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Suggested Citation:"Front Matter." National Research Council. 2004. Biological Confinement of Genetically Engineered Organisms. Washington, DC: The National Academies Press. doi: 10.17226/10880.
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Committee on Biological Confinement of Genetically Engineered Organisms Board on Agriculture and Natural Resources Board on Life Sciences Division on Earth and Life Studies THE NATIONAL ACADEMIES PRESS Washington, DC www.nap.edu

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 Govern- ing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineer- ing, 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 supported by Agreement No. 59-0790-1-182 between the National Academy of Sciences and the U.S. Department of Agriculture. Any opinions, find- ings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the views of the organizations or agencies that provided support for the project. Library of Congress Cataloging-in-Publication Data Biological confinement of genetically engineered organisms / Committee on Biologi- cal Confinement of Genetically Engineered Organisms, Board on Agriculture and Natural Resources, Board on Life Sciences, Division on Earth and Life Studies. p. cm. Includes bibliographical references and index. ISBN 0-309-09085-7 (hardcover)--ISBN 0-309-52778-3 (pdf) 1. Transgenic organisms--Safety measures. 2. Confinement farms. 3. Agricultural biotechnology. 4. Infertility in animals. 5. Transgenic organisms--Risk assessment. I. National Research Council (U.S.). Committee on Biological Confinement of Ge- netically Engineered Organisms. QH442.6.B54 2004 577'.18--dc22 2004004051 Additional copies of this report are available from the National Academies Press, 500 Fifth Street, N.W., Lockbox 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu Copyright 2004 by the National Academy of Sciences. All rights reserved. Printed in the United States of America

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 Acad- emy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Bruce M. Alberts 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 engi- neers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineer- ing programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Wm. A. Wulf is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sci- ences 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 con- gressional 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 federal 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 gov- ernment, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Bruce M. Alberts and Dr. Wm. A. Wulf are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

COMMITTEE ON BIOLOGICAL CONFINEMENT OF GENETICALLY ENGINEERED ORGANISMS T. KENT KIRK, Chair, University of Wisconsin, Madison JOHN E. CARLSON, Pennsylvania State University, University Park NORMAN ELLSTRAND, University of California, Riverside ANNE R. KAPUSCINSKI, University of Minnesota, St. Paul THOMAS A. LUMPKIN, Asian Vegetable Research and Development Center, Shanhua, Taiwan DAVID C. MAGNUS, Stanford University, Palo Alto, California DANIEL B. MAGRAW, JR., Center for International Environmental Law, Washington, DC EUGENE W. NESTER, University of Washington, Seattle JOHN J. PELOQUIN, American Protein Corporation, Inc., Ames, Iowa ALLISON A. SNOW, The Ohio State University, Columbus MARIAM B. STICKLEN, Michigan State University, East Lansing PAUL E. TURNER, Yale University, New Haven, Connecticut STAFF KIM WADDELL, Study Director MICHAEL KISIELEWSKI, Research Assistant PETER RODGERS, Research Intern DONNA WILKINSON, Research Intern ANNE H. KELLY, Editor CINDY LOCHHEAD, Project Assistant JULIE COFFIN, Project Assistant v

COMMITTEE ON AGRICULTURAL BIOTECHNOLOGY, HEALTH, AND THE ENVIRONMENT BARBARA SCHAAL, Chair, Washington University, St. Louis, Missouri DAVID ANDOW, University of Minnesota, St. Paul FREDERICK AUSUBEL, Harvard Medical School, Boston, Massachusetts NEAL FIRST, University of Wisconsin, Madison LYNN FREWER, Institute of Food Research, Norwich, United Kingdom HENRY GHOLZ, National Science Foundation, Arlington, Virginia EDWARD GROTH, Consumers Union, Yonkers, New York ERIC HALLERMAN, Virginia Polytechnic Institute and State University, Blacksburg RICHARD HARWOOD, Michigan State University, East Lansing CALESTOUS JUMA, Harvard University, Cambridge, Massachusetts SAMUEL LEHRER, Tulane University, New Orleans, Louisiana SANFORD MILLER, Center for Food and Nutrition Policy, Virginia Polytechnic Institute and State University, Alexandria PHILIP PARDEY, University of Minnesota, St. Paul PER PINSTRUP-ANDERSON, Cornell University, Ithaca, New Yor ELLEN SILBERGELD, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland ROBERT SMITH, R.E. Smith Consulting, Inc., Newport, Vermont ALLISON SNOW, Ohio State University, Columbus PAUL THOMPSON, Michigan State University, East Lansing DIANA WALL, Colorado State University, Fort Collins vi

