THE IMPACT OF GENETICALLY ENGINEERED CROPS ON FARM SUSTAINABILITY IN THE UNITED STATES

Committee on the Impact of Biotechnology on Farm-Level Economics and Sustainability

Board on Agriculture and Natural Resources

Division on Earth and Life Studies

NATIONAL RESEARCH COUNCIL
OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS

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Committee on the Impact of Biotechnology on Farm-Level Economics and Sustainability Board on Agriculture and Natural Resources Division on Earth and Life Studies

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, N.W. Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Gov- erning Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engi- neering, and the Institute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance. This study was funded by the National Academies. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the views of the organizations or agencies that provided support for the project. I nternational Standard Book Number-13: 978-0-309-14708-8 (Book) International Standard Book Number-10: 0-309-14708-5 (Book) I nternational Standard Book Number-13: 978-0-309-14709-5 (PDF) International Standard Book Number-10: 0-309-14709-3 (PDF) Library of Congress Control Number: 2010927922 Additional copies of this report are available from the National Academies Press, 500 Fifth Street, NW, Lockbox 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu. Suggested Citation: National Research Council. 2010. The Impact of Genetically Engineered Crops on Farm Sustainability in the United States. Washington, DC: National Academies Press. Copyright 2010 by the National Academy of Sciences. All rights reserved. Printed in the United States of America.

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal govern - ment on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its mem - bers, sharing with the National Academy of Sciences the responsibility for advis - ing the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the fed - eral government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government, the public, and the scientific and engineer- ing communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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COMMITTEE ON THE IMPACT OF BIOTECHNOLOGY ON FARM-LEVEL ECONOMICS AND SUSTAINABILITY DAVID E. ERVIN (Chair), Portland State University, Oregon YVES CARRIÈRE, University of Arizona, Tucson WILLIAM J. COX, Cornell University, Ithaca, New York JORGE FERNANDEZ-CORNEJO, Economic Research Service, U.S. Department of Agriculture, Washington, DC1 RAYMOND A. JUSSAUME, JR., Washington State University, Pullman MICHELE C. MARRA, North Carolina State University, Raleigh MICHEAL D.K. OWEN, Iowa State University, Ames PETER H. RAVEN, Missouri Botanical Garden, St. Louis L. LAREESA WOLFENBARGER, University of Nebraska, Omaha DAVID ZILBERMAN, University of California, Berkeley Project Staff KARA N. LANEY, Study Director KAMWETI MUTU, Research Associate ROBIN A. SCHOEN, Director, Board on Agriculture and Natural Resources KAREN L. IMHOF, Administrative Assistant NORMAN GROSSBLATT, Senior Editor 1 The views expressed here are those of the authors and may not be attributed to the Eco - nomic Research Service or the U.S. Department of Agriculture. 

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BOARD ON AGRICULTURE AND NATURAL RESOURCES NORMAN R. SCOTT (Chair), Cornell University, Ithaca, New York PEGGY F. BARLETT, Emory University, Atlanta, Georgia HAROLD L. BERGMANN, University of Wyoming, Laramie RICHARD A. DIXON, Samuel Roberts Noble Foundation, Ardmore, Oklahoma DANIEL M. DOOLEY, University of California, Oakland JOAN H. EISEMANN, North Carolina State University, Raleigh GARY F. HARTNELL, Monsanto Company, St. Louis, Missouri GENE HUGOSON, Minnesota Department of Agriculture, St. Paul KIRK C. KLASING, University of California, Davis VICTOR L. LECHTENBERG, Purdue University, West Lafayette, Indiana PHILIP E. NELSON, Purdue University, West Lafayette, Indiana KEITH PITTS, Marrone Bio Innovations, Davis, California CHARLES W. RICE, Kansas State University, Manhattan HAL SALWASSER, Oregon State University, Corvallis PEDRO A. SANCHEZ, The Earth Institute, Columbia University, Palisades, New York ROGER A. SEDJO, Resources for the Future, Washington, DC KATHLEEN SEGERSON, University of Connecticut, Storrs MERCEDES VAZQUEZ-AÑON, Novus International, Inc., St. Charles, Missouri Staff ROBIN A. SCHOEN, Director KAREN L. IMHOF, Administrative Assistant AUSTIN J. LEWIS, Senior Program Officer EVONNE P.Y. TANG, Senior Program Officer PEGGY TSAI, Program Officer CAMILLA YANDOC ABLES, Associate Program Officer KARA N. LANEY, Associate Program Officer RUTH S. ARIETI, Research Associate JANET M. MULLIGAN, Research Associate KAMWETI MUTU, Research Associate ERIN P. MULCAHY, Senior Program Assistant i

