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The Pennsylvania State University The Graduate School Department of Entomology ECOLOGICAL TRADE-OFFS ASSOCIATED WITH INSECTICIDE USE, FROM PENNSYLVANIA TO BANGLADESH A Dissertation in Entomology and International Agriculture & Development by Margaret R. Douglas © 2016 Margaret R. Douglas Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy August 2016 The dissertation of Margaret R. Douglas was reviewed and approved* by the following: Dr. John Tooker Associate Professor of Entomology & Extension Specialist Dissertation Advisor Chair of Committee Dr. Mary Barbercheck Professor of Entomology Dr. Christopher Mullin Professor of Entomology Dr. Armen Kemanian Associate Professor of Production Systems and Modeling Dr. Gary Felton Professor of Entomology Head of the Department of Entomology *Signatures are on file in the Graduate School iii ABSTRACT Integrated Pest Management (IPM) requires an understanding of the interaction between chemical and biological control tactics. In recent decades, seed treatment with neonicotinoids has become increasingly widespread in field crop production, but the full ecological and agronomic effects of these insecticides are still far from understood. This dissertation helps to fill this knowledge gap by describing the use of neonicotinoid seed treatments in U.S. agriculture, and examining the influence of these insecticides on pest and predatory invertebrates. In Chapter 1, I synthesized data from various government sources and pesticide use labels to estimate the national use of seed-applied neonicotinoids in the United States. In Chapters 2 and 3, I used laboratory and field studies together with insecticide residue testing to explore the movement of seed-applied neonicotinoids through a crop-slug-beetle food chain and its agronomic consequences in Pennsylvania no-till soybean and corn systems. I found that seed-applied neonicotinoids variably disrupt biological control of non-target pest slugs. Furthermore, field-collected slugs, earthworms, and caterpillars contained concentrations of neonicotinoids likely to harm predatory arthropods that consume them. In Chapter 4, I tested the generality of the effects of neonicotinoid seed treatments on arthropod natural enemies through a meta- analysis of field studies. By assembling almost 1,000 observations from North American and European experiments, I found that seed-applied neonicotinoids have a negative effect on insect natural enemies corresponding to a roughly 16% seasonal reduction in abundance. Taken together, my results shed light on the agro-ecological effects of iv neonicotinoid seed treatments and inform their targeted use. Finally, Chapter 5 comprised the international component of my dissertation. In a lablab bean production system in Bangladesh, I tested the hypothesis that biorational pesticides can replace broad-spectrum synthetic insecticides in insect pest management. Additionally, I used DNA barcoding to characterize emerging thrips pests and determine whether they need to be incorporated into lablab bean IPM programs. Biorational pesticides were variably effective against lablab bean insect pests, and my preliminary evidence suggests that flower thrips (mainly Megalurothrips spp.) pose a significant threat to lablab bean production and should be included in insect control efforts in this crop. v TABLE OF CONTENTS LIST OF FIGURES ..................................................................................................... ix LIST OF TABLES ....................................................................................................... xiv PREFACE .................................................................................................................... xvii ACKNOWLEDGEMENTS ......................................................................................... xviii Introduction .................................................................................................................. 1 Dissertation objectives .......................................................................................... 2 Chapter 1 Large-scale deployment of seed treatments has driven rapid increase in use of neonicotinoid insecticides and preemptive pest management in U.S. field crops ............................................................................................................. 5 Abstract ................................................................................................................. 5 Introduction ........................................................................................................... 6 Materials & Methods ............................................................................................ 10 Pesticide data sources .................................................................................... 10 Seed treatments as a proportion of neonicotinoid use in major U.S. row crops ....................................................................................................... 12 Proportion of U.S. maize and soybean area planted with neonicotinoid- treated seeds ........................................................................................... 13 Neonicotinoid seed treatments in U.S. maize and soybean pest management ........................................................................................... 15 Results ................................................................................................................... 15 Neonicotinoid use in the U.S. by product type, crop, and active ingredient ................................................................................................ 15 Neonicotinoids applied as seed treatments in major U.S. row crops ............ 16 Hectares planted with neonicotinoid-treated seed in major U.S. row crops ....................................................................................................... 17 Neonicotinoid seed treatments and pest management trends in U.S. maize and soybeans ................................................................................ 19 Discussion ............................................................................................................. 22 Acknowledgements ............................................................................................... 29 Tables .................................................................................................................... 30 Figures .................................................................................................................. 39 vi Chapter 2 Neonicotinoid insecticide travels through a soil food chain, disrupting biological control of non-target pests and decreasing soybean yield ................... 41 Abstract ................................................................................................................. 41 Introduction ........................................................................................................... 42 Materials & Methods ............................................................................................ 45 Laboratory experiments ................................................................................. 45 Field experiment ............................................................................................ 48 Insecticide analyses ....................................................................................... 50 Statistical analyses ......................................................................................... 51 Results ................................................................................................................... 54 Laboratory experiments ................................................................................. 54 Field experiment ............................................................................................ 55 Insecticide residues ........................................................................................ 57 Discussion ............................................................................................................. 58 Acknowledgements ............................................................................................... 63 Data accessibility .................................................................................................. 64 Tables .................................................................................................................... 65 Figures .................................................................................................................. 69 Chapter 3 Neonicotinoid seed treatments move through a no-till corn food web but fail to influence biological control or yield .................................................... 78 Abstract ................................................................................................................. 78 Introduction ........................................................................................................... 79 Materials & Methods ............................................................................................ 82 Laboratory experiments ................................................................................. 82 Field experiments .......................................................................................... 85 Insecticide analyses ....................................................................................... 88 Statistical