Vocal Behaviour of White-Cheeked Crested Gibbons (Nomascus leucogenys): Vocal Production, Usage and Response.

Hou-Chun Chen, BSc.

A thesis submitted for the Degree of Doctor of Philosophy of the University of New England

July, 2011

1 CERTIFICATION

I certify that the substance of this thesis has not already been submitted for any degree and is not currently being submitted for any other degree or qualification.

I certify that any help received in preparing this thesis and all sources used has been acknowledged in this thesis.

Signature

2 ACKNOWLEDGEMENT I would like to express my appreciation to my supervisors, Drs. Jim McFarlane and Stuart Cairns for helping and supervising me to complete this thesis. I also wish to thank Dr. Boyd Wright for spending many hours of proof-reading work.

Lots of appreciations expressed to staff in Head office of Zoological Park Organization of , , , Nakhornratchasima Zoo, Zoo, Chiang Mai and Endanger Primate Rescue Center of Vietnam, your help and assistance do support many ways of my overseas research field work. Special thanks to Sumate Kamolnorranath, Wanchai Tunwattanai, Wanlaya Tipkantha and Tilo Nadler for their valuable assistance in all kinds of aspect for making my overseas research work possible.

This thesis could not have been completed without support from Zoological Park Organization, Thailand and Endanger Primate Rescue Center, Vietnam. I also want to thank the Directors of Dusit Zoo, Khao Kheow Open Zoo, Nakhornratchasima Zoo, , Chiang Mai Night Safari and Melbourne Zoo for granting me permission to collect data.

Thanks for the Conservation International Primate Action fund, University of New England, and Zoological Park Organization for funding my research.

Finally, I would like to give my very special thanks to my grandfathers (Chin-lin, Chen and De-Lu Weng), my parents (We-shin Chen and Li-fang Weng) and other family members as I have been away from them for all these years. Their support is the key for me to complete this thesis.

3 PAPERS PUBLISHED DURING CANDIDATURE

Refereed papers

Chen, H.-C.; Kaplan, G. & Rogers L-J.2009, Contact calls of common marmosets (Callithrix jacchus): Influence of age of caller on antiphonal calling and other vocal responses. America Journal of Primatology 71 165-170

Chen, H.-C., Kamolnorranath, S & Kaplan, G., 2008. Female crested gibbons (genus Nomascus) sing male song. Vietnamese Journal of Primatology 2 47-53

Published Abstracts

Chen, H.-C. & Kaplan, G. 2008. Vocal individuality in white-cheeked crested gibbons (Nomascus leucogenys): Acoustic features and song organization. XXIInd congress of the International Primatological Society, 4th-9th August, 2008, Edinburgh, United Kindom, P 4

Kamolnorranath, S.; Chen, H-C. & Dumnui, S. 2007: Population assessment of crested gibbons (Nomascus spp.) in Zoological Park Organization of Thailand by using vocal identification – A non-invasive method. 16th Conference of South East Asian Zoos Association (SEAZA) 2nd – 4th September Zoo Negara, Kuala Lumpur, Malaysia.

Chen, H-C; Kaplan, G. & Rogers, L. J. (2006): Contact behaviour in the isolated marmoset (Callithrix jacchus) and its natal group. Abstract of 2006 Australian Society for the Study of Animal Behaviour (ASSB) Annual Conference, 20th-23rd April. 2006 pp. 29 Macquarie University, Sydney, Australia.

Chen, H-C; Kaplan, G. & Rogers, L. J. (2006): Vocal behaviour in isolated marmosets (Callithrix jacchus) on presentation of stimuli. Abstract of 2006 Australian Society for the Study of Animal Behaviour (ASSB) Annual Conference, 20th-23rd April. 2006 pp. 29 Macquarie University, Sydney, Australia.

