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Passive Anti-Bat Defences in Nocturnal Lepidoptera Novel Wingbeat-Powered Sound Production in Deaf Microlepidoptera, and Acoustic Crypsis in Moths

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Passive Anti-Bat Defences in Nocturnal Lepidoptera Novel Wingbeat-Powered Sound Production in Deaf Microlepidoptera, and Acoustic Crypsis in Moths This electronic thesis or dissertation has been downloaded from Explore Bristol Research, http://research-information.bristol.ac.uk Author: O'Reilly, Liam J Title: Passive anti-bat defences in nocturnal Lepidoptera novel wingbeat-powered sound production in deaf microlepidoptera, and acoustic crypsis in moths General rights Access to the thesis is subject to the Creative Commons Attribution - NonCommercial-No Derivatives 4.0 International Public License. A copy of this may be found at https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode This license sets out your rights and the restrictions that apply to your access to the thesis so it is important you read this before proceeding. Take down policy Some pages of this thesis may have been removed for copyright restrictions prior to having it been deposited in Explore Bristol Research. However, if you have discovered material within the thesis that you consider to be unlawful e.g. breaches of copyright (either yours or that of a third party) or any other law, including but not limited to those relating to patent, trademark, confidentiality, data protection, obscenity, defamation, libel, then please contact [email protected] and include the following information in your message: •Your contact details •Bibliographic details for the item, including a URL •An outline nature of the complaint Your claim will be investigated and, where appropriate, the item in question will be removed from public view as soon as possible. Passive anti-bat defences in nocturnal Lepidoptera: novel wingbeat-powered sound production in deaf microlepidoptera, and acoustic crypsis in moths Liam Joseph O’Reilly A dissertation submitted to the University of Bristol in accordance with the requirements for award of the degree Doctor of Philosophy in the Faculty of Life Science October 2019 Word count: 31,343 ABSTRACT Nocturnal moths and echolocating bats have been in a co-evolutionary arms race for 65 million years. Resulting adaptations are complex, diverse, and often convergently evolved. Notable examples include anti-bat hearing providing an early warning of approaching predators, sound production to startle, warn, or jam an approaching bat, and potential acoustic camouflage afforded by the wing scales and body fur of nocturnal moths. Here, I investigate two aspects of passive anti-bat defence, wingbeat-powered anti-bat sound and acoustic camouflage. I present the first combined description and acoustic characterisation of the novel wing-embedded sound-producing structure in the microlepidopteran genus Yponomeuta, which I term the aeroelastic tymbal (AT). By investigating the life history of Yponomeuta and comparing their acoustic characteristics with those of moth sounds in the literature, I conclude that they are acoustic Müllerian mimics of the chemically defended Arctiinae. I then show that ATs likely convergently evolved 15 times in the microlepidoptera, confirming sound production from five (including Yponomeuta) of the 15 examples. Due to their acoustic characteristics being similar to known anti-bat sounds and the life histories of some taxa placing them at high risk of bat predation, I conclude that these ATs too produce anti-bat sounds. Research into potential acoustic camouflage in moths has previously focussed on small numbers of species, so I present the first species-rich, phylogenetically widespread study on the topic. Using acoustic tomography, I compare the ultrasonic retroreflection of nocturnal moths and two groups of diurnal Lepidoptera, butterflies and diurnal moths. Unlike previous work I find no differences between moths based on their diel (day-night) activity; however, moths as a whole show reduced echo intensity over all the tested frequencies for both their bodies and wings when compared to butterflies. It appears that moths are adapted for broadband acoustic camouflage against bats; whereas, butterflies are not. i DEDICATION In memory of Matthew O’Reilly ii ACKNOWLEDGEMENTS Firstly, I thank my supervisor Dr Marc Holderied, for his incredible support, guidance, and advice, but also for giving me this opportunity and believing in me. I have learnt so much from him and without his supervision I would not have achieved what I have. I must also thank Dr David Agassiz greatly. Since our chance meeting at the Bristol and District Moth Group AGM, we have made discovery after discovery. David’s advice and specimen donation has been integral to my work, and without him I would not have delved into the wonderful world of microlepidopteran acoustic research. Thank you to every member of the BASELab, you made working not feel like working, maybe because sometimes we weren’t (perhaps you should get new oscilloscope that doesn’t have a Tetris mode, Marc). Particular thanks go to Tom, Caitlin, Liam, and Dan for their moral support in my (happy) hours of need. All jesting aside, I have made great friends during my time with the BASELab, and that is in no short part down to the positive environment created by Marc and his lab members. Thank you to the Coffee and Crossword Crewe, I always looked forward to 11am. A special thank you goes to Nia; throughout this process you’ve made the rough times great and the great times greater. I do wish you wouldn’t kill my study species though, even if they might eat your clothes. Thank you to my family for their unwavering support over the years through the good and the bad. Thanks Mum, for always being there with wholesome food and a pint when I needed it most, and Dan for being a fantastic brother and an even better friend. I would also like to thank the University of Bristol Science Faculty for funding my project through the Graduate Teaching Assistant Scheme. iii AUTHOR’S DECLARATION I declare that the work in this dissertation was carried out in accordance with the requirements of the University’s Regulations and Code of Practice for Research Degree Programmes and that it has not been submitted for any other academic award. Except where indicated by specific reference in the text, the work is the candidate’s own work. Work done in collaboration with, or with the assistance of, others is indicated as such. Any views expressed in the dissertation are those of the author. SIGNED:……………………………………………………………………………… DATE:………………………………………………………………………………… iv TABLE OF CONTENTS ABSTRACT ............................................................................................................................................ I DEDICATION ....................................................................................................................................... II ACKNOWLEDGEMENTS ................................................................................................................ III AUTHOR’S DECLARATION ........................................................................................................... IV LIST OF TABLES ............................................................................................................................ VIII LIST OF FIGURES ............................................................................................................................. IX LIST OF ABBREVIATIONS ............................................................................................................. XI CHAPTER 1: GENERAL INTRODUCTION ..................................................................................... 1 1.1 THE BAT-MOTH CO-EVOLUTIONARY ARMS RACE ............................................................................ 2 1.1.1 Hearing .................................................................................................................................. 2 1.1.2 Anti-bat sound production ..................................................................................................... 4 1.1.3 Echo manipulation ................................................................................................................. 7 1.2 CHAPTER OUTLINES ........................................................................................................................ 8 CHAPTER 2: ACOUSTIC MÜLLERIAN MIMICRY IN A DEAF MOTH: ACOUSTIC CHARACTERISATION AND PROPOSED FUNCTION OF YPONOMEUTA (YPONOMEUTIDAE: LEPIDOPTERA) SOUNDS* ....................................................................... 11 2.1 ABSTRACT ...................................................................................................................................... 12 2.2 INTRODUCTION ............................................................................................................................. 12 2.2.1 The bat-moth evolutionary arms race .................................................................................. 12 2.2.2 Acoustic communication in Lepidoptera .............................................................................. 13 2.2.3 Mechanisms of sound production in Lepidoptera, with particular focus on tymbals .......... 13 2.2.4 Yponomeuta.......................................................................................................................... 15 2.2.5 Aims ..................................................................................................................................... 16 2.3 METHODS ..................................................................................................................................... 17 2.3.1 Insect selection and collection ............................................................................................
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