Mechanisms Underlying Outbreaks of Spider Mites Following Applications of Imidacloprid
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ABSTRACT Title of Dissertation: MECHANISMS UNDERLYING OUTBREAKS OF SPIDER MITES FOLLOWING APPLICATIONS OF IMIDACLOPRID. Adrianna Szczepaniec, Ph.D., 2009 Directed By: Professor Michael J. Raupp, Department of Entomology Imidacloprid is a widely used neonicotinoid insecticide with high efficacy and long residual activity, and it is frequently applied to manage insect pests in urban landscapes. Recent reports of secondary outbreaks of spider mites after imidacloprid applications have prompted research endeavors to explain the driving force of the abrupt increases in abundance of mites. In this research, I documented outbreaks of spider mites in field and greenhouse experiments, and explored the three main mechanisms that have been proposed to explain the outbreaks: elimination of natural enemies, direct stimulation of spider mite fecundity and changes in plant quality, specifically, changes in defense pathways. To this end, I examined if the outbreaks occur in field and greenhouse experiments, and tested if imidacloprid applications disrupted communities of beneficial insects and caused increased reproductive performance of spider mites in two woody ornamental systems, elm trees and boxwood shrubs. Additionally, I used a model organism, tomato plants, to address the hypothesis of altered plant defenses in plants treated with imidacloprid. I found overwhelming evidence that outbreaks of spider mites occur consistently following applications of imidacloprid in landscape and greenhouse experiments. Moreover, surveys of arthropods on elms and boxwoods showed no evidence of disruption of a key predator of spider mites that could explain the outbreaks. Importantly, I found a plant-mediated effect of imidacloprid on fecundity of spider mites, while there was no evidence that the insecticide applied directly to the mites exerted the same effect on their reproductive performance. Lastly, two genes involved in jasmonic and salicylic acid showed a differential expression in tomatoes treated with imidacloprid, indicating that it affected plants’ defense pathways in ways that could render plants more suitable for spider mites. This research demonstrated that changes in quality of plants brought about by imidacloprid seem to be the driving mechanism of secondary outbreaks of spider mites. MECHANISMS UNDERLYING OUTBREAKS OF SPIDER MITES FOLLOWING APPLICATIONS OF IMIDACLOPRID. By Adrianna Szczepaniec Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2009 Advisory Committee: Professor Michael J. Raupp, Chair Professor Pedro Barbosa Professor James Culver Associate Professor Leslie Pick Professor Raymond StLeger Associate Professor Joseph Sullivan © Copyright by Adrianna Szczepaniec 2009 Acknowledgments I would like to thank my committee members, Leslie Pick, Pedro Barbosa, Jim Culver, Ray StLeger, and Joe Sullivan for their time, insightful comments and guidance, without which this work would not have amounted to much. I am also grateful to Galen Dively for always having time to chat about statistics and helping me meander through pitfalls of statistical analysis. Galen is without a doubt one of the most amazing scientists (and statisticians) I have met, but he is foremost a great man loving what he does and putting all of his heart into it. His availability to colleagues and students alike is amazing, and it is best exemplified by the presence of his home phone number in the departmental directory. I am very grateful to Paula Shrewsbury for all her kindness, coaching and lessons in what it takes to succeed that she bestowed on me over the years. Paula has been a fantastic role model, a great colleague and a valuable mentor. I could never thank her enough for her subtle yet powerful support, and her faith in my abilities carried me through the toughest time in my studies I was fortunate to share my journey through graduate school with great lab mates in Raupp and Shrewsbury labs. I learned a lot about science, life and myself through our interactions. I am forever indebted to all of the graduate and undergraduate technicians, who have passed through the lab over the years and spent countless hours at a microscope. The work is tedious and boring, only a few are tough enough for it and we were incredibly fortunate to find some of the best summer helpers over the years. My success is partly theirs. I would also like to thank the entire Department of Entomology at the University of Maryland, professors, staff and students. I am particularly indebted to John Davidson for sharing his wisdom with me, for great lessons in life, entomology and history, for his immense support and great company on Friday afternoons. This department is truly a unique place and I am fortunate to have been a part of it. None of this however, would be possible had I not met Mike Raupp in early 2001, and had he not trusted that a young and gullible student of molecular biology could handle bugs, sticky Maryland summers and long hours at the microscope. I had nothing for the bugs before I met Mike and I would have led a sad life unaware of their beauty, puzzling habits and fascinating interactions. Mike spent a lot of time with me that first summer, teaching me about doing science and telling bug stories. It was a hard summer, but I stuck with it because the stories were just too good and learning about bugs from Mike was just too much fun. I have always considered this my formative field season, and while every summer brought a lot of fun along with hard work, there is not another time in the eight years in Mike’s lab that I will remember with greater fondness than that first summer. Mike has been a wonderful adviser, mentor and friend. He has given me independence, allowed me to fail where I needed to learn from my mistakes, and celebrated every one of my successes with enthusiasm and pride. I consider myself very lucky to have received training from one of the best entomologists and a man I respect so much. One of the most important things Mike taught me was to get out of my comfort zone and treat every challenge as an adventure, once-in-a-lifetime opportunity, and have fun with it. I will pass on this wise lesson. ii I owe great many thanks to my entire family in Poland, Germany and the U.S. In particular, my Mom, Basia Szczepaniec I thank for her enthusiasm and support, encouragement and, indirectly, teaching me not to be afraid of anything. My Grandma, Irena Stachurska, I thank for having more faith in me than I could ever deserve. I am grateful to my sisters, Ania Caponiti and Monika Szczepaniec, their husbands, Tony Caponiti and Jon Youngs, my big-little brother, Bartek Szczepaniec, and my niece and nephew Basia and Nick Caponiti for their love and support, and for keeping me well grounded. I would also like to thank JoAnn and Henry Perkins for their love, kindness and extraordinary generosity, and Kathy and Fred Caponiti for putting a roof over my head on many different occasions. I have many wonderful friends in Poland, Spain and the U.S., whose friendship and encouragement helped me along this journey. I am especially grateful to two people, who made this last year of my studies an unbelievably good year. I thank Estefania Walsh and Maik Strecker for instantly making me feel at home in their place, for many evenings with wine, good food and great music and all that we shared in the short time we had together. To all of you mentioned here and all who have influenced me and helped me achieve this: it is in part your success and I thank you. iii Table of Contents Acknowledgments............................................................................................................... ii Table of Contents ............................................................................................................... iv List of Tables ..................................................................................................................... vi List of Figures ................................................................................................................... vii Chapter 1: Abundance of a non-target pest, spider mites (Acari: Tetranychidae), increases abruptly following applications of imidacloprid to woody ornamental plants. .................. 1 Abstract ........................................................................................................................... 1 Introduction ..................................................................................................................... 2 Methods........................................................................................................................... 9 Study system: Tetranychus schoenei McGregor (Acari: Tetranychidae) and Ulmus americana Linn. (Urticales: Ulmaceae) ...................................................................... 9 Study system: Eurytetranychus buxi Garman (Acari: Tetranychidae) and Buxus sempervirens Linn. (Euphorbiales: Buxaceae) ......................................................... 11 Study system: Oligonychus ilicis McGregor (Acari: Tetranychidae) and Cotoneaster salicifolius Franch (Rosales: Rosaceae).................................................................... 13 Effect of imidacloprid applications on abundance of spider mites on elm trees and boxwood shrubs in managed landscapes .................................................................. 14 Effect of imidacloprid applications