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If a Bird Flies in the Forest, Does Anyone Hear It? Avian Flight Sound Cues and Hearing in Lepidoptera

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If a Bird Flies in the Forest, Does Anyone Hear it? Avian Flight Sound Cues and Hearing in Lepidoptera By Jean-Paul G. Fournier A thesis submitted to the Faculty of Graduate and Postdoctoral Affairs in partial fulfillment of the requirements for the degree of Master of Science in Biology Carleton University Ottawa, Ontario ©2011 Jean-Paul G. Fournier Library and Archives Bibliotheque et 1*1 Canada Archives Canada Published Heritage Direction du Branch Patrimoine de I'edition 395 Wellington Street 395, rue Wellington Ottawa ON K1A 0N4 Ottawa ON K1A 0N4 Canada Canada Your file Votre reference ISBN: 978-0-494-81698-1 Our file Notre reference ISBN: 978-0-494-81698-1 NOTICE: AVIS: The author has granted a non­ L'auteur a accorde une licence non exclusive exclusive license allowing Library and permettant a la Bibliotheque 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 extra its 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. 1+1 Canada Abstract Insectivorous birds exert a strong selection pressure on insects. Insects have many anti-predator mechanisms that they employ in response to avian predation. The least investigated of these mechanisms is the use of hearing. I tested the hypothesis that insects can hear the sounds produced by attacking birds. The bird flight sound cues of two insectivorous species, the black-capped chickadee, Poecile atricapillus, and the eastern phoebe, Sayornis phoebe, were found to be pulsed, broad-frequency sounds with peak frequencies in the sonic range, but also with a large ultrasonic component. Bird flight sound cues are produced at biologically relevant intensities (~75 dB at 30 cm) and are audible to the human ear from over three meters away. Physiological recordings of the moth, Trichoplusia ni, demonstrated that they are capable of hearing the bird flight cues at natural distances at which a bird would attack. This study provides the first evidence of insects detecting the passive flight cues of an avian predator. 11 Acknowledgements I would like to thank my committee members Dr. John Lewis and Dr. Jeff Dawson for their input and recommendations throughout my Master's thesis. Specifically, I would like to thank Dr. Lewis for sparking my interest in neuroscience and introducing me to the incredible field of neuroethology. If it were not for you taking the time to answer all my questions and directing me to Dr. Jayne Yack, I would not be writing these words right now. I thank Dr. Jeff Dawson for showing me what a true scientist really is. The field of neuroethology is multidisciplinary and requires a wide range of skills and techniques to ultimately explain the neural basis of behaviour. I am envious of the vast amounts of information this scientist has at the ready for any troubled "lesser" scientist. There were countless times I approached Dr. Dawson with a problem and he not only supplied me with an answer, but sat me down and gave me a complete lesson regarding the topic on his white-board. 1 really appreciate the time you took to do that for me. More than anyone, I have to thank my supervisor, Dr. Jayne Yack, for taking me on as a graduate student and allowing me to take on an amazing project that was number one on my list. I had no intentions of ever working with insects. Now I couldn't imagine a life without them. Outside of Academia, I have officially become the weird bug guy who captures moths and puts them in his pocket for "later use". It is because of you, Dr. Yack, and your lab, that I have become this person and I thank you for that. You have taught me so much, not only about insect bioacoustics, but about research and the life of a scientist. I love this life and though it is an incredible amount of work that never ends, it is meaningful and exciting. I am very grateful you saw the love of biology I have in me and allowed me to work in your lab and with great people. iii I would like to thank the entire Yack lab for showing me the ropes and helping me get started here. Specifically, I have to thank Sen Sivalinghem. First