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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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PREPUBLICATION COPY Forest Health and Biotechnology: Possibilities and Considerations Committee on the Potential for Biotechnology to Address Forest Health Board on Agriculture and Natural Resources Division on Earth and Life Studies A Consensus Study Report of

THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 This study was supported by the U.S. Endowment for Forestry and Communities (Grant Agreement E17-49); the Agricultural Research Service (Agreement No. 59-0790-7-0018); the Animal and Plant Health Inspection Service (Agreement No. 16-2000-0094-GR), the National Institute of Food and Agriculture (Agreement No. 2017-38832-26613), and the U.S. Forest Service (Agreement No. 16-DG-11132650-299) of the U.S. Department of Agriculture; and the U.S. Environmental Protection Agency (Contract No. EP-C-14-005). Any opinions, findings, conclusions, or recommendations expressed in this publication do not necessarily reflect the views of any organization or agency that provided support for the project. International Standard Book Number-13: 978-0-309-XXXXX-X International Standard Book Number-10: 0-309-XXXXX-X Digital Object Identifier: https://doi.org/10.17226/25221 Additional copies of this publication are available from the National Academies Press, 500 Fifth Street, NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www.nap.edu. Copyright 2019 by the National Academy of Sciences. All rights reserved. Printed in the United States of America Suggested Citation: National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: https://doi.org/10.17226/25221. Prepublication Copy

The National Academy of Sciences was established in 1863 by an Act of Congress, signed by President Lincoln, as a private, nongovernmental institution to advise the nation on issues related to science and technology. Members are elected by their peers for outstanding contributions to research. Dr. Marcia McNutt is president. The National Academy of Engineering was established in 1964 under the charter of the National Academy of Sciences to bring the practices of engineering to advising the na- tion. Members are elected by their peers for extraordinary contributions to engineering. Dr. C. D. Mote, Jr., is president. The National Academy of Medicine (formerly the Institute of Medicine) was established in 1970 under the charter of the National Academy of Sciences to advise the nation on medical and health issues. Members are elected by their peers for distinguished contri- butions to medicine and health. Dr. Victor J. Dzau is president. The three Academies work together as the National Academies of Sciences, Engineer- ing, and Medicine to provide independent, objective analysis and advice to the nation and conduct other activities to solve complex problems and inform public policy deci- sions. The National Academies also encourage education and research, recognize out- standing contributions to knowledge, and increase public understanding in matters of science, engineering, and medicine. Learn more about the National Academies of Sciences, Engineering, and Medicine at www.nationalacademies.org. Prepublication Copy

Consensus Study Reports published by the National Academies of Sciences, Engineer- ing, and Medicine document the evidence-based consensus on the study’s statement of task by an authoring committee of experts. Reports typically include findings, conclu- sions, and recommendations based on information gathered by the committee and the committee’s deliberations. Each report has been subjected to a rigorous and independ- ent peer-review process and it represents the position of the National Academies on the statement of task. Proceedings published by the National Academies of Sciences, Engineering, and Medi- cine chronicle the presentations and discussions at a workshop, symposium, or other event convened by the National Academies. The statements and opinions contained in proceedings are those of the participants and are not endorsed by other participants, the planning committee, or the National Academies. For information about other products and activities of the National Academies, please visit www.nationalacademies.org/about/whatwedo. Prepublication Copy

COMMITTEE ON THE POTENTIAL FOR BIOTECHNOLOGY TO ADDRESS FOREST HEALTH Chair SUSAN E. OFFUTT, U.S. Government Accountability Office (retired), Oakland, MD Members VIKRAM E. CHHATRE, University of Wyoming, Laramie JASON A. DELBORNE, North Carolina State University, Raleigh STEPHEN DIFAZIO, West Virginia University, Morgantown DORIA R. GORDON, Environmental Defense Fund, Washington, DC INÉS IBÁÑEZ, University of Michigan, Ann Arbor GREGORY JAFFE, Center for Science in the Public Interest, Washington, DC MARK D. NEEDHAM, Oregon State University, Corvallis CLARE PALMER, Texas A&M University, College Station JEANNE ROMERO-SEVERSON, University of Notre Dame, Notre Dame, IN RONALD R. SEDEROFF (NAS), North Carolina State University, Raleigh DIANA L. SIX, University of Montana, Missoula RICHARD A. SNIEZKO, U.S. Forest Service, Cottage Grove, OR Staff KARA N. LANEY, Study Director JENNA BRISCOE, Research Assistant Prepublication Copy v

