Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides i
Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides
Council for Agricultural Science and Technology, Ames, Iowa, USA Printed in the United States of America
Cover design by Brianne Osborn, Brianne Osborn Design, Boone, Iowa Graphics and layout by Tom Hiett, Instructional Technology Center, Iowa State University, Ames
ISBN 1-887383-27-1 ISSN 0194-407x
Special Publication No. 24 June 2004
Council for Agricultural Science and Technology Ames, Iowa, USA ii
Steering Committee Members
Barry J. Jacobsen, Symposium Chair, Department of Plant Science and Plant Pathology, Montana State University, Bozeman
Sharlene R. Matten, Proceedings Chair, U.S. Environmental Protection Agency, Office of Pesticide Programs, Washington, D.C
Harold Coble, U.S. Department of Agriculture–Agricultural Research Service, Raleigh, North Carolina
Timothy J. Dennehy, Department of Entomology, University of Arizona, Tucson
Les Glasgow, R&D Weed Control Group, Syngenta Crop Protection, Vero Beach, Florida
Doug Gurian-Sherman, Biotechnology Project, Center for Science in the Public Interest, Washington, D.C.
Graham P. Head, Global Insect Resistance Management, Monsanto, St. Louis, Missouri
Rick Hellmich, U.S. Department of Agriculture–Agricultural Research Service, Ames, Iowa
Thomas O. Holtzer, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins
Wolfram Koeller, Department of Plant Pathology, Cornell University, Geneva, New York
Rodney G. Lym, Department of Plant Sciences, North Dakota State University, Fargo
Carol Mallory-Smith, Department of Crop and Soil Science, Oregon State University, Corvallis
Patricia F. O’Leary, Agricultural Research, Cotton Incorporated, Cary, North Carolina
Anthony M. Shelton, Department of Entomology, Cornell University, Geneva, New York
Nicholas P. Storer, Regulatory Laboratories, Dow AgroSciences, Indianapolis, Indiana
Gary D. Thompson, Insect Management Global, Dow AgroSciences LLC, Indianapolis, Indiana
Mark E. Whalon, Pesticide Research Center, Michigan State University, East Lansing
Hendrik L. Ypema, Biology Project Leader, BASF Corporation, Research Triangle Park, North Carolina
ii Managementiii of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides iii
Symposium Contributors
*Ralph Bagwell, Cooperative Extension Service, Louisiana State University, Winnsboro
Jerry J. Baron, Center for Minor Crop Pest Management, Rutgers University, North Brunswick, New Jersey
*Pierre Beauchamp, Pest Management Regulatory Agency, Health Canada, Ottawa, Ontario
*Charles Benbrook, Benbrook Consulting Services, Sandpoint, Indiana
Patrick S. Bills, Department of Entomology, Michigan State University, East Lansing
*Michael P. Braverman, Center for Minor Crop Pest Management, Rutgers University, North Brunswick, New Jersey
*Kevin Brussell, Rainy Creek Farms, Casey, Illinois
Brett Bussler, Monsanto Company, St. Louis, Missouri
*Dennis D. Calvin, Department of Entomology, The Pennsylvania State University, University Park
*Frank L. Carter, National Cotton Council of America, Memphis, Tennessee
*Roger Carter, AMS Incorporated, Clayton, Louisiana
*Timothy J. Dennehy, Department of Entomology, University of Arizona, Tucson
*Natalie DiNicola, Regulatory Affairs, Monsanto Company, St. Louis, Missouri
Greg Elmore, Monsanto Company, St. Louis, Missouri
David Ehnis, Electric Software LLC, East Lansing, Michigan
Wendy Gelernter, PACE Turfgrass Research Institute, San Diego, California
*Les Glasgow, R&D Weed Control Group, Syngenta Crop Protection, Vero Beach, Florida
Erin Gould, Department of Entomology, Michigan State University, East Lansing
*Teresa A. Gruber, Council for Agricultural Science and Technology, Washington, D.C.
*Doug Gurian-Sherman, Biotechnology Project, Center for Science in the Public Interest, Washington, D.C.
Aaron G. Hager, Department of Crop Sciences, University of Illinois at Urbana–Champaign, Urbana
*D. D. Hardee, Southern Insect Management Research Unit, U.S. Department of Agriculture–Agricultural Research Service, Stoneville, Mississippi
iii iv Symposium Contributors
*Graham P. Head, Global Insect Resistance Management, Monsanto, St. Louis, Missouri
*Ian M. Heap, International Survey of Herbicide–Resistant Weeds, Weed Smart LLC, Corvallis, Oregon
*David C. Heering, Roundup Technical Lead, Monsanto Company, St. Louis, Missouri
Robert Hollingworth, Department of Entomology, Michigan State University, East Lansing
Robert E. Holm, Center for Minor Crop Pest Management, Rutgers University, North Brunswick, New Jersey
*Thomas O. Holtzer, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins
*Barry J. Jacobsen, Department of Plant Science and Plant Pathology, Montana State University, Bozeman
*Monte P. Johnson, U. S. Department of Agriculture–Cooperative State Research, Education, and Extension Service, Washington, D.C.
Roger P. Kaiser, Bayer CropScience, Research Triangle Park, North Carolina
*John Keeling, National Potato Council, Washington, D.C.
*Wolfram Koeller, Department of Plant Pathology, Cornell University, Geneva, New York
Daniel L. Kunkel, Center for Minor Crop Pest Management, Rutgers University, North Brunswick, New Jersey
*Carol Mallory-Smith, Department of Crop and Soil Science, Oregon State University, Corvallis
Dean K. Malvick, Department of Crop Sciences, University of Illinois at Urbana–Champaign, Urbana
*Sharlene R. Matten, U.S. Environmental Protection Agency, Office of Pesticide Programs, Washington, D.C.
*Charles Mellinger, Glades Crop Care, Jupiter, Florida
David Mota-Sanchez, Department of Entomology, Michigan State University, East Lansing
Terry L. Niblack, Department of Crop Sciences, University of Illinois at Urbana–Champaign, Urbana
Robert L. Nichols, Agricultural Research, Cotton Incorporated, Cary, North Carolina
*Gilberto Olaya, Fungicides, Syngenta Crop Protection, Vero Beach, Florida
*Patricia F. O’Leary, Agricultural Research, Cotton Incorporated, Cary, North Carolina
*Eldon E. Ortman, U. S. Department of Agriculture–Cooperative State Research, Education, and Extension Service, Plant and Animal Systems, Washington, D.C.
*Michael D. Orzolek, Department of Horticulture, The Pennsylvania State University, University Park
*Scott Pace, Registration and Marketing, Helena Chemical Company, Memphis, Tennessee Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides v
*Cindy Lynn Richard, Council for Agricultural Science and Technology, Washington, D.C.
*Richard Roush, Statewide IPM Program, University of California–Davis, Davis
Joseph M. Russo, ZedX, Bellefonte, Pennsylvania
R. Sammons, Monsanto Company, St. Louis, Missouri
*Caydee Savinelli, Insecticides, Syngenta Crop Protection, Greensboro, North Carolina
*Marvin Schultz, Dow AgroSciences, Indianapolis, Indiana
*David Scott, Office of the Indiana State Chemist, Purdue University, West Lafayette, Indiana
*Dale L. Shaner, U.S. Department of Agriculture–Agricultural Research Service, Water Management Research, Ft. Collins, Colorado
*Anthony M. Shelton, Department of Entomology, Cornell University, Geneva, New York
*Thomas Slunecka, National Corn Growers Association, Chesterfield, Missouri
*Margaret E. Smith, Department of Plant Breeding, Cornell University, Ithaca, New York
Christy L. Sprague, Department of Plant and Soil Science, Michigan State University, East Lansing
*Kevin L. Steffey, Department of Crop Sciences, University of Illinois at Urbana–Champaign, Urbana
*Walter R. Stevenson, Department of Plant Pathology, University of Wisconsin–Madison, Madison
*Ronald E. Stinner, Center for IPM, North Carolina University, Raleigh
*Nicholas P. Storer, Regulatory Laboratories, Dow AgroSciences LLC, Indianapolis, Indiana
*Larry Stowell, PACE Turfgrass Research Institute, San Diego, California
*Gary D. Thompson, Insect Management Global, Dow AgroSciences LLC, Indianapolis, Indiana
*Mark E. Whalon, Department of Entomology, Michigan State University, East Lansing
*Wayne F. Wilcox, Department of Plant Pathology, Cornell University, Geneva, New York
*Hendrik L. Ypema, Biology Project Leader, BASF Corporation, Research Triangle Park, North Carolina
J. Z. Zhao, Department of Entomology, Cornell University, Geneva, New York
* Speaker at the symposium vi
Contributing Organizations Symposium Sponsors
BASF Corporation Bayer Crop Science Cotton Incorporated CropLife America DuPont Agricultural Products/Pioneer Hi-Bred International, Inc. Fungicide Resistance Action Committee (FRAC) (A Specialist Technical Group of CropLife International) Global Herbicide Resistance Action Committee (Global HRAC) Insecticide Resistance Action Committee (IRAC)–United States (A member organization of CropLife America) National Corn Growers Association
Proceedings Sponsor
USDA/CSREES Grant No. 2003-38836-01790
Additional Contributors
Dow AgroSciences (Loan of equipment) Fourth National Integrated Pest Management Symposium, Organizing Committee (Meeting space) National Science Foundation Center for Integrated Pest Management, North Carolina State University (Web posting of symposium presentations) U.S. Environmental Protection Agency (Interagency Personnel Act Agreement, Sharlene R. Matten, Ph.D., staff support to CAST, February–June 2003)
vi Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides vii
Acknowledgments
The Council for Agricultural Science and Technology (CAST) thanks the Steering Committee for planning and organizing this exciting and enlightening symposium. CAST recognizes and appreciates the many organi- zations, named in the Contributing Organizations List, who provided support for the symposium and these pro- ceedings. CAST also wishes to thank all the speakers, moderators, rapporteurs, participants, and contributing authors who made the symposium a success.
The Steering Committee recognizes the outstanding efforts of two persons who provided leadership and as- sistance at many stages of the project: Cindy Lynn Richard, CIH, Program Coordinator at CAST, for extensive symposium planning; and Sharlene R. Matten, Ph.D., U.S. Environmental Protection Agency, on loan to CAST at the time of the symposium, for assiduous coordination work on the symposium and the proceedings as well as drafting key sections of the publication.
vii viii
Contents
Interpretive Summary ...... 1 Keys to Effective Resistance Management, 2 Symposium Conclusions, 2 Symposium Recommendations, 2
Introduction ...... 4
1.1 Scope of North American Pest Resistance Problems in 2003: An Overview, Mark E. Whalon and Robert Hollingworth ...... 6 Introduction, 6 Environmentalism and Consumerism, 6 Regulations, 7 Summary, 8 Literature Cited, 8
1.2 Arthropods Reported to Be Resistant to Pesticides, Mark E. Whalon, Patrick S. Bills, David Mota-Sanchez, Robert Hollingworth, Gary D. Thompson, and David Ennis ...... 9
1.3 Scope and Magnitude of Herbicide-Resistant Weeds in North America, Ian M. Heap...... 12 Introduction, 12 Herbicide Resistance, 12 Occurrence of Resistance, 12 Resistance Management Strategies, 14 Adoption of Resistance Management, 15 Literature Cited, 15
1.4 Pathogens, Wolfram Koeller ...... 17 Introduction, 17 Fungicides and Fungicide Resistance, 17 Antiresistance Strategies, 18 Challenges, 18 Literature Cited, 19
2.1 Resistance Issues in Fruit and Vegetable Production Systems, Charles Mellinger ...... 20 Insect Management, 20 Disease Management, 21 Weed Management, 21 Current Resistance Management Efforts, or, What Is Being Done?, 22 Barriers to Resistance Management, 23 Literature Cited, 23
2.2 Resistance Issues in Cotton Pest Management, Patricia F. O’Leary and Robert L. Nichols ...... 25 Introduction, 25 Current Status, 25
viii Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides ix
Management Strategies, 27 Current Concerns, 27 Barriers to Resistance Management, 28 Literature Cited, 28
2.3 Resistance Issues in Potatoes, John Keeling ...... 30
2.4 Resistance Issues in Corn/Soybean Cropping Systems, Kevin L. Steffey, Aaron G. Hager, Dean K. Malvick, Terry L. Niblack, and Christy L. Sprague ...... 33 Introduction, 33 Insect Management, 33 Nematode Management, 34 Plant Disease Management, 35 Weed Management, 36 Literature Cited, 37
2.5 Resistance Issues in Golf Course Turf, Wendy Gelernter and Larry Stowell ...... 38 Introduction, 38 Pesticide Resistance Issues, 38 Barriers to Adoption of Resistance Management Programs, 40 Solutions, 41 Literature Cited, 42
2.6 Resistance Issues in Organic Cropping Systems, Kevin Brussell ...... 43
3.1 Triazines, Acetolactate Synthase Inhibitors, and Protoporphyrinogen Oxidase Inhibitors, Les Glasgow ...... 44 Introduction, 44 Triazines, 44 ALS Inhibitors, 45 Protoporphyrinogen Inhibitors, 47 Factors Influencing Resistance Evolution and Management, 48 Barriers to Resistance Management, 49 Overall Conclusion, 49 Literature Cited, 49 Suggested Reading, 50
3.2 Glyphosate: A New Model for Resistance Management, David C. Heering, Natalie DiNicola, R. Sammons, Brett Bussler, and Greg Elmore ...... 51 Introduction, 51 Chemical Properties of Glyphosate, 51 Weed Management Strategies for Glyphosate, 53 ALS Herbicide Case Study in Iowa, 54 Summary, 54 Literature Cited, 54
3.3 Demethylation Inhibitor Fungicide Resistance in Fruit Crops, Wayne F. Wilcox ...... 56 Introduction, 56 Management of the Problem, 56 Barriers to Resistance Management, 58 Literature Cited, 59 x Contents
3.4 Diamondback Moth Resistance in Crucifers, Anthony M. Shelton and J. Z. Zhao ...... 61 Background, 61 Early Surveys for Resistance, 61 Examples of Resistance Development in Individual States, 62 Transgenic Plants, 63 Lessons Learned and Recommendations, 64 Literature Cited, 64
3.5 Insect Resistance Management for Transgenic Bt Crops, Graham P. Head...... 66 Introduction, 66 IRM Approaches, 66 Relevant Characteristics of Bt Crops, 66 IRM for Bt Crops, 67 Adapting IRM for Bt Crops to Local Conditions, 67 Lessons Learned about How to Make IRM Successful, 68
4.1 What Have Insect Resistance Management Models Taught Us?, Nicholas P. Storer ...... 69 Introduction, 69 Some Learning from Simple Models, 69 Adding Complexity—Spatial and Stochastic Processes, 69 Handling Uncertainty, 70 Applications of Spatial Models, 70 Conclusions, 70 Literature Cited, 71
4.2 Resistance Management Strategies: Have Models Helped?, Richard Roush...... 73 Introduction, 73 High Doses Versus Low Doses: The Importance of Heterozygotes, 73 Two Toxins: Mosaics, Rotations, and Mixtures, 74 Validation, 75 Literature Cited, 75
4.3 Herbicide Resistance Models: Have They Helped?, Carol Mallory-Smith ...... 77 Predictive Role of Models, 77 How Models Were Used to Identify Data Gaps, 77 Uncertainty Associated with Various Parameters, 78 Validation of Models, 79 Literature Cited, 79
4.4 Lessons Learned in Predicting and Assessing the Risk of Fungicide Resistance: Have Models Helped?, Hendrik L. Ypema ...... 80 Introduction, 80 Models Addressing Fungicide Resistance Development, 80 Model Assumptions, 80 An Example: Resistance Development to QoI Fungicides, 81 Have Models Helped?, 82 Conclusions, 82 Literature Cited, 82
5.1 Pesticide Resistance Management: Is There a Role for Consumers?, Doug Gurian-Sherman...... 84 Introduction, 84 Consumers, Pesticides, and PRM, 84 Barriers to Consumer Support for PRM, 87 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides xi
Solutions and Conclusions, 87 Literature Cited, 88
5.2 Role of Stakeholders in Resistance Management: Crop Consultants, Roger Carter ...... 89 Introduction, 89 Barriers to RM and How to Eliminate Them, 89 Goals of Independent Agricultural Consultants, 90 Perception of Other Stakeholders’ Goals, 90 Economics Should Always Be First, 90 Summary, 91
5.3 Role of Producers in Management of Resistance, Frank L. Carter ...... 92 Introduction, 92 Background, 92 Current Cotton Pest Situation, 92 Question #1: What Are the Barriers to RM?, 92 Question #2: What Are the Goals of RM Implementation for Producers?, 93 Question #3: What Are the Goals of Others in Pest RM?, 93 Summary of Questions, 93 Producer Perspective Summary, 93
5.4 Industry’s Perspective on Insect Resistance Management and Its Implementation, Caydee Savinelli, Graham P. Head, and Gary D. Thompson ...... 95 Introduction, 95 Industry Goals, 95 Key Tactics, 95 Barriers, 96 Conclusions, 96
5.5 Role of Stakeholders in Resistance Management: Pesticide Manufacturers, Gilberto Olaya ...... 97 Introduction, 97 Barriers to Resistance Management Implementation, 97 Goals of Resistance Management Implementation, 98 Goal of Others in Fungicide Resistance Management, 98
5.6 Barriers to Implementation, Marvin Schultz ...... 100 Introduction, 100 Barriers to Implementation, 100 Stakeholders’ Interests, 101
5.7 The Environmental Protection Agency and the Pest Management Regulatory Agency: Pest Resistance Management Goals and Challenges, Sharlene R. Matten and Pierre Beauchamp ...... 102 Introduction, 102 Overall Pesticide Resistance Management Goals, 102 Status of Mode of Action Labeling under NAFTA, 103 Other EPA Resistance Management Regulatory Activities, 103 Barriers to Proactive Resistance Management Implementation, 104 Challenges to Proactive Resistance Management Implementation, 104 Roles of Other Stakeholders in Resistance Management, 105 Summary, 106 Literature Cited, 106 xii Contents
5.8 Issues in Pest Resistance Management, Eldon E. Ortman ...... 107 Introduction, 107 Recommended Resistance Management Strategy, 107 Questions about Pest Resistance, 107 Questions about Regulation, 108 A Final Example, 108
5.9 Interregional Research Project No. 4 Program and Minor Crops: Developing Choices for Pest Resistance Management, Michael P. Braverman, Daniel L. Kunkel, Jerry J. Baron, and Robert E. Holm 109 Introduction, 109 Choices in Pest Management, 109 Biopesticides, 110 Reduced-Risk Products, 110 Crop Grouping, 111 Impacts of Biotechnology, 112 Literature Cited, 113
5.10 Pesticide Education and Training Programs, Monte P. Johnson ...... 114 Pesticide Safety Education Program Information, 114 Pest Resistance Survey, 114
5.11 Role of Stakeholders: State Pesticide Regulation, David Scott...... 115 Role of the Pesticide State Lead Agency, 115 Barriers to Resistance Management Implementation, 115 Goals of Resistance Management Implementation, 115
5.12 Role of Extension in Management of Pest Resistance, Walter R. Stevenson...... 116 Introduction, 116 Resistance Management Plans, 116 Role of Extension, 116
5.13 Regulation, Research, and Funding, Thomas O. Holtzer...... 118 Introduction, 118 Researchers’ Interests, 118 Funding, 118 Partnership Opportunities, 119
6.1 Industry’s Suggestions for Solutions and Working Together, Gary D. Thompson, Graham P. Head, and Caydee Savinelli ...... 120 Introduction, 120 Current Barriers, 120 Solutions, 120
6.2 How Can We Alleviate Barriers?, Roger P. Kaiser ...... 122 Introduction, 122 Current Efforts, 122 Eliminating Barriers, 123
6.3 Ways to Work Together, Natalie DiNicola ...... 124 Introduction, 124 Goals, 124
6.4 Eliminating Barriers, Roger Carter...... 126 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides xiii
6.5 Lessons Learned: Growers’ Perspective, John Keeling ...... 127
6.6 Stakeholder Roles in Resistance Management: Time to Get with the Program, Charles Benbrook ...... 128 Introduction, 128 Whose Job Is Resistance Management?, 128 Cracking the Resistance Management Nut, 129 Goal of Resistance Management, 130 Wisconsin–Florida RAMP Project RM Goals, 131 Next Generation RMPs, 131 Concluding Thoughts, 132 Literature Cited, 132
6.7 Lessons Learned: Academic Research Perspective, Thomas O. Holtzer ...... 133
6.8 Potential Resources to Address Resistance Management, Eldon E. Ortman ...... 134 Introduction, 134 Regionally Focused Programs, 134 Nationally Focused Programs (Discovery to Implementation), 134
6.9 Lessons Learned: State Regulatory Perspective, David Scott ...... 137
6.10 Public Sector Plant Breeding and Pest Resistance Management, Margaret E. Smith, ...... 138 Introduction, 138 Designing for Sustainability, 138 Durable Resistance, 138 Background Resistance Underlying Transgenes, 139 Identifying Optimal Refuge Varieties, 139 Heterogeneous Varieties, 139 Novel Sources of Resistance, 140 Need for Public Sector Plant Breeding, 140 Literature Cited, 140
6.11 Working Together to Remove Resistance Management Barriers and to Adopt Proactive Resistance Management Strategies: A U.S. Perspective, Sharlene R. Matten ...... 141 Introduction, 141 Removing Barriers and Working Together to Achieve Proactive Resistance Management, 141 Summary, 141
6.12 Working Together to Remove Resistance Management Barriers and to Adopt Proactive Resistance Management Strategies: A Canadian Perspective, Pierre Beauchamp ...... 142 Introduction, 142 Removing Barriers and Working Together to Achieve Proactive Resistance Management, 142 Summary, 142
7.1 Herbicide Resistance Management Strategies for Weeds, Dale L. Shaner ...... 143 Introduction, 143 Proactive Versus Reactive Herbicide Resistance Management, 143 Role of Resistance Monitoring, 143 Strategies for Herbicide Resistance Management, 144 Literature Cited, 145 xiv Contents
7.2 Pest Resistance Management Goals: Monitoring Insects, D. D. Hardee ...... 147 Introduction, 147 Pests in Cotton, 147 Monitoring Program, 148 Literature Cited, 149
7.3 Resistance Management Strategies for Plant Pathogens, Barry J. Jacobsen ...... 150 Introduction, 150 Risk Assessment, 150 Management of Plant Pathogen Resistance, 151 Creating the Environment for Management of Plant Pathogen Resistance, 151 Literature Cited, 151
7.4 Use of Information Technology in Resistance Management and Refuge Compliance, Dennis D. Calvin and Joseph M. Russo ...... 153 Introduction, 153 Value of Bacillus thuringiensis Corn Hybrids, 153 Effective Resistance Management Programs, 153 Predicting the Value of a Technology, 154 Information Technology Tools for Refuge Compliance, 155 Literature Cited, 156
7.5 Resistance Management Education and Communication: Weeds in Vegetable Crops, Michael D. Orzolek ...... 157 Introduction, 157 Weed Management Programs, 157 Cultural Controls, 157 Sweet Corn: A Case Study, 159
7.6 The Resistant Pest Management Newsletter and Resistant Arthropods Database, Mark E. Whalon and Erin Gould ...... 160 Introduction, 160 RPM News, 160 Resistance Database, 161
7.7 Resistance Management Education and Communication, Ronald E. Stinner...... 162 Introduction, 162 Four Cooperators, 162
7.8 A Producer’s View of Managing Bacillus thuringiensis Technology, Thomas Slunecka ...... 164 Introduction, 164 Insect Resistance Management Requirements, 164 Role of the National Corn Growers Association, 164 Literature Cited, 165
Conclusions and Recommendations ...... 166 Conclusions, 166 Recommendations and Suggestions, 167 Literature Cited, 169
Appendix A: Abbreviations and Acronyms ...... 170 Appendix B: Glossary...... 172 Appendix C: Symposium Agenda ...... 174 Appendix D: Symposium Attendees ...... 178 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides xv
Figures
1.2.1. Profile of resistance for Leptinotarsa decemlineata, 9
1.2.2. Timeline of arthropod pesticide resistance and pesticide registrations in the United States, 10
1.3.1. Chronological increase in the number of herbicide-resistant weeds in the United States and worldwide, 13
1.3.2. Chronological increase in the number of herbicide-resistant weeds worldwide to six herbicide classes, 14
1.3.3. Chronological increase in the number of herbicide-resistant weeds in the United States to six herbicide classes, 14
3.2.1. Compounds in modes of action versus resistant species, 52
5.9.1. The number of new uses for conventional pesticides obtained through IR–4 petitions to the EPA, 1990 to 2001, 110
7.4.1. High-resolution landscape map of projected economic value of a 100-day Bt corn hybrid planted on May 1, 2002 using the European corn borer management model, 154
7.4.2. Example of how fields, bounded with GPS coordinates, can be used for hybrid location and the calculation of resistance management compliance, 156
xv xvi
Tables
1.2.1. Summary of documented cases of arthropods resistant to pesticides, 11
1.3.1. Number of herbicide-resistant biotypes reported by country for the top ten countries, 13
1.3.2. Herbicide resistance summary table for the United States, 13
2.2.1. Cotton insect pests with populations resistant to one or more classes of insecticides, 25
2.2.2. Weeds in cotton with populations resistant to one or more herbicide modes of action, 26
2.5.1. Turfgrass diseases that have been reported to have resistance to fungicides, 40
2.5.2. Turfgrass insects that have been reported to have resistance to insecticides, 40
2.5.3. Turfgrass weeds that have been reported to have resistance to herbicides, 40
2.5.4. Risk factors for pest resistance in turfgrass: High-risk pesticides. Pesticide classes and products char- acterized by frequent usage, single-site and/or specific modes of action, systemic activity/long residual activity, and/or with a history of causing resistance are considered high risk, 41
2.5.5. Risk factors for pest resistance in turfgrass: High-risk pests. High-risk pests have one or more of the following characteristics: dominate control practices on a consistent basis, multiple generations per year, sexual reproduction, high reproductive rates, and/or a history of resistance to pesticides, 42
5.9.1. Potential and adopted biotechnology-derived pest management in minor crops, 112
xvi Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides xvii
Foreword
Following a recommendation by the CAST National who made additional contributions to assist in the Concerns Committee, the CAST Board of Directors preparation of this document. The members of CAST authorized development of a symposium to address deserve special recognition because their unrestrict- issues regarding pest resistance management. An ed contributions in support of CAST financed the eminent group of experts was chosen as a Steering preparation and online presentation of this Special Committee, under the leadership of Dr. Barry J. Ja- Publication. cobsen. The committee planned and conducted the CAST is providing electronic access to this docu- symposium, which was held on April 10–11, 2003 in ment to a broad range of government officials includ- Indianapolis, Indiana in conjunction with the Fourth ing Members of Congress, the White House, the U.S. National Integrated Pest Management Symposium Department of Agriculture, the Food and Drug Ad- that took place on April 8–10. After the CAST sym- ministration, the Environmental Protection Agency, posium, Dr. Sharlene R. Matten chaired the develop- and the Congressional Research Service. Additional ment of this Special Publication. recipients include media personnel and institutional Symposium authors submitted drafts of their pre- members of CAST. Individual members of CAST may sentations that were edited by the CAST editorial access the document free of charge through the CAST staff. The CAST Executive Committee and Editorial website at
xvii Interpretive Summary
These proceedings reflect presentations and discus- 1. Scope of North American Pest Resistance sions from the two-day national symposium held April Problems in 2003. The first session presented 10–11, 2003 in Indianapolis, Indiana, entitled “Man- assessments of the scope and magnitude of pest/ agement of Pest Resistance: Strategies Using Crop pesticide resistance problems in North America Management, Biotechnology, and Pesticides.” The among insects, weeds, and pathogens by respec- symposium, convened by the Council for Agricultur- tive experts in the field. al Science and Technology (CAST), was the first U.S.- 2. Issues in Pest Resistance Management. based multidisciplinary stakeholder meeting on pest Speakers addressed pest resistance issues for resistance management (PRM) since the 1995 Amer- major North American crops, looking at what has ican Chemical Society meeting on mechanisms of pest been and is being done to protect against resis- resistance and the 1984 National Research Council tance and assessing barriers to PRM. The discus- meeting on pest resistance. The symposium provid- sion included fruits and vegetables, cotton, pota- ed the opportunity for stakeholders involved in insect, to, small grains, corn/soybean, turf/ornamental weed, and pathogen pest management to come togeth- crops, and organic agriculture. er in a fruitful discussion of issues, laying the foun- 3. Lessons Learned I: Balance between Indus- dation for future collaborations addressing PRM. try, Academia, Users, and Regulators. Case The overall goal of the symposium was to provide studies were presented to examine how the pest/ a collective framework in which more effective and pesticide resistance concerns raised in the previ- preventative pest resistance management could be de- ous two sessions actually have been addressed in veloped. The major objectives of the symposium were the field. The studies included glyphosate and ac- to (1) identify the common issues related to PRM etolactate synthase herbicide resistance, fungi- across disciplines; (2) identify ways to remove barri- cide resistance in fruit and vegetable crops, insec- ers that hinder more effective and preventive resis- ticide resistance in pests of cotton and crucifers, tance management (RM); (3) provide opportunities for and insect RM in Bacillus thuringiensis (Bt) crops. further discussions on PRM; (4) identify research ac- 4. Lessons Learned II: Have Models Helped? tivities in RM; and (5) provide this information to law- Speakers addressed the predictive and descriptive makers, federal agencies—especially the U.S. Envi- roles modeling plays in RM. Issues discussed in- ronmental Protection Agency (EPA) and the U.S. cluded how models have been used to identify data Department of Agriculture (USDA)—academia, ex- gaps/needs, the uncertainty associated with input tension, industry, consultants, and the public. parameters, and, ultimately, the validity and ap- The agenda was developed by a steering commit- plicability of modeling as an effective assessment tee composed of representatives from the EPA, the tool. USDA, industry (Resistance Action Committees), ac- 5. Role of Stakeholders. Speakers from various ademia, public interest groups, and grower organiza- stakeholder groups addressed their own roles and tions. Forty-seven speakers gave a total of 55 presen- the roles of others in PRM, as well as barriers and tations, 52 of which are compiled in this publication. challenges in RM. Most of the eight sessions included an opportunity for 6. Lessons Learned III: How Can We Work to public comment and discussion. Approximately 120 Remove Barriers to Comprehensive Resis- stakeholders from industry, academia, extension, con- tance Management Implementation? How sultancies, federal and state governments, grower or- Can We Work Together Better? This two-part ganizations, and public interest groups participated session examined the opportunities for consum- in the symposium. ers, pesticide distributors and producers, federal The organization of these proceedings reflects the and state regulators, researchers, and educators eight sessions of the symposium agenda. to overcome common obstacles to effective RM.
1 2 Interpretive Summary
7. Pest Resistance Management Goals. This ses- •Resistance management benefits must be demon- sion focused on specific strategies for PRM. Speak- strated to growers. ers outlined the reasons for proactive rather than • Successful RM should be profitable, sustainable, reactive RM, assessed the role of monitoring and and environmentally beneficial. agricultural information technology, and high- • Federally funded RM research is important to the lighted practical measures to limit selection pres- successful development and implementation of ef- sure. The role of education and communication in fective RM strategies and should be a component long-term PRM also was discussed. of federally funded IPM grant programs. 8. Symposium Conclusions and Recommenda- • The USDA and the EPA play important roles in tions. The last section of these proceedings is a PRM and pesticide regulation. compilation of conclusions and recommendations • Central and permanent databases of pest and pes- that were reached during the presentations and ticide resistance information are important and discussions throughout the symposium. need continued funding. • Agricultural information technology provides a mechanism for disseminating forecast tools to Keys to Effective Resistance know where and when to use a pest control tech- nology. Management • Barriers exist that impede the development of ef- fective RM strategies. These barriers include (1) The coverage of different classes of pesticides (her- limited understanding of the factors affecting re- bicides, fungicides, and insecticides) made evident the sistance evolution, (2) limited product availabili- important differences among and within these class- ty, (3) economic factors, (4) short-term solutions, es in terms of RM needs and highlighted the necessi- (5) focus on individual crops/pests rather than a ty of addressing these needs on a case-by-case basis. holistic systems approach for the agroecosystems, The overall conclusion of the symposium was that (6) lack of clear goals and objectives, (7) lack of PRM is very important to the sustainability of agri- clear RM regulatory policy, (8) limited federally cultural production systems. Achieving proactive or funded and industrial funded RM research, and preventive RM is a desirable goal, but how to achieve (9) competitive marketing practices within indus- it is a complex process that requires extensive input try that discourage proactive/preventative RM. and commitment by all stakeholders. The keys to ef- •Predictive models are useful for comparing RM fective RM are strong science; environmentally be- options and identifying key data gaps, but they nign, feasible, and cost-effective strategies; and edu- offer a simplified reality. cation about the benefits of implementation. In • Resistance monitoring plays an important role in addition, multiple pest control tactics including cul- surveillance and detection of resistance before tural practices, biological control, transgenic plants field failure when suitable tools are available. producing pesticidal substances (such as Bt insecti- • Plant breeding can be an important component in cidal toxins), and chemical pesticides (with different successful implementation of effective RM and modes of action) can help decrease the selection pres- should be encouraged in this context. sure for the evolution of pest resistance. Further re- • In organic production of short-term annuals, pest search into the development, implementation, and resistance has been a big issue because of the ex- adoption of RM is necessary. tensive focus on crop rotation and other cultural management practices, soil management, and the use of biological pesticides. Symposium Conclusions
• Understanding of the scientific basis for why a Symposium Recommendations strategy works is fundamental to the success of effective, preventative RM strategies. Participants made several RM recommendations • Formulating RM plans before commercialization and suggestions in a discussion held at the end of the of a new chemical active ingredient is desirable. symposium. These recommendations focused on four • Education and training are fundamental to the areas: (1) Science, (2) Research and Extension, (3) Ed- implementation and adoption of RM strategies. ucation, and (4) Policy. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 3
Science Recommendations Policy Recommendations
• Resistance management strategies should be de- • Although all stakeholders noted the EPA’s role in veloped on a case-by-case basis, considering char- RM as being important, there was disagreement acteristics of the chemistry, the target pests, and about the scope and regulatory nature of this role. the management system using certain guiding Some participants recommended a mandatory principles. role for the EPA in RM, but consensus was not • Guidance and direction are needed in developing achieved in the limited time available. resistance monitoring programs for new technol- • Several suggestions were made that Farm Bill ogies including establishment of baseline suscep- priorities should be changed to provide better tibility, detection techniques, and sampling strat- funding of RM research and education, e.g., the egies. Natural Resources Conservation Service should • Resistance management strategies should be flex- recognize RM as a conservation practice. ible to allow changes over time due to the tempo- ral and spatial variation in the pest/crop/pesticide situation. Databases can be used to measure the extent of resistance both temporally and spatial- ly. Further funding of resistance databases is rec- ommended. • Standard definitions should exist for resistance for pest/pesticide combinations and methods of documentation and validation. • Economic benefits and costs of effective RM should be clearly developed and articulated.
Research and Extension Recommendations • There should be explicit RM priorities within the federal government, e.g., create a new competitive grants program to focus on RM, strengthen exist- ing USDA competitive grants research programs to provide more explicit priorities to fund RM re- search, strengthen RM research for minor crops and Regional Integrated Pest Management Cen- ters. • Create an RM research initiative supported joint- ly by funds from a user fee associated with pesti- cide sales and funds from the federal government.
