed that similar habitat type of study areas (e.g. green triangles) were grouped together indicating that it supports similar species as opposed to other habitat. ML2 and F9 are considered as outliers.

Figure 8.7 Values of the average taxonomic distinctness (∆+) for the 171 bird communities of natural habitats and rice fields of Peninsular Malaysia, plotted against the number of species

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on the 95% confidence funnel. The dotted thin line represents the ‘expected’ value of ∆+ derived from a list of the 493 species recorded in this study.

Figure 8.8 Values of variation in taxonomic distinctness (ʌ+) for the 172 bird communities of natural habitats and rice fields of Peninsular Malaysia, plotted against the number of species on the 95% confidence funnel. The dotted thin line represents the ‘expected’ value of ʌ+ derived from a list of the 493 species recorded in this study.

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LIST OF ABBREVIATIONS

ACE Abundance-based coverage estimator

AU Approximately unbiased

AvTD average taxonomic distinctness

BP Bootstrap probability

BPO Borneo Post Online

Chao1 Abundance-based estimator Chao1

Chao2 Incidence-based estimator Chao2

CR Critically endangered

DOS Department of Statistics, Malaysia

IADA Integrated Agriculture Development Area

IADA BLS Barat Laut Selangor Integrated Agriculture Development Area

IADA KETARA North Terengganu Integrated Agriculture Development

IADA KSM Kerian Integrated Agriculture Development Area

ICE Incidence-based coverage estimator

IUCN International Union for Conservation of Nature

Jack1 Jackknife1

Jack2 Jackknife2

KADA Kemubu Agricultural Development Authority

LC Least Concern

MADA Muda Agricultural Development Authority

MMMean Michaelis-Menten model based estimator

MMMRun Michalis-Menten runs

NE Northeastern

xiv nMDS Nonmetric multidimensional scaling

NT Near-threatened

NW Northwestern

PAST Paleontological Statistics

SW Southwestern

UPMGA Unweighted Pair-Group Mean Arithmetic

VarTD Variation in Taxonomic Distinctness

VU Vulnerable

LIST OF SYMBOLS

∆+ Average taxonomic distinctness

∆s Taxonomic similarity

ʌ+ Variation in taxonomic distinctness

Α Alpha diversity

Β Beta diversity

βW Whittaker’s β-diversity

γ Gamma diversity

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STUKTUR KOMUNITI DAN KEPELBAGAIAN BURUNG DI

SEMENANJUNG MALAYSIA

ABSTRAK

Semenanjung Malaysia mempunyai kepelbagaian flora dan fauna yang tinggi.

Kebanyakannya masih belum didokumentasikan. Avifauna merupakan satu kumpulan penting yang kurang mendapat perhatian, secara ekologi di negara ini.

Pelbagai pendekatan pengukuran kepelbagaian ditunjukkan di dalam tesis ini bertujuan menilai kepelbagaian burung di habitat semulajadi dan bukan semulajadi.

Objektif kajian ini adalah untuk menentukan komposisi dan kepelbagaian terkini spesies burung, menganalisa β-diversiti burung, menyiasat corak kelangkaan dikalangan burung di habitat semulajadi, dan mengkaji sumbangan sawah padi terhadap kepelbagaian burung di Semenanjung Malaysia dengan menggunakan pelbagai kaedah pengukuran kepelbagaian. Data ada/tiada diperoleh daripada sumber primer (2002-2013) dan sekunder (1992-2015) yang telah direkodkan dari 53 kawasan habitat semulajadi. Data primer dan sekunder burung juga telah dikumpul sejak tahun 2013-2014 daripada 83 kawasan sawah padi di sembilan buah negeri,

Semenanjung Malaysia. Kaedah point count dan pemasangan jaring kabut (mist- netting) telah digunakan untuk bancian burung. Keluk pengumpulan spesies telah diplot untuk menerangkan komposisi spesies burung. Tujuh penganggar spesies telah diuji untuk menganggarkan bilangan spesies burung dan menilai prestasi penganggar. β-diversiti telah dihuraikan melalui pengiraan variasi, pulangan perolehan (turnover), dan kesamaan taksonomi. Corak kelangkaan dikalangan burung hutan telah ditentukan dengan menggunakan tujuh bentuk kelangkaan

Rabinowitz. Manakala sumbangan sawah padi terhadap jumlah keseluruhan bilangan spesies burung di Semenanjung Malaysia telah dianalisa menggunakan pengukuran

xvii keberbezaan taksonomik (taxonomic distinctness measures). Empat ratus tiga puluh lapan spesies burung telah direkodkan dari 53 kawasan tapak kajian. MMMeans telah menganggarkan 482 spesies burung untuk habitat semulajadi, Semenanjung