BOARD ON AGRICULTURE AND NATURAL RESOURCES MAY BERENBAUM, Chair, University of Illinois, Urbana SANDRA BARTHOLMEY, University of Illinois, Chicago DEBORAH BLUM, University of Wisconsin, Madison H. H. CHENG, University of Minnesota, St. Paul BARBARA P. GLENN, Biotechnology Industry Organization, Washington, DC LINDA F. GOLODNER, National Consumers League, Washington, DC W. R. (REG) GOMES, University of California, Oakland PERRY R. HAGENSTEIN, Institute for Forest Analysis, Planning, and Policy, Wayland, Massachusetts JANET C. KING, Children's Hospital Oakland Research Center, Oakland, California DANIEL P. LOUCKS, Cornell University, Ithaca, New York WHITNEY MACMILLAN, Cargill, Inc., Minneapolis, Minnesota TERRY L. MEDLEY, DuPont Agriculture and Nutrition, Wilmington, Delaware OLE NIELSEN, Ontario Veterinary College, Canada ALICE N. PELL, Cornell University, Ithaca, New York BOBBY PHILLS, Florida A&M University, Tallahassee SHARRON S. QUISENBERRY, Virgnia Polytechnic and State University, Blacksburg SONYA B. SALAMON, University of Illinois at Urbana-Champaign, Urbana G. EDWARD SCHUH, Humphrey Institute of Public Affairs, Minneapolis, Minnesota BRIAN J. STASKAWICZ, University of California, Berkeley JACK WARD THOMAS, University of Montana, Missoula JAMES H. TUMLINSON, Pennsylvania State University, University Park B. L. TURNER, Clark University, Worcester, Massachusetts STAFF CHARLOTTE KIRK BAER, Director KAREN IMHOF, Administrative Assistant vii

BOARD ON LIFE SCIENCES COREY S. GOODMAN, Chair, University of California, Berkeley RUTH BERKELMAN, Emory University, Atlanta R. ALTA CHARO, University of Wisconsin, Madison DENNIS CHOI, Merck Research Laboratories, West Point, Pennsylvania JOANNE CHORY, The Salk Institute for Biological Studies, La Jolla, California JEFFREY L. DANGL, University of North Carolina, Chapel Hill PAUL R. EHRLICH, Stanford University, Palo Alto, California JAMES M. GENTILE, Hope College, Holland, Michigan LINDA GREER, Natural Resources Defense Council, Washington, DC ED HARLOW, Harvard Medical School, Cambridge, Massachusetts DAVID HILLIS, University of Texas, Austin KENNETH F. KELLER, University of Minnesota, Minneapolis RANDALL MURCH, Institute for Defense Analyses, Alexandria, Virginia GREGORY A. PETSKO, Brandeis University, Waltham, Massachusetts STUART L. PIMM, Duke University, Durham, North Carolina BARBARA A. SCHAAL, Washington University, St. Louis, Missouri JAMES TIEDJE, Michigan State University, East Lansing KEITH YAMAMOTO, University of California, San Francisco STAFF FRANCES SHARPLES, Director DENISE GROSSHANS, Senior Project Assistant viii