4 TABLE OF CONTENTS

CERTIFICATION ...... 2 ACKNOWLEDGEMENT ...... 3 PAPERS PUBLISHED DURING CANDIDATURE ...... 4 TABLE OF CONTENTS ...... 5 TABLE OF FIGURES ...... 9 LIST OF TABLES ...... 11 ABSTRACT ...... 13 CHAPTER 1 INTRODUCTION ...... 17 1.1 Vocal communication in primates ...... 17 1.1.1 Limitation on gibbon research ...... 19 1.2 Vocal behaviour in gibbons ...... 21 1.2.1 Song structure and organization...... 24 1.3 Vocal individuality...... 27 1.3.1 Individual differences in gibbon song ...... 28 1.4 Vocal development in juveniles and sub-adults ...... 30 1.4.1 Song development of juvenile gibbons ...... 31 1.5 Vocal plasticity in adults ...... 32 1.5.1 Sex-specificity in gibbon song ...... 33 1.5.2 Gibbon social structure and its relation to vocal plasticity ...... 35 1.6 Functions of gibbon song ...... 36 1.6.1 Territorial defence ...... 37 1.6.2. Pair bonding ...... 39 1.7 Research aims and original contribution of this thesis ...... 41 CHAPTER 2 GENERAL METHODOLOGY ...... 46 2.1 Study sites ...... 46 2.2 Subjects ...... 48 2.2.1 Sample size and species ...... 48 2.2.2 Identification of sex and age ...... 49 2.3 Housing ...... 52 2.4 Husbandry ...... 53 2.5 Data collection ...... 54 2.5.1 Vocalisation recording ...... 54 2.5.2 Vocalisation analysis ...... 55 2.5.2.1 Analysis of vocalisations made by males ...... 57 5 2.5.2.2 Analysis of vocalisations made by females ...... 60 2.6 Statistics ...... 61 CHAPTER 3 VOCAL INDIVIDUALITY IN WHITE-CHEEKED CRESTED GIBBONS (NOMASCUS LEUCOGENYS) ...... 63 3.1 Introduction ...... 63 3.2 Method ...... 65 3.2.1 Subjects ...... 65 3.2.2 Procedures ...... 66 3.2.3 Sound analysis ...... 66 3.2.4 Statistical analysis ...... 70 3.3 Results ...... 71 3.3.1 General description of song phrases ...... 71 3.3.1.1 Duration of duet song in pairs ...... 72 3.3.1.2 Total of call phrases of duet song in pairs ...... 72 3.3.1.3 Calling rate of the duet song ...... 73 3.3.1.4 Male song phrases ...... 74 3.3.1.5 Female song phrases ...... 77 3.3.2 Acoustic features of call phrases ...... 79 3.3.2.1 Male call phrases ...... 79 3.3.2.2 Female song phrases ...... 84 3.3.3 Context and structure of song ...... 86 3.3.3.1 Male song phrase ...... 87 3.3.3.2 Female song phrase ...... 90 3.4 Discussion ...... 92 CHAPTER 4 SONG CHANGE AND VOCAL PLASTICITY IN WHITE-CHEEKED CRESTED GIBBONS (NOMASCUS LEUCOGENYS) ...... 98 4.1 Introduction ...... 98 4.2 Method ...... 101 4.2.1 Subjects ...... 101 4.2.2 Procedures ...... 102 4.2.2.1 Development in juvenile and sub-adult white-cheeked crested gibbons ...... 102 4.2.2.2 Vocal plasticity in adult white-cheeked crested gibbons...... 103 4.2.3 Sound analysis ...... 104 4.2.4 Statistics ...... 105 4.3 Results ...... 105

