PHYTOSEIIDS AS BIOLOGICAL CONTROL AGENTS OF PHYTOPHAGOUS MITES IN WASHINGTON APPLE ORCHARDS By REBECCA ANN SCHMIDT-JEFFRIS A dissertation submitted in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY WASHINGTON STATE UNIVERSITY Department of Entomology MAY 2015 © Copyright by REBECCA ANN SCHMIDT-JEFFRIS, 2015 All Rights Reserved © Copyright by REBECCA ANN SCHMIDT-JEFFRIS, 2015 All Rights Reserved To the Faculty of Washington State University: The members of the Committee appointed to examine the dissertation of REBECCA ANN SCHMIDT-JEFFRIS find it satisfactory and recommend that it be accepted. Elizabeth H. Beers, Ph.D., Chair David W. Crowder, Ph.D. Richard S. Zack, Ph.D. Thomas R. Unruh, Ph.D. Nilsa A. Bosque-Pérez, Ph.D. ii ACKNOWLEDGEMENT I would like to thank Dr. Elizabeth Beers for giving me the opportunity to work in her lab and for several years of exceptional mentoring. She has provided me with an excellent experience and is an outstanding role model. I would also like to thank the other members of my committee, Drs. Thomas Unruh, David Crowder, Nilsa Bosque-Pérez, and Richard Zack for comments on these (and other) manuscripts, and invaluable advice throughout my graduate career. Additionally, I thank the entomology faculty of Washington State University and the University of Idaho for coursework that acted as the foundation for this degree, especially Dr. Sanford Eigenbrode and Dr. James “Ding” Johnson. I also thank Dr. James McMurtry, for input on manuscripts and identification confirmation of mite specimens. I would like to acknowledge the assistance I received in conducting these experiments from our laboratory technicians, Bruce Greenfield and Peter Smytheman, my labmate Alix Whitener, and the many undergraduate technicians that helped collect data: Denise Burnett, Allie Carnline, David Gutiérrez, Kylie Martin, Benjamin Peterson, Mattie Warner, Alyssa White, and Shayla White. I would especially like to acknowledge my assistants, Jordan Takasugi and Kaitlin Parsons, without which most of this work could not have been done. I also thank Drs. Bahman Shafii, William Price, Mark Evans, and David Crowder for statistical advice. I would also like to express my gratitude to the many cooperating fieldmen and growers who allowed me to work in their orchards. I appreciate the support (both emotional and financial) that I have received from my mother, father, and sister while completing this degree and for encouraging my love of learning and science. I would also like to thank my in-laws, the entomology graduate students in Pullman, and Emily Wolfe for providing me with a family while away from home. Finally, I would like to iii thank my husband, Dennis Jeffris, for being an incredible listener and a constant source of encouragement. iv PHYTOSEIIDS AS BIOLOGICAL CONTROL AGENTS OF PHYTOPHAGOUS MITES IN WASHINGTON APPLE ORCHARDS Abstract by Rebecca Ann Schmidt-Jeffris, Ph.D. Washington State University May 2015 Chair: Elizabeth H. Beers The integrated mite management (IMM) program in Washington has depended on the biological control of spider mites provided by Galendromus occidentalis (Nesbitt). We explored methods of improving this program. A series of inundative releases of G. occidentalis was performed in commercial apple orchards. None of the releases increased G. occidentalis numbers or reduced pest spider mite populations. It was concluded that a cost prohibitive number of predators would be necessary to maintain pest mites below economic thresholds, emphasizing the importance of conservation biological control. Phytoseiids in apple orchards across Washington were sampled to determine diversity and elucidate factors affecting abundances. While the community was expected to be completely dominated by G. occidentalis , Amblydromella caudiglans (Schuester) was also highly abundant. G. occidentalis abundance was positively affected by conventional pesticide regimes and bifenazate use, whereas A. caudiglans was negatively affected by bifenazate and positively affected by herbicide strip weediness. This indicated that A. caudiglans was more susceptible to disruptive pesticide inputs than G. v occidentalis . This was confirmed by an assay wherein several orchard pesticides caused higher mortality of A. caudiglans than G. occidentalis . The recent phase out of certain orchard pesticides may have allowed A. caudiglans to become more common. To understand the mite species complex in the absence of pesticides, an insecticide-free research orchard was monitored at regular intervals during two growing seasons. Generalist phytoseiids were more common than G. occidentalis throughout both seasons. These species were nearly dependent on Aculus schlechtendali (Nalepa) as a food source, as spider mites remained scarce. This emphasizes the role of spider mites as induced pests and suggests that in the absence of pesticide applications, a complement of generalist predators is capable of maintaining spider mite populations at very low densities. G. occidentalis was also found to be less affected by leaf surfaces than generalist phytoseiids examined in previous studies. These findings indicate that G. occidentalis is biological different from the generalist phytoseiids that may replace it as pesticide use changes. Therefore, IMM must constantly be re-evaluated in order to meet orchardists’ needs. vi TABLE OF CONTENTS Page ACKNOWLEDGEMENT ......................................................................................................... iii-iv ABSTRACT ................................................................................................................................ v-vi LIST OF TABLES ...........................................................................................................................x LIST OF FIGURES ...................................................................................................................... xii CHAPTER ONE: REVIEW OF BIOLOGICAL CONTROL PRINCIPLES USING PHYTOSEIIDS AS MODELS, WITH SPECIAL REFERENCE TO INTEGRATED MITE MANAGEMENT IN WASHINGTON APPLE ............................................................................. 1 Introduction ..................................................................................................................................... 1 Phytoseiids as Model Biological Control Agents ........................................................................... 3 Classical Biological Control ........................................................................................................... 5 Augmentative Biological Control ................................................................................................. 13 Conservation Biological Control .................................................................................................. 16 Integrated Mite Management in Washington Apple ..................................................................... 24 References Cited ........................................................................................................................... 27 CHAPTER TWO: RELEASES OF INSECTARY-REARED GALENDROMUS OCCIDENTALIS (ACARI: PHYTOSEIIDAE) IN COMMERCIAL APPLE ORCHARDS ...... 55 Abstract ......................................................................................................................................... 55 Introduction ................................................................................................................................... 55 Materials and Methods .................................................................................................................. 58 Results ........................................................................................................................................... 65 vii Discussion ..................................................................................................................................... 68 References Cited ........................................................................................................................... 71 CHAPTER THREE: ASSESSMENT OF MARKING TECHNIQUES FOR THE PURPOSE OF MONITORING PHYTOSEIID RELEASES ............................................................................... 87 Abstract ......................................................................................................................................... 87 Introduction ................................................................................................................................... 87 Materials and Methods .................................................................................................................. 89 Results and Discussion ................................................................................................................. 92 References Cited ........................................................................................................................... 95 CHAPTER FOUR: PHYTOSEIIDS IN WASHINGTON COMMERCIAL APPLE ORCHARDS: BIODIVERSITY AND FACTORS AFFECTING ABUNDANCE ................... 101 Abstract ....................................................................................................................................... 101 Introduction ................................................................................................................................. 102 Materials and Methods ...............................................................................................................