BOARD ON AGRICULTURE AND NATURAL RESOURCES Chair CHARLES W. RICE, Kansas State University, Manhattan Members SHANE C. BURGESS, University of Arizona, Tucson SUSAN CAPALBO, Oregon State University, Corvallis GAIL CZARNECKI-MAULDEN, Nestlé Purina PetCare, St. Louis, MO GEBISA EJETA, Purdue University, West Lafayette, IN JAMES S. FAMIGLIETTI, California Institute of Technology, Pasadena FRED GOULD (NAS), North Carolina State University, Raleigh DOUGLAS B. JACKSON-SMITH, The Ohio State University, Wooster JAMES W. JONES (NAE), University of Florida, Gainesville STEPHEN S. KELLEY, North Carolina State University, Raleigh JAN E. LEACH, Colorado State University, Fort Collins JILL J. MCCLUSKEY, Washington State University, Richland KAREN I. PLAUT, Purdue University, West Lafayette, IN JIM E. RIVIERE (NAM), Kansas State University, Manhattan Staff ROBIN A. SCHOEN, Director CAMILLA YANDOC ABLES, Senior Program Officer JENNA BRISCOE, Research Assistant KARA N. LANEY, Senior Program Officer PEGGY TSAI YIH, Senior Program Officer vi Prepublication Copy

Preface Nearly one-third of the United States is covered by forests, accounting for more than one million square miles, an area exceeded only in Canada, Brazil, and Russia. These forest ecosystems play vital roles in carbon storage, nutrient cycling, and air and water purification, as well as in supplying habitat for wild- life. Forests hold historical, cultural, and social significance for Americans and are sources of both food and fiber. Today, these valued resources are endangered as never before. Global commerce has hastened the introduction of nonnative, invasive tree pests and diseases, and those native to the country are becoming more virulent due to external drivers such as climate change. The loss of a tree species can have cascading adverse effects on the forest ecosystem and on the range of services it provides and the values it represents to human populations. Against this backdrop, a consortium of federal agencies asked the National Academies of Science, Engineering, and Medicine to consider the potential for the use of biotechnology to mitigate these threats to the health of the nation’s forests. Accordingly, our committee took up the tasks of assessing the ecolog- ical, economic, and social implications of deployment of a genetically modified tree and of identifying the knowledge needed to evaluate the ways such a tree might affect the prospects for forest health. The circum- stances of introduction of a long-lived biotech tree into a forest ecosystem would be novel compared with the use of the technology in industrial plantations or, indeed, in annual agricultural crops. The release of a tree developed to be resistant to a pest or disease would be intended to promote its survival and proliferation in a natural forest setting. The committee’s members represent an unusually wide range of disciplines, from genetics to ecology and from the law to social science and philosophy. The group embraced the holistic view set out in its charge and probed the biophysical and the cultural and social impacts that might arise from the introduction of a biotech tree. Contemplating the rapidly evolving science and emerging public views relevant to the use of biotechnology in forest trees, the committee found itself surveying a frontier of possibilities for different kinds of trees and ecosystems. The release of a biotech tree has no direct precedent, and so the committee listened to a range of voices in the scientific community and in civil society as they speculated on the likely implications of an introduction. Unease about the advisability of the use of biotechnology in the environ- ment will continue to be a factor in public dialogue as biotech trees are considered further. As might be imagined, the committee’s discussions have been lively as we have tried to accommodate a diversity of perspectives, anticipate key information needs, and chart the way forward for researchers, government sci- entific and regulatory officials, and society at large. None of the work the committee has done would have been possible without the stalwart support of Kara Laney, study director, and Jenna Briscoe, research assistant, of the Board on Agriculture and Natural Resources. Kara has been a gracious and steadying presence as we have tried to meld our disparate thoughts into a cohesive narrative. In our meetings, Jenna was a wizard when it came to listening to our fragmented discussion and transforming it instantly into text that we could see and use to move deliberations forward. All of the members of our committee have invested significant time and energy in meeting the challenge of our task, and I am grateful for their dedication. I have learned much from their expertise and their wisdom, and I am the better for it. Finally, thanks go to those who reviewed our draft report and provided comments and advice that have made it a better product for our sponsors and for the public concerned with the future of America’s forests. Susan E. Offutt, Chair Committee on the Potential for Biotechnology to Address Forest Health Prepublication Copy vii

Acknowledgments This Consensus Study Report was reviewed in draft form by individuals chosen for their diverse per- spectives and technical expertise. The purpose of this independent review is to provide candid and critical comments that will assist the National Academies of Sciences, Engineering, and Medicine in making each published report as sound as possible and to ensure that it meets the institutional standards for quality, 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 thank the following individuals for their review of this report: Sally N. Aitken, University of British Columbia Ann M. Bartuska, Resources for the Future Steven P. Bradbury, Iowa State University Joseph P. Brewer II, University of Kansas John E. Carlson, The Pennsylvania State University Melissa M. Goldstein, The George Washington University Shannon M. Hagerman, University of British Columbia Lynn A. Maguire, Duke University Louis Pitelka, University of Maryland Center for Environmental Science Ronald Sandler, Northeastern University Roger R. Schmidt, IBM Corporation Kathleen Segerson, University of Connecticut Daniel Simberloff, University of Tennessee Although the reviewers listed above provided many constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations of this report nor did they see the final draft before its release. The review of this report was overseen by May R. Berenbaum, University of Illinois at Urbana-Champaign. She was responsible for making certain that an independent examination of this report was carried out in accordance with the standards of the National Academies and that all review comments were carefully considered. Responsibility for the final content rests entirely with the authoring committee and the National Academies. Prepublication Copy ix

