Feasibility of Using Mycoherbicides
for Controlling Illicit Drug Crops






Committee on Mycoherbicides for Eradicating Illicit Drug Crops

Board on Agriculture and Natural Resources

Board on Environmental Studies and Toxicology

Division on Earth and Life Studies







NATIONAL RESEARCH COUNCIL
OF THE NATlONAl ACADEMIES







THE NATIONAL ACADEMIES PRESS
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Committee on Mycoherbicides for Eradicating Illicit Drug Crops Board on Agriculture and Natural Resources Board on Environmental Studies and Toxicology Division on Earth and Life Studies

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Insti- tute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance. This project was supported by Contract OND-GEN-C-09-0004 between the National Academy of Sciences and the Office of National Drug Control Policy. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the organizations or agencies that pro- vided support for this project. International Standard Book Number-13: 978-0-309-22171-9 International Standard Book Number-10: 0-309-22171-4 Additional copies of this report are available from The National Academies Press 500 Fifth Street, NW Box 285 Washington, DC 20055 800-624-6242 202-334-3313 (in the Washington metropolitan area) http://www.nap.edu Copyright 2011 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 government 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 members, sharing with the National Academy of Sciences the responsibility for advising 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 re- sponsibility 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 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 Na- tional Academy of Engineering in providing services to the government, the public, and the scientific and engineering 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 MYCOHERBICIDES FOR ERADICATING ILLICIT DRUG CROPS Members RAGHAVAN CHARUDATTAN (Chair), University of Florida, Gainesville, FL JOAN W. BENNETT, Rutgers University, New Brunswick, NJ JEROME J. CURA, The Woods Hole Group, Falmouth, MA WILLIAM E. FRY, Cornell University, Ithaca, NY GUY KNUDSEN, University of Idaho, Moscow, ID JOHN F. LESLIE, Kansas State University, Manhattan, KS NU-MAY RUBY REED, California Environmental Protection Agency, Sacramento, CA JUDITH C. RHODES, University of Cincinnati, Cincinnati, OH JOHN W. TAYLOR, University of California, Berkeley, CA DAVID O. TEBEEST, University of Arkansas, Fayetteville, AR ARIENA H.C. VAN BRUGGEN, University of Florida, Gainesville, FL MAURIZIO VURRO, National Research Council, Bari, Italy ALAN K. WATSON, McGill University, Ste. Anne de Bellevue, Quebec, Canada CHARLES P. WOLOSHUK, Purdue University, West Lafayette, IN Staff SUSAN N. J. MARTEL, Project Director CAMILLA YANDOC ABLES, Program Officer JANET M. MULLIGAN, Research Associate NORMAN GROSSBLATT, Senior Editor TAMARA DAWSON, Program Associate Sponsor OFFICE OF NATIONAL DRUG CONTROL POLICY v

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BOARD ON AGRICULTURE AND NATURAL RESOURCES Members NORMAN R. SCOTT, Chair, Cornell University, Ithaca, NY PEGGY F. BARLETT, Emory University, Atlanta, GA HAROLD L. BERGMAN, University of Wyoming, Laramie, WY RICHARD A. DIXON, Samuel Roberts Noble Foundation, Ardmore, OK DANIEL M. DOOLEY, University of California, Oakland, CA JOAN H. EISEMANN, North Carolina State University, Raleigh, NC GARY F. HARTNELL, Monsanto Company, St. Louis, MO GENE HUGOSON, Minnesota Department of Agriculture, St. Paul, MN KIRK C. KLASING, University of California, Davis, CA VICTOR L. LECHTENBERG, Purdue University, West Lafayette, IN PHILIP E. NELSON, Purdue University, West Lafayette, IN KEITH PITTS, Marrone Bio Innovations, Davis, CA CHARLES W. RICE, Kansas State University, Manhattan, KS HAL SALWASSER, Oregon State University, Corvallis, OR ROGER A. SEDJO, Resources for the Future, Washington DC KATHLEEN SEGERSON, University of Connecticut, Storrs, CT MERCEDES VÁZQUEZ-AÑÓN, Novus International, Inc., St. Charles, MO Staff ROBIN A. SCHOEN, Director AUSTIN J. LEWIS, Senior Program Officer EVONNE P.Y. TANG, Senior Program Officer PEGGY TSAI, Program Officer CAMILLA YANDOC ABLES, Program Officer KARA N. LANEY, Program Officer RUTH S. ARIETI, Research Associate JANET M. MULLIGAN, Research Associate KAREN L. IMHOF, Administrative Assistant KATHLEEN REIMER, Program Assistant vi