Malaysia. Analisis β-diversiti menunjukkan kepelbagaian burung adalah berkadar negatif dengan jarak tetapi berkadar positif dengan ketinggian manakala keberbezaan taksonomik mencadangkan dengan berpandukan kepada kehadiran burung daripada order Passeriformes, bahagian barat menunjukkan kepelbagaian beta yang tinggi dengan skor 0.797. Dari segi kelangkaan pula, 46 burung residen telah dikategorikan sebagai spesies burung yang paling langka dengan saiz populasi yang jarang, habitat spesifikasi yang terhad, dan julat taburan yang terhad. Keputusan daripada analisis functional diversity menunjukkan kelangkaan dalam burung mudah berlaku apabila spesies tersebut dikategorikan sebagai ‘isospecies’, spesies bawah kanopi, pemakan buah, dan residen biasa di habitat semulajadi tanah tinggi. Di lanskap pertanian tradisional kita, sawah padi mempunyai sumbangan yang signifikan terhadap kepelbagaian burung di Semenanjung Malaysia kerana terdapat banyak burung air di kawasan ini. Keputusan yang didapati akan meningkatkan pemahaman terhadap stuktur komuniti burung di Semenanjung Malaysia dan membantu dalam merangka amalan pengurusan yang baik untuk memulihara kepelbagaian biologi habitat. Kajian ini juga telah berjaya mengaplikasikan pelbagai pendekatan pengukuran kepelbagaian spesies dan mencadangkan cara-cara dalam mengaplikasikan pengukuran-pengukuran ini untuk menilai kumpulan fauna yang mempunyai kepelbagaian yang tinggi. Oleh itu, hasil kajian mestilah dirujuk kerana kajian ini telah menilai secara terperinci pelbagai cara mengukur kepelbagaian dan komuniti struktur burung di Semenanjung Malaysia.

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BIRD COMMUNITY STRUCTURE AND DIVERSITY IN PENINSULAR

MALAYSIA

ABSTRACT

Peninsular Malaysia has rich and diverse flora and fauna. Much of these have yet to be documented. The avifauna is an important group that has received little attention, ecologically in this country. Different approaches of diversity measurements are presented in this thesis in order to evaluate the bird diversity in natural and man-made habitats. The objectives of this study are to determine the current bird species composition and diversity, to analyse β-diversity of birds, to investigate patterns of rarity among birds in natural habitats, and to study the contribution of rice fields to the bird diversity in Peninsular Malaysia by using multiple diversity measurements. The presence/absence data were obtained from primary (2002-2013) and secondary sources (1992-2015) recorded from 53 sites of natural habitats. Primary and secondary of bird data were also collected since year

2013-2014 from 83 sites of rice fields in nine states, Peninsular Malaysia. Point counts and mist-netting methods were used for bird census. Species accumulation curve was plotted to describe the species composition of birds. Seven species estimators were performed to estimate the current bird species richness and evaluate estimators’ performance. The β-diversity was described through calculation of variation, turnover, and taxonomic similarity. The pattern of rarity among forest birds were determined by using Rabinowitz’s seven forms of rarity. Meanwhile the contribution of rice fields on the total bird species in Peninsular Malaysia was analysed by using taxonomic distinctness measures. Four hundred and thirty eight bird species were recorded from 53 sites of study areas. The MMMeans estimated

482 bird species for natural habitats of Peninsular Malaysia. The β-diversity analysis

xix showed that bird diversity was negatively correlated with distance but positively influenced by elevation, whilst taxonomic similarity suggests that based on the presence of birds from order Passeriformes, the west region displayed the greatest beta diversity with score of 0.797. In terms of rarity, 46 resident birds were categorised as the rarest bird species which has a scarce population size, restricted habitat specificity, and narrow distribution range. Result from the functional diversity analysis showed that rarity in birds easily occurred when the species are categorised as ‘isospecies’, understorey species, frugivores, and common resident of high altitude natural habitats. In our traditional landscape, rice fields have a significant contribution to the diversity of birds in Peninsular Malaysia, as many waterbird species were found here. The results obtained will enhance the understanding of bird community structure in Peninsular Malaysia and assist in developing good management practice for conserving such biodiverse habitats. This study also successfully applied different approaches of species diversity measurements and had suggested ways in applying these measurements to examine the high diversity group of fauna. Hence, the outcomes should be referred as the current study has thoroughly evaluated various ways of measuring bird community structure and diversity in Peninsular Malaysia.

CHAPTER 1

INTRODUCTION

1.1 Bird diversity in the tropics

Bird is one of the largest vertebrate group that have adapted to every unique environment although some species are found only in a very restricted areas while others have a wide range of habitat around the globe (Gaston, 2000). Birds are found almost everywhere on earth, and the exact number of total species is unknown since new species are still being discovered (Sætre et al., 2001; Robson, 2008; Alström et al., 2010). To date, there are 10,814 known species of birds represented by 240 families and 2292 genus in the world, 17 years after reaching 9,000 species in 1999

(May, 1992; Gill & Donsker, 2016). According to the International Ornithologists’

Union, approximately 20,500 subspecies of birds have been discovered (Gill &

Donsker, 2016).