Education Recommendations • Resistance management education programs should continue to be developed and implement- ed as part of ongoing pesticide education pro- grams. • Consumer education programs should include the cost of producing “blemish-free” food in the mar- ketplace and the use of reduced-risk pesticides. • The USDA grading standards and the marketing of food internationally should be examined for their impact on RM. Introduction
Pesticide resistance1 can be defined as a heritable Strategies Using Crop Management, Biotechnology, and significant decrease in the sensitivity of a pest and Pesticides” to encourage a cross-disciplinary di- population to a pesticide. Pests are found in groups alogue among different stakeholders working on pest as diverse as insects, mites, fungi, bacteria, viruses, resistance management issues involving insects, weeds, nematodes, and certain mammalian species pathogens, and weeds. The overall goal of the sympo- such as rodents. Worldwide, more than 540 insect and sium was to provide a collective framework in which mite species (MSU–CIPS 2000), more than 100 plant more effective and preventative resistance manage- pathogen species, and more than 270 weed biotypes ment could be developed. The major objectives of the (WeedScience 2003) are reported to have evolved re- symposium were to (1) identify the common issues sistance to pesticides (Hart and Pimentel 2002). Vir- related to pest resistance management across disci- tually every chemical pest suppression tactic known plines; (2) identify ways to remove barriers that has elicited some form of adaptive biochemical re- hinder more effective and preventative resistance sponse in the target pest. Behavioral adaptation to management; (3) provide opportunities for further pest management practices also is known. For exam- discussions on pest resistance management; (4) iden- ple, certain corn rootworm populations no longer are tify research activities in resistance management; and controlled by rotating soybean with corn. Pesticide (5) provide this information to lawmakers, federal resistance can lead to unsatisfactory pest control, in- agencies—especially the U.S. Environmental Protec- creased crop losses, increased control costs, and in- tion Agency (EPA) and the U.S. Department of Agri- creased use of pesticides, especially in the absence of culture (USDA)—academia, extension, industry, con- viable alternatives. Pest resistance management is a sultants, and the public. very important component of integrated pest manage- The symposium was held April 10–11, 2003 in In- ment (IPM) because it can help to ensure sustainable dianapolis, Indiana. The agenda was developed by a production-scale agriculture, uninterrupted food safe- steering committee consisting of representatives from ty, and continued environmental protection. the USDA, the EPA, industry (Resistance Action The United Nations Environmental Program list- Committees), academia, public interest groups, and ed pest resistance to pesticides as the third most se- grower organizations. Forty-seven speakers gave a rious threat to global agriculture behind soil erosion total of 55 presentations. (After the symposium the and water pollution. Crop losses due to pesticide re- talks were posted on the CAST website,
4 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 5
among insects, weeds, and pathogens by respec- lighted practical measures to limit selection pres- tive experts in the field. sure. In addition, the role of education and com- 2. Issues in Pest Resistance Management. In munication in long-term pest resistance manage- the second session, speakers addressed pest ment was discussed. resistance issues for major North American crops, 8. Symposium Recommendations for Pest Re- looking at what has been and is being done to sistance Management—Where to Now? The protect against resistance and assessing barriers final session was a moderated discussion on the to pest resistance management. The discussion important messages from the symposium. included fruits and vegetables, cotton, potato, small grains, corn/soybean, turf/ornamental The last section of these proceedings is a compila- crops, and organic agriculture. tion of conclusions and recommendations. The conclu- 3. Lessons Learned I: Balance between Indus- sions are those that were reached during the presen- try, Academia, Users, and Regulators. This tations and discussions throughout the symposium. session used case studies to examine how the pest/ The recommendations emerged from Session 8 and pesticide resistance concerns raised in the previ- focus on four topics: science, research and extension, ous two sessions actually have been addressed in education, and policy. the field. Case studies included glyphosate and ac- etolactate synthase (ALS) herbicide resistance, fungicide resistance in fruit and vegetable crops, Literature Cited insecticide resistance in pests of cotton and cruci- fers, and insect resistance management in Bt Hart, K. and D. Pimentel. 2002. Environmental and crops. economic costs of pesticide use. Pp. 237–239. In D. 4. Lessons Learned II: Have Models Helped? Pimentel (ed.). Encyclopedia of Pest Management. Speakers addressed the predictive and descriptive Marcel Dekker, New York. roles modeling plays in resistance management. Michigan State University–Center for Integrated The following issues were discussed: how models Plant Systems (MSU–CIPS). 2000. Database of ar- have been used to identify data gaps/needs, the thropods resistant to pesticides,
1.1 Scope of North American Pest Resistance Problems in 2003: An Overview Mark E. Whalon and Robert Hollingworth
Introduction Environmentalism and consumerism together have several pest management and resistance manage- In 2001 the world's pesticide market exceeded $34 ment impacts. First, North American societies source billion, while in the United States it exceeded $11 bil- products globally and transport these goods rapidly lion. It has been estimated by Hart and Pimentel into the country. Second, more than 60% of North (2002) that pesticide resistance surpasses $1.4 billion American pests historically have been introduced, in environmental, ecological, and human impact costs. with new introductions occurring almost weekly. At What are some of the features driving resistance de- this rate, will North American societies eventually velopment in North American societies? Consumer- import most of the ecologically compatible global pest ism certainly drives much of the globalization and species despite our phytosanitary barriers? Emerg- free-market decisions in North America today. Bilat- ing with consumerism on a global scale, market ac- eral trade agreements and falling tariffs have opened cess through nontariff phytosanitation barriers has the way to new markets and products. Both pesticide become a gauntlet that every entrepreneur must run. regulations and the enactment of the Food Quality Both the introduction of invasive species and phy- Protection Act (FQPA 1996) are seen by some as emer- tosanitation requirements dictate additional pesticide gent properties of consumerism (Kramer 1990) and applications and potentially accelerate resistance se- the environmental movement (Stroshane 1999). Con- lection. sumers demand inexpensive blemish-free fruits and Within this context is resistance, in which the ge- vegetables. Federal and state regulations require netic-based adaptation of pests to man's effort to con- wholesome and labeled products as well as numerous trol them has become more and more important as glo- other quality-related characteristics. Thus, consum- balism, consumerism, and market access concerns erism in its myriad forms swiftly has overtaken out- drive pesticide use. From this point of view, it is not dated forms of production, marketing, and sales of ag- difficult to believe that resistance problems will ricultural products. Consumers have power in the plague agriculture and human and animal health pro- marketplace today, and their power is partially trans- tection for the foreseeable future. lated into increased pressure toward “perfect” prod- As authors, we represent applied ecology and in- uct quality that only can be delivered through increas- sect toxicology. In our view, it is difficult to look past ingly intense pest management systems. the inference that resistance is a symptom of a dys- functional ecosystem. That is, agricultural produc- tion systems often are defined as disrupted ecosys- Environmentalism and tems (Southwood 1973). Resistance can be viewed Consumerism logically as a symptom or indicator of an ecosystem that has been disrupted beyond its natural equilibri- The environmental movement also has fostered um, resulting in an ecologically negative outcome. new awareness and a drive toward new legislation Therefore, resistance is a consequence of pesticide and regulations targeting pesticides in agriculture overuse in a utilitarian and reductionist sense. and health protection. Environmental concern also This perspective also could be adopted in human has been linked to the consumer movement (Burger and animal health protection where the problem with 1990) in Western societies, and together they are glo- antimicrobial resistance has surfaced repeatedly in bal in scope (Gilley 2001), extending even into Third the popular media. It is somewhat ironic that media World countries. Environmentalism transects the de- would focus on antibiotic resistance and human mographics of Western societies and strongly affects health while resistance issues with insecticides, her- the regulatory policies in the United States, Canada, bicides, and fungicides in food production rarely sur- and Mexico. face. Insecticide, acaracide, and filaricide resistance
6 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 7 also is a critical issue for human health protection in maintenance of a permanent repository of clearly doc- North America, but the media surprisingly overlooks umented cases of resistance” (Dover and Croft 1986). it, too, and ignores efforts by the U.S. Centers for Dis- To our knowledge, however, no divisional program ease Control and the World Health Organization to within the U.S. Environmental Protection Agency track various disease-vector resistance development (EPA) has ever followed up on this part of the FQPA in the Americas, Asia, and Africa. With the recent law other than voluntary reporting of resistance de- media attention in North America on the introduction velopment by registrants. of the mosquito-vectored West Nile virus into subur- Presumably one measure of the impact of recent ban and urban population centers, one might expect regulations on the availability of resistance manage- a somewhat broader articulation of the fragile nature ment tools is the number of different formulations, of human health protection against arthropod-borne pesticide and biopesticide modes of action, effective diseases, including vector resistance. A further iro- natural enemies, and other management strategies, ny, some might note, is that North American media tactics, and tools. Approximately 6,000 pesticides in concert with environmental and consumer move- have been cancelled or their uses reduced significantly ments would skewer certain insecticide use such as since passage of the FQPA (see Figure 1.2.2). On the organophosphates in food production yet approve—or other hand, the FQPA and related activities of the even champion—the direct exposure of large numbers EPA have accelerated the registration of reduced-risk of people during mosquito vector control operations. pesticides and organophosphate alternatives. Unfor- Apparently it is not appropriate to expose people to tunately, however, this legislation also has practically minuscule residues in the diet, but inhalation and eliminated the experimental use permit process contact exposure for human health protection are less whereby land-grant universities, private technical newsworthy. service providers, and commodity researchers histor- ically have adapted new pesticide tools to various pro- duction systems. In addition, the FQPA has provid- Regulations ed an array of new risk-science developments estimating the aggregate exposure to pesticides that When addressing the scope of North American re- exhibit common modes of action, the cumulative hu- sistance development, new regulations dealing with man pesticide exposure over a lifetime, and the im- resistance are of critical interest. For example, with pact of endocrine disruption on nontarget organisms. the promulgation of regulations governing the regis- Potentially all of these risk-science innovations could tration of genetically modified plants containing in- have unique or integrated impacts on resistance and secticidal proteins, resistance management plans resistance management in North America as the EPA were required as a prominent portion of the registra- evolves these policies. tion portfolio (USEPA 2002). With one exception, all As previously mentioned, resistance is a genetic- of the current conditional registrations for genetical- based decrease in the susceptibility of a population ly modified plants containing insecticidal proteins to a control measure. It has been observed across her- have a resistance management plan based on high bicides, fungicides, and bactericides, as well as insec- dose and refugia strategies (the single exception is ticides and miticides. An array of evolving pest bio- Mon 863 for corn rootworm control) (USEPA 2003). types or races also has overcome conventionally The European Union (EU) also has recently taken selected crop varieties showing host-plant resistance. some strides to require resistance management guide- Perhaps even cultural control strategies such as crop lines in its regulatory system. The EU-EPPO-PP1/ rotation may be overcome by genetic adaptation in a 213(1) guidelines require resistance risk assessment, pest (Levine and Oloumi-Sadeghi 1991; Levine, development, and implementation of a resistance Oloumi-Sadeghi, and Ellis 1992). The economic, so- management plan and baseline monitoring of resis- cial, and environmental consequences for the various tance for all new registrations within the EU (EPPO types of resistance include pest control failures, dis- 2003). The 1996 FQPA also has a provision for resis- rupted pest management systems (including limita- tance monitoring contained in its details. Essential- tions in the development of integrated pest manage- ly, this prescription for resistance monitoring is word- ment options), and increased pest control costs. Such ed much like a series of recommendations by the U.S. costs have been classified variously as (1) pest man- Board on Agriculture of the National Research Coun- agers forced to resort to newer, higher-priced pesti- cil, one of which states that, “Federal agencies should cide alternatives and (2) additional applications. support and participate in the establishment and Certainly there are arrays of environmental, social, 8 1.1 Scope of North American Pest Resistance Problems in 2003: An Overview and disrupted ecosystem consequences of the in- Literature Cited creased pesticide use induced by resistance. Function- ally, disrupted ecosystems and environmental im- pacts could be measured in increased off-target effects Burger, E. J., Jr. 1990. Health as a surrogate for the on biodiversity and/or endangered species. Additional environment. Dædalus 119:133–153. social impacts may include consequences on humans Dover, M. J. and B. A. Croft. 1986. Integration of pol- from increased pesticide residues, worker exposure, icy for resistance management. Pp. 422–435. In or increased disease spread where vector control is Pesticide Resistance Strategies and Tactics for diminished as a result of resistance. Management. National Research Council, National Academy Press, Washington, D.C. European and Mediterranean Plant Protection Orga- Summary nization (EPPO). 2003. EPPO standards,
1.2 Arthropods Reported to Be Resistant to Pesticides Mark E. Whalon, Patrick S. Bills, David Mota-Sanchez, Robert Hollingworth, Gary D. Thompson, and David Ehnis
Since the first report of a “resistant” insect (Me- lander 1914) there have been 543 arthropod species reported to be resistant to one or more pesticides. Our work on a resistance database at Michigan State Uni- versity (MSU) updates that of Georghiou and La- gunes-Tejeda (1991). The resistant arthropod count is based on an examination of over 3,863 peer-re- viewed journal articles. This information currently resides in an electronic database at the MSU Depart- ment of Entomology and is available via the Internet at
9 10 1.2 Arthropods Reported to Be Resistant to Pesticides
strain defined by the statistic used (e.g., LD50, LC50, KD50, or TL50) to a known susceptible strain, of 10 or more has been a general threshold for defining a re- sistance “case.” Occasionally, reports with an RR less than tenfold are included when the authors clearly demonstrated that resistance was high enough to cause field failure. Laboratory cases of resistance that clearly demon- strate the potential for resistance development to com- pounds that have not been observed to fail in the field also are reported in the MSU database as a harbin- ger. Therefore, the factors involved in deciding to accept a resistance report relied on the Whalon and McGaughey definition of resistance (1998): intrinsic Figure 1.2.2 Timeline of arthropod resistance and pesticide and extrinsic factors of the test itself (Busvine 1968) registrations in the United States. and the statistical significance of the bioassay used to report the resistance level. and their resultant fitness in biointensive IPM pro- The MSU database makes every effort to include grams (Croft 1990; Theiling and Croft 1988). all scientifically validated reported cases of resistance, Georghiou and Legunes-Tejeda, supported by the but we are hesitant to say that we have uncovered all United Nations Food and Agriculture Organization cases in our review given the scope of this worldwide (UN FAO), published a compendium of resistance phenomenon. For instance, our review focused pri- cases in 1991. marily on journals published in English. A number The U.S. Board on Agriculture of the National Re- of Russian, Spanish, French, and Italian journals, search Council made a series of recommendations, one however, also have been included. Still, there are of which states that “Federal agencies should support undoubtedly other documented cases of resistance and participate in the establishment and mainte- that should be included. To facilitate this process we nance of a permanent repository of clearly document- have developed a web-based resistance survey ed cases of resistance” (Dover and Croft 1986). This tool:
Table 1.2.1. Summary of documented cases of arthropods resistant to pesticides
Compound mode # of Category of resistant arthropods Total cases by of action/ compounds chemical class Agricultural, Medical, Predators / Other / Pollinators Chemical class with forest, and veterinary, Parasites miscella- resistance ornamental and urban neous plant pests pests arthropods Organophosphates 112 715 358 52 10 1135 44.1% Organochlorines 26 484 329 10 15 2 840 32.6% Pyrethroids 33 133 74 11 1 219 8.5% Carbamates 35 132 57 14 1 204 7.9% Bacterials 38 42 4 46 1.8% Miscellaneous 30 37 8 1 46 1.8% Fumigants 6 21 21 0.8% Insect Growth 10 16 2 3 2 0.8% Regulators Organotins 3 8 8 0.3% Formamidines 2 4 2 6 0.2% Arsenicals 2 2 11 13 0.5% Avermectins 2 2 3 1 6 0.2% Chloronicotinoids 1 2 1 3 0.1% Rotenone 1 2 2 0.1% Dinitrofenols 1 1 1 0.0% Sulfur compounds 2 1 1 2 0.1% Phenylpyrazoles 1 1 1 0.04% Total cases by 1602 850 90 30 2 2574 arthropod category 62.2% 33.0% 3.5% 1.2% 0.1%
Pesticide Resistance Strategies and Tactics for secticides with Novel Modes of Action: Mechanism Management. National Research Council, Nation- and Application. Springer-Verlag, New York. al Academy Press, Washington, D.C. Whalon, M. E., R. M. Hollingworth, and E. A. Gould. Georghiou, G. P. and A. Lagunes-Tejeda. 1991. The 2002. Resistant Pest Management Newsletter, occurrence of resistance to pesticides in arthropods:
1.3 Scope and Magnitude of Herbicide-Resistant Weeds in North America Ian M. Heap
Introduction phate synthase (EPSPS), and triazine-resistant weeds. Overexpression of the target enzyme also can In the developed world, and increasingly world- result in resistance. wide, herbicides are the primary method of weed con- In addition to altered target sites weeds may evolve trol, and their effectiveness is largely responsible for resistance due to the exclusion of herbicides from the the current abundance of food globally (Avery 1995). site of action (reduced absorption, reduced transloca- Herbicides have become the primary method of weed tion, or sequestration) or by rapid detoxification of control because of their efficacy and cost effectiveness; herbicides. It is this final mechanism, rapid detoxifi- however, heavy reliance on herbicides has resulted in cation conferred by elevated cytochrome P450 mo- the widespread occurrence of herbicide-resistant nooxygenase activity, that often results in resistance weeds. Herbicide resistance continues to increase to a wide array of chemical modes of action and in- globally, causing significant yield losses and increas- deed is one of the mechanisms found in Lolium rigi- ing the cost of food production. The first herbicide- dum Gaudin. (Christopher et al. 1991; Cotterman and resistant weeds occurred in the United States. This Sarri 1992). paper will outline some of the current and future prob- To add to the complexity of resistance there are lems of herbicide-resistant weeds in the United many instances where more than one resistance States. mechanism is found in a population (multiple resis- tance), and often within the same individual. The most complex examples are those of multiple-resis- Herbicide Resistance tant Lolium rigidum (Hall, Tardif, and Powles 1994; Heap and Knight 1982, 1986; Holtum and Powles In presenting the introductory herbicide resistance 1991) from Australia, and Alopecurus myosuroides paper to this CAST symposium I will give a brief def- Huds. (Hall, Tardif, and Powles, 1994; Moss and Cus- inition of resistance and its causes in weeds. sans 1991; Sharples and Cobb 1996) from Europe, “Herbicide resistance” is the evolved capacity of a where rapid detoxification and a number of target site previously herbicide-susceptible weed population to resistances often occur in the same population, mak- withstand a herbicide and complete its life cycle when ing research into the mechanisms of resistance diffi- the herbicide is used at its normal rate in an agricul- cult and advice to the farmers about effective alter- tural situation (Heap and LeBaron 2001). natives even more difficult (Willis et al. 1997). “Evolved capacity” in this definition implies that resistance is caused by a heritable change (mutation) in the genetic makeup of the weed that confers the Occurrence of Resistance ability to withstand a herbicide. Most herbicides act by inhibiting a specific enzyme (different for differ- A few reports of weeds exhibiting reduced (less ent herbicide modes of action) within the plant (De- than fivefold) levels of control with 2,4-D in the 1950s vine, Duke, and Fedtke 1993). The majority of herbi- did not receive much attention by farmers or scien- cide resistance cases are due to the selection of rare tists. The discovery of simazine-resistant Senecio individuals with genes that code for a modification of vulgaris L. populations in a Washington state nurs- the target enzyme such that the herbicide no longer ery in the late 1960s (Ryan 1970) is commonly cited binds to or inhibits the enzyme. Classic examples of as the first case of herbicide resistance. This case this are commonly found in acetyl-CoA carboxylase received a great deal of attention because it had ma- (ACCase) inhibitor, acetolactate synthase (ALS) inhib- jor implications for triazine-dependent maize produc- itor, dinitroaniline, 5-enolpyruvylshikimate-3-phos- ers in the United States and Europe, and indeed more than 30 triazine-resistant weed species were identi-
12 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 13 fied in maize by the end of the 1970s. Triazine-resis- particularly troublesome herbicide-resistant weeds in tant weeds were extensively researched but did not the United States and account for 7 of the 59 resis- inflict as much economic damage to producers as first tant species and a significant percentage of the area feared because alternative herbicide modes of action infested with resistant weeds. There also are numer- had arrived to market in time to avoid serious weed ous instances where Amaranthus spp. have evolved control problems. resistance to more than one herbicide mode of action, which complicates control strategies. The rate of identification of new herbicide resis- The United States Versus the World tance cases is surprisingly constant for both the glo- In April 2003 the International Survey of Herbi- cide-Resistant Weeds recorded 275 herbicide-resis- tant weed biotypes in 59 countries (Heap 2002). The United States has the highest number of herbicide- resistant weeds, having documented 100 resistant weed biotypes in 59 species (Tables 1.3.1 and 1.3.2). A new resistant biotype refers to the first instance of a weed species evolving resistance to one or more herbicides in a herbicide group. Amaranthus spp. are
Table 1.3.1. Number of herbicide-resistant biotypes reported by country for the top ten countries
Country Resistant biotypes Figure 1.3.1. Chronological increase in the number of herbicide- United States 100 resistant weeds in the United States and worldwide. Canada 39 Australia 38 France 30 bal and the U.S. data. Worldwide there have been ap- Spain 26 proximately nine new cases of resistance per year United Kingdom 24 since 1980, and in the same time period the United Israel 19 Belgium 18 States has added about four new cases each year (Fig- Germany 18 ure 1.3.1). Japan 16 The ALS and ACCase inhibitors account for the largest increases in new resistance cases worldwide and in the United States (Figures 1.3.2 and 1.3.3). Table 1.3.2. Herbicide resistance summary table for the United Statesa
Herbicide group HRAC/WSSA classification Example herbicide Total
ALS inhibitors B/2 Chlorsulfuron 35 Photosystem II inhibitors C1/5 Atrazine 18 ACCase inhibitors A/1 Diclofop-methyl 15 Synthetic auxins O/4 2,4-D 7 Dinitroanilines and others K1/3 Trifluralin 6 Thiocarbamates and others N/8 Triallate 5 Ureas and amides C2/7 Chlorotoluron 4 Bipyridiliums D/22 Paraquat 3 Glycines G/9 Glyphosate 2 Nitriles and others C3/6 Bromoxynil 1 PPO inhibitors E/14 Oxyfluorfen 1 Carotenoid biosynthesis inhibitors F1/12 Flurtamone 1 Organoarsenicals Z/17 MSMA 1 Pyrazoliums Z/8 Difenzoquat 1 Total number of unique herbicide-resistant biotypes 100 a HRAC = Herbicide Resistance Action Committee; WSSA = Weed Science Society of America; PPO = protoporphyrinogen oxidase; MSMA = monosodium salt of methanearsonic acid. 14 1.3 Scope and Magnitude of Herbicide-Resistant Weeds in North America
tus in part because it is broad spectrum, translocat- ed, is used postemergence, has low soil residual, has low nontarget toxicity, and has low environmental im- pact. It became available as a selective herbicide in Roundup Ready crops in 1996 and is widely used on a variety of those crops in the United States and many other countries. While there were early reports of artificial selec- tion of glyphosate-resistant plants, such as birdsfoot trefoil (Lotus corniculatus) (Boerboom et al. 1991) and perennial ryegrass (Lolium perenne), the first glypho- sate-resistant weed (L. rigidum) was selected in the field in 1996, 22 years after the first commercial use of glyphosate. Thus it is clear that glyphosate is a “low Figure 1.3.2. Chronological increase in the number of herbicide- risk for resistance” herbicide when used nonselective- resistant weeds worldwide to six herbicide classes. ly. The introduction of Roundup Ready crops has led to the potential use of glyphosate two or more times a year, each year, however, dramatically increasing the selection pressure for glyphosate-resistant weeds. The cases of glyphosate-resistant L. rigidum and cas- es of glyphosate resistance in three other species (L. multiflorum L., Eleusine indica (L.) Gaertn., and Co- nyza canadensis (L.) Cronq.) have major implications for the management of glyphosate-resistant crops glo- bally. Although it is clear that glyphosate is a low- risk herbicide for selection of resistant weeds, these cases have made it equally clear that glyphosate-re- sistant weeds will appear given sufficient selection pressure and time. Conyza canadensis is the first glyphosate-resistant weed to appear in Roundup Ready crops and has spread rapidly since its appear- Figure 1.3.3. Chronological increase in the number of herbicide- ance in Delaware in 2000. It now infests over 200,000 resistant weeds in the United States to six herbicide acres in six states and likely will be found in much of classes. the range of Roundup Ready soybean in the United States over the next few years, due to its rapid spread There are 79 ALS inhibitor-resistant weed species by airborne seed. Undoubtedly there will be several worldwide, and 35 of these occur in the United States. new cases of glyphosate-resistant weeds that appear The ALS-resistant weeds are found in all major crops in response to the increased use of glyphosate in and have become particularly troublesome in cereal Roundup Ready crops over the next 10 years. The real production in the Pacific Northwest and in corn/soy- challenge will be to limit their impact on the utility bean production in the Midwest. Of the 32 grass spe- of this valuable herbicide. cies resistant to ACCase inhibitors 15 can be found in the United States, primarily in cereal crops and the corn/soybean rotation (Heap 2002; Table 1.3.2). The Resistance Management graphs and data presented in this paper are summa- ries of the International Survey of Herbicide-Resis- Strategies tant Weeds (Heap 2002). In North America and Europe the primary resis- tance management strategy has been the use of her- Glyphosate Resistance bicide rotations, mixtures, or sequences that involve different herbicide modes of action. Common resis- Glyphosate was first commercially available in tance-management strategies currently used (to vary- 1974 and is the most successful and most important ing degrees) by farmers around the world include: herbicide in the world today. It has achieved this sta- Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 15
ignores this advice and promotes repeated use of the • Herbicide rotation. Rotating between herbicide same product year after year. modes of action from year to year is one of the In addition, there is a common (and so far relatively most widespread and probably most cost-effective accurate) perception by farmers that by the time they methods of resistance management. have a resistance problem, industry will provide a new • Herbicide mixtures or sequences. In this herbicide to effectively solve the problem, thus mak- strategy different herbicide modes of action are ing proactive and expensive resistance management used at full rates to control the same weed spe- strategies unnecessary. This is a dangerous assump- cies, thus making the probability of target site tion, as the economic consequences are severe if/when resistance extremely low, as the same individual industry is unable to provide the next solution in time. would require a mutation to both herbicide modes Glyphosate is the most important herbicide re- of action. Expense usually is the major deterrent source that farmers have left, and the introduction of to using mixtures or sequences, particularly with Roundup Ready crops provides them with a useful tool sequences, as they require additional applica- for controlling existing resistant weeds. Unless care- tions. Care must be taken to choose herbicides fully managed, however, Roundup Ready crops are that will not select for metabolism-based resis- not likely to be a long-term “silver bullet.” Widespread tance to both modes of action. appearance of glyphosate-resistant weeds will take • Cultural/Nonchemical control. Strategies considerably longer than it took for widespread resis- that include nonchemical control often are sug- tance to ALS- or ACCase-inhibitor herbicides, but gested in resistance management but rarely complete reliance on glyphosate for weed control both adopted unless they provide immediate econom- preplant and postemergence probably will spell the ic benefit to the farmer—usually this happens beginning of its demise within a decade. after the appearance of resistance. Most strate- gies are aimed at reducing seed production or the seed bank before cropping. They include crop ro- Acknowledgments tation, stubble burning, cultivation to stimulate weed germination, delayed sowing to maximize The author thanks the Herbicide Resistance Action pre-sowing weed kill, spray-topping, crop-topping, Committee, the North American Herbicide Resistance hay cutting, and capture of weed seed during har- Action Committee, and the Weed Science Society of vest (Mathews and Powles 1996). Establishment America for funding the International Survey of Her- of a highly competitive crop probably is the best bicide-Resistant Weeds, the primary source of data for example of a cultural control that provides imme- this paper. Many thanks also are due to all of the re- diate economic benefits. search and extension weed scientists who contribut- ed to the online survey. Adoption of Resistance Management Literature Cited Over the last 30 years scientists have studied the Avery, D. T. 1995. Saving the Planet with Pesticides mechanisms of herbicide resistance, cross-resistance and Plastic. Hudson Institute, Indianapolis, Indi- patterns, distribution of resistance, genetics, gene ana. flow, biology, and ecology of resistance. All of these Boerboom, C. M., N. J. Ehlke, D. L. Wyse, and D. A. studies are necessary for an understanding of herbi- Somers. 1991. Recurrent selection for glyphosate cide resistance and are useful in the development of tolerance in birdsfoot trefoil. Crop Sci 31:1124– resistance management strategies. Often the devised 1129. strategies are extended to farmers via fact sheets, Christopher, J. T., S. B. Powles, D. R. Liljegren, and workshops, and the popular press. Unfortunately, the J. A. M. Holtum. 1991. Cross-resistance to herbi- weak link in the chain is the adoption of resistance cides in annual ryegrass (Lolium rigidum). II. management strategies by farmers. While the re- Chlorsulfuron resistance involves a wheat-like search and development arm of industry has been detoxification system. Plant Physiol 95:1036–1043. proactive in supporting herbicide resistance research, Cotterman, J. C. and L. L. Sarri. 1992. Rapid meta- and the development of resistance management strat- bolic inactivation is the basis for cross-resistance egies, the sales and marketing arm of industry often 16 1.3 Scope and Magnitude of Herbicide-Resistant Weeds in North America
to chlorsulfuron in a diclofop-methyl-resistant rigid ryegrass (Lolium rigidum) biotype SR4/84. Pesti- cide Biochem Physiol 43:182–192. Devine, M. D., S. O. Duke, and C. Fedtke. 1993. Phys- iology of Herbicide Action. Prentice-Hall, Engle- wood Cliffs, New Jersey. Hall, L. M., F. J. Tardif, and S. B. Powles. 1994. Mech- anisms of cross and multiple herbicide resistance in Alopecurus myosuroides and Lolium rigidum. Phytoprotection 75:17–23. Heap, I. M. 2002. International Survey of Herbicide- Resistant Weeds, U.S.A. WeedSmart, Corvallis, Or- egon. Available online,
1.4 Pathogens Wolfram Koeller
Introduction though both are still in wide use and certified in or- ganic food production, the level of disease control Most of our economically important plant diseas- achieved with sulfur and the copper fungicides is low es are caused by fungal pathogens. They are eucary- for many of the important diseases to be managed. otic micoorganisms and reproduce exclusively or pre- More efficacious organic fungicides were introduced dominantly asexually. This clonal character of during the 1940s and 1960s, with the ethylenebis- reproduction, which has impact on the monitoring and dithiocarbamates (EBDCs), captan, and chlorotha- combat of fungicide resistance, differentiates fungal lonil as important examples. Their commonality is a plant pests from insects and weeds. Most fungicides nonspecific mode of action through the indiscriminate in the United States currently are used in the produc- chemical modification of numerous enzymes (Köller tion of grapes, tree and berry fruits, vegetables and 1999). In order to avoid phytotoxicity, these fungi- potatoes, and in the maintenance of turf with its high cides must be confined to the surfaces of plants, where recreational value in an urban environment. This list they inhibit the germination of attacking fungal of commodities does not include major field crops such spores. This inherently protective rather than cura- as wheat, corn, or soybean. All seeds used in the tive mode of physical action is of limited value in in- United States, however, are coated with fungicides to tegrated pest management (IPM) programs with their protect seedlings from soil- and seedborne diseases. “only when needed” paradigm of pesticide use. An Fungicide resistance rarely has become a problem in additional concern is the B2-carcinogen classification such seed dressing applications, because most soil of several of these older fungicides, a characteristic pathogens reproduce and disperse slowly and only remaining under the scrutiny of the Food Quality infect plants during the relatively brief seedling stage. Protection Act (FQPA). The advantage of convention- Resistance has become a problem in foliar appli- al protectants is that resistance never has become a cations of fungicides indispensable in the production limitation. This positive experience with resistance of numerous high-value crops. Here, losses caused by combined with low treatment costs is the major rea- fungal diseases have become increasingly costly. For son for the continued use of these conventional pro- example, apples grown on 200,000 acres are affected tectants. by apple scab, a disease routinely managed with four Curative postinfection control of plant diseases re- to eight fungicide applications per season. The mar- quires systemic uptake of fungicides and, therefore, ket potential of apples produced for the fresh market pathogen-specific modes of actions. Starting in the is $6,000–$8,000 per acre. A single blemish caused late 1960s with the introduction of the benzimida- by the apple scab fungus will lead to the downgrad- zoles, several classes of specific foliar fungicides have ing of apples to 10% of their fresh market value. Com- been introduced and widely used: the dicarboximides mercially acceptable apple cultivars and biological in the 1970s, the phenylamides and sterol demethy- control agents are not available, leaving fungicides as lation inhibitors (DMIs) in the 1980s, and the new the only option in the management of the disease. class of broad-spectrum strobilurins in the 1990s. The Numerous high-value crops cultivated in the United various classes of pathogen-specific fungicides allowed States mirror the apple scab example. growers to manage diseases with postinfection appli- cations and at prolonged spray intervals. The inher- ent disadvantage of these specific fungicides was that Fungicides and Fungicide resistance has developed more or less rapidly to all Resistance classes (Brent 1995; Köller 2001). The first case of practical fungicide resistance in The first disease-control agents introduced over a the United States was reported in 1960 for the aro- century ago were sulfur and the copper fungicides. Al- matic hydrocarbons used in the postharvest control
17 18 1.4 Pathogens of citrus rot caused by Penicillium. The first case of Strategies for the delay of resistance development resistance to a foliar fungicide was reported in 1968 have included rotation among different classes of fun- for dodine used in the postinfection control of apple gicides. This rotation strategy was enforced for the scab (Brent 1995). Since then, all major fungal patho- new class of strobilurins by restricting the number of gens managed with pathogen-specific fungicides have applications allowed per season. While the rotation developed resistance to at least one of the pathogen- among chemical classes will undoubtedly delay the specific fungicides. The current concern is that sev- speed of resistance development when measured in eral pathogens have developed multiple resistance. numbers of useful seasons, the inherent problems to For example, the apple scab fungus has responded such rotation programs are the restricted availabili- consecutively with resistance to dodine, benzimida- ty of rotation partners. In many cases, alternatives zoles, and the DMIs, and clear indications of resis- have been and will be the conventional protectants tance to the new class of strobilurin fungicides exist. with their inherent limitations, because previous Several powdery mildews have become resistant to rounds of resistance already have affected the postin- the benzimidazoles, the DMIs, and more recently, the fection alternatives. strobilurins. Indications are that repeated develop- Another delaying tactic is the use of fungicides at ment of resistance might even accelerate the speed of high doses (Köller and Wilcox 1999). High doses will future rounds of resistance (Köller and Wilcox 2001). be effective only in cases of multiple-gene resistance, however, where resistant phenotypes continue to re- spond to the inhibitors. This type of resistance has Antiresistance Strategies been identified for the DMIs (Brent 1995; Köller 2001; Köller and Wilcox 2001). For many other fungicides, The sharp rise of fungicide resistance in the 1980s resistance is caused by target site mutations render- required the development and implementation of ing mutants to respond immune to any feasible dose antiresistance strategies. Goals of such strategies are of the inhibitor (Brent 1995; Köller 2001). In these to delay the speed of resistance development and to cases, high doses will not slow the selection of resis- manage resistance once first cases of practical resis- tant phenotypes. tance have emerged. These two goals are not exclu- In summary, fungicide resistance has curtailed the sive. Initial occurrences of resistance most often are sustained usefulness of most of our modern postinfec- restricted to particular regions, and management of tion fungicides. Antiresistance strategies employed resistance in these regions can and should be com- have been mixtures of these fungicides with a conven- bined with delaying tactics in other regions. The first tional protectant or the rotation among chemical antiresistance strategy introduced in the late 1970s classes of fungicides. Limitations imposed on these for the benzimidazoles was to mix a fungicide under strategies are that conventional protectants in mix- risk with a conventional protectant. Initially this ture do not delay resistance development when used strategy was implemented through recommendations. in postinfection applications and the limited choices Later, implementation was enforced by the market- of postinfection fungicides not yet affected by previ- ing of prepacked mixtures in the control of high-risk ous rounds of resistance. A second matter of concern diseases. The advantage of this mixture strategy was relates to the fact that growers cannot expect nor pre- that resistant subpopulations of pathogens were man- dict substantial crop losses caused by resistance. Such aged by the protective partner. Respective mixtures, crop losses are experienced first during the initial however, did not delay the selection of resistant sub- emergence of practical resistance and by growers, who populations when they were used in postinfection continue to rely on certain fungicides without the applications typical for the systemic partner (Köller addition of other management practices. This status and Wilcox 1999). Consequently, contributions to the quo determines the future challenges. overall level of disease control achieved by the system- ic mixture components declined over time. At a giv- en threshold level of resistance frequencies, manage- Challenges ment of diseases entirely depended on the conventional protectant (Köller and Wilcox 1999). The delay of resistance development to a new fun- Although mixtures of two fungicides with postinfec- gicide is most effective, if strategies are implement- tion activities might delay the development of resis- ed from the start of their commercial use. Appropri- tance (Köller and Wilcox 2000), they have been stud- ate antiresistance strategies will vary for different ied or used rarely. fungicides and different pathogens. For example, a Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 19 high-dose strategy will be effective only in cases of Brent, K. J. and D. W. Hollomon. 1998. Fungicide multigenic resistance but ineffective in cases of Resistance: The Assessment of Risk. Fungicide Re- target site mutations rendering immunity (Köller sistance Action Committee Monograph 2. Global 2001; Köller and Wilcox 1999). The nature of expect- Crop Protection Federation, Brussels, Belgium. ed resistance can be examined in proactive risk as- Köller, W. 1999. Chemical approaches to managing sessment studies. Such risk assessments have been plant pathogens. Pp. 337–376. In J. R. Ruberson implemented in a European Union Registration Di- (ed.). Handbook of Pest Management. Marcel De- rective, but reliable tools for risk assessments and kker, New York. their interpretation remain coarse and unreliable. Köller, W. 2001. Fungicide resistance. Pp. 483–488. For example, most risk assessments had predicted a In O. C. Maloy and T. D. Murray (eds.). The Ency- moderate risk for the new class of strobilurin fungi- clopedia of Plant Pathology. John Wiley, New cides (Brent and Holloman 1998). Instead, resistance York. developed rapidly for many diseases in spite of limi- Köller, W. and W. F. Wilcox. 1999. Evaluation of tac- tation in the number of applications allowed per sea- tics for managing resistance of Venturia inaequal- son (Bartlett et al. 2002). In view of current uncer- is to sterol demethylation inhibitors. Plant Dis tainties, the implementation of antiresistance 83:857–863. strategies derived from risk assessments must be ac- Köller, W. and W. F. Wilcox. 2000. Interactive effects companied by the continuous monitoring of pathogen of dodine and the DMI fungicide fenarimol in the responses to pathogen-specific fungicides. Only reli- control of apple scab. Plant Dis 84:863–870. able monitoring procedures already in place will al- Köller, W. and W. F. Wilcox. 2001. Evidence for the low for adjustments of antiresistance strategies be- predisposition of fungicide-resistant isolates of Ven- fore threshold levels of practical resistance are turia inaequalis to a preferential selection for re- reached. At present, monitoring programs are prima- sistance to other fungicides. Phytopathology rily aimed at the confirmation of resistance once it has 91:776–781. reached a level of commercial ineffectiveness. At that stage, implementation of antiresistance strategies will be too late in many cases. Both the improvement of methodologies employed in resistance risk assessments and the monitoring of pathogen responses to pathogen-specific fungicides require substantial commitment to the task. The fi- nancial resources presently committed by both the private and the public sectors are very small in com- parison with the economical importance of plant dis- eases controlled with modern low-risk fungicides. But even if the level of financial resources were increased, it will hardly be possible to assess the relative risks and to monitor population responses for all diseases managed with modern postinfection fungicides. Re- sults obtained for key pathogens with model charac- ter will have to be transferred to the majority of dis- eases affected by fungicide resistance.
Literature Cited
Bartlett, D. W., J. M. Clough, J. R. Godwin, A. A. Hall, M. Hamer, and B. Parr-Dobranzki. 2002. The stro- bilurin fungicides. Pest Manag Sci 58:649–662. Brent, K. J. 1995. Fungicide Resistance in Crop Pathogens: How Can It Be Managed? Fungicide Resistance Action Committee Monograph 1. Glo- bal Crop Protection Federation, Brussels, Belgium. 20
2.1 Resistance Issues in Fruit and Vegetable Production Systems Charles Mellinger
Every season brings new adventures in managing nosad (SpinTor, Conserve). Key pests vulnerable to resistance wherever fruits and vegetables are grown resistance or already showing signs of slipping effi- on large-scale, intensive farm operations. Resistance cacy include diamondback moth in a number of geo- has triggered far more profound changes in our South graphical regions and certain thrips species in the Florida integrated pest management (IPM) systems Southeast. and pesticide use patterns than regulation. Plus, re- Spinosad is a remarkably versatile product that sistance often beats the Environmental Protection meets a number of pressing needs for a softer midsea- Agency (EPA) to the punch. Resistance-triggered son insecticide. Its range of uses, coupled with its spe- change in pesticide use is one reason our grower-cli- cific mode of action, makes spinosad vulnerable to re- ents have for the most part not been impacted ad- sistance. Farmers and IPM practitioners must resist versely by implementation of the Food Quality Pro- the temptation to rely too heavily on this excellent tection Act (FQPA), at least not yet. new tool if they are to preserve its efficacy. Looking ahead though, we see tough new challeng- A significant level of adult pest movement from one es. The phaseout of methyl bromide is bound to bring crop to the next is being reported, where spinosad about big changes in pest management systems in to- might be used several times in the same period for a matoes and peppers. Some growers are making the range of pests. (Adult pest movement also is a big con- transition in an orderly, incremental manner, where- cern in managing whitefly and aphid resistance to nic- as other growers are betting that methyl bromide will otinoids.) Complicated patterns of spatial and tem- get a reprieve and the day of reckoning will be delayed poral selection pressure pose equally complicated several years. If this latter group is wrong and the resistance management challenges. phaseout proceeds on the current schedule, some The third priority is managing the development for farmers will be scrambling and a few may find them- resistance to avermectin (Agrimek) in dipterous leaf- selves excessively reliant on certain pesticides, mak- miners and various mites. Mite control is a tough ing resistance management more difficult. Newly challenge, in large part because of the propensity of arrived invasive species also can trigger major chang- mites to develop resistance to new acaricides quick- es in pesticide use patterns and dramatically change ly. We continue to focus much effort on managing resistance management dynamics. resistance to avermectin in citrus rust mites and two My task is to summarize pressing fruit and vege- spotted spider mites on various crops. Other recent- table resistance management issues. There is fairly ly registered miticides pose important resistance man- widespread agreement on the most pressing challeng- agement challenges, as well. The application rate of es in weed, insect, and plant disease control. avermectin for leafminer control has increased two- fold during the past decade, a clear sign we are los- ing ground. Insect Management The fourth priority is keeping old organophosphate (OP), carbamate, and synthetic pyrethroid chemistry The first priority is preserving the efficacy of the effective. We will have a very difficult time manag- nicotinoids including imidacloprid (Admire, Provado), ing resistance to reduced-risk chemistries, insect thiamethoxam (Actara, Platinum), acetamiprid (As- growth regulators (IGRs), and the nicotinoids with- sail), and thiacloprid (Calypso). Key target pests like- out the ability to apply a relatively hot, broad-spec- ly to develop resistance, or already showing signs of trum material from time to time. Not having metha- slipping efficacy in some regions include Colorado midophos (Monitor) for control of western flower potato beetles and whiteflies. Other pests belong on thrips as a rotation partner for spinosad (SpinTor) is this list in certain regions. an important example. But virtually all of these prod- The second priority is preserving the efficacy of spi- ucts already are compromised to some degree by re-
20 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 21 sistance, and all are highly vulnerable if even a few Avoiding Use of No-Longer farmers choose to build their control programs on Effective Products them. Managing resistance to OPs and carbamates is Because of resistance, some fungicides just do not made more difficult—and important—by limits im- work anymore. For a variety of reasons, though, they posed on their use by the FQPA. As fewer of these are still used, costing farmers money and possibly materials are available, the remaining products like- making matters worse. Somehow the pest manage- ly are to be used more intensively, possibly leading ment community needs to find a more effective way to a proliferation of resistance insects and in some to stop the use of legal products in places where re- cases, control failures. For example, methomyl and sistant phenotypes have taken over target-pathogen oxamyl are excellent rescue pesticides for control of populations. The steps necessary to monitor suscep- Thrips palmi in peppers. If either one should become tibility are known, but the resources are not routine- unavailable, the use of the remaining active ingredi- ly accessible to get the job done. I hope this sympo- ent will certainly increase, even if only by a few ap- sium will trigger some new thinking regarding how plications per growing season. to overcome this practical reality. On the soilborne insect and nematode front, we face In some parts of the country, processors and buy- some emerging resistance management challenges. ers also need to rethink the mandatory fungicide If, and as, methyl bromide is phased out, many grow- treatment requirements they impose on grower-con- ers will increase their use of Telone and other fumi- tractors. These companies have an obligation to their gants and soil insecticides. We need to be vigilant in growers, and the communities in which they work, to monitoring resistance in pest complexes, which could assure that any mandatory fungicide or fumigant lead to dramatic shifts in species composition and root applications are worth the expense and that risks are feeding damage. Glades Crop Care is working hard manageable. to develop new scouting and sampling techniques to understand better the scope and distribution of nem- atode problems across a field. How to deal with re- Monitoring Chlorothalonil Susceptibility sistance management as control programs change will Chlorothalonil (Bravo) remains a very valuable, af- have to be figured out in real-time, which leaves lit- fordable product. It is heavily used in many fruit and tle room for experimentation or error. vegetable systems, and for the most part, resistance has not been a major concern. There is some evidence, I am told, (Holm et al. 2003) of modest levels of resis- Disease Management tance in certain potato pathogens in a few states. It seems unlikely that chlorothalonil efficacy will col- Managing Resistance to Strobilurin lapse suddenly, but we should not take this product Fungicides for granted. More systematic resistance-monitoring efforts should be put in place in a number of major For years we have struggled in South Florida to growing regions until we are certain that resistance keep up with blight diseases of tomato and potato and ratios are stable. bacterial spot in tomatoes and peppers. Over the years the EPA has placed progressively strict limits on the total pounds of ethylenebisdithiocarbamates Weed Management (EBDCs) that can be applied, forcing growers to in- troduce other fungicides into their programs. The Managing Resistance to Sulfonylurea strobilurins are very welcome new tools, yet are much and Other Acetolactate Synthase (ALS) more vulnerable to resistance than the EBDCs, cop- Inhibitor Herbicides pers, and chlorothalonil. Indeed, already we are fac- ing resistance to the strobilurins in the gummy stem A half-dozen major crops drive herbicide discovery blight pathogen in cucurbits. Fortunately, some oth- and registration priorities. The minor use crop prob- er new fungicides that employ novel modes of action lem is severe and persistent, although vegetable grow- are well along the registration pipeline and will pro- ers are pleased to have access to some new sulfony- vide some additional options. lurea herbicides. Sulfonylurea herbicides have a rich history in triggering resistance. A visit to
Holm, A. L., V. V. Rivera, G. A. Secor, and N. C. Gud- mestad. 2003. Temporal sensitivity of Alternaria solani to foliar fungicides. Am J Pot Res 80:33– 40. Stall, W. M., S. R. Kostewicz, and R. L. Brown. 1987. Reduction in control of common nightshade (Solanum americanum Mill.) by Paraquat due to copper fungicides. Proc Florida State Hort Soc 100:222–224. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 25
2.2 Resistance Issues in Cotton Pest Management Patricia F. O’Leary and Robert L. Nichols
Introduction Resistance Survey: Cotton Working Group 2003). Of these, the tobacco budworm (Heliothis virescens) and Cotton (Gossypium hirsutum) is a major agronom- the cotton bollworm (Helicoverpa zea) are the most ic crop, grown on 5–6 million hectares (12–15 million destructive, costing the cotton industry more than acres) in the southern half of the United States from $250 million in 2002 (Williams 2003). Pyrethroid re- Virginia to California. The value of the crop averag- sistance in the tobacco budworm was first detected in es approximately $6 billion per year. Pesticides are the mid-1980s (Platt, McWhorter, and Vance 1987). important tools used to protect the crop each year from Resistant populations now have become prevalent in a diverse complex of pests. It is not surprising that the eastern portion of the Cotton Belt, and pyrethroids pest resistance has become a problem with some of are no longer recommended for tobacco budworm the more frequently used products. management in several mid-Southern states. Resistance in Lygus spp. and cotton aphids (Aphis gossypii) does not appear to be stable. In these spe- Current Status cies, variation in susceptibility occurs from year to year, among locations, and depending on the pesticide, Insects within the season. As an example, L. hesperus popu- lations monitored for susceptibility to various Serious problems with insecticide resistance began insecticides in California’s San Joaquin Valley over to develop shortly after the chlorinated hydrocarbon several years were found to be resistant to organo- insecticides were adopted for general use on cotton phosphates and carbamates, but the level and fre- after World War II. At that time, resistant popula- quency of resistance fluctuated from year to year. In tions of two species were reported (King, Phillips, and contrast, pyrethroid resistance was quite high and Coleman 1996). Today, ten cotton insect pests have intensified over the study period (Grafton-Cardwell been identified by the Insecticide Resistance Action et al. 2000). Louisiana researchers have found that Committee (IRAC) as having populations resistant to susceptibility of populations of Lygus lineolaris to one or more classes of insecticides (Table 2.2.1; IRAC cypermethrin, acephate, and oxamyl decreases
Table 2.2.1. Cotton insect pests with populations resistant to one or more classes of insecticides (IRAC Resistance Survey: Cotton Working Group 2003)
Pesticide class Pests Pyrethroid Carbamate Organophosphate Organochlorine
Tobacco budworm X X X X Cotton bollworm X X X Beet armyworm X Fall armyworm X X X X Soybean looper X X X Boll weevil X Cotton aphid X X X X Silverleaf whitefly X X Lygus X X X Western flower thrips X X X X
25 26 2.2 Resistance Issues in Cotton Pest Management throughout the growing season (Halloway et al. 1998). Inhibition of acetolactate synthase (ALS) is a com- In the early 1990s resistance to pyrethroids and mon mode of action in herbicides. Registration of the pyrethroid–organophosphate combinations led to dev- ALS herbicide Staple® in 1994 was a major step for- astating outbreaks of the silverleaf whitefly (Bemisia ward, because Staple could be used as a true over-the- argentifolii) in cotton–vegetable systems in southern top herbicide in cotton. ALS resistance in populations California and Arizona. Substantial economic losses of cocklebur (Xanthium strumarium) and more re- were sustained by growers due to exorbitant costs of cently in Palmer amaranth (Amaranthus palmeri), insect control. In addition, whitefly feeding deposits however, has limited the utility of this otherwise very honeydew on exposed cotton lint, creating “sticky cot- valuable compound. In addition, many of the locations ton.” Not only was the cotton discounted over the affected by cocklebur resistant to ALS herbicides also entire region, but also, the reputation for stickiness have cocklebur resistant to the organoarsenical her- has had a negative impact on domestic sales and ex- bicides, MSMA and DSMA, the principal class of port orders of cotton from the Southwest (Ellsworth chemistries used for management of cocklebur es- et al. 1999). capes in cotton before the registration of Staple. In South Carolina, Palmer amaranth also is resistant to dinitroaniline herbicides. Weeds With the advent of transgenic, herbicide-resistant The Herbicide Resistance Action Committee technology, glyphosate (a glycine herbicide) has be- (HRAC) and the Weed Science Society of America come the dominant herbicide in U.S. cotton and soy- (WSSA) list five weed species that are common and beans (Carpenter and Gianessi 2001). A recent and troublesome in cotton and are resistant to one or more troubling development is the identification of resis- herbicide modes of action (Table 2.2.2; International tance to glyphosate in the United States (van Gessel Survey of Herbicide Resistant Weeds: USA 2003). As 2001). Although resistance to glycine herbicides has might be expected, most incidences of resistance have occurred previously in other weed species, positive been reported in the mid- and southeastern states identification of glycine resistance in horseweed (Co- where herbicide use is heaviest. Johnsongrass (Sor- nyza canadensis) is the first incidence that has affect- ghum halepense) is a major weed in agronomic crops ed row-crop agriculture directly (Feng, Pratley, and throughout the southern half of the United States. Bohn 1999; Lee and Ngim 2000). There is additional Johnsongrass was heavily treated with postemer- concern because of the extensive adoption of Round- gence graminicides following their introduction in the up-resistant varieties in cotton, soybean, and other early 1980s, and as a result, resistance to herbicides crops where glyphosate may be used two, three, or with inhibition of acetyl CoA carboxylase (ACCase) as more times per season and is sometimes the only her- their mode of action occurred in the mid-South in the bicide used. Such patterns of use represent strong 1990s. challenges to the maintenance of glyphosate suscep- tibility.
