Feasibility of Using Mycoherbicides for Controlling Illicit Drug Crops (2011)

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
Washington, D.C.
http://www.nap.edu

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 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 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.

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

THE NATIONAL ACADEMIES

Advisers to the Nation on Science, Enginnering and Medicine

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 responsibility 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 National 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

This page intentionally left blank.

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.

This page intentionally left blank.

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

This page intentionally left blank.

Contents

SUMMARY

1         INTRODUCTION

           Fungal Terminology

           Statement of Task

           Committee’s Interpretation of its Task

           Committee’s Approach

           Organization of the Report

2         BIOLOGICAL CONTROL OF UNDESIRABLE PLANTS

           Background

           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

3         TARGET ILLICIT CROPS

           Cannabis: Cannabis Sativa

           Coca: Erythroxylum Species

           Opium Poppy: Papaver Somniferum

4         FUSARIUM OXYSPORUM FORMAE SPECIALES AS CANDIDATE BIOLOGICAL CONTROL AGENTS FOR CANNABIS AND COCA

           Background on the Specific Fungi

           Efficacy and Implementation

           Inoculum Production and Delivery

           Persistence in the Environment

           Effects on Nontarget Organisms

           Mutation

           What We Can Learn From A Natural Epidemic of fusarium oxysporum f.sp. erythroxyli Wilt of Coca in Peru

5         CRIVELLIA PAPAVERACEA AND BRACHYCLADIUM PAPAVERIS AS CANDIDATE BIOLOGICAL CONTROL AGENTS AGAINST OPIUM POPPY

           Efficacy and Implementation

           Inoculum Production and Delivery

           Persistence in the Environment

           Effects on Nontarget Organisms

           Mutation

           A Presumptive Disease Epidemic in Opium Poppy in Afghanistan

6         ANSWERS TO CHARGE QUESTIONS

           Effectiveness

           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

REFERENCES

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

3-1   Cannabis sativa

3-2   Erythroxylum coca

3-3   Major coca-producing countries in the Andean region

3-4   Papaver somniferum

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

4-10 Greenhouse and Field Studies of Effects of Environmental Factors on Survival of Fusarium oxysporum f.sp. erythroxyli

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