Nowadays, bird classification is not dependent on the overall structure, plumage characteristics, and habits since these are strongly influenced by sexual selection, which can lead to misidentification; however with more advanced technology of DNA analysis many new bird species are being discovered (Kress et al., 2015). As an example, results from mitochondrial DNA sequence analysis showed that a sympatric population of Pied Flycatcher, Ficedula hypoleuca and

Collared Flycatcher, Ficedula albicollis contains another black and white new species of Ficedula known as the Atlas Flycatcher, Ficedula speculigera (Sætre et

al., 2001). Mahood et al. (2013) also discovered a new species of lowland tailorbird from the Mekong floodplain of Cambodia using genetic analysis to support evidence of study, instead of using the straightforward morphological comparisons.

Accordingly, more new bird species could be discovered.

Tropical countries that have broad range of habitats such as lowland forest, montane forest, hill dipterocarp forest, mangrove forest, peat swamp forest, gardens, and orchards certainly supports a variety of bird species (Hughes et al., 2002; Jetz &

Rahbek, 2002; Nagelkerken et al., 2008; Peh et al., 2011). The chances of getting new species with identification aid from DNA analysis in the tropics has been increasing lately. As an example, with the utilisation of DNA analysis, scientists have discovered a new species known as the Limestone Leaf Warbler, Phylloscopus calciatilis that is closely related with Sulphur-breasted Warbler, P. ricketti and

Yellow-vented Warbler, P. cantator (Alström et al., 2010). This species that was found in the central and northern Vietnam, and central and northern Laos, is believed to have a restricted breeding range in limestone karst environments (Alström et al.,

2010).

Furthermore, the taxonomic classification also changes from time to time.

Robson (2008) documented 1,327 bird species in his second edition of book entitled

‘A field guide to the birds of South-east Asia’, and listed all new species to the region, omitted in accurate classification , and made changes in nomenclature since the previous edition of the book. Thirty two species were completely new taxa to the region of South-east Asia; six species were omitted due to the recent taxonomic

change, 48 additional species to the region due to taxonomic splits, and more than

150 species of existing species with changes in nomenclature due to taxonomic splits

Robson (2008). Most of the variations were because of the recent taxonomic changes and the resolution of gender issue (Robson, 2008).

1.2 Bird diversity in natural habitats of Peninsular Malaysia

The terrestrial ecosystems in Peninsular Malaysia include various types of natural and man-made habitats ranging from the coast to highland. The varieties of natural habitats that exist in Peninsular Malaysia such as lowland rainforest, hilly forest, mountain rainforest, and mangrove forest have become home to a variety of birds (Nagelkerken et al., 2008; Nur Munira et al., 2011; Peh et al., 2011). Natural habitats of Peninsular Malaysia supports a large number of resident birds, and receives hundreds of migratory species that migrate from northern hemisphere to southern hemisphere during the winter migratory season (September-March every year) (DeCandido et al., 2004). Natural habitats also record the highest number of bird species compared with man-made habitats (i.e. oil palm plantations and rice fields) (Nur Munira et al., 2011).

Seven hundred and twenty six bird species have been recorded throughout the country to date (eBird, 2016). In Peninsular Malaysia, Selangor has recorded the highest number of bird species with a total of 529 species were known to date, followed by Pahang (517), and Perak (515) (Figure 1.1). Most of the birding

hotspots in Peninsular Malaysia are characterised as natural forests and highland areas. Among the top birding hotspots, include (1) Taman Negara, Kuala Tahan,

Pahang, (2) Fraser Hill, Pahang, (3) Gunung Panti Forest Reserve, Johor, (4) Kuala

Selangor Nature Park, Selangor, and (5) Bukit Larut, Perak (Figure 1.2). Taman

Negara is among the most important forest reserve in this country. Taman Negara is located at the centre of Peninsular Malaysia and spreads over 4343 km2 within areas of three states namely Kelantan, Terengganu, and Pahang (Latif et al., 2012). Taman

Negara is also known as one of the world’s oldest rainforest estimated about 130 million years (Latif et al., 2012) and this forest reserve is home to 388 bird species

(Figure 1.2) (eBird, 2016).

These forest reserves are important for the survival of resident breeding bird species. The Blue-winged Pitta Pitta moluccencis, for example, was found to extend their breeding range to Taman Negara National Park, Pahang although previously known to breed only in the north of Peninsular Malaysia (Hutchinson & Mears,

2006). Besides, highland areas such as Fraser Hill, Cameron Highland, and Bukit

Larut are important areas for high latitude bird species such as Silver-eared Mersia

(Leithrix argentauris), Mountain Bulbul (Ixos mcclellandii) and Common Green

Magpie (Cissa chinensis) (Robson, 2008).

2198 Selangor 529 2637 Pahang 517 959 Perak 515 532 Kedah 482 670 No. of surveys Johor 457 865 Pulau Pinang 415 No. of species 289 Negeri Sembilan 379 181 Perlis 364 88 Terengganu 292 34 Kelantan 286 132 Melaka 243 0 500 1000 1500 2000 2500 3000 No. of bird species

Figure 1.1 Total number of bird species recorded and field observations according to states in Peninsular Malaysia (eBird, 2016).