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Preface Not since the introduction of hybrid corn seed have we witnessed such a sweeping technological change in U.S. agriculture. Hundreds of thousands of farmers have adopted the first generation of genetically engineered (GE) crops since their commercialization in 1996. Although not all GE varieties that have been commercialized have succeeded, those targeted at improved pest control now cover over 80 percent of the acres planted to soybean, cotton, and corn—that is, almost half of U.S. crop - land. Forecasts suggest an expansion in GE-crop plantings in many other countries. GE crops originate in advances in molecular and cellular biology that enable scientists to introduce desirable traits from other species into crop plants or to alter crop plants’ genomes internally. Those powerful scientific techniques have dramatically expanded the boundaries that have constrained traditional plant breeding. A new technology adopted so widely and rapidly has substantial economic, social, and environmen - tal impacts on farms and their operators. Inevitably, both advantages and risks or losses emerge from such massive changes. The National Research Council has conducted multiple studies of specific aspects of GE crops, such as regulatory-system adequacy and food safety. However, the assigned tasks restricted the scope of their reports. As pressure mounts to expand the use of GE crops for energy, food security, environmental improvement, and other purposes, the scope and intensity of impacts will grow. Now is an opportune time to take a comprehensive look at the track record of GE crops and to identify the opportunities and challenges loom- ii

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iii PREFACE ing on the horizon. The National Research Council therefore supported the Committee on the Impact of Biotechnology on Farm-Level Economics and Sustainability to investigate this topic. Despite the rapid spread of GE crops in U.S. agriculture, the technol - ogy continues to stir controversy around scientific issues and ideological viewpoints. The committee focused on the scientific questions associated with the farm-level impacts of the adoption of genetic-engineering tech - nology and refrained from analyzing ideological positions, either pro or con. The committee adopted an “evidentiary” standard of using peer- reviewed literature on which to form our conclusions and recommenda- tions. It is my hope that the report will give readers a firm grasp of the state of evidence or lack thereof on the scientific issues. True to its charge, the committee adopted a sustainability frame- work that required an evaluation of environmental, economic, and social impacts of GE crops. Those three dimensions constitute the essential pillars of sustainability science. The summary and opening and closing chapters bring together the three perspectives for a fuller view of the technology’s impact. Given the controversies, readers will want to know the committee’s composition and how it conducted its work in arriving at conclusions and recommendations. The biographies in Appendix C show a group of highly accomplished natural and social scientists who possess a broad array of research experience and perspectives on GE crops. That diversity of disciplines and expertise proved beneficial in introducing checks and balances in evaluating information from many angles. The committee members divided into teams to work on the various sections of the report on the basis of the members’ expertise. The drafts by each team were reviewed by the full committee to ensure that everyone had a chance to comment on and improve and approve each section. I was continually impressed with the members’ dedication to a hard-nosed and impartial evaluation of the best science on GE crops. Equally important, they kept open minds in considering new evidence presented by their colleagues and external experts. The result was a model multidisciplinary research process in which each of us learned from the others and improved the report quality. In closing, I want to express my deep appreciation to the committee members for their tireless work and good humor in completing such a challenging task while working full time at their regular jobs. Their com- mitment and professionalism exemplify the best of public science. Each member made significant contributions to the final report. The commit - tee also benefited from the testimony of several experts in the field and from the numerous comments of many conscientious external reviewers.

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ix PREFACE Finally, the quality of the report would not have been attained without excellent support and substantive input by study director Kara Laney, the valuable assistance of Kamweti Mutu, the insightful counsel of Robin Schoen, and the editorial work of the National Research Council. David E. Ervin, Chair Committee on the Impact of Biotechnology on Farm-Level Economics and Sustainability

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Acknowledgments T his report has been reviewed in draft form by persons chosen for their diverse perspectives and technical expertise in accordance with procedures approved by the National Research Council Report Review Committee. The purpose of the independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards of objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberative process. We wish to thank the following individuals for their review of the report: David A. Andow, University of Minnesota, St. Paul Charles M. Benbrook, The Organic Center, Enterprise, Oregon Lawrence Busch, Michigan State University, East Lansing Stephen O. Duke, Agricultural Research Service, U.S. Department of Agriculture, University, Mississippi Robert T. Fraley, Monsanto Company, St. Louis, Missouri Dermot J. Hayes, Iowa State University, Ames Molly Jahn, University of Wisconsin, Madison Nicholas Kalaitzandonakes, University of Missouri, Columbia Peter M. Kareiva, The Nature Conservancy, Seattle, Washington Michelle A. Marvier, Santa Clara University, California Paul D. Mitchell, University of Wisconsin, Madison xi

