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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
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Printed in the United States of America
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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of
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tional Academy of Engineering in providing services to the government, the public, and
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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
