University of Pennsylvania ScholarlyCommons Master of Environmental Studies Capstone Department of Earth and Environmental Projects Science 12-2012 The Producer-Pollinator Dilemma: Neonicotinoids and Honeybee Colony Collapse Benjamin W. Reynard Follow this and additional works at: https://repository.upenn.edu/mes_capstones Reynard, Benjamin W., "The Producer-Pollinator Dilemma: Neonicotinoids and Honeybee Colony Collapse" (2012). Master of Environmental Studies Capstone Projects. 50. https://repository.upenn.edu/mes_capstones/50 This paper is posted at ScholarlyCommons. https://repository.upenn.edu/mes_capstones/50 For more information, please contact [email protected]. The Producer-Pollinator Dilemma: Neonicotinoids and Honeybee Colony Collapse Abstract Neonicotinoid insecticides are the most important new insecticide class introduced in the past 40 years. They are the number one selling insecticide in the world, and are used on over 90% of the corn produced in the U.S. However, neonicotinoids could very likely be causing widespread and severe impairment to bee colonies, and possibly contributing to Colony Collapse Disorder (CCD). This is problematic since bees, and honey bees in particular, are the single most important pollinator for global agriculture. Pollination services contribute to one of every three mouthfuls of food consumed (Xerces Society, 2011). Direct pollination services were recently valued in a Cornell University study to be worth 16 billion dollars a year in U.S. farm income (Calderone, 2012). As more is learned about the nature of systemic neonicotinoids and their adverse effects on beneficial pollinators, a potential conflict between crop protection and pollinator conservation becomes clear, posing a dilemma between food production required to feed a growing global population and the risk of widespread colony collapses. The scientific community has been examining the phenomenon of CCD, and anecdotal links between the bee losses and the application of neonicotinoid insecticides, since it was first noticed by French beekeepers in 1994 and then in the U.S. in 2006. While previous studies failed to demonstrate links to CCD, a new generation of field-realistic studies has chronicled the synergistic and sublethal effects of neonicotinoids on individual bees and colonies over longerterm exposure using real-world foraging conditions. Recent studies strongly support the link between neonicotinoids and CCD (Henry et al., 2012; Whitehorn et al., 2012; Gill, Ramos- Rodriguez, and Raine, 2012; Lu et al., 2012; Tapparo et al., 2012; Krupke et al., 2012). However, independent researchers such as James Cresswell, Jim Frazier, and USDA scientist Jeffrey Pettis (Cresswell, 2011; Cresswell, Desneux, and vanEngelsdorp, 2012; Frazier et al., 2011; Frazier 2012; Grist.org) along with farming and crop protection interests and the producers of the neonicotinoid products all caution that there is not yet enough evidence to draw definitive conclusions, and that there are a variety of causal factors behind CCD. Can these pesticides continue to be used safely in the U.S. or do their risks to pollinators outweigh their benefits ot humans and animals? This presentation is available at ScholarlyCommons: https://repository.upenn.edu/mes_capstones/50 THE PRODUCER-POLLINATOR DILEMMA: NEONICOTINOIDS AND HONEYBEE COLONY COLLAPSE Benjamin W. Reynard December 2012 Sarah A. Willig, PhD Robert F. Giegengack, PhD DEDICATION To my mom for her brilliance, guidance, inspiration, and love. Thank You. ii ACKNOWLEDGMENTS Many thanks to Dr. Sarah Willig and Dr. Robert Giegengack for their direction, wisdom, and patience throughout the writing process. Special thanks to Dr. Yvette Bordeaux, Willistown Conservation Trust, Rushton Sustainable Farm, Lisa Kiziuk, Fred de Long, Noah Gress, Joannah Whitnah, Blake Goll, William Hartman, and Bonnie Van Alen for helping me develop my knowledge and appreciation of sustainable agriculture and land conservation. Thank you to Sam Droege, Stephanie Wilson, Sue Costello, and Dr. Tatyana Livshultz for lending their time, expertise, and advice in support of my bee studies. Also, thanks to Jeffrey Johnson and Dr. Barry Baysinger for their encouragement and support. iii ABSTRACT THE PRODUCER-POLLINATOR DILEMMA: NEONICOTINOIDS AND HONEYBEE COLONY COLLAPSE Benjamin Reynard Sarah Willig, Ph.D. Robert Giegengack, Ph.D. Neonicotinoid insecticides are the most important new insecticide class introduced in the past 40 years. They are the number one selling insecticide in the world, and are used on over 90% of the corn produced in the U.S. However, neonicotinoids could very likely be causing widespread and severe impairment to bee colonies, and possibly contributing to Colony Collapse Disorder (CCD). This is