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Hymenoptera: Encyrtidae) As a Potential Biological Control Agent of Bagrada Hilaris (Heteroptera: Pentatomidae

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Hymenoptera: Encyrtidae) As a Potential Biological Control Agent of Bagrada Hilaris (Heteroptera: Pentatomidae UNIVERSITY OF CALIFORNIA RIVERSIDE Evaluation of the Parasitoid Ooencyrtus mirus (Hymenoptera: Encyrtidae) as a Potential Biological Control Agent of Bagrada hilaris (Heteroptera: Pentatomidae) A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Entomology by Nancy Reisig Power June 2020 Dissertation committee: Dr. Thomas M. Perring, Chairperson Dr. Timothy D. Paine Dr. Mark Hoddle Dr. Daniel Jeske Copyright by Nancy Reisig Power 2020 The Dissertation of Nancy Reisig Power is approved: Committee Chairperson University of California, Riverside Acknowledgements One of the many things Tom Perring taught me as my major professor was to put the most important things first. So, first off, THANK YOU, TOM, for taking me on as a transfer from the Cardé lab and for sharing so generously of your time and expertise. One of the greatest privileges of my life has been learning firsthand from someone so brilliant and competent. Thank you for going beyond the dissertation to also give feedback on presentations, interpersonal communication and job interviews, including helping me get hired for my dream job. My deep gratitude also extends to Dr. Fatemeh Ganjisaffar for indispensable statistical and writing advice and endless patience. Many thanks to Dr. Ring Cardé for taking me on as a student and, when it became painfully clear that navel orangeworm mating behavior was not my calling, for finding another professor for me to work with. I love your wicked sense of humor. I am also profoundly grateful to all the Entomology professors who taught, advised, wrote letters of recommendation and/or assisted me or allowed their staff to assist me over the past six years, including my dissertation committee members Drs. Tim Paine, Mark Hoddle and Dan Jeske, guidance committee members Drs. Matt Daugherty, Kerry Mauck, Jocelyn Millar and Peggy Mauk, advisors Drs. Brad Mullens and Christiane Weirauch, and Drs. Michael Adams, Dong-Hwan Choe, Anupama Dahanukar, John Heraty, Quinn McFrederick, Naoki Nishiyama, Monique Rivera, Richard Stouthamer, John Trumble, Kirk Visscher, Greg Walker, Bill Walton, Erin Wilson-Rankin and Hollis Woodard. You are not only world-class scholars but also amazing, wise human beings. I have so iv appreciated the culture of collaboration you create in the department. I have been thrilled to explore with you the frontiers of knowledge. I deeply appreciate the Perring Lab staff, who made my work both possible and fun: Shayla Hampel for being both proficient and amiable, Dr. Sharon Andreason, Colt Bellman, Seanathan Chin, Henderson Hsu, Greg Kund, Tim Lewis, Blake Miles, Dr. Darcy Reed and fellow Ph.D. student Dani Ruais. I would also like to thank my Entomology classmates. I deeply admire your leadership and competence. I would particularly like to acknowledge Ben Sumner, who “saved my life” on multiple occasions, and Chrissy Dodge and Paul Masonick, who faithfully attended my presentations. I am grateful to Scott Heacox, Luke Kresslein Rochelle Hoey-Chamberlain and Ian Wright for taking photos of Ooencyrtus mirus, to Daniel Pierce for a photo of Bagrda hilaris, and to Austin Baker for editing photos. I am grateful to taxonomist Dr. Serguei Triapitsyn for offering me the privilege of naming my wasp species and participating in its description, Dr. Doug Yanega who catalogued my voucher specimens and helped identify alternate host species, and Dr. Roger Burks who showed me how to distinguish male from female Ooencyrtus mirus. I thank Lucio Rodriguez in the Ring Cardé lab for supplying Helicoverpa zea eggs and Jesús Lara and Vincent Strode in the Mark Hoddle lab for supplying Halyomorpha halys eggs. Outside the Entomology Department, I would like to thank Dr. Georgios Vidalakis for the wonderful field course that toured California agriculture and helped me realize that my first-choice position was to be a Farm Advisor. Many thanks to Dr. Karen v Xu and Dr. Anthony Gamst for assisting with the more difficult statistical analyses. Thank you to Drs. Hsu and Cui for teaching statistics. Finally, I would like to thank Bernice and the other librarians who processed my many inter-library loan requests so swiftly and cheerfully. Thomas M. Perring directed and supervised all the research which forms the basis for this dissertation. Chapter 2 is, in part, material as it will appear in Power N, Ganjisaffar F, Xu K & Perring TM, “Effects of parasitoid age, host egg age, and host egg freezing on reproductive success of Ooencyrtus mirus on Bagrada hilaris eggs,” in preparation. Chapter 3 is, in part, material as it will appear in Power N, Ganjisaffar F & Perring TM, “Fecundity, fertility and longevity