1.6 Parasitoids of Giant Whitefly
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UC Riverside UC Riverside Electronic Theses and Dissertations Title Life Histories and Host Interaction Dynamics of Parasitoids Used for Biological Control of Giant Whitefly (Aleurodicus dugesii) Cockerell (Hemiptera: Aleyrodidae) Permalink https://escholarship.org/uc/item/8020w7rd Author Schoeller, Erich Nicholas Publication Date 2018 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA RIVERSIDE Life Histories and Host Interaction Dynamics of Parasitoids Used for Biological Control of Giant Whitefly (Aleurodicus dugesii) Cockerell (Hemiptera: Aleyrodidae) A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Entomology by Erich Nicholas Schoeller March 2018 Dissertation Committee: Dr. Richard Redak, Chairperson Dr. Timothy Paine. Dr. Matthew Daugherty Copyright by Erich Nicholas Schoeller 2018 The Dissertation of Erich Nicholas Schoeller is approved: Committee Chairperson University of California, Riverside Acknowledgements This dissertation was made possible with the kind support and help of many individuals. I would like to thank my advisors Drs. Richard Redak, Timothy Paine, and Matthew Daugherty for their wisdom and guidance. Their insightful comments and questions helped me become a better scientist and facilitated the development of quality research. I would particularly like to thank Dr. Redak for his endless patience and unwavering support throughout my degree. I wish to also thank Tom Prentice and Rebeccah Waterworth for their support and companionship. Their presence in the Redak Lab made my time there much more enjoyable. I would like to thank all of the property owners who kindly allowed me to work on their lands over the years, as well as the many undergraduate interns who helped me collect and analyze data from the experiments in this dissertation. Last but not least, I express my deepest appreciated to my parents for their love and many years of endless support of my aspirations. If it wasn’t for their steadfast belief in me I would not be where I am today. Chapter 4 was previously published as: Erich N. Schoeller, Maher Yassin, and Richard A. Redak (2018) Host-produced Wax Affects the Searching Behavior and Efficacy of Parasitoids of the Giant Whitefly Aleurodicus dugesii (Hemiptera: Aleyrodidae). Biological Control. 121:74–79. DOI: 10.1016/j.biocontrol.2018.02.002. It is included in this dissertation with permission from Elsevier. Co-authors Maher Yassin assisted with a large portion of data collection, and Dr. Richard A. Redak provided the laboratory resources and supervision for this project. iv The research conducted in this dissertation was funded in part by the UC Riverside Department of Entomology Outreach Program, the UC Dissertation-Year Fellowship, the Robert and Peggy van den Bosch Memorial Scholarship, the California Association Nurseries and Garden Centers, and the United States Department of Agriculture NIFA pre-doctoral fellowship (2016-67011-25164). v Dedication To all the people in my life who are no longer here to see me achieve my dreams. vi ABSTRACT OF THE DISSERTATION Life Histories and Host Interaction Dynamics of Parasitoids Used for Biological Control of Giant Whitefly (Aleurodicus dugesii) Cockerell (Hemiptera: Aleyrodidae) by Erich Nicholas Schoeller Doctor of Philosophy, Graduate Program in Entomology University of California, Riverside, March 2018 Dr. Richard A. Redak, Chairperson Whether interactions among biocontrol agents limits their ability to control shared prey has been one of the most important and controversial questions surrounding biological control. In California multiple parasitoid wasp species have been introduced to control the invasive giant whitefly Aleurodicus dugesii Cockerell (Hemiptera: Aleyrodidae). The overall goal of this dissertation was to determine aspects of these species’ basic biologies and investigate factors contributing to the efficacy of these parasitoids. Findings of these studies will provide a better understanding of how parasitoid community complexity affects biological control and may enhance biological control of A. dugesii in California and elsewhere. First the effects of temperature on survival and development of A. dugesii were assessed. Starting at 10°C development rate of A. dugesii increased until an optimum of 29°C was reached, then development ceased at 30°C. Using these data developmental degree days were calculated for A. dugesii. vii Second, host stage preferences of the three parasitoids were determined. All host nymphal stages were accepted by I. affinis for oviposition, while only the 2nd–4th and 3rd– 4th instars were accepted by E. noyesi and E. krauteri respectively. Host stage preferences overlapped