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BOARD ON ENVIRONMENTAL STUDIES AND TOXICOLOGY1 Members ROGENE F. HENDERSON (Chair), Lovelace Respiratory Research Institute, Albuquerque, NM PRAVEEN AMAR, Clean Air Task Force, Boston, MA TINA BAHADORI, American Chemistry Council, Washington, DC MICHAEL J. BRADLEY, M.J. Bradley & Associates, Concord, MA JONATHAN Z. CANNON, University of Virginia, Charlottesville GAIL CHARNLEY, HealthRisk Strategies, Washington, DC FRANK W. DAVIS, University of California, Santa Barbara RICHARD A. DENISON, Environmental Defense Fund, Washington, DC CHARLES T. DRISCOLL, JR., Syracuse University, New York H. CHRISTOPHER FREY, North Carolina State University, Raleigh RICHARD M. GOLD, Holland & Knight, LLP, Washington, DC LYNN R. GOLDMAN, George Washington University, Washington, DC LINDA E. GREER, Natural Resources Defense Council, Washington, DC WILLIAM E. HALPERIN, University of Medicine and Dentistry of New Jersey, Newark PHILIP K. HOPKE, Clarkson University, Potsdam, NY HOWARD HU, University of Michigan, Ann Arbor SAMUEL KACEW, University of Ottawa, Ontario ROGER E. KASPERSON, Clark University, Worcester, MA THOMAS E. MCKONE, University of California, Berkeley TERRY L. MEDLEY, E.I. du Pont de Nemours & Company, Wilmington, DE JANA MILFORD, University of Colorado at Boulder, Boulder FRANK O’DONNELL, Clean Air Watch, Washington, DC RICHARD L. POIROT, Vermont Department of Environmental Conservation, Waterbury KATHRYN G. SESSIONS, Health and Environmental Funders Network, Bethesda, MD JOYCE S. TSUJI, Exponent Environmental Group, Bellevue, WA Senior Staff JAMES J. REISA, Director DAVID J. POLICANSKY, Scholar RAYMOND A. WASSEL, Senior Program Officer for Environmental Studies ELLEN K. MANTUS, Senior Program Officer for Risk Analysis SUSAN N.J. MARTEL, Senior Program Officer for Toxicology EILEEN N. ABT, Senior Program Officer RUTH E. CROSSGROVE, Senior Editor MIRSADA KARALIC-LONCAREVIC, Manager, Technical Information Center RADIAH ROSE, Manager, Editorial Projects 1 This study was planned, overseen, and supported by the Board on Environmental Studies and Toxicology. vii

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Preface There is long-standing interest in developing mycoherbicides as a means of combating the production of illicit drug crops. However, efforts to develop and test mycoherbicides for that purpose have been limited by the need for spe- cial permission and requirements for growing illicit crops experimentally and for testing biological agents. Proposals to conduct field tests of mycoherbicides on drug crops in the United States and abroad have also been rejected because of scientific and political concerns. Scientific issues include concerns about the efficacy of the mycoherbicides; risks to nontarget plants, organisms, animals, and humans; and ecological effects. To address such scientific questions, Con- gress directed the Office of National Drug Control Policy to commission a study of the feasibility of developing mycoherbicides against illicit drug crops (PL 109-469, Sec. 1111). The agency commissioned the National Research Council to perform the study. The National Research Council convened the Committee on Mycoherbi- cides for Eradicating Illicit Drug Crops, which prepared this report. The mem- bers of the committee were selected for their expertise in plant pathology; my- cotoxins; fungal genetics, evolution, and ecology; mycoherbicide development, evaluation, formulation, and application; plant-disease epidemiology; soil mi- crobiology; medical mycology; human toxicology and risk assessment; and eco- logical risk assessment (see Appendix A for biographic information on the members). To help the committee in its review, public meetings were held April 20, June 23, and September 15, 2010, to gather information from relevant federal government agencies; government, academic, and industry researchers; and the general public. The committee is grateful to those who gave presentations on topics relevant to the committee’s task, including Terry Zobeck, Office of Na- tional Drug Control Policy; Jay Ellenberger and Christopher Wosniak, U.S. En- vironmental Protection Agency; John Bargeron and Scott Harris, U.S. Depart- ment of State; Henry Appleton and Bryan Bailey, U.S. Department of Agriculture; Mark Wach, Sylvan Biosciences; David Sands, Montana State Uni- versity; Christopher Eusebi, Harness, Dickey & Pierce, PLC; and Brent Nowak, University of Texas at San Antonio. ix

