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Diaphorina Citri) in Southern California UNIVERSITY OF CALIFORNIA RIVERSIDE Predators of Asian Citrus Psyllid (Diaphorina citri) in Southern California A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Entomology by Aviva Goldmann December 2017 Dissertation Committee: Dr. Richard Stouthamer, Chairperson Dr. Matt Daugherty Dr. Jocelyn Millar Dr. Erin Rankin Copyright by Aviva Goldmann 2017 The Dissertation of Aviva Goldmann is approved: Committee Chairperson University of California, Riverside Acknowledgements I would like to thank my graduate advisor, Dr. Richard Stouthamer, without whom this work would not have been possible. I am more grateful than I can express for his support and for the confidence he placed in my research. I am very grateful to many members of the Stouthamer lab for their help and contributions. Dr. Paul Rugman-Jones gave essential support and guidance during all phases of this project, and contributed substantially to the design and troubleshooting of molecular analyses. The success of the field experiment described in Chapter 2 is entirely due to the efforts of Dr. Anna Soper. Fallon Fowler, Mariana Romo, and Sarah Smith provided excellent field and lab assistance that was instrumental in completing this research. I could not have done it alone, especially at 4:00 AM. Janet Hare and Daniel Manzo reared all the ACP used for the experiments described in Chapter 5. Their good nature, accommodation, and reliability were key in the success of these studies. This manuscript was much improved by help and feedback from my dissertation committee members: Dr. Matt Daugherty, Dr. Jocelyn Millar, and Dr. Erin Rankin. Sincere thanks to Dr. Anupama Dahanukar, Dr. Joseph Morse, Dr. Leonard Nunney, and Dr. William Walton for serving on my guidance committee. Many members of the UCR Entomology and campus community were very generous with their time and resources. Dr. Douglas Yanega helped many times with identifications, museum resources, and taxonomic literature. Dr. Steve McElfresh provided key guidance in early stages of my research. Dr. Roger iv Burks worked with me to produce professional-quality photographs of my study organisms. The smooth functioning of the I&Q and other facilities is owed to Imad Bayoun’s constant work. Melissa Gomez and Kathy Redd went to extra trouble to help me clear every administrative hurdle. The entire Entomology administrative office unfailingly took care of essentials that made this work possible: funding, facilities, supplies, scheduling, and more. The UCR Graduate Writing Center, GradQuant, and Graduate Academic Affairs were extremely helpful. The Institute for Integrative Genome Biology staff often went above and beyond. Sincere thanks go to experts who graciously provided identifications of key predator species: Dr. Robert Gordon, Dr. Catherine Tauber, Dr. Natalia Vandenberg, and Dr. Richard Vetter. The Entomology department works hard to connect graduate students with financial support throughout their degree programs, for which I am very grateful. The Citrus Research Board provided three years of funding, important guidance, feedback, and opportunities to present my work. The Robert and Peggy van den Bosch Scholarship for Graduate Student Research in Biological Control and the Harry Scott Smith Biological Control Scholarship enabled me to hire technicians, obtain training in spider identification, travel to conferences, and enhanced my research and professional development in many ways. My first year was funded by the Dean’s Distinguished Fellowship Award. I am also indebted to the Charles W. Coggins, Jr. Endowed Scholarship Fund, the Homer v & Daisy Chapman Endowed Scholarship Fund for Citrus Research, UCR GradSlam, and the Adam Repán Petko Memorial Book Collection contest. Huge thanks to the members of my graduate cohort and many other Entomology graduate students for being such great classmates, colleagues, and friends. You are too many to list, but if you weren’t an MVP you wouldn’t be reading this—so thank you, sincerely. Thank you to all the incarnations of the Three Sentence Club, including Dr. Ariane Helou, Dr. Andrea Lankin, Vivien Lee, MS, Dr. Eve Levavi Feinstein, soon-to-be Dr. Carlotta Falzone Robinson (who is an ace at Word formatting), and Dr. Bridget Sousa. Thank you to my pomodoro buddies, soon-to-be Dr.’s Diane Gonzalez and Kelsi Perttula. Thank you to Dr. Nicholas Mills for starting me on this journey, and to my colleagues from the Mills lab for being outstanding co-workers and role models. To the faculty, staff, and students of California Ecology and Conservation, Sp. 2017 for the best quarter ever. Special thanks to Yuhan Pan for translation. To my wonderful family, for constant love and support throughout my entire life, for being exemplary human beings and role models, for all they have done to help me and each other, and for always seeing a bright future for me. To my spouse, Andrew Moll, my favorite person and fellow traveler, whose love, support, and faith in my abilities has made all the difference. vi ABSTRACT OF THE DISSERTATION Predators of Asian Citrus Psyllid (Diaphorina citri) in southern California by Aviva Goldmann Doctor of Philosophy, Graduate Program in Entomology University of California, Riverside, December 2017 Dr. Richard Stouthamer, Chairperson Asian citrus psyllid (ACP) threatens the viability of California citriculture because it spreads a bacterium, Candidatus Liberibacter asiaticus, that kills citrus trees. Preliminary observations suggested that predatory arthropods in southern California reduce the ACP population, but it was not known which predator species were important. The goal of this PhD project was to identify potentially effective natural enemies of ACP among southern California predatory arthropods for use as biological control agents. To accomplish this, we first measured the natural mortality of ACP in a southern California orange orchard by conducting a predator exclusion experiment monthly for seven months. Overall, ACP survival was nearly four times higher in cohorts protected from predators than in control cohorts. To detect which predator species contribute to ACP mortality, we conducted a year-long survey of predatory arthropods in two orange orchards. Among the predators collected, ten were abundant. We designed a vii molecular assay to detect ACP DNA in predator gut contents and used it to test field-collected specimens of these predators for recent predation of ACP. Three insects and all five spiders were positive for ACP predation in over 10% of specimens tested. Older C. comanche larvae and afternoon-collected adult D. pumilio were significantly more likely to test positive for ACP predation than conspecifics which were younger (C. comanche) and collected before dawn (D. pumilio). The two insects that tested positive most frequently, Diomus pumilio (Coleoptera: Coccinellidae) and Chrysoperla comanche (Neuroptera: Chrysopidae) were investigated further because of their potential for use in augmentative and/or conservation biological control. For each species, we conducted timed feeding trials to calculate a half-life for the detectability of ACP remains following predation, and conducted prey choice assays with all life stages of ACP to determine which were most likely to be consumed after being probed by the predator. D. pumilio adults preferentially preyed upon ACP eggs and first-third instar nymphs, while C. comanche larvae most frequently consumed eggs and third-fourth instar nymphs. We recommend development of these insects as biological control agents of ACP, and suggest developing spider conservation tactics compatible with citrus IPM. viii TABLE OF CONTENTS Introduction ......................................................................................... 1 Dissertation objectives .................................................................................... 10 References ...................................................................................................... 12 Natural mortality of ACP in Southern California ................................ 17 Abstract ........................................................................................................... 18 Introduction ..................................................................................................... 18 Materials and methods .................................................................................... 25 Results ............................................................................................................ 30 Discussion ....................................................................................................... 34 Conclusion ...................................................................................................... 41 References ...................................................................................................... 43 Survey of predatory arthropods in southern California commercial citrus ................................................................................................................... 51 Abstract ........................................................................................................... 52 Introduction ..................................................................................................... 52 Materials and methods .................................................................................... 59 Results ...........................................................................................................
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