Table 2.2.2. Weeds in cotton with populations resistant to one or more herbicide modes of action (International Survey of Herbicide Resistance Weeds: USA 2003)
Mode of action Pests Organoarsenicals ALSa Glycines ACCaseb DNA
Cocklebur X X Horseweed X Johnsongrass X Goosegrass X Palmer amaranth X X a Acetolactate synthase. b Acetyl CoA carboxylase. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 27
Pathogens Management Plans and Guidelines
Fungicides are used chiefly in cotton as seed or hop- Resistance management plans and guidelines have per box treatments, or applied in furrow at planting been developed for several cotton insect species. for control of seedling diseases caused by Pythium spp. These guidelines have taken many different forms, and Rhizoctonia solani. There are no known instances depending on the pest, location, and pesticide class of pesticide resistance in the organisms that cause or mode of action involved. Basic guidelines for man- diseases in cotton. aging resistance, such as those found in Oklahoma State University’s “Cotton Aphid Resistance Manage- ment Guidelines” (Karner 1997) and the University Management Strategies of California’s “Herbicide Resistance—How to Delay or Prevent Problems” (Vargas and Wright 2001), are Strategies for managing pesticide resistance have based on integrated pest management (IPM) practic- been developed on a case-by-case basis. There are two es to minimize the chance of a widespread infestation components common to most situations, however: of the pest. monitoring and the development of management Other plans have been developed that are similar plans and guidelines. to those drafted for managing pyrethroid resistance in Heliothis armigera in Australia (Pyrethroid 1983). A “windows” approach is used to schedule insecticide Monitoring applications to decrease selection pressure and to pre- Monitoring programs for insect pests to certain in- serve a specific product for use against the most dam- secticide families has been conducted at both local and aging pest population. The most widely adopted plans regional levels. Entomologists in Louisiana have were developed to manage pyrethroid resistance in monitored cotton pest populations since 1986 for sus- the tobacco budworm in the mid-South (Luttrell and ceptibility to various insecticides. This program has Roush 1987) and to preserve susceptibility of two in- tracked the evolution of pyrethroid resistance in to- sect growth regulators and manage pyrethroid resis- bacco budworm, providing information to tailor man- tance in the silverleaf whitefly in Arizona and Cali- agement recommendations to match the current lev- fornia (Ellsworth, Dennehy, and Nichols 1996; el of resistance. Goodell and Godfrey 2002). The whitefly plan is still A recent example of a multistate resistance-moni- an important component of pest management recom- toring effort is a program sponsored by IRAC and Cot- mendations in the West, whereas the tobacco bud- ton Incorporated. Following reports of field failures worm plan is less used today due to the introduction in several southern states, a program was initiated and widespread adoption of Bacillus thuringiensis in 1998 to assess the extent of pyrethroid resistance (Bt) transgenic cotton and the loss of pyrethroid in- in cotton bollworm populations. The monitoring ef- secticides as effective management tools for tobacco fort involved 21 scientists in 12 states: Alabama, budworm in the mid-South. The plan has been mod- Arkansas, Florida, Georgia, Louisiana, Mississippi, ified, however, and is still in place in locations where Missouri, North Carolina, South Carolina, Tennessee, potential pyrethroid resistance in cotton bollworm Texas, and Virginia. and tarnished plant bug exists. Whereas insects generally produce multiple gen- erations per year in temperate regions, weeds gener- ally reproduce once annually, even when they germi- Current Concerns nate throughout the year. Thus, assaying resistance in weeds is a multiyear process. Through the present Sustainability of Transgenic Varieties time, weed resistance has almost always been discov- ered after the fact. Weed scientists are currently ex- The cotton industry has a major investment in ploring how best to assemble information for the pur- transgenic technology. In 2002, 71% of U.S. cotton pose of recommending programs to decrease the acreage was planted in varieties that either express potential for early development of resistance to her- introduced genes for herbicide resistance or insecti- bicide modes of action. cidal proteins, or both (USDA 2003). A resistance management plan is a requirement for use of the Bt cottons, but is not required with the herbicide-resis- tant varieties. 28 2.2 Resistance Issues in Cotton Pest Management
Pyrethroid Resistance in Cotton Bollworm will never be resistant to a specific chemical, or re- sistance is inevitable. In fact, development of resis- The cotton bollworm is still relatively susceptible tance is a risk to the sustained use of any pesticide. to the pyrethroid insecticides. In the last few years, however, there has been an increase in the number of reports of populations with increased tolerance to Economic Factors pyrethroids. In the multistate monitoring program The overriding influence on decisions made by described earlier, mean survival of cotton bollworm many growers and apparently by certain pesticide to a diagnostic dose of cypermethrin increased sixfold manufacturers is the short-term bottom line. Unless from 1998 to 2001 (Payne et al. 2002). there is a crisis, resistance management strategies have to show immediate economic benefits before they will be implemented. Short-term solutions are pop- Susceptibility of Boll Weevil to Malathion ular and easy to invest in because an immediate ben- After 25 years and over $1 billion in program costs, efit can be realized. Resistance management is often the Boll Weevil Eradication Program is nearing com- unpopular because the benefit is delayed. Further pletion. Entire states have been declared weevil-free, hindering resistance management, consultants and with total eradication nationwide expected by 2006. growers are relatively adverse to risk. “Insurance Malathion is essential to the success of the program. spraying” of pesticides is not uncommon to protect In 2002, approximately 4 million hectares (9 million investment in the crop. acres) of cotton were in the active phase of the pro- Development of resistance is a risk to the sustained gram, putting tremendous selection pressure on this use of any pesticide. That risk depends on the pest, insect from one insecticide. the pesticide, the pattern of use in the crop, and the pattern of use in the local cropping system. Our task is to develop means to manage such risks. Decreased Efficacy of Aldicarb Aldicarb is the most widely used chemistry avail- able for effective management of nematodes. Recently Literature Cited there have been reports of ineffective field applica- Carpenter, J. and L. Gianessi. 2001. Agricultural tions of this nematicide against the reniform nema- biotechnology: Updated benefits estimates. Nation- tode (Rotylenchulus reniformis) in Mississippi and al Center for Food and Agricultural Policy, Wash- Alabama. Accelerated degradation of the product is ington, D.C. 48 pp. suspected as the cause (McLean and Lawrence 2003). Ellsworth, P., T. Dennehy, and R. Nichols. 1996. Whitefly management in Arizona cotton 1996. Uni- versity of Arizona Cooperative Extension IPM Se- Barriers to Resistance ries Number 3. 6 pp. Management Ellsworth, P., R. Tronstad, J. Leser, P. Goodell, L. Godfrey, T. Henneberry, D. Hendrix, D. Brush- Barriers to the implementation of effective resis- wood, S. Naranjo, S. Castle, and R. Nichols. 1999. tance management programs are not unique to cot- Sticky cotton sources and solutions. University of ton. Two barriers reflect a lack of confidence in the Arizona Cooperative Extension IPM Series No. 13. availability of new products and concern about the 4 pp. economics of such programs. Feng, P., J. Pratley, and J. Bohn. 1999. Resistance to glyphosate in Lolium rigidum II. Uptake, trans- location, and metabolism. Weed Sci 47:412–415. Confidence in Availability of New Products Goodell, P. and L. Godfrey. 2002. Silverleaf whitefly The crop protection industry has been prolific in management strategies for San Joaquin Valley cot- providing tools for managing pests in cotton. Many ton. California Cotton Rev 64:4–6. growers, consultants, and agrochemical distributors Grafton-Cardwell, B., J. Christiansen, R. Striggo, G. still believe that there is an infinite stream of new pes- Montez, and W. Brindley. 2000. Insecticide resis- ticide products in development. Moreover, the con- tance trends in San Joaquin Valley lygus bug, cept of resistance still is met too often with one of two
Halloway, J., R. Leonard, J. Ottea, J. Pankey, and J. production—prospective plantings,
2.3 Resistance Issues in Potatoes John Keeling
Thank you for the opportunity to provide remarks at any given time may vary, but aphids, Colorado to the Pest Resistance Management Symposium on potato beetles, and late blight often are the most chal- behalf of the National Potato Council (NPC) and the lenging pests. Maintaining efficacy for these pests is potato growers we represent. There are 18 major critical. potato-producing states in the United States that pro- The NPC has made the adoption of resistance man- duced a number of potato varieties with a total farm agement a key component of the Environmental Pro- gate value of more than $3 billion in 2001. In that tection Agency’s (EPA) Pesticide Environmental same year U.S. potato producers planted 1.27 million Stewardship Program (PESP). The PESP program is acres of potatoes. Although both of these figures are a partnership between the EPA and agriculture to significant, the size of the potato industry in the Unit- increase grower adoption of pesticide strategies that ed States is small compared with major row crops. For decrease the overall risk from the use of pesticides. that reason potatoes are considered a minor crop. The NPC believes successful resistance management Potatoes are a capital-intensive crop with signifi- delivers the dual benefits of effective crop protection cant pest and disease pressures requiring a lengthy and overall decrease in pesticide application, which and complicated rotational regimen. The cost of plant- decreases environmental and worker risk. ing an acre of potatoes is more than $2,500, and rota- The potato industry was an early adopter of inte- tion with other vegetable and small grain crops results grated pest management (IPM) techniques and was in potatoes being planted on a single piece of ground among the first commodities to develop an industry- only every 3 to 5 years. Potatoes are vulnerable to wide IPM protocol and to establish a baseline for eval- yield or crop loss from fungi, insects, viruses, and uating farming IPM practices. The NPC regularly weeds. Resistance management for these pests is crit- administers a grower survey that evaluates grower ical to successful crop production and is a key compo- adoption of IPM techniques. Adoption of resistance nent in the cropping plan of most potato growers. The management techniques is an integral part of that unique characteristics of potato production offer both survey. For example, the following practices are spe- challenges and opportunities toward managing pest cifically identified in the survey as key decisions im- resistance. pacting resistance management: The NPC believes that effective resistance manage- ment is broadly dependent on two key components: Preplanting decisions grower education and adequate availability of crop • Rotate crops where the preceding crop is a non- protection chemicals or biological agents capable of pest host for potatoes controlling pests of concern. The NPC is strongly com- • Maintain spatial diversity from previous and mitted to delivering the educational component to present potato fields growers. • Use only minimum tillage in the spring to devel- Although decreasing pesticide use is not 100% syn- op a reservoir of beneficial insects onymous with managing resistance, the NPC believes that decreasing the overall amount of the active in- Weed management decisions gredient used while maintaining efficacy will result •Maintain and review individual field weed histo- in significantly less resistance pressure from all pests. ries Good stewardship of pesticides almost always is go- • Use mechanical tillage ing to lessen resistance pressure. The NPC empha- • Base chemical applications on scouting and deter- sizes that the smart, reasoned use of pesticides makes mination of efficacy good sense environmentally and economically. • Rotate herbicide mode of action Potatoes are subject to infestation from insects, • Clean equipment when moving between fields fungi, viruses, and weeds. The most critical threat • Use chemicals on rotational crops not labeled for potatoes 30 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 31
Insect management decisions for Colorado potato Potato disease management decisions beetles • Use disease-forecasting models • Use trap or barrier crops to house beneficial in- • Remove volunteer potatoes sects • Assess blight genotype prior to treatment • Leave a refuge or breeding ground for nonresis- • Use biological control where possible tant pests • Rogue virus-infected fields and eliminate all cull • Limit use of broad-spectrum pesticides piles • Use chemicals on rotational crops not labeled for • Vine-kill infected fields potatoes •Restrict number of times and classes of pesticides Farm management decisions applied to a single generation of insect • Maintain records of all applications and effective- • Apply spot or border treatments where possible ness • Base pesticide selection decisions on results of • Calibrate sprayers and use positive displacement mortality test kits application equipment • Use mechanical means when practical (vacuum •Manage storage diseases or flamer) The process used by successful growers to make Insect management decisions for aphids pesticide application decisions can decrease dramat- • Use narrow-spectrum or reduced-risk biological ically the development of resistance on individual compounds farms and in limited geographic areas. But positive • Only use reduced-rate application where recom- actions by any one commodity or geographic area will mended be ineffective without widespread adoption by all pro- • Use spot or field border spray ducers. There are limited chemistries and modes of • Use chemicals on rotational crops not labeled for action available to producers. Particular chemicals potatoes are labeled for a variety of crops, likely giving pests •Restrict number of times and classes of pesticides some exposure even before that product is considered applied to a single generation of insect for use on a potato farm. The educational effort must • Use beneficial insects timed to aphid arrivals extend to all growers in all regions of the country. • Segregate seed production to isolated areas The key barriers to addressing pest resistance ef- •Scout fectively are limited grower educational efforts and difficulty in obtaining the registration or reregistra- Insect management decisions for potato tion of the broadest toolbox of chemical and biologi- leafhoppers cal controls possible. The NPC believes that grower • Scout using sweep nets and review migration input and participation in EPA programs including progress reports the PESP helps ensure that strategies developed to • Use narrow-spectrum or reduced-risk biological address resistance management are practical and compounds workable in the real world. The development of a • Use same pesticide only once a year clear industry definition of IPM and resistance man- • Use spot sprays agement techniques in conjunction with the EPA has helped the NPC develop a consistent and effective Insect management decisions for spider mites educational message. Conducting grower surveys on • Scout fields using hand lens a regular basis has helped evaluate grower under- • Treat only at economic thresholds standing and adoption of key resistance management • Use narrow-spectrum or reduced-risk biological practices. compounds Continued availability of effective chemical and bi- ological controls is largely a function of the regulato- Insect management decisions for wireworms ry process and economic decisions made by chemical • Bait and calculate economic thresholds for larvae manufacturers. Due to the fact that potatoes are a •Rotate with alfalfa and small grains for 3–4 years minor crop, the economic issues for pesticide registra- • Sample soil tions always will be a significant obstacle. Develop- • Deep-plow alfalfa fields in August ment of controls with unique modes of action that are less susceptible to resistance development clearly should be a priority. Continuing to evaluate the 32 2.3 Resistance Issues in Potatoes effectiveness of the Interregional Research Project Number 4 (IR–4) in assisting the registration of pest control products for minor crops or minor uses should be a priority. Expanded federal funding for the IR–4 program should be evaluated and supported by the industry if the program directly addresses actual grower needs. The NPC appreciates the opportunity to provide comments to this symposium. Our growers take the issue of resistance management seriously and support the efforts of the Council for Agricultural Science and Technology and the EPA to create a forum for these discussions. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 33
2.4 Resistance Issues in Corn/Soybean Cropping Systems Kevin L. Steffey, Aaron G. Hager, Dean K. Malvick, Terry L. Niblack, and Christy L. Sprague
Introduction and soybean cultivars (i.e., with traditional plant breed- ing methods) resistant to specific pests will continue, Corn and soybeans were grown on an estimated with the concomitant concern about the target pest’s 61.3 million hectares (ha) (151.4 million acres [a.]) in ability to overcome the crop’s resistance. the United States in 2002, representing approximate- The aforementioned issues will be discussed within ly 47% of the field crop acres in the nation (NASS the following sections: insect management, nematode 2002). Corn was grown on an estimated 25.1 million management, plant disease management, and weed ha (61.9 million a.) in ten midwestern states (Illinois, management. An overview of the pest resistance man- Indiana, Iowa, Kansas, Minnesota, Missouri, Nebras- agement issues will be presented, with references to ka, Ohio, South Dakota, and Wisconsin), 79% of the specific current and potential challenges. Although estimated corn acres in the United States. In these interactions among all pests and pest resistance man- same ten states, soybeans were grown on an estimat- agement programs in corn and soybeans are likely, ed 22.9 million ha (56.45 million a.), 77% of the esti- such interactions will not be discussed in this paper. mated soybean acres in the United States. Through- out these ten midwestern states, corn and soybeans are rotated annually for improved production of both Insect Management crops and management of pests, whose populations would increase if either crop were grown continuous- Since the mid-1990s, the most widely discussed and ly. Consequently, the corn/soybean cropping system hotly debated issue associated with insect resistance is the most prevalent type of cropping system used in in the corn/soybean cropping system has been the po- field crops grown in the United States. tential for target insects to become resistant to Bacil- The corn/soybean cropping system presents unique lus thuringiensis (Bt) in transgenic Bt corn. To address opportunities and challenges for management of pests this concern, the U.S. Environmental Protection Agen- (insects, pathogens, and weeds) and the potential for cy (EPA) requires companies that submit Bt plant-in- pest resistance, especially in the twenty-first centu- corporated protectants for registration also to submit ry. The amount of land devoted to production of trans- insect resistance management plans (EPA 2002). Such genic corn and soybeans has increased significantly plans for Bt corn are intended to prevent or to slow since the introduction of those crops (CBI 2003). The down the development of resistance to Bt within pop- prospective plantings of transgenic soybeans and corn ulations of target insects. Until 2003, all Bt corn prod- have been estimated at 80% and 38% of all U.S. soy- ucts registered by the EPA were transgenic hybrids bean and corn acres, respectively, in 2003 (NASS developed for control of Lepidoptera pests, primarily 2003). The success of the current transgenic corn the European corn borer and southwestern corn bor- hybrids and soybean cultivars will encourage the de- er. Other Lepidoptera pests controlled by some or all velopment of new and different transgenic hybrids of these registered Bt corn products include armyworm, and cultivars that will be major factors in pest man- black cutworm, corn earworm, and fall armyworm. In agement well into the future. The advent of trans- February 2003, the EPA registered a Bt corn product genic crop technology also has had an impact on de- for control of western, northern, Mexican, and south- velopment of new chemical pesticides, decreasing the ern corn rootworms. The insect resistance manage- number of active ingredients being developed by com- ment plan for all Bt corn products to date includes a panies. As a consequence, the number of classes of requirement for a 20% structured refuge of non-Bt corn. chemical fungicides, herbicides, and insecticides has In the near future, corn hybrids with traits for resis- declined to just a few that are being used or could be tance against both Lepidoptera pests and corn root- used on most of the planted corn and soybean acres. worms will be available. Finally, the development of conventional corn hybrids
33 34 2.4 Resistance Issues in Corn/Soybean Cropping Systems
Another recent development in management of (Levine et al. 2002). The western corn rootworm has corn insect pests has been the increase in use of in- had a history of adapting to intense selection pressure secticidal seed treatments for control of subterranean (including development of resistance to chlorinated insects, including corn rootworms, white grubs, and hydrocarbons throughout the Midwest, first report- wireworms. All of the most recently registered insec- ed in Nebraska [Ball and Weekman 1962]), so there ticidal seed treatments—Gaucho and Prescribe (ac- is reason for concern regarding widespread exposure tive ingredient imidacloprid), and Cruiser (active in- of this pest to a limited number of pest management gredient thiamethoxam)—have been in the nicotinoid tactics. chemical class, and all of these insecticides are sys- While we have fixated on the potential for devel- temic. Another nicotinoid seed treatment—Poncho opment of insect resistance to Bt in transgenic Bt (active ingredient clothianidin)—is being developed, crops, we have ignored some basic principles of inte- although it was not registered at the time this paper grated pest management (IPM). Applying chemical was written. The current Bt corn products for root- insecticides only when an insect population density worm control do not control other subterranean in- has reached an economic threshold is one of the te- sects such as white grubs and wireworms, pests for nets of IPM. This simple tenet is both economically which rescue treatments are not effective. Conse- and ecologically sound. One of the refuge require- quently, all Bt corn for rootworm control will be treat- ments for event MON 863 (the event from which ed with one of the nicotinoid seed treatments. In ad- YieldGard Rootworm corn was derived), however, is dition, the required non-Bt corn refuge can be treated contrary to this tenet. The EPA’s Notice of Pesticide for control of corn rootworms, so it is possible that a Registration, EPA Reg. Number 524-528, February large percentage of refuges will be planted with corn 24, 2003 states: “Growers will not be permitted to seeds treated with a nicotinoid insecticide. Despite apply CRW [corn rootworm] labeled insecticides to the this possibility, the EPA has not required a resistance refuge for control of insect pests while adult corn root- management plan for registration of these nicotinoid worm are present unless the Cry3Bb1 field is treated seed treatments or for other chemical insecticides. in a similar manner.” If the pest density in the Yield- Furthermore, the companies that have manufactured Gard Rootworm field has not exceeded an economic the nicotinoid seed treatments are pursuing registra- threshold, the requirement suggests that concerns tion for their use on soybean seeds for control of bean about economics and the environment are subordinate leaf beetles and soybean aphids. It is possible that a to insect resistance management. significant percentage of the corn and soybean acres Finally, the crop protection industry is focused pri- in the ten midwestern states indicated previously will marily on development of products that are prophy- be treated with nicotinoid insecticides in the relatively lactic, rather than responsive to insect densities–Bt near future. proteins for control of corn rootworms and European Although insects that feed above ground in corn or corn borers and insecticidal seed treatments for both soybean fields are not controlled with insecticides on corn and soybeans. Many acres of corn and soybeans as many acres as insects that feed below ground in will be “treated” unnecessarily, placing considerable corn, it is important to note that most of the foliar- selection pressure on many species of insects. Al- applied insecticides currently registered for use in though insect resistance management is important for corn and soybeans are pyrethroids. Due to their ef- a viable future in crop protection, insect resistance fectiveness and economics, pyrethroids are used pref- management strategies should be developed within erentially when outbreaks of insect pests of corn and a framework of IPM, the very foundation of sustain- soybeans occur. able crop protection programs. Two other issues regarding insect pest resistance in corn are associated with western corn rootworms. As a result of wide-scale spraying of insecticides for Nematode Management multiple years in succession to manage adult west- ern corn rootworms in Nebraska, some populations Nematodes are responsible for significant yield have developed resistance to methyl-parathion and losses in both corn and soybeans throughout the Unit- carbaryl (Meinke et al. 1998). In the eastern Corn ed States (Koenning et al. 1999). The species that Belt, a strain of western corn rootworm that lays eggs causes the greatest concern throughout its range, and in crops other than soybeans has developed, proba- for which many specific resistance management strat- bly as a consequence of intense selection pressure egies have been developed, is the soybean cyst nema- imposed by rigid annual rotation of corn and soybeans tode (SCN). The use of resistant soybean cultivars has Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 35 become the standard for management of SCN, and also offered some control of nematodes. No known resistant cultivars are available from both public cases of resistance of nematodes to these insecticides breeders and private companies. Unfortunately, the were reported. The insecticides used most frequent- lack of diversity among SCN-resistant cultivars pos- ly today have little to no activity against nematodes es a challenge. For example, 93% of the SCN-resis- in corn. Current Bt corn products have no effect on tant cultivars in Illinois have the same source of nematodes in corn. resistance—PI88788. Because SCN populations adapt readily to sources of resistance, most soybean cultivars labeled as SCN-resistant can be damaged by Plant Disease Management approximately 50% of the SCN populations that oc- cur in the state. Consequently, growers experience Host plant resistance is the cornerstone for man- lower-than-anticipated yields and become dissatisfied agement of plant diseases in corn and soybeans. In with plant resistance for managing SCN. corn, major problems with pathogens overcoming re- Management recommendations for SCN in soy- sistance in host plants have not occurred. Conse- beans differ in different areas of the United States. quently, no formal resistance management programs The most common recommended cropping sequence have been implemented. In soybeans, however, rac- in the South is (1) nonhost, (2) SCN-resistant culti- es of the Phytophthora sojae fungus, which causes root var, (3) nonhost, and (4) susceptible cultivar. The ra- rot, have adapted to the major genes for resistance in tionale for the susceptible cultivar is that nonvirulent some locations (Kaitany, Hart, and Safir 2001; SCN within the population will reproduce the most, Schmitthenner, Hobe, and Bhat 1994). Although stabilizing selection within the SCN population many different genes for resistance against Phytoph- (Young 1998). The recommended cropping sequence thora are widely deployed, in some areas none of the in Iowa is (1) nonhost, (2) SCN-resistant cultivar type major genes is effective for managing the fungus. 1 (PI88788 resistance), (3) nonhost, (4) SCN-resistant Breeders are looking for new genes for resistance to cultivar type 2 (Peking resistance), (5) nonhost, and Phytophthora, and some genes for partial resistance (6) susceptible cultivar. The susceptible cultivar can (i.e., tolerance) have been deployed. In the meantime, be grown safely after two cultivars with different in places where Phytophthora seems to have overcome sources of resistance have been grown during the two the genes for resistance, growers are encouraged to preceding years when soybeans were planted. The select soybean cultivars with the highest rated levels recommendation in Illinois is to rotate different SCN- of partial resistance. resistant cultivars with nonhost crops and never grow The use of seed treatments has been a standard a susceptible cultivar. The ultimate goal of all of these practice for decades to protect corn and soybean seeds recommendations is to protect subsequent crops of and seedlings from fungal infections. Although the soybeans by decreasing the population densities of use of foliar fungicides in corn and soybeans has not SCN with resistant varieties without exerting exces- been as common as the use of fungicidal seed treat- sive selection pressure on the SCN population. ments, foliar fungicides can be applied to manage fun- New ways of labeling SCN-resistant cultivars and gal leaf blights, gray leaf spot, and rust in corn and assessing the virulence of SCN populations may help white mold, pod and stem blight, and anthracnose in growers match sources of SCN resistance with viru- soybeans. To date, no incidents of resistance of fun- lence of SCN (Niblack et al. 2002). Also, public breed- gal pathogens to fungicides in corn or soybeans have ers are emphasizing a search for new sources of re- been confirmed. Concern about the potential devel- sistance to improve diversity. Ultimately these efforts opment of resistance in some populations of fungi may should result in better management of SCN and as- escalate, however, because many new foliar fungicides sociated SCN resistance management strategies. for corn and soybeans are in the same class—strobil- Although there are some sources of resistance to urins. Azoxystrobrin, a strobilurin, is the active in- some nematodes that attack corn, host resistance is gredient for the widely used product Quadris, and tri- not a common practice for managing nematodes in floxistrobin is one of the active ingredients in the corn. Unfortunately, corn nematode damage often recently registered fungicide Stratego. SoyGard is a goes unnoticed because it cannot be diagnosed easily recently registered fungicidal seed treatment for soy- from symptoms of injury. When some organophos- beans, and one of its active ingredients is azoxystrob- phate and carbamate insecticides (e.g., Counter, in. New seed treatment products containing azox- Furadan, Mocap) were applied more widely to control ystrobin are under development and may be labeled corn rootworms and other insect pests, these products soon for control of seed and seedling diseases of both 36 2.4 Resistance Issues in Corn/Soybean Cropping Systems corn and soybeans. Strobilurins all have the same are being developed, contributing to the concern about specific site of action in the target fungi, so the development of glyphosate resistance in weed popu- danger for development of strobilurin resistance is lations. Because the system of applying glyphosate real. Widespread use of strobilurin-based fungicides in Roundup Ready soybeans is quick, easy, inexpen- potentially will place considerable selection pressure sive, and effective for weed control, it has replaced the on populations of fungi in both corn and soybeans. use of other herbicides and significantly slowed the The most effective strategy for avoiding the devel- development of new herbicides. opment of resistance to widely used fungicides is to Resistance of weeds to herbicides other than gly- abide by simple IPM practices to minimize depen- phosate also has been verified. In Illinois alone, the dence on the use of fungicides, decrease the overall list of weeds resistant to acetolactate synthase (ALS)- prevalence of disease organisms, and keep the popu- inhibiting herbicides, protoporphyrinogen oxidase lation size of pathogens low. If application of a fungi- (PPO) herbicides, and triazine herbicides is relative- cide is justified, the number of applications per sea- ly lengthy. Waterhemp populations are resistant to son should be limited, the number of consecutive ALS-inhibiting herbicides, PPO herbicides, and triaz- applications should be limited, the fungicide should ine herbicides. Smooth pigweed and kochia are re- be applied during an early stage of disease develop- sistant to ALS-inhibiting and triazine herbicides. ment, and different types of fungicides should be used Common cocklebur, giant foxtail, giant ragweed, and to minimize selection pressure by one class of fungi- common ragweed are resistant to ALS-inhibiting her- cides. The IPM principles form the foundation, and bicides, and common lambsquarters is resistant to tri- resistance management strategies should be compat- azine herbicides. ible with these principles. Weed scientists throughout the United States have prepared guidelines for minimizing the risk of devel- opment of herbicide-resistant weeds. As with so many Weed Management other IPM strategies, minimizing the risk of herbi- The registration of Roundup Ready crops, especial- cide-resistant weeds begins with scouting to deter- ly Roundup Ready soybeans, has altered significant- mine the species of weeds present and whether weed ly the way in which growers manage weeds. As indi- densities justify a herbicide application. Nonherbicide cated in the “Introduction,” the prospective plantings alternatives—mechanical cultivation, delayed plant- of transgenic soybeans, primarily Roundup Ready ing, weed-free crop seeds—should be considered. Re- soybeans, have been estimated at 80% of all soybean garding the application of herbicides to minimize the acres in the United States (NASS 2003). The acres risk of herbicide-resistant weeds, the following resis- of Roundup Ready corn have been more limited be- tance management strategies are recommended: cause the European Union will not accept imports of the grain. If Roundup Ready corn becomes acceptable • Rotate crops with a concomitant rotation of her- for export to Europe, it is possible that glyphosate (the bicides to avoid using herbicides with the same active ingredient of the herbicide Roundup) will be site of action in the same fields. used in both corn and soybeans every year, subject- • Limit the number of applications of a single her- ing weed populations to significant selection pressure. bicide or herbicides with the same site of action Concern about glyphosate resistance among differ- within a single growing season. ent species of weeds is widespread in agriculture. • Use mixtures or sequential treatments of herbi- Weed species that have become resistant to glypho- cides that control the weeds in question, but use sate have been confirmed throughout the world (Heap herbicides with different sites of action. 2003): horseweed or marestail (Conyza canadensis) in • Clean equipment before leaving fields that are in- Delaware, Indiana, Kentucky, Maryland, New Jersey, fested with or suspected to have resistant weeds. Ohio, and Tennessee; goosegrass (Eleusine indica) in Malaysia; Italian ryegrass (Lolium multiflorum) in After herbicide application, fields should be scout- Chile; rigid ryegrass (L. rigidum) in Australia, South ed to detect weed escapes or shifts. If a potentially Africa, and California; and wild radish in Canada. resistant weed population is detected, available con- Although not all of these weed species have been trol methods that prevent seed deposition in the field found in corn/soybean cropping systems, the ability should be used. of weeds to become resistant to glyphosate has been Recommendations specifically for minimizing the documented. risk of development of glyphosate-resistant weeds Few new herbicides with different modes of action Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 37 begin with all the aforementioned strategies. Other National Agricultural Statistics Service (NASS). glyphosate resistance management strategies include 2002. Acreage, June 28,
Ball, H. J. and G. T. Weekman. 1962. Insecticide re- sistance in the adult western corn rootworm in Ne- braska. J Econ Entomol 55:439–441. Council for Biotechnology Information (CBI). 2003. U.S. farmers continue to embrace biotech crops, says survey, Articles: Farmers, April,
2.5 Resistance Issues in Golf Course Turf Wendy Gelernter and Larry Stowell
Introduction • Pest complexes. Frequently, no one pest domi- nates control practices on golf course turf. In- The turfgrass industry, encompassing golf cours- stead, pesticide applications usually are target- es, parks, athletic fields, and home lawns, has grown ed at a complex of diseases, insects, or weeds, thus in tandem with the urbanization of the U.S. popula- increasing the exposure of several pests simulta- tion. Golf course turf, the most intensively managed neously to a given product. segment of this industry and the focus of this paper, • Role of stress in increased pest infestations. was responsible in 2000 for direct revenues of $20.5 Most golf course turf, particularly the 2–3 acres billion (SRI International 2002). As a rough compar- per golf course used for putting greens, is grown ison, the 1994 retail value of cotton, corn, soybeans, under severe stress conditions that increase the and wheat were $120.6, $99.0, $72.0, and $24.0 bil- likelihood and the damage associated with pest lion, respectively (National Cotton Council 1994). infestations, as well as the frequency of pesticide There currently are approximately 16,000 golf cours- treatments. Stress factors include heavily traf- es in the United States serving 35 million golfers (SRI ficked, highly compacted soils; decreased photo- International 2002). With roughly 40.5 hectares (ha) synthetic capacity due to low mowing heights; (100 acres [a.]) of managed turf and landscape plant- lack of appropriate cultivation; and suboptimal ings per course, golf courses represent approximate- irrigation practices due to their interference with ly 648,000 ha (1.6 million a.) of managed landscape. golf play. Competition among courses for golfers, the popu- • Demand for blemish-free turf leads to pre- larity of televised tournaments, and demands by golf- ventive programs. Unlike many crops in which ers for high-quality turf are continually rising, plac- successful management is judged primarily on ing added pressures on turf managers to provide yield, golf course turf is judged exclusively on ap- perfect, blemish-free turf. This backdrop underlies pearance (color, uniformity, density) and playabil- the discussion of issues and barriers in the implemen- ity. As a result, there is significant pressure on tation of resistance management programs for golf turf managers to prevent pest infestations before course turf. they develop. This reliance on preventive pro- grams, although necessary for preservation of current expectations for turf quality as well as for Pesticide Resistance Issues the superintendent’s job, results in more pesticide applications per year than for crops with higher Pesticide resistance management for golf course damage thresholds. turf is characterized by a complex interplay between • Lack of independent information sources. factors that create high risk for development of resis- Because retail markups for turf products are high tance and those that act to decrease that risk signifi- and competition among product sales forces is cantly. High-risk factors include the following: stiff, turf managers are one of the most heavily serviced end-user groups in agriculture. Because • Perennial crop. With crop rotation as one of the a turf manager typically is visited by several dis- key tenets of resistance management, the peren- tributor or agrochemical company representatives nial nature of turfgrass is a significant and inflex- each week, it is not surprising that sales people ible barrier in avoiding the development of resis- are the most popular source of agronomic infor- tance. In the turfgrass system, there is no option mation for turf managers. In contrast, the influ- to rotate to a nonsusceptible crop, no ability to lay ence of university research and extension efforts fallow, and no opportunity for deep cultivation has diminished over the past few decades, as practices that may decrease inoculum or bury funding for applied research has decreased. This weed seeds. 38 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 39
lack of funding has the additional (and perhaps •Emphasis on cultural management practic- unintentional) effect of strengthening the link es. Turf managers are well educated on the rela- between university research programs and the tionship between pest infestations and plant agrochemical industry, which funds an increas- stress. As a result, there is a strong emphasis on ing proportion of the university’s applied research cultural practices including regular soil and wa- programs. The result is a further decrease in the ter testing; optimized soil nutrition programs; ir- number of completely independent sources of ag- rigation management; aerification to promote gas ronomic and pest management information. The exchange and improve soil properties; regular issue of influence and independence extends be- monitoring for soil salinity, weather patterns, and yond university and extension programs to pri- pest infestations; and selection of pest-resistant vate consultants and contract researchers (includ- and climate-appropriate turf varieties during new ing PACE Turfgrass Research Institute), whose construction or renovations. As a result, many research programs typically are funded, at least potential pesticide applications are avoided. in part, by the agrochemical industry. While the • Diverse spectrum of pesticide products. A credibility of university, extension, and indepen- large number of products, representing different dent private consultants still is quite high among pesticide classes, typically are available in the turf end users (based on continued production of high- market. This selection allows end users to rotate quality research and a determined, successful ef- among pesticide classes if they choose to do so, and fort to remain independent of product sales), there importantly, allows turf managers to find effec- are few, if any, research or educational organiza- tive substitute products easily when other prod- tions whose operations remain completely unas- ucts are rendered ineffective by resistance. sociated with the agrochemical industry. • Availability of broad spectrum products. • Lack of proven benefits and guidelines for Fungicides such as chlorothalonil and mancozeb resistance management. Turfgrass research- have been used with success for many years, with ers who deal with the question of pest resistance no reports of pest resistance. Although there are are not unified in their approaches to resistance new regulatory restrictions on the use of these management. Recommendations range from a products, they continue to play an important role focus on rotations among pesticide classes to a in disease control and in avoiding reliance on sin- “use it or lose it” strategy of sequential applica- gle-site products that are more likely to cause re- tions of the same or similar products; and from sistance. an emphasis on mixtures of low-labeled pesticide • Reservoirs of susceptibility. For mobile pests rates to a reliance on high-labeled rates of single such as insects, the existence of large reservoirs products. These disagreements are highly publi- of untreated turfgrass (in the form of home lawns, cized and well known to end users, who are ex- parks, and less-maintained areas of the golf posed regularly to the arguments in continuing course such as roughs) can act as a tool for pre- education courses and through a tight-knit, na- serving pest populations that are unexposed and, tionwide communication network of turf manag- therefore, susceptible to pesticides. The constant ers. The confusion that this lack of unity creates mixing of these susceptible populations with is buttressed by a lack of concrete data that dem- treated (and potentially resistant) pest popula- onstrate the benefits of one approach versus an- tions may decrease the likelihood of resistance. other—or even the benefits of any resistance management program at all—for avoidance of re- The result of the interaction between these high sistance. Without a clear set of guidelines avail- and low risk factors is that several documented cases able, and without evidence that investment in re- of resistance have occurred on golf course turf (Tables sistance management efforts will yield results, 2.5.1–2.5.3), but usually in relatively localized popu- turf managers are likely to relegate resistance lations. Product failures due to resistance typically management to a low priority as they design their have been limited in scope, due to the availability of management programs. substitute products with alternate modes of action. Because of a lack of clear guidelines for avoidance of Factors that decrease the risk of pest resistance in resistance, turf managers generally place a low pri- golf course turf systems include the following: ority on incorporating resistance management prac- tices into their programs. The relatively low frequen- cy of resistance problems is therefore more a 40 2.5 Resistance Issues in Golf Course Turf
Table 2.5.1. Turfgrass diseases that have been reported to have resistance to fungicides (FRAC 2003; Vargas 1994)
Disease Fungicide
Dollar spot Rubigan, Bayleton, Banner, Chipco 26019, Vorlan Pythium Subdue and related products Pink snow mold Dicarboximides (Chipco 26019, Vorlan) Anthracnose Heritage, Compass, thiophanate-methyl (Cleary’s 3336, Fungo) Gray leaf spot Heritage, Compass
Table 2.5.2. Turfgrass insects that have been reported to have resistance to insecticides (Potter 1998; Vittum, Villani, and Tashiro 1999)
Insect Insecticide
White grubs Chlordane, dieldrin Chinch bugs Diazinon, chlorpyrifos Black turfgrass ataenius Aldrin, chlordane, dieldrin, heptachlor Sod webworms Aldrin, dieldrin
Table 2.5.3. Turfgrass weeds that have been reported to have resistance to herbicides (WeedScience.com 2003)
Weed Herbicide
Goosegrass Team and related DNA products (Balan, Surflan, Pendulum) Annual bluegrass Simazine (Princep) and related triazine products; Prograss Smooth crabgrass Acclaim and related aryloxyphenoxy products (Fusilade)
fortuitous outcome of good integrated pest manage- mixed messages delivered from the turfgrass re- ment (IPM) practices and availability of a wide spec- search community on optimal resistance manage- trum of products, rather than a result of a concerted ment strategies further exacerbate this situation. effort to avoid resistance. • Economic realities within the agrochemical industry. Competition among companies that market products with the same mode of action is Barriers to Adoption of a strong disincentive to resistance management Resistance Management stewardship. For example, in the instance of a new class of site-specific pesticides with a high Programs level of risk for causing resistance, companies have choices on how to market their products. A Obstacles in the path of more proactive resistance company that acts “responsibly” by voluntarily management programs exist as a result of informa- restricting product use based on resistance man- tion deficits, agrochemical company economic pres- agement principles will be willing to limit their sures, and lack of end-user incentives. Specific bar- sales (via restrictive label language, sales pro- riers include the following: grams, etc.) because they believe that their ac- tions will extend the life (and sales) of the prod- • Lack of data on benefits of resistance man- uct. But if there is a less scrupulous company that agement. The lack of hard data demonstrating markets a product within the same pesticide re- the operational, economic, or environmental ben- sistance management group without regard to efits of implementation of turfgrass resistance avoiding resistance, the benefits of resistance management programs has resulted in a parallel management are destroyed. When resistance and lack of incentive among agrochemical companies cross-resistance finally develop as the result of in- and end users to invest in what is considered by discriminate use of one or more of these products, some to be an unproven academic theory. The the “responsible” company will be penalized by Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 41
failing to capture sales in the early, nonresistant istries is nearly impossible are sometimes accept- window of time. The less responsible companies ed with a minimum of skepticism. Yet it seems will be conversely (and contrarily) rewarded for prudent, especially in light of recent “surprise” implementing more aggressive marketing strat- cases of resistance (e.g., QoI fungicides and Ba- egies that ignore resistance concerns. cillus thuringiensis) to assume that resistance de- velopment is likely to occur, at least until proven In an age in which product development costs are otherwise. Under this assumption, all products increasing and the effective life of a patent is short- would be handled as if resistance were an immi- ened by the length of time involved in getting a prod- nent threat, rather than waiting for resistance to uct to market, the emphasis is on achieving maximum appear before management guidelines are put in profitability as soon as possible. The benefits of “sav- place. ing” a product from resistance, thus ensuring its long- term use, is intellectually appealing but may not make practical sense to company planners and stockhold- Solutions ers. The short-term solutions described here are those • Fear of “global warning.” Researchers, in used by the PACE Turfgrass Research Institute and their attempts to transmit information responsi- are based on the assumptions that the issues and bly, are sometimes excessively cautious in relay- barriers described in this paper remain unaddressed, ing their suspicions that resistance may be in- but that knowledge of biology and resistance manage- volved in product failures. Unfortunately, by ment experiences in other crops (along with a sprin- waiting until resistance can be documented con- kling of common sense), can form the basis for rea- clusively before warning end users of a problem, sonable turfgrass guidelines. researchers sometimes inadvertently support additional applications of products to which resis- • Based on current understanding of resistance, the tance has developed, resulting in additional prod- products and pests most at risk for resistance uct failures and crop damage. should be identified, as shown in Tables 2.5.4 and • Unwarranted optimism. Company claims that 2.5.5, and should be the focus of research, educa- development of resistance to new pesticide chem- tion, and prevention efforts.
Table 2.5.4. Risk factors for pest resistance in turfgrass: High-risk pesticides. Pesticide classes and products characterized by fre- quent usage, single-site and/or specific modes of action, systemic activity/long residual activity, and/or with a history of causing resistance are considered high risk. For some of the products listed, resistance has not yet been detected among turfgrass pests, but we believe the likelihood of detection in the future is high if frequency of application is not limited in some fashion
Pesticide class Examples
QoI fungicides Azoxystrobin, pyraclostrobin, trifloxystrobin Benzimidazole fungicides Thiophanate-methyl Dicarboximide fungicides Iprodione, vinclozolin Phenylamide fungicides Mefonoxam, metalaxyl Chlorinated hydrocarbon insecticidesa Aldrin, dieldrin, chlordane, DDT, heptachlor Organophosphate insecticides Chlorpyrifos, diazinon (acetylcholinesterase inhibitors) Pyrethroid insecticides Bifenthrin, cyfluthrin, deltamethrin, cyhalothrin Acetyl chlorine receptor agonists/ Imidacloprid antagonists insecticides Ecdysone agonist/disruptor insecticides Halofenozide Triazine herbicides Atrazine, simazine DNA herbicides Benefin, oryzalin, pendimethalin Sulfonylurea herbicides Chlorsulfuron, metsulfuron, foramsulfuron, trifloxysulfuron, rimsulfuron Aryloxyphenoxy herbicides Fenoxaprop, fluazifop
a No longer labeled for use in turf in the United States. 42 2.5 Resistance Issues in Golf Course Turf
Table 2.5.5. Risk factors for pest resistance in turfgrass: High-risk pests. High-risk pests have one or more of the following characteristics: dominate control practices on a consistent basis, multiple generations per year, sexual reproduction, high reproductive rates, and/or a history of resistance to pesticides
Diseases Insects Weeds
Anthracnose White grubs (Japanese beetle, black Annual bluegrass Dollar spot turfgrass ataenius, chafers) Crabgrass Gray leaf spot Chinch bugs Goosegrass Pink snow mold Sod webworms Pythium
• In the absence of more specific information, prod- aggressive regulatory involvement in enforce- ucts at risk of resistance should be used in block ment, more restrictive labeling, mandatory mon- rotations, with no more than two sequential ap- itoring, and public reporting programs. This ap- plications of each product. proach, however, is feasible only if there are data • For products with longer residual activity that are available to support the use recommendations applied only once or twice per year (imidacloprid that would receive regulatory oversight. Without and halofenozide), alternating annual single ap- strong science as its basis, additional regulation plications of one product per year should be con- will do nothing to delay or to avoid resistance, and sidered. will squander time, money, and credibility. • The use of pesticide rotations based on the resis- tance management groups proposed by the Fun- gicide Resistance Action Committee (FRAC 2003), Literature Cited the Herbicide Resistance Action Committee (HRAC 2002), and the Insecticide Resistance Ac- Fungicide Resistance Action Committee (FRAC). tion Committee (IRAC 2002) should be followed. 2003. FRAC Fungicide List, http://www.frac.info/ •When product failures do occur and resistance is (11 June 2003) suspected to have a role, the company involved Herbicide Resistance Action Committee (HRAC). should be notified, qualified university research- 2002. Classification of Herbicides According to ers should be involved to determine the existence Modes of Action,
2.6 Resistance Issues in Organic Cropping Systems Kevin Brussell
Organic farmers have encountered few problems A good example is Robert Boettcher’s organic farm with pest resistance. Organic farms do not base pest- in the Big Sandy area of Montana. Wheat stem saw- control management on killing pests; it is used only fly, a significant pest in conventional wheat, is almost as a last resort. The focus is on preventing pest de- nonexistent in his organic wheat, which is rotated velopment in the first place. Outbreaks of pests real- with sunflowers and lentils instead of the convention- ly are indications of problems that should be ad- al wheat-barley-summer fallow rotation. dressed culturally. We work on figuring out why the Other beneficial management practices used to pre- pest occurs in significant numbers, what happened to vent pest problems include tillage, flaming, and vac- create a favorable condition/environment for the pest, uuming. Manipulation of the crop canopy for shad- and how to implement management measures that ing or sunlight inhibits weeds and diseases. Proper correct the underlying problem. The bottom line for use of manures and compost greatly improves soil organic farmers is soil health = plant health = animal health; soil mineral balance of major and minor ele- health. A healthy plant in a healthy environment is ments also is important in controlling weeds, insects, seldom bothered by pests. and diseases. For instance, corn borer seems to af- The foundation for preventing pest problems in or- fect only corn significantly when there is a fertility ganic farming is developing and maintaining the high- imbalance. A connection between plant chemistry est-quality ecosystem possible. A diversified 3- to 7- and the attractiveness of the plant to insects has been year crop rotation, alternating spring- and demonstrated by Dr. Larry Phelan at Ohio State. This fall-planted crops, is key. This rotation creates a dif- study showed that European corn borer, given a choice ferent environment in a given field each year. Row between organic plants and conventional plants, crops are alternated with solid-seeded crops and crops would avoid laying eggs on the organic plants. of different botanical families. Cover crops are plant- The biggest barrier to pest resistance management ed between cash crops to improve soil structure, sup- is industrial monocropping. We need to design the en- port a diversified soil microbe population, and provide tire agricultural system around diversity, and to do beneficial insect habitat. A soil with a balance of spe- this we need to think outside the box. University re- cies diversity works to keep pathogens in check. Only search and extension systems already have the infra- biocides that do not harm beneficial species are used, structure to accomplish this if they so choose. and then only as a last resort. Anything that disrupts the balance of microbes in the soil creates an environ- ment favorable for pests.