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x Preface This report has been reviewed in draft form by persons chosen for their diverse perspectives and technical expertise in accordance with procedures ap- proved by the National Research Council’s Report Review Committee. The pur- pose 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 manu- script remain confidential to protect the integrity of the deliberative process. We thank the following for their review of the report: Basil Acock, Acock Info, LLP; Mary Acock, Acock Info, LLP; Karen Bailey, Agriculture and Agri-Food Canada; Michael Braverman, Rutgers University; Davie Geiser, Pennsylvania State University; Joseph Heitman, Duke University; Walter Marasas, PROMEC Unit of the South African Medical Research Council (retired); Terry Medley, E I du Pont de Nemours & Company; Louise Morin, CSIRO Entomology; and Jan Carel Zadoks, Agricultural University at Wageningen (retired). 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 the report was overseen by Laurence Madden, Ohio State Univer- sity, and May Berenbaum, University of Illinois. Appointed by the National Research Council, they were responsible for making certain that an independent examination of the report was carried out in accordance with institutional proce- dures and that all review comments were carefully considered. Responsibility for the final content of the report rests entirely with the author committee and the institution. The committee is grateful for the assistance of National Research Council staff in preparing the report. It particularly acknowledges the support of Susan Martel, Camilla Ables, and Janet Mulligan, who coordinated the project and contributed to the committee’s report. Other staff members who contributed to this effort are Robin Schoen, director of the Board on Agriculture and Natural Resources; Tamara Dawson, program associate; and Norman Grossblatt, senior editor. Finally, I thank all the members of the committee for their efforts through- out the development of this report. Raghavan Charudattan, PhD, Chair Committee on Mycoherbicides for Eradicating Illicit Drug Crops

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Abbreviations and Acronyms APHIS Animal and Plant Inspection Service ARS Agricultural Research Service ATCC American Type Culture Collection BWC Biological Weapons Convention CBN Central Bureau of Narcotics (India) CFR Code of Federal Regulations CFU colony-forming units DAA days after application DAI days after inoculation DEA Drug Enforcement Agency ENACO Empresa Nacional de Coca EPA U.S. Environmental Protection Agency EIS environmental impact statement ESA Endangered Species Act EU European Union FFDCA Federal Food, Drug, and Cosmetic Act FIFRA Federal Insecticide, Fungicide, and Rodenticide Act FOC Fusarium oxysporum complex f. sp. forma specialis f. spp. formae speciales IOBC International Organization for Biological Control of Noxious Animals and Plants IPPC International Plant Protection Convention ISPM International Standards for Phytosanitary Measures NEPA National Environmental Policy Act NPPO National Plant Protection Office ONDCP Office of National Drug Control Policy RAPD random amplified polymorphic DNA THC delta-9-tetrahydrocannabinol UNDCP UN International Drug Control Programme UNODC UN Office of Drugs and Crime USDA U.S. Department of Agriculture VCG vegetative compatibility group xi

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Contents SUMMARY ........................................................................................................ 3 1 INTRODUCTION ............................................................................. 12 Fungal Terminology, 18 Statement of Task, 21 Committee’s Interpretation of its Task, 21 Committee’s Approach, 25 Organization of the Report, 25 2 BIOLOGICAL CONTROL OF UNDESIRABLE PLANTS ......... 27 Background, 27 Key Attributes of Effective Mycoherbicides in Use, 30 Challenges to and Constraints in the Development and Large-Scale Use of Mycoherbicides, 35 Pesticide Regulation in the United States, 37 Considerations for International Testing and Use of Mycoherbicides, 39 Risk to Nontarget Plants and Organisms, 41 3 TARGET ILLICIT CROPS ............................................................. 47 Cannabis: Cannabis Sativa, 47 Coca: Erythroxylum Species, 52 Opium Poppy: Papaver Somniferum, 56 4 FUSARIUM OXYSPORUM FORMAE SPECIALES AS CANDIDATE BIOLOGICAL CONTROL AGENTS FOR CANNABIS AND COCA ......................................................... 61 Background on the Specific Fungi, 62 Efficacy and Implementation, 64 Inoculum Production and Delivery, 72 Persistence in the Environment, 84 Effects on Nontarget Organisms, 92 xiii

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xiv Contents Mutation, 98 What We Can Learn From A Natural Epidemic of fusarium oxysporum f.sp. erythroxyli Wilt of Coca in Peru, 99 5 CRIVELLIA PAPAVERACEA AND BRACHYCLADIUM PAPAVERIS AS CANDIDATE BIOLOGICAL CONTROL AGENTS AGAINST OPIUM POPPY ........................................... 101 Efficacy and Implementation, 104 Inoculum Production and Delivery, 110 Persistence in the Environment, 115 Effects on Nontarget Organisms, 117 Mutation, 119 A Presumptive Disease Epidemic in Opium Poppy in Afghanistan, 120 6 ANSWERS TO CHARGE QUESTIONS ...................................... 121 Effectiveness, 121 Feasibility of Large-Scale Manufacture and Delivery, 123 Persistence in the Environment, 124 Toxicity to Nontarget Organisms, 126 Potential for Mutation and Resulting Toxicity to Target and Nontarget Organisms, 127 Research and Development Needs, 129 REFERENCES ............................................................................................... 132 APPENDIXES A BIOGRAPHIC INFORMATION ON THE COMMITTEE ON MYCOHERBICIDES FOR ERADICATING ILLICIT DRUG CROPS .......................................................................................153 B EPA REQUIREMENTS AND GUIDELINES UNDER 40 CFR 158, SUBPART V .....................................................................158 BOXES, FIGURES, AND TABLES BOXES 1-1 Questions Posed in the Statement of Task, 22 2-1 Requirements for Tiered Toxicity Testing and Tiered Toxicity and Pathogenicity Testing under FIFRA (40 CFR 158, Subpart V), 38