of all, he is a walking encyclopedia of all things science and more. Sen you made doing physiology all night a pleasure (not that doing physiology all night isn't a pleasure in itself) and I thank you for being a good friend. I thank Ed Bruggink for enthusiastically helping with butterfly and moth rearing. When busy or stressed there was no better way to clear my mind than to have a good conversation with you in the greenhouse. I thank Mike Jutting for help with all things electronic. I would also like to thank Jennifer Mongrain and Matt Jackson for their help at QUBS with collecting moths. I thank my family and friends for their support and for believing in me. Lastly, I would like to thank Dr. James Fullard for allowing me to use his lab and equipment at QUBS and most of all for joking with me that my project would never work. It felt fantastic proving him wrong. The short time I knew him was a pleasure. Funding for this study was provided to Dr. J. E. Yack by the Natural Sciences and Engineering Research Council and the Canadian Foundation for Innovation (CFI). Funding to J-P Fournier was provided by Carleton University. IV Table of Contents Abstract ii Acknowledgements iii Table of Contents v List of Figures vii List of Tables ix 1. General Introduction 1 1.1 Hearing in Lepidoptera 3 1.2 Thesis Objectives 9 2. Acoustic Signals and Cues Associated with Flight in Insectivorous Birds .... 11 2.1 Introduction 11 2.1.1 Active Signals and Passive Cues of Insectivorous Predators 11 2.1.2 Acoustic Cues Produced by Avian Predators 15 2.1.3 Chapter Objectives 21 2.2 Materials and Methods 22 2.2.1 Animals and Location 22 2.2.2 Setup of Audio and Video Recordings 23 2.2.3 Analysis 26 2.3 Results 30 2.3.1 General Foraging Flight Characteristics 30 2.3.2 Temporal Analysis 42 2.3.3 Spectral Analysis 44 2.3.4 Sound Level Analysis 45 2.4 Discussion 46 2.4.1 Variation in the Foraging Techniques of the Eastern Phoebe 47 2.4.2 Foraging Techniques of the Black-Capped Chickadee 49 2.4.3 Avian Flight Sound Cues 50 2.4.4 Comparison of Avian Flight Sound Cues and Signals 52 3. Are Insects Capable of Detecting Avian Flight Sound Cues? 56 3.1 Introduction 56 3.1.1 Insect Ears: Single or Multi-Functional 57 3.1.2 Could Insects be Listening for Passive Cues from Predators? 60 3.1.3 Chapter Objectives 62 3.2 Materials and Methods 64 3.2.1 Animals 64 3.2.2 Extracellular Physiology 64 3.2.3 Data Analysis 68 3.3 Results 70 3.3.1 Are Moths Capable of Hearing Bird Flight Sounds? 70 3.3.2 Bird Flight Sound Playbacks 72 3.4 Discussion 81 v 3.4.1 Are Bird Flight Sounds Relevant to Moths? 81 3.4.2 Are Bird Flight Sounds Capable of Eliciting a Behavioural Response in Moths? 83 3.4.3 Detection Distances 86 3.4.4 A2 Cell Firing Patterns - A Possible Safety Mechanism 88 4. General Conclusion 91 5. References 94 VI List of Figures 1.1 Phylogeny of the Lepidoptera 5 1.2 Location and external morphology of the tympanal organs found in Lepidoptera 7 2.1 Bird flight sound recordings set-up 25 2.2 Comparison of filtered and unfiltered eastern phoebe {Sayornis phoebe) flight sound cues 33 2.3 Eastern phoebe {Sayornis phoebe) direct attack (1) 34 2.4 Eastern phoebe {Sayornisphoebe) direct attack (2) 35 2.5 Eastern phoebe {Sayornis phoebe) "swift-like" attack 36 2.6 Eastern phoebe {Sayornisphoebe) hover attack (1) 37 2.7 Eastern phoebe {Sayornisphoebe) hover attack (2) 38 2.8 Eastern phoebe {Sayornisphoebe) aerial glean attack 39 2.9 Black-capped chickadee {Poecile atricapillus) take-off flight 40 2.10 Black-capped chickadee {Poecile atricapillus) approach and take-off flight 41 3.1 Typical sensory response to sound stimuli from extracellular nerve recordings from IIINlb's Al cell in Trichoplusia ni 70 3.2 Audiograms from extracellular nerve recordings of IIINlb's Al cell in Trichoplusia ni 71 3.3 Comparison of Trichoplusia ni audiogram to Sayornis phoebe flight sound power spectrum 72 3.4 Representative traces of the response of Trichoplusia ni's auditory receptors (Al and A2 cells) to the flight sounds produced by an approaching Sayornis phoebe 73 3.5 Measurements of Trichoplusia nfs Al cell response to single flight cycle playbacks of Sayornis phoebe 76 vii 3.6 Trichoplusia
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