43 44
3.1 Triazines, Acetolactate Synthase Inhibitors, and Protoporphyrinogen Oxidase Inhibitors Les Glasgow
Introduction occurrence of new triazine-resistant populations has not been as rapid as with acetolactate synthase (ALS) In contrast to entomologists and plant pathologists inhibitors and some other herbicide modes of action who have been dealing with pesticide resistance for during the last decade. approximately 50 years, weed scientists have been Despite the occurrence of atrazine-resistant popu- relatively free from dealing with herbicide resistance lations, its use has been constant over the years. Atra- up until the past 20 years. Scientists hypothesized zine is applied to approximately 70% of the U.S. field as long ago as the 1950s, however, that resistance corn area, and to 65–70% of the sorghum area. In would develop in plants (Abel 1954; Harper 1956). sugarcane, depending on the state, this can be as high This speculation occurred about the time of introduc- as 90% of the crop area. tion of the first triazine—atrazine—that was regis- tered for use in corn in 1958. Although weed resis- tance first was documented, in 1962 (Daucus carota Factors Influencing Resistance to 2,4-D on a roadside in Canada), the resistant pop- Evolution and Management ulation did not spread, nor has resistance to auxin • Mechanism and fitness. Although there are two herbicides become a major problem. There are a num- examples of resistance due to increased herbicide ber of probable reasons for the slow early development metabolism in velvetleaf and rigid ryegrass, re- of herbicide resistance: sistance in most cases is target site based, which is due to a change in the herbicide-binding domain 1. There was usually only one application of a prod- on the D1 protein of PSII (Gronwald 1994). Be- uct per year (low selection pressure). cause the D1 (QB) protein is a chloroplast gene 2. Populations were diluted with sensitive individ- product, triazine resistance is inherited maternal- uals emerging from the seed bank. ly. This mutation not only decreases affinity of 3. Tillage normally was used before and after plant- D1 for triazines, but also decreases the rate of ing. electron transfer between PSII acceptors. Because 4. Herbicides with multiple modes of action were this effect occurs in a process that is fundamen- used. tally important for plant survival and growth, it 5. Applications were made preemergence as well as is not surprising that resistant biotypes have re- postemergence. duced photosynthetic rates, biomass production, fecundity, and competitiveness relative to suscep- tible biotypes. Triazines • Frequency. Studies have shown the initial fre- quency of the triazine resistance trait in weed pop- History and Evolution of Resistance ulations to be low, 1 x 10-10 to 1 x 10-20, compared with that of other herbicide groups such as ALS Herbicide resistance first was noted in 1968 with inhibitors, 1 x 10-6 (Gressel 1991). the identification of a biotype of common groundsel • Multiple and cross-resistance. Multiple and that was resistant to simazine (Princep). Resistance cross-resistance occur, but are limited in extent to atrazine was first documented in the 1970s in Penn- considering the 45 years of use and having been sylvania, Virginia, Delaware, and Maryland. Since documented in only eight species, of which three 1968, more than 60 triazine-resistant species (or bio- (Amaranthus rudis, Kochia scoparia, and Portu- types) have been identified (40 dicots and 20 grasses laca oleracea) are found in the United States in 35 genera) worldwide; they have been found in 31 (Heap 2003). This relatively low occurrence of U.S. states and in 18 countries (Heap 2003). The multiple or cross-resistance probably is a
44 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 45
reflection of the fitness penalty apparent in tri- • Label statements. For more than 20 years the azine-resistant biotypes that makes them more following statement has been included on all Syn- sensitive to other herbicides. genta triazine labels (Syngenta 2003): • Herbicide mixture and rotation. The use of herbicides with alternative modes of action, and Following many years of continuous use of hence a decrease in selection pressure, has been this product and chemically related products, the primary reason for atrazine and other triaz- biotypes of some of the weeds listed on this la- ines remaining viable and valuable tools for farm- bel have been reported which cannot be effective- ers. There are several other herbicides used in ly controlled by this and related herbicides. corn with different modes of action and a broad Where this is known or suspected, and weeds range of activity, such as the chloracetanilides in controlled by this product are expected to be tank mix and dicamba or 2,4-D postemergence, present along with resistant biotypes, we recom- that provide good control of the species that have mend the use of this product in combinations or evolved triazine resistance and are used in com- in sequence with other registered herbicides bination with triazines. which are not triazines. If only resistant biotypes • Crop rotation. In arable crops, triazine-resis- are expected to be present, use a registered non- tant weeds first proliferated in those areas of the triazine herbicide. Consult with your state Ag- Northeast where continuous corn cultivation was ricultural Extension Service for specific recom- practiced and growers relied predominantly on mendations. atrazine for broadleaf weed control. For econom- ic reasons, growers rotate corn with other crops such as soybeans and alternative herbicides that Conclusion have excellent activity on resistant biotypes and The use and value of atrazine, and other triazines, have been used for many years in those crops. It will continue into the future because they are effec- is unlikely with these rotations and availability tive, economical, and the cornerstone of residual weed of alternative herbicides that triazine resistance control in corn, sorghum, sugarcane, and other crops. will escalate as a problem. They remain important tools for weed control in many • Tillage. Until the advent of Roundup Ready most crops as a component of a program, and despite the soybean crops in the rotation received tillage. presence of resistant biotypes, they provide excellent Where tillage was not employed, crops received a control of a wide range of other species and suscepti- sequence of applications, including burndown ble biotypes. with mixtures such as paraquat and triazines and multiple herbicides applied preemergence. • Performance assessment. It is important to ALS Inhibitors note that for many years Syngenta and its legacy companies have provided, and still provide, a ser- History and Evolution of Resistance vice for detection of resistance to its herbicides. Syngenta representatives can send samples of The first ALS-inhibiting herbicide, chlorsulfuron, suspect plants or seeds to Vero Beach Research was introduced for weed control in cereals in 1982. Center for bioassay. Susceptibility to other her- Chlorsulfuron and other sulfonylurea (SU) herbicides bicide chemistries or modes of action also is de- are active at very low rates; gram (g)/hectare (ha) termined and advice on control of the resistant rather than the kilogram (kg)/ha for those previously biotypes is provided. developed. Since their introduction, there are now • Education. Partly because of the major depen- four additional chemical classes that inhibit ALS: im- dence of farmers on triazine herbicides and the idazolinones (IMI), triazolopyrimidines (TP), sulfony- quick response of industry, researchers, extension lamino-carbonyl-triazolinones (SCT), and pyrimidi- personnel, and farmers, as soon as weeds evolved nyl-thio-benzoates (PTB). resistance to these herbicides the information was Significant changes in herbicide potency, selectiv- distributed and changes were made in the herbi- ity, and weed control are achieved by relatively small cide use in order to avoid more serious and wide- structural alterations within a herbicide class. Con- spread problems (LeBaron, H. M., personal com- sequently, many chemical manufacturers, including munication 2003). Syngenta, continue to develop ALS-inhibiting herbi- cides with better properties and/or new uses. All 46 3.1 Triazines, Acetolactate Synthase Inhibitors, and Protoporphyrinogen Oxidase Inhibitors inhibit the ALS or acetohydroxyacid synthase (AHAS) the situation with target-site, triazine resistance, enzyme, which is the first enzyme common to the bio- resistant ALS alleles are disseminated by both synthesis of the branched chain amino acids isoleucine, pollen and seed. valine, and leucine. Selection of resistant weed populations with ALS- • Target-site plasticity. Several single amino inhibiting herbicides became apparent in 1987, with acid substitutions that convert ALS from a her- the discovery of chlorsulfuron-resistant biotypes of bicide-sensitive to a herbicide-resistant enzyme prickly lettuce (Lactuca serriola) and kochia (Kochia have been identified. Target-site resistance to scoparia) in wheat in United States. Since then, ALS- ALS inhibitors in all weed biotypes, investigated inhibitor resistance has been documented for at least thus far in natural populations, has been caused 23 monocot and 50 dicot weed species in a total of 25 by substitutions at one of five conserved regions countries (Heap 2003). of the gene with multiple substitutions having In contrast to the triazines, ALS-inhibitor resis- been identified for two of these amino acid do- tance has become so common and so widespread that mains (Tranel and Wright 2002). Thus there is a it poses a real threat to the continued use of these her- relatively large amount of flexibility in the her- bicides in certain cropping systems. For example, so bicide-binding site of the ALS enzyme (i.e., this much of the waterhemp (Amaranthus rudis) in Illinois site can tolerate substitutions with minimal con- is resistant to ALS inhibitors that these herbicides are sequences to normal catalytic function of the en- no longer recommended for its control (Hager et al. zyme). A likely explanation is that the ALS-bind- 1997). A similar situation exists for control of kochia ing site is different from its active site, although in wheat where resistant biotypes now are widespread probably in close proximity. in intensive cereal crops in the United States and Can- ada (Guttieri, Eberlein, and Thill 1995). • Cross-resistance. Data for all ALS-inhibiting herbicides and ALS substitution combinations are far from complete; nevertheless, several trends Factors Influencing Resistance have become apparent in recent years (Tranel and Evolution and Management Wright 2002). It is common to find that once a • Mechanism and fitness. The ALS inhibitors are weed has evolved resistance to one ALS inhibitor, at high risk for the evolution of resistance in weeds the resistant biotype is cross-resistant or less sen- because they have a single target site, are effec- sitive to many of the other herbicides in this class. tive against a broad spectrum of weeds, are used Although exceptions exist, resistance caused by extensively on many crops, and are relatively per- ALS inhibitors generally can be classified into sistent, often providing season-long control of ger- three types on the basis of cross-resistance: minating seeds. All data on the ALS-resistant bio- types show they are equally as fit and vigorous as 1. SU and TP the susceptible native populations, or differences 2. IMI and PTB are very subtle (Saari, Cotterman, and Thill 1994). 3. SU, IMI, TP, and PTB (broad cross- resistance) • Selection pressure. A major factor in the ap- pearance of resistance is the high selection pres- There is limited information about the newer chem- sure imposed by ALS-inhibitor herbicides on very istries, and thus earlier descriptions of cross-resis- sensitive weed species. Predominantly, resistance tance were made as follows: occurs as a result of decreased sensitivity of the target ALS enzyme to inhibition by the herbicide, 1. SU-specific although there are biotypes that have evolved a 2. IMI-specific lower level of resistance through increased herbi- 3. Broad cide metabolism and rapid detoxification thereof. Target-site insensitivity has been used to develop • Inheritance. During selection pressure from the a number of sulfonyl-urea-resistant crops, including herbicide, resistant ALS alleles are dominant over varieties of wheat, oilseed rape, tomato, soybean, and susceptible alleles. Although ALS functions in others. In addition, IMI-resistant crops such as rice plastids, ALS is a nuclear gene and follows nor- and corn are available. mal Mendelian inheritance. Hence, in contrast to Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 47
• Multiple resistance. Crucial to resistance man- as soybeans and rice, ALS inhibitors remain impor- agement and using other herbicides is the degree tant tools as part of a more complex, long-term, and of multiple resistance present in an ALS-resistant perhaps more sustainable, integrated approach to population. Although not as prevalent as cross- weed control using crop rotations, herbicide mixtures, resistance, there is substantial evidence for mul- or rotations and tillage. tiple resistance involving ALS inhibitors in a number of species (17 species worldwide, Heap 2003). Syngenta has provided a performance as- Protoporphyrinogen Inhibitors sessment service for ALS-inhibitor resistance for Company representatives and advice on use of History and Evolution of Resistance alternatives. With an understanding of the pat- terns of multiple or cross-resistance and careful The first inhibitors of the enzyme protoporphyrino- consideration of alternative or complementary gen oxidase (Protox) were launched during the 1970s herbicides, which could include the older, estab- and soon were established as excellent postemer- lished herbicides such as 2,4-D, dicamba, atra- gence-applied herbicides for control of broadleaf zine, chloracetanilides, and glyphosate, ALS re- weeds. Although there has been decline in their use sistance is managed. Recent observations of with the advent of genetically modified crops, over 5 decreased sensitivity of waterhemp populations million ha of crops were treated with these herbicides to glyphosate, however, along with resistance to in 2001. other herbicides, make it essential that growers There are now eight different Protox-inhibiting plan their weed-control programs with resistance chemistries, including diphenyl ethers (DPEs), N-phe- management in mind. nylphthalimides, oxadiazoles, oxazolidinediones, phe- nylpyrazoles, pyrimidinediones, thiadiazoles, and tri- • Label statements. In common with their state- azolinones, plus three additional herbicides that are ments for the triazine herbicides, Syngenta has as yet unclassified. Of these, the DPEs, N-phe- included resistant-management statements on nylphthalimides and triazolinones are the most com- their ALS-inhibitor product labels for many years monly used in the United States. (Syngenta 2003): Despite the extensive use of Protox inhibitors over the past 30 years, the first-ever case of evolved resis- This herbicide controls weeds by inhibiting a bio- tance was documented in waterhemp in 2001 in Kan- chemical process which produces certain essen- sas (Heap 2003). The grower had used acifluorfen (and tial amino acids necessary for plant growth. The ALS inhibitors) for many years prior to 2000. Re- inhibited enzyme system is acetolactate syn- searchers at Kansas State University demonstrated thase (ALS). Occurrence of ALS-resistant weeds that this biotype was resistant to all the Protox in- can be prevented or delayed by using this prod- hibitors tested and also to ALS inhibitors (Shoup, Al- uct in sequence or tank mixtures having a dif- Khatib, and Peterson 2003). Although the mechanism ferent mode of action, and by using some form of resistance is not yet known, no differences in ab- of mechanical control or a herbicide with a dif- sorption or translocation of foliar-applied herbicide ferent mode of action to control weed escapes between the sensitive and resistant biotypes have before they set seed. Both modes of action should been observed. provide acceptable control of the specific weed At a recent North Central Weed Science Society if applied alone at the rates used in tank mix- meeting, researchers from Kansas State University, ture. University of Illinois, Southern Illinois University, and University of Missouri gave papers on the occur- rence and management of waterhemp biotypes resis- Conclusion tant to Protox inhibitors. Resistant biotypes were 10– Resistance by a single weed species does not nec- 40 times more tolerant than susceptible biotypes to essarily prevent the use of that herbicide for the many foliar applications of DPEs (acifluorfen, fomesafen, other target species in a cropping system. There must and lactofen). be careful consideration of the tactics used, however, to avoid proliferation of this resistance into an intrac- table, economically significant, long-term problem. Despite the decline in their use in certain crops, such 48 3.1 Triazines, Acetolactate Synthase Inhibitors, and Protoporphyrinogen Oxidase Inhibitors
Factors Influencing Resistance control this particular biotype in soybeans, and there are concerns from university researchers Evolution and Management that waterhemp biotypes also are showing de- creased sensitivity to glyphosate. • Mechanism and fitness. Protox-inhibiting her- bicides have a complex mechanism of action • Performance assessment. In common with (Duke et al. 1997). Protoporphyrinogen is a key their service for the other herbicide groups men- enzyme catalyzing the last common step in heme tioned earlier, Syngenta provides a monitoring and chlorophyll biosynthesis (i.e., conversion of service to Company representatives for resistance protoporphyrinogen IX to protoporphyrin IX). to Protox inhibitors, determines susceptibility to Protox inhibition results in accumulation and herbicides with alternative modes of action, and leakage of protoporphyrinogen into the stroma provides advice on controlling the resistant bio- and or cytoplasm where it is converted into pro- types. toporphyrin IX causing light-dependent mem- brane damage and cell death. This complicated • Education. Although resistance to Protox inhib- mechanism of action provides several sites at itors is not widespread, Syngenta sponsors a field which resistance could evolve. program with universities to test resistance man- agement strategies. Pending test results, Syngen- Weed resistance to Protox inhibitors may not have ta as well as state extension scientists are recom- evolved previously because of the usually short-lived mending a two-pass program, with preemergence selection pressure of most of the herbicides that have and postemergence applications such as: been used, as well as their use as part of a program, in mixture or in rotation (alternate years) with her- Boundary or Dual II Magnum at the highest bicides with different modes of action. There currently rate for your soil type followed by either Flex- is no evidence for decreased fitness in resistant bio- star or Touchdown (only in Roundup Ready™ types, although this may be a factor considering the soybeans), applied at the appropriate use rate site of action of the Protox inhibitors. In addition, for the size of waterhemp present. there has been considerable work on adjuvants to In those situations where Protox-resistant optimize and strengthen the activity of postemer- waterhemp is present or suspected, use Bound- gence-applied Protox inhibitors. ary or Dual II Magnum at the highest rate for The absence of evolved resistance for many years your soil type, followed by Touchdown, applied is surprising––Protox inhibitors appear to have a sin- at the appropriate use rate for the size of water- gle site of action at which they are highly potent as hemp present. inhibitors at the molecular level. Many structurally The use of a Protox-inhibiting herbicide such diverse effective Protox inhibitors have been discov- as Canopy XL, Authority, or Valor preemergence ered, implying that the protogen-binding site is plas- followed by a Protox-inhibiting herbicide such as tic, like the binding sites for other herbicides that have Flexstar, Ultra Blazer, Phoenix, or Cobra poste- large numbers of effective herbicides (e.g., ALS inhib- mergence for waterhemp control should be dis- itors). couraged because use of the same mode of action will apply additional selection pressure. • Cross-resistance. It has become apparent in a When used properly, herbicide mode of action number of field and greenhouse studies that the rotation can reduce the likelihood of weed resis- biotypes tested are resistant to a range of foliar- tance development, whereas repeated use of the applied Protox inhibitors. Soil-applied Protox in- same mode of action can lead to the selection of hibitors still were effective against these resistant resistant weeds (Syngenta unpublished). biotypes, however.
• Multiple resistance. University of Illinois re- Conclusion searchers also reported a waterhemp biotype that Although resistance to Protox-inhibitor herbicides exhibited resistance to triazines, ALS inhibitors, has not, as yet, become as widespread as that to oth- and Protox inhibitors (Patzolt, Hager, and Tranel er herbicide groups, it is important to implement re- 2002). This resistance pattern leaves glyphosate sistance management strategies in these early days as the only postemergence herbicide available to of its discovery. The Protox inhibitors have an Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 49 important place in weed management, and for them practices. These include cultivation, use of full labeled to remain effective it is essential that their perfor- rates, rotation of herbicide mode of action as crops are mance be carefully monitored and best management rotated or in a continuous crop rotation, use of tank practices put in place that avoid intensive selection mixtures or sequential applications to control specif- pressure, which leads to the evolution of resistant ic weeds, and prevention of seed production and populations. spread. Well-designed, integrated management sys- tems exist that will delay the onset of, or control ex- isting, resistant weeds. Industry long has supported Barriers to Resistance and will continue to support efforts to ensure respon- Management sible use of herbicides in resistant weed management. The barriers to resistance management are com- mon to all herbicide groups and are probably similar Acknowledgments for all agrochemicals, although their significance may vary: I thank my colleagues for their valuable comments on this manuscript. • Suitable, cost-effective alternatives are unavail- able—fewer alternative chemistries or modes of action will be available. Literature Cited
• Efficacy on many weeds is still excellent—the Abel, A. L. 1954. The rotation of weedkillers. Pp. 249– product still is used at the same intensity and 255. In Proc of the British Weed Control Conference. without mixture or alternation of mode of action. The British Crop Protection Council, Farnham, U.K. • Potential for resistance development is not rec- Duke, S. O., H. J. Lee, M. V. Duke, K. N. Reddy, T. D. ognized—selection pressure is too high with too Sherman, J. M. Becerril, U. B. Nandihalli, H. Mat- many applications of a single mode of action and sumoto, N. J. Jacobs, and J. M. Jacobs. 1997. Mech- decrease of application rates, leading to selection anisms of resistance to protoporphyrinogen oxi- of tolerant individuals. dase-inhibiting herbicides. Pp. 155–160. In R. De, J. Jorrin, and L. Garcia-Torres (eds.). Weed and • Resistance is not recognized—other explanations, Crop Resistance to Herbicides. Kluwer Academic, such as wrong growth stage at application, poor Norwell, Massachusetts. conditions for activation of the herbicide, misap- Gressel, J. 1991. Why get resistance? It can be pre- plication, and late weed emergence are given for vented or delayed. Pp. 1–25. In J. C. Caseley, G. W. failure to control individuals in a population. Cussans, and R. K. Atkins. (eds.). Herbicide Re- sistance in Weeds and Crops. Butterworth-Heine- • Growers may be reluctant to use alternative mann, Oxford, U.K. methods or products—the cost of the solution can Gronwald, J. 1994. Resistance to Photosystem II In- be higher or there is a cost increase with small or hibiting Herbicides. Pp. 27–60. In S. B. Powles and no short-term benefit. Alternative programs also J. A. Holtum (eds.). Herbicide Resistance in Plants: may have a cost in complexity and a need for more Biology and Biochemistry. CRC Press, Boca Raton, knowledge of new or different techniques. Florida. Guttieri, M. J., C. V. Eberlein, and D. C. Thill. 1995. • Industry may be reluctant to recommend tactics Diverse mutations in the acetolactate synthase that decrease sales—there is a concern that es- gene confer chlorsulfuron resistance in kochia (Ko- tablishment of resistance management tactics can chia scoparia) biotypes. Weed Sci 43:175–178. decrease individual company competitiveness. Hager, A. G., L. M. Wax, F. W. Simmons, and E. W. Stoller. 1997. Waterhemp Management in Agro- nomic Crops. University of Illinois, Urbana. 12 pp. Overall Conclusion Harper, J. L. 1956. The evolution of weeds in relation to resistance to herbicides. Pp. 179–188. In Proc of Growers with the problem of controlling herbicide- the British Weed Control Conference. The British resistant weeds are advised to use good management Crop Protection Council, Farnham, U.K. 50 3.1 Triazines, Acetolactate Synthase Inhibitors, and Protoporphyrinogen Oxidase Inhibitors
Heap, I. M. 2003. International Survey of Herbicide Resistant Weeds. Web page,
Suggested Reading
Caseley, J. C., G. W. Cussans, and R. K. Atkins (eds.). Herbicide Resistance in Weeds and Crops. Butter- worth-Heinemann, Oxford, U.K. De Prado, R., J. Jorrin, and, L. Garcia-Torres (eds.). 1997. Weed and Crop Resistance to Herbicides. Klu- wer Academic, Norwell, Massachusetts. Herbicide Resistance Action Committee. Web page,
3.2 Glyphosate: A New Model for Resistance Management David C. Heering, Natalie DiNicola, R. Sammons, Brett Bussler, and Greg Elmore
Introduction to glyphosate, and the long history of extensive use of glyphosate over the past 28 years has re- For Monsanto, product stewardship is a fundamen- sulted in few instances of resistant weeds (Brad- tal component of customer service and business prac- shaw et al. 1997); tices. The issue of glyphosate resistance is important 2. Selection for glyphosate resistance using whole to Monsanto because it can adversely impact the util- plant and cell/tissue culture techniques was un- ity, sales, and life cycle of its products if it is managed successful, and therefore is expected to occur rare- improperly. The risk of developing resistance and the ly in nature under normal field conditions. potential impact of resistance on the usefulness of a 3. Glyphosate has many unique chemical properties, herbicide vary significantly across modes of action, such as its mode of action, small biomimetric however, and are dependent on a combination of dif- chemical structure, limited metabolism in plants, ferent factors. As a leader in the development and and lack of residual activity in soil, which make stewardship of glyphosate products for almost 30 the development of resistance less likely. years, Monsanto invests considerably in research to understand the proper uses and stewardship of the glyphosate molecule, including some of the factors Chemical Properties of that can contribute to the development of weed resis- Glyphosate tance. Today, some 275 herbicide-resistant weed biotypes Target-Site Specificity have been identified in various cropping systems in the United States, many of which are resistant to the Target-site alteration is a common resistance triazine, imidazolinone, and sulfonylurea herbicide mechanism among many herbicide classes (e.g., ace- families (Heap 2003; Holt and Le Baron 1990; Shan- tolactate synthase [ALS]-inhibitors and triazines). er 1995). The development of resistance depends on Glyphosate competes for the binding site of the sec- a number of factors including chemical properties of ond substrate, phosphoenolpyruvate (PEP) in the ac- the herbicide and its target-site specificity, character- tive site of 5-enolpyruvylshikamate-3-phosphate syn- istics of the plant, and agronomic practices. The on- thase (EPSPS) and is a transition state inhibitor of set of resistance to glyphosate has taken 23 years and the reaction (Steinrucken and Amrhein 1984). This affected far fewer weeds with a lower level of resis- was recently verified by X-ray crystal structure tance than with other herbicides. Based on current (Schonbrunn et al. 2001). As a transition state inhib- use data and the criteria listed here, glyphosate is itor, glyphosate binds only to the key catalytic resi- considered to be a herbicide with a low risk for weed dues in the active site. Catalytic residues are critical resistance (Benbrook 1991; Heap 2003). After almost for function and cannot be changed without a lethal three decades of worldwide use, confirmed resistance or serious fitness penalty. Furthermore, very few to glyphosate exists in biotypes of Lolium rigidum selective changes can occur near the active site of the (annual ryegrass) in Australia, South Africa, and enzyme to alter glyphosate’s competitiveness without California; Lolium multiflorum (Italian ryegrass) in interfering with normal catalytic function. Therefore, Chile; Eleusine indica (goosegrass) in Malaysia; and target-site resistance is highly unlikely for glyphosate. Conyza canadensis (marestail) in certain states of the This was further illustrated in that laboratory selec- eastern United States. tion for glyphosate resistance using whole plant or The development of weed resistance to glyphosate cell/tissue culture techniques was unsuccessful (Jan- is considered rare due to the following characteristics: der et al. 2003; OECD 1999; Widholm et al. 2001). A herbicide’s mode of action is classified by the in- 1. Most weeds and crops are inherently susceptible terference of a critical metabolic process in the plant
51 52 3.2 Glyphosate: A New Model for Resistance Management by binding to a target protein and disrupting the re- ture or function and changing them is easily accom- quired function. The “specificity” of this interaction plished while maintaining functionality (Fersht is critical for the opportunity to develop target-site- 1977). These changes represent the majority of ge- mediated resistance. Because the herbicide contacts netic diversity in a particular gene. discreet amino acids during protein binding, chang- Specificity of inhibitor binding is dependent on the ing one of these contact point amino acids can inter- number and type of the amino acids serving as con- rupt this binding. The question of how important tact points and can be measured indirectly by count- these particular amino acids are to the protein’s struc- ing the number of unique compounds that can bind ture and function versus their importance in herbi- in the same site (Figure 3.2.1). On one extreme, gly- cide binding warrants further discussion. phosate is the only herbicide compound that can bind There are three classes of amino acids in a protein’s to EPSPS. Single amino acid substitutions near the primary sequence: (1) those critical for the function active site have been observed for EPSPS, and while that describes the “active site”; (2) those important for glyphosate binding is slightly weaker, these enzymes structure (i.e., configuring the exact geometry of the also are less fit. Similarly, high specificity also is ob- active site); and (3) those not important for structure served for glutamine synthetase, binding three com- or function. In terms of those critical for function, pounds including phosphinothricin in the active site changing one of these few amino acids almost always (Crespo, Guereo, and Florencio 1999). Paraquat and incapacitates or creates a very “unfit” protein. In com- diquat are the only two herbicides inhibiting photo- parison, changing one of the many amino acids re- system I. No target-site mutations have been report- sponsible for structure, the second class, sometimes ed to be responsible for resistance in these systems can be accomplished while maintaining functionality (Powles and Holtum 1994). if the substitution is homologous. Finally, in most On the other extreme are target enzymes that are proteins many amino acids are not critical for struc- efficiently inhibited by a wide array of compounds
(Legend for Figure 3.2.1.)
Modes of Actiona Compounds Species ALS 53 79 PPO 27 1 Triazines, C1 26 64 ACCase 21 30 Auxins 21 23 Ureas, C2 20 20 Thiocarbamates 18 7 Dinitroanilines, K1 15 10 Chloroacetamides 12 2 HPPD 7 0 Quats 2 22 Glyphosate 1 4 Phosphinothrecin 1 0
Figure 3.2.1. Compounds in modes of action versus resistant species. aMode of Action (MOA), Compounds, Acetolactate synthase (ALS), Protoporphyrinogen Oxidase (PPO), Acetyl Co-A carboxylase (ACCase), Chloroacetamides were limited to just chloro derivatives, 4-Hydroxyphenyl-Pyru- vate-Dioxygenase (HPPD). Number of compounds taken from Herbicide Resistance Action Committee (2002). Classification of Herbicides According to Mode of Action,
(e.g., ALS) is inhibited by 53 and acetyl CoA carboxy- phosate, using a lethal dose of herbicide is critical. lase [ACCase] is inhibited by 21 separate herbicide Results that support these strategies are beginning compounds that bind both within and outside the ac- to emerge from recent field research studies at sev- tive site; (HRAC 2003; Tranel and Wright 2002). eral universities where it is documented that studies These cases demonstrate that numerous noncritical must be done in the field in the crop (Roush, Ra- amino acids are involved (outside the active site) of- dosevich, and Maxwell 1990). Various weed manage- fering a relatively large range of permissible muta- ment programs have been evaluated since 1998 to tions. In these two cases, a single amino acid change determine how they impact weed population dynam- can result in virtual immunity to the class of herbi- ics. Studies were initiated in Colorado, Kansas, Ne- cides and has led directly to the preponderance of re- braska, Wyoming (Wilson, R. G., et al. 2002, unpub- sistant weed species for these mode-of-actions lished data), and Wisconsin (Stoltenberg 2002) to (MOAs), 79 and 30, respectively. evaluate continuous use of Roundup Ready technolo- gy with exclusive use of glyphosate or inclusion of her- bicides with other MOAs, and rotation away from Limited Metabolism in Plants Roundup Ready technology. These treatment regimes Metabolism of the herbicide active moiety often is were compared with a conventional herbicide program a principal mechanism for the development of herbi- for each crop evaluated. General observations after cide resistance. The lack of glyphosate metabolism 5 years are the following: or significantly slow glyphosate metabolism has been reported in several species and reviewed in various 1. Use of a continuous Roundup Ready cropping sys- publications (Coupland 1985; Duke 1988), and there- tem with either glyphosate alone at labeled rates fore, it is unlikely that this specific mechanism would or incorporation of herbicides with other MOAs come into play with glyphosate. resulted in excellent weed control with no weed shifts or resistance reported. 2. Use of glyphosate at below-labeled rates result- Lack of Soil Residual Activity ed in a weed shift to common lambsquarters at Herbicides with soil residual activity dissipate over two locations (Nebraska and Wyoming). time in the soil resulting in a sublethal exposure and 3. In Wisconsin, ALS-resistant giant ragweed was in effect low-dose selection pressure. Glyphosate ad- selected for in the broad-spectrum residual her- sorption to soils occurs rapidly, usually within 1 hour bicide regime implemented in the conventional (Franz, Mao, and Sikorski 1997). This binding makes corn cropping system. The continuous glyphosate glyphosate unavailable to plant roots, and hence no system (using labeled rates) resulted in no signif- impact to plants is observed from soil-bound glypho- icant weed shifts. sate. Glyphosate’s postemergent-only activity allows the use of a high-dose weed management strategy. The use of glyphosate at the recommended lethal dose has prevented the buildup of weeds with great- er inherent tolerance, and any potential resistance al- Weed Management Strategies leles have been avoided over the duration of these for Glyphosate studies. Rotating herbicide MOAs every other year has been postulated as a way to prevent or significant- A key element of good weed management is using ly delay resistance to glyphosate. It is not well un- the correct rate of glyphosate at the appropriate win- derstood, however, whether occasional abstinence dow of application for the weed species and size from using a weed control tool will have any substan- present. Higher herbicide doses result in higher weed tial impact on delaying resistance development. It mortality and less diversity of resistance genes in the may depend on the characteristics of the specific her- surviving population (Matthews 1994). Low herbicide bicide or method of control. Gressel (2002) states that rates also may allow both heterozygous- and homozy- abstinence that allows weed seed buildup can have gous-resistant individuals to survive (Maxwell and very negative effects. Preliminary results from the Mortimer 1994), further contributing to the buildup university studies mentioned previously indicate that of resistant alleles in a population. As resistance is continuous Roundup Ready systems used over several dependent on the accumulation of relatively weak years did not create weed shifts or resistant weeds genes, which may be the case for one or more of the when the correct rate of glyphosate was applied and four weed species that have evolved resistance to gly- good weed management was practiced. 54 3.2 Glyphosate: A New Model for Resistance Management
Much of the industry’s experience with weed resis- very difficult to predict accurately, and no single ag- tance is based on triazine and ALS resistance. With ronomic practice will mitigate resistance for all her- over 130 weeds resistant to these chemistries global- bicides or all weeds. As a result, weed resistance ly (Heap 2003), most weed management recommen- needs to be managed on a case-by-case basis and tai- dations are based on traditional weed management lored for the particular herbicide and grower needs. recommendations that include rotation of herbicide Using good weed management principles built on MOA and tank mixing. Because this has driven cur- achieving high levels of control through proper appli- rent industry recommendations, Monsanto believes it cation rate, choice of cultural practices, and appropri- is critical to study the epidemiology of specific cases. ate companion weed control tools will allow continued, effective use of glyphosate. The key principles for effective stewardship of gly- ALS Herbicide Case Study phosate use, including Roundup Ready crops, include in Iowa (1) basing recommendations on local needs and using the tools necessary to optimize weed control; (2) es- This information outlines general herbicide use in tablishing proper rate and timing of application; and a typical corn/soybean rotation. (3) responding rapidly to instances of unsatisfactory weed control. Corn from 1990 through 1997: • 84% of the corn acres were cultivated. • 58 to 72% of the corn acres were treated with atra- Literature Cited zine. • 35 to 60% of the corn acres were treated with me- Benbrook, C. 1991. Racing against the clock. Ag- tolachlor, alachlor, or acetochlor. richem Age 35:30–33. • 24 to 50% of the corn acres were treated with di- Bradshaw L. D., S. R. Padgette, S. L. Kimball, and B. camba or 2,4-D. H. Wells. 1997. Perspectives on glyphosate resis- •From 1991 to 1997, 5 to 17% of the acres were tance. Weed Technol 11:189–198. treated with nicosulfuron, which has no activity Coupland, D. 1985. Metabolism of glyphosate in on waterhemp. plants. Pp. 25–34. In E. Grossbard and D. Atkin- son (eds.). The Herbicide Glyphosate. Butter- Soybeans from 1990 through 1997: worths, London. • 22 to 74% of the soybean acres were treated with Crespo J. L., M. G. Guereo, and F. J. Florencio. 1999. imazethapyr. Mutational analysis of Asp51 of Anabaena azollae • 54 to 73% of the soybean acres were treated with glutamine synthetase. D51E mutation confers re- pendimethalin or trifluralin (National Agricultur- sistance to the active site inhibitors L-methionine- al Statistics Service 2002). DL-sulfoximine and phosphinothricin. Eur J Bio- chem 266:1202–1209. Based on the above information, growers in Iowa Duke, S. O. 1988. Glyphosate. Pp. 1–70. In P. C. Kear- utilized crop rotations that resulted in a herbicide use ney and D. D. Kaufman (eds.). Herbicides: Chem- pattern with multiple MOAs that were effective on istry, Degradation and Mode of Action, Vol. 3. Mar- waterhemp. Even with this commonly promoted and cel Dekker, New York. accepted practice for preventing weed resistance, Fersht, A. 1977. Enzyme Structure and Mechanism. waterhemp resistant to ALS herbicides was selected W. H. Freeman. San Francisco, California. rapidly. Franz, J. E., M. K. Mao, and J. A. Sikorski. 1997. Gly- phosate: A Unique Global Herbicide. ACS Mono- graph 189. American Chemical Society, Washing- Summary ton, D.C. Gressel, J. 2002. Molecular Biology of Weed Control. Glyphosate has unique characteristics that have Taylor and Francis, London. made it difficult for plants to avoid its lethal effects, Heap, I. 2003. The International Survey of Herbicide so we should not assume that employing weed resis- Resistant Weeds. Web page, tance management tactics developed for other herbi-
Holt, J. S. and H. M. Le Baron. 1990. Significance and Tranel, P. J. and T. R. Wright. 2002. Resistance of distribution of herbicide resistance. Weed Technol weeds to ALS-inhibiting herbicides: What have we 4:141–149. learned? Weed Sci 50:700–712. Jander, G., S. R. Baerson, J. A. Hudak, K. A. Gonza- Widholm, J. M., A. R. Chinnala, J. H. Ryu, H. S. Song, lez, K. J. Gruys, and R. L. Last. 2003. Ethyl- T. Eggett, and J. E. Brotherton. 2001. Glyphosate methanesulfonate saturation mutagenesis in Ar- selection of gene amplification in suspension cul- abidopsis to determine frequency of herbicide tures of 3 plant species. Physiol Plant 112:540–545. resistance. Plant Physiol 131:139–146. Matthews, J. M. 1994. Management of herbicide re- sistant populations. Pp. 317–335 . In S. B. Powles and J. A. M. Holtum (eds.). Herbicide Resistance in Plants, Biology and Biochemistry. Lewis, Ann Ar- bor, Michigan. Maxwell, B. D. and A. M. Mortimer. 1994. Selection for herbicide resistance. Pp. 1–26. In S. B. Powles and J. A. M. Holtum (eds.). Herbicide Resistance in Plants, Biology and Biochemistry. Lewis, Ann Ar- bor, Michigan. National Agricultural Statistics Service. 2002. Web page,
3.3 Demethylation Inhibitor Fungicide Resistance in Fruit Crops Wayne F. Wilcox
Introduction by the fungicide dose. In contrast, practical resistance to the DMI fungicides results typically from direction- Scab (Venturia inaequalis) and powdery mildew al selection, whereby fungicide sensitivities within the (Uncinula necator) are the two most common targets original baseline population are distributed normal- of fungicides applied to apples and grapes, respective- ly and unimodally, with no immune subgroup. When ly, both in the United States and internationally. In fungicide exposure rates are decreased, through such the United States, sterol demethylation inhibitor factors as dilution within the growing plant, inade- (DMI) fungicides have been registered for the control quate spray coverage, or an intentional decrease of use of both diseases since the 1980s and have been used rates, the least-sensitive members of the population heavily for these purposes since then. Practical re- are selected and gradually come to predominate. sistance to the DMI fungicides (unacceptable disease Losses in disease control often are gradual and incre- control attendant with a selection of resistant patho- mental over time (Köller and Scheinpflug 1987). gen phenotypes) first was suspected for V. inaequal- is within 5 to 6 years after commercial introduction of the fungicides, and documentation finally was pub- Management of the Problem lished in 1997 (Köller et al. 1997). Now, DMI resis- tance is considered common in regions with intensive A three-pronged approach was taken in the north- apple scab pressure such as Michigan and New York, eastern United States to managing DMI resistance in where the utility of these materials in disease control apple and grape production systems: (1) Defining the programs has been limited seriously as a result. Re- problem within a commercial context; (2) Determin- sistance also is widespread in the apple-growing re- ing the utility of theoretical resistance management gions of Europe and is suspected (but not document- (RM) strategies under field conditions; and (3) Using ed) in parts of South America. Similarly, this information as the basis for educating growers compromised control of grapevine powdery mildew and their advisors about the issue. was noted a comparable time after the DMIs first were registered on this crop (e.g., Travis and Muza 1991). Practical resistance was documented in both Califor- Defining the Problem nia (Gubler et al. 1996) and New York (Erickson and Prior to the introduction of DMI fungicides into the Wilcox 1997) a few years later, and now is considered apple market, a resistance-monitoring technique was to be widespread in the United States and Europe; it developed for Venturia inaequalis, and baseline sen- also has been documented in South Africa and is sus- sitivity distributions were determined (Köller, Park- pected (but not documented) in parts of Australia and er, and Reynolds 1991; Smith, Parker, and Köller South America. Although the DMIs still are used to 1991). When commercial control problems subse- control this disease, their importance is now dimin- quently arose, these techniques and data were used ished seriously from what it was previously. to compare the fungicide sensitivities of pathogen Practical resistance to some types of fungicides populations within affected orchards with those in (e.g., the benzimidazoles) develops as a result of dis- baseline settings. Such comparisons showed that the ruptive selection. Although the vast majority of the least-sensitive members of the pathogen population, baseline population of the target fungus is highly sen- which were present at a frequency of <2% under base- sitive to the toxicant, a distinct subgroup is virtually line conditions, had been selected to a frequency of immune and undergoes rapid selection as the mate- ≥40% in orchards where scab control with DMI fun- rial is used in disease management programs, result- gicides had been compromised. Such phenotypes ing in the potential for a sudden loss of control (Köller therefore were defined as resistant, and it was shown and Scheinpflug 1987). Such selection is not affected that commercial rates of the labeled DMI products
56 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 57 provided approximately 50–75% control of them ver- cide in mixture does not allow a decrease of the DMI sus 100% control of sensitive phenotypes in green- rate from an RM viewpoint, and use of both strate- house evaluations (Köller et al. 1997). gies (high DMI rate plus inclusion of a protectant) is Similarly for Uncinula necator, the least-sensitive the preferred tactic (Köller and Wilcox 1999a). In con- phenotypes that originally constituted a mere fraction trast, mixing a second systemic compound (dodine) of the baseline population were found to constitute with a low rate of fenarimol distinctly decreased se- >90% of the population in vineyards where practical lection of the DMI-resistant isolates. It was conclud- resistance to triadimefon had developed, and the ed that mixing DMI fungicides with protective com- median ED(50) (the effective dose for 50% inhibition pounds such as mancozeb does not decrease the of mycelial growth) was 30-fold higher than in base- selection of DMI-resistant phenotypes because the line populations. In contrast, median ED(50) values two fungicides inhibit the fungus in spatial and tem- for two other DMIs, fenarimol and myclobutanil, had poral isolation. In contrast, dodine and fenarimol increased by only two- to eightfold in the same vine- inhibit the fungus in concert both temporally and spa- yards, and these materials still were providing accept- tially; hence selection will occur only for fungal iso- able powdery mildew control, although prospects for lates that are resistant to both (Köller and Wilcox their continuing efficacy was considered tenuous 1999a, 2000). (Erickson and Wilcox 1997). Resistance management strategies for Uncinula necator were tested over 4 years in a commercial vine- yard where practical resistance to triadimefon had Field Tests of Resistance Management been documented, but where sensitivity shifts with Strategies respect to myclobutanil, another DMI with greater For Venturia inaequalis, a 3-year trial was conduct- intrinsic activity, was less pronounced and this ed in an orchard where the frequencies of phenotypes material was still effective. The specific strategies deemed resistant to fenarimol and the unrelated fun- tested were (1) using a high DMI rate (112 versus gicide, dodine, were representative of commercial set- 56 grams (g)/hectare (ha) of myclobutanil); (2) limit- tings in which sensitivity shifts had begun but were ing DMI use (three applications of myclobutanil still well short of conferring practical resistance. The rotated with three of sulfur versus six of myclobuta- RM strategies investigated were (1) use of a high DMI nil only); and (3) limiting the size of the pathogen rate (30 versus 15 micrograms (µg)/milliliter (ml) fe- population against which DMIs are applied (three narimol); (2) application of the DMI fungicide in mix- sprays of myclobutanil early in the season followed ture with a surface protectant (mancozeb); and (3) by sulfur versus the converse; i.e., applying at the application of the DMI in mixture with another, un- start of the epidemic rather than once it is in related, systemic compound (dodine). Each year, dis- progress). Disease control and myclobutanil sensitiv- ease incidence and severity data were gathered and ities within treatment populations were determined fungicide sensitivity distributions were determined as stated previously. for a collection of single-spore isolates from each treat- The full 112 g/ha rate of myclobutanil provided ment population. From these data, the control of both equivalent disease control when used in all six appli- the sensitive and resistant subpopulations was cal- cations or only three times at the start of the season; culated for each treatment. however, improved control of the resistant subpopu- Whereas both fenarimol rates provided statistically lation (less selection) was provided by the lower spray equivalent control of the DMI-sensitive and DMI-re- frequency. Furthermore, this rate also was signifi- sistant subpopulations, the lower rate provided in- cantly less effective, both with respect to disease con- tense selection pressure for the resistant phenotypes trol and the selection of resistant phenotypes, when (i.e., it provided only 25% as much control of the re- applied in the last three sprays rather than the first sistant subpopulation as of the susceptible popula- three. Halving the myclobutanil rate to 56 g/ha de- tion). Tank mixing with mancozeb improved control creased disease control by approximately 50%, and of both subpopulations equally. Therefore, although control of the resistant subpopulation by 50–75%, mixing mancozeb with a low rate of fenarimol de- relative to the full rate (Wilcox 2003). creased the overall level of disease relative to the fe- narimol-only treatments, it did not decrease the fre- quency (selection) of DMI-resistant phenotypes within Educational Efforts the pathogen population that survived treatment with The theory of resistance development, basic RM this mixture. Thus, inclusion of a protectant fungi- strategies, and the results of supporting research 58 3.3 Demethylation Inhibitor Fungicide Resistance in Fruit Crops projects were presented to growers and advisors many of the fungicidal alternatives to the DMI mate- through a repeated series of oral presentations, state- rials; for example, Venturia inaequalis versus dodine wide newsletter articles, and regional and national (Köller, Wilcox, and Jones 1999), Uncinula necator trade publications (e.g., Köller and Wilcox 1999b; versus boscalid, and both pathogens versus the QoI Wilcox 1999, 2003; Wilcox and Köller 1996). In 1999, fungicides. In fact, it seems that pathogen popula- a survey was commissioned among the majority of tions that already have been selected for resistance wine grape growers in New York, to determine the to one group of fungicides may be predisposed to de- relative importance that they attached to RM with veloping resistance to additional unrelated groups respect to other factors that might influence their (Köller and Wilcox 2001). Another limitation is the choice of a fungicide. These factors, in decreasing temporal and spatial separation of protectant com- order of importance to the respondents (% respon- pounds from the DMIs when the two are applied in dents rating the factor as “highly important”) were: mixture. For example, DMI fungicides function (1) efficacy (100); (2) resistance management (86); (3) against V. inaequalis from within the plant after in- handler and worker safety (50); (4) cost (43); and (5) fection has occurred, whereas traditional protectant environmental toxicity (36) (G. B. White and W. F. compounds (e.g., mancozeb, captan) prevent infection Wilcox unpublished). Such data demonstrate that the by inhibiting spore germination on the outer tissue importance of RM is recognized by growers, although surfaces. Thus, if a DMI is applied within a few days it does not indicate to what extent growers employ the after an infection has occurred (the only time that it recommended practices. Anecdotal observations sug- is effective), the protectant fungicide mixed with it will gest that compliance is high, however, provided that provide no additional control of that infection event the recommended practices are practical and overtly (i.e., it will do nothing to decrease the selection of connected with efficacy in growers’ perception. DMI-resistant isolates that might result from that particular spray). Barriers to Resistance Management Regulatory Issues Broad-spectrum protectant fungicides (captan, Various economic, technical, and social barriers chlorothalonil, mancozeb, ferbam, etc.) have been exist with the potential to limit RM, most of which used for over a half century with no development of apply to other at-risk fungicides in addition to the resistance and are common components in RM pro- DMIs. They include cost, technical limitations of al- grams in fruit and other crops. Many of these com- ternative fungicides used in rotation or tank mixes, pounds will be reviewed under the Food Quality Pro- regulatory issues, conflicts with marketing strategies, tection Act as potential carcinogens, however, and and lack of research support. their regulatory future is uncertain. Furthermore, regulatory issues have precluded the use of DMIs with higher intrinsic activities than those that are now Cost allowed. For example, the ED(50) for baseline popu- The use of high rates and the inclusion of a tank lations of Venturia inaequalis with respect to flusila- mix partner involve an additional cash outlay rela- zole, a DMI that is registered for use on apples in both tive to avoiding these practices. Experience suggests Europe and Canada, is 0.008 µg/ml. In contrast, those that cost is a more important factor in the choice of with respect to fenarimol and myclobutanil, the two fungicide options than indicated in the grower survey standard DMIs registered for apple scab control in the referenced in the preceding section. For instance, United States, are approximately five- and ninefold there may be a tendency to decrease the rates of both as great, respectively (Köller, Parker, and Reynolds components of a tank mix to more closely approximate 1991). Substituting one DMI of greater activity than the cost of using either one alone. This is not a good another is tantamount to increasing the rate of the RM practice. original; and in fact, flusilazole and a similarly active compound (difenconazole) are the only two DMIs that still provide some control of scab in European or- Technical Limitations of Alternative chards where practical resistance is rampant. Nei- Fungicides Used in Rotation or Tank Mixes ther is registered in the United States. Paramount, perhaps, among several limitations is the actual or potential occurrence of resistance to Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 59
