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1 UNIVERSITY of CALIFORNIA RIVERSIDE Implications Of UNIVERSITY OF CALIFORNIA RIVERSIDE Implications of Argentine Ant Management for Biological Control of the Asian Citrus Psyllid and Other Ant-Tended Pests in Citrus A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Entomology by Kelsey Ann McCalla December 2019 Dissertation Committee: Dr. Mark Hoddle, Co-Chairperson Dr. Richard Redak, Co-Chairperson Dr. Erin Wilson-Rankin Dr. Matthew Daugherty 1 Copyright by Kelsey Ann McCalla 2019 2 The Dissertation of Kelsey Ann McCalla is approved: Committee Co-Chairperson Committee Co-Chairperson University of California, Riverside 3 Acknowledgments I would like to begin by expressing my sincerest gratitude to my advisor Dr. Mark Hoddle. Thank you for teaching me how to stay organized and reliable, how to effectively and efficiently communicate, and how to write and speak like a champ. Thank you for pushing me to learn novel concepts independently, for helping me push past my own limitations (80/20 rule!), and instilling in me a passion for research. Your financial support and guidance allowed me to design and execute truly ambitious projects, projects that the rest of my career will be built upon and that I can truly be proud of. I appreciate your dependability, honesty, humor, and enthusiasm (it’s infectious)! I have flourished in this lab and it was all made possible by your unwavering commitment to the achievement of excellence. It is sad to see the end of an era, but I look forward to a career’s worth of collaborative opportunity - there is still so much more work for us to do! The future is bright and my trajectory (as you say) ‘meteoric’! I am grateful to my committee members Dr. Richard Redak, Dr. Erin Wilson- Rankin, and Dr. Matthew Daugherty for their feedback on my dissertation work and their advice and support in many of my academic affairs. Special thanks to Matt and Erin for helping me develop a strong statistical background and teaching me how to program in R. Without you I may have forever been bound to a life of ANOVAs and t-tests. I would like to express my gratitude to the members of the Hoddle lab. I thank Ruth Amrich and Mike Lewis for teaching me how to survive as a new graduate student in the lab, for many fun conversations and sage-level advice, and for helping me solve problems and skirt certain disaster. Thank you to our postdocs, Ivan Milosavljević and iv Erica Kistner for your patience, kindness, advice, and support. You taught me both how to succeed in an academic career and how to (gracefully) accept failure. Because of you I am not only a better entomologist but also a better co-worker and friend. Finally, I would like to recognize the incredible contributions of our many field and laboratory technicians who made my dissertation work possible: Elizabeth Carpenter, Kelly Giordano, Sam Figueroa, Martin Castillo, Vincent Strode, Nagham Melhelm, Michael Lewis, Michael Patini, Emily Shin, Carly Pierce, Mike Jones, Mariana Romo, Allison Bistline-East, Mehmet Keçeci, Ricky Lara, Meghan Vankosky, Nic Irvin, and Christina Hoddle. Many thanks to Ken Kupfer for supplying the bait stations used in chapter 3 and for his continued support of my dissertation work. I thank Suterra LLC. for providing the microencapsulated (Z)-9-hexadecenal used in the liquid bait formulation in chapters 3 and 4. I acknowledge the support of cooperating pesticide applicators who assisted with the identification of field sites and citrus growers who provided orchard access for conducting field trials. Thank you to Dr. David Morgan and Grace Radabaugh of the California Department of Food and Agriculture for supplying me with suggestions for field sites and parasitoids and plants for chapter 2. Finally, thank you to my family and friends for your love, encouragement, and emotional support throughout this long and arduous journey. Kaleigh Russell, Jackie Serrano, Tessa Shates, Sam Figueroa, Megan Fentress, Emily Shin, and many others made my time in graduate school not only tolerable but fun and memorable! To my parents Tom and Lisa Schall, my sister Sara Schall, my husband and best friend Scott McCalla, and my fur baby Maple, I am greatly indebted. I am blessed to have such a v loving and encouraging family and I cannot imagine how I would have navigated the many, many obstacles of graduate school without you. You always saw the best in me - even in the darkest of times - and helped make your vision of me into my reality. This dissertation was truly a collaborative effort and labor of love on behalf of us all. This work would not have been possible without the financial support provided by the California Department of Pesticide Regulation agreement number 15-PML-R002, the Citrus Research Board agreement number 5500-194, the Robert