6 4.3.1 Vocal development in juvenile white-cheeked crested gibbons ...... 106 4.3.1.1 Development of acoustic features in the case of a juvenile male white-cheeked crested gibbon...... 106 4.3.1.2 Comparison between two female juvenile white-cheeked crested gibbons ...... 110 4.3.2 Development of acoustic features in four male sub-adult white-cheeked crested gibbons...... 111 4.3.2.1 Female-like great call phrases of the four sub-adult males ...... 111 4.3.2.2 Comparison of male song phrases of four male sub-adults ...... 111 4.3.3 Comparison of song length and onset of song between adult males and their offspring (one male juvenile and two sub-adult males) ...... 114 4.3.4 Vocal plasticity in adult white-cheeked crested gibbons ...... 117 4.3.4.1 Vocal plasticity in adults before and after pairing ...... 117 4.3.4.2 Vocal plasticity in the adult male before and after the death of his female partner ...... 119 4.4 Discussion ...... 121 CHAPTER 5 PRIMARY FUNCTION OF SONG IN WHITE-CHEEKED CRESTED GIBBONS (NOMASCUS LEUCOGENYS) ...... 129 5.1 Introduction ...... 129 5.2 Materials and Methods ...... 131 5.2.1 Materials ...... 131 5.2.2 Playback song selection ...... 132 5.2.3 Procedure ...... 136 5.2.3.1 Pre-playback experiment observation ...... 136 5.2.3.2 Playback experiment observation ...... 136 5.2.4 Behaviour recording ...... 138 5.2.5 Statistics analysis ...... 139 5.3 Results ...... 140 5.3.1 Behaviour observation before, during and after song without sound playback ...... 140 5.3.2 Vocal and non-vocal response to playback samples ...... 142 5.4 Discussion ...... 149 CHAPTER 6 GENERAL DISCUSSION ...... 155 6.1 Individuality ...... 155 6.2 Development and plasticity...... 158 6.2.1 Development ...... 158

7 6.2.2 Plasticity ...... 161 6.3 Primary song function ...... 161 6.3.1 Ability of discrimination ...... 161 6.3.2 Primary song function ...... 163 6.4 Limitation of the current project ...... 164 6.5 Conclusion ...... 165 REFERENCES ...... 166 APPENDIX LIST OF SONG RECORDING DETAIL ...... 175

8 TABLE OF FIGURES

Figure 2.1: Map of South-East Asia and the location of the six research sites...... 47 Figure 2.2: The appearance of male and female white-cheeked crested gibbons...... 50 Figure 2.3: The island enclosure of white-cheeked crested gibbons...... 52 Figure 2.4: The sonogram of a complete duet song sung by a pair of white-cheeked crested gibbons...... 56 Figure 2.5: The examples of song phrases in male white-cheeked crested gibbons recorded in this study...... 57 Figure 2.6: The acoustic measurements made of boom call (A) and staccato call phrases (B)...... 58 Figure 2.7: The acoustic measurements in the first note of multi-modulated call phrases...... 60 Figure 2.8: An example of a great call phrase in female white-cheeked crested gibbons...... 60 Figure 2.9: An example of first note of female great call phrase...... 61 Figure 3.1: The sonogram of twelve types of sub-catalogued multi-modulated call phrases in male white-cheeked crested gibbons...... 67 Figure 3.2: The mean duration of duet song produced by white-cheeked crested gibbons.. ... 72 Figure 3.3: The mean call phrases contained in the duet song of white-cheeked crested gibbons...... 73 Figure 3.4: The mean number of call phrases produced per minute by the pair during the duet song...... 74 Figure 3.5: The mean duration of male song phrases...... 75 Figure 3.6: The number of male song phrases produced in male white-cheeked crested gibbons...... 76 Figure 3.7: The percentage of each type of call phrases produced by male white-cheeked crested gibbons...... 76 Figure 3.8: The mean duration of female song phrases. Each bar represents the length of song phrases (mean ± sem) in female white-cheeked crested gibbons...... 77 Figure 3.9: The number of female song phrases produced in female white-cheeked crested gibbons...... 78 Figure 3.10: The mean number of call phrases produced per min during the duet song...... 79 Figure 3.11: The plot of canonical discriminant functions in function 1 versus function 2.. ... 83 Figure 3.12: The start frequency and the peak frequency (mean ± sem) of great call and non-great call phrases...... 84 Figure 3.13: The plot of canonical discriminant functions in function 1 versus function 2.. ... 86 Figure 3.14: An example of a staccato call phrase produced by a male white-cheeked crested gibbon (M2) that contained more than 14 notes...... 87 Figure 3.15: The percentage of sub-catalogued multi-modulated types in male white-cheeked crested gibbons...... 89 Figure 3.16: Representative great call phrases of the five subject females. 1 to 5 represents the female individual of the pairs housed at Dusit Zoo, Night-Safari, Endangered Primate Rescue Center, Nakhornratchasima Zoo and Chiangmai Zoo, respectively...... 91 Figure 3.17: The mean number of notes within one great call phrase produced by each female individual...... 92 Figure 4.1: A represents the example of a female great call and male “female-like” great call phrases ...... 104 Figure 4.2: Changes of song parameters on the juvenile at different sampling time points. . 108 Figure 4.3: Changes of call parameters on the juvenile at different sampling time points. ... 109 Figure 4.4: The great call phrases produced between two female juvenile white-cheeked crested gibbons in EPRC...... 110 Figure 4.5: Boxplot of song duration, showing song duration of the male adult and its offspring in Dusit Zoo, EPRC and Nakhornratchasima Zoo, respectively...... 114 Figure 4.6: The mean initial singing timings of onset song of the juvenile and sub-adult white-cheeked crested gibbons compared to their parents...... 115 Figure 4.7: Boxplot of onset of song of the juvenile and sub-adult white-cheeked crested gibbons in Dusit Zoo, Nakhornratchasima Zoo and EPRC across three time points...... 116 Figure 4.8: The number of call phrases produced by the female adult in Chiangmai Zoo before, after and three months after the pairing...... 119 Figure 4.9: The number of sub-catalogued multi-modulated types produced by the white-cheeked crested gibbons before and after the change of social status. . ... 120 Figure 5.1: The sonogram of playback samples...... 135 Figure 5.2: Behaviour of white-cheeked crested gibbons changes before, during and after sing...... 142 Figure 5.3: Responses to white-cheeked crested gibbon duet song playback sample...... 146 Figure 5.4: Results of playback testing white-cheeked crested gibbons...... 148 Figure 6.1: The relationship between the age of the individual (X-axis) and the number of call phrases produced per song (Y-axis) in male white-cheeked crested gibbons in the present study...... 160