Conflicts with Marketing Strategies Gubler, W. D., H. L. Ypema, D. G. Ouimette, and L. J. Bettiga. 1996. Occurrence of resistance in Although high use rates are an important compo- Uncinula necator to triadimefon, myclobutanil, and nent of RM strategies for DMI fungicides, these prod- fenarimol in California grapevines. Plant Dis ucts often are priced so that only marginal rates are 80:902–909. economically competitive. Recently the conflict be- Köller, W. and H. Scheinpflug. 1987. Fungal resis- tween marketing and RM strategies has become ap- tance to sterol biosynthesis inhibitors: A new chal- parent with respect to the new QoI fungicides, which lenge. Plant Dis 71:1066–1073. have supplanted the DMIs to some extent for use Köller, W. and W. F. Wilcox. 1999a. Evaluation of against both Venturia inaequalis and Uncinula neca- tactics for managing resistance of Venturia tor. Although it is known that use of the QoI materi- inaequalis to sterol demethylation inhibitors. als in a curative (rather than preventive) mode pro- Plant Dis 83:857–863. vides significant selection pressure favoring the Köller, W. and W. F. Wilcox. 1999b. Sustained con- least-sensitive segment of a fungal population (Wong trol of apple scab: Fungicide options, fungicide re- and Wilcox 2002), such a use pattern is being promot- sistance, and FQPA. NY Fruit Quart 6(4):14–18. ed for these products by some advertising and sales Köller, W. and W. F. Wilcox. 2000. Interactive effects personnel in order to improve the products’ commer- of dodine and the DMI fungicide fenarimol in the cial appeal. control of apple scab. Plant Dis 84:863–870. Köller, W. and W. F. Wilcox. 2001. Evidence for the predisposition of fungicide-resistant isolates of Ven- Lack of Research Support turia inaequalis to a preferential selection for re- Effective RM recommendations should be based on sistance to other fungicides. Phytopathology proven principles rather than dogma or guesses. Fur- 91:776–781. thermore, experience shows that growers are far more Köller, W., D. M. Parker, and K. L. Reynolds. 1991. likely to implement recommended strategies when Baseline sensitivities of Venturia inaequalis to ste- their utility has been demonstrated rather than mere- rol demethylation inhibitors. Plant Dis 75:726– ly pontificated. Thus, it is both perplexing and dis- 728. quieting that public support for the science of RM has Köller, W., W. F. Wilcox, and A. L. Jones. 1999. Quan- all but vanished. Resistance management is too “ap- tification, persistence, and status of dodine resis- plied” for the National Research Initiative and other tance in New York and Michigan orchard popula- programs pertaining to agricultural research that tions of Venturia inaequalis. Plant Dis 83:66–70. focus on fundamental sciences. The preservation, Köller, W., W. F. Wilcox, J. Barnard, A. L. Jones, and rather than replacement, of registered pesticide P. G. Braun. 1997. Detection and quantitation of tools—even those considered “reduced risk” by the En- resistance of Venturia inaequalis populations to vironmental Protection Agency—does not appear to sterol demethylation inhibitors. Phytopathology fit the priorities of national integrated pest manage- 87:184–190. ment research programs. Those concerned and im- Smith, F. D., D. M. Parker, and W. Köller. 1991. pacted by RM have not marshaled the political where- Sensitivity distribution of Venturia inaequalis to withal to get this topic recognized as a legitimate the sterol demethylation inhibitor flusilazole. Phy- objective within new, narrowly targeted programs. As topathology 81:392–396. old pesticides are replaced by newer and often safer Travis, J. W. and A. J. Muza. 1991. Evaluation of materials, these will face increasing risk of loss to disease management strategies for the control of resistance if it is not possible to discover how best to Bayleton resistant Uncinula necator on grapes, maintain their longevity. 1990. Fungic Nematic Tests 46:94–95. Wilcox, W. and W. Koeller. 1996. Apple scab resis- tance to sterol inhibitor fungicides? Great Lakes Literature Cited Fruit Grower News, April 1996, pp. 54–55. Wilcox, W. F. 1999. Understanding and managing Erickson, E. O. and W. F. Wilcox. 1997. Distribution fungicide resistance. Wine East 27(2):10–13. of sensitivities to three sterol demethylation inhib- Wilcox, W. F. 2003. Strategies to control powdery itor fungicides among populations of Uncinula ne- mildew. Prac Wine Vine 24(6):16–24. cator sensitive and resistant to triadimefon. Phy- topathology 87:784–791. 60 3.3 Demethylation Inhibitor Fungicide Resistance in Fruit Crops
Wong, F. P. and F. W. Wilcox. 2002. Sensitivity to azoxystrobin among isolates of Uncinula necator: Baseline distribution and relationship to myclob- utanil sensitivity. Plant Dis 86:394–404. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 61
3.4 Diamondback Moth Resistance in Crucifers Anthony M. Shelton and J. Z. Zhao
Background thousands, of miles so resistant genes may be spread rapidly over a large geographic area (Talekar and Crucifers are a diverse plant family containing Shelton 1993). There also is evidence of considerable many species of weeds, vegetables such as cabbages variation in esterase activity between DBM popula- and broccoli, and the field crop rapeseed/canola. In tions, leading to differences in susceptibility to spe- North America and Central America in 2002, 119,431 cific insecticides (Maa 2001). From an agronomic hectares (ha) of vegetable crucifers and 3,720,990 ha standpoint, in areas in which crucifers are grown con- of rapeseed/canola were harvested (FAOSTAT 2003). tinuously DBMs can move from one crop to the next The climatic conditions for growing crucifer crops in and be selected for resistance while they reside in each North America vary dramatically, but the diamond- crop. back moth (DBM), Plutella xylostella, can be a prob- lem in all areas where crucifers are grown. It is es- Early Surveys for Resistance pecially problematic in warmer areas where crucifers are present year-round. In the temperate parts of North America, DBMs may not be able to overwinter For decades DBMs have been reported as pests and must be reintroduced into these areas by aerial throughout the United States, but generally they were movement of adults (Hopkins 1999) or on plant ma- able to be controlled with the available insecticides. terial grown in other areas (Shelton et al. 1996). Be- In the late 1980s at a national entomology conference, cause of their high cosmetic standards, vegetable cru- there was considerable discussion about how insecti- cifers generally sustain higher losses by DBMs than cidal control of DBMs seemed to be failing in many do field crucifers. The area grown to the field cruci- parts of the United States. In 1988, a cooperative fer rapeseed is more extensive, however, and in some program was developed to examine the susceptibili- years DBM can cause considerable damage. ty of DBM populations throughout much of North Diamondback moths have become a problem in sev- America (Shelton et al. 1993a). Forty-four popula- eral parts of the world, primarily for two reasons: it tions of DBMs were collected from 19 states within has been able to develop resistance to a number of the United States, Mexico, Canada, and Belize dur- different insecticide classes, and the use of broad-spec- ing the peak activity of DBMs in each area. Using a trum insecticides has decreased its natural enemy leaf dip assay, the populations were examined for sus- complex. Diamondback moths appear able to devel- ceptibility to three commonly used classes of insecti- op resistance to some insecticides faster than one of cides: pyrethroid (permethrin-Ambush 2E), carbam- their principal natural enemies, Diadegma insulare, ate (methomyl-Lannate 1.8L), and organophosphate and this can exacerbate the problem (Xu, Shelton, and (methamidophos- Monitor 4E). Resistance ratios (RR) Cheng 2001). Diamondback moths were the first ag- varied the most for methomyl (up to 780-fold); 15% of ricultural pests to develop resistance to DDT (Ank- the populations had RR values ≥50, and 46% had val- ersmit 1953), and since that time some populations ues <10. The highest RR value for permethrin was of DBMs have been able to develop resistance to ev- 81; 17% of the populations had RR values >50 and ery major class of insecticide (Talekar and Shelton 56% had values <10. The highest RR value for meth- 1993). There are biological characteristics of the in- amidophos was 42; none had values >50 and 83% had sect and agricultural characteristics of crucifer pro- values <10. No geographic patterns for resistance duction that seem to enhance the development of re- were evident, because different populations within the sistance. For example, DBMs have rapid life cycles same state or region may have varied considerably in in which a generation may be produced in less than 2 their susceptibility. From this survey and an assess- weeks. An individual adult also may produce nearly ment of field performance where the samples were 200 eggs, and adults may travel hundreds, or even taken, provisional concentrations were developed to categorize susceptibility to each insecticide. 61 62 3.4 Diamondback Moth Resistance in Crucifers
Another survey was conducted in 1990 with 11 pop- Although long-range movement of adult DBMs has ulations of DBMs collected from six U.S. states to as- been documented to occur (e.g., Hopkins 1999), con- sess susceptibility to methomyl and permethrin and taminated transplants may be a more direct source two different products containing Bacillus thuringien- because the majority of cabbage grown in New York sis subsp. kurstaki. In this survey (Shelton et al. originates from transplants grown in southern re- 1993b) the highest RR value for methomyl was 875, gions. Transplants, grown in the field or in green- and for permethrin 237. The highest RR value was houses, enable earlier production of cabbage in the 178 for Dipel 2X and 211 for Javelin WG and this oc- northern regions of the United States. curred in a population from New York, an area in Samples collected from 1989 to 1992 documented which DBMs do not overwinter. Two populations that DBMs were introduced into New York in the from Florida had RR values to Dipel 2X > 50. In a early spring on cabbage (Shelton et al. 1996). Dur- subsequent survey that just focused on populations ing 1989, transplant shipments from five transplant from Florida, one population had an RR of 1,641 to companies in Florida, Georgia and Maryland were Javelin (Shelton et al. 1993b). A follow-up spray tri- sampled for DBMs, and the seasonal average infes- al conducted in Florida in 1992 (Shelton et al. 1993b) tation per company ranged from 1.3 to 3.5 DBMs per indicated that both formulations provided <30% con- 100 transplants. One shipment in June, however, trol in the field. Another product, XenTari, contain- when the majority of transplants arrive, had 8.2 ing Bacillus thuringiensis subsp. aizawai with its DBMs per 100 transplants. In 1990, the seasonal additional Cry1C protein, provided 60% control. Since average infestation per company ranged from 1.8 to that time, however, populations resistant to Cry1C 12.0 DBMs per 100 plants, but one shipment had 17.4 also have been noted (Cao et al. 1999). DBMs per 100 plants. It was discovered that some Results from these early surveys indicated high lev- DBM populations on these transplants had RR val- els of resistance to some of the major insecticide class- ues >200 to methomyl and up to 20 to permethrin. es used at that time. The differences within states Thus it was concluded that the high levels of resis- and regions were assumed to be caused by practices tance observed in New York in the 1988 national sur- of individual growers. To examine this hypothesis vey likely were the result of bringing transplants into more carefully, it is worthwhile to discuss the devel- New York that were contaminated with resistant pop- opment of resistance in individual states. ulations of DBMs. Because of this, most New York growers have become far more cautious and demand- ing about the quality of transplants they use. Like- Examples of Resistance wise, there has been an effort in the transplant pro- Development in Individual States duction areas to use a more integrated approach to decrease DBM populations. Some practices that New York transplant growers can do include not locating trans- plant beds near production beds (a source of DBM The 1988 and 1990 surveys indicated that some of infestations), raising transplants in screened-in areas, the highest levels of resistance to commonly used in- and rotating insecticides to decrease resistance to any secticides occurred in New York. This was surpris- single insecticide. Another technique that seems to ing for several reasons. First, there may be only five work quite effectively is the use of better application to seven generations of DBMs in New York, far fewer techniques. A Maryland grower who had a seasonal than the approximately 20 generations that can be infestation of 3.5 DBMs in 1989 was able to lower it produced in warmer areas of the county. Hence, se- to 0.3 in 1990 and keep it < 0.5 per 100 transplants lection pressure for the development of resistance in 1991 and 1992 through improved scouting practic- should be far less in New York. Second, it is commonly es and switching from aerial to ground applications considered that DBM populations cannot survive the of an insecticide. cold winters of upstate and western New York, where the majority of cabbage is grown. Thus, even if a DBM population developed resistance within a single grow- Florida ing season, it would be eliminated during the winter Unlike in New York, populations of DBMs can oc- and not be present for the next year. Therefore, we cur throughout the year in Florida, and this ability hypothesized that resistant DBM populations may be increases the opportunity for resistance. The princi- moving into New York either through aerial move- pal insecticides used in Florida in the 1980s were ment of adults or through contaminated transplants. pyrethroids, but beginning in the mid-1980s growers Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 63 started to notice control failures (Leibee and Savage Maui, and Hawaii) between September 2000 and 1992). By the winter of 1986–1987, pyrethroids in April 2001 and examined in the laboratory using leaf- general provided no control of DBMs. A population dip assays (Zhao et al. 2002). Results from this study of DBMs collected from central Florida that was re- indicated that 6 of the 12 populations were highly sistant to fenvalerate also was resistant to methomyl tolerant to spinosad (TR >100-fold). Two populations (a carbamate) but susceptible to several organophos- resistant to spinosad also were examined for poten- phates, thiodicarb (a carbamate), and a Bacillus thu- tial cross resistance to emamectin benzoate (Proclaim) ringiensis (Bt) product. Once growers switched from and indoxacarb (Avaunt), two new insecticides from pyrethroids, intense use of the alternative insecticides novel classes. Fortunately, no cross-resistance was produced populations resistant to a number of differ- observed. A “postmortem” examination of the devel- ent products, including Bt. Beginning in the last 5 opment of resistance to spinosad was done to deter- years, growers have been able to use new insecticides mine what had caused resistance, and the following with novel modes of action, including spinosad (Spin- conclusions were drawn. Insecticide resistance man- Tor), emamectin benzoate (Proclaim), and indoxacarb agement (IRM) strategies had been incorporated into (Avaunt). These products seem to be the choice of the label for spinosad prior to its introduction. The growers at present, but there is a high likelihood of manufacturer recommended an IRM strategy that developing resistance to these materials if they are limited use to ≤3 applications in a 30-day period, fol- not used properly. lowed by at least 30 days of nonuse, and a maximum of 6 applications per crop. Such IRM restrictions prob- ably were helpful in maintaining spinosad suscepti- California bility in populations of DBM in most areas. In some During an outbreak of DBMs in California in 1997, areas of Hawaii, however, resistance developed de- nine populations of DBMs were collected from the spite labeled restrictions designed to prevent overuse. major broccoli areas throughout the state and assayed Although the guidelines may have been followed, they for their susceptibility to currently used materials did not take into account a more “regional” approach (Bacillus thuringiensis subsp. kurstaki, permethrin, for resistance management where as many as 50 ap- and methomyl). Elevated levels of resistance were plications per year might have been made to a com- seen only with permethrin, and seven of the nine pop- mon DBM population due to continuous sequential ulations had RR values >100 (Shelton et al. 2000). plantings on adjacent farms. Crucifers were planted These data indicate that resistance to at least one and harvested to meet fresh-market needs every week of the commonly used insecticides (permethrin) may of the year. have played a role in the outbreak during 1997. Oth- Spinosad was voluntarily removed from some ar- er factors may have been at least equally important, eas in Hawaii when control failures occurred. Fortu- however. The winter of 1996–1997 was warmer than nately, as resistance to spinosad was developing, Pro- normal, and during the period from February through claim and Avaunt became available. Since spinosad’s August of 1997, the amount of rainfall was <50% of removal from the market, continued monitoring has normal. Hot and dry conditions are known to be con- indicated a decline in resistance in many populations ducive to outbreaks of DBMs. in Hawaii, so it is gradually being reintroduced, and this will take some of the pressure off Proclaim and Avaunt (Mau, R. 2003. Personal communication). Hawaii Time will tell whether growers in Hawaii will be able In the mid-1990s in Hawaii, resistance in DBMs to develop a more durable IRM for DBMs. to all available insecticides was so severe that mar- ketable yields of crucifers were decreased, and cruci- fers were imported to supplement local production Transgenic Plants (Mau and Gusukuma-Minuto 2001). Spinosad was commercialized for pest control in crucifers in Hawaii Because DBMs are the only insects to have devel- in April 1998 and provided excellent initial control of oped resistance to Bt toxins in the field, it also has DBMs (Mau and Gusukuma-Minuto 1999). In some served an important role in helping to evaluate resis- areas in Hawaii, however, control failures became tance management strategies for transgenic plants evident in 2000. To examine whether these failures that produce Bt toxins. In greenhouse (Tang et al. were due to resistance, 12 populations of DBMs in 2001) and field trials (Shelton et al. 1999) the value total were established from three islands (Oahu, of a refuge for conserving susceptible alleles and the 64 3.4 Diamondback Moth Resistance in Crucifers importance of refuge placement within the system Literature Cited have been shown empirically. Likewise, field tests also examined the strategy of spraying the refuge Ankersmit, G. W. 1953. DDT resistance in Plutella to prevent economic loss to the crop while maintain- maculipennis (Curt.) (Lepidoptera) in Java. Bull ing susceptible alleles in the population. Results Entomol Res 44:421–425. indicate that great care must be taken to ensure that Cao, J., J. D. Tang, N. Strizhov, A. M. Shelton, and refuges, particularly those sprayed with efficacious E. D. Earle. 1999. Transgenic broccoli with high insecticides, produce adequate numbers of suscepti- levels of Bacillus thuringiensis Cry1C protein con- ble alleles. trol diamondback moth larvae resistant to Cry1A In addition to the currently available resistance or Cry1C. Mol Breed 5:131–141. management strategies for plants that express a sin- Cao, J., A. M. Shelton, and E. D. Earle. 2001. Gene gle Bt toxin at a high dose, plants also have been de- expression and insect resistance in transgenic broc- veloped plants that will only express Bt toxins when coli containing a Bacillus thuringiensis cry1Ab gene induced to do so, thereby creating a “within-plant” with the chemically inducible PR-1a promoter. Mol refuge until the plants need to be protected (Cao, Breed 8:207–216. Shelton, and Earle 2001). This strategy may be use- Food and Agricultural Organization of the United ful for crops in which the marketable portion is pro- Nations, Statistical Database. (FAOSTAT). 2003, duced during the latter half of the plant’s growth (e.g.,
Shelton, A. M., J. A. Wyman, N. L. Cushing, K. Apfel- beck, T. J. Dennehy, S. E. R. Mahr, and S. D. Eigen- brode. 1993a. Insecticide resistance of diamond- back moth in North America. J Econ Entomol 86:11–19. Shelton, A. M., J. L. Robertson, J. D. Tang, C. Perez, S. D. Eigenbrode, H. K. Preisler, W. T. Wilsey, and R. J. Cooley. 1993b. Resistance of diamondback moth to Bacillus thuringiensis subspecies in the field. J Econ Entomol 86:697–705. Shelton, A. M., M. K. Kroening, S. D. Eigenbrode, C. Petzoldt, M. P. Hoffmann, J. A Wyman, W. T. Wil- sey, R. J. Cooley, and L. H. Pedersen. 1996. Dia- mondback moth (Lepidoptera: Plutellidae) contam- ination of southern-grown cabbage transplants and the potential for insecticide resistance problems. J Entomol Sci 31:347–354. Shelton, A. M., J. D. Tang, R. T. Roush, T. D. Metz, and E. D. Earle. 1999. Field tests on managing re- sistance to Bt-engineered plants. Nature Biotech 18:339–342 Shelton, A. M., F. V. Sances, J. Hawley, J. D. Tang, M. Boune, D. Jungers, H. L. Collins, and J. Farias. 2000. Assessment of insecticide resistance after the outbreak of diamondback moth (Lepidoptera: Plu- tellidae) in California in 1997. J Econ Entomol 93:931–936. Talekar, N. T. and A. M. Shelton. 1993. Biology, ecol- ogy and management of the diamondback moth. Annu Rev Entomol 38:275–301. Tang, J. D., H. L. Collins, T. D. Metz, E. D. Earle, J. Zhao, R. T. Roush, and A. M. Shelton. 2001. Green- house tests on resistance management of Bt trans- genic plants using refuge strategies. J Econ Ento- mol 94:240–247. Xu, J., A. M. Shelton, and X. Cheng. 2001. Variation in susceptibility of Diadegma insulare to per- methrin. J Econ Entomol 94:541–546. Zhao, J. Z., Y. Li, H. L. Collins, L. Gusukuma-Minu- to, R. F. L. Mau, G.D. Thompson, and A. M. Shel- ton. 2002. Monitoring and characterization of di- amondback moth resistance to spinosad. J Econ Entomol 95:430–435. Zhao, J., J. Cao, Y. Li, H. L. Collins, R. T. Roush, E. D. Earle, and A. M. Shelton. 2003. Plants express- ing two Bacillus thuringiensis toxins delay insect resistance compared to single toxins used sequen- tially or in a mosaic. Nature Biotech 21:1493–1497. 66
3.5 Insect Resistance Management for Transgenic Bt Crops Graham P. Head
Introduction 1. Minimize the selection pressure for resistance. Insect resistance management (IRM) plans have This can be achieved by ensuring that a product been proactively implemented for all transgenic Ba- contains only a relatively low dose of the active cillus thuringiensis (Bt) crops that have been commer- ingredient or by limiting the use of the product cialized. Central to these IRM plans has been the two- in the field. The latter approach can occur uni- pronged strategy of expressing a highly effective dose formly by requiring a low-labeled use rate or het- of the insecticidal protein in all relevant plant tissues erogeneously by setting aside locations where the together with the provision of refuge areas for suscep- product will not be used at all (i.e., “refuges” for tible insects. These approaches have been combined susceptible individuals). with measurements of baseline susceptibility for the 2. Remove resistant alleles from the target pest pop- target pest species, routine and reactive monitoring ulation. In contrast to the first strategy, this ap- for resistance in the target species, integration of IRM proach typically involves using high enough dos- into existing pest management systems, intensive es of an insecticide to control heterozygous educational programs for farmers, and development resistant insects, thereby making resistance func- of subsequent generations of products with multiple tionally recessive. insecticidal proteins. For any particular Bt crop and 3. Use multiple selection mechanisms in combina- country, the specific implemented IRM practices have tion. This approach can work through mixing in- been carefully adapted to local needs, reflecting local secticides with different modes of action (or pyr- and regional differences in pest biology and agronomic amiding insecticidal genes in transgenic plants) practices. Differences in the size of structured refuge or rotating insecticides over time. required among crops and countries illustrate this process of local adaptation. The most important les- Because of a desire to ensure their durability, all son for the design of IRM plans has been the need to three approaches have been proactively applied in the balance technical considerations with the practical case of transgenic crops engineered with genes con- and economic needs of farmers. Because implemen- ferring protection against certain pest insect species tation of IRM practices by farmers is critical to the (so-called Bt crops). Subsequent sections discuss how success of IRM for Bt crops, farmers must be aware and why this has been done, and what lessons have of their responsibilities, understand the need for IRM, been learned in doing so. and regard the required IRM practices as logistically and economically feasible. This underscores the need for inclusion of such considerations in the design Relevant Characteristics phase of IRM plans and highlights the critical nature of Bt Crops of farmer education programs. With the development of genetic engineering tech- niques, it has become possible to achieve high, con- IRM Approaches stitutive, season-long expression of insecticidal pro- teins in certain crops. These techniques have been Insect resistance management aims to delay or pre- used in field corn and cotton (and, on a smaller scale, vent resistance development through appropriate in a number of other crops such as potatoes) to pro- product design and deployment. Three general IRM duce plants that are protected from a set of important approaches have been proposed and pursued over the lepidopteran pests. The proteins expressed are de- past three decades: rived from the common soil bacterium, Bacillus thu- ringiensis, and are crystalline endotoxins (hence
66 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 67 known as Cry Bt proteins). Because of the high, sea- 1. Establishing baseline measurements of Bt protein son-long levels of expression of the insecticidal pro- susceptibility for each target pest species prior to tein in each instance, it is recognized that high adop- widespread commercialization of the Bt crop. tion of these products without careful management This practice is the basis for future assessments could strongly select for resistance. This is one of the of resistance. reasons that IRM plans have been proactively imple- 2. Monitoring for resistant insects in populations of mented for all of these products. At the same time, the target pest species. This practice is based on the nature of Bt crops provides an opportunity to routine monitoring of pest populations in poten- employ IRM strategies that were not feasible for most tially high-risk areas, reactive monitoring for sus- conventional insecticides. First, the high expression pect populations, and broad monitoring of levels of Bt protein (much higher than can be achieved product performance. In all instances, the using Bt proteins in foliar sprays) mean that these baseline measurements are used for comparison products deliver a high dose of insecticide through- purposes. out the life of most of the target pest species. As not- 3. Using alternative insect control methods where ed previously, this helps to ensure that resistance will appropriate (including cultural, biological, and be functionally recessive. For example, the expres- chemical tools), as a part of fitting IRM practices sion of Cry1Ab protein achieved in all important tis- into existing integrated pest management sys- sues of a transgenic YieldGard corn plant exceeds the tems. LC99 of the primary target pest, the European corn 4. Targeting comprehensive educational programs borer (Ostrinia nubilalis), by several orders of mag- at farmers and other relevant stakeholders. nitude. Second, the defined in-plant distribution of 5. Developing subsequent products that express insecticidal protein makes it possible to manipulate multiple Bt proteins with different insecticidal how much of the pest population is exposed through properties. As described previously, the first such the creation of refuges. It also makes it possible to product already has been commercialized. combine multiple insecticidal genes and thus to ex- press multiple insecticidal proteins within a single plant. The first such product has just been commer- Adapting IRM for Bt Crops to cialized in the United States in the form of Bollgard Local Conditions II cotton, which expresses the Cry1Ac and Cry2Ab proteins for control of lepidopteran pests. Bt crops have been commercialized at a global lev- el, with the use of both Bt corn and Bt cotton in North and South America, Asia, and Africa; and Bt corn in IRM for Bt Crops Europe. A critical piece of this effort has been to develop locally appropriate IRM plans for each prod- The basic IRM strategy employed for all Bt crops uct in each country involved. In doing so, local, crop- thus far commercialized builds upon the opportuni- specific aspects of target pest biology, agronomic prac- ties provided by the nature of Bt crops themselves. tices, and grower behavior have been taken into The two-pronged strategy involves expressing a high- account. Where resistance risks are higher because ly effective dose of insecticidal protein throughout the of aspects of pest biology and the nature of agronom- transgenic plant to make resistance functionally re- ic practices, more conservative IRM practices may cessive where possible, together with ensuring that be needed. Conversely, where resistance risks are refuge areas are provided for susceptible pest insects. inherently low because of these same factors, IRM The many susceptible insects coming from the refuge practices can be adapted accordingly. Similarly, IRM areas can mate with the few resistant insects surviv- practices must fit with local grower needs and ing on the Bt crop, thus diluting out the resistant al- agricultural practices. leles in the pest population. Note that the refuge need An illustration of this local adaptation can be seen not be something specifically planted by a farmer for in the specific details of the refuge strategy used with that purpose (a structured refuge); the refuge can con- different crops in different countries, and even for a sist of nontransgenic plants of any species that can given crop in different regions of the same country. be used as a host by the target insects. For example, in the United States, Bt corn has a re- This is not the full extent of IRM for Bt crops, how- quired refuge size of 20% in the main Corn Belt, but ever; other complementary practices also are em- a 50% refuge is required in southern cotton-growing ployed. These practices include the following: areas. In both instances, these refuges can be 68 3.5 Insect Resistance Management for Transgenic Bt Crops treated as needed for lepidopteran pest species. The as well as because of chance environmental factors larger refuge size for Bt corn in cotton-growing areas that constrain farmers’ options at any given time. reflects the additional selection pressure for Bt resis- Consequently IRM practices must be flexible, and tance exerted by the use of Bt cotton in these areas. IRM plans should include multiple options that are In contrast to the requirements for Bt corn, Bt cotton adapted to different systems. This local adaptation in the United States requires either a 20% refuge that of IRM practices for practical reasons complements may be treated with insecticides (comparable to the the local adaptation that occurs for technical reasons Bt corn option in the main Corn Belt) or a 5% refuge (see the earlier discussion of differences in refuge size that cannot be treated for the target lepidopteran in different countries). pests of Bt cotton. The unsprayed refuge option is Third and equally important, it must be recognized included because cotton farmers in some regions of the that the IRM practices required for Bt crops are cost- United States need a high adoption option for econom- ly for farmers, in terms of both money and time (the ic reasons, and because few alternative control meth- opportunity cost of the practices). This issue can be ods are available for the target pests. In Argentina, addressed partially by ensuring that IRM practices Bt corn requires a 10% refuge that may be treated are sufficiently adapted to existing agricultural sys- with insecticides. The smaller refuge size in Argen- tems to be simple and inexpensive for farmers to im- tina relative to the United States is based on appar- plement. Educational programs also are critical in ently lower resistance risks for the target pests, pri- this respect. marily because of their broad host range. This More generally, the design of IRM plans must bal- situation is seen in a more extreme form in countries ance the technical need to mitigate the risk of resis- such as China with many small-holder farmers. In tance development with the practical and economic China, farmers are not required to plant any struc- needs of growers. The former dictates that IRM plans tured refuge in association with their Bt cotton be- must have a strong scientific base to be effective. They cause alternative host crops of the key target pest, the also must be flexible over time because scientific Old World bollworm (Helicoverpa armigera), provide knowledge is continually increasing. These technical a substantial source of refuge for Bt cotton. considerations, however, cannot be so rigidly applied that they limit the availability of the product to farm- ers. If farmers regard IRM practices as impractical Lessons Learned about How to or unaffordable, they may choose not to use the prod- Make IRM Successful uct, and both they and society lose the benefits that product adoption could have brought. Alternatively, Seven years of experience with corn and cotton farmers simply may not implement the IRM practic- farmers in the United States, and comparable es and the durability of the product will suffer. Thus amounts of experience in countries as diverse as Ar- carefully balancing the various factors involved in gentina, Australia, and China, have provided valuable IRM is the key to developing effective and implement- lessons on what sorts of IRM strategies can be effec- able IRM plans. tive technically and implemented successfully. First and foremost has been the recognition of the importance of farmers in making IRM successful. Be- cause the IRM plans associated with Bt crops require a variety of actions on the part of farmers, such as planting refuges, farmers must be aware of their re- sponsibilities, they must understand the need for IRM, and they must regard the IRM practices that are required of them as logistically and economically fea- sible. This highlights the need for consistent and ef- fective educational programs and illustrates why the needs of farmers must be considered in the design of IRM plans. Second, but related to the first point, IRM plans must take into account the local and regional varia- tion present in farming practices. Farming practices vary because of differences in agricultural systems, Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 69
4.1 What Have Insect Resistance Management Models Taught Us? Nicholas P. Storer
Introduction egies for transgenic insecticidal crops (Bacillus thur- ingiensis [Bt] corn and Bt cotton) in the United States As with all models, insect resistance management and Australia. The models have helped to provide an (IRM) models can be constructed with varying degrees understanding, for example, of the “high-dose + ref- of complexity. At one extreme, grossly simplified uge” strategy, and the conditions upon which the ef- models can provide overly simplistic answers that fectiveness depends (Gould 1998). It has been learned may not provide useful insight into the processes af- that larger refugia and higher doses give longer du- fecting resistance evolution in the field. At the oppo- rability (Roush 1997), and that deployment of two in- site extreme, overly complex models that aim to sim- secticidal traits in a stack can extend significantly the ulate the real world are very costly and require durability of each (Gould 1986; Roush 1997). significant knowledge of the system being modeled. Interpretation of such models in order to draw useful conclusions can be very difficult. The literature pro- Adding Complexity—Spatial vides a wide range of examples between these two and Stochastic Processes extremes. Simple models tend to be descriptive and deterministic, exclude population dynamics, handle The simpler models mentioned previously are very spatial processes only in abstract ways, and simulate generalized and have lent themselves to additional a fixed environment (e.g., Roush 1989). More com- development to better understand the underlying plex models account for population dynamics and processes. For example, one of the conditions that migration between patches (e.g., Caprio 2001; Comins favors the effectiveness of the high-dose + refuge ap- 1977; Georghiou and Taylor 1977a,b). The most com- proach is that there is random mating among insects plex models are more mechanistic, integrate system- produced from the refuge and from the transgenic specific processes, and can incorporate stochasticity, crop. In order to understand how the real world im- model spatial relationships more explicitly, and even pacts this condition, it is necessary to examine the account for variable environments (e.g., Onstad and effect of the spatial distribution of refugia and trans- Gould 1998; Onstad et al. 2001; Peck, Gould, and Ell- genic fields, and how the insects move among the dif- ner 1999; Storer et al. 2003). Proponents of the sim- ferent patches. ple approach cite the broad applicability and gener- Several models have suggested that high levels of ality of the results and the ability to produce dispersal between patches can accelerate the spread analytical solutions to specific questions. Proponents of resistance, whereas very low levels of dispersal can of the complex models cite their utility in understand- allow localized foci of resistance to develop (Caprio ing more fully the unique aspects of any insect resis- and Tabashnik 1992; Mallet and Porter 1992; Peck, tance evolutionary system. The easy access to pow- Gould, and Ellner 1999). By further accounting for erful computers enables mechanistic simulation stochasticity in models, Peck, Gould, and Ellner models to be more common. (1999) showed that the balance between dispersal pre- venting the buildup of foci of resistance and the dis- persal allowing resistant populations to spread can Some Learning from Simple depend critically on random factors, such as patch Models distribution and local population size. Indeed, Peck, Gould, and Ellner (1999) showed that there are sev- Simple models, beginning with Comins (1977), eral scenarios in which extinction of a resistance al- have taught some very important principles of resis- lele in the tobacco budworm, Heliothis virescens, is tance management. Such lessons have led to the de- more likely than its spread in the face of intense se- velopment and widespread deployment of IRM strat- lection pressure from Bt cotton.
69 70 4.1 What Have Insect Resistance Management Models Taught Us?
Handling Uncertainty levels of technology adoption (e.g., Storer et al. 2003). Such models provide insight into pest adaptation to One criticism often leveled at IRM models, espe- competing technologies, such as different rootworm- cially as they become more complex and system-spe- resistance traits in maize (N. Storer, unpublished cific, is that there is uncertainty around the process- data). This analysis leads to an improved understand- es and parameters included in the model. Many of ing of the way pest adaptation occurs in complex en- these are naturally highly variable (such as nonspe- vironments, improved understanding of the need to cific mortality, weather, dispersal patterns) or not manage resistance, and improved understanding of predictable with accuracy (such as grower adoption). the effectiveness of different IRM strategies. It is therefore very important to interpret the output Although models generally have been used to ex- of IRM models with this uncertainty in mind. Insect amine proactive resistance management strategies, resistance management models generally provide a they also have been used to design effective reactive prediction of the change in frequency of resistance al- strategies once resistance has appeared (Sisterson, M. leles over time, and the results often are expressed 2001. Personal communication). Much of the uncer- as the number of years until some frequency of the tainty in assumptions and parameter values can be alleles is reached. As the actual rate is unpredictable resolved once resistance occurs, such as the fitness of due to the process and parameter uncertainties, such heterozygous- and homozygous-resistant insects on output should be considered in relative terms. Storer different crops, cross-resistance (or negative cross- (2003) expresses model output as rate of adaptation resistance) to other control technologies, and the num- relative to a standard benchmark. For example, a rel- ber of genes involved. The models, therefore, can be ative adaptation rate of 2 means that adaptation is regarded as being more predictive in absolute terms expected to occur at twice the rate of, or in half the (although considerable uncertainty will remain). time of, the benchmark. This output variable there- Options for reactive plans generally consist of easing fore allows direct comparison of the effect of different the selection pressure across the affected area and IRM practices or different circumstances on the du- may include additional measures designed to impact rability of an insect-control tool. resistant genotypes differentially over susceptible genotypes. Spatially explicit models can provide use- ful indications of the area over which such actions Applications of Spatial Models should be taken, and provide predictions of the time until reversion to susceptibility under different reme- Storer (2003) provides an example using a model dial action plans. simulating adaptation to rootworm-protected maize. This model predicts that if the refuge is held in the same location each year then the durability of the root- Conclusions worm-protected maize is many-fold longer than if the refuge locations are random each year (thus usually `Insect resistance management models by defini- on land that was planted to the rootworm-protected tion represent a simplified reality and often fail to ac- crop the year before). This results from the fixed ref- count for all the uncertainties inherent in evolution- uge supporting large populations of susceptible root- ary genetics. Therefore, care must be taken in worms over many years, increasing the effectiveness interpreting them for real-world applications. There of the refuge. Such a finding can be used to improve is uncertainty in the future agricultural environment, the design of refuge-based IRM programs for root- uncertainty in the value of input parameters, and worm transgenics, and would not be evident from a uncertainty that all relevant processes have been ac- simple, nonspatial model. counted for. Furthermore, IRM models are difficult These more complex spatially explicit models en- to validate. The models make predictions over many able additional questions to be addressed. They can years, even decades. If a model’s predictions were to be used to investigate the effect of different farmers coincide with actuality, there would be little certain- employing different pest-control tactics on the rate of ty that the actual events resulted from the processes adaptation to any one tactic. For example, they can exactly as modeled. Alternatively, if actuality fails be used to examine the effect of a patchy distribution to follow predictions, there would be uncertainty as of Bt crops and non-Bt crops on the spatial distribu- to whether the model processes, assumptions, or pa- tion of resistance alleles through time and help to un- rameter values caused the discrepancy. Partial vali- derstand the effect of a structured refuge at different dation can be possible, for example, by comparing Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 71 predictions of pest population dynamics in the absence Georghiou, G. P. and C. E. Taylor. 1977a. Genetic and of or the presence of the insecticidal technology. biological influences in the evolution of insecticide For several important pests there are additionally resistance. J Econ Entomol 70:319–323. documented historical instances of resistance that can Georghiou, G. P. and C. E. Taylor. 1977b. Operation- be compared with model predictions. al influences in the evolution of insecticide resis- The cautious approach to the application of results tance. J Econ Entomol 70:653–658. of computer models to the real world is similar to that Gould, F. 1986. Simulation models for predicting for the laboratory (e.g., with Plodia interpunctella durability of insect-resistant germplasm: Hessian described in Roush 1994), greenhouse (e.g., with Plu- fly (Dipter: Cecidomyiidae)-resistant winter wheat. tella xylostella by Tang et al. 2001), or small-scale field Environ Entomol 15:11–23. experiments (e.g., with P. xylostella by Shelton et al. Gould, F. 1998. Sustainability of transgenic insecti- 2000). Each of these environments provides insight cidal cultivars: Integrating pest genetics and ecol- into natural processes, under controlled conditions, ogy. Annu Rev Entomol 43:701–726. and therefore provides a valid forum for investigat- Mallet, J. and P. Porter. 1992. Preventing insect ad- ing IRM strategies. Physical experiments, however, aptation to insect resistant crops: Are seed mix- are necessarily limited by the size of the test arena, tures or refugia the best strategy. Proc R Soc Lon- by the number of different selection regimes that can don Ser B 250:165–169. be tested, and usually by the duration of the grant/ Onstad, D. W. and F. Gould. 1998. Modeling the dy- publication cycle. Full field experiments on IRM are namics of adaptation to transgenic maize by Euro- impractical, as the necessary control treatments will pean corn borer (Lepidoptera: Pyralidae). J Econ be designed to create the very problem that IRM is Entomol 91:585–593. designed to avoid. Cyberspace provides the only suit- Onstad, D. W., C. A. Guse, J. L. Spencer, E. Levine, able environment to perform long-term, large-scale and M. E. Gray. 2001. Modeling the dynamics of IRM experiments testing multiple IRM strategies adaptation to transgenic corn by western corn root- under multiple sets of assumptions. worm (Coleoptera: Chrysomelidae). J Econ Ento- Interpreting model output as relative predictions mol 94:529–540. helps to account for much of the uncertainty and al- Peck, S. L., F. Gould, and S. P. Ellner. 1999. Spread lows the true value of the models to be revealed. The of resistance in spatially-extended regions of trans- models enable IRM practitioners to improve their genic cotton: Implications for management of He- understanding of a pest/crop/geography system. liothis virescens (Lepidoptera: Noctuidae). J Econ Through sensitivity analysis, models enable IRM re- Entomol 92:1–16. searchers to focus their resources on understanding Roush, R. T. 1989. Designing resistance management those processes that have the largest effects on resis- programs: How can you choose? Pestic Sci 26:423– tance evolution. Insect resistance management mod- 441. els enable objective evaluation of IRM strategies that Roush, R. T. 1994. Managing pests and their resis- minimize the risk of pest adaptation while maximiz- tance to Bacillus thuringiensis: Can transgenic ing the benefits of the pest control technology. crops be better than sprays? Biocontrol Sci Tech 4:501–516. Roush, R. T. 1997. Managing resistance to transgen- Literature Cited ic crops. Pp. 271–294. In N. Carozzi and M. Ko- ziel (eds.). Advances in Insect Control: The Role of Caprio, M. A. 2001. Source-sink dynamics between Transgenic Plants. Taylor and Francis, London. transgenic and non-transgenic habitats and their Shelton, A. M., J. D. Tang, R. T. Roush, T. D. Metz, role in the evolution of resistance. J Econ Entomol and E. D. Earle. 2000. Field tests on managing 94:698–705. resistance to Bt-engineered plants. Nature Biotech- Caprio, M. A. and B. E. Tabashnik. 1992. Gene flow nol 18:339–342. accelerates local adaptation among finite popula- Storer, N. P. 2003. A spatially-explicit model simu- tions: Simulating the evolution of insecticide resis- lating Western corn rootworm (Coleoptera: Chry- tance. J Econ Entomol 85:611–620. somelidae) adaptation to insect resistant maize. J Comins, H. N. 1977. The development of insecticide Econ Entomol 96:1530–1547. resistance in the presence of migration. J Theor Biol 64:177–197. 72 4.1 What Have Insect Resistance Management Models Taught Us?