Taman Negara Bukit Fraser Gunung Panti FR Kuala Selangor Nature Park Panti Bird Sanctuary Bukit Larut FRIM Pedu Lake No. of species Air Hitam Dalam FR Sg. Sedim RF Merapoh Bukit Wang FR Bukit Tinggi Krau WR Cameron Highlands 0 100 200 300 400 No. of bird species

Figure 1.2 Total number of species recorded in 15 birding hotspots in Peninsular Malaysia. Seven hundred and twenty six bird species have been recorded throughout the country to date (eBird, 2016).

Nevertheless, human activities and deforestation have been among the major threatening factors on the decline of birds in this country (Wilcove et al., 2013). Prior to land conversion, the activities are heightened, and it is very important to measure the diversity of birds in their natural habitats in order to obtain more information for conservation purposes. Most of the recent studies on birds conducted in Malaysia mainly focused on the affected forest habitats caused by activities such as logging and habitat conversion (Soh et al., 2006; Edwards et al., 2013). There is a relative paucity of studies on the detail measure of bird diversity in their natural habitats in

Peninsular Malaysia (Rahman, 2002; Sheldon et al., 2009a). Detail and accurate biodiversity assessment is crucial in diverse natural habitats; however there is lack of documentation on this matter.

1.3 The importance of birds

Birds play an important role to the environment and are beneficial to humans.

Bird is an important dispersal agent for flora and fauna. The frugivores bird species such as flowerpeckers, bulbuls, and hornbills are seed dispersers or pollinators, which also influence the pattern of seed distribution and thus formation of forest structure (Moermond & Denslow, 1985; Clark et al., 2001). A study on bats and birds at pastures in the tropical rainforest in Mexico also revealed that both the taxa are important in spreading the seeds of pioneer and umbrella species (ficus, shrubs, herbs, and epiphytes) in pastures which in turn connect forest fragments and conserve forest diversity (Galindo‐González, 2000). Birds also help in the dispersal

of small creature in the forest such as Hemlock Wooly Adelgid Adelges tsugae, (a small aphidlike insect), from one area to another (Orwig et al., 2002).

Birds are also important in regulating the populations of insects. Murakami and Nakano (2002) conducted a manipulative field experiment to determine the effect of birds on the insect herbivore population in the riparian forest. The study revealed that the insect herbivore population near the stream areas was more influenced by bird predation compared to the upland forest (Murakami & Nakano,

2002). Instead of regulating the population of insect, raptors (bird of prey) in rice fields were found to help farmers control the population of pests. Field observation in the rice fields of Permatang Damak, Penang, by Nur Munira et al. (2014b) found that raptors such as Brahminy Kite, Haliastur indus and Black-shouldered Kite, Elanus caeruleus often prey on rodents especially during harvesting season.

In addition, birds are frequently chosen as indicators to predict the effects of environmental stress. It is the best indicator for habitat loss and food availability

(Lim & Sodhi, 2004; Lehmkuhl et al., 2007). Bird is an animal group that is always documented by many studies on habitat destruction (Naidoo, 2004; Waltert et al.,

2005; Ko et al., 2009). As explained by Lawton et al. (1998) and Louette et al.

(1995), birds are frequently depicted as the indicator or ‘flagship taxa’ in biodiversity inventories because birds are widespread and present in most habitats. Birds are easy to observe or detect compared to the other fauna due to their loud vocalization; most of them have bright colour patterns and they are abundant in many habitat.

High bird diversity in Peninsular Malaysia is the main reason that Malaysia is the ultimate birdwatching paradise for recreational activity. There are 55 Important

Bird Areas in Malaysia, whereby 18 areas are located in Peninsular Malaysia (Yeap et al., 2007). Birdwatching activity provides awareness among citizens to become receptive on the importance of nature and wildlife. The collaboration between local authorities and non-governmental organisations (NGOs) on the establishment of bird-related events such as Raptor Watch in Tanjung Tuan, the Fraser’s Hill

International Bird Race, and the Wing of Kuala Kubu Baru provides an avenue for bird enthusiasts from around the world to return every year to Malaysia (Kudus,

2011). The annual project of “My Garden Birdwatch” organised by Malaysia Nature

Society (MNS) and its Bird Conservation Council has also encouraged Malaysians from all ages to be more aware on the existence of birds in their own backyard (Tiah,

2015).

For many centuries, human and birds are intertwined. Many people see birds as a symbol of freedom and strength. However, some people believe that blackbird denotes bad luck whereas white birds and feathers denote good fortune. Bird symbols are often used as name for sports team, images on stamps, coins, paintings, songs, cereals, automobile, greeting cards and shoes. In East Malaysia, Sarawak is known as the land of hornbills where eight out of 54 species hornbills in the world are found

(Bennett et al., 1997). The Rhinoceros hornbill is the official emblem of the state of

Sarawak, and important as a cultural symbol for the people of Sarawak especially the

Dayak communities (BPO, 2016).