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xii ACKNOWLEDGMENTS George E. Seidel, Colorado State University, Fort Collins Greg Traxler, The Bill & Melinda Gates Foundation, Seattle, Washington Although the reviewers listed above have provided many construc- tive comments and suggestions, they were not asked to endorse the con- clusions or recommendations, nor did they see the final draft of the report before its release. The review of the report was overseen by Drs. Alan G. McHughen, University of California, Riverside, and May R. Berenbaum, University of Illinois, Urbana-Champaign. Appointed by the National Research Council, they were responsible for making certain that an inde- pendent examination of the report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of the report rests with the authoring committee and the institution.

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Contents ABBREVIATIONS AND ACRONYMS xix SUMMARY 1 1 INTRODUCTION 19 Committee Charge and Approach, 21 Study Framework, 24 Genetically Engineered Traits in Crops, 28 Adoption and Distribution of Genetically Engineered Crops, 30 Deterrents to Genetically Engineered Trait Development in Other Crops, 47 From Adoption to Impact, 50 Conclusion, 52 References, 52 2 ENVIRONMENTAL IMPACTS OF GENETICALLY ENGINEERED CROPS AT THE FARM LEVEL 59 Environmental Impacts of Herbicide-Resistant Crops, 60 Environmental Impacts of Insect-Resistant Crops, 83 Gene Flow and Genetically Engineered Crops, 104 Conclusions, 111 References, 112 xiii

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xi CONTENTS 3 FARM-LEVEL ECONOMIC IMPACTS 135 Economic Impacts on Adopters of Genetically Engineered Crops, 135 Economic Impacts on Other Producers, 164 Socioeconomic Impacts of Gene Flow, 169 Conclusions, 174 References, 175 4 FARM-SYSTEM DYNAMICS AND SOCIAL IMPACTS OF GENETIC ENGINEERING 187 Social Impacts of On-Farm Technology Adoption, 188 Social Networks and Adoption Decisions, 191 Interaction of the Structure of the Seed Industry and Farmer Decisions, 192 Social and Information Networks Between Farmers and Industry, 199 Interaction of Legal and Social Issues Surrounding Genetic Engineering, 203 Conclusions, 206 References, 207 5 KEY FINDINGS, REMAINING CHALLENGES, AND FUTURE OPPORTUNITIES 213 Key Findings, 214 Remaining Challenges Facing Genetically Engineered Crops, 216 Future Applications of Genetically Engineered Crops, 219 Research Priorities Related to Genetically Engineered Crops, 227 Advancing Potential Benefits of Genetically Engineered Crops by Strengthening Cooperation Between Public and Private Research and Development, 229 References, 232 APPENDIXES A Herbicide Selection 237 B Tillage Systems 245 C Biographical Sketches of Committee Members 247

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List of Tables, Figures, and Boxes TABLES 1-1 Percentage of Soybean Acres in Genetically Engineered Soybean Varieties, by State and United States, 2000–2009, 36 1-2 Insect Pests of Corn Targeted by Bt Varieties, 37 1-3 Percentage of Corn Acres in Genetically Engineered Corn Variet- ies, by State and United States, 2000–2009, 38 1-4 Insect Pests of Cotton Targeted by Bt Varieties, 42 1-5 Percentage of Cotton Acres in Genetically Engineered Upland Cotton Varieties, by State and United States, 2000–2009, 44 1-6 National Soybean Survey Descriptive Statistics by Adoption Cat - egory, 47 2-1 Weeds That Evolved Resistance to Glyphosate in Glyphosate- Resistant Crops in the United States, 74 2-2 Weeds Reported to Have Increased in Abundance in Glyphosate- Resistant Crops, 76 2-3 Regional Effects of Deployment of Bt Crops on Population Dynamics of Major Pests of Corn and Cotton, 88 3-1 Summary of Farm-Level Impact Evidence for Genetically Engi- neered Cotton in the United States, 1996–1999, 152 3-2 Fuel Consumption by Tillage System, 153 3-3 Value and Relative Importance of Nonpecuniary Benefits to Farmers, 156 x