Storer, N. P., S. L. Peck, F. Gould, J. W. Van Duyn, and G. G. Kennedy. 2003. Spatial processes in the evolution of resistance in Helicoverpa zea (Lepi- doptera: Noctuidae) to Bt transgenic corn and cot- ton in a mixed agroecosystem: A biology-rich sto- chastic simulation model. J Econ Entomol 96:156–172. Tang, J. D., H. L. Collins, T. D. Metz, E. D. Earle, J. Z. Zhao, R. T. Roush, and A. M. Shelton. 2001. Greenhouse tests on resistance management of Bt transgenic plants using refuge strategies. J Econ Entomol 94:240–247. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 73
4.2 Resistance Management Strategies: Have Models Helped? Richard Roush
Introduction application rates) are more effective than low doses, and that pesticide mixtures are more effective than “Ignorance ain’t what you don’t know, it’s what you do rotations. Although mixtures and high doses can be know that ain’t correct.” the more effective strategies in certain special cases, —Will Rogers, American humorist they generally are not so. Indeed, experiments on these ideas have given results that are inconclusive Resistance management is a scientifically and with respect to general rules in managing resistance, practically vexing problem in pest management. As and the models have explained why (e.g., Roush 1994, scientists, we prefer to test ideas with experiments be- 1997a,b, 1998). fore making recommendations on management, but Space limitations prohibit a detailed explanation long-range movement of pests and diseases, and the of these conclusions. Instead, the aim here is to pro- time frames required for any meaningful results, vide a summary and to point readers to other papers makes it very difficult and costly to conduct convinc- that provide more detail and lead to the primary lit- ing experiments on resistance management. Due to erature. pest and disease dispersal, however, realistic field ex- periments for some of the most vexing pests for resis- tance management would require tens of square ki- High Doses Versus Low Doses: lometers. Couple this with the need to maintain the The Importance of Heterozygotes experiments for at least 4 to 7 years (about the mini- mum time for resistance in many key pests and It was once a popular idea that low application weeds), not to mention the ethical issues of including rates could be good for managing resistance because treatments expected to generate resistance faster they would allow some susceptible individuals to sur- than the alternatives being tried (Tabashnik 1986), vive. Simple arithmetic and simulation models, how- and the prospects of proving through experiments ever, show that one must allow a large proportion (10– about how to manage resistance are dim. 20%) of the treated individuals to survive if resistance Still, even in the absence of experiments that gen- is to be delayed significantly. In general, this would erally can be accepted as informative, decisions about be impractical because it can allow too much damage the deployment of pesticides and transgenic crops to occur (Curtis 1985). One can illustrate this by us- must be made, especially by regulators. On the basis ing the dose response data for Bacillus thuringiensis of history, it can be asserted that resistance will (Bt) resistance in the diamondback moth to set the fit- evolve, generally far too rapidly, if proactive steps are ness at each dose to be considered (Roush 1994). For not taken to slow it down. As a consequence of this example, a dose of 1 part per million (ppm) kills 95% reality, and not with any joy, scientists have let math- of susceptible individuals and approximately 70% of ematical models assume a critical role. At the very heterozygotes (Roush 2003; Tang et al. 1997). least, by forcing a precise statement of assumptions On the other hand, another popular idea is that use and the mathematical implications thereof, models of high doses generally will delay resistance. With the have played an essential role in building a conceptu- high-dose approach, resistance could be delayed in al framework for resistance. theory because the great majority of resistant het- Especially during the last 15 years, this framework erozygotes (carrying one R and one S allele), the most has revealed clearly the condition described by Will common carriers of resistance, and perhaps even Rogers. Much of what is commonly believed about many resistant homozygotes are killed by the dose of resistance management simply is not supported by toxin used. The survivors are so rare that the over- the logical analysis forced by the models. This in- whelming majority will mate with susceptible ho- cludes “urban myths” such as that high doses (or mozygotes that escaped treatment and thereby
73 74 4.2 Resistance Management Strategies: Have Models Helped? produce heterozygous (effectively susceptible) off- Two Toxins: Mosaics, Rotations, spring. As clearly demonstrated in modeling by Tabashnik and Croft (1982), however, the doses need- and Mixtures ed often must be very high and yet cannot interfere with the successful mating of resistant survivors of Another choice often faced in resistance manage- the treatment with susceptible immigrants. Further, ment arises when there is more than one pesticide or the resistance frequencies must be low, so the strate- toxin that can be used. Historically, the introduction gy cannot be very effective if not adopted before re- of new pesticides has been uncoordinated and gener- sistance is first observed. In fact, the doses needed ally is driven by market considerations. This means must kill approximately 95% of the heterozygotes to that insecticides have been used in haphazard mosa- delay resistance significantly (Roush 1989, 1994, ics in which neighboring crops carrying interbreed- 1997a,b, 2003). These conditions rarely are met for ing populations of pests are treated with a few differ- insecticides. Worse, high doses generally destroy bi- ent pesticides. Models (Roush 1989) and experiments ological control agents needed in integrated manage- (Roush 1993, 2003), however, show that mosaics never ment programs for insects and mites (Roush 1989; are better and often are worse than rotations. Tabashnik and Croft 1982). It seems widely believed that mixtures of pesticides Given the high resistance levels found in heterozy- or toxins generally will or nearly always will delay gous herbicide-resistant weeds, it also seems unlike- resistance better than using them individually in se- ly that high doses will help for herbicides, nor have quences or rotations. This is not supported by exper- experiments shown a consistent advantage for fungi- iments (Tabashnik 1989) or by models (Comins 1986; cides (Brent 1995). It is conceivable that higher dos- Gould 1986b). In contrast to the high-dose strategy, es may help somewhat for cases of polygenic resis- in which heterozygotes are controlled by applying tance, as may be true for fungicides. enough of a single pesticide, the mixture strategy re- High expression of toxins looks promising for Bt lies on a second pesticide to control the individuals transgenic crops (Roush 1994, 1997a,b), however, il- heterozygous for resistance. This means that each lustrating how models identify the key assumptions of the toxicants must be used at doses that effective- that drive the success of one strategy or another. The ly kill completely susceptible individuals twice, which models also show the importance of effective refuges has been called “redundant killing” (Comins 1986; to provide susceptible insects to mate with any sur- Gould 1986a). As with the high-dose strategy, how- vivors of the transgenic plants. This is consistent with ever, mixtures are effective only if the mortalities of the longer history of resistance management (e.g., susceptible insects are very high (>95%) when exposed Roush and Croft 1986; Tabashnik and Croft 1985). to each individual toxicant. Even then, resistance to Recent experiments also have supported the use of at least one of the pesticides must be somewhat re- refuges specifically for Bt crops (Liu and Tabashnik cessive for resistance to be significantly delayed 1997; Shelton et al. 2000; Tang et al. 2001). (Gould 1986b; Mani 1985; Roush 1989, 1997a,b, 1998, Models developed for addressing this debate also 2003). Mixtures of insecticides are not promising due illustrate the factors that are critical to the evolution to incomplete coverage of the treated habitat (i.e., of resistance. The reason the high-dose strategy at- very few pesticides provide even 95% control) and res- tracted such attention even in the late 1970s (see idue decay (as pesticides break down, susceptible Tabashnik and Croft 1982) reflects the fact that sim- pests that have dispersed into the habitat or emerged ulation models clearly demonstrated the critical im- from protected sites will not always be killed). portance of the survival of heterozygotes to the rate Again, running a few numbers in models shows of selection. A twofold increase in mortality of het- that what seems a good idea does not stand up; it is erozygotes from 50% to 100% can mean more than a the rigor of the model that exposes the weaknesses of fivefold increase in the number of generations to re- the mixture strategy, which otherwise seems intu- sistance. By contrast, even a 100-fold difference in itively appealing. As with Bt crops and the high-dose the initial frequency of the resistance allele general- strategy, however, the same kinds of models suggest ly makes less than a fivefold difference in the time to that pyramiding two Bt toxins in the same plants can resistance (Roush 1997a,b). Given that the survival be effective in managing resistance, because the key of heterozygotes cannot be measured until resistance assumptions are more likely to be met (Roush 1998). in the pest has evolved somewhere, this is a key fac- Similarly, although pyramiding classical host plant tor that limits the ability of the models to make some resistance factors generally may not provide much predictions. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 75 advantage (Gould 1986a), in the specific case of the Brent, K. J. 1995. Fungicide Resistance in Crop Patho- Hessian fly, the available data suggest that pyramid- gens: How Can It Be Managed? Fungicide Resis- ing would be very effective (Gould 1986b). tance Action Committee, Monograph No. 1. Inter- national Group of National Associations of Manufacturers of Agrochemical Products, Brussels, Validation Belgium. Carriere, Y., C. Ellers-Kirk, M. Sisterson, L. Antil- Although it is very difficult to test these models la, M. Whitlow, T. J. Dennehy, and B. E. Tabash- explicitly, many of the models’ predictions, such as the nik. 2003. Long-term regional suppression of pink importance of refuges and problems with mosaics, bollworm by Bacillus thuringiensis cotton. Proc have been tested, as discussed in this paper. Other Natl Acad Sci, USA 100:1519–1523. predictions also have been met, at least in terms of Comins, H. 1986. Tactics for resistance management population dynamics. For example, predictions of a using multiple pesticides. Agric, Ecosyst, Environ “halo” of low pest density in nontransgenic crops near 16:129–148. Bt crops have been met in the field (Andow and Hutch- Curtis, C. F. 1985. Theoretical models of the use of ison 1998). Roush (1997b, Fig. 9) predicted that re- insecticide mixtures for the management of resis- sistance in the pink bollworm to Bt cotton in Arizona tance. Bull Entomol Res 75:259–265. would take at least 20 generations to evolve, even if Gould, F. 1986a. Simulation models for predicting the proportion of nontransgenic cotton was only 20%, durability of insect-resistant germplasm: A deter- but that the population of pink bollworm would be- ministic diploid, two locus model. Environ Ento- gin to decline because it would be unable to replace mol 15:1–10. itself. In fact, pink bollworm populations have begun Gould, F. 1986b. Simulation models for predicting to decline after adoption of approximately 65% Bt cot- durability of insect-resistant germplasm: Hessian ton, and still there are no resistance problems after fly (Diptera: Cecidomyiidae)-resistant winter approximately 24 generations (6 years) of use (Carri- wheat. Environ Entomol 15:11–23. ere et al. 2003). Liu, Y. B. and B. E. Tabashnik. 1997. Experimental Have models helped in managing resistance? They evidence that refuges delay insect adaptation to Ba- certainly have, by informing the decision-making pro- cillus thuringiensis toxin Cry1C in diamondback cess when no other means were available. Models moth. Appl Environ Microbiol 63:2218–2223. clearly help to compare different strategies under the Mani, G. S. 1985. Evolution of resistance in the pres- same range of conditions and thereby to identify ence of two insecticides. Genetics 109:761–783. which strategies are likely to be most effective across Roush, R. T. 1989. Designing resistance management any set of assumptions. Models also can identify programs: How can you choose? Pestic Sci 26:423– which features about the genetics, ecology, and man- 441. agement of resistance are most likely to be most im- Roush, R. T. 1993. Occurrence, genetics and manage- portant, and have played a key role in regulatory de- ment of insecticide resistance. Parasitol Today cisions. Scientists need to continue testing their 9:174–179. intuition with the models and the models with exper- Roush, R. T. 1994. Managing pests and their resis- iments. Otherwise they run the risk of repeatedly tance to Bacillus thuringiensis: Can transgenic acting out the mistake articulated by Will Rogers. crops be better than sprays? Biocontrol Sci Tech- What is today’s ignorance? What do we actually nol 4:501–516. “know”? These are the continuing challenges for re- Roush, R. T. 1997a. Bt-transgenic crops: Just anoth- sistance modeling. er pretty insecticide or a chance for a new start in resistance management? Pestic Sci 51:328–334. Roush, R. T. 1997b. Managing resistance to trans- Literature Cited genic crops. Pp. 271–294. In N. Carozzi and M. Ko- ziel (eds.). Advances in Insect Control: The Role of Andow, D. A. and W. D. Hutchison. 1998. Bt-corn Transgenic Plants. Taylor and Francis, London. resistance management. Pp. 19–66. In M. Mellon Roush, R. T. 1998. Two toxin strategies for manage- and J. Rissler (eds.). Now or Never: Serious New ment of insecticidal transgenic crops: Can pyramid- Plans to Save a Natural Pest Control. Union of ing succeed where pesticide mixtures have not? Concerned Scientists, Cambridge, Massachusetts. Philosoph Trans R Soc London, Ser B, Biol Sci 149 pp. 353:1777–1786. 76 4.2 Resistance Management Strategies: Have Models Helped?
Roush, R. T. 2003. Resistance management strategies: Have models helped? CAST Pest Resistance Management Symposium: Management of Pest Re- sistance: Strategies Using Crop Management, Bio- technology, and Pesticides, Indianapolis, Indiana, April 10–11, 2003,
4.3 Herbicide Resistance Models: Have They Helped?
Carol Mallory-Smith
The first model to predict the occurrence of herbi- (1990) included gene flow and population dynamic cide resistance was published by Gressel and Segel aspects. Other models have addressed specific weed in 1978. This model, which was fairly simplistic, in- species, herbicide classes, or the impact of herbicide- cluded the parameters of mutation rate, selection resistant crops on the system (Cavan, Cussans, and pressure, fitness, and seedbank. The authors drew Moss 2001; Diggle and Neve 2001; Hanson, Ball, and from the information available about resistance to Mallory-Smith 2002; Shaner, Feist, and Retzinger other pesticides and heavy metals. The model was de- 1997). veloped nearly 10 years after the first report of a her- bicide-resistant weed (Ryan 1970). The authors con- tended that resistance would be an infrequent event Predictive Role of Models in part because there were few herbicides with high enough selection pressure or persistence. They also With or without models, it still would be predicted suggested that the resistant weed biotype would be that the herbicide that exerted the highest selection less fit than the susceptible biotype and so would be pressure would be at risk to select a herbicide-resis- less competitive when the herbicide was not used and tant biotype. Selection pressure includes the effica- the buffering capacity of the soil seedbank would cy of the herbicide combined with the number of ap- maintain susceptibility in the population. In 1978, plications. It would be predicted that the most data about herbicide resistant weeds were limited, sensitive weed species would be the most likely to and the only major resistance reported was resistance evolve resistance. to the triazine herbicides. The models are descriptive of what had happened It should be noted that although there are analo- but have not been particularly effective in resistance gous features among insects, diseases, and plants, the prevention or management. It still is not possible to differences are so great that one should be cautious predict when or where resistance will occur or why in transferring predictions or recommendations from one species and not another will develop resistance. one system to another. If some of the differences are High- and low-risk herbicides have been identified, evaluated, it is apparent why caution is needed. after the fact. Plants are stationary, although pollen and seed do move. A refuge would not have the same impact for How Models Were Used to weeds as it does for insects. The highest degree of cross-pollination occurs between adjacent plants, so Identify Data Gaps there would not be enough movement of susceptible All of the models contain common parameters. The genes into the population to maintain susceptibility. models made it very apparent that there were data In most cases, the generation time for weeds is much gaps related to predicting the occurrence of herbicide longer than for insects or microbes. The most signif- resistance in a weed species or to a specific herbicide. icant difference is that there is not the dissimilarity In order for the models to be accurate, better data between the host and the pest that exists with insects were needed. The models also raised questions about and microbes. When herbicides are applied, the goal the assumptions included in the models. Research- is to kill one plant, the weed, and not injure the other ers have addressed components of the models, but still plant, the crop. there are major data gaps 25 years later. In part this In the ensuing 25 years since the Gressel and Seg- is due to the long-term nature of the studies that el model (1978) was published, several other theoret- would be needed and the cost of conducting the stud- ical models have been created. These models includ- ies. It also is because there are no experimental meth- ed more parameters or were more specific. The model ods to determine some of the parameters such as constructed by Maxwell, Roush, and Radosevich mutation rate.
77 78 4.3 Herbicide Resistance Models: Have They Helped?
• Mutation rate. Mutation rates for resistance that mutations for certain resistance alleles are are unknown and are theoretical, so any number more common than others, but the actual rate still included in a model is highly suspect. The fact is unknown. Mutations for resistance to the that resistance appears in some populations of a acetolactate synthase (ALS) inhibitors are species but not in other populations of the same frequent, and multiple mutations occur that pro- species at other sites raises the question of how vide resistance to these herbicides. Mutation mutations for resistance arise. rates for other herbicides such as glyphosate and • Mode of inheritance. The models assumed that 2,4-D are lower. the trait would be a single gene and nuclear-en- • Mode of inheritance. Caution should be taken coded trait. Polyploidy was not considered in the with interpretation of inheritance data because models. A limited number of studies have been the number of studies on inheritance is limited. conducted to determine the mode of inheritance Polygenic resistance has not been documented but of herbicide resistance. is expected to be responsible for multiple resis- • Fitness. It was assumed that there would have tance that is metabolism based. Most often re- to be a cost associated with resistance, and that sistance has been due to mutations in a single the resistant biotypes would be less fit. There has nuclear-encoded gene (Jasieniuk, Brule-Babel, been, and still is, a great deal of debate over how and Morrison 1996). Resistance to the sulfony- fitness should be evaluated and which parame- lurea and imidazolinone herbicides has been re- ters should be measured. Some researchers have ported to be a single, nuclear-encoded dominant argued that in order to get an accurate measure- or semidominant trait. There is only one report ment isogenic lines must be used, and that the of resistance as a recessive trait. Resistance to studies must be conducted under typical field con- the triazines is maternally inherited, so the trait ditions (Jasieniuk, Brule-Babel, and Morrison does not move in with pollen. 1996). By the time a resistant population is iden- • Fitness. In the absence of the herbicide, fitness tified, it often is difficult to find a susceptible plant and competitive differences between resistant and in the same population. It could be argued just susceptible biotypes have been compared. The as logically that weed populations are diverse so only consistent differences have been measured multiple biotypes of both resistant and suscepti- between triazine-susceptible and triazine-resis- ble plants should be used. In addition, “typical tant biotypes. In most studies for the parameters field conditions” do not exist; environmental con- measured, the triazine-susceptible biotype was ditions differ every year. more fit than the triazine-resistant biotype. Neg- • Gene migration. Gene migration through seed ative consequences for resistance to other herbi- or pollen movement was included in the Maxwell, cides have not been shown. Roush, and Radosevich (1990) model. The au- • Gene migration. Field data still are not avail- thors contended that a susceptible gene migration able for gene migration. None of the models in- from a susceptible population would slow resis- cluded prediction of movement of resistance from tance. Jasieniuk, Brule-Babel, and Morrison one site to another. Research in gene migration (1996) concluded that gene migration from a sus- has increased not to determine the influence that ceptible population to a resistant population susceptible plants could have on the decrease of would not slow the occurrence of resistance. resistance in weeds but because of the question of gene flow from herbicide-resistant crops into weedy and native species. Pollen movement will Uncertainty Associated with be responsible for short-distance movement of a Various Parameters trait, and seed movement has the potential for short- or long-distance movement, depending on Even though there has been considerable research the dispersal mechanism. on herbicide-resistant weeds, there is still a great deal • Selection pressure. Selection pressure for most of uncertainty associated with various parameters. herbicides can be estimated. Efficacy data are col- Data gaps still exist, and weed scientists continue to lected over a wide range of environments and for debate the parameters and their importance. many weed species. A national data base contain- ing this information would be useful for predict- • Mutation rate. Mutation rates are unknown, ing which species might be most likely to evolve and mutations are random events. It is obvious resistance to a particular herbicide. Soil Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 79
persistence is determined as part of the herbicide- Literature Cited development process, and half-lives under differ- ent environments are known. The impact of her- bicide rotation versus herbicide mixtures on Cavan, G., J. Cussans, and S. Moss. 2001. Managing selection pressure is not known, however. De- the risks of herbicide resistance in wild oat. Weed creased herbicide rates have been suggested as a Sci 49:236–240. way of decreasing selection pressure. Theoreti- Diggle, A. J. and P. Neve. 2001. The population dy- cally, this practice might be a viable means to namics and genetics of herbicide resistance—a decrease selection pressure; however, the idea of modeling approach. Pp. 61–99. In S. B. Powles maintaining a weed population, susceptible or and D. L. Shaner (eds.). Herbicide Resistance and not, is unacceptable to most growers. Prediction World Grains. CRC Press, Boca Raton, Florida. of cross-resistance has proved difficult. The sup- Gressel, J. and L. A. Segel. 1978. The paucity of plants position was that if a weed was resistant to one evolving genetic resistance to herbicides: Possible herbicide in a group then it would be resistant to reasons and implications. J Theor Biol 75:349–371. other herbicides within that same group. This is Hanson, D. E., D. A. Ball, and C. A. Mallory-Smith. not always the case. 2002. Herbicide resistance in jointed goatgrass (Ae- • Seedbank longevity. The longer seed lasts in gilops cylindrica): Simulated responses to agro- the soil, the longer susceptibility could be main- nomic practices. Weed Tech 16:156–163. tained in a population. Many weeds have a soil Jasieniuk, M., A. L. Brule-Babel, and I. N. Morrison. seed life from 2 to 5 years. Unfortunately, by the 1996. The evolution and genetics of herbicide re- time that resistance is recognized in a field, much sistance in weeds. Weed Sci 44:176–193. of the susceptible seedbank would be depleted. Maxwell, B. D., M. L. Roush, and S. R. Radosevich. The seedbank is analogous to the refuge for in- 1990. Predicting the evolution and dynamics of her- sects but is not as renewable. bicide resistance in weed populations. Weed Tech 4:2–13. Ryan, G. F. 1970. Resistance of common groundsel Validation of Models to simazine and atrazine. Weed Sci 18:614–616. Shaner, D. L., D. A. Feist, and E. J. Retzinger. 1997. The models for the most part have not been vali- Samoa: One company’s approach to herbicide-re- dated. In order to truly validate them, the compo- sistant weed management. Pestic Sci 51:367–370. nents should be tested, which requires the production of a resistant biotype based on the parameters of the model. The resistance gene must occur in the popu- lation, and this is a random event. Resistance in a weed species may or may not occur under similar con- ditions. Resistance is an economic and social issue for grow- ers. Many growers do not see the value in prevention of herbicide resistance, and instead of using a proac- tive approach, will react if and when the problem oc- curs on their farm. Resistance management requires long-term planning and commitment. In many re- gions of the United States, the agricultural economy does not allow farmers to choose a production prac- tice that might be more costly in the short term, even if it would be a good resistance management strate- gy. This may seem shortsighted but it is the reality of production agriculture today. 80
4.4 Lessons Learned in Predicting and Assessing the Risk of Fungicide Resistance: Have Models Helped? Hendrik L. Ypema
Introduction 1. Nature of the mode of action of the fungicides in question; The main purpose of this presentation is to assess 2. Estimated frequency of individuals in the popu- whether models addressing development of fungicide lation that is completely controlled, partially con- resistance have been helpful in the effort to improve trolled, or not controlled; resistance management (RM) strategies for fungi- 3. Rate of pathogen reproduction; cides. It provides a brief overview of the role of mod- 4. Numbers of genes involved in resistance develop- els in predicting or assessing development of fungi- ment; cide resistance, and in identifying factors that 5. Use of the product (number of applications: in a influence the time period in which resistance devel- sequence and throughout the season, use in mix- ops to the point of compromising fungicide efficacy. es, or as a solo product, rates); A general description of a model found in several dic- 6. “Fitness” of resistant isolates; and tionaries is the following: A preliminary pattern rep- 7. Levels of exposure of the pathogen to a fungicide: resenting an item not yet constructed, and serving as rates, coverage, degradation, unexposed sub-pop- the plan from which the finished work, usually larg- ulations, and fungicide distribution properties. er, will be constructed. Specifically in fungicide re- sistance research and management, a model is a tool Unfortunately, for a newly introduced fungicide to aid in predicting how fungicide resistance will de- many of these factors cannot be estimated accurate- velop in nature and to identify factors important for ly, because the data on which the estimates are based resistance development. The design of models is are difficult or impossible to quantify (Brent 1995; based on three concepts, which all can be found in the Brent and Hollomon 1998). general description of a model just cited. First, a model is a “preliminary pattern,” therefore it is based on assumptions about reality. Second, it is “represent- Model Assumptions ing,” therefore the goal is to approach reality with the model. Third, the real-life project, in this case occur- Models predicting or describing scenarios of resis- rence of resistance, is “not yet constructed,” in other tance development are likely to be most precise when words has not been detected yet. the assumptions underlying their operation are clos- est to the situation in nature. In many cases, factors important for resistance development are estimated Models Addressing Fungicide from past experiences with other fungicide-pathogen Resistance Development combinations or from laboratory experiments. For in- stance, fungicide-target fungi such as Botrytis spp. There are a large number of publications available and powdery and downy mildew fungi have shown in on modeling for fungicide resistance development (Jo- the past to be prone to resistance development; there- sepovits and Dobrovolszky 1985; Kable and Jeffery fore they are assumed to be the first to develop resis- 1979; Levy and Levy 1986; Levy, Levi, and Cohen tance to newly introduced fungicides (Brent 1995). 1983; Milgroom and Fry 1988; Shaw 1989a,b, 1993, Multisite inhibitors were shown to be at a lower risk 2000; Skylakakis 1981, 1982). For the design of a of encountering resistant strains of target fungi com- model, several factors need to be quantified as accu- pared with single-site inhibitors. Introduction of a rately as possible to approximate the real-life situa- new single-site inhibitor, therefore, may raise more tion. Some of these factors are the following: immediate concern about resistance development (Brent 1995). Past resistance risk assessments of sin- gle-site inhibitors do not always represent resistance
80 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 81 risk of future single-site inhibitors, however. For 1999), there was no information as to which propor- instance, resistance to benzimidazoles and phenyla- tion of the population was actually controlled by field mides compromised use of these products against application. The same was true for most other fungi- some pathogens after one or two seasons of use, cides at the time of their introduction. whereas it took approximately 7 years of use of ste- Recently, a few publications have addressed sur- rol-inhibitor fungicides before resistance became a vival of individuals of the apple scab fungus, Venturia concern (Brent 1995; Brent and Hollomon 1998). inaequalis, in an orchard population following appli- Would it have been possible to predict the resistance cations of half and full rate of DMI fungicides alone risk of Quinone outside Inhibitor (QoI)-fungicides or in combination with protectants (Köller 1995; when they were introduced commercially in Europe Köller and Wilcox 1999). At the moment of introduc- in 1996 based on past experiences with other fungi- tion, there was no clear information about the num- cides? Probably not; the last major group of fungicides bers of genes involved in resistance development to encountering resistant strains of target pathogens in QoIs. Several target site mutations were identified the field were the demethylation-inhibitor (DMI) fun- in yeasts, hinting at a resistance scenario that would gicides, where resistance levels increased in a gradu- be multigenic in character, and hopefully leading to al pattern, whereas with QoI fungicides resistance a gradual development of resistance in the field (Jor- development has been more disruptive (Brent 1995; dan et al. 1999). Upon introduction, it was not known Brent and Hollomon 1998). how use of QoIs with regard to rates, number of ap- plications, and intervals would impact the develop- ment of resistance. At the moment of introduction, An Example: Resistance true resistant strains of target pathogens had not Development to QoI Fungicides been encountered; therefore, indications of all char- acteristics that make up “fitness,” the ability to com- Most QoI fungicides currently marketed were de- pete (sporulation, growth, lifecycle, survival), certain- veloped from strobilurin A, a fungal metabolite of ly were not known. Also unknown was how patterns Strobilurus tenacellus, and all share the same mode of exposure of the pathogen to a fungicide based on of action. The antifungal activity of strobilurin A distribution properties of the fungicide, applied rate, helped the fungus compete with other fungi in estab- coverage achieved, and the presence of unexposed lishing itself on its food source of decaying pine cones subpopulations in, for instance, untreated areas or on on the forest floor. The metabolite was chemically alternate hosts, affected development of resistance. modified for better utility as a fungicide and has stood These factors all have been estimated and used in at the base of several QoI fungicides currently mar- models to assess development of resistance (Josepo- keted (Ypema and Gold 1999). vits and Dobrovolszky 1985; Kable and Jeffery 1979; Looking at the factors that needed to be quantified Levy and Levy 1986; Levy, Levi, and Cohen 1983; to predict and manage the development of resistance Milgroom and Fry 1988; Shaw 1989a,b, 1993, 2000; at the moment when QoI fungicides were launched Skylakakis 1981, 1982). But it was impossible to commercially, it becomes clear that many could not quantify these factors for most fungicides accurately be quantified adequately. Because a model system— at the moment of introduction. a fungus producing the lead fungicidal molecule—was A few years after introduction of QoI fungicides, available, the mode of action of strobilurin A could be more information was gathered about certain factors elucidated fairly quickly, and for the majority of fun- influencing resistance development (Heaney, Hall, gicides currently commercialized the mode of action and Olaya 2000). Compared with the moment of in- is known. Several QoIs exhibited excellent activity troduction, the mechanisms of resistance and under- against a number of pathogens with many short veg- lying mutations that were found in target pathogens etative generation cycles and high reproduction rates in treated areas were much better known, and some that were shown to be prone to resistance develop- mutations were found to be quite different from the ment, such as the powdery mildew fungi. At the mo- original target-site mutations identified in yeasts. ment of introduction, however, it was not known Limited information also was known about the fitness whether resistance would affect QoI fungicides simi- of resistant isolates collected from treated areas and larly compared with, for instance, benzimidazoles. mutants generated in the laboratory (Heaney, Hall, Although the QoI lead molecule, strobilurin A, was and Olaya 2000). Any study conducted with these extremely active against several target fungi at ex- strains, however, was limited to only a small sample tremely low rates in in vitro assays (Ypema and Gold of one to a very few individuals. Conclusions based 82 4.4 Lessons Learned in Predicting and Assessing the Risk of Fungicide Resistance: Have Models Helped? on the study of these individuals were difficult to can manipulate with ease, such as the number of ap- extrapolate to the large pool of genetic variation and plications of a particular fungicide, the concentration potential resistant phenotypes in a fungal population at which a fungicide is applied, and whether it is ap- in nature, making it impossible to provide a general plied alone or in a tank mix with other fungicides. prediction for the development of resistance to QoI Such recommendations focus primarily on reduction fungicides. Information about how rate of pathogen of selection pressure and satisfactory, economically reproduction, use of the product, and level of exposure feasible control of most individuals in a pathogen pop- affect development of fungicide resistance in detail is ulation with multiple types of chemistry. Other fac- still elusive, several years after QoI fungicides were tors identified by models as being important are not launched. It can be concluded that many factors un- at all or only superficially included in the formulation derlying the development of resistance still could not of RM guidelines, because they cannot be measured be quantified accurately several years after introduc- accurately or because they cannot be controlled by the tion of QoI fungicides at a time when the first cases end user. For the foreseeable future, due to the diffi- of resistance were encountered in the field, limiting culty in accurately quantifying these other factors, the the utility of models to predict development of resis- role of models to predict “real-life” resistance risk sce- tance in practical situations. The situation has been narios likely will remain limited. This may change similar for most other fungicides several years after only when future research is directed more toward their launch. fields and orchards where fungicides are used. The role of models as a tool in understanding resistance Have Models Helped? development and factors important to resistance de- velopment will continue to be important.
Did models help in predicting development of re- sistance or in identifying factors that influence fun- Literature Cited gicide resistance development? To date, knowledge of resistance and RM is based mainly on past experi- Brent, K. J. 1995. Fungicide resistance in crop patho- ences with fungicides to which resistance has devel- gens: Can it be managed ? Fungicide Reisitance Ac- oped. It continues to be difficult—if not impossible— tion Committtee Monograph 1. Global Crop Protec- to assess accurately the resistance risk to a newly tion Federation, Brussels, Belgium. introduced fungicide compound until resistance devel- Brent, K. J. and D. W. Hollomon. 1998. Fungicide ops. Verification of the actual success and validity of resistance: The assessment of risk. Fungicide Re- a model in predicting risk of resistance development sistance Action Committee Monograph 2. Global and identifying factors important for resistance de- Crop Protection Federation, Brussels, Belgium. velopment for a given fungicide-pathogen combination Heaney, S. P., A. A. Hall, and G. Olaya. 2000. Resis- has been difficult, because many factors identified by tance to Fungicides in the QoI-STAR Cross-resis- models as being important in influencing resistance tance Group: Current Perspectives. The British development cannot be quantified accurately in na- Crop Protection Council Conference—Pests and ture. Those factors include fitness of resistant strains Diseases, Brighton, U.K. Pp. 755–762. in a fungal population, level of exposure to a fungi- Jordan, D. B., R. S. Livingston, J. J. Bisaha, K. E. cide, and the presence of untreated target pathogen Duncan, S. O. Pember, M. A. Picollelli, R. Schwartz, subpopulations. Although the predictive power of S. Scharz, J. A. Sternberg, and Z. S. Tang. 1999. models to assess the risk of resistance development Mode of action of famoxadone. Pestic Sci 55:105– of a given fungicide-pathogen combination is limited, 118. models have been and will be very useful in identify- Josepovits, G. and A. Dobrovolszky. 1985. A novel ing factors that may influence the development of re- mathematical approach to the prevention of fun- sistance in general. gicide resistance. Pestic Sci 16:17–22. Kable, P. F. and H. Jeffery. 1979. Selection for toler- ance in organisms exposed to sprays of biocide mix- Conclusions tures: A theoretical model. Phytopathology 70:8–12. Köller, W. 1995. Recent developments in DMI resis- As for today’s formulation of fungicide RM strate- tance. Pp. 301–311. In H. Lyr, P. E. Russell, and gies before detection of resistance, such recommenda- H. D. Sisler [eds.]. Modern Fungicides and Antifun- tions are based primarily on factors that the end user gal Compounds. Intercept Andover, Hampshire, U.K. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 83
Köller, W. and W. F. Wilcox. 1999. Evaluation of tac- tics for managing resistance of Venturia inaequal- is to sterol demethylation inhibitors. Plant Dis 83:857–863 Levy, Y. and R. S. Levy. 1986. Control strategies us- ing systemic fungicides for limiting disease devel- opment and resistance buildup: Practical implica- tions of a simulation model. Phytoparasitica 14(4):303–312. Levy, Y., R. Levi, and Y. Cohen. 1983. Buildup of a pathogen subpopulation resistant to a systemic fungicide under various control strategies: A flex- ible simulation model. Phytopathology 73:1475– 1480. Milgroom, M. G. and W. E. Fry. 1988. A simulation analysis of the epidemiological principles for fun- gicide resistance management in pathogen popu- lations. Phytopathology 78:44–55. Shaw, M. W. 1989a. Independent action of fungicides and its consequences for strategies to retard the evolution of fungicide resistance. Crop Protect 8:405–411. Shaw, M. W. 1989b. A model of the evolution of poly- genically controlled fungicide resistance. Plant Pathol 38:44–55. Shaw, M. W. 1993. Theoretical analysis of the effect of interacting activities on the rate of selection for combined resistance to fungicide mixtures. Crop Protect 12:120–126. Shaw, M. W. 2000. Models of the effects of dose het- erogeneity and escape on selection pressure for pes- ticide resistance. Phytopathology 90:333–339. Skylakakis, G. 1981. Effects of alternating and mix- ing pesticides on the buildup of resistance. Phyto- pathology 71:1119–1121. Skylakakis, G. 1982. The development and use of models describing outbreaks of resistance to fun- gicides. Crop Protect 3:249–262. Ypema, H. L. and R. E. Gold. 1999. Kresoxim-meth- yl: Modification of a naturally occurring compound to produce a new fungicide. Plant Dis 83:4–19. 84
5.1 Pesticide Resistance Management: Is There a Role for Consumers? Doug Gurian-Sherman
Introduction support, pesticides typically are not viewed as a re- source by the general public. Instead, pesticides of- Consumers are an untapped resource, and a poten- ten are equated with environmental and human tially powerful force, for promoting pesticide resis- harm. At best, the public considers pesticides to be a tance management (PRM). They are largely unaware “necessary evil,” the use of which should be mini- of the importance of PRM, but they are concerned mized. As already noted, however, a decrease of pes- about the effects of pesticides on health and the envi- ticide use is compatible with both PRM and IPM. ronment. Those concerns about pesticides could pro- Despite the importance of PRM/IPM, there are vide an avenue for consumer support of PRM if a con- barriers that prevent consumers from supporting it. certed effort were made to promote such support. Those barriers are the lack of understanding that Consumer support for PRM could be mobilized by in- pesticide use can be decreased under IPM, the lack corporating PRM into integrated pest management of standardized IPM goals that are consistent with (IPM), which in turn may be supported through the consumer interests, and the sometimes-divergent marketplace or by consumer groups. needs of farmers and consumers concerning pesticide Pesticide resistance management needs IPM as a use. Those barriers are not insurmountable, and sug- vehicle for consumer support because otherwise PRM gestions for overcoming them are provided. is too specialized and complex to attract consumer Consumer goals of decreasing pesticide use and attention. Both PRM and IPM may promote de- adopting the use of safer pesticides can coincide with creased pesticide use, which is an important consumer the goals of PRM and the needs of farmers. That in- goal that arises from concern about the safety of pes- tersection of interests can be incorporated into IPM, ticides. Consumer groups may additionally recognize if IPM is defined and standardized properly, thereby the value of “safer,” or reduced-risk, pesticides and providing a vehicle for consumer support and bene- may support PRM for those pesticides. Resistance fits to society. management of safer pesticides can, like pesticide use reduction, be accomplished through IPM. Pesticide resistance management is a resource con- Consumers, Pesticides, and PRM servation issue, and consumers support conservation. Like many natural resources, pesticides can be “used Although there is no evidence that consumers are up” if not conserved. And as natural resources can concerned about pest resistance, their aversion to be conserved by judicious use, pesticides can be con- pesticides can be used to support PRM. Consumer served by PRM. Loss of pesticides as a resource concern about pesticides leads to a desire for de- through pest resistance can have negative impacts on creased pesticide use, which could contribute to PRM. the environment. For example, estimates of crop yield Decrease of pesticide use facilitates PRM generally by losses in the absence of pest control typically range decreasing selection pressure on pesticides, thereby from approximately 20% to 80% depending on the crop decreasing the likelihood of resistance. The goal of and where and how it is grown. In the absence of decreased pesticide use also is a goal of organic farm- adequate pest control, the acreage needed for farm- ing. The exclusion of many pesticides under organic ing could increase to offset yield losses. The additional farming standards, however, limits the value of organ- acreage devoted to agriculture would decrease land ic farming for PRM. In contrast, IPM is less restric- available for other uses and increase the environmen- tive about the kinds of pesticides used, can decrease tal impacts associated with agriculture. And loss of the use of pesticides, and is supported by consumers. reduced-risk pesticides may result in replacement by Consumers want decreased pesticide use because more dangerous pesticides. they generally equate pesticides with environmental Although resource conservation has broad public and human harm. The long shadow of Silent Spring
84 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 85
(Carson 1962) remains, occasionally reinforced by farming that only organic farming embodies. For ex- stories about the recovery of ospreys and eagles after ample, organically grown food allows the use of dif- the banning of DDT, atrazine-deformed frogs, and ferent pesticides than IPM-grown crops allow. In hermaphroditic alligators found in lakes on flooded particular, pesticides approved for organic farming farmland. are derived from natural substances rather than syn- Concern about pesticides also can be seen for the thetic ones. That gives organic pesticides an aura of new technology of genetically engineered (GE) pesti- safety. On the other hand, consumers may be inter- cidal plants. For example, a laboratory study suggest- ested in purchasing IPM-grown food that uses less ed that GE corn pollen containing an insecticidal pro- pesticide even if certain other goals of organic produc- tein from Bacillus thuringiensis (Bt) bacteria may tion are not accomplished. have harmed Monarch butterflies (Losey, Rayor, and A survey conducted by Rutgers University about Carter 1999). Although later field experiments con- consumer attitudes toward IPM revealed that con- cluded that it was very unlikely that Bt corn pollen sumers would respond positively to the decreased use harmed Monarchs (Sears et al. 2001), the damage to of conventional pesticides. Seventy-one percent of public perception already had occurred. consumers surveyed were willing to purchase IPM- An indication that consumers are concerned about labeled food, and 88% of those consumers were will- pesticides can be found in consumer surveys. A re- ing to pay a premium for food grown using IPM meth- cent survey conducted by the Center for Science in the ods (premiums ranged up to 20%) (Govindasamy Public Interest showed that 76% of consumers desired et al. 1998). Respondents, however, typically did labeling of food from crops treated with pesticides, not understand IPM prior to reading definitions more than the percentage that desired labeling for GE supplied with the survey. This indicates that consum- crops (Center for Science 2001). In fact, despite con- ers must be educated about how IPM addresses their cern about GE foods, approximately 21% of consum- concerns about pesticides to market IPM-grown food ers said that GE foods that decrease pesticide use are effectively. safer than conventional foods, whereas only 7% felt An indication of the market potential for IPM- GE foods without pesticide reduction were safer. A grown food is demonstrated by IPM-labeled food sold recent survey by Rutgers University found that pes- by the Wegman’s grocery chain of the northeast Unit- ticide residue on food was an important food safety ed States. With the help of Cornell University, Weg- concern (Govidasamy et al. 1998). man’s began labeling food grown using IPM in 1995. Organically grown food often is purchased because The crops grown for the Wegman’s IPM label expand- it is produced without using synthetic pesticides. ed from 1,413 hectares (ha) in 1996 to an estimated Sales of organically grown food can therefore act as 3,654 ha in 1998 (Cornell University 1999). The Weg- an indicator of consumer interest in decreasing or man IPM program includes pesticide reduction, with eliminating pesticides. In recent years, consumption adoption of 80% of the recommended IPM methods of organically grown food has increased at over 20% giving a predicted 30%–50% decrease in pesticide use per year according to U.S. Department of Agriculture (Cornell University 1999). data (Dimitri and Greene 2002). These dramatic Integrated pest management also may have an increases have occurred despite substantial premi- economic advantage over organic farming, even in the ums, often over 50%, charged for organically grown absence of the high premiums paid for organically food. Although organically grown food makes up only grown food. That is because organic production, with a very small percentage of U.S. agricultural produc- its philosophical as well as biological justification, tion, the Rutgers survey indicated that over two- may sacrifice yield and increase labor compared with thirds of consumers would buy organic food if it were conventional farming. By comparison, IPM is based not so expensive. That potential market for organi- on maintenance of high yields, thereby allowing high- cally grown food suggests a parallel interest among er profit at lower prices than for organically grown consumers for decreased pesticide use. food. It does not necessarily follow, however, that con- A second means for consumers to support PRM is sumers who favor organically grown food also would through environmental and consumer advocacy orga- favor crops grown using IPM. Although both organi- nizations that recognize the importance of PRM. This cally grown and IPM-grown food may decrease pesti- does not require most consumer-members of those cide use, they are distinguished by several other prac- groups to understand the details of PRM, but only to tices, as well as by a general philosophy of natural trust the consumer organization to represent their 86 5.1 Pesticide Resistance Management: Is There a Role for Consumers? interests concerning the broader goals of human Several types of reduced-risk pesticides are regis- health and environmental protection. By this means tered by the Environmental Protection Agency (EPA). the problem of technical complexity being a barrier Unlike the narrower spectrum of pesticides approved to consumer understanding and support of PRM may for organic farming, synthetic pesticides are includ- be avoided. ed among the reduced-risk pesticides registered by the Consumer organizations are unlikely to support EPA. According to a recent EPA list, 32 pesticides are IPM if they believe that all uses of chemical pesticides registered under the reduced-risk program (plus sev- are harmful and unnecessary. Certain environmen- eral previously registered pesticides have been reclas- tal groups may support organic farming, for example, sified as reduced-risk) (EPA 2003). Those reduced- as an alternative to conventional farming in part be- risk pesticides include 10 fungicides, 11 herbicides, cause synthetic pesticides are not used. and 12 insecticides (one of which functions as both But certain consumer activists and consumer insecticide and herbicide). In addition, biopesticides, groups have shown support for IPM, including the use such as biological control agents like microbial Bt and of certain nonorganic pesticides. For example, other microbes, often are considered reduced-risk Charles Benbrook, a prominent agricultural environ- pesticides. A recent EPA list includes 195 biopesti- mentalist and critic of agricultural biotechnology, has cides (not including transgenic crops or beneficial supported the use of synthetic pyrethroid insecticides pest-eating insects such as ladybugs—the latter are in arguments against the use of Bt crops (Union 2001). not included because they require no EPA registra- In a publication for the Consumers Union, Benbrook tion) (EPA 2002). defines “Biointensive IPM” as a “range of preventa- One measure of pesticide safety or perceived safe- tive tactics and biological controls to keep pest popu- ty may be based on the origin of the pesticide, in par- lation within acceptable limits. Reduced-risk pesti- ticular whether it is derived from a naturally occur- cides are used if other tactics have not been ring substance. For example, synthetic pyrethroid adequately effective, as a last resort and with care to insecticides derived from the botanical insecticide minimalize [sic] risks” (Gold 1999, p. 18). At least one pyrethrum often are considered to be acceptable and other prominent environmental organization that relatively safe. Other new and effective pesticides are endorses biointensive IPM, the World Wildlife Fund, synthetic versions of compounds found in nature. For considers PRM to be critically important (World Wild- example, the strobiluran fungicides are synthetic ver- life Fund 2003). sions of antifungal compounds found in fungi of the The specific acceptance by certain consumer groups genus Strobilus. of reduced-risk pesticides, as opposed to synthetic A specific example of the support of PRM by con- pesticides generally, should not be overlooked. Un- sumer organizations as well as their impact on PRM derstanding the acceptance by consumer groups of policy is found in insect resistance management (IRM) certain synthetic pesticides, such as synthetic pyre- for genetically engineered Bt crops. Environmental throids as opposed to organophosphates, is critical to organizations, along with agricultural scientists and gaining the support of those groups for IPM/PRM. regulators, promoted the development of mandatory Support of biointensive IPM by consumer groups resistance management plans for Bt crops. The high- indicates a willingness to accept, if somewhat grudg- dose refuge strategy that emerged from the debates ingly, a legitimate role for certain synthetic pesticides. concerning Bt crops is unique, inasmuch as no regu- By implication, if pesticides are accepted as having a lations mandate PRM for other pesticides.1 In addi- legitimate role in biointensive IPM, then it follows tion, Bt crops have led to a decrease in chemical in- that their effectiveness should be conserved. There- secticide use in Bt cotton in several parts of the United fore the recognition of pesticides as a resource by en- States. Due to the controversy surrounding GE crops, vironmental organizations represents an opportuni- however, acceptance by many consumer groups of Bt ty for them to endorse PRM practices to conserve crops as an alternative for chemical pesticide use cur- those resources. rently is not an option.