considerably between species. Third, the effects of A. dugesii nymphal wax production on I. affinis and E. noyesi efficacy was determined. Wax production decreased parasitoid effectiveness, with I. affinis being more negatively impacted by wax than E. noyesi. Wax was found to serve as an effective defense against parasitism. Finally, the effects of climate and season on population dynamics of species in this system were assessed. Population densities of A. dugesii were found to not differ across climate types in southern California. Total and E. noyesi parasitism rates also did not differ across climate types. Parasitism rates of I. affinis were highest in inland climate sites. Parasitism by E. noyesi and I. affinis was high throughout the year, except during the early spring. The contribution of E. krauteri to A. dugesii biological control appears to be negligible. viii Contents 1 Introduction 1 1.1 The Rational Basis for the Study of Biological Control . 1 1.2 Coexistence in Parasitoid Communities . 2 1.3 Competitive Interactions between Parasitoids . 5 1.4 Parasitoid Competition and Biological Control Success . 9 1.5 The Giant Whitefly Aleurodicus dugesii . 14 1.6 Parasitoids of Giant Whitefly . 20 1.7 Objectives of Dissertation . 27 1.8 Literature Cited . 28 2 Temperature-Dependent Development and Survival of Giant Whitefly at Constant Temperatures. 42 2.1 Introduction . 42 2.2 Materials and Methods . 45 2.3 Results . 52 2.4 Discussion . 60 2.5 Literature Cited . 64 3 Host Stage Preferences of Parasitoids of the Giant Whitefly. 69 3.1 Introduction . 69 3.2 Materials and Methods . 71 3.3 Results . 76 ix 3.4 Discussion . 86 3.5 Literature Cited . 90 4 Host-produced Wax Affects the Searching Behavior and Efficacy of Parasitoids of the Giant Whitefly 94 4.1 Introduction . 94 4.2 Materials and Methods . 99 4.3 Results . .. 105 4.4 Discussion . .. 107 4.5 Literature Cited . 113 5 Effects of Temperature on Phenology and Biological Control of Giant Whitefly in Southern California. 117 5.1 Introduction . 117 5.2 Materials and Methods . 122 5.3 Results . 129 5.4 Discussion . 138 5.5 Literature Cited . 142 6 Concluding Remarks 150 6.1 Additional Remarks . 150 6.2 Conclusions . 157 6.3 Literature Cited . 158 x List of Figures 1.1 The Giant Whitefly Aleurodicus dugesii . 15 1.2 Distribution of Giant Whitefly in California . 17 1.3 Collection Origin of Entedononecremnus krauteri . 22 1.4 Collection Origin of Encarsia noyesi and Idioporus affinis . 24 1.5 Parasitoids of Giant Whitefly . 25 2.1 Aleurodicus dugesii Temperature-dependent Development Models . 55 2.2 Aleurodicus dugesii Survival Curves at Constant Temperatures . 59 3.1a-c Parasitoid Host Stage Preference Paired-Choice Tests . 79 3.2a-c Parasitoid Host Stage Preference Simultaneous-Choice Tests . 80 3.3a-c Parasitoid Host Stage Preference No-Choice Tests . 81 3.4a-c Parasitoid Host Stage Handling Times . 85 4.1 Nymphal and Adult Aleurodicus dugesii Wax Production . 98 4.2 Experimental Design for Parasitoid Wax Exposure Efficacy Tests . 100 4.3 Effects of Aleurodicus dugesii Nymphal Wax on Parasitism Rates . 106 4.4 Effects of Aleurodicus dugesii Wax on Parasitoid Foraging Behavior . 108 4.5 Nymphal Wax Particle Accumulation on the Body of Idioporus affinis . 108 5.1 Map of Study Sites Locations in Southern California . 123 5.2 Illustration of Sampling Methodology for Experimental Plants . 125 5.3 Temperature Profiles of Study Sites within Different Climate Types . 130 5.4 Mean Seasonal Temperatures of Study Sites of Different Climate Types . 130 xi 5.5 Least Squared Means of the Interaction between Season and Climate Type on Aleurodicus dugesii Population Densities . 131 5.6 Plot of Mean Total Aleurodicus dugesii Population Densities against Mean Total Parasitism Rates . 132 5.7 Least Squared Means of the Seasonal Differences in Total Parasitism Rates . 133 5.8 Least Squared Means of the Climactic Differences in Total Idioporus affinis Parasitism Rates . 134 5.9 Least Squared Means of the Seasonal Differences in Total Idioporus affinis Parasitism Rates . 136 5.10 Least Squared Means of the Seasonal Differences in Total Encarsia noyesi Parasitism Rates . 136 5.11 Mean Total Entedononecremnus krauteri Parasitism Rates over Time . 137 6.1 Visual identification of Encarsia noyesi hyperparasitism . 156 6.2 Mean Total Encarsia noyesi Hyperparasitism Rates over Time . 157 xii List of Tables 1.1 Summary of Parasitoid Coexistence Mechanisms . 3 1.2 Partial List of Giant Whitefly Host Plants . 18 2.1 Aleurodicus dugesii Development at Seven Constant Temperatures . 53 2.2 Parameter Estimates for Aleurodicus dugesii Developmental Models . 56 2.3 Goodness-of-fit Criteria for Aleurodicus dugesii Developmental Models . 58 2.4 Degree Day Estimates