problematic since bees, and honey bees in particular, are the single most important pollinator for global agriculture. Pollination services contribute to one of every three mouthfuls of food consumed (Xerces Society, 2011). Direct pollination services were recently valued in a Cornell University study to be worth 16 billion dollars a year in U.S. farm income (Calderone, 2012). As more is learned about the nature of systemic neonicotinoids and their adverse effects on beneficial pollinators, a potential conflict between crop protection and pollinator conservation becomes clear, posing a dilemma between food production required to feed a growing global population and the risk of widespread colony collapses. The scientific community has been examining the phenomenon of CCD, and anecdotal links between the bee losses and the application of neonicotinoid insecticides, since it was first noticed by French beekeepers in 1994 and then in the U.S. in 2006. While previous studies failed to demonstrate links to CCD, a new generation of field-realistic studies has chronicled the synergistic and sublethal effects of neonicotinoids on individual bees and colonies over longer- term exposure using real-world foraging conditions. Recent studies strongly support the link between neonicotinoids and CCD (Henry et al., 2012; Whitehorn et al., 2012; Gill, Ramos-Rodriguez, and Raine, 2012; Lu et al., 2012; Tapparo et al., 2012; Krupke et al., 2012). However, independent researchers such as James Cresswell, Jim Frazier, and USDA scientist Jeffrey Pettis (Cresswell, 2011; Cresswell, Desneux, and vanEngelsdorp, 2012; Frazier et al., 2011; Frazier 2012; Grist.org) along with farming and crop protection interests and the producers of the neonicotinoid products all caution that there is not yet enough evidence to draw definitive conclusions, and that there are a variety of causal factors behind CCD. Can these pesticides continue to be used safely in the U.S. or do their risks to pollinators outweigh their benefits to humans and animals? iv TABLE OF CONTENTS Dedication ii Acknowledgments iii Abstract iv List of Tables vi List of Figures vii Introduction 1 A Green Revolution 3 An Agricultural Necessity for Feeding the World 5 Pesticide Overview 8 Major Pesticide Classes Over Time 13 Botanical 13 Inorganic 15 Organochlorines 16 Organophosphates 18 Carbamates 20 Synthetic Pyrethroids 21 Resistance and Cross-Resistance 24 Pesticide Treadmill 25 Pesticide Summary as of 1990 (Pre-Neonicotinoids) 27 Development and Spread of Neonicotinoids 29 A New Mode of Action Based on a Natural Compound 29 Neonicotinoid Types 34 The Versatility and Spread of Neonicotinoids 40 Market and Economic Success 43 Persistence in Nature 47 Ecotoxicology 47 Soils 49 Water 50 Plants 51 Metabolism 51 Unintended Consequences for Pollinators 52 Possible Links to Colony Collapse Disorder 60 Concern for Beekeepers 60 Complex Interactions 61 Realistic Field Studies 64 Neonicotinoid Regulation in the U.S. and Europe 68 European Restrictions 69 U.S. Conditional Registration and Regulation 71 Conclusions: Weighing Evidence and Measuring Risks 83 Appendix of Tables and Figures 97 Works Cited 107 v LIST OF TABLES Table 1. 2007 EPA Market Estimate for Pesticide Sales and Usage 8 Table 2. Neonicotinoid Heterocyclic Subclasses 35 Table 3. Neonicotinoid Pharmacophore Subclasses 37 Table 4. Neonicotinoid Chart 39 Table 5. Neonicotinoid Applications 41 Table 6. 2008 Top Ten Agrochemicals in terms of Global Sales 43 Table 7. Relative Toxicity of Nicotine and Imidacloprid 47 Table 8. Neonicotinoid Half-life in Soils 49 Table 9. Mass Balance of Imidacloprid in soil leaching Experiments 50 Table 10. Neonicotinoid Toxicity to Bees 53 Table 11. Results of field realistic dose and long-term exposure study 66 Table 12. Total 2006 U.S beekeeper losses 73 Table 13. Some major pesticides used over time 97 Table 14. Neonicotinoid synergy with common DMI-fungicides 99 Table 15. Major products and companies in the neonicotinoid market 100 Table 16. Neonicotinoid crop use patterns in the U.S. 106 vi LIST OF FIGURES Figure 1. Dr. Norman Borlaug 3 Figure 2. 2012 Global Hunger Index 6 Figure 3. 1991 Insecticide Market by Mode of Action 27 Figure 4. Development of insecticide classes, 1990 to 2008 28 Figure 5. Synthesis of Nithiazine and structural similarity to Nicotine 29 Figure 6. Synthesis of Nithiazine, Intermediate Prototype, Imidacloprid 31 Figure 7. Structural Elements of Neonicotinoids 33 Figure 8. Substitutions leading to Second Generation Thiamethoxam 36 Figure 9. Three Generations of Neonicotinoids and Lead Compounds 38 Figure 10. Development of seed treatment from 1990 to 2008 42 Figure 11. Neonicotinoid Seed & Sapling 9 and 21 Days After Planting 45 Figure 12. Partial Positive Charge of Nicotinoids