Juvenile song learning in regent honeyeaters, Anthochaera phrygia, at Taronga Zoo, Australia. by Michelle Vecsei Thesis Presented to the Faculty of Science, Department of Biological Sciences Macquarie University, Sydney, NSW Australia in partial fulfilment of the requirements for the degree of Master of Research. 9th October 2015 1 To the examiners, The style and formatting of this thesis has been written according to the author guidelines for a journal article from the Journal of Avian Biology. Deviations from this journal style are in accordance with the Macquarie University Masters of Research thesis guidelines. Declaration I certify that the research presented in this thesis is my original work. However this research could not have been undertaken without the highly appreciated assistance of my supervisor K-lynn Smith. K-lynn Smith assisted with experimental design, data collection, data analysis, interpretation and provided feedback on the introduction, methods, and results sections, but did not have access to the discussion section. Bernard Lohr provided feedback on the discussion section. Drew Allen also assisted with the statistical analysis. This work has not been presented for a higher degree to any other university or institution, and contains no material previously published or written by any other person except where due reference is made in the text. Michelle Vecsei 2 Acknowledgments First and foremost I would like to thank my supervisor, K-lynn Smith, for all her support throughout this project and for her valuable expertise in helping me to complete it. This project would not have been possible without her. I would like to thank all the people in the Bird Department at Taronga Zoo, NSW Australia including Michael Shiels, Nick Boyle, Dave Wilkin, Katy Horsinburgh, Mark Domenici and Sonia Fisher Dobin for their cooperation needed to undertake this project and assistance in accessing aviaries. Also, thank you to Corrine Symons of Taronga Zoo for providing the title page photo. The statistical analysis of this research would not have been possible without K-lynn Smith and Drew Allen. Thank you to Bernard Lohr for valuable feedback on this project. I would also like to thank my family and friends for their constant support throughout the many stressful hours spread out over this 8 month project, especially Ron Vecsei, Kim Vecsei, James Vecsei, Sue Gumley and Zenta Staley. Lastly I want to thank the Department of Biological Sciences at Macquarie University for providing the funding for my thesis. 3 Abstract Songbirds show tremendous variation in when, how and from whom they learn their songs. Song learning may involve directly imitating another bird, known as a tutor, or may involve the recombination of song elements from multiple tutors. This study investigated song learning in a captive population of a critically endangered bird, the regent honeyeater, Anthochaera phrygia, at Taronga Zoo, NSW. The aim of this study was to add to the limited body of knowledge of song learning within the honeyeater family and provide valuable information that may assist with the regent honeyeater recovery program. Twenty-nine related and unrelated birds were recorded and the most common song types were selected for song similarity analysis. Song similarity was assessed using dynamic time warping followed by cluster analysis to determine which birds produced similar song types. The results revealed wide variation in tutor selection by juveniles, with 78% singing similar songs to multiple tutors. Song types produced included songs from tutors with which the juveniles had direct social interaction, as well as ones in which they were only able to hear. This suggests that social experience is important but not essential for song learning in this species. This study is the first to investigate song learning in regent honeyeaters. Key words: birds; regent honeyeater; Anthochaera phrygia; song learning; birdsong; tutor 4 Table of contents List of tables…………………………………………………………………………………….........6 List of figures………………………………………………………………………………….....…..7 1. INTRODUCTION 8 1.1 When do birds learn?........................................................................................8 1.2 How do birds learn?........................................................................................11 1.3 From whom do birds learn?............................................................................14 1.4 Song learning and species conservation…………………………….............17 1.5 The regent honeyeater………………………………………....................…18 1.6.1 Regent honeyeater ecology……………………………..…………......18 1.6.2 Recovery programme: captive breeding and release….…………..…..18 1.6.3 Regent honeyeater song………………………………...…………..…19 1.6 Project aims…..