10 LIST OF TABLES Table 2.1: Information on study animals...... 51 Table 2.2: Group composition of observed individuals...... 53 Table 3.1: Information about the five observed pairs...... 65 Table 3.2: The visit period and days for collecting duet song bouts in the pair of white-cheeked crested gibbons ...... 66 Table 3.3: The subcategories multi-modulated call phrases in male white-cheeked crested gibbons...... 68 Table 3.4: The description of variables of general song structure and acoustic features measured...... 69 Table 3.5: The number of call phrases that were collected and analysed by each individual. Each column refers to each type of call phrases produced by males or females. ... 71 Table 3.6: Standardised coefficients and correlations of acoustic measurements with the four discriminant functions...... 81 Table 3.7: Standardized coefficients and correlations of acoustic measurements with the three discriminant functions...... 85 Table 3.8: The maximum number of notes in one staccato call phrase made by male white-cheeked crested gibbons ...... 87 Table 3.9: The number of sub-catalogued multi-modulated call types used within a song of white-cheeked crested gibbons (n=10) ...... 88 Table 4.1: Personal information for each individual white-cheeked crested gibbon used in this study...... 102 Table 4.2: The number of call phrases collected and analysed in each individual...... 106 Table 4.4: The types of sub-catalogued multi-modulated call phrases produced by the male adult in EPRC at the different sampling points...... 113 Table 4.5: The types of sub-catalogued multi-modulated call phrases produced by the male adult in Chiangmai Zoo at the different sampling points...... 118 Table 4.6: The types of sub-catalogued multi-modulated call phrases produce by the male adult in Nakornratchasima Zoo at the different sampling points...... 121 Table 5.1: Housing, duration of pairing and presence of offspring in the tested groups...... 132 Table 5.2 The definition of each scored behavior catalogued and recorded before, during and after white-cheeked crested gibbons produced a song...... 139 Table 5.3: Each scored behavior expressed by the gibbons before, during and after singing (mean ± sem) ...... 141 Table 5.4: Attention and approach of white-cheeked crested gibbons to the different playback sound samples, while the white-cheeked crested gibbons produced their song.. . 143

11 Table 5.5: Attention, approach and song producing of white-cheeked crested gibbons to the different playback sound samples two hours after the white-cheeked crested gibbons produced their song. Five playbacks per sample were conducted...... 144

