NATURAL ENEMY ABUNDANCE AND BIOLOGICAL CONTROL IN BT MAIZE USING SIMULATIONS OF PREDATOR-PREY INTERACTIONS by Christopher Regan Brown A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Ecology and Environmental Sciences MONTANA STATE UNIVERSITY Bozeman, Montana July 2017 ©COPYRIGHT by Christopher Regan Brown 2017 All Rights Reserved ii DEDICATION The spirit of adventure that led to this undertaking and the perseverance to get through the tough times are credited to the inspiration of Ryan Brown. iii ACKNOWLEDGMENTS I give my sincere thanks to my parents who started me on this path and always gave me freedom to pursue my interests however unconventional they may have been; my wife, Jessica, who has been the backbone of our family over the last four years and has inspired me by her own experiences during this time, which have been as profound as my own; my kids, Mason, Avery, and Summer, who have been a great motivation for me to “do my best” but also provided welcome distractions from this effort; my advisor, Dr. Bob Peterson, for his support, insights, and, not least, for putting the “philosophy” into my PhD; my lab mates, Claire Donahoo, Alyssa Piccolomini, Collin Preftakes, and Shavonn Whitten for friendship, support, and great discussions; my committee members, Laura Burkle, David Weaver, Paul Stoy, and Jeff Wolt, for their time, support, and technical advice; Jeff Wolt for giving the initial idea that led to my project; my computer savvy colleagues, Geoffrey Caron-Lormier, Adam Schapaugh, Joao Rossi, Daniel Salinas Duron, and Chris Sehy for sharing their vast technical skills with me; and, lastly, Monsanto company that made it all possible, in particular, Tracey Reynolds and Michael Horak, and other Monsanto colleagues who helped along the way, including Aqeel Ahmad, Dave Carson, Peter Jensen, and Roger Effertz. iv TABLE OF CONTENTS 1. INTRODUCTION ........................................................................................................... 1 Natural Enemies, Biological Control, and Integrated Pest Management ........................ 4 Current Understanding of Potential Effects of Bt Crops on Arthropod Communities ................................................................................................................. 11 Bt Proteins ............................................................................................................. 11 Exposure of Natural Enemies to Bt Proteins ........................................................ 11 Lab and Greenhouse Studies ................................................................................. 12 Field Biodiversity and Arthropod Abundance Field Studies ................................ 14 Off-field Non-target Effects .................................................................................. 16 Meta-analyses ....................................................................................................... 16 Long Term, Landscape Effects ............................................................................. 19 Computer Simulation Models to Evaluate Non-target Organism Effects from Bt Crops ....................................................................................................... 22 Objectives ...................................................................................................................... 24 References Cited ........................................................................................................... 27 2. SIMULATING INTERACTIONS BETWEEN NATURAL ENEMIES AND PESTS IN MAIZE TO ASSESS THE INFLUENCE OF ALTERNATIVE FOOD, CANNIBALISM, AND INTRAGUILD PREDATION ................................................................................................................. 51 Abstract ......................................................................................................................... 54 Introduction ................................................................................................................... 55 Methods ......................................................................................................................... 61 Results ........................................................................................................................... 71 Discussion ..................................................................................................................... 77 Acknowledgments ......................................................................................................... 81 References Cited ........................................................................................................... 96 v TABLE OF CONTENTS (CONTINUED) 3. SIMULATING INTERACTIONS BETWEEN NATURAL ENEMIES AND PREY IN BT AND CONVENTIONAL MAIZE .............................................. 103 Abstract ....................................................................................................................... 106 Introduction ................................................................................................................. 107 Methods ....................................................................................................................... 111 Results ......................................................................................................................... 122 Discussion ................................................................................................................... 125 Acknowledgments ....................................................................................................... 127 References Cited ......................................................................................................... 133 APPENDICES .................................................................................................................. 139 CHAPTER 2 SUPPORTING INFORMATION ....................................................... 140 References Cited ....................................................................................................... 150 CHAPTER 3 SUPPORTING INFORMATION ....................................................... 153 ADDITIONAL INFORMATION GATHERED IN SUPPORT OF THE PROJECT ......................................................................................................... 