1 Support for Bt IRM by consumer organizations initially was motivated by the desire to prevent cross-resistance to microbial Bts used by organic growers. Advocacy for Bt IRM has continued for new Bt products, however, such as MON 863 for corn rootworm, for which there is no important microbial counterpart used by organic growers. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 87
Barriers to Consumer times difficult to achieve. Decreased pesticide use in certain instances actually could accelerate resistance Support for PRM if not done in a biologically sound manner. For ex- ample, resistance management plans for Bt crops There are several barriers to consumer support for have depended on the use of a high effective dose of IPM/PRM resulting from problems in marketing IPM/ the insecticidal Bt Cry protein. That is because re- PRM or from IPM standards (or lack of standards) sistance alleles that can overcome high pesticide doses that do not meet consumer goals of decreasing pesti- typically are present at much lower frequencies than cide use or using safer pesticides. Marketing barri- alleles effective at lower doses. Often such high-dose ers include lack of consumer understanding of IPM alleles also are recessive. The recessive nature of the and inconsistent market supply (Pool, W. 2003. Per- resistance genes facilitates PRM by necessitating the sonal communication). mating of two heterozygous parents that each carry Another potential barrier could develop concerning a resistance allele, the chances of which are decreased standards for reduced-risk pesticides that may differ by planting non-Bt “refuges” (Shelton, Zhao, and between consumer groups and others interested in Roush 2002). For Bt crops, a high level, or dose, of IPM. For example, GE pesticidal crops are registered the pesticidal protein is therefore considered to be along with other biopesticides as de facto reduced-risk desirable for resistance management. Similar prin- pesticides, but often are considered to be unacceptable ciples also may apply to certain other pesticide uses. by environmental groups. The definition of other re- Integrated pest management standards acceptable duced-risk pesticides by the EPA also may not be to farmers do not always require a decrease in pesti- stringent enough to suit certain environmental cide use or PRM compared with conventional farm- groups.2 Similarly, definitions of acceptable pesti- ing, although often they include pesticide reduction cides under biointensive IPM/PRM by consumer or- as a laudable goal. For example, applying insecticide ganizations may not always be acceptable to farmers. based on a measure of insects reaching an economic That divergence between how farmers apply IPM/ threshold, a common IPM practice, may result in high- PRM and how consumers define IPM may act as a er pesticide application than scheduled spraying un- barrier to consumer support for PRM. der conventional farming in certain circumstances. Farmers may not want to be restricted to the use Perhaps due to disagreements concerning accept- of reduced-risk pesticides, or even to the preferential able definitions of IPM, and unlike the situation for use of such pesticides. Many reduced-risk pesticides organic farming, there is no standardization of IPM are relatively new and still under patent protection, that allows broad certification of IPM/PRM-grown and therefore often are more expensive than old non- food. That lack of standards also limits both the kind reduced-risk pesticides. Furthermore, reduced-risk of commercial marketing that might otherwise be pesticides may not be available to control all pests on done to promote IPM/IRM and the broad promotion all crops for which nonreduced-risk pesticides are of IPM/PRM by consumer groups. It also limits the available. Even when available, some reduced-risk availability of food grown under IPM protocols accept- pesticides may be less effective than available nonre- able to consumers. duced-risk pesticides. This often may be the case for the reduced-risk biopesticides. Additionally, many pesticides are safer because they have a narrower Solutions and Conclusions spectrum of activity and therefore are less likely to harm nontarget organisms. But a narrow spectrum The IPM/PRM standards that provide for substan- of activity also may mean that fewer types of pests are tial decreases in pesticide use and the use of reduced- controlled than by nonreduced-risk, broad-spectrum risk pesticides will encourage consumer acceptance of pesticides. Farmers may not want to be restricted to IPM-labeled foods. The IPM standards also allow nonreduced-risk pesticides if a decrease in yields is a product discrimination that facilitates marketing and consequence. willingness of consumers to pay a premium for foods In practice, decreased pesticide use depends on labeled as IPM. Consistency between those standards adequate pest control at lower levels that is some- regionally or nationally will facilitate an adequate
2 The requirements for reduced-risk status are essentially a demonstration of less risk in any of several categories compared with currently used pesticides. The amount of risk reduction is not specified clearly. 88 5.1 Pesticide Resistance Management: Is There a Role for Consumers? supply of IPM/PRM-grown food. Such standards also Dimitri, C. and C. Greene. 2002. Recent growth pat- allow a consistent message to be conveyed to terns in the U.S. organic foods market. USDA Eco- consumers that such foods are grown with less pesti- nomic Research Service Agriculture Information cide and safer chemicals. Because of regional varia- Bulletin No. AIB777,
5.2 Role of Stakeholders in Resistance Management: Crop Consultants Roger Carter
Introduction program will ensure a firmer economic base for farm- ers and thereby improve participation. Guarantee- Resistance management (RM) is considered the ing profitability through either government payments mainstay of many agricultural consultants’ repertoire or insurance programs if growers adapt updated ver- of strategies. Although RM is considered to be “some- sions of RM will enhance participation. thing new” or a “key word,” independent agricultural There is currently a severe lack of different tools consultants have been recommending practices sup- to control many pests. A prime example is the con- porting RM for more than 40 years. trol of the brown stinkbug in soybeans. Methyl par- Without RM, agricultural producers would find it athion is the only efficacious and practical treatment difficult to remain in business. Yet there is the mis- to control this insect. Both the government (i.e., the conception that RM is not as widely adopted as nec- U.S. Environmental Protection Agency [EPA]) and in- essary to facilitate environmental enhancement. dustry must give RM practitioners more tools. The Because of this misconception, there must be dialog more tools consultants have in their bags, the more to discuss the role of all players in the RM scheme. likely we are to have a good RM program. A bag will never get too full of tools. Certainly, the more tools consultants have, the harder the decision-making Barriers to RM and How to becomes, but at least there will be multiple choices Eliminate Them in order to practice RM. Economic restraints caused by yield or quality re- A few consultants and producers lack appreciation duction from certain practices, programs, or treat- for RM science. Many of these are of the “old school” ments designed to embellish RM put hardship on pro- and have not realized yet that the key to profitability ducers. The cost of alternative control practices often is the adaptation to “new thinking,” including the “up- can be very great. These constraints must be paid for dated version of RM.” They have developed apathy by the public (the government) through payments or not just to RM, but also to other scientifically proven insurance designed to offset losses. Or, the public (the programs to enhance profitability. Training those government) can help to pay for the development, from the old school and putting more independent through industry, of new practices, programs, or prod- unbiased consultants in the field will increase the ucts that work in RM programs without desecrating chances that apathy will not be an issue in the future. profit. There also seems to be a lack of ethics necessary Many producers are in a short-term survival mode for self-imposed compliance. The repeated use of the due to the poor farm economy. Improving the farm same chemistry on the same insect spectrum and program with payments on what is produced (not on transgenic refugia abuse are two examples. Both base acres), crop insurance reform (adopting the cost practices can be “controlled” by industry’s imposing of production insurance), and a change in foreign stricter punishments for abusers. Abusers can be trade policy will be necessary to improve short-term found through more stringent monitoring programs cash crunches and to help the producers and consult- conducted by industry. As a last resort, government ants adopt long-term goals. And integrated pest man- regulation may be necessary to dictate punishment. agement (IPM) programs must be created with long- Producers and consultants currently are relying on term vision in order to facilitate those goals. the most efficacious and profitable treatments and Management skills of a few producers may impede practices due to poor farm economics. Increasing gov- RM adoption by agriculture as a whole. The RM pro- ernment payments for increased use of “healthy” RM grams often can be complicated, yet workable. Edu- programs will increase participation in RM programs. cation of the next generation of producers will enhance An improved cost-of-production crop insurance the adoption of the most efficacious RM programs.
89 90 5.2 Role of Stakeholders in Resistance Management: Crop Consultants
Goals of Independent Researchers (industry and public) should search for new chemistry and strategies. They should develop Agricultural Consultants RM programs for ever-changing pest complexes, crop- ping systems, and management tools, and they should Although consultants work with a diversity of pursue new thresholds and scouting techniques to be crops, pests, and conditions, our goals are similar. used with new technologies. Finally, researchers should develop novel transgenic or conventional pest 1. We must maintain long-term vision and not look control or pest resistance traits. only at short-term relief. The key to most RM pro- Industry should develop new chemistry and tech- grams is longevity. nology (new and more tools). Companies should mon- 2. We also must maintain RM as a facet of IPM and itor and help to develop RM programs—rotating pro- integrated crop management (ICM). One of the grams, modes of action, etc.—especially in weed results of good IPM and ICM programs is a good management. Mandating compliance through closer RM program. The sciences of all embellish each inspections and stiffer penalties should be a priority. other. Activation of terminator genes is a must for biotech- 3. While monitoring crops, consultants must be look- nology. Another key concern should be protecting ing vigilantly for the early warning signs of re- U.S.-developed technology so that U.S. producers do sistance and communicating their findings as not subsidize foreign competitors, as is occurring now. quickly as possible to the scientific community. And, finally, industry must keep marketing and sales 4. Consultants must educate their clientele con- balanced with RM programs. stantly regarding RM. And they themselves must Government’s goals should include establishing remain updated constantly on all facets of science federal guidelines or restrictions developed with con- that affect RM. sultants, industry, and grower groups. It should mon- 5. Consultants also must help industry and public itor the effects of RM programs on farm economics and research develop updated RM programs and eval- on the environment. It should also protect U.S.-gen- uate those programs before they are fully imple- erated technology from foreign competitors. Estab- mented in the fields. lishing “fast-track” clearance on novel products to 6. Consultants must maintain contact with all oth- increase RM tools is necessary. The U.S. government er stakeholders. All stakeholders in RM should should finance university and private research brain- “work and play well with others.” A consistent storming activities that seek novel approaches. And interaction must be maintained among all stake- government should promote independent, unbiased holders. agricultural consultants as the medium best suited to deliver the most-efficacious RM systems to the end users—the producers. Perception of Other Stakeholders’ Goals Economics Should Consultants perceive that the goals of all other Always Be First stakeholders should be the following: Grower groups, independent consultants, the EPA, 1. to work and play well with other stakeholders, the U.S. Department of Agriculture, university re- 2. to consider economics at all times, search and extension, and industry (basic to dealer) 3. to see everything from the farmers’ perspectives, each have a role to play if efficacious, profitable, and 4. to keep goals do-able, long-term RM programs are to be embellished. Al- 5. to look “outside the box,” though certain goals are somewhat unique, each 6. to protect American technology, and stakeholder should list economics first and foremost 7. to evaluate new RM strategies before as a backbone to any viable program. If it doesn’t implementing them. show a profit on the farm, then don’t waste the time, manpower, and money to try to make it fit. The pro- The producers’ number one goal should be economic ducer must have a profit from every investment. Oth- survival. They also should have long-term vision and erwise, the practice will be dropped. a goal of working with nonbiased consultants to im- plement RM programs. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 91
Summary There are certain barriers to achieving complete adoption of all RM techniques. These barriers can be decreased primarily by making it economically feasi- ble for producers to adapt RM programs through gov- ernment support or through improved yields and quality at a lower cost per unit. Secondly, the con- tinued development of more efficacious, more easily managed RM tools and programs will decrease bar- riers. And third, communication among all stakehold- ers is imperative. Having an unbiased opinion as a delivery mechanism for RM systems and techniques is one key to the success of RM. 92
5.3 Role of Producers in Management of Resistance Frank L. Carter
Introduction same time, in 1996, Bt cotton was introduced and rap- idly adopted. Bt cotton further decreased insecticides This session is on the role of stakeholders in resis- applied for control of lepidopterous pests. As a result, tance management. My topic is to discuss the role(s) pesticide use per season declined from an average of of producer stakeholders. I will give an overview 6.7 applications per season in 1995 to 3.2 in 2003. of the current pest situation in cotton and specifical- In addition, several new products have been devel- ly address each of the three questions posed to this oped recently for cotton, giving cotton a selection of panel. modes of action (MOAs) with both transgenes and con- ventional chemistry now available for insect pests. Weed control under the current trend of minimum Background tillage is in need of new MOAs. Resistance manage- ment planning should focus on this environment rath- I am an entomologist with the National Cotton er than the 30-year history of dealing with resistance Council. I am not a cotton producer. My remarks are in cotton. based on a long-standing professional interest in re- sistance and 22 years of experience working with na- tional cotton producer groups. I also have worked Question #1: What Are the closely with the Insecticide Resistance Action Com- Barriers to RM? mittee (IRAC) for the more than 15 years. For this discussion, I will confine my remarks to cotton pro- The following is a list of some of the barriers to re- ducers only. sistance management from the viewpoint of produc- The history of resistance in the cotton system has ers. These are listed in no particular order of impor- been well documented. At this workshop alone, cot- tance. ton has been the “poster child” in several sessions. Dr. O’Leary outlined cotton resistance issues, and cotton • Must be alternatives available. Effective RM was the topic in four of the seven presentations in the capabilities improve when two or more MOAs are “Lessons Learned” session. Glyphosate resistance in available to be used in some combination, either weeds in cotton was discussed by Dr. Heering, and Dr. in mixtures or in alternating applications. Bagwell gave an overview of insect resistance in mid- • Pick your RM target. Cotton, like most other Southern cotton. Dr. Dennehy talked of resistance crops, has a long list of pests. Cotton has 12 in- issues in Western cotton, and Dr. Head discussed re- sect pests; 25 or more weed pests; a list of diseas- sistance management (RM) in Bacillus thuringiensis es including seedling diseases, root rots, vascular (Bt) crops, including cotton. wilts, and boll rots; and 3 major nematode pest species. Obviously, we cannot conduct an RM plan for each pest-by-product combination. This Current Cotton Pest Situation very likely is unnecessary anyway. • RM plan. Producers look to others to identify pri- We now are in a new era in cotton. I think that ority needs for RM. this will set the stage for future RM strategies in cot- • Lack of ownership or leadership. In some ton because the insecticide use in cotton has been de- cases, resistance management leaders are bound creased significantly. There are two reasons for this. by state lines or other geographic boundaries. First, boll weevil eradication expanded in the mid- Possibly more important, especially in today’s 1990s and effectively has removed the boll weevil “lean and mean” environment, most of those lead- along with the associated insecticide use. About the ers are spread too thin in their responsibilities to
92 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 93
look beyond simply meeting the next deadline. • Scientific community. Producers must rely on Planning and executing an RM plan requires a the scientific community for science-based pro- time commitment that may be a luxury in today’s posed RM plans, and the research community work environment. must be responsible for monitoring the effective- • Survival mode. Producers often are in a surviv- ness and progress of the plans. al mode. Their philosophy is “Let’s take care of this • Private industry. Private industry has a huge season first!” role in resistance management. Protecting exist- • Lack of incentive. Incentive may not be the cor- ing products against resistance development and rect word here, but I think that producers need a developing alternative products are obvious re- good reason to support RM plans aggressively. sponsibilities. Private industry plays an impor- Recent examples are the Bt cotton refuge RM plan tant role in the IRAC, the Fungicide Resistance to protect that valued technology and the white- Action Committee, and the Herbicide Resistance fly RM plan in Arizona to avoid return to the cri- Action Committee programs. Interactions with sis mode with whitefly. In this vein, I think that producer groups, consultants, and the scientific producers are more willing to support RM after community are key roles. emerging from a crisis situation. • Extension and consultants. Extension and • Must be cost neutral. Producers generally de- consultants must work with scientists and grow- sire that RM strategies are cost neutral. Again, ers to evaluate proposed plans. the exception is after recovering from a crisis, as • Extension, consultants, and producer orga- Arizona did with whitefly. nizations. Extension, consultants, and produc- • Impediment to new replacement or compet- er organizations are needed for communication to ing technology. It may sound strange at this those ultimately responsible for carrying out RM meeting where RM is considered a method to pre- strategies. serve existing technology, but there is some truth • Economists. Economists must provide input on to the idea that preserving one technology actual- the economic impact of protecting the technology ly may serve as an impediment to a new replace- and the cost of implementing such measures. ment or competing technology. Other speakers • Producers. Producers are needed to provide have referred to this already in this workshop. grower input on modifications or new plan strat- egies, to serve as a reality check on proposed strategies, and to help evaluate science-based Question #2: What Are the Goals strategies. of RM Implementation for Producers? Summary of Questions
The goals of RM are more straightforward. These The important barriers in the view of producers in- are listed here, and there may be more goals that could clude alternative tools, a clear target or objective, be included. leadership, and identified incentive. Key goals con- sidered by producers are clear need, effective plan, • Clearly identified objective practical strategies, minimal economic economical • Effective plan and strategies impact on producers, and a good monitoring plan. The • Practical strategies that are producer friendly roles of others include key roles for the scientific com- • Strategies that are cost neutral to producers munity, private industry stewardship, extension and •RM plan that covers host range of the target pest consultants for education, and research for monitor- ing and modifications to the plan as needed. Produc- ers have important roles in carrying out successful Question #3: What Are the Goals RM plan strategies. of Others in Pest RM? Effective RM requires the participation and involve- Producer Perspective Summary ment of stakeholders involved in production of a com- modity. The following is a list of some of the specific In summary, the cotton industry is entering a new roles of others that I think are most important. era, one in which insecticide input is decreased sig- 94 5.3 Role of Producers in Management of Resistance nificantly. Producers now expect that consideration of RM plans should be conducted in light of these new developments and not on the 30-year-old history of re- sistance and insecticide use in cotton. Producers ex- pect that target-specific RM plans will be identified on those pest–by-product(s) combinations that are thought to be high resistance risk. Producers want RM strategies to be of minimal economic impact to them and suggested practices to be practical in na- ture. Producers ultimately will make or break any RM plan, so it makes sense to strive for practicality when choosing RM strategies. Last but not least, producers will not be in favor of increasing regulation of RM. Producers encounter an increasing regulato- ry environment in all farm practices, so they do not want to see RM regulated. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 95
5.4 Industry’s Perspective on Insect Resistance Management and Its Implementation Caydee Savinelli, Graham P. Head, and Gary D. Thompson
Introduction Key Tactics Pest management resistance is a serious issue for Once the industry goals are established for resis- the agricultural chemical industry. The development tance management, there are a number of key tactics of pest resistance to a company’s product poses sig- employed by companies in their resistance manage- nificant problems, in terms of poor product perception ment programs. It is important to define the mode of in the eyes of the customers, loss of tools for the grow- action of a product. Because not all products have the ers, and revenue loss for the company. The decrease same mode of action, this is an important step in iden- in product use is a significant motivation for the in- tifying which products may be used or should be avoid- dustry to engage in the issue of pest management. ed in a resistance management program. It also is Companies are aware of the consequences of resis- essential that the effective rates are labeled because tance development, and it is imperative that they take this minimizes selection pressure. Labeled use pat- the lead in developing strategies that will manage terns, both in terms of application timing and num- resistance both for new product development and cur- bers of applications, should be consistent with good rent product maintenance, with the goal of sustain- resistance management principles. If it has been de- ing product use in a resistance management frame- termined that continual use of one product has the work. The essence of the resistance management potential to cause resistance, then it is important that programs needs to be flexible in nature to fit the lo- the manufacturer has labeling that addresses this cal conditions. issue. This labeling decision needs to be made by the manufacturer and not as a regulatory requirement. Another key tactic in a resistance management pro- Industry Goals gram is to monitor key pest populations for changes in sensitivities to specific technologies or products. The agricultural chemical industry has several For example, when pyrethroid resistance was first goals in the development and implementation of re- observed in cotton, the manufacturers formed a task sistance management programs. One goal for resis- force that monitored the insect resistance levels and tance management implementation is to have insect coordinated resistance management strategies. resistance management be a key component of the Other key tactics for resistance management pro- company’s product stewardship departments. Man- grams include product labels and educational litera- agement plans that delay or minimize resistance are ture. Resistance management statements on product an integral part of new product development and cur- labels can limit the applications to be made in a sea- rent product maintenance. As part of new product de- son as well as indicate the types of chemistries that velopment, sensitivity baselines are established and should be avoided or alternated. Educational litera- monitored after the product is registered. Another ture that increases awareness to resistance manage- example of company product stewardship efforts in ment issues should be developed and used in train- resistance management is the annual review of prod- ing programs. Industry should involve the research ucts and resistance management plans. Other efforts community in the development of resistance manage- in product stewardship include the development of ment strategies. It also is important that industry resistance management plans for transgenic plants; communicates with regulatory authorities about the such plans include technical teams who oversee the status of resistance management efforts. deployment of insect resistance management plans in the field. Certain companies also have resistance management pages on their websites.
95 96 5.4 Industry’s Perspective on Insect Resistance Management and Its Implementation
Barriers and implementation of insect resistance management programs. The involvement of the U.S. Environmen- In spite of the efforts of industry to develop resis- tal Protection Agency (EPA) and other regulators in tance management programs that are flexible and insect resistance management discussions has elevat- adapted to local conditions, barriers to resistance ed the importance of this subject. The EPA also has management implementation still exist. Knowledge realized the complexities of insect resistance manage- about resistance management is increasing, and re- ment and has kept most insect resistance manage- sistance management plans need to be reviewed reg- ment proposals on a voluntary or trial basis. Grow- ularly and to reflect the state of the current science. ers provide valuable practical input and need to be The complexity of insect biology, cropping practices, more active in insect resistance management plans. and the size of the systems makes it difficult to have The technical community should help in the develop- one plan that fits every situation. With this complex- ment of flexible programs based on sound science. ity, it is a challenge to implement resistant manage- ment plans efficiently and to make programs as prac- tical and flexible as possible. Another barrier in the Conclusions implementation of resistance management plans is relying on a single tactic in order to save costs. Delaying the development of pest resistance or Some barriers to resistance management imple- maintaining susceptibility is the desired goal of all mentation are strict regulations that may conflict stakeholders in this debate. But good intentions with local resistance management programs. If the turned into permanent regulations or requirements label has mandated recommendations for resistance in this situation create as many, or more, problems management that conflict with local resistance man- as they solve. History has demonstrated clearly that agement programs, there will be confusion as to which resistance situations can change rapidly and that at is the correct program to use. least annual reviews and revisions to programs are Industry views restrictive regulations as decreased needed. The rapidly escalating costs of implement- incentives for development of new insect management ing insect resistance management, borne as they are options. Resistance management regulations have today by the manufacturers, growers, universities, the potential to increase the amount of time and re- and extension services, can decrease the incentive for sources required for the development and mainte- developing and adopting new insect management nance of new crop protection technologies that would options and distract from more effective educational be important tools in insect management. Potential- efforts. ly, restrictive regulations may add little or no benefit Resistance management is a dynamic, evolving sci- to managing insect resistance and may decrease or ence that should be widely debated at all levels with- delay the number of new options for resistance man- in academia and by industry and growers. Industry agement. has the most to gain or lose from actions or inactions. Resistance management regulations also can add Industry can manage and react to resistance issues a significant burden to the registration process and more effectively without specific regulatory require- be a deterrent for minor use registrations. Addition- ments. For resistance management to work effective- ally, with strict regulations, there will be a shift ly, there needs to be active participation and buy-in of resources to the implementation of resistance from the entire crop protection community, including management programs that would focus on a less- growers, crop consultants, commodity groups, univer- effective tactic, that of label enforcement rather than sity and extension personnel, and industry. education. Another consequence of complex insect resistance management programs is that growers will not use these programs. The net result is that the growers will not avoid using the product but will avoid using the insect resistance management plans. Growers are aware of the costs of IRM practices and will imple- ment those practices that are affordable, simple, and flexible. Industry holds the view that there needs to be par- ticipation from all stakeholders in the development Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 97
5.5 Role of Stakeholders in Resistance Management: Pesticide Manufacturers Gilberto Olaya
Introduction and possible resistance management guidelines are discussed. A new fungicide is ready to be introduced Fungicide resistance risk studies, the establish- into the marketplace when an agreement between ment of baseline sensitivity distributions, and the im- technical managers and sales managers is reached plementation of resistance management strategies based on studies completed on the efficacy of the fun- are key components of the research, development, and gicide, the resistance risk, and marketing plans. commercialization of a new fungicide in the agrochem- One of biggest limitations for implementation of re- ical industry today. sistance management programs is the lack of regis- Several factors associated with either the fungicide, tered alternative chemistries to rotate or to tank mix the plant pathogen, the epidemiology of the disease, with the fungicide at risk. For example, there were or the programs implemented for disease control could no suitable alternatives to azoxystrobin for control of contribute to the development of resistance to a fun- foliar diseases on pistachios in California. Due to this gicide. In many cases, fungicide resistance is caused limitation, the resistance risk was high for strobil- by misuse of the product. In the past, growers de- urins on this crop. Another barrier to resistance man- creased the impact of fungicide resistance by switch- agement implementation could be the sales price of ing to new, very efficacious products. But few new alternative chemistries. The potential fungicide part- fungicides are reaching the market today because ner for rotation or tank mixing with the fungicide at higher quality standards are required for the regis- risk may be very expensive, thereby limiting the ac- tration of new fungicides, including increased safety ceptance of the resistance management program. for users and the environment. This circumstance often leads growers to cut use rates The implementation of fungicide resistance man- or to stretch spray intervals. agement programs requires that several different fun- To identify the potential for resistance development gicides with different modes of action be available to as new fungicides move closer to market introduction, the user to avoid or delay resistance development. Re- resistance risk studies are implemented. These stud- sistance management is essential for stewardship and ies focus on historic information on fungicides in sim- preservation of the fungicide products. General re- ilar classes of chemistry as well as on studies on the sistance management guidelines can be drawn from mode of action. If this information raises any level of estimated resistance risk studies, which consider all concern, isolates of candidate fungi are collected for the chemical and physical characteristics of the fun- use in baseline sensitivity studies and evaluation of gicide and all factors related to the biology of the fun- potential cross-resistance. The specific company or gus and the epidemiology of the disease. Fungicide the industry (if fungicides with a similar mode of ac- resistance should be managed at the local level, how- tion are already in the market or are to be introduced ever, according to the epidemiology of the disease in shortly) can then design and implement a strategy to the area, the use pattern of the fungicide, and the minimize the risk of resistance. After the commer- overall fungicide spray programs used by growers. cial launch of the product, the resistance management program that was implemented could change depend- ing on the evolution of resistance. Lack of fungicide Barriers to Resistance resistance risk studies and/or characterization of the Management Implementation mode of action could affect the prediction regarding the stability and inheritance of the resistance and The positioning of a new fungicide in the market whether resistance is triggered by changes at the tar- usually generates much debate between scientists and get site. marketing managers in the industry. The potential Education of the user, disease control profession- number of sprays, number of sequential applications, als, consultants, regulators, extension plant
97 98 5.5 Role of Stakeholders in Resistance Management: Pesticide Manufacturers pathologist, distributors, and technical and sales per- North America QoI subgroup of the Fungicide Resis- sonnel is very important for the success of resistance tance Action Committee (FRAC) also has been very management implementation. Some users believe active in the implementation and modification of re- that resistance is not their problem and that new and sistance management programs and has been work- better products are coming from industry. The users’ ing toward the industry goal of product stewardship focus is on the control of the diseases in their crop in and prolonging the market life of QoI fungicides. this season and in their profitability. This short-sight- Fungicide producers also need to develop resistance ed view can lead to development of resistance, which management programs to fit the programs currently impacts other growers and the entire agrochemical in place. For example, there are new fungicide prod- industry. ucts that are in the same cross-resistance group as the current fungicides on the same crop but that target different diseases. For example, there are QoI inhib- Goals of Resistance itors with strength on the Oomycetes versus the QoI Management Implementation inhibitors that are more efficacious on Ascomycetes and Basidiomycetes. Resistance develops in plant pathogens after a high Fungicide resistance management programs im- selection pressure is exerted by the use of a fungicide. plemented by industry also need the support of uni- The goal of any resistance management program in versities and extension plant pathologists. Our ex- industry or any other institution is to manage the perience with universities and the QoI-based potential for resistance by decreasing the selection fungicides has been very positive and has helped us pressure, which is usually done by decreasing the ensure the proper use patterns of the fungicide by number of applications. growers. Industry also brings the message about the There are critical studies that help in the imple- appropriate use of the fungicides to sales and techni- mentation of resistance management. These studies cal service personnel inside the company. This pro- focus on the mode of action, resistance risk assess- gram of resistance management is key for the success ments, baseline sensitivity distributions, and the of the fungicide strategy and needs to be improved identification of the mechanism of resistance. Stud- further in the future. ies of this nature are conducted by industry and in After all studies on efficacy and resistance are com- many cases, in collaboration with universities. The pleted, the recommendations for use and resistance research programs can focus only on key representa- management are in place, and collaboration and tive plant pathogenic fungi. Another component re- guidelines are in agreement with university and reg- quired to implement resistance management proper- ulatory agencies, we wait for resistance developments ly is the identification of the level and extent of hoping that they do not show up. cross-resistance among related members of a fungi- cide chemistry. This information guides the use of fungicides and decreases potential selection pressure Goal of Others in Fungicide through restricting the use of fungicides in the same Resistance Management cross-resistance group. For example, most of the stud- ies described here have been conducted on the newly A major objective of agrochemical producers is to developed QoI fungicides. Predictions about resis- match a resistance management strategy with state tance development based on those studies have been recommendations and IPM programs. The growers relatively accurate whereas with other fungicides, the would better handle single and local resistance rec- information has been limited and has failed to lead ommendations. Users, disease control professionals, to the appropriate prediction. consultants, regulators, extension plant pathologists, After fungicide resistance management programs distributors, and technical and sales personnel all are developed for the targeted crop diseases, resis- need to get all involved and contribute to resistance tance monitoring usually is initiated to monitor the management. performance of the product and to detect early devel- University research could include studies on mech- opment of resistance. Industry has been proactive in anisms of resistance and influence on epidemics as the implementation of resistance monitoring with well as studies on baseline sensitivity distributions. studies done in-house or in collaboration with univer- Proper education and training of fungicide users as sities. Resistance monitoring has helped to improve well as personnel from the different sectors involved or optimize resistance management guidelines. The Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 99 in agriculture is required. Extension bulletins always have been an excellent part of grower education. Fungicide resistance management by industry and working groups also should be supported by FRAC International. The EPA needs to evaluate label lan- guage on the resistance management recommenda- tions. Industry and users could be benefit if the re- view of the resistance recommendations could be expedited. 100
5.6 Barriers to Implementation Marvin Schultz
Introduction Barriers to Implementation Weed resistance to herbicides concerns many sec- The HRAC believes there are a number of barriers tors of the agricultural community: growers, advisors, that prevent the implementation of effective weed researchers, registration authorities, and the agro- resistance strategies, and it looks for ways to allevi- chemical industry. Weed resistance is of concern to ate these barriers as part of its goals and objectives. herbicide manufacturers as it may adversely impact One major barrier is the lack of sufficient informa- the sales and longevity of a product if not managed tion available to understand the resistance complex properly, decreasing the number of tools available for and mitigation practices. A number of factors impact growers to ensure an abundant food supply and prof- the development of weed resistance to various herbi- itable production. Resistance management strategies cides. It is important to understand how these fac- must be effective, reliable, practical, and economical. tors contribute to the development of the management These strategies, along with the necessity of proper strategy appropriate for a specific situation. For in- stewardship, must then be communicated effectively stance, how do characteristics of the herbicide (mo- to the grower. lecular, physical, and environmental) impact resis- To help achieve these goals, the Herbicide Resis- tance development? How does the way we use tance Action Committee (HRAC) fosters cooperation herbicides impact resistance development? Can we between industry, government researchers, advisors, identify which weeds, modes of action, and cropping registration authorities, and growers. The HRAC is systems are most prone toward selection for resis- an industry-based group chartered by CropLife Inter- tance? Why does resistance occur in certain field national to foster stewardship and to communicate situations but not in other fields with similar use the basic principles of herbicide resistance including patterns? Can we predict where or when herbicide resistance will occur? One of the goals of the HRAC • Promotion of a responsible approach and proper is to work with academic researchers to identify these use of herbicides; information gaps and to promote incentives, includ- • Support and participation in research, conferenc- ing funding, to improve our pool of knowledge es, and seminars, which increase understanding about what these factors are and how they impact and scientific knowledge of the causes and miti- each other. gation of herbicide resistance; Another barrier, related to the lack of technical in- • Communication of the causes and consequences formation already mentioned, is that herbicide resis- of herbicide resistance; tance management strategies need to be tailored, tar- • Communication of herbicide resistance manage- geted, and practical in each particular situation to be ment strategies and support for their implemen- effective—a “one-size-fits-all” approach is not appro- tation through practical guidelines; priate. From a global viewpoint, herbicide-resistant • Promotion of active collaboration between public weeds are a minor issue, because only a few weeds and private researchers, especially in the areas have developed resistance in a few areas, fields, or of potential problem identification, management patches. At a local level, however, it can be a signifi- strategy development, and implementation; and cant issue. Therefore, resistance management strat- • Facilitation of discussion of proper product stew- egies must be tailored to a specific situation and lo- ardship among industry representatives. cation. The risk of resistance varies among products, weeds, cropping systems, and cultural practices. Blanket prescriptive approaches cost growers money and may not be appropriate for all products. Instead,
100 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 101 strategies must be clear, flexible, and practical for the awareness of herbicide resistance and product stew- grower to use. As a result, the HRAC believes that ardship is a primary goal of the HRAC. rigid mandatory federal regulations are not the ap- propriate method to improve implementation of resis- tance management strategies. Instead, tailored strat- Stakeholders’ Interests egies based on product characteristics and grower The HRAC views the goals of other stakeholders practices should be developed and promoted through to be similar in many cases to its own. For instance, cooperative industry efforts where appropriate. there is general consensus that all sectors of the ag- Still another barrier is that growers generally care ricultural community have a role to play in weed re- about resistance only when it happens on their farm, sistance management. The ultimate audience is the and also they believe that when it does occur it usu- grower who needs to hear consistent resistance man- ally can be managed fairly easily. This perception is agement messages from all stakeholders. The HRAC based on their history and experience with weed re- believes that other stakeholders also would like to see sistance problems. In most cases, alternative prod- industry expand its educational efforts to raise grower ucts or practices have been and still are available to awareness of weed resistance and encourage proper manage weeds that become resistant to a particular product use, and we share this goal. The HRAC be- herbicide. And growers generally believe that herbi- lieves that other stakeholders share its view that in- cides with new modes of action will continue to become creased research is needed to improve our under- available to control the resistant weed. It also is im- standing of the mitigation and economics of weed portant to note that most herbicides control many resistance management. At this time, there is a lack target weed species and maintain most of their value of consensus regarding the role of federal regulations to the grower despite cases of resistance to a particu- in herbicide resistance management. Some stake- lar weed species. In this way herbicides may differ holders believe that resistance management can from other pesticides such as insecticides and fungi- be mandated through regulations, whereas others cides that have fewer target species, and growers may believe, as does the HRAC, that a more flexible perceive the impact of weed resistance to be less seri- and tailored approach fostered through industry is ous than pesticides with a smaller number of selec- appropriate. tive target pests. Perhaps most importantly, grow- ers will focus on short-term economics and most often will optimize weed control for a current season. Pre- ventative resistance management strategies may re- quire additional input costs without any obvious ben- efit to the grower’s bottom line. One of the goals of the HRAC is to improve grower understanding of potential product-specific resistance risks through educational efforts. Another goal is for industry to continue its investment in research and development to identify and fill market needs. To that end, it is important to consider that mandatory regu- latory requirements are likely to burden and delay the registration process, thus negatively impacting effec- tive herbicide resistance management by discourag- ing research investment and registration of new weed control tools. Finally, one of the greatest challenges to implemen- tation is simply education. Management strategies, once developed, need to reach multiple levels of the distribution chain including manufacturers, retailers, extension personnel, consultants, farm managers, landlords, and growers. Furthermore, educational efforts need to be tailored to reach each of those tar- get audiences. Enhancing education efforts to raise 102
5.7 The Environmental Protection Agency and the Pest Management Regulatory Agency: Pest Resistance Management Goals and Challenges Sharlene R. Matten and Pierre Beauchamp
Introduction Under FIFRA, the EPA has considered the devel- opment of pesticide resistance in its regulatory deci- The U.S. Environmental Protection Agency (EPA) sions, but it does not have an official overall policy or and the Pest Management Regulatory Agency standard data requirements in place yet. Although (PMRA) of Canada are committed to promoting and lacking an overall policy, the EPA has endorsed and endorsing proactive pesticide resistance management. promoted the use of proactive resistance management Under the auspices of the North American Free Trade to decrease the likelihood of resistance and potentially Agreement (NAFTA), the United States and Canada the use of pesticides that pose higher risks to humans have joined together to develop and publish guidelines and the environment. It is in both the user’s and the for voluntary pesticide resistance management label- public’s interest to prevent or to manage pesticide ing for implementation in North America: PR Notice resistance. The EPA has developed voluntary resis- 2001-5 and DIR 99-06, respectively. The development tance management labeling guidelines based on the of these guidelines was part of the activities of the rotation of mode of action as part of a joint activity Risk Reduction Subcommittee of the NAFTA Techni- under NAFTA. These guidelines are published as cal Working Group on Pesticides. Both countries be- EPA Pesticide Registration Notice 2001-5 (USEPA lieve that a harmonized approach based on rotation 2001). The EPA believes that this approach to resis- of target site/mode of action for pesticide resistance tance management is sound and would be highly ben- management would help reduce the development of eficial to pesticide manufacturers and pesticide users. pest resistance. A uniform approach to resistance Because of the adoption of the Food Quality Pro- management labeling will help support a harmonized tection Act (FQPA), pesticide resistance management approach to joint registration decisions in any or all has become more critical to achieving the EPA’s per- NAFTA countries and worldwide. formance goals. This is because FQPA has led to the elimination of many uses of two broad-spectrum pes- ticides classes, organophosphate and carbamate, that Overall Pesticide Resistance were key components of resistance management pro- Management Goals grams. Pesticides within these two classes have been noted to pose risks to human health and to the envi- The Environmental Protection Agency ronment. Loss of these broad-spectrum pesticides will put more selection pressure on pests to develop resis- The EPA endorses and promotes the use of effec- tance to the remaining pesticide product classes, es- tive, proactive resistance management for pesticides pecially the narrower spectrum, reduced-risk class- to delay pest resistance. For resistance management, es, and transgenic crops. Without broad-spectrum the EPA may examine under the Federal Insecticide, pesticides, such as the organophosphate insecticides, Fungicide, and Rodenticide Act (FIFRA) whether pest minor pests are becoming more major problems and resistance will pose an increased environmental or resistance is expected to increase. Pesticide resistance human health risk or if resistance would lead to an is, thereby, expected to increase in importance as the increase in pesticides that not only would increase pol- diversity of broad-spectrum active ingredients de- lution but also might pose higher human health and creases and the target spectrum is narrowed. environmental risk. Two of the EPA’s strategic goals are (1) to ensure the protection of food safety from the use of pesticides including adoption of reduced-risk pesticides and biopesticides and (2) pollution preven- tion. Resistance management helps preserve these goals.