Contents SELECTED ACRONYMS AND ABBREVIATIONS .......................................................................... xiii SUMMARY ................................................................................................................................................. 1 1 INTRODUCTION ............................................................................................................................ 13 The Committee and Its Charge, 14 The Committee’s Process, 16 Organization of the Report, 16 References, 17 2 FOREST HEALTH .......................................................................................................................... 19 Defining Forest Health, 19 The Value of Healthy Forests, 20 Threats to Forest Health from Insect Pests and Pathogens, 22 Effects of Insect Pests and Pathogens on Trees and Ecosystem Services, 28 Conclusions, 41 References, 42 3 MITIGATING THREATS TO FOREST HEALTH .................................................................... 51 Preventing Introductions, 52 Early Detection and Rapid Response, 53 Containment and Long-Term Management, 53 Time Lines and Costs of Different Management Options for Forest Health, 71 Conclusions and Recommendations, 75 References, 76 4 ECOLOGICAL, ECONOMIC, SOCIAL, AND ETHICAL CONSIDERATIONS IN THE USE OF BIOTECHNOLOGY IN FOREST TREES ..................................................... 88 Ecological Considerations, 88 Economic Considerations, 93 Social and Ethical Considerations, 97 Conclusions and Recommendations, 110 References, 113 5 AN INTEGRATED IMPACT ASSESSMENT FRAMEWORK ............................................... 122 Impact Assessment Framework, 122 Tools Available to Inform an Impact Assessment Framework, 130 Use of Adaptive Management, 135 Conclusions and Recommendations, 139 References, 140 Prepublication Copy xi

Contents 6 CURRENT REGULATORY SYSTEM FOR BIOTECH TREES AND OTHER METHODS USED TO ADDRESS FOREST HEALTH ............................................................ 146 U.S. Department of Agriculture, 147 U.S. Environmental Protection Agency, 152 U.S. Food and Drug Administration, 153 Stakeholder Criticism of Federal Oversight of Biotech Plants and Trees, 155 Movement of Biotech Trees Developed to Address Forest Health Across National Borders, 155 Current Regulatory System for Other Interventions to Address Forest Health, 156 Conclusions and Recommendations, 159 References, 161 7 MOVING AHEAD ......................................................................................................................... 165 Improving the Effectiveness of Biotechnology, 165 Improving Impact Assessment, 167 Research and Investment Needs Beyond Biotechnology, 168 References, 171 GLOSSARY ............................................................................................................................................ 172 APPENDIXES A BIOGRAPHICAL SKETCHES OF COMMITTEE MEMBERS ............................................. 175 B OPEN SESSION MEETING AGENDAS .................................................................................... 180 C BIOTECH TREE RESEARCH AND DEVELOPMENT, 1987–2018 ...................................... 185 D CHRONOLOGICAL SUMMARY OF STUDIES EMPIRICALLY EXAMINING PUBLIC AND OTHER STAKEHOLDER RESPONSES TO THE USE OF BIOTECHNOLOGY IN TREES AND FORESTS ..................................................................... 198 Prepublication Copy xii

Selected Acronyms and Abbreviations APHIS Animal and Plant Health Inspection Service Bt Bacillus thuringiensis CFR Code of Federal Regulations CRISPR Clustered Regularly-Interspaced Short Palindromic Repeats EA Environmental Assessment EAB emerald ash borer EIS Environmental Impact Statement EPA U.S. Environmental Protection Agency FDA U.S. Food and Drug Administration FFDCA Federal Food, Drug, and Cosmetic Act FIFRA Federal Insecticide, Fungicide, and Rodenticide Act FONSI Finding of No Significant Impact FWS Fish and Wildlife Service HERA Human Health and Ecological Risk Assessment Mbp megabase pair NEPA National Environmental Policy Act OxO oxalate oxidase QTL quantitative trait locus PERAL Plant Epidemiology and Risk Assessment Laboratory PIP Plant-Incorporated Protectant RNAi RNA interference USDA U.S. Department of Agriculture Prepublication Copy xiii

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The American chestnut, whitebark pine, and several species of ash in the eastern United States are just a few of the North American tree species that have been functionally lost or are in jeopardy of being lost due to outbreaks of pathogens and insect pests. New pressures in this century are putting even more trees at risk. Expanded human mobility and global trade are providing pathways for the introduction of nonnative pests for which native tree species may lack resistance. At the same time, climate change is extending the geographic range of both native and nonnative pest species.

Biotechnology has the potential to help mitigate threats to North American forests from insects and pathogens through the introduction of pest-resistant traits to forest trees. However, challenges remain: the genetic mechanisms that underlie trees’ resistance to pests are poorly understood; the complexity of tree genomes makes incorporating genetic changes a slow and difficult task; and there is a lack of information on the effects of releasing new genotypes into the environment.

Forest Health and Biotechnology examines the potential use of biotechnology for mitigating threats to forest tree health and identifies the ecological, economic, and social implications of deploying biotechnology in forests. This report also develops a research agenda to address knowledge gaps about the application of the technology.

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