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xi TABLES, FIGURES, AND BOXES 3-4 Effect of Global Adoption of Genetically Engineered Crops on Commodity Prices, 160 3-5 Adoption of Genetically Engineered Crops and Their Distribu- tion, 161 4-1 Estimated Seed Sales and Shares for Major Field Crops, United States, 1997, 195 4-2 Four-Firm Concentration Ratio in Field-Release Approvals from USDA Animal and Plant Health Inspection Service, by Crop, 1990–2000, 196 FIGURES S-1 Application of herbicide to soybean and percentage of acres of herbicide-resistant soybean, 4 S-2 Application of herbicide to cotton and percentage of acres of herbicide-resistant cotton, 5 S-3 Application of herbicide to corn and percentage of herbicide- resistant corn, 6 S-4 Pounds of active ingredient of insecticide applied per planted acre and percent acres of Bt corn, respectively, 7 S-5 Pounds of active ingredient of insecticide applied per planted acre and percent acres of Bt cotton, respectively, 8 1-1 Genetically engineered crop adoption and impact framework, 28 1-2 Share of major crops in total pesticide expenditures, 1998–2007, 31 1-3 Nationwide acreage of genetically engineered soybean, corn, and cotton as a percentage of all acreage of these crops, 32 1-4 Herbicide-resistant soybean acreage trends nationwide, 36 1-5 Genetically engineered corn acreage trends nationwide, 40 1-6 Genetically engineered cotton acreage trends nationwide, 42 2-1 Application of herbicide to soybean and percentage of acres of herbicide-resistant soybean, 62 2-2 Application of herbicide to cotton and percentage of acres of herbicide-resistant cotton, 63 2-3 Application of herbicide to corn and percentage of herbicide- resistant corn, 64 2-4 Trends in conservation tillage practices and no-till for soybean, cotton, and corn, and adoption of herbicide-resistant crops since their introduction in 1996, 65

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xii TABLES, FIGURES, AND BOXES 2-5 Soybean acreage under conventional tillage, conservation tillage, and no-till, 1997, 67 2-6 Number of weeds with evolved glyphosate resistance, 78 2-7 Pounds of active ingredient of insecticide applied per planted acre and percent acres of Bt corn, 84 2-8 Pounds of active ingredient of insecticide applied per planted acre and percent acres of Bt cotton, 85 2-9 Cumulative number of cotton pests evolving resistance to Bt cot - ton and DDT in the years after these management tools became widely used in the United States, 98 3-1 Seed-price index and overall index of prices paid by U.S. farmers, 147 3-2 Estimated average seed costs for U.S. farmers in real (inflation- adjusted) terms, 147 3-3 Real (inflation-adjusted) cotton seed prices paid by U.S. farmers, 2001–2007, 148 3-4 Real (inflation-adjusted) corn seed prices paid by U.S. farmers, 2001–2008, 148 3-5 Real (inflation-adjusted) soybean seed price paid by U.S. farmers, 2001-2008, 149 3-6 U.S. corn use, 165 3-7 U.S. soybean use, 165 4-1 Public and private research expenditures on plant breeding, 194 4-2 Share of planted acres of corn and soybean seeds by largest four firms (CR4), 195 4-3 Evolution of Pioneer Hi-Bred International, Inc./E.I. DuPont de Nemours and Company, 197 5-1 Number of permits for release of genetically engineered varieties approved by APHIS, 222 5-2 Approved field releases of plant varieties for testing purposes by trait (percent), 222 BOXES S-1 Statement of Task, 2 1-1 Statement of Task, 22 1-2 Other Commercialized Genetically Engineered Crops, 33

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xiii TABLES, FIGURES, AND BOXES 2-1 Limitations to Evaluating the Magnitude of Environmental Effects, 61 3-1 Measuring Impacts, 136 5-1 New Traits Reduce Refuge Requirement and Introduce Second Mode of Herbicide Resistance, 219

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Abbreviations and Acronyms ACCase acetyl-CoA carboxylase ALS acetolactate synthase AMPA aminomethylphosphonic acid APHIS Animal and Plant Health Inspection Service (U.S. Department of Agriculture) BST bovine somatotropin Bt Bacillus thuringiensis Cry crystal-like (protein) DNA deoxyribonucleic acid EIS environmental impact statement EPA U.S. Environmental Protection Agency EPSPS enzyme 5-enolpyruvyl-shikimate-3-phosphate synthase GE genetically engineered GMO genetically modified organism HPPD hydroxyphenylpyruvate dioxygenase HR herbicide-resistant IPR intellectual-property rights xix

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xx ABBREVIATIONS AND ACRONYMS IR insect-resistant ISHRW International Survey of Herbicide Resistant Weeds MCL maximum contaminant level NOP National Organic Program NOSB National Organic Standards Board OFPA Organic Foods Production Act PTO U.S. Patent and Trademark Office R&D research and development USDA U.S. Department of Agriculture USDA-ERS U.S. Department of Agriculture, Economic Research Service USDA-NASS U.S. Department of Agriculture, National Agricultural Statistics Service VR virus-resistant