of Ooencyrtus mirus (Hymenoptera: Encyrtidae),” in preparation. Chapter 4 is partly a reprint of the material in Power N, Ganjisaffar F & Perring TM, “Effect of temperature on the survival and developmental rate of immature Ooencyrtus mirus (Hymenoptera: Encyrtidae),” in press in the Journal of Economic Entomology. Chapter 5 was directed, in part, by Richard Stouthamer, and is material that will appear in Power N, Rugman-Jones P, Stouthamer R, Ganjisaffar F & Perring TM, “The impact of high temperature mortality of Wolbachia on the sex ratio of host Ooencyrtus mirus (Hymenoptera: Encyrtidae),” to be submitted to Peer J. Chapter 6 is, in part, material that will appear in Power N, Ganjisaffar F & Perring TM, “Evaluation of the physiological host range for the parasitoid Ooencyrtus mirus, a potential biocontrol agent of Bagrada hilaris,” in preparation. The Introduction and Conclusion of this dissertation may contain text from any of the above publications. vi The research conducted for this dissertation was funded in part by the U.C. Riverside Department of Entomology Outreach Program, the Robert and Peggy van den Bosch Memorial Scholarship, the Harry K. Smith Award, the Ernest Propes Travel Award and the California Department of Food and Agriculture 2016 Specialty Crop Block Grant Program, PIN 33469. vii Dedication To my most enthusiastic cheerleaders in this endeavor (in alphabetical order): Liz Goetz, Dr. Peter Ilott and Frances Power. Thank you for your hospitality, generosity and boundless encouragement! viii ABSTRACT OF THE DISSERTATION Evaluation of the Parasitoid Ooencyrtus mirus (Hymenoptera: Encyrtidae) as a Potential Biological Control Agent of Bagrada hilaris (Hemiptera: Heteroptera: Pentatomidae) by Nancy Reisig Power Doctor of Philosophy, Graduate Program in Entomology University of California, Riverside, June 2020 Dr. Thomas M. Perring, Chairperson In an effort to find a biological control agent of Bagrada hilaris, an invasive pentatomid pest on brassica crops in western North America, three hymenopteran egg parasitoids were recovered from brassica plant debris in Pakistan and sent to California, USA for evaluation. One of these, a uniparental species, has since been described as Ooencyrtus mirus. To evaluate O. mirus as a potential biological control agent, I investigated its host range and reproductive capacity. I also tested parameters for maximizing its reproduction, including temperature and the age of the parasitoid and host eggs. Finally, I examined O. mirus’ ability to find host eggs on broccoli plants and in soil, where B. hilaris lays them. The results show O. mirus to be a generalist parasitoid species with a preference for B. hilaris. Under lab conditions O. mirus lays an average of 118 eggs and lives an average of 58 days. The immatures undergo quiescence at 14° or 16°C. They can be stored at these temperatures for at least 3 months with no loss of reproductive success. The immatures develop fastest at 36°C, but the best temperature for rearing is 30°C. Above 30°C, the second generation has an increase in the proportion of males, due to the high temperature killing the symbiotic Wolbachia bacteria that enable unfertilized ix eggs to develop as females. Wasps of age 3-11 days have better reproductive success than wasps aged 0-2 days. Wasps are most successful on 0- and 1-day-old B. hilaris eggs, and they can reproduce on frozen eggs. The ability of O. mirus to find host eggs was poor in soil, and even worse on plants. These studies describe the biological characteristics of O. mirus that suggest it could be an effective biological control agent. However, more testing is needed on its host preferences under natural conditions to determine if it would be safe to release in the field; i.e., not a threat to native or beneficial host species. x Table of Contents Chapter 1. Introduction to the Dissertation ……...……………………………………... 1 Part I. Reproductive Biology of Ooencyrtus mirus Chapter 2. Effects of parasitoid age, host egg age, and host egg freezing on reproductive success of Ooencyrtus mirus on Bagrada hilaris eggs.........15 Chapter 3. Life History of Ooencyrtus mirus ..…………………………………….. 44 Chapter 4. Effect of temperature on the survival and developmental rate of immature Ooencyrtus mirus ……………………….………………….... 60 Chapter 5. The impact of high temperature mortality of Wolbachia on the sex ratio of host Ooencyrtus mirus …………………………………….. 85 Part II. Ecology of Ooencyrtus mirus as a potential classical biological control agent Chapter 6. Evaluation of the physiological host range of Ooencyrtus mirus …….. 106 Chapter 7. Ability of Ooencyrtus mirus to find Bagrada hilaris eggs in soil and on broccoli plants ………………………………………………… 138 Chapter 8. General Conclusions of the Dissertation ………………………………… 150 References ....................................................................................................................
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