City University of New York (CUNY) CUNY Academic Works All Dissertations, Theses, and Capstone Projects Dissertations, Theses, and Capstone Projects 2-2018 Social Influences on Songbird Behavior: From Song Learning to Motion Coordination Iva Ljubičić The Graduate Center, City University of New York How does access to this work benefit ou?y Let us know! More information about this work at: https://academicworks.cuny.edu/gc_etds/2521 Discover additional works at: https://academicworks.cuny.edu This work is made publicly available by the City University of New York (CUNY). Contact: [email protected] Social Influences on Songbird Behavior: From Song Learning to Motion Coordination By Iva Ljubičić A dissertation submitted to the Graduate Faculty in Biology in partial fulfillment of the requirements for the degree of Doctor of Philosophy, The City University of New York 2018 © 2018 Iva Ljubičić All Rights Reserved ii Social Influences on Songbird Behavior: From Song Learning to Motion Coordination By Iva Ljubicic This manuscript has been read and accepted for the Graduate Faculty in Biology in satisfaction of the dissertation requirement for the degree of Doctor of Philosophy. __________________________ ______________________________ Date Chair of Examining Committee Dr. Ofer Tchernichovski, Hunter College __________________________ ______________________________ Date Executive Officer Dr. Cathy Savage-Dunn ______________________________ Dr. Mark Hauber, Hunter College ______________________________ Dr. David Lahti, Queens College ______________________________ Dr. Carolyn Pytte, Queens College ______________________________ Dr. Sébastien Derégnaucourt, Paris West University The City University of New York iii Social Influences on Songbird Behavior: From Song Learning to Motion Coordination Iva Ljubičić Advisor: Dr. Ofer Tchernichovski Abstract Social animals learn during development how to integrate successfully into their group. How do social interactions combine to maintain group cohesion? We first review how social environments can influence the development of vocal learners, such as songbirds and humans (Chapter 1). To bypass the complexity of natural social interactions and gain experimental control, we developed Virtual Social Environments, surrounding the bird with videos of manipulated playbacks. This way we were able to design sensory and social scenarios and test how social zebra finches adjust their behavior (Chapters 2 & 3). A serious challenge is that the color output of a video monitor does not match the color vision of zebra finches. To minimize chromatic distortion, we eliminated all of the colors from the videos, except in the beak and cheeks where we superimposed colors that match the sensitivity of zebra finch photoreceptors (Chapter 2). Birds strongly preferred to watch these manipulated ‘bird appropriate’ videos. We also designed Virtual Social Environments for assessing how observing movement patterns might affect behavior in real-time (Chapter 3). We found that presenting birds with manipulated movement patterns of virtual males promptly affects the mobility of birds watching the videos: birds move more when virtual males increase their movements, and they decrease their iv movements and ‘cuddle’ next to virtual males that stop moving. These results suggest that individuals adjust their activity levels to the statistical patterns of observed conspecific movements, which can explain zebra finch group cohesion. Finally, we studied the song development process in the absence of social input to determine how intrinsic biases and external stimuli shape song from undifferentiated syllables into well-defined categorical signals of adult song (Chapter 4). Do juveniles learn the statistics of early sub-song to guide vocal development? We trained juvenile zebra finches with playbacks of their own, highly variable, developing song and showed that these self-tutored birds developed distinct syllable types (categories) as fast as birds that were trained with a categorical, adult song template. Therefore, the statistical structure of early input seems to have no bearing on the development of phonetic categories. Overall, our results uncover social forces that influence individual behaviors, from motion coordination to vocal development, which have implications for how group structures and vocal culture are maintained. v Acknowledgements I am so grateful to the many people who made this work possible. My biggest thanks go to my advisor, Ofer Tchernichovski, for encouraging the never-ending lab discussions about science, politics, philosophy and art. Thank you for the light-hearted atmosphere that allowed us to make fun of you, and each other. I am so glad that your hiring policy is “intelligence is overrated,” which