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Sound Production in Bombycoidea Caterpillars: a Comparative Study of Taxonomic Diversity, Mechanisms and Function

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Sound Production in Bombycoidea Caterpillars: a Comparative Study of Taxonomic Diversity, Mechanisms and Function Sound Production in Bombycoidea Caterpillars: A Comparative Study of Taxonomic Diversity, Mechanisms and Function By Veronica Bura A dissertation submitted to the Faculty of Graduate Studies and Research in partial fulfillment of the requirements for the degree of Master of Science in Biology Carleton University Ottawa, Ontario ©2010 Veronica Bura Library and Archives Bibliothfeque et 1*1 Canada Archives Canada Published Heritage Direction du Branch Patrimoine de I'gdition 395 Wellington Street 395, rue Wellington OttawaONK1A0N4 OttawaONK1A0N4 Canada Canada Your file Votre reference ISBN: 978-0-494-71552-9 Our file Notre reference ISBN: 978-0-494-71552-9 NOTICE: AVIS: The author has granted a non­ L'auteur a accorde une licence non exclusive exclusive license allowing Library and permettant a la Bibliothdque et Archives Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par telecommunication ou par I'lnternet, preter, telecommunication or on the Internet, distribuer et vendre des theses partout dans le loan, distribute and sell theses monde, a des fins commerciales ou autres, sur worldwide, for commercial or non­ support microforme, papier, electronique et/ou commercial purposes, in microform, autres formats. paper, electronic and/or any other formats. The author retains copyright L'auteur conserve la propriete du droit d'auteur ownership and moral rights in this et des droits moraux qui protege cette these. Ni thesis. Neither the thesis nor la these ni des extraits substantiels de celle-ci substantial extracts from it may be ne doivent etre imprimes ou autrement printed or otherwise reproduced reproduits sans son autorisation. without the author's permission. In compliance with the Canadian Conformement a la loi canadienne sur la Privacy Act some supporting forms protection de la vie privee, quelques may have been removed from this formulaires secondaires ont ete enleves de thesis. cette these. While these forms may be included Bien que ces formulaires aient inclus dans in the document page count, their la pagination, il n'y aura aucun contenu removal does not represent any loss manquant. of content from the thesis. •+• Canada ABSTRACT Anti-predator adaptations have been widely studied in caterpillars, but the majority of studies focus on visually communicated defences. In this thesis I introduce defensive airborne sound production in Bombycoidea caterpillars by documenting the taxonomic diversity and, where possible, function and mechanisms. Fifteen of 42 species from two families and five subfamilies produced sound, providing evidence for both convergent and divergent evolution within the superfamily. Four different mechanisms are reported; mandible clicking, mandible stridulation, whistling through spiracles, and possibly, air expulsion through the buccal cavity. Based on experimental trials with artificial and live predator attacks, I conclude that sounds function to startle and/or warn predators of a chemical defence or general unprofitability. Sound characteristics and preliminary predator trials suggest these defensive sounds are directed primarily at avian predators and possibly bats and rodents. Hypotheses proposing evolutionary origins of sound production are presented based on comparative analysis of signal characteristics and associated defensive behaviours. ACKNOWLEDGEMENTS I would like to start by thanking past and present members of the Yack lab, the working environment created by everyone's presence is one of the best that I've ever had the pleasure of sharing in. More specifically I'd like to thank Jackie Scott and Sarah Matheson, both of whom started out with different names and helped me through days, and sentences, I thought I would never get through. Thank you for Family Feud, arts and crafts and for taking care of my caterpillars when I was away. To Katie Lucas for checking all my emails and introducing me to sites I still use when procrastinating. Thanks to AJ Fleming (Don Alan!), who helped me with everything from collecting data to acting as a personal translator in Costa Rica, and for always asking the wrong questions at the wrong times. A big thank-you also goes to everyone who's ever given me moths or caterpillars, especially Jenn Mongrain for all her intensive (and sometimes fear- ridden) labour last summer. I am also very grateful to Dr. Dan Janzen and Winnie Hallwachs and everyone at the Area de Conservation Guanacaste in Costa Rica for letting me come down and "torture" all the big caterpillars they worked so hard to find. Thank you for the high-speed drives down long winding roads and lending your expertise to my study. Thank you to Dr. Paul Martin and Vanya Rohwer for allowing me access to their yellow warblers and the facilities that housed them. And of course, thank you to Sarah Davis for