Acknowledgments This report represents the integrated efforts of many individuals. The committee thanks all those who shared their insight and knowledge to bring the document to fruition. We also thank all those who provided information at our public meetings and who participated in our public sessions. During the course of its deliberations, the committee sought assistance from several people who gave generously of their time to provide advice and information that were considered in its deliberations. Special thanks are due the following: WILLY DE GREEF, Syngenta Seeds, Basel, Switzerland CATHLEEN ENRIGHT, APHIS / USDA, Riverdale, Maryland PHILIP J. EPPARD, Monsanto Protein Technologies, St. Louis, Missouri PAL MALIGA, Rutgers University, Piscataway, New Jersey MICHAEL H. PAULY, Epicyte Pharmaceutical, Inc., San Diego, California JANE RISSLER, Union of Concerned Scientists, Washington, DC MICHAEL SCHECHTMAN, USDA, Washington, DC ANTHONY M. SHELTON, Cornell University, Geneva, New York STEVEN H. STRAUSS, Oregon State University, Corvallis, Oregon The committee is grateful to members of the National Research Council (NRC) staff who worked diligently to maintain progress and quality in its work. We also would like to thank Robert McDonald, Melissa Brandt, Sarah De Belen, Tazeen Hasan, and Rene Milet for their research assistance. ix

x ACKNOWLEDGMENTS This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with proce- dures approved by the National Research Council's Report Review Com- mittee. The purpose of this 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 for 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 this report: DAVID ADELMAN, University of Arizona College of Law, Tucson, Arizona KLAUS AMMANN, University of Bern, Bern, Switzerland R. JEFFREY BURKHARDT, University of Florida, Gainesville, Florida JEFFREY DANGL, The University of North Carolina, Chapel Hill, North Carolina DONALD N. DUVICK, Iowa State University, Ames, Iowa VIRGINIA S. HINSHAW, University of California, Davis, California CALESTOUS JUMA, Harvard University, Cambridge, Massachusetts STEVEN E. LINDOW, University of California, Berkeley, California TERRY MEDLEY, DuPont Agriculture and Nutrition, Wilmington, Delaware WILLIAM MUIR, Purdue University, West Lafayette, Indiana CHRISTOPHER SOMERVILLE, Stanford University, Stanford, California STEVEN STRAUSS, Oregon State University, Corvallis, Oregon GREG TRAXLER, Auburn University, Auburn, Alabama Although the reviewers listed above have provided many constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations nor did they see the final draft of the report before its release. The review of this report was overseen by Dr. Robert A. Frosch, Harvard University, Cambridge, Massachusetts, and Dr. Fred Gould, North Carolina State University, Raleigh. Appointed by the National Research Council, they were responsible for making certain that an independent ex- amination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Re- sponsibility for the final content of this report rests entirely with the authoring committee and the institution.

Preface Genetically engineered microbes have been used commercially for many years to make products useful to humans. Production is confined to vessels that are sterilized between batches. There has been little concern about these genetically engineered (GE) microbes escaping into the wild and doing damage, in part because they are confined physically and in part because they are weakened by foreign genetic material that makes them unlikely to survive in the wild. But 10 years ago genetically engineered crop plants were introduced into field environments, a situation quite different from having GE microbes in fermentors. This outplanting of GE plants raised, and continues to raise, public and scientific concerns on the potential consequences of escape of genetically engineered organisms (GEOs) and their associated transgenes into natural and managed ecosystems. The acreage planted with GE crop plants has steadily and rapidly increased, as have the number of types of GE plants. GE fish and other animals have now been developed, some with remarkable potentials. This increased use and development of new GEOs obviously reflects the fact that GEOs can have substantial advantages over their progenitors. Agricultural biotechnology has enormous potential to better the human condition. However, concern about the possible risks posed by some GEOs has led to questions about the regulation they receive, and has increased interest in assuring that certain GEOs are confined. While no serious consequences have ensued because of a failure of GEO confinement, with the growing diversity and number of GEOs being developed and released, the potential for unwanted consequences increases, and scientists can envision undesirable scenarios. xi