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xv Contents FIGURES 1-1 Life cycle of a heterothallic Ascomycota fungus, 19 1-2 Life cycle for a homothallic Ascomycota fungus, 19 1-3 Life cycle for a mitosporic Ascomycota fungus, 20 1-4 Phylogenetic relationships of Crivellia and Brachycladium species according to Inderbitzin et al. (2006), 20 2-1 An example of a generalized conceptual model for mycoherbicide exposure that traces the potential physical exposure pathways of toxins, spores, and vegetative bodies from a particular application method to the general classes of ecological and human receptors, 45 3-1 Cannabis sativa, 48 3-2 Erythroxylum coca, 52 3-3 Major coca-producing countries in the Andean region, 54 3-4 Papaver somniferum, 57 4-1 A simplified diagram for commercial production of a bioherbicide using standard fermentation and downstream processing equipment, 74 TABLES 1-1 Major Cannabis-Cultivating and Cannabis-Producing Countries (2008, unless otherwise stated), 13 1-2 Global Illicit Cultivation of Coca and Production of Cocaine, 1995-2009, 14 1-3 Global Illicit Cultivation of Opium Poppy and Production of Opiates, 1995-2009, 15 2-1 Classical vs Bioherbicide Approach, 28 2-2 Status of Registered Mycoherbicides (2010), 31 4-1 Greenhouse and Field Studies in Italy by McCain and Noviello (1985), 65 4-2 Greenhouse and Field Studies in Kazakhstan by Tiourebaev et al. (2001), 66 4-3 Growth-Chamber and Field Studies by Sands et al. (1997), 69 4-4 Field Studies in Hawaii by Bailey et al. (1997, 1998), 70 4-5 Media and Methods Used for Production of Fusarium oxysporum f.sp. cannabis and Fusarium oxysporum f.sp. erythroxyli for Field Trials, 76 4-6 Estimated Amounts of Proposed Fusarium oxysporum Mycoherbicides Needed for Single Application Against Illicit Cannabis and Coca Crops Worldwide, 78 4-7 Developed and Tested Formulations of Fusarium oxysporum f.sp. cannabis and Fusarium oxysporum f.sp. erythroxyli, 79 4-8 Methods of Delivering Fusarium oxysporum f.sp. cannabis and Fusarium oxysporum f.sp. erythroxyli in Greenhouse and Field Experiments, 83

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xvi Contents 4-9 Effects of Temperature, Soil Type, and Matric Potential on Proliferation and Survival of Fusarium oxysporum f.sp. erythroxyli (Strain EN4-FT) in the Laboratory, 86 4-10 Greenhouse and Field Studies of Effects of Environmental Factors on Survival of Fusarium oxysporum f.sp. erythroxyli, 87 4-11 Plants Reportedly Tested in Host-Range Studies of Fusarium oxysporum f.sp. cannabis, 93 4-12 Plants Reportedly Tested in Host-Range Studies of Fusarium oxysporum f.sp. erythroxyli, 94 4-13 Classes of Mycotoxins Produced by Fusarium oxysporum, 96 5-1 Fungi Used in Various Papaver Mycoherbicide Studies, 102 5-2 Attributes of the Papaver Mycoherbicides Crivellia papaveracea and Brachycladium papaveris, 103 5-3 Greenhouse Study by Del Serrone and Annesi (1990), 106 5-4 Growth-Chamber Studies by O’Neill et al. (2000), 107 5-5 Field Trials in Uzbekistan and Tajikistan (2000-2001), 108 5-6 Methods Used for Production of C. papaveracea/B. papaveris Inoculum for Experimental Trials, 111 5-7 Estimated Amounts of the Proposed C. papaveracea/B. papaveris Needed for a Single Application against Illicit Opium-Poppy Crops Worldwide, 112 5-8 Effect of Adjuvants on the Efficacy of C. papaveracea/B. papaveris in Greenhouse and Field Experiments, 113 B-1 Microbial Pesticides Product Analysis Data Requirements, 158 B-2 Microbial Pesticides Residue Data Requirements, 159 B-3 Microbial Pesticides Toxicology Data Requirements, 160 B-4 Microbial Pesticides Nontarget Organisms and Environmental Fate Data Requirements, 162 B-5 Series 885—Microbial Pesticide Test Guidelines as of January 2010, 167