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Vocal Communication in Zebra Finches: a Focused Description of Pair Vocal Activity

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Vocal Communication in Zebra Finches: a Focused Description of Pair Vocal Activity Vocal communication in zebra finches: a focused description of pair vocal activity Dissertation Fakultät für Biologie Ludwig-Maximilians-Universität München durchgeführt am Max-Planck-Institut für Ornithologie Seewiesen vorgelegt von Pietro Bruno D’Amelio München, 2018 Erstgutachter: Prof. Dr. Manfred Gahr Zweitgutachter: Prof. Dr. Niels Dingemanse Eingereicht am: 06.03.2018 Tag der mündlichen Prüfung: 08.05.2018 Diese Dissertation wurde unter der Leitung von Prof. Dr. Manfred Gahr und Dr. Andries ter Maat angefertigt. i ii Table of Contents Summary ...................................................................................................................................................... iv General Introduction ..................................................................................................................................... 1 Vocal communication ................................................................................................................................ 1 Methodological challenges and how they were approached .................................................................... 8 Vocal individual recognition ................................................................................................................... 10 Pair communication ................................................................................................................................ 11 References ................................................................................................................................................... 14 Chapter 1 - A minimum-impact, flexible tool to study vocal communication of small animals with precise individual-level resolution .......................................................................................................................... 20 Chapter 2 - Individual recognition of opposite sex vocalizations in the zebra finch .................................. 37 Chapter 3 - Vocal exchanges during pair formation and maintenance in the zebra finch (Taeniopygia guttata) ...................................................................................................................................................... 723 Chapter 4 - Synchronized recording of position and vocalization helps to understand the function of bird vocalizations 94 General discussion .................................................................................................................................... 117 New tools for old questions: the importance and challenge of quantifying individual vocal behavior . 118 Individuality in zebra finch unlearned calls and the importance of timing ........................................... 120 Consistency and flexibility of calling interactions ................................................................................. 123 Partners’ relative spatial position clarifies zebra finch repertoire ....................................................... 125 The study of calls in birds: status, and prospects .................................................................................. 126 Overall conclusions ............................................................................................................................... 130 References ................................................................................................................................................. 131 Author contributions ................................................................................................................................. 141 Acknowledgements ................................................................................................................................... 142 Curriculum vitae ....................................................................................................................................... 144 Statutory declaration and statement .......................................................................................................... 147 iii Summary Vocal communication is the primary mode of signaling in a wide variety of species and commonly plays a decisive role in reproduction and survival of both the sender and the receiver. In birds, vocal signals have evolved to be astonishingly diverse, with thousands of different vocalizations used for highly disparate functions. Some vocalizations are loud and broadcast to reach the greatest possible number of receivers; others are barely audible and directed to a specific individual, often a mate. The function of each element of a bird’s vocal repertoire is not always simple to interpret and the same signal can have multiple functions. To understand the role and influence of each vocal signal of a species, and thus the principles of vocal communication, we need to precisely quantify not only each sender vocalization, but also the context of its emission. In my thesis, I used the zebra Finch (Taeniopygia guttata) as a model species to study the vocal communication of birds. I focused on pair communication as the smallest functional unit of a group. I considered all the vocal signals emitted but I focused my attention on the calls: of which thousands are emitted daily. These vocalizations are unlearned, very soft (low amplitude), very short (>100 milliseconds) and very similar among different individuals. Therefore, my colleagues and I developed and evaluated a method to individually record small animals (chapter 1). I describe a device, miniaturized backpack microphones, able to record birds singularly and the tools needed to record several individuals synchronously. This tool can be employed in many experimental settings to quantify the vocal behavior of multiple individuals with only a transient effect on their behavior and capable of capturing the softest of their vocalizations. I first used this tool to verify that birds were able to tell who was calling (chapter 2). I found that even the short unlearned calls have an individual vocal signature and birds are particularly eager to answer their mate’s vocalizations. Then, I studied the development of, and signals used in within pair communication (chapter 3). I described in detail the timed vocal exchanges of paired zebra finches; I observed that their antiphonal calling resembled duets. Moreover, I found that pair communication iv develops along with pair formation, so that by the time the pair is formed the number of calls used to answer each other is similar between partners. Finally, I aimed to discover when the calling interactions were taking place to have insights into the functions of these short, soft, unlearned vocalizations of zebra finches. To do so, I assembled a simple method to track automatically the position of the birds while recording their vocalizations. I was then able to describe how the relative positions of partners within a pair influenced the probability of calling (chapter 4), which revealed the precise meaning of a specific vocalization. This experiment also shows the accuracy and precision of our behavioral quantification, marking an important step towards new methods to automatically generate ethograms. Altogether, my dissertation contributes to our understanding of bird vocalization by determining that the continuous calling of zebra finches is not just “a soft background hum”, but rather the foundation of organized vocal networks. v General Introduction Vocal communication Understanding communication is part of studying how animals make decisions, which can be a conscious process or not (Schmidt, Dall, & van Gils, 2010). Focusing on the vocal channel, I developed and used tools to accurately describe bird behavior, quantify their decisions, and infer communicative principles. Vocal communication is a widespread form of conveying messages. It is rapid, works over short to medium distances, and does not leave tracks (Bradbury & Vehrencamp, 1998). It is used by many taxa across the animal kingdom, primarily as a signal to inform and modify the decision process of receivers. For human listeners, birds hold a special place among animals. This is due to several practical reasons besides the aesthetic and euphonious fascination: they are common around us, often extremely chatty, and some species are easy to raise and manipulate. What also makes birds special for us is that they share with humans the ability to learn their vocalizations (Barrington, 1773; Doupe & Kuhl, 1999). As a result, birds became the most common model to study vocal communication and learning (Brainard & Doupe, 2013). Vocal communication studies have mainly focused on compiling and understanding vocal repertoires (Fischer, Wadewitz, & Hammerschmidt, 2017) and, more recently, constructing vocally defined social networks (Gill, Goymann, Ter Maat, & Gahr, 2015). Vocal learning is the capability to modify the spectral and temporal features of vocalizations using a template, and is quite rare in the animal kingdom (Petkov & Jarvis, 2012). Vocal learning is a relatively rare trait even in birds; it has evolved only 2 or 3 times; in the order of hummingbirds (Apodiformes) (Baptista & Schuchmann, 1990) and in the progenitor of parrots (Psittaciformes) and passerines (Passeriformes) (Suh et al., 2011). The independent evolution of vocal learning in these two clades is also possible (Zhang et al., 2014). Thus, only a few of the circa 20 (depending on the different taxonomies) orders of birds learn vocalizations. However, all birds communicate vocally. 1| General Introduction
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