xii PREFACE Confinement can be accomplished not only by physical but also by bio- logical means. Several examples of long-used biological confinement methods (used with non-GEOs) are described in this report. Genetic engi- neering, however, makes new biological confinement strategies possible. We refer to all biological confinement methods, whether genetically engineered or not, as bioconfinement methods. The NRC convened a committee of 12 members from a variety of complementary specialties; the reader is urged to read the brief biographical sketches. Members were selected who could not only cover the different aspects of bioconfinement, but who could also assure a flexible view of the committee's charge and provide overall and realistic balance. Our task was challenging. Bioconfinement of GEOs is in its infancy as a focused science. But the science is fast-moving, rapidly evolving. We found ourselves dealing with a lack of published data on many of the existing and potential methods. Entirely new methods of bioconfinement were announced by the scientific community while we worked on the report. Consequently, we did not focus exclusively on methods in commercial use but tried to anticipate future developments. An exhaustive literature search was not part of our charge; only a few illustrative examples were provided for each confinement approach. Our statement of task of six questions (see the Execu- tive Summary and Chapter 1) limited us further because effective bio- confinement will require more than sound science. It will require safe practices and commitment by those who design and develop the GEOs; effective regulatory oversight; a public commitment to investing in this tech- nology; a high level of public confidence and acceptance; effective commu- nication between stakeholders; respect for regional and cultural differences in values, experience, ethics; recognition of the international dimensions; and more. We met four times, for a total of about eight days. Most of the research and writing was done individually between meetings, so that the meetings could be devoted to critique and improvement. We began with presentations by and discussions with the sponsoring agency and outside experts from industry, academia, and nongovernmental organizations (NGOs). We then prepared a report outline which was continuously revised, and wrote the report via numerous iterations. This report is a consensus document. Each committee member had the opportunity to question and modify the content of each paragraph. We all learned in this process. The procedure resulted in improvements in every section. In-depth reviews by outside experts from academia and industry resulted in further improvements in the report's clarity, balance, and presentation. Chapter 1 provides an introduction to the subject, gives the scope of the study, provides a brief history of GEOs and their confinement, and gives an introduction into ethical and other social considerations. The committee

PREFACE xiii recognized that many GEOs will not warrant confinement. We therefore addressed the issue of when and why bioconfinement might be necessary and described briefly some of the possible undesirable consequences of escape of some GEOs (Chapter 2). Chapters 3, 4, and 5 detail what is presently known about bioconfinement methodologies for plants, animals, and microbes (and fungi and viruses), respectively. Chapter 6 summarizes the biological and operational considerations for bioconfinement and points to some important research needs. Serving as chair of this committee was a most interesting and enlighten- ing experience for me personally. Bioconfinement is not my field, nor is genetic engineering, so I was afforded significant learning opportunities. At the outset I was surprised at the breadth of subject matter that "bio- confinement of GEOs" invites. This is especially true since we considered plants, animals and microbes. It is my hope, that we have written a report that not only will be valuable to the sponsoring agency and other stake- holders, but also one that reflects the committee's concerted effort to adequately characterize a rapidly evolving and complex subject in a National Academies' report. I also hope that our efforts contribute much to the ongoing discussion about biotechnology and the opportunities to utilize the biological tools available to minimize the concerns and risks surrounding the release of GEOs into the environment. Most of all, I hope readers enjoy what we have prepared. I want to thank the committee members sincerely for their participation and hard work; they are all busy people, and NRC work is pro bono. We all thank our NRC study director, Dr. Kim Waddell, for his excellent leader- ship, and we thank his staff of Julie Coffin, Michael Kisielewski, Cindy Lochhead, Peter Rodgers, and Donna Wilkinson. T. Kent Kirk, Chair Committee on Biological Confinement of Genetically Engineered Organisms

Contents EXECUTIVE SUMMARY 1 Rationale for Bioconfinement, 3 Methods of Bioconfinement, 4 Ensuring Bioconfinement Efficacy, 6 Detecting and Mitigating Bioconfinement Failure, 10 Ecological Consequences of Large-Scale Use of Bioconfinement, 11 Conclusions, 12 1 INTRODUCTION 14 What Are Genetically Engineered Organisms?, 14 What is Bioconfinement?, 15 Other Confinement Methods,16 Scope of the Report, 17 International Aspects, 19 History of Confinement, 19 Social Acceptability of Bioconfinement Methods, 25 2 WHEN AND WHY TO CONSIDER BIOCONFINEMENT 29 Introduction, 29 What is Risk?, 30 Concerns, 35 Effects on Nontarget Species, 52 Delaying the Evolution of Resistance, 52 Food Safety and Other Issues, 53 When and Why to Consider Bioconfinement: The Need for Preventive Actions, 53 xv

