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Aerial Warfare Between Bats and Moths: Efficacy of Acoustic Aposematism, Flight Behaviors of Unpalatable Prey, and Two Novel Anti-Bat Strategies

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Aerial Warfare Between Bats and Moths: Efficacy of Acoustic Aposematism, Flight Behaviors of Unpalatable Prey, and Two Novel Anti-Bat Strategies AERIAL WARFARE BETWEEN BATS AND MOTHS: EFFICACY OF ACOUSTIC APOSEMATISM, FLIGHT BEHAVIORS OF UNPALATABLE PREY, AND TWO NOVEL ANTI-BAT STRATEGIES BY NICOLAS J. DOWDY A Dissertation Submitted to the Graduate Faculty of WAKE FOREST UNIVERSITY GRADUATE SCHOOL OF ARTS AND SCIENCES in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY Biology May 2017 Winston-Salem, North Carolina Approved By: William E. Conner, Ph.D., Advisor Jennifer M. Zaspel, Ph.D., Chair T. Michael Anderson, Ph.D. Susan E. Fahrbach, Ph.D. Kathy A. Kron, Ph.D. ACKNOWLEDGMENTS “If I have seen further than others, it is by standing upon the shoulders of giants.” — Sir Isaac Newton Science is a collaborative effort. Progress is made by building on the discoveries and hard work of those who have come before us. I believe this extends both to colleagues as well as to family and friends. Our triumphs are their triumphs. I hope to acknowledge some of the people who have influenced me and my dissertation, either directly or indirectly, throughout the execution of this work. First, I must thank my advisor and mentor, Dr. William E. Conner. He has painstakingly cultivated my growth as a scientist. One of my greatest joys was knowing that we were kindred spirits, fascinated by the same natural phenomenon. I knew with certainty there was no better person from which I could learn. I will forever be in his debt for the knowledge and opportunities he has given me. My dissertation committee members also greatly shaped me and this work. I thank Drs. T. Michael Anderson, Susan E. Fahrbach, Kathy A. Kron, and Jennifer M. Zaspel for their time, patience, and insight. I must especially thank Dr. Zaspel for her strong support of my research. I always felt like I had a second doctoral mentor in her. I am grateful for the opportunity to work more closely with her in the future. Jeff Muday and Drs. Glen Marrs, Marcus Wright, and Kim Nelson helped me tremendously. They graciously imparted to me knowledge of computing, microscopy, and chemistry. Without them much of my work would not have been possible. ii To me, lab mates are a special sort of family. They understand your research problems more deeply than anyone else because they have been through it themselves. I am so deeply indebted to my academic brother, Dr. Aaron J. Corcoran. He is one of the most caring, thoughtful, and intelligent people I know. He continues to be a model that I strive to emulate. I did not directly overlap with Drs. Jesse Barber and Nickolay Hristov during my time in the Conner Lab, however without their ground-breaking work on acoustic aposematism in tiger moths, I would not be where I am today. I thank them for that and hope we can work together more closely in the future. Over the course of my dissertation I had the great pleasure of working with 16 Wake Forest University undergraduate students, some multiple times. To each of you I express my deepest thanks. My goal was to enrich your lives by exposing you to science and how it is conducted, but I also found that each of you enriched my life and work. I have to extend special thanks to Drs. Santiago Burneo, Jim Miller, Lee Dyer, Thomas Walla, and Harold Greeney as well as to José Simbaña and my Ecuadorian field assistants Andrea Vallejo, Andrea Vargas, and José Tinajero. Without them my South American studies would not have been possible. My family and friends have also had a strong effect on me throughout this process. I thank all of them, especially my mother and father for their continued love and support of everything I do. Above all, I thank my wife, Megan N. Starkey, for her unconditional love, care, support, friendship, and for the many sacrifices she has made and continues to make for me so that I can follow my passions. iii I could add so many more names to this list and say so much more about each person included. I thank everyone for everything you have done or will do for me. It is greatly appreciated and never forgotten. Thank you! Finally, I hope this work will act to support the scientific endeavors of future scientists. I dedicate this work to them. May they stand upon this work and see further. iv TABLE OF CONTENTS ACKNOWLEDGEMENTS .............................................................................................. ii LIST OF TABLES ........................................................................................................... ix LIST OF FIGURES ......................................................................................................... xi ABSTRACT ................................................................................................................... xiv CHAPTER I ...................................................................................................................... 1 Acoustic aposematism and evasive action in select chemically defended Arctiine (Lepidoptera: Erebidae) species: nonchalant or not? Published in PLOS ONE (2016) ABSTRACT ................................................................................................... 3 INTRODUCTION ......................................................................................... 4 RESULTS ...................................................................................................... 5 DISCUSSION .............................................................................................. 12 METHODS .................................................................................................. 17 ACKNOWLEDGEMENTS ......................................................................... 27 REFERENCES............................................................................................. 28 CHAPTER II ................................................................................................................... 50 Nonchalant flight behavior in tiger moths (Erebidae: Arctiinae) is correlated with unpalatability v ABSTRACT ................................................................................................. 52 INTRODUCTION ....................................................................................... 53 METHODS .................................................................................................. 54 RESULTS .................................................................................................... 57 DISCUSSION .............................................................................................. 58 CONCLUSION ............................................................................................ 60 ACKNOWLEDGEMENTS ......................................................................... 60 REFERENCES............................................................................................. 61 CHAPTER III ................................................................................................................. 69 Can characteristics of tiger moth (Erebidae: Arctiinae) anti-bat sounds be predicted from morphology? ABSTRACT ................................................................................................. 73 INTRODUCTION ....................................................................................... 74 METHODS .................................................................................................. 79 RESULTS .................................................................................................... 90 DISCUSSION .............................................................................................. 95 CONCLUSIONS ........................................................................................ 103 ACKNOWLEDGEMENTS ....................................................................... 104 REFERENCES........................................................................................... 105 vi CHAPTER IV ............................................................................................................... 136 Novel use of moth flocculent as a defense against bat predation ABSTRACT ............................................................................................... 138 INTRODUCTION ..................................................................................... 139 METHODS ................................................................................................ 139 RESULTS .................................................................................................. 149 DISCUSSION ............................................................................................ 153 ACKNOWLEDGEMENTS ....................................................................... 156 REFERENCES........................................................................................... 157 CHAPTER V ................................................................................................................ 171 A novel anti-bat function of pheromone disseminating structures in the tiger moth Eucereon zizana (Lepidoptera: Erebidae: Arctiinae) ABSTRACT ............................................................................................... 173 INTRODUCTION ..................................................................................... 174 METHODS ................................................................................................ 175 RESULTS .................................................................................................. 180 DISCUSSION ...........................................................................................
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