1.4 Contribution of rice fields on bird diversity in Peninsular Malaysia

Rice field is a temporary wetland landscape that is important as a feeding ground and stop over area for various type of birds such as waterbirds, raptors, pigeons, sparrows, and munias (Nur Munira et al., 2014a). The environment of rice fields are repeatedly changing due to the influence from human activities i.e. ploughing, seasonal flooding, and planting (Stafford et al., 2010). Thus, rice fields are a unique habitat where every stage of planting attracts different bird groups for foraging (Stafford et al., 2010). This was evident by with the study by Nur Munira et al. (2014a) where distinct variation of bird richness and abundance was observed in every planting stage. Besides, a study on the use of rice fields by raptors in northern

Peninsular Malaysia revealed that at least 10 migratory raptors were observed which include two vulnerable raptor species, i.e., Greater-spotted Eagle, Aquila clanga and

Eastern Imperial Eagle, Aquila heliacal (Nur Munira et al., 2014b). This had proven that rice fields play an important role in providing suitable habitats for foraging, shelter, and breeding activities for diverse birds (Wood et al., 2010).

Between 2010 and 2016, only a small number of researches related to the bird diversity of rice field were conducted. Example of studies that have been carried out within this period interval were bird use of rice fields in Korea and Japan (Fujioka et al., 2010), bird use of rice fields in the Indian subcontinent (Sundar & Subramanya,

2011), birds of rice fields in the Americas (Acosta et al., 2010) and the temporal distribution of birds in rice-growing landscape in northern Peninsular Malaysia (Nur

Munira et al., 2014a). Nur Munira et al. (2014a) also state the lack of ecological study on bird’s assemblages in the rice fields of Malaysia.

These studies have highlighted the importance of rice field cultivation areas that served as breeding habitats for waterbirds. Rice fields can also uphold the most diverse and abundant amount of breeding waterbirds in the world as shown in

Southwestern Louisiana (Pierluissi et al., 2010). This has proven that rice field ecosystem exhibits a good habitat to support diverse bird groups. Based on this information, more studies should be conducted in order to ascertain the current situation of bird diversity especially in Peninsular Malaysia’s rice fields. This study aims to identify the contribution of rice fields on the total bird diversity in Peninsular

Malaysia.

1.5 Rationale

Recent studies on birds in Malaysia revealed that, few approaches of bird measurements have been conducted. Most studies on birds in various habitats have used the common diversity measures such as Simpson’s diversity index (Rahman,

2002), Shannon-Wiener formula (Sheldon et al., 2009a; Nur Munira et al., 2011), and Fisher’s alpha (Bing et al., 2013). Bird diversity study in Paya Indah Wetland

Reserve have used the regular measurement as most of the previous studies i.e.

Shannon’s and Simpson’s index for diversity indices, Margalef’s and Menhinik’s index for richness indices, and McIntosh’s and Pielou J index for evenness indices

(Zakaria et al., 2009). The simplest data analysis i.e. describing bird diversity in percentage was also found in the study of bird diversity in Kenaboi Forest Reserve,

Jelebu (Ramli et al., 2009)

However, there were several studies on bird diversity in Malaysia that used species estimators to determine the estimated species richness (Peh et al., 2005; Peh et al., 2006). This species estimator is very useful for ecologists to estimate the total number of species in any particular area from limited dataset or with different approaches (Herzoq et al., 2002). Since this approach of measurement has only been applied to the birds of logged forest and mixed-rural habitats in southern Peninsular

Malaysia (Peh et al., 2005; Peh et al., 2006), the present study aims filled this gap by applying a similar approach to the wider range of birds in natural habitats throughout

Peninsular Malaysia. The estimation of total number of species in natural habitats is important to be examined, as it can aid in formulating management actions that will provide maximum benefits for bird communities.

Many previous studies have also been restricted on the local diversity or known as alpha diversity (Styring & Ickes, 2001; Zamri & Zakaria, 2002; Styring &

Zakaria, 2004). According to Jankowski et al. (2009), the investigation of bird diversity should not be restricted to only within the habitat but also important to assess the diversity among habitats on a landscape scale. Thus, beta diversity across the region in Peninsular Malaysia is another important aspect to be discovered in this study. To date, there have been no attempts to evaluate beta diversity on a broader scale that involve natural habitats in Peninsular Malaysia. The investigation of beta

diversity is able to provide additional knowledge for better understanding of birds in natural habitats across the region of Peninsular Malaysia.

The assessment based on the incidence data is frequently limited to the percentage of species or family list and often unable to generate optimal information from the abundance data (Ramli et al., 2009). However, this study fills the gap by analysing the incidence bird data in detail to generate maximum information that is believed to be useful in bird assessment. The pattern of rarity in birds is assessed from the incidence data, which is able to give better understanding on conservation actions (Brooks et al., 2002). In addition, functional diversity for each bird species can also be assessed through the incidence base data (Barbaro & Halder, 2008). This study also aims to analyse the functional life traits of rare species in order to link to their limited occurrences in natural habitats.