…………………………………………………..................20 2. METHODS 21 2.1 Study site and equipment setup………………………….………….............21 2.2 Subjects………………………………………………………………......…22 2.3 Data collection…………………………………………………...................26 2.4 Data analysis………………………………….………………………..….. 27 3. RESULTS 29 4. DISCUSSION 38 4.1 From whom do regent honeyeaters learn? ……………………………..…..38 4.1.1 learning from different tutors ……...……………………………....... 38 4.1.2 learning from multiple tutors……………………………....................39 4.1.3 Why select particular tutors? ………………………...……………….40 4.2 How do regent honeyeaters learn? …….…………………….……….....….41 4.3 When do regent honeyeaters learn? ……..……………………………........43 4.4 Implications …………………………………………………….............…..44 CONCLUSION 45 REFERENCES 46 APPENDIX 52 5 List of Tables Table 1: Adult regent honeyeaters recorded for analysis…………….………………....….23 Table 2: Juvenile regent honeyeaters recorded for analysis…………………....….……….24 Table 3: Song types produced by juvenile regent honeyeaters at Taronga Zoo….............…36 Table 4: Stage at which song types produced by the tutors were heard by the juvenile……………………………………………………………………………...............37 6 List of figures Figure 1: Satellite image of enclosures at Taronga Zoo, NSW Australia. Breeding.................................................................................................................................22 Figure 2: Timeline of juveniles’ location and acoustic environment………..……...............26 Figure 3: Pre-release enclosure equipment set up……………………………...…………...27 Figure 4: Dendogram and silhouette scores for song clusters………………..…….............29 Figure 5: Representative songs from cluster one………………………………...........……31 Figure 6: Representative songs from cluster two…………………………………..………32 Figure 7: Representative songs from cluster three……………………………….…………33 Figure 8: Representative songs from cluster four………………………………..……...…..33 Figure 9: Representative songs from cluster five………………………………...…...….…34 Figure 10: Representative songs from cluster six…………………….…………….....…….35 7 1. INTRODUCTION Many species of animals use vocalisations to communicate, but only a subset of these must learn their signals. Of these, songbirds (oscines) are one of the most intensely studied, second only to humans. More than 50 years of research on songbirds has uncovered many parallels between song learning in birds and speech learning in humans (Slater 2003). Parallels include; early sensitive learning periods, learning by imitation of an adult model, a dependence of vocal behaviour on auditory feedback and lateralisation in vocal processing brain regions (Woolley 2012). Many other parallels exist between human and songbird vocal learning, consequently song learning in birds has become the model system for exploring the evolution of vocal learning (Brainard and Doupe 2002). Further exploration into song learning in birds may subsequently expand knowledge regarding the evolution of human vocal learning. There is tremendous diversity in the song learning programs between species of birds. Differences have been clearly demonstrated in regard to when, how and from whom birds learn their songs (Brenowitz and Beecher 2005). These differences are often related to the life-history traits of the species (e.g. sedentary or migratory, territorial or colonial breeding; Catchpole and Slater 2008) but there is still controversy over the general patterns of song learning programs. Song learning has also received much attention because of its importance in avian ecology. Male song can serve many functions including individual identification, species recognition, inter-sexual signalling (e.g. female attraction; Bensch and Hasselquist 1992) and intra-sexual signalling (e.g. territorial defence; Nowicki and Searcy 2014). Song types may also vary from region to region within a species (Marler and Tamura 1964; Mundinger 1982), which can affect dispersal, mate choice and male-male interactions (see Baker and Cunningham 1985 for review). Understanding the song learning program of a specific species is hence relevant for conservation and management programs. It may be particularly important for captive breeding and release programs where the primary goal is to rear and release fully-competent individuals into the wild (Whitehead 2010). 1.1 WHEN DO BIRDS LEARN? It has long been accepted that timing plays an important role in song learning among birds. This notion arose from the observations that the majority of songbird species do not began life with the ability to sing perfectly, but rather progress along a development path over time eventually 8 producing their species specific song (Catchpole and Slater 2008). Male chaffinches (Fringilla coelebs), for example, hatch between May and July but