158 References Cited ....................................................................................................... 173 COMPLETE REFERENCES CITED .............................................................................. 174 vi LIST OF TABLES Table Page 2.1. Model input file descriptions ............................................................................ 83 2.2. Modifications made to the TrophicLINK model for this project...................... 84 2.3. Key parameter values and growth and development outcomes under ideal conditions for the ECB, lady beetle, and lacewing trophic functional types ................................................................................................ 85 2.4. Mean peak mass of the herbivore and natural enemy trophic functional types from each scenario ................................................................. 86 3.1. Key parameter values and growth and development outcomes under ideal conditions for the ECB, lady beetle, and lacewing trophic functional types .................................................................................. 129 3.2. Mean peak mass of the herbivore and natural enemy trophic functional types from each scenario ............................................................... 130 A.1. Initial traits input file parameter descriptions ................................................ 141 A.2. Maize trait parameter values .......................................................................... 143 A.3. Aphid “super” individual trophic functional type individual trait parameter values ........................................................................................... 144 A.4. European corn borer trophic functional type trait parameter values .............. 145 A.5. Lady beetle trophic functional type trait parameter values ............................ 146 A.6. Lacewing trophic functional type trait parameter values ............................... 147 A.7. Invertebrate efficiency of conversion of ingested food rates when feeding for the different trophic functional type feeding combinations .................................................................................................. 148 A.8. Food preference tier values for the different trophic functional type feeding combinations .............................................................................. 149 B.1. Maize yield across scenarios .......................................................................... 154 vii LIST OF TABLES (CONTINUED) Table Page C.1. Initial traits input file key ............................................................................... 160 C.2. Complete list of modifications made to TrophicLINK to enable current project ................................................................................................. 165 C.3. Life history measurements of European corn borer, Ostrinia nubilalis, reared at 25 ºC ................................................................................................ 167 C.4. Developmental measurements of European corn borer, Ostrinia nubilalis, reared at 25 ºC ................................................................... 168 C.5. Life history measurements of fall armyworm, Spodoptera frugiperda, reared at 25 ºC ................................................................................................ 169 C.6. Developmental measurements of fall armyworm, Spodoptera frugiperda, reared at 25 ºC .......................................................... 170 C.7. Life history measurements of four species of lady beetles (Coleoptera: Coccinellidae) ............................................................................ 171 C.8. Late instar, pupal, and adult weight measurements of the cabbage white butterfly, Pieris rapae (Lepidoptera: Pieridae) ..................................... 172 viii LIST OF FIGURES Figure Page 2.1. Flow diagram of the model. .............................................................................. 87 2.2. Maize yield variability depending on simulation number. ............................... 88 2.3. Variability of a) aphid, b) European corn borer, c) lady beetle, d) lacewing trophic functional type mass (g) over time with data combined from 20 simulations of a 120-day season. ....................................... 89 2.4. Effects of varying daily pollen degradation rates on pollen amounts over time ........................................................................................................... 90 2.5. Invertebrate trophic type mass across the season with foraging radius values varied for a) lady beetle and b) lacewing and resulting prey mass of c) aphids and d) European corn borer. ........................................ 91 2.6. Invertebrate trophic type mass across the season for each scenario for a) aphid, b) European corn borer, c) lady beetle, and d) lacewing. ............ 92 2.7. The amount of maize plant consumed by the herbivore trophic types, European corn borer (ECB) and aphid for different TrophicLINK simulations. ....................................................................................................... 93 2.8. Amount of food consumed in each trophic interaction combination................ 94 2.9. Maize yield across scenarios............................................................................. 95 3.1. Herbivore trophic functional type mass across the season for each scenario for a) aphid, b) European corn borer with high infestation, and c) European corn borer with low infestation. ................................................. 131 3.2. Natural enemy trophic functional type mass across the season for each scenario for a) lady beetle and b) lacewing. ........................................... 132 B.1. Amount of plant consumed by the aphid (left) and European corn borer (right) trophic functional type. .............................................................. 155 B.2. Amount of pollen and aphid (top) and ECB (bottom) consumed by the natural enemy trophic functional types. ................................................... 156 ix LIST OF FIGURES (CONTINUED) Figure Page B.3. Amount of food consumption through cannibalism and intraguild predation within the natural enemy trophic functional types. ........................ 157