Managing Halyomorpha halys: Effects of cold tolerance, insecticides, and linguistic uncertainty A Dissertation SUBMITTED TO THE FACULTY OF UNIVERSITY OF MINNESOTA BY Theresa Marie Cira IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Dr. William D. Hutchison (advisor) June 2017 © Theresa M. Cira 2017 Copyright Permission Chapter 1 has previously been published (citation: Cira, TM, RC Venette, J Aigner, T Kuhar, DE Mullins, SE Gabbert, WD Hutchison. 2016. Cold tolerance of Halyomorpha halys (Hemiptera: Pentatomidae) across geographic and temporal scales. Environ Entomol 45:479-483). Permission for use here granted by first author Theresa M. Cira and publisher Oxford University Press. Chapter 3 has previously been published (citation: Cira, TM, EC Burkness, RL Koch, WD Hutchison. 2017. Halyomorpha halys mortality and sublethal feeding effects following insecticide exposure. J Pest Sci doi: 10.1007/s10340-017-0871-y). Permission for use here granted by first author Theresa M. Cira and publisher Springer-Verlag Berlin Heidelberg. i Acknowledgements Completing this dissertation was only possible through the generous support, mentorship, and encouragement I have received from a great many people. I am deeply grateful to all who have provided their time and expertise, and to the organizations which funded my work. My adviser, Dr. Bill Hutchison has afforded extensive opportunities for me to learn and grow as an entomologist, scientist, and person. I sincerely appreciate all he has done for me and his genuine acceptance of my path through graduate school. I have relied heavily on the expertise of my committee members, Dr. Bob Koch, Dr. Kathy Quick, and Dr. Rob Venette. It has been a pleasure to get to work closely with all of them, and their feedback has been invaluable in this process. Eric Burkness has been an essential and irreplaceable teacher, who has provided level-headed answers to the diverse and endless stream of question I have asked him. I would also like to acknowledge the profound impact that my early entomological mentors, Su Borkin and Dr. Dan Young have had on my life’s trajectory. Su’s mentorship and advice, starting when I was in high school, and has continued to inspire and guide me. I didn’t know I could be an entomologist until I started working for Su at the Milwaukee Public Museum. As an undergraduate at UW Madison, Dan further encouraged my pursuit of entomology. His infectious enthusiasm and deep knowledge of the field were a steady source of motivation, and the personalized advising Dan provided, kept me on the entomological track when I was being pulled in so many other ways. I am also thankful for financial support from the following sources: USDA/MDA Specialty Crop Block grant, McLaughlin Gormley King Corp., Fdn. Graduate Student Fellowship, University of Minnesota Agricultural Experiment Station, Minnesota’s Discovery, Research, and InnoVation Economy (MnDRIVE) Global Food Ventures Graduate Student Fellowship, Interdisciplinary Center for the Study of Global Change Global Food Security Fellowship, University of Minnesota Graduate School Doctoral Dissertation Fellowship, University of Minnesota Graduate School Dissertation Travel Grant, and the Hueg-Harrison Fellowship. ii To my friends and colleagues, I thank you for assisting me in so many ways through the years: Joe Kaser, Matt Kaiser, Suzanne Wold-Burkness, Adam Kokotovich, Shelby Flint, Erica Nystrom, Mark and Annie Asplen, Jeremy and Megan Chacón, Jaana Iverson, Sarah Holle, Connor Mikre, Tavvs Alves, Anh Tran, Dominique Ebbenga, Byju Govindan, Carrie Deans, Carla Dutra, Zdeňka Svobodová, Wally Rich IV, Lindsey Christianson, Jesse Klumb, Kristy Ebert, Ben Miller, Leah Walker, Dave Wilsey, Galen Dively, Thomas Kuhar¸ Mark Abrahamson, the Stoyke family, and all the past and current members of the Salt Institute, and Reading Group. I am deeply grateful to my parents, Mike and Lenore Cira who raised me to value and respect all creatures great and small. They have always nurtured creativity and curiosity about the natural world which has been vital in getting me to this point. I also appreciate the role my brothers, Nate and Mat Cira, have played: creating joyful moments amid hardship and thinking deeply about life and science. I would like to wholeheartedly thank Amy Morey who has had a tremendously positive influence on my dissertation and my life. Her love and companionship have enriched and brightened my world and I have immense gratitude for the wisdom she has shared and help she has offered me. iii Dedication To my parents, Mike and Lenore Cira. iv Abstract Managing pests effectively and efficiently requires knowledge about their biology. Likewise, clear communication about scientific research pertaining to management is needed for managers to make well-informed decisions. My research pertains to the biology of the brown marmorated stink bug, Halyomorpha halys and communication between scientists about insecticidal categorization. Halyomorpha halys is an exotic invasive species in North America. Many horticultural and agricultural plants in North America are at risk for economic damage due to the highly polyphagous nature of this species. Additionally, H. halys has become a serious nuisance pest in human-made structures in some areas when, in preparation for winter, they aggregate in sheltered structures. Therefore, factors such as cold and insecticides, which affect H. halys distribution and ability to cause crop injury are of particular interest to develop management plans. I first conducted several studies of cold tolerance on H. halys in North America. I found that H. halys exhibits a chill-intolerant cold tolerance strategy, that season, sex, and acclimation location affect cold tolerance (i.e., supercooling points), and that laboratory assays of lethal temperature were able to accurately forecast winter mortality in the field. Second, I studied H. halys diapause in more depth. I present a protocol for rearing diapausing H. halys in the laboratory that exhibit similar cold tolerance (i.e., supercooling points and lower lethal temperatures) as individuals with field-induced diapause. I found that H. halys diapause confers greater cold tolerance than a non-diapausing state, and appears to be necessary to survive overwintering. Additionally, I showed diapausing H. halys actively feed for at least three weeks post-diapause induction, but feeding is mediated by temperature and adult age. Third, I investigated and critiqued the current paradigm for determining insecticidal efficacy on H. halys. I highlighted important sublethal effects of insecticides on feeding that can significantly reduce crop injury without the necessity of high direct mortality to H. halys. Lastly, using an interdisciplinary lens I examined linguistic uncertainty as it pertains to categories and descriptors of insecticides. I demonstrated the presence and consequences of v linguistically uncertain terms associated with insecticides and encouraged entomologists to more adequately acknowledge and address these uncertainties in future research. vi Table of Contents Copyright Permission........................................................................................................... i Acknowledgements ............................................................................................................. ii Dedication .......................................................................................................................... iv Abstract ............................................................................................................................... v Table of Contents .............................................................................................................. vii List of Tables ..................................................................................................................... xi List of Figures .................................................................................................................. xiii Introduction ....................................................................................................................... 1 Insecticides ...................................................................................................................... 2 Insect cold tolerance ....................................................................................................... 2 Uncertainty ...................................................................................................................... 4 Halyomorpha halys ......................................................................................................... 4 Insecticidal management of Halyomorpha halys ........................................................ 5 Cold tolerance of Halyomorpha halys ........................................................................ 5 Chapters .......................................................................................................................... 6 Chapter 1: Cold tolerance of Halyomorpha halys (Hemiptera: Pentatomidae) across geographic and temporal scales ..................................................................................... 10 Summary ....................................................................................................................... 10 Introduction ................................................................................................................... 10 Materials and