investigating the first clicking caterpillar and starting this wonderful project. I would also like to extend my gratitude to the members of my committee, Dr. Jean-Francis Landry and Dr. Tom Sherratt, for their comments and input, as well as for reading the tome that is my thesis. Thank you also to Dr. Jeff Dawson for answering any ii questions I had and for lending me the use of his tools as needed. Last, but never least, to Miss Canada, Dr. Jayne Yack, for getting me to do all of this in the first place. Thank you for welcoming me into your lab and then keeping me there, for challenging me and making things interesting, for never pretending not to be in your office (that I know of) and for ensuring that a caterpillar will never get past me without getting its bum pinched. Finally I'd like to thank my family; to my parents for agreeing that it wasn't a bad idea to become a student again and to my sister for always wanting to help, but being too artsy to take advantage of. My most heartfelt thanks go to Snuffaluffagus, for supporting me no matter what, for putting up with all my drama while I was writing and for taking care of all the housework that I've been neglecting. And also to the cats, for waking me up in the mornings and making sure to lay on whatever I needed most. Funding for this study was provided to Dr. J. E. Yack by the Natural Sciences and Engineering Research Council (NSERC) and the Canadian Foundation for Innovation (CFI). Funding to V. Bura was provided by Carleton University, the David and Rachel Epstein Foundation and NSERC (CGS-M). iii TABLE OF CONTENTS ABSTRACT i ACKNOWLEDGEMENTS ii TABLE OF CONTENTS iv LIST OF TABLES vii LIST OF FIGURES viii CHAPTER 1: General Introduction 1 Acoustic communication in caterpillars 2 Defensive sounds in insects 5 Thesis Objectives 11 CHAPTER 2: Defensive clicking in the tobacco hornworm, Manduca sexta (Bombycoidea: Sphingidae) 12 2.1 Introduction 13 2.2 Methods 14 Animals 14 Sound recordings and analysis 16 Attack experiments 18 2.3 Results 19 General behavioural observations 19 Sound characteristics 20 Sound production mechanism 20 Attack trials 24 2.4 Discussion 27 CHAPTER 3: Acoustic stridulatory signals in caterpillars of the great peacock moth (Saturnia pyri: Bombyoidea, Saturniidae) 32 3.1 Introduction 33 3.2 Methods 34 Animals 34 Sound production mechanism 34 Sound recording and analysis 35 Attack trials 36 3.3 Results 37 Sound production mechanism 37 Sound characteristics 39 Attack trials 41 3.4 Discussion 43 CHAPTER 4: Defensive whistles of the Walnut sphinx caterpillar, Amorphajuglandis (Bomycoidea: Sphingidae) 46 4.1 Introduction 47 4.2 Methods 48 Animals 48 iv Sound recordings and analysis 48 Sound production mechanism 50 Anatomy of spiracles 51 Attack trials 52 4.3 Results 53 Sound characteristics 53 Sound production mechanism 57 Spiracle anatomy 57 Attack experiments 60 4.4 Discussion 63 CHAPTER 5: Sound Production in Caterpillars: A comparative survey of defensive behaviours in Bombycoidea and other large caterpillars 69 5.1 General Introduction 70 5.2 PART A: Survey of Sound Production and Associated Behaviours 72 5.2.1 Introduction 72 5.2.2 Methods 73 Animals 73 Attack experiments 77 Sound recording and analysis 78 Head capsule and mandible morphology 79 5.2.3 Results and Discussion 81 Species accounts 81 Defensive behaviours 82 Mandible morphology 90 Sheets FAMILY: BOMBYCIDAE 92 SUBFAMILY: APATELODINAE 92 FAMILY: SATURNIIDAE 95 SUBFAMILY: CERATOCAMPINAE 95 SUBFAMILY: HEMILEUCINAE 112 SUBFAMILY: SATURNIINAE 118 FAMILY: SPHINGIDAE. 138 SUBFAMILY: SMERINTHINAE 138 SUBFAMILY: SPHINGINAE 155 SUBFAMILY: MACROGLOSSINAE 181 OUTGROUPS 209 SUPERFAMILY: LASIOCAMPOIDEA 209 FAMILY: LASIOCAMPIDAE 209 SUPERFAMILY: NOCTUOIDEA 211 FAMILY: NOCTUIDAE 211 FAMILY: NOTODONTIDAE 215 FAMILY: NYMPHALIDAE. 221 FAMILY: HESPERIIDAE 229 Taxonomic distribution of airborne sound production in Lepidoptera caterpillars 235 v 5.3 PART B: Evolutionary Origins of Communication signals 241 5.3.1 Introduction 241 5.3.2 Methods 243 5.3.3 Results and Discussion 244 Proposed origins of mandible signals 244 Proposed origins of spiracular sounds 245 Proposed origins of rasping sounds 248 5.4 PART C: Why do Some Caterpillars use Defensive Sounds? 252 5.4.1 Introduction 252 5.4.2 Results and Discussion 253 What is the function of airborne sound production in caterpillars? 253 Why don't all caterpillars make defensive sounds? 264 GENERAL CONCLUSIONS 271 REFERENCES 273 APPENDIX 1 285 vi LIST OF TABLES 1.1 Summary table of current knowledge of sound production in Bombycoidea caterpillars 4 4.1 Spectral and temporal characteristics of sounds in A. juglandis 56 5.1 List of species examined in the survey 74 5.2 Summary of defensive behaviours and morphological features 231 5.3 Spectral and temporal characteristics of defensive sounds 234 5.4 Specific behaviours observed in Bombycoidea caterpillars 254 5.5 Combinations of behaviours observed in Bombycoidea caterpillars 255 vii LIST OF FIGURES 2.1 A fifth instar Manduca sexta larva 15 2.2 Behavioural response to an attack 21 2.3 Sounds made by M.
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