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
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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 provided support for this project.
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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
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
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
1This study was planned, overseen, and supported by the Board on Environmental Studies and Toxicology.
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 special 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, Congress 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 Mycoherbicides for Eradicating Illicit Drug Crops, which prepared this report. The members of the committee were selected for their expertise in plant pathology; mycotoxins; fungal genetics, evolution, and ecology; mycoherbicide development, evaluation, formulation, and application; plant-disease epidemiology; soil microbiology; medical mycology; human toxicology and risk assessment; and ecological 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 National Drug Control Policy; Jay Ellenberger and Christopher Wosniak, U.S. Environmental Protection Agency; John Bargeron and Scott Harris, U.S. Department of State; Henry Appleton and Bryan Bailey, U.S. Department of Agriculture; Mark Wach, Sylvan Biosciences; David Sands, Montana State University; Christopher Eusebi, Harness, Dickey & Pierce, PLC; and Brent Nowak, University of Texas at San Antonio.
This 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’s 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 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 University, 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 procedures 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 throughout the development of this report.
Raghavan Charudattan, PhD, Chair
Committee on Mycoherbicides for
Eradicating Illicit Drug Crops
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 |
Contents
Committee’s Interpretation of its Task
2 BIOLOGICAL CONTROL OF UNDESIRABLE PLANTS
Key Attributes of Effective Mycoherbicides in Use
Challenges to and Constraints in the Development and Large-Scale Use of Mycoherbicides
Pesticide Regulation in the United States
Considerations for International Testing and Use of Mycoherbicides
Risk to Nontarget Plants and Organisms
Opium Poppy: Papaver Somniferum
4 FUSARIUM OXYSPORUM FORMAE SPECIALES AS CANDIDATE BIOLOGICAL CONTROL AGENTS FOR CANNABIS AND COCA
Background on the Specific Fungi
Inoculum Production and Delivery
5 CRIVELLIA PAPAVERACEA AND BRACHYCLADIUM PAPAVERIS AS CANDIDATE BIOLOGICAL CONTROL AGENTS AGAINST OPIUM POPPY
Inoculum Production and Delivery
Persistence in the Environment
Effects on Nontarget Organisms
A Presumptive Disease Epidemic in Opium Poppy in Afghanistan
Feasibility of Large-Scale Manufacture and Delivery
Persistence in the Environment
Toxicity to Nontarget Organisms
Potential for Mutation and Resulting Toxicity to Target and Nontarget Organisms
Research and Development Needs
APPENDIXES
A BIOGRAPHIC INFORMATION ON THE COMMITTEE ON MYCOHERBICIDES FOR ERADICATING ILLICIT DRUG CROPS
B EPA REQUIREMENTS AND GUIDELINES UNDER 40 CFR 158, SUBPART V
BOXES, FIGURES, AND TABLES
BOXES
1-1 Questions Posed in the Statement of Task
2-1 Requirements for Tiered Toxicity Testing and Tiered Toxicity and Pathogenicity Testing under FIFRA (40 CFR 158, Subpart V)
FIGURES
1-1 Life cycle of a heterothallic Ascomycota fungus
1-2 Life cycle for a homothallic Ascomycota fungus
1-3 Life cycle for a mitosporic Ascomycota fungus
1-4 Phylogenetic relationships of Crivellia and Brachycladium species according to Inderbitzin et al. (2006)
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
3-3 Major coca-producing countries in the Andean region
4-1 A simplified diagram for commercial production of a bioherbicide using standard fermentation and downstream processing equipment
TABLES
1-1 Major Cannabis-Cultivating and Cannabis-Producing Countries (2008, unless otherwise stated)
1-2 Global Illicit Cultivation of Coca and Production of Cocaine, 1995-2009
1-3 Global Illicit Cultivation of Opium Poppy and Production of Opiates, 1995-2009
2-1 Classical vs Bioherbicide Approach
2-2 Status of Registered Mycoherbicides (2010)
4-1 Greenhouse and Field Studies in Italy by McCain and Noviello (1985)
4-2 Greenhouse and Field Studies in Kazakhstan by Tiourebaev et al. (2001)
4-3 Growth-Chamber and Field Studies by Sands et al. (1997)
4-4 Field Studies in Hawaii by Bailey et al. (1997, 1998)
4-5 Media and Methods Used for Production of Fusarium oxysporum f.sp. cannabis and Fusarium oxysporum f.sp. erythroxyli for Field Trials
4-6 Estimated Amounts of Proposed Fusarium oxysporum Mycoherbicides Needed for Single Application Against Illicit Cannabis and Coca Crops Worldwide
4-7 Developed and Tested Formulations of Fusarium oxysporum f.sp. cannabis and Fusarium oxysporum f.sp. erythroxyli
4-8 Methods of Delivering Fusarium oxysporum f.sp. cannabis and Fusarium oxysporum f.sp. erythroxyli in Greenhouse and Field Experiments
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
4-11 Plants Reportedly Tested in Host-Range Studies of Fusarium oxysporum f.sp. cannabis
4-12 Plants Reportedly Tested in Host-Range Studies of Fusarium oxysporum f.sp. erythroxyli
4-13 Classes of Mycotoxins Produced by Fusarium oxysporum
5-1 Fungi Used in Various Papaver Mycoherbicide Studies
5-2 Attributes of the Papaver Mycoherbicides Crivellia papaveracea and Brachycladium papaveris
5-3 Greenhouse Study by Del Serrone and Annesi (1990)
5-4 Growth-Chamber Studies by O’Neill et al. (2000)
5-5 Field Trials in Uzbekistan and Tajikistan (2000-2001)
5-6 Methods Used for Production of C. papaveracea/B. papaveris Inoculum for Experimental Trials
5-7 Estimated Amounts of the Proposed C. papaveracea/B. papaveris Needed for a Single Application against Illicit Opium-Poppy Crops Worldwide
5-8 Effect of Adjuvants on the Efficacy of C. papaveracea/B. papaveris in Greenhouse and Field Experiments
B-1 Microbial Pesticides Product Analysis Data Requirements
B-2 Microbial Pesticides Residue Data Requirements
B-3 Microbial Pesticides Toxicology Data Requirements
B-4 Microbial Pesticides Nontarget Organisms and Environmental Fate Data Requirements
B-5 Series 885—Microbial Pesticide Test Guidelines as of January 2010