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ABSTRACT

White-cheeked crested gibbons (Nomascus leucogenys), one of the most endangered primate species in South-East Asia, produce a series of loud calls to communicate. This special vocal behaviour is termed “song” and was previously thought to be a fixed stereotyped system of communication. However, recent research has raised questions as to whether or not white-cheeked crested gibbons express their vocal individuality under such a fixed and stereotyped call structure and song organisation. Whether or not any additional factors are involved with changes and process of song development is also unclear. Moreover, the adaptive functions of song remain inconclusive. It is unknown whether the primary function of white-cheeked crested gibbon songs is the same as that of other previously studied lar group gibbons (Hylobates spp). The aims of the present study were to investigate the vocal individuality of adult white-cheeked crested gibbons along with patterns and change of song in terms of their social status. In association with this, preliminary playback experiments were conducted to investigate the possible primary function of song.

This thesis investigated the vocalisations of nineteen white-cheeked crested gibbons housed at six different sites in Thailand and Vietnam between 13th August 2006 and 30th April 2008. A

13 total of 178 complete song bouts with visual identity were recorded. A total of 14,101 call phrases were identified and analysed. Twenty-nine song variables were selected and analysed through sound analysis software (Raven Pro 1.4). Results were analysed using the general statistical method of analysis of variance (ANOVA). One of a selection of non-parametric tests

(Friedman test, Cochran’s Q test, Wilcoxon signed rank test and McNemar test) was used in the analysis if the transformed data were still not normally distributed. One-way repeated-measures

ANOVA was used in a number of instances to test for differences in relation to age groups or social context across different sampling periods, and to also determine whether or not acoustic features changed during development of an individual’s song.

In Chapter 3, duet song of adult pairs of white-cheeked crested gibbons was examined. Results showed that within the pair in every measured song parameters, each pair produced relatively stable songs. There were significant differences among the pairs in terms of song context and call parameters. Individual white-cheeked crested gibbons performed songs differently in terms of vocal production and usage. Discriminant Function Analysis (DFA) was used to analyse the vocal individuality. It showed that both 95% of male calls and 76% of female calls could be correctly identified in relation to the responsible individuals. Results also indicated that

14 frequency-related parameters were the major factor that discriminated males, whereas temporal parameters mainly discriminated females.

In Chapter 4, measures at different sampling points showed that juveniles adjusted their call phrase usage in their song. The physical call structure, however, did not change over different sampling points. Similar results were also found among sub-adult individuals. Moreover, sub-adults that were of similar age, but keep under different social conditions, used the call phrases differently depending upon the changes of social context. Adults also expressed a certain level of vocal plasticity in both newly paired and long-term bonded individuals. The change of social context may also influence their call phrases usage.

In Chapter 5, behavioural observations were recorded before, during and after white-cheeked crested gibbons produced their song. Playback experiments were conducted at least three months after the purely behavioural observations. Results showed that although there was no particular behavioural change before gibbons initiated their song, all individuals tended to move to the canopy of the tree and stay in position during production of the song. It was found that hanging behaviour significantly increased after gibbons had finished their song. Although the results of playback experiments did not provide a conclusive answer to the precise function of 15 song, the results suggested that white-cheeked crested gibbon song is chiefly for intra-group communication rather than inter-group communication.

Overall, the result of the present study showed that white-cheeked crested gibbons performed their duet song with a high degree of coordination and maintained song stability in each pair.

Moreover, vocal individuality of white-cheeked crested gibbons can be identified through different kinds of acoustic parameters such as frequency factors of call phrases in males and temporal factors of female great call phrases. This current study also provided new evidence to support the idea that vocal development of white-cheeked crested gibbons may not only be inherited, but also be influenced by social factors. This suggests that white-cheeked crested gibbons are capable of adjusting the production and usage of various call phrases. The ability for vocal flexibility and plasticity may allow song in white-cheeked crested gibbons to have multiple functions. This may result in inconclusive song function while conducting playback experiments. The findings of this study provide more understanding of white-cheeked crested gibbon in terms of vocal individuality and possible individual status. As vocalisations of gibbons have been used in population survey, this study may help managers assess and monitor population status of endangered white-cheeked crested gibbons in the wild.

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