Native versus Exotic Grasses: The Interaction between Generalist Insect Herbivores and Their Host Plants A dissertation submitted to the Graduate School of the University of Cincinnati in partial fulfillment of the requirements for the degree of Doctor of Philosophy In the Department of Biological Sciences of the College of Arts and Sciences by Alina Avanesyan Candidate of Science Degree, Zoology Herzen State University, April 2002 Committee Chair: T. M. Culley, Ph.D. i ABSTRACT Although the interaction between native and exotic plants and their insect herbivores has been examined extensively, experimental studies on plant responses to generalist insects as well as feeding preferences of generalist insects on native versus exotic plants have provided inconsistent results. This dissertation addresses this issue by incorporating recent methodological recommendations and by exploring interactions between generalist herbivores and native and exotic plants from both the plant and insect perspectives. Using native (Andropogon gerardii and Bouteloua curtipendula) and exotic grasses (Miscanthus sinensis and Bothriochloa ischaemum) with generalist Melanoplus grasshoppers, I combined behavioral and molecular approaches to explore (1) plant resistance and tolerance to grasshopper herbivory, and (2) feeding preferences of Melanoplus grasshoppers for native and exotic plants. Overall, the results from this dissertation project have demonstrated lower resistance of exotic grasses to generalist grasshopper herbivory compared to native grasses; and similar level of plant tolerance to herbivory in native and exotic grasses. Melanoplus grasshoppers demonstrated strong feeding preferences for exotic plants in most of the behavioral experiments and under natural conditions. This suggests that exotic M. sinensis and B. ischaemum grasses with a lack of coevolutionary history with native generalist Melanoplus grasshoppers might have lower physical and chemical defenses than native grasses. Furthermore, generalist Melanoplus grasshoppers may provide biotic resistance to these exotic grasses should they invade natural areas. The results from this dissertation project have important applications for predicting the interaction between exotic plants and generalist herbivores in the introduced range, and if plant invasion has already occurred, for developing effective control plans. ii Copyright 2014 By Alina Avanesyan iii ACKNOWLEDGMENTS I thank my research advisor, Dr. Theresa Culley, for all her help, support and guidance that she provided during all my years in my doctoral program. I am very grateful to Dr. Culley that she accepted me almost without any botanical background in her lab and gave me freedom to choose any topic I would enjoy, and to go in any, even narrow entomological research direction. I thank Dr. Culley for introducing me to the world of plants and to molecular techniques which became a substantial part of my dissertation. I’ve learned a lot about field work, growing plants, genetic analysis, as well as the world of US academia – an experience which is hard to overestimate. I am very grateful to Dr. Culley’s time and help with improving my scientific writing - for numerous revisions of my manuscripts, for all her suggestions on better wording, and for all the countless corrections she made of my sometimes terrible grammar. Thank you for being a very good mentor and very helpful friend, who was always available for advice, for teaching, and for simply listening to my complaints about my life; who even drove me several days in a row to the lab and back home while my car was broken. Dr. Culley’s unconditional support, her insightful comments, and the numerous conversations we have had on my academic progress and future career plans have been the key to my success at UC. I thank Dr. Josh Gross for helping me with my research from the very early stages in my program. Dr. Gross helped me understand molecular biology since his very first days at our department - even before he became a member of my dissertation committee. I am grateful for all his help - for guiding me through primer design, for having long discussions with me, for introducing me to the DNASTAR and later to the EthoVision programs. I am very lucky to have Dr. Gross on my committee and I am thankful for his helpful suggestions on the molecular part iv of my dissertation project, for being always available to discuss my work, for his encouragement and support in my research progress. I thank Dr. Stephen Matter for introducing me to the world of data analysis, for making the R program "become my friend", for helping me with research design and the analysis of the experimental data I used in my dissertation. I am grateful to Dr. Matter for his in-depth reviews of my dissertation proposal and my revised paper. I am also grateful for our frequent discussions, which were most helpful in many ways, but especially in developing my skills of effective communication about data analysis and my research in general. I thank Dr. George Uetz for his kindness, support, and encouragement during all my years in my doctoral program. I will never forget his help - at a time in my doctoral program when I needed it most - I will be forever grateful for this. I also thank Dr. Uetz for his thoughtful comments on my dissertation proposal, for helping me with literature on animal behavior and suggestions on feeding trials with grasshoppers, as well as for allowing me to keep my grasshoppers in his lab during several experiments. The conversations we have had over the past years on my research interests and future plans have been both useful and inspiring; they helped me in my academic progress and always made me believe in my abilities and feel proud of my work. I thank Dr. Bill Lamp for being a mentor, colleague, and friend, whose continuing support and encouragement, beyond his duties as a committee member, are hard to quantify. I am forever grateful for Dr. Lamp’s trust in my abilities and providing me with access to research facilities, as well as research seminars, at the University of Maryland – one half of my dissertation simply would not have been possible without it. I am grateful to Dr. Lamp for “adopting me” as an external lab member and introducing me to his lab; I had a great time with his students at the v entomological meetings, and they became my good friends and colleagues. Our numerous discussions on my dissertation and my future in academia were encouraging and most helpful. I am especially grateful for the opportunity to co-organize and co-moderate the symposium with Dr. Lamp at the upcoming ESA meeting - thank you for this invaluable experience! But, most importantly, thank you for believing in me. There are many people besides my committee whom I would like to thank for helping me in my research, which has led to this dissertation, and, ultimately, to my Ph.D. The following list is, most likely, incomplete – and I apologize to those whom I have not mentioned. I thank Tim Ellis for all his help during the past two field seasons – establishing the plot for my experiments at the Western Maryland Research and Education Center, watering my plants, advice on planting and taking care of my plants. I’ve learned a lot about agricultural techniques from him, and I’ve never felt alone while commuting and working at my distant plot in Maryland. I enjoyed working with Tim, who became my good friend. I thank Angelo Randaci for his help with planting seeds, watering my plants and transferring hundreds of them from pots to pots. We had many discussions on plant cultivars and methods for removing weeds, that were very helpful to me. I thank Roger Ruff for establishing the plot for my experiments at the University of Cincinnati field station and for being always available there to help me with watering or mowing. I thank my fellow Ph.D. students and lab mates - Sunita, Kim, Allison, Susan, Yamini, Megan, Eric - for their help, their friendship and support. My special thanks go to my parents Dzhaneta and Vachagan Avanesyan, and to my brother, Artem Avanesyan, for their love, support, and believing in me during these years and all my life. vi I am infinitely grateful to my husband Sergey Golitsynskiy. Without his patience, advice, and constant support this dissertation would not have been be possible. He has been the greatest friend I have ever had, who while finishing his own dissertation and doing crazy weekly commutes to Maryland and then to Iowa, was always there for me. vii TABLE OF CONTENTS Abstract ........................................................................................................................................... ii Acknowledgments ..........................................................................................................................iv List of Tables ................................................................................................................................. ix List of Figures ................................................................................................................................ xi Chapter 1: General introduction ......................................................................................................1 Chapter 2: Resistance of native and exotic grasses to herbivory by nymph Melanoplus grasshoppers .................................................................................................................................. 10 Chapter 3: Comparison of native and exotic grasses in their