guaranteed that I would be surrounded by like-minded people. I could not have survived the PhD process without the support from you and the lab-family you built. I know that when I think back on the years in the lab, I won’t remember the disappointments and frustrations, but will instead think fondly of the laughter and good times we had whenever we were together. Thank you to my Doctoral Committee for your time and expertise in “Bird Science” – Drs. Mark Hauber, David Lahti, Carolyn Pytte and Sébastien Derégnaucourt. Your feedback was invaluable in shaping my thesis. Special thanks go to my collaborators Drs. Olga Fehér and James Gordon. Olga was the first person I met when I visited the lab, and her vehement arguments with Ofer during lunchtime inspired me to join his lab. I learned a lot from you, and I am glad we got to work on experiments together. Jim, thank you for lending us your spectrophotometer, and for always making yourself available to (patiently) answer my questions. Thank you to the staff and faculty at the Graduate Center and Hunter College for their support over the years. I am especially grateful to the Psychology Department at Hunter for providing me with the opportunity to teach undergraduates who were eager to learn about human and animal behavior. I am deeply grateful to the many friends in and out of academia who supported me and kept me sane: Kristel Shu Bassett, Anisa Dhimarko, Jill Guzzo, Julia Hyland Bruno, Dina Lipkind, Martina Ljubičić, Petra Ljubičić, Alesandra Nahodil, M. Aaron Owen, Christina Roeske, and many, many others along the way. Thank you to my parents, who supported me in all my endeavors, even when I made the “weird” decision to study animal behavior. Finally, thank you to the two little zebra finches that were always looking over my shoulder while I worked on my thesis: you were a daily source of joy over the last few years. vi Table of Contents Abstract iv Acknowledgements vi List of Figures viii List of Tables ix Chapter 1 Introduction: Social Influences on Vocal Development 1 Chapter 2 Designing Virtual Environments to Study Social Influences on Behavior 11 Chapter 3 Zebra Finches Adjust their Activity Levels to Match Mobility Patterns of Virtual Males 27 Chapter 4 Statistical Learning in Songbirds: From Self-Tutoring to Song Culture 45 Appendix Song Learning from Virtual Tutors: A Pilot Study 63 References 71 vii List of Figures Figure 1.1 A schematic of the complexity of possible social interactions throughout vocal development............................................................... 4 Figure 1.2 A schematic of a Virtual Social Environment to test how developing songbirds use statistical rules to guide vocal learning........................... 10 Figure 2.1 Spectral sensitivity of individual cone photoreceptors of the zebra finch and phosphor radiance spectra of the tablets................................ 17 Figure 2.2 Video stimuli manipulations................................................................. 18 Figure 2.3 Comparison of cheek and beak reflectance between live males and video males............................................................................................ 19 Figure 2.4 Relative cone outputs for red beaks and orange cheeks........................ 21 Figure 2.5 Results of video preference tests........................................................... 24 Figure 3.1 Schematic of the arena setup................................................................. 31 Figure 3.2 Movement speeds of birds across the two configurations..................... 35 Figure 3.3 The Introduction Effect......................................................................... 36 Figure 3.4 Comparison of movement ratios between time points of high and low disparity between speeds....................................................................... 37 Figure 3.5 Birds dynamically adjust their activity levels over time....................... 39 Figure 3.6 Scatterplots of the combined movements across all birds where video speeds are decreasing............................................................................ 40 Figure 3.7 Scatterplots of the combined movements across all birds where video speeds are increasing............................................................................. 41 Figure 3.8 Heatmaps reveal that birds tend to settle in front of tablets with males when the video is a static image............................................................ 42 Figure 4.1 Transition from continuous to categorical signal over development.... 48 Figure 4.2 Self-tutoring in zebra finches................................................................ 50 Figure 4.3 Adult songs of isolate and self-tutored sibling pairs............................