The incidence base data are further used to analyse the taxonomic distinctness of birds in natural and man-made habitats. This can be considered as a new tool for measurement of bird diversity in Peninsular Malaysia because measure of species richness (i.e. diversity indices) in the aforementioned habitat is a common objective.

Investigation of bird diversity through taxonomic make-up in various habitats is an alternative method that gives meaningful information to species that are more taxonomically distinct (Xu et al., 2012). If two or more habitats have similar number of species richness, it is not necessary that all habitats are equally diversified, but one habitat may have species that are taxonomically related to one another or vice versa

(Warwick & Clarke, 1998).

1.6 Thesis outline

This thesis consists of five general chapters and five research chapters. The first general section, Chapter 1 focuses on the introduction of avifauna at global and local scale as well as overview on the contribution of rice field habitats on the diversity of avifauna in Peninsular Malaysia. Chapter 2 presents literature review of this study. Chapter 3 describes the general materials and methods used. General chapters also include Chapter 9 where general discussions from all research chapters are consolidated and Chapter 10 provides general conclusions of the study.

Chapter 4 to 8 are the main research chapters of this thesis. Chapter 4 is the overview on the species richness and community structure of bird in natural habitats of Peninsular Malaysia. This chapter describes the species accumulation curve in order to determine the sampling effort sufficiency, identifies the bird status (i.e. residential status, population trend, and IUCN status), and overview of bird occurrence across study sites.

Chapter 5 thus estimates the bird species richness for natural habitats in

Peninsular Malaysia. Seven types of estimators are used to analyse the bird incidence data obtained from both primary and secondary sources. The performance for each estimator is evaluated in order to choose best performing estimators. This chapter also discusses whether species richness estimator tools are able to generate reasonable estimations of diversity although the data used may have been obtained

through different sampling efforts. Assessment on regional biodiversity of birds in natural habitats in Peninsular Malaysia is explored in Chapter 6. Spatial patterns of bird community structure are documented using a range of methods and patterns of bird diversity within and between regions and throughout Peninsular Malaysia are discussed. It is predicted that bird species diversity between areas can be affected by distance, whereby close distance sites show high similarity in bird diversity and vice versa.

Chapter 7 further explores the pattern of rarity among birds based on geographic range, habitat specificity, and local population. The functional diversity for each rare species found in natural habitats is also analysed in this chapter. It is predicted that some species are common and abundant whilst there is a large portion of rare species found in natural habitats. Chapter 8 is the case study in order to ascertain the contribution of rice fields on bird diversity in Malaysia. Bird diversity in every stage of planting activities is also assessed in this chapter. Taxonomic relatedness of bird species in natural habitats and rice fields is explored in this chapter.

The predominant goal of this study is to measure bird diversity and analysis of community composition and community assemblage structure among birds across natural habitats of Peninsular Malaysia. Various measurements are applied to the bird data, which is hoped to enhance understanding and knowledge of the diversity and assemblage structure of bird in natural habitats of Peninsular Malaysia. In future,

these data can be used as a reference to the other similar studies in order to explain the vast diversity of avifauna in such systems.

1.7 Objectives

The primary objectives of the study according to each research chapter are as follows:

1. To determine the status of birds and population trend based on IUCN Red

List at natural habitats of Peninsular Malaysia from primary and

secondary data.

2. To estimate the total number of bird species in natural habitats by using

seven types of non-parametric estimators.

3. To analyse the beta diversity of bird communities among study areas

based on turnover and variation concepts.

4. To identify the forms of rarity among bird species in natural habitats of

Peninsular Malaysia by using the rarity classification system.

5. To compare the bird taxa in natural habitats and rice fields in order to see

the contribution of bird species in the rice fields to the diversity of birds

in Peninsular Malaysia.

CHAPTER 2

LITERATURE REVIEW

2.1 Birds in natural habitats

Tropics consist of a region surrounding the equator that includes Tropical

Andes, Madagascar, Caribbean, Indo-Burma, Western Ghats and Sri Lanka,

Wallacea, Philippines, and Sundaland (Brummitt & Lughadha, 2003). These lands are among the 25 biodiversity hotspots in the world that are homes to 2,821 endemic birds (Myers et al., 2000). Tropical Andes records the highest number of bird species with total of 1,666, and 677 are endemics (Myers et al., 2000). The Sundaland that encompasses the Peninsular Malaysia on the Asian mainland, the large islands of

Borneo, Sumatra, Java and its surrounding islands consist of a total of 815 bird species, whereby 139 are endemics to this region (Myers et al., 2000). The number of bird species records an increase from time to time, hence discovery of new bird species are occasionally described (Sheldon et al., 2009b; Lohman et al., 2010).