and Peggy van den Bosch Memorial Scholarship, the Charles Coggins Jr. Endowed Scholarship, and the Harry Scott Smith Biological Control Scholarship. Chapter 2 of this dissertation is a reprint of material previously published as: Kelsey A. McCalla, Mehmet Keçeci, Ivan Milosalvjević, David A. Ratkowsky, and Mark S. Hoddle, The Influence of Temperature Variation on Life History Parameters and Thermal Performance Curves of Tamarixia radiata (Hymenoptera: Eulophidae), a Parasitoid of the Asian Citrus Psyllid (Hemiptera: Liviidae). Journal of Economic Entomology, Volume 112, Issue 4 (2019), pages 1560-1574. It is included in this dissertation with permission from Oxford Academic. KM, MK, and MH conceived and designed the experiment. KM and MK conducted the laboratory trials. KM ran analyses on collected data with considerable input from DR and IM. KM prepared the manuscript in full. All authors reviewed, provided feedback, and approved of the manuscript. vi ABSTRACT OF THE DISSERTATION Implications of Argentine Ant Management for Biological Control of the Asian Citrus Psyllid and Other Ant-Tended Pests in Citrus by Kelsey Ann McCalla Doctor of Philosophy, Graduate Program in Entomology University of California, Riverside, December 2019 Dr. Mark Hoddle and Dr. Richard Redak, Co-Chairpersons The establishment of the Asian citrus psyllid-huanglongbing (Diaphorina citri Kuwayama [Hemiptera: Liviidae]) pest-disease complex has severely diminished the profitability of the citrus trade worldwide. California’s citrus industry is valued at $7.1 billion annually and supports some 21,700 full-time positions. Economic forecasts predict that the spread of huanglongbing into major production areas from the residential areas within which it is currently restricted would have devastating financial consequences for the state. My doctoral research investigates the use of integrated, sustainable strategies for improving biological control of D. citri. A major impediment to this pest management approach is the invasive Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae), a notorious tramp ant species that is ubiquitous across southern California. Linepithema humile establishes trophobiotic mutualisms with honeydew-producing hemipterans in the citrus agroecosystem, many of which are invasive, economically damaging pests. Although ant-hemipteran pest partnerships are well-documented for vii many systems, little is known about the long-term consequences of the relationship between L. humile and D. citri. I aimed to bridge this knowledge gap by first, determining the host-killing capacity of the D. citri parasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) under field realistic thermal cycles, second, examining the impact of L. humile control on infestation and biological control of D. citri and other ant-associated citrus pests, and third, developing and evaluating an alginate hydrogel bait transport system as a high efficacy, low-cost treatment option for control of L. humile in commercial citrus. Results indicated that T. radiata inflicts a significant portion of D. citri mortality through host feeding. Consequently, its biocontrol contributions may have previously been undervalued. In addition, L. humile management is critical to achieving optimal biological control of populations of D. citri and other hemipteran pest populations. Finally, excellent L. humile suppression can be achieved with both a traditional liquid-bait-and-dispenser program or applications of bait-loaded alginate hydrogels. The work presented herein provides foundational information on the relationships among L. humile, D. citri, other ant-associated hemipteran species, and biological control agents. Application of these results could greatly improve the existing integrated pest management framework for control of these pests in California citrus. viii Table of Contents Chapter 1: Introduction....................................................................................................1 References.......................................................................................................................14 Chapter 2: The Influence of Temperature Variation on Life History Parameters and Thermal Performance Curves of Tamarixia radiata (Hymenoptera: Eulophidae), a Parasitoid of the Asian Citrus Psyllid (Hemiptera: Liviidae)......................................22 Abstract...........................................................................................................................22 Introduction.....................................................................................................................23 Materials and Methods....................................................................................................27
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