xvi CONTENTS How Much Confinement Is Enough?, 54 Need for Bioconfinement, 55 Predicting the Consequences of Failure, 56 Who Decides, 58 3 BIOCONFINEMENT OF PLANTS 65 Methods of Bioconfinement, 65 Genetically Engineered Trees, 98 Transgenic Grasses, 115 Transgenic Algae, 121 Effectiveness at Different Spatial and Temporal Scales, 122 Monitoring and Managing Confinement Failure, 124 4 BIOCONFINEMENT OF ANIMALS: FISH, SHELLFISH, AND INSECTS 130 Bioconfinement of Fish and Shellfish, 132 Bioconfinement of Insects, 153 5 BIOCONFINEMENT OF VIRUSES, BACTERIA, AND OTHER MICROBES 159 Introduction, 159 Potential Effects or Concerns, and Need for Bioconfinement in Viruses, Fungi, and Bacteria, 160 Bioconfinement of Bacteria, Viruses, and Fungi, 169 6 BIOLOGICAL AND OPERATIONAL CONSIDERATIONS FOR BIOCONFINEMENT 180 What Biology Tells Us about Confinement and Bioconfinement, 180 Execution of Confinement, 185 International Aspects, 193 Bioconfinement Failure, 194 Looking to the Future: Strategic Public Investment in Bioconfinement Research, 195 REFERENCES 199 ABOUT THE AUTHORS 235 BOARD ON AGRICULTURE AND NATURAL RESOURCES PUBLICATIONS 241 INDEX 245

Tables, Figures, and Boxes TABLES 2-1 Systematic Risk Assessment and Management, 33 2-2 Genetically Engineered Organisms, 39 3-1 Bioconfinement Methods in Plants, 66 3-2 Genetically Engineered Woody Plants, Permits Approved by APHIS for Field Tests in the United States, 1989­2003, 99 3-3 Genetically Engineered Turfgrasses, Permits Approved by APHIS for Field Tests in the United States, 1993­2003, 116 4-1 Genetic Bioconfinement Strategies for Fish, 147 4-2 Insects Subjected to the Sterile Insect Technique, 155 FIGURES 2-1 A Risk Assessment Matrix, 32 3-1 Proposed Transgenic Bioconfinement Methods in Plants, 73 3-2 Repressible Seed--Lethal Bioconfinement, 86 3-3 A Wild Hybrid, F. arundinacea and L. multiflorum Lam, 119 4-1 Normal Steps in Gamete Fertilization and Early Cell Division, 134 4-2 Production Cycle for All-Female Lines of Fish in Species with an XY Sex Determination System, 143 xvii

xviii TABLES, FIGURES, AND BOXES BOXES 2-1 Confinement Failure: StarLink Corn, 34 3-1 Stability of Transgenic Confinement, 102 3-2 When Will Bioconfinement be Necessary for Trees?, 105 3-3 Turfgrass Might be Difficult to Confine, 120 4-1 Proposed Bioconfinement of Transgenic Atlantic Salmon, 137 5-1 1776, 172

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Genetically engineered organisms (GEOs) have been under development for more than 20 years while GE crops have been grown commercially during the last decade. During this time, a number of questions have cropped up concerning the potential consequences that certain GEOs might have on natural or managed ecosystems and human health. Interest in developing methods to confine some GEOs and their transgenes to specifically designated release settings has increased and the success of these efforts could facilitate the continued growth and development of this technology.

Biological Confinement of Genetically Engineered Organisms examines biological methods that may be used with genetically engineered plants, animals, microbes, and fungi. Bioconfinement methods have been applied successfully to a few non-engineered organisms, but many promising techniques remain in the conceptual and experimental stages of development. This book reviews and evaluates these methods, discusses when and why to consider their use, and assesses how effectively they offer a significant reduction of the risks engineered organisms can present to the environment.

Interdisciplinary research to develop new confinement methods could find ways to minimize the potential for unintended effects on human health and the environment. Need for this type of research is clear and successful methods could prove helpful in promoting regulatory approval for commercialization of future genetically engineered organisms.

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