In tropical regions of South-east Asia, bird diversity is very high across the countries (Myers et al., 2000; Sodhi et al., 2004a; Robson, 2008). For example,

Peninsular Malaysia or West Malaysia is the southernmost extension of mainland

Asia, which is located between Thailand and Singapore, harbours more than 638 species of birds (Strange & Jeyarajasingam, 1999). Although the landmass coverage of Peninsular Malaysia is small (approximately 131, 235 km2), factors such as habitat

16 variation, its location near to the equator, and stable tropical climate have promoted high bird diversity in this country (Hughes et al., 2002). The bird composition in

Peninsular Malaysia has similarity with other Sunda subregion areas (i.e. Sumatra,

Java, and Borneo) because during the last Ice-Age, approximately 15,000 years ago, when sea-levels was much lower than today, the landmass in Sunda subregion was connected and probably bird species in the subregion were shared (Sodhi et al.,

2004a). The Sunda subregion recorded 129 endemics while only two endemics were found in Peninsular Malaysia (i.e Mountain Peacock-Pheasant, Polyplectron inopinatum and Malayan Whistling Thrush, Myophonus robinsoni).

Myers et al. (2000) stated that the Sundaland (including Peninsular Malaysia) was listed among the 25 biodiversity hotspot areas in the world. Bird is a wonderful fauna that lives in various habitats. Natural habitats in Peninsular Malaysia comprised of several types of forests such as lowland, montane, mangrove and peat swamp forest. Natural habitats have contributed the large proportion of bird species compared with man-made habitats include plantations (monoculture), orchards, and mix-shrubs (Peh et al., 2005, Aratrakorn et al., 2006; Nur Munira et al., 2011).

Conducive environments in natural habitats offer high availability of food sources

(Iwata, 2003), stable climate for egg incubation and hatchery (Zanette & Jenkins,

2000), and wide ranges of habitat niches (Siebert, 2002) to support a variety of bird species to live in this habitat.

Natural habitats especially rainforests play a vital role in serving as home, shelter, and provide abundance of food sources to resident and migratory birds. Birds that can be found in natural habitats are categorised as either common, rare, or endemic birds. A study on bird diversity in Kenaboi Forest Reserve, Jelebu, Negeri

Sembilan recorded 51 species that were commonly found in the study area (7-45 occurrences), 49 uncommon (3-6 occurrences), and 46 considered rare (unique and duplicate) (Ramli et al., 2009). According to Ramli et al. (2009) although the

Kenaboi Forest Reserve had been extensively logged for the past 20 years, this forest reserve is able to regenerate and provide sufficient resources for 152 bird species including 31 near-threatened species.

Continuous habitat destruction and degradation, over-exploitation (e.g. urbanisation), presence of exotic species, disease, pollution and contaminants, climate change, and other threats have resulted in the decline of the population and extinction of birds worldwide (Baillie et al., 2004; Sodhi et al., 2010). There are many reviews on bird diversity from 2000 to 2015 that have discussed the effects of forest fragmentation on bird species richness (Echeverría et al., 2006; Flaspohler et al., 2010), effects of plantation on bird diversity (Fitzherbert et al., 2008), bird species composition and feeding guilds in wetland reserve (Zakaria & Rajpar, 2010), disappearance of insectivores birds from tropical forest fragements (Şekercioḡlu et al., 2002), and response of mixed-species flocks to habitat alteration and deforestation (Zuluaga & Rodewald, 2015). It is concluded that bird diversity is significantly affected by human activities and deforestation.

2.2 Estimating bird species richness

The total number of bird species richness in Malaysia remains unknown. To date, more than 746 bird species have been recorded in Peninsular Malaysia, Sabah and Sarawak in the Borneo Island (MacKinnon & Phillipps, 1993; Wells, 1999 &

2007). In Malaysia, several studies have employed species estimator analysis in order to estimate bird species richness. Peh et al. (2006) conducted a study on the conservation value of degraded habitats for forest birds in southern Peninsular

Malaysia. In their study, nine types of non-parametric estimators are used (i.e., ACE,

ICE, Chao1, Chao2, Jackknife1, Jackknife2, MMMean, MMRun, and Bootstraps) to estimate forest bird species that were present in rubber tree plantations, oil palm plantations, and open areas. The results showed that these habitats supported 46-76 bird species which highest in rubber tree plantations compared to oil palm plantations and open habitats (Peh et al., 2006).

A year earlier Peh et al. (2005) conducted a study on the persistence of primary forest birds in selectively locked forests and mixed-rural habitats in Johor

(southern of Peninsular Malaysia). This study used non-parametric estimators including incidence-based estimator Chao2, incidence-based coverage estimator ICE and Michaelis-Menten model based estimator MMMean to estimate bird species richness. The choice of these three estimators were based on the best performance of the estimators in predicting tropical bird species as studied by Walther & Martin

(2001), Matlock et al. (2002), and Herzog et al. (2002). Soh et al. (2006) also used non-parametric estimators (i.e. ACE, ICE, Chao1, Chao2, Jack1, Jack2, Bootstrap,

MMRuns, MMMean) for bird study in montane areas of Peninsular Malaysia.

According to Soh et al. (2006) several estimators were employed since the performances of different estimators vary according to data sets. However, none of these bird studies in Peninsular Malaysia evaluated the performance of the estimators used.

In year 2011, a group of researchers from Universiti Putra Malaysia conducted a study on the conservation value of oil palm plantation estates and logged peat swamp forest for birds in the west coast of Peninsular Malaysia (Azhar et al.,

2011). This study used four mean of abundance estimators (ACE, Chao1, Jack1, and

Bootstrap) due to the unstandardized sample size among site types, and to estimate bird species in the study sites. Recently, Azhar et al. (2015) also used Chao1 and

ACE estimators to estimate understory birds, fruit bats, and butterfly that exist in the oil palm agricultural matrix. Both of these studies used abundance data, and none of bird studies in Peninsular Malaysia attempted to estimate species richness using the presence/absence data.

Other studies also used non-parametric estimators in other group of fauna such as a study on ground-dwelling ants in Sabah by Brühl & Eltz (2010) and study on tree species diversity in Borneo Island by Cannon et al. (1998). According to

Brühl & Eltz (2010), Jack2 estimates the highest species richness, i.e. 48, while

MMMean estimates the lowest, i.e. 25 ant species in oil palm plantations. Meanwhile a study by Cannon et al. (1998) stated a total of 329 and 340 tree species estimated by Chao2 in unlogged forest and eight-year logged forest, respectively.

According to Colwell & Coddington (1994), Bunge & Fitzpatrick (1993) and

Magurran (2004) several approaches have been used in estimating species richness and are categorised as follows: (1) extrapolation of species accumulation curves, (2) fitting parametric distributions of relative abundance, and (3) using non-parametric estimators based on abundance or incidence based data of species among samples.

Nonetheless, non-parametric estimators became the most preferred approach by researchers in biodiversity task for more than a decade (Walther & Martin, 2001).

The non-parametric estimators used rare species information of assemblage- singleton and doubleton (those represented by one or two individuals) or unique and duplicate (those represented once or twice) to predict the number of species that were not presented in the dataset (Gotelli & Colwell, 2001). Examples of studies that used non-parametric species richness estimator in their studies are shown in Table 2.1.

Table 2.1 Various ecological studies that used species richness estimator over the last two decades.

Source Country Organism Sampling Evaluation on estimator Performance of estimator method(s) Walther & UK & Parasites from Secondary data Bias and precision Chao2 and Jackknife 1 Morand (1998) France different host estimators performed best for (woodcreepers, real data sets fish, frogs, rabbits and tawny owls) Toti et al. USA Spider Aerial hand Reach asymptote of Michaelis-Menten means (2000) collection, ground estimator curve with fewer (MMMean) performed better hand collection, samples and close to than other estimators beating, Tullgren reasonable visual funnel litter asymptote extraction, and sweep-netting Chiarucci et al. Italy Plant Plots Relative error (RE) and Jack 1 and Jack 2 had the best (2001) square relative deviation performances (SRD) Melo & South- Macro- Using U-net Based on four criteria: Bootstrap estimator was the Froehlich east invertebrate 1. The smallest sub-sample best estimator followed by (2001) Brazil size needed to estimate Jack2. total richness in the sample, 2. Constancy of this size, 3. Lack of erratic behaviour in curve shape, and 4. Similarity in curve shape through different data sets

Table 2.1 Continued

Source Country Organism Sampling Evaluation on estimator Performance of estimator method(s) Walther & Canada Birds Point counts Bias and precision Chao2 was the best estimator Martin (2001) followed by Jackknife2 Brose (2002) East Carabid beetle Pitfall trapping Accuracy and precision Chao2 was the most accurate Germany and precise estimator Herzog et al. Bolivia Birds Species-list Accuracy, sensitivity to MMMean performed best for (2002) method (visual sample size, sensitivity to empirical and most simulated and acoustical true species richness and data sets observations) and the influence of underlying mist-netting species-abundance or species-detectability distribution Longino et al. Costa Ants Fogging, Malaise, Evaluation through data Tested only on ICE and (2002) Rica Berlese, Winkler, partitions and sample-based MMMean Barger, rarefaction plots Thompson, Longino, and other Sørensen et al. Tanzania Spiders Pitfall traps, Good estimator should Chao1 performed better than (2002) cryptic searching, asymptote accurately and other estimators sweep netting, early ground & areal hand collecting, and vegetation beating

Table 2.1 Continued

Source Country Organism Sampling Evaluation on estimator Performance of estimator method(s) Foggo et al. United Reef fish, Beach Sampling used Bias, precision, and Chao1 represents the best (2003) Kingdom macrofauna, and deep box core accuracy estimator among others Estuarine and secondary Oligochaetes data Hortal et al. North Arthropod Transects and Bias and precision ACE and Chao1 showed (2006) Atlantic pitfall traps the best performance throughout the different sampling effort unit González- Northern Plant Quadrat sampling Bias, precision, and Jackknife 1 was the best Oreja et al. Spain with different accuracy estimator (2010) environmental conditions