102 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 103
The Pest Management Regulatory Agency include resistance management; (4) use up-to-date technical information regarding resistance manage- A key goal of the Canadian PMRA is to prevent or ment, provided by technical representatives from in- at least delay the development of pest resistance. It dustry, academia, extension, and consultants; and (5) is an important part of sustainable pest management report any suspected instances of resistance. and, in conjunction with alternative pest management The EPA and the PMRA believe that this approach strategies and integrated pest management pro- to resistance management is sound and would be grams, can make significant contributions to decreas- highly beneficial to pesticide manufacturers, pesti- ing risks to humans and the environment. The PMRA cides users, and the public. It is hopeful that regis- believes that all pesticides registered for commercial/ trants will embrace this approach and work with the agricultural use should incorporate resistance man- EPA and the PMRA to implement the PR Notice 2001- agement statements and the Mode of Action (MOA) 5 and Regulatory Directive 99-06 for all relevant prod- classification system on the label as specified in DIR ucts. Both the United States and Canada believe that 99-06 (Health Canada 1999) by January 1, 2004. The this approach is an important element of internation- primary focus of this goal—implementation of DIR 99- al harmonization. A uniform approach to resistance 06, the voluntary pesticide resistance management management labeling will help decrease the develop- guidelines based on mode/site of action rotation—is ment of pest resistance and support a harmonized considered to be the linchpin of any program to delay approach to joint registration decisions in any or all or to prevent development of pest resistance. In ad- NAFTA countries and worldwide. dition, the PMRA believes that resistance manage- To date, the PMRA has approved nearly 300 pesti- ment should be part of the core pesticide use training cide labels having either the classification and/or the at all levels: users, industry, academia, provincial, and resistance management labeling statements. This federal. Finally, the PMRA feels that it is important represents approximately 18% of the 1,600 eligible to harmonize resistance management efforts under pesticide products registered as approved for agricul- NAFTA, as well as globally. tural uses in Canada. In contrast, the EPA has ap- proved only 6 pesticides labels with both the classifi- cation and resistance management labeling Status of Mode of Action statements. The PMRA has set a target date of Jan- Labeling under NAFTA uary 1, 2004 for full implementation of these guide- lines. The EPA has not set a target date, but feels The EPA and the PMRA endorse and promote the that harmonization with the PMRA is important. use of voluntary pesticide resistance management strategies for all pesticides to mitigate the develop- ment of pest resistance. One such pesticide resistance Other EPA Resistance management strategy is the rotation of mode of ac- Management Regulatory tion of pesticide classes to decrease the selection pres- sure posed by reliance on only one class of chemistry, Activities thus increasing the likelihood of resistance. As pre- viously noted, the EPA and the PMRA developed vol- Section 18 Policy Revisions untary resistance management labeling guidelines based on the rotation of mode of action as part of a The EPA also believes that effective resistance joint activity under NAFTA. These guidelines are management should be considered in its issuance of published as EPA Pesticide Registration Notice 2001- emergency exemptions under Section 18 of FIFRA. 5 (USEPA 2001) and Canada Regulatory Directive This is not currently allowed under existing Section DIR 99-06 (Health Canada 1999). These voluntary 18 regulations, however. Approximately 30–50% of guidelines provide a numerical system of classifica- the 600 Section 18 requests per year cite resistance tion to identify the mode of action of the pesticide on problems with existing registered alternatives as part the front panel of the label and to provide resistance of the basis of their request. The EPA is in the pro- management labeling statements in the “Use Direc- cess of developing criteria for public comment as to tions.” The labeling statements encourage users to when an unregistered pesticide could be used for the (1) rotate between pesticides with different modes of purposes of resistance management. action; (2) monitor for loss of field performance; (3) use integrated pest management (IPM) programs that 104 5.7 The Environmental Protection Agency and the Pest Management Regulatory Agency: Pest Resistance Management Goals and Challenges
Mandatory Insect Resistance incidents of resistance as a way to gauge the extent Management for Bt Crops of resistance in the United States to a particular pes- ticide. Since this change went into effect, the EPA has In contrast to the program for synthetic pesticides, received approximately 50 substantiated reports of the EPA has mandated an unprecedented insect re- resistance. sistance management (IRM) program for Bacillus thu- ringiensis (Bt) plant-incorporated protectants (PIPs), or Bt crops. The EPA believes that Bt IRM is impor- Barriers to Proactive Resistance tant because of the threat insect resistance poses to Management Implementation the high benefits and low risk of using Bt proteins in transgenic crops (Bt PIPs) and in Bt microbial sprays. The EPA and the PMRA have identified several im- Both IRM for Bt crops and pesticide resistance man- portant barriers to implementation of proactive resis- agement for pesticides, in general, were discussed at tance management strategies. These barriers are the the Office of Pesticide Program Dialogue Committee following: (PPDC) in July 1996. At this meeting, the PPDC in- dicated that the EPA should play a role in pest resis- 1. A lack of endorsement and implementation of pro- tance management, but that it should not make re- active resistance management strategies because sistance management mandatory for all instances for of different stakeholder values, beliefs, interpre- all pesticides. The PPDC agreed, however, that genes tation of available data, and cost. from Bt were in a special category and that protec- 2. A lack of research funding and focus for develop- tion of their susceptibility was in the “public good.” ment and implementation of proactive resistance The EPA has mandated seven basic IRM elements for management strategies. Bt PIPs: (1) structured refuges, (2) grower agree- 3. Industry reluctance to develop and promote the ments that impose binding contractual obligation on adoption of voluntary resistance management the grower to comply with the IRM requirements and guidelines, PR Notice 2001-5 and DIR 99-06. annual affirmation of these obligations, (3) grower 4. A general lack of information on the effectiveness education programs, (4) grower compliance assurance of resistance management strategies. This means programs, (5) annual resistance monitoring pro- that proactive resistance management strategies grams, (6) remedial action plans should resistance be are adopted before they can be validated in the suspected or confirmed, and (7) annual reports (sales, field. research, compliance, monitoring). 5. In the United States, a lack of stakeholder con- sensus on the need for EPA involvement in resis- tance management. This is especially true for Special Review mandatory resistance management require- The EPA also has considered pesticide resistance ments. when determining whether an unreasonable adverse 6. In the United States, a lack of a clear resistance effect could occur if registered uses of a pesticide are management policy. Under FIFRA, the EPA has suspended or cancelled as part of a Special Review the authority to examine the likelihood of resis- process under FIFRA Section 6 (Matten et al. 1996). tance (resistance risk) and the consequences of re- To date, pesticide resistance was a primary consider- sistance to human health and the environment as ation in assessing the benefits of the continued use of well as the benefits of resistance management. the ethylene bisthiocarbamate fungicides (e.g., man- cozeb, maneb, metriam, and nabam). There were no reports of fungicide resistance to this class, which is Challenges to Proactive widely used in fruit and vegetable crops. Resistance Management Implementation Adverse Effects Reporting In 1998, the EPA revised its adverse effects report- The EPA and the PMRA have identified several im- ing rule (FIFRA Section 6[a]2) to require that substan- portant challenges that must be tackled before there tiated incidents of resistance be reported to the Agen- can be effective implementation of resistance manage- cy. The Agency’s goal was to use the substantiated ment. These challenges are the following: Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 105
1. The need for appropriate incentives to implement roughly the same in the United States and in Cana- proactive resistance management strategies. For da, are described briefly here. example, one possible incentive mechanism would be to use promotional programs for adoption of re- 1. Industry: The primary role of industry is to pro- sistance management that would reward users vide leadership, education, and financial support and the pesticide industry. This may be achieved for the development and implementation of pro- through regulatory and nonregulatory mecha- active resistance management strategies. This nisms. should include development of new reduced-risk 2. The need for a more consistent dissemination, dif- active ingredients that can be used in existing in- fusion, and adoption of resistance management tegrated pest management programs, as well as strategies. That is, pesticide education programs innovative ways to use nonchemical alternatives should have a strong focus on proactive versus re- to minimize resistance development or its spread. active pesticide resistance management and its 2. States/Provinces: The primary role of states/prov- long-term (vs. short-term) economic and environ- inces is to provide regulatory oversight, leader- mental benefits. ship, education, and financial support for the de- 3. The need for clearly identified ways to minimize velopment and implementation of proactive the use of negative marketing and sales cam- resistance management strategies. paigns that impact the adoption of proactive re- 3. The U. S. Department of Agriculture (USDA)/Ag- sistance management strategies. That is, there riculture and Agri Food Canada (AAFC): The pri- is a concern that if one registrant adopts resis- mary role of the USDA/AAFC Canada is to pro- tance management strategies for products with- vide leadership in active research, education, in a particular mode of action class, they will be extension, funding, and promotion of proactive at a competitive disadvantage if another regis- resistance management and its integration into trant with products in the same class does not. pest management programs. These federal in- There should be a “level playing field.” stitutions should be especially important in devel- 4. The need for further discussion of resistance man- oping innovative pest management technologies agement strategies, policies, and mode of classi- for minor uses that are financially less attractive fication systems on a global scale. to industry. 5. The need for a greater focus on proactive resis- 4. Academia and Extension: The primary role of ac- tance management for reduced-risk pesticides in- ademia and extension is to perform research on cluding both chemical and biopesticides. In the proactive resistance management strategies (i.e., United States, implementation of the FQPA has testing and evaluation). In addition, both aca- led to a decrease in the number of broad-spectrum demia and extension are critical to pesticide edu- active ingredients used for pest control. This has cation and implementation of resistance manage- led to a greater focus on resistance management ment strategies. This includes evaluation of the for the remaining active ingredients, including cost effectiveness of different pest control technol- reduced-risk pesticides and biopesticides includ- ogies as well as dissemination and distillation of ing plant-incorporated protectants (e.g., Bt crops) resistance management information into simple, that are more targeted, focus on a single target effective messages. site of action, and are believed to be more prone 5. Consultants: The key role of consultants is to pro- to resistance development. The same changes vide advice to growers on appropriate resistance also are occurring in Canada through the reeval- management practices and strategies for a par- uation of already registered products. ticular farming operation. They are critical to the successful implementation of proactive (or reac- tive) resistance management strategies. Roles of Other Stakeholders in 6. Users: The primary role of users is to adopt re- Resistance Management sistance management strategies. They are the key to the success of any resistance management The EPA and the PMRA have indicated that all program whether it is proactive or reactive in na- stakeholders have important roles to play in develop- ture. ing and implementing proactive (or reactive) resis- 7. Public Interest Groups: The primary role of pub- tance management strategies. These roles, which are lic interest groups is to foster debate and demand 106 5.7 The Environmental Protection Agency and the Pest Management Regulatory Agency: Pest Resistance Management Goals and Challenges
accountability by all stakeholders to use resis- tance management to provide for continued and improved food safety and environmental health.
Summary
The EPA and the PMRA believe that proactive pes- ticide resistance management is important to de- crease the likelihood of resistance. Both countries have adopted similar voluntary resistance manage- ment guidelines based on rotation of mode of action, PR Notice 2001-5 and DIR 99-06. To date, these guidelines have not been adopted fully; approximately 300 labels in Canada and only 6 labels in the United States have used these voluntary labeling guidelines. There are many barriers and challenges to the suc- cessful adoption of resistance management strategies, and all stakeholders play a vital role in the develop- ment and implementation of proactive strategies.
Literature Cited
Health Canada. 1999. Voluntary Pesticide Resis- tance-Management Labeling Based on Target Site/ Mode of Action, DIR99-06,
5.8 Issues in Pest Resistance Management Eldon E. Ortman
Introduction Questions about Pest Resistance Resistance management has taken a more promi- When pest resistance occurs, one question should nent role in integrated pest management (IPM) pro- be, “Why did this happen?” Generally, the primary grams with an apparent ever-increasing number of oc- situation that leads to pest resistance is the unilat- currences of pest resistance or adaptation to control eral or overuse of a single pest control tactic. Why is tactics. The development of pest resistance is a con- there “overuse”? The tactic’s “silver bullet” proper- stant reminder of the plasticity of biological systems. ties in terms of cost, ease of use, and efficacy are a Pest resistance, or adaptation to control tactics, is not common cause. Overuse may have resulted from a confined to resistance to synthetic pesticides, al- lack of viable alternatives, inadequate education, reg- though that arena provides the most obvious exam- ulatory constraints, or a profit-maximizing position. ples of this phenomenon. Adaptation has occurred In many parts of the world the overriding consider- with resistant cultivars created by traditional plant ation for using a control tactic is cost. New chemis- breeding mechanisms and to cultural pest control tries are expensive to develop, market, and deploy. practices. The most notable recent example of the The target specificity of some newer products is prob- latter is Western corn rootworm (WCRW) laying eggs lematic for growers/users in areas where economics in soybean fields, which can have a significant impact is limiting. An inexpensive, broad-spectrum product on the subsequent year’s corn crop. In a significant may be affordable and provide control, whereas a area of the Corn Belt, the use of (an annual) soybean/ more targeted material frequently is more costly and corn rotation as a primary option for managing the may require use of additional tactics. WCRW is no longer efficacious. Another question might be, “Has IPM failed when pest resistance occurs?” It seems that some of the basic elements, including the use of multiple manage- Recommended Resistance ment tactics and a pragmatic education on the biolo- Management Strategy gy and ecology of the target pest as components in an IPM program, may not have been in a highly opera- What should be our resistance management tive or productive mode. strategy(s)? I propose drawing on and paraphrasing A third question might be, “Is the best approach to the PAMS approach used to describe IPM: preven- pest resistance management voluntary or regulato- tion, avoidance, monitoring, and suppression. Tak- ry?” The voluntary approach is the most desirable ing those actions that will prevent or avoid the devel- when all involved parties in the public and private opment of pest resistance should be the first and sector can reach consensus on the right approach. A primary approach. Monitoring is an important step; basic belief is that people will do the “right thing” if however, resources likely will be a limiting factor in there are good options and these options are clearly the development and deployment of sampling and articulated (i.e., a good educational program). There monitoring technology. Therefore, it will be critical have been problems in gaining broad-scale commit- to prioritize the pest/tactic combinations that are the ment in a voluntary program, however. Further, some highest priority for a monitoring activity. Finally, options may be costly or problematic to implement, suppression/remediation must be done when a tactic and thus there may be a need to consider incentives. fails. The basic causes for failures should be identi- For example, when an alternative presents an in- fied and the more sustainable approaches to mitigat- creased cost to the user, is it appropriate for a pro- ing pest problems should be sought. ducer to bear the entire burden for a higher-cost al- ternative when the basis is a general benefit to the environment or to the general public? If it is “a
107 108 5.8 Issues in Pest Resistance Management public good alternative,” would it be appropriate for sian fly. the public to share some of the costs? In addition, In addressing the matter of pest resistance man- some alternative tactics or materials may present a agement it would seem most advantageous and sus- greater risk to production. Is some form of insurance tainable to place the primary emphasis on research a viable option? The regulatory approach is fraught and education through public and private sector col- with complications: who regulates, and on what ba- laboration rather than regulation. Furthermore, pre- sis; who pays; how is enforcement implemented; what vention should be of higher priority than remediation. is the cost, etc? The cost for a potentially broad regu- latory approach likely will be prohibitive.
Questions about Regulation
Currently there is a limited number of resistance management plans logged in an enforcement or reg- ulatory mode. Bacillus thuringiensis (Bt) is a prime example for which there are significant questions about regulation. Some questions have included
•Why is Bt regulated in a genetically modified or- ganism (GMO) but not as a spray or dust? •Why are other pesticides that are created, for ex- ample, by the culturing of a natural organism not required to have a regulatory protocol for resis- tance management? •Why are other GMO crops not required to have a resistance management plan in force? • Why are resistance management plans not in place for regulation of synthetic chemicals when already there are hundreds of examples of pest re- sistance?
There are numerous significant issues that would need to be addressed in developing the basis for a reg- ulatory approach.
A Final Example A voluntary, research-based, genetic deployment of insect-resistant wheat has been employed in a limit- ed east/central wheat area. Host plant resistance to Hessian fly developed via conventional breeding has been the primary control tactic for decades. An an- nual survey was conducted to monitor the Hessian fly field population for virulent strain development. Al- ternative, resistant, host genes were deployed in sub- sequent years when virulent strains were detected. This approach made it possible to stay ahead of pest evolution and maintain a traditional host plant resis- tance breeding program as a viable control for Hes- Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 109
5.9 Interregional Research Project No. 4 Program and Minor Crops: Developing Choices for Pest Resistance Management Michael P. Braverman, Daniel L. Kunkel, Jerry J. Baron, and Robert E. Holm
Introduction in minor crops because multiple pesticide applications often are needed to protect minor crops at a level nec- The Interregional Research Project No. 4 (IR–4) essary to maintain their marketability. In many mi- was organized in 1963 to obtain regulatory clearanc- nor crops there may be no registered product or only es for crop protection chemicals on specialty or minor one for a given pest, thereby limiting the choices avail- food crops. Most of the minor crops are fruits and veg- able for resistance management. etables. This paper focuses on how the IR–4 enables Although varietal selection, cultural practices, and growers to make choices in pest control products. all forms of pest management are important, IR–4 fo- More specifically, it describes how biopesticides can cuses on registration of crop protection chemicals. The be used in pest resistance management. The objec- IR–4 is the only program dedicated to assisting the tive of this paper is to describe some aspects of the registration of crop protection tools for minor crops. IR–4 activities on the registration of conventional crop By increasing grower options, there is at least the op- protection chemicals and biopesticides and how they portunity to develop a pest resistance management pertain to pest resistance management. The issues program. The IR–4 program is involved with both addressed include biopesticides, reduced-risk prod- conventional pest management products and biopes- ucts, crop grouping, and biotechnology. ticides. Considering the resistance management problems and limited choices, both conventional chemicals and biopesticides are needed to develop a Choices in Pest Management meaningful resistance strategy. In the early 1990s the IR–4 program focused on defending older products As part of growing crops, producers make choices going through reregistration and had approximately about varieties and cultural practices that can influ- 100 new conventional pesticide uses per year. As a ence crop yield. Pest management is based on mak- consequence of the Food Quality Protection Act, a ing choices among available pest management tools strategic partnership was developed between the IR– including chemical and biological methods. The de- 4 program and the Environmental Protection Agen- velopment of resistance to pesticides can be influenced cy (EPA). The cornerstone of the partnership was the by those choices. Subsequently, the management of decision to focus on reduced-risk pesticides for the pest resistance also is based on making choices in con- magnitude of residue projects that facilitated the reg- trol techniques management. If cultural methods are istration process. As a consequence of the reduced- not adequate and pesticides are deemed necessary for risk strategy and other efficiencies since the year control, the proper tools must be available so that 2000, the IR–4 program has had approximately 500 choices can be made. Whereas poor choices may in- new uses per year (Figure 5.9.1) (IR–4 2003). The crease the risk or perpetuate resistance problems, development of “Super Crop Groups” that involve the lack of available options can leave producers without development of residue data on reduced data sets has the ability to choose. Because choice is the key com- successfully hastened registrations for spinosad and ponent of pest resistance management, the availabil- azoxystrobin, and expanded uses of glyphosate into ity of conventional crop protection chemicals and bi- crops that have no preexisting registered products. opesticides is critical for pest resistance management. Registration costs, low acreage, limited potential for return on investment, and greater liability of minor crops have limited pesticide development in minor crops. Resistance problems are more likely to occur
109 110 5.9 Interregional Research Project No. 4 Program and Minor Crops: Developing Choices for Pest Resistance Management
Figure 5.9.1. The number of new uses for conventional pesticides obtained through IR-4 petitions to the EPA, 1990 to 2001. Biopesticides often involve label expansion, such as adding a new pest or new crop to the label. Through the grant pro- gram, IR–4 project members have been involved in- Biopesticides are a key component in pest resis- directly in the development of the most widely used tance management. In the 1970s IR–4 helped obtain biopesticides in production agriculture. tolerance exemptions for Bacillus thuringiensis (Bt) in minor crops. In 1982, the IR–4 formally started a biopesticide program. In 1995 the biopesticide pro- Reduced-Risk Products gram was expanded to include a grant program. The biopesticide program focuses on assisting registrants Many of the newer, reduced-risk pesticides have through the EPA regulatory process and has a grants narrow modes of action. Many registrants of strobil- program to promote the development of new biopes- urin fungicides have constructed their labels with re- ticides and expanded product uses. In 2002 the IR–4 sistance management in mind. In order to maintain was instrumental in obtaining 91 new biopesticide the use of their products they have limited the num- uses. Registrants need to develop efficacy data on ber of applications per crop. One criterion of being their products to feel confident about placing addition- classified as a biochemical biopesticide by the EPA is al pests on their label. Many biopesticide registrants that the product has a nontoxic mode of action (Jones are small venture capital companies and may consist 2001). Biopesticides tend to have broader modes of of a single individual. There have been over $2 mil- action, are generally safer on beneficial organisms, lion in grant funds distributed to university and U.S. and offer less selection pressure for resistant individ- Department of Agriculture (USDA) researchers, with uals within the pest population compared with con- over $400,000 in 2003 alone. The grant program ventional products, making them useful in resistance emphasizes efficacy studies. Projects are classified as management programs. Implementing biopesticides early or advanced stage. Early-stage proposals are into a pest resistance program requires adoption by for products that have an incomplete toxicology pack- growers. As they are with conventional products, age and are not registered yet. Advanced-stage growers are keenly interested in the efficacy of the projects are with products that are registered, and products they use. Part of the problem in adoption of Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 111 biopesticides is that in the attempt to use them, there Grouping Symposium to develop new crop groups and is a corresponding drop in replacements for conven- expand current ones (Markle et al. 2002). tional products. Conditions such as the age, size, and Risk avoidance is a key part of pest management concentration of a pest influence the ability of a bio- decisions, and there are multiple barriers to biopes- pesticide to obtain adequate control. The potential ticide adoption that are beyond the scope of this pa- range and consistency of efficacy should be considered per. Incentives for adoption such as eco-labeling and in the selection of a biopesticide. Some biopesticides improved market value would lead growers toward are suited better for use under early season, low-lev- incorporating biopesticides into their pest manage- el pest pressure, or in rotation with conventional prod- ment program and thus indirectly influence pest re- ucts. The early season use may extend the time that sistance management. a pest is kept below economic thresholds through the Several biopesticide products for which the IR–4 combination of its own activity and the maintenance has assisted in the registration process (Benmhend, of beneficial insects or organisms. Use as a rotation- 1999) have been adopted or show great potential for al product helps decrease the selection pressure to- adoption. They also offer pest management solutions ward resistance through repeated use of convention- under conditions prone toward resistance. Kaolin al products. A more proactive approach to the use of (trade name Surround) currently holds an approxi- biopesticides would be helpful in avoiding pest resis- mately 70% market share for the control of pear psylla tance problems. There are other incentives that grow- in pears of the Pacific Northwest (Sekutowski, D. ers need to consider with biopesticides. Biopesticides 2003. Personal communication). Kaolin also has been also can be used in situations when a short reentry found effective in decreasing glassy winged sharp- interval is needed to allow cultural practices to be shooter adults and oviposition (Puterka et al. 2003). conducted. In addition, using biopesticides close to Part of the IR–4 process involves obtaining project harvest can help avoid possible residue problems from request forms from public sector scientists, commod- a conventional product. As part of the IR–4 Biopesti- ity groups, and growers. Mites are a common pest in cide Grant Program, it is requested that proposals be many minor crops. Mites are very prone to having re- designed in an integrated pest management (IPM) sistance problems due to multiple generations being program with biopesticides and conventional products produced through a cropping season and great fecun- to facilitate use in resistance management. Greater dity. Sucrose octanoate and sorbitol octanoate are two emphasis on IPM approaches to project design will be sugar esters that have shown good activity on mites emphasized in the future. and soft-bodied insects. Thymol (Api Life VAR) is a natural product found in thyme and is effective in control of Varroa mite in honeybees. Thymol for hon- Crop Grouping eybees has generated more grower project requests than any biopesticide or conventional product in the The risk for pest resistance in ultra-minor crops is 40-year history of the IR–4 program. It has been ap- even greater because they are more likely to have very proved by the EPA for a Section 18 (an emergency use) few pest control options. The IR–4 program has been in several states. Varroa mites already have been addressing this issue through the use of crop groups. found to be resistant to fluvalinate (a pyrethroid) and Crop groups are a system of crops with similar botan- coumaphos (an organophosphate), which currently ical and cultural potentials for pesticide exposure and are under a Section 18. This highlights the need for dissipation modes, such that they can be grouped for the EPA to take a more proactive stance in allowing purposes of setting residue tolerances. Within each for multiple Section 18 registrations whereby a con- crop group there are representative crops that are ventional pesticide and a biopesticide could both ob- used for magnitude of residue studies, and the resi- tain Section 18s as pest resistance management tools. due levels on the representative crops are used to set This is especially important because Section 18s are tolerances for all members of the crop group. With- commonly issued to products that have new chemis- out crop grouping there would have to be individual tries and modes of action. The limitation to this one tests on each crop. There are currently 19 crop groups new mode of action accelerates the selection pressure in the United States and 20 in Canada. There still that can lead to pest resistance problems. In addi- are many crops such as tropical fruit that are not cur- tion, pests that need Section 18 approvals often are rently in an official crop group, making it difficult to hard to control and are in outbreaks due to the pests’ obtain registrations. The IR–4 recently held a Crop preponderance to develop multiple resistance to pre- existing pesticide chemistries. When successful, new 112 5.9 Interregional Research Project No. 4 Program and Minor Crops: Developing Choices for Pest Resistance Management chemistries are developed, other analogs are rapidly and cotton. Its success also has decreased the devel- produced; therefore, the selection pressure during opment of new herbicides for major crops. Develop- Section 18 use can impact an entire new line of prod- ment of new herbicides for minor crops is dependent ucts. on having new products developed for major crops first, because major crops dictate the decision of com- panies to move forward with the registration process. Impacts of Biotechnology Therefore, the sharp decrease in herbicide develop- ment has greatly lessened the chance of finding new Biotechnology has had positive and negative im- herbicides for minor crops. Most of the herbicides pacts on pest control for minor crops. Several pest currently used in minor crops were developed over 25 control systems have been developed and some have years ago. been adopted for minor crops (Table 5.9.1) (Gianessi Some of the newer products that have adequate se- et al. 2001). Several of the developed technologies lectivity in vegetables are sulfonylurea herbicides. have not moved forward due to grower concerns about These herbicides are inhibitors of branched chain potential consumer reaction. Unlike major crops such amino acid synthesis by inhibiting a single enzyme as corn or soybeans, which can be stored for long pe- acetolactate synthase. The dependence on a single riods, most fruits and vegetables are perishable. Any enzyme system has made sulfonylurea herbicides negative public perceptions of most minor crops would prone to develop resistance in weeds. Although the be disastrous. Plant incorporated protectants are timeline for development of pest resistance general- evaluated in the Biopesticides and Pollution Preven- ly has been shorter for insecticides and fungicides, the tion Division of the EPA, the same division that eval- lack of new herbicide products makes the long-term uates microbial and biochemical biopesticides. Plant- prospects for herbicide resistance increase. Overall, incorporated protectant data packages tend to have the percentage of acres that have benefited from specialized studies resulting in greater resources be- biotechnological approaches has been vastly greater ing needed for their review. This also has delayed the for major than for minor crops. time required to have a new product complete the In summary, the key to avoiding pest resistance review and registration process for non-transgenic problems is to have choices for pest management. The microbial and biochemical biopesticide products. IR–4 program helps to register products for pest One of the more prominent biotechnology advance- control in minor crops so that a greater number of ments has been the development of crops resistant to choices are available. These choices are essential for glyphosate, which has provided an effective and less- the development of a pest resistance management expensive weed control program for corn, soybean, program.
Table 5.9.1. Potential and adopted biotechnology-derived pest management in minor crops (Adapted from Gianessi et al. 2002)
Pest category Approved and adopted uses Potential uses
Diseases Papaya, Squash Citrus, Raspberry, Stone fruit Insects Sweet corn Broccoli, Eggplant Weeds Canola Sweet corn, Lettuce, Strawberry Nematode ——— Pineapple Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 113
Literature Cited Benmhend, D. 1999. Kaolin. Biopesticides and Pol- lution Prevention Division of the Environmental Protection Agency,
5.10 Pesticide Education and Training Programs Monte P. Johnson
Pesticide Safety Education Pest Resistance Survey Program Information Thirty PSEP Coordinators responded to a recent survey on pest resistance training activities that Each state/territory has a Pesticide Safety Educa- asked the following questions: tion Program (PSEP) Coordinator who directs the training activities and typically conducts training ses- • In your pesticide safety education sessions, do you sions for commercial pesticide applicators. Training address pest resistance? Yes—30; Comments: re- for private pesticide applicators—typically growers sistance management is covered extensively; par- applying to their own land—mostly is done through ticularly with vegetable and fruit growers; prima- county extension offices by county agriculture agents. rily private recertification. Commercial applicators apply pesticides as a business • If you cover pest resistance, is it in initial train- and are grouped into specialized categories such as ing, recertification training, or both? Both—20; ornamental and turf, agricultural plant, aerial, or Initial—2; Recertification—8; Comments: covered right-of-way. After successfully completing training in initial training materials; covered in IPM; cat- and/or an examination, both private and commercial egory specific for commercial applicators. applicators will be certified to purchase, use, and su- • Is pest resistance covered in private or commer- pervise the use of restricted-use pesticides. The PSEP cial training or both? Both—25; Private—1; Com- Coordinators also conduct recertification sessions, mercial—2; No Response—2. Comments: com- which allow applicators to retain their certification by mercial only now, but plans for private; accumulating a certain number of credits during the emphasized more for private applicators; empha- certification period. sized more for commercial applicators. Annual PSEP funding sources include Environ- • How do you cover pest resistance? Inclusion with mental Protection Agency (EPA) pass-through funds organic agriculture so conventional growers un- at $1.88 million, other federal funds (such as compet- derstand impact; discussed with label comprehen- itive grants) at $1 million, state funds at $3.93 mil- sion, pesticide mode of action (MOA), IPM; discus- lion, and other funds (such as fees, etc.) at $2.34 mil- sions on alternative pest management practices; lion. The PSEP staff supported by these funds give examples, usually diseases and MOAs; dis- includes 55 full time equivalents (FTEs) by the EPA cuss how resistance happens, cover species of re- funds and 356 FTEs by other funds. The program also sistant pests; resistance management statements is supported by 1,956 volunteers. on labels, complying with resistance management The PSEP Coordinators submit work plans and an- for transgenic crops; discuss how to assess MOA, nual reports through the Performance Planning and cross-resistance, multiple resistance; discuss her- Reporting System. From these reports for fiscal year bicide resistance in weeds; resistance manage- (FY) 2002, we learned that the number of people re- ment presented as a cost-savings tool; discussed ceiving initial certification training was 114,859, the as part of pest control failures; have weed special- number receiving recertification training was ists or entomologists cover it; covered in study 311,634, and the number receiving noncertification guides. training was 285,394, resulting in a total of 711,887 people.
114 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 115
5.11 Role of Stakeholders: State Pesticide Regulation David Scott
Role of the Pesticide State Barriers to Resistance Lead Agency Management Implementation
The current role of pesticide state lead agencies The experience of the SLAs suggests that regulat- (SLAs) in the issue of resistance management (RM) ing effective use is a difficult task. In addition, regu- seems to be somewhat limited. The SLAs are respon- lating prudent use also is difficult. A good example sible primarily for pesticide product registration and of this is a review of states that have tried to man- pesticide use regulation in their respective states. For date or regulate integrated pest management (IPM). the most part, state product registration efforts are Although IPM is a concept that most states embrace, the result of state laws that originally were intended developing rules and regulations to make it happen to provide truth-in-labeling for the consumer. States has not been successful consistently. As a further sample pesticide products for purity, focusing prima- complication, pest resistance may be regional in na- rily on verifying the correct amount of active ingredi- ture, thereby requiring regional management plans. ents and screening for contaminants. Most SLAs rely This does not bode well for national product labels. on the U.S. Environmental Protection Agency for From a regulator’s perspective, motivating pesti- human and environmental screening and assuranc- cide users to read and follow all parts of a label has es. States also rely on the marketplace, researchers, been a life’s work. Labels in general, however, already and user and producer industries for efficacy issues, are too long and contain far too much advisory infor- including pest resistance issues. In certain instanc- mation. The longer the label, the less likely the user es, however, states require the submission of efficacy is to read it. In addition, most regulators have limit- data for registration when exaggerated or doubtful ed interest in lots of advisory language. claims appear on product labels. Indiana is one of those states. The SLAs also are active in product registration re- Goals of Resistance lated to the federal processes involved in the Federal Management Implementation Insecticide, Fungicide, and Rodenticide Act (FIFRA) Section 18 (emergency exemption) registrations and Simply stated, the goals of RM implementation FIFRA Section 24c (special local needs) registrations. should be to keep safe products effective and avail- Although it has not been an issue in many registra- able for as long as they are needed. With a record of tion decisions to date, a question for future consider- limited success in dealing with pesticide efficacy is- ation by states will be whether RM can be an accept- sues, most SLAs would prefer to limit regulatory in- able emergency exemption for a product. volvement. A more reasonable goal would be to edu- The other area for SLA involvement in RM is pes- cate and motivate pesticide users to implement RM ticide use regulation. Currently the use of RM lan- for their own benefit. guage on product labels is voluntary, and where the label language does exist, it is advisory rather than mandatory. Therefore, there is no role for state en- forcement.
115 116
5.12 Role of Extension in Management of Pest Resistance Walter R. Stevenson
Introduction Resistance Management Plans The economical production of healthy, pest-free Resistance management must be a team effort. plants depends on the careful integration of multilay- Success over time will require a careful integration ered components into effective pest management pro- of thinking and actions of stakeholders including grams. During the past 50 years, however, some in growers and their representative organizations, pest agriculture often have viewed pest control as a “sil- management consultants, pesticide manufacturers ver bullet” exercise in which a single tactic, typically and suppliers, the U.S. Environmental Protection dependent on a new pesticide or a new family of chem- Agency (EPA) and government regulators, consum- istry, solves a long-standing problem. If a particular ers, and those involved in university research and material fails in a few years because of pest resistance extension, all playing essential roles. It is in the best issues, which is often the case, the sense is that there interest of all parties, present and future, that pest will soon be another pesticide with equal or even management systems remain as effective, safe, and greater efficacy. And so goes the treadmill of opti- as economical as possible. mism, pesticide evolution, and always-changing pes- In the past few years, there have been important ticide use patterns. Resistance management has long breakthroughs in the development of “next genera- been a concern in the world of entomology. In recent tion” pesticides that are safer to the applicator, the years, however, as new herbicide and fungicide chem- environment, and consumers, and that often replace istries have evolved from multisite to single-site tox- more risky pesticides targeted by the Food Quality icants, weed scientists and plant pathologists have Protection Act. Often these “reduced-risk” pesticides begun to pay much closer attention to managing pest are characterized by a highly specific mode of action resistance. that can be overcome quickly by a single mutation in Agriculture has a dismal record in managing resis- contrast to older, broader-based chemistries that have tance of pests to pesticides. In short, the insects, been used for years without the appearance of resis- weeds, and plant pathogens we are attempting to con- tance in the target pest populations. The challenge trol are winning the battle. Pest resistance is turn- before us is how to move the newer, safer chemistries ing out to be much more complicated than envisioned into well-integrated pest management programs in and the tools we are currently employing to manage which we can avoid selecting for pest resistance and resistance are simply not meeting the challenge. As ultimately losing these new materials. Because all the flow of new pesticide chemistries slows and older stakeholders lose when pest resistance becomes wide- chemistries are no longer available for use because of spread in a pest population, proactive approaches toxicological and environmental concerns and regu- must be developed for stability in pest management latory restrictions, a crisis is unfolding that needs programs. immediate focused attention. The question of the hour focuses on how we retain the efficacy of those pesticides currently in use and what will be our plan Role of Extension for use of new chemistries currently in the develop- mental pipeline so that we can continue to achieve an The traditional role of extension in pest manage- acceptable level of pest control. ment programs involves working with producers in understanding the pest problems they face, the con- trol measures that are the most economical, effective, and safe to use, and the integration of multiple con- trol tactics with crop production practices. Extension personnel regularly evaluate new and currently avail-
116 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 117 able chemistries for efficacy, effect on yield, and crop sity research and extension faculty and growers, it is quality and then formulate state- or region-wide pest ironic and worrisome that the chemical industry also management recommendations based on extensive is going through aggressive consolidation leading to field trials and evaluation. Results of their observa- loss of field research programs and expertise and vast tions and experience are shared with producers at reductions in technical service to growers. There are educational meetings and field days, and in a variety intense marketing efforts directed at larger-scale cor- of publications. Because of the complexity of pest re- porate farms at a time when there is less direct con- sistance concerns and the need to pay much closer tact with smaller-scale family farms that often need attention to the structure and effectiveness of resis- hands-on assistance in planning their pest manage- tance management plans, however, the role of exten- ment options. It is absolutely critical that collabora- sion in this arena needs to evolve at a rapid pace. tive relationships evolve between stakeholders with There is a critical need for extension to build upon common goals and interests for the effective manage- its historical role and to serve as a leader, drawing ment of pest resistance to become a reality. I see ex- together all stakeholders so that proactive, collective tension acting as a catalyst in developing these rela- thinking can develop to assure routine, widespread tionships and playing the lead role in ensuring the compliance with effective resistance management development and implementation of effective resis- strategies. Some of the areas where extension can tance management tools. play a critical role include the following:
• Establish the baseline of pest sensitivity to new pesticides prior to their introduction on the com- mercial market and continuously monitor chang- es in discriminating dosages. • Provide critical evaluation of new pesticide chem- istries in field trials with rate studies to determine the dosage needed for effective pest control. • Cooperate with the EPA and pesticide manufac- turers on focused Experimental Use Permit (EUP) programs before broadscale marketing of new products to better judge how new materials will fit into local and areawide crop pest management programs. • Evaluate the likelihood of emerging resistance for each new chemistry (Resistance Risk Profile) based on projected use patterns, mode of action, and known genetics of target pests. • Formulate Resistance Management Plans before commercial sales of each new chemistry, with spe- cial focus on plan efficacy in the first few years of widespread use. • Work with pesticide manufacturers in the design of labels to include information on use patterns and resistance management information. •Work closely with growers so that they are fully aware of the importance of resistance manage- ment and what they can do to decrease the risk of pest resistance.
The proactive management of pest resistance is not a goal that is easily achieved given how pesticides are marketed and used by most pest managers. At a time when extension resources are dwindling and there is less, rather than more, interaction between univer- 118
5.13 Regulation, Research, and Funding Thomas O. Holtzer
Introduction they had done research specifically related to a particular issue and that particular work had been Rather than simply providing my own opinions, I supported financially by an involved corporation. Al- made a few phone calls to people who have been in- though there was some appreciation for the fact that volved heavily in academic research on resistance there could be a perception of conflict of interest, there management for some time. From these people I remained the frustration that those who actually gleaned some good ideas and insights, and I appreci- know the most about the system under consideration ate their willingness to share their thoughts with me. often are excluded from the advisory process. What I will provide here is a distillation of some of A much bigger issue for the research community those conversations. relates to support for research. There is a strong sense that the need for sound research far exceeds the avail- able funding—particularly regarding research that is Researchers’ Interests longer term in scope and focused on the intermediate area between narrow product-oriented efforts and So what did I find out? Not surprisingly, it is safe very basic investigations. to say that academic researchers are most interested in finding out how things work—that’s why they do science. And many also are excited about focusing on Funding how particular systems work so that the information they generate can help solve some very practical prob- The obvious next question is: “Where should ad- lems. Just as clearly, academic researchers do not ditional funding come from?” There were only two want to be policymakers and regulators. On the con- sources that surfaced as potential possibilities: the trary, most are very happy to have someone else do- federal government and industry. Programs within ing that job. the U.S. Department of Agriculture (USDA)/Cooper- Researchers are fully aware that policymakers and ative State Research, Education, and Extension Ser- regulators have to weigh information and make judg- vice (CSREES) that could expand funding for resis- ments using factors and perspectives in addition to tance management research are the National the sciences of ecology, evolutions, genetics, genom- Research Initiative, regional IPM grants, and the Bio- ics, and the like. That is as it should be. Often, how- technology Risk Assessment program. The U.S. En- ever, I heard the somewhat frustrated plea from aca- vironmental Protection Agency (EPA) also could be- demic researchers that they certainly want decision come more involved in funding. Industry sources were makers to understand the data and the interpretation seen as including pesticide manufacturers, corpora- of that data from a scientific perspective, and they tions that provide seed for genetically modified (GM) want that research-based information to be given full crops, and pesticide users such as farmers and pest and fair consideration in the decision process. In other control operators. words, they want decision makers to use the contri- Among the researchers I interviewed I found a va- butions of science to the fullest extent possible. The riety of ways to look at the funding picture, depend- researchers also felt that they have much to offer de- ing on whether the researcher saw the benefits of re- cision makers in an advisory role, and that sometimes search on resistance management as flowing decision makers do not make extensive enough use primarily to the public or to private individuals or cor- of this expertise. porations. Benefits to the public are those that occur Along these lines, perhaps the most frustrated re- when, for example, the federal government builds a searchers were those who felt they had been exclud- road that benefits everyone. With respect to resis- ed from being part of the advisory process because tance management, public benefits may be such
118 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 119 things as longer useful lives of cheaper pesticides or Partnership Opportunities GM crops that we already know a lot about (and therefore understand the risks associated with their use). Prolonged useful lives of some products (e.g., In the spirit of one of the main themes of the Fourth products known to pose low risks) would keep food National IPM Symposium held just before this meet- costs lower and keep environmental and human ing, I would raise the obvious idea that there is a health concerns in check. Another public benefit of wonderful opportunity for a public-private partner- longer useful lives of pesticides would be that public ship. My suggestion would be that the pesticide and funds have been spent to register pesticides through GM crop producers join with the CSREES and the the EPA and to expand the registration of pesticides EPA to establish and fund a Resistance Management through the USDA’s Interregional Research Project Research Program. The program would invest in re- 4 (IR–4) program. So by investing in resistance man- search in the intermediate range of basic to applied— agement research, the public would be protecting its focusing on understanding the principles of resistance previous, considerable investment in these pesticides. and addressing the most pressing applied research Research that decreases pesticide resistance prob- needs. It would not target narrow, specific product- lems may benefit private individuals and corporations oriented research, however. Detailed research prior- by increasing profit potential, by prolonging the prof- ities for the program would be developed by represen- itability of the manufacture and sale of a particular tatives of industry, the CSREES, the EPA, and other pesticide, or by prolonging the profitability of the pro- stakeholders. duction and sale of a particular GM crop. Farmers Manufacturers would establish a funding mecha- might benefit from the prolonged effectiveness of a nism (or request Congress to do so on their behalf) pesticide or GM crop that is cost effective from their that would provide half the total dollars through a perspective. mechanism functioning essentially like a sales tax on Regarding benefits to industry, in my discussions pesticides. The CSREES and the EPA would join with with researchers I heard the idea that research that industry (including farmers and other users) to re- improves our understanding of resistance manage- quest that Congress fund the other half of the program ment primarily benefits the manufacturers because through a new investment of federal general dollars. their products remain profitable longer; but also I If the messages we received at the Fourth Nation- heard a contrasting perception that pesticide manu- al IPM Symposium are valid, Congress would look facturers actually benefit from the development of quite favorably on a plan that brought together the resistance. This is because the development of resis- pesticide and GM crop industries with the CSREES tance gets rid of cheaper products that have been in and the EPA. the marketplace for a while and that may be off patent. Resistance facilitates replacement of these products by new ones that provide a higher profit potential to manufacturers. In the course of my conversations, an old idea re- surfaced. It goes something like this: a healthy re- search program could be established from a modest check off or tax on pesticide sales receipts. There also was a variation of this idea: the EPA could increase the fee on new registrations and reregistrations and use this source of funding to support a research pro- gram. In some of my conversations, however, the oth- er side of the coin came up—that the beneficiary of resistance research was primarily the public and that the public should therefore fund the research out of general funds (not out of a tax on pesticide sales or a fee on registrations). 120
6.1 Industry’s Suggestions for Solutions and Working Together Gary D. Thompson, Graham P. Head, and Caydee Savinelli
Introduction tactics or there is one tactic that is more cost effective, providing an incentive for growers to over- The creation of this CAST conference and the large rely on it. volume of work on resistance issues in recent years clearly illustrates that many of us believe that insec- ticide resistance can have serious consequences for a Solutions crop production segment and for the company that developed the product. You will, however, hear widely There is no easy solution to working together and diverse opinions on how best to address resistance coordinating efforts; it requires a lot of hard work. threats. The logic behind certain opinions comes from Controversy is common and consensus is rare when the fact that no compound has been totally lost be- it comes to resistance issues. Industry has found, cause of the local and transient nature of resistance. however, that for working on broad issues such as re- It also is notable that susceptibility often can be man- sistance management, participating in CropLife task aged after it develops. A good example is mite resis- forces such as the Resistance Action Committees tance to dicofol, or Kelthane, that developed over thir- (RACs) is much more effective than working alone as ty years ago. Today, Kelthane still can be used a individual companies. An individual company does limited number of times in most locations and re- not have the resources or the need to focus continual- mains a valuable effective tool if growers follow the ly on resistance management, and a single voice of- crop- and pest-specific recommendations. Regardless, ten has much less impact than a united one. there is widespread consensus in industry that resis- The Insecticide Resistance Action Committee tance management is good for business and that it is (IRAC) also has facilitated workshops on resistance most effective when practiced on a proactive basis management for various audiences. We have found with the first introduction of a product or trait. that large audiences and broad general debates can raise awareness, but they typically result in little progress towards tangible solutions. Likewise, at- Current Barriers tempts to provide general strategies on solutions through national regulations are very limited in their Before addressing solutions to barriers and im- effectiveness due to the exceptions required for di- proved ways of working together it is helpful to read- verse crop production systems. What has worked well dress briefly some of the current barriers seen by in- are workshops for growers and continued support of dustry. Often cited are that the crop systems are too focused local or regional programs that involve grow- large, complex, and dynamic and that it is impossi- ers. It is the growers’ understanding of the value to ble to get consensus across all parties involved. Our sustainable profitability for their farms and their knowledge is continually increasing, options are neighbors’ farms that changes behavior from only changing, and it ranges from difficult to impossible using the least expensive or most effective tactic all to validate resistance management theories due to the of the time to something more sustainable and appro- long evolutionary processes involved. With this back- priate for insect resistance management . These lo- drop, it is very difficult to get companies to work to- cal or regional programs must be practical, simple to gether—much less all stakeholders including grow- implement, and flexible, with regular reviews that ers, consultants, distribution, extension personnel, adapt to changing situations. the U.S. Department of Agriculture–Agricultural Re- The IRAC also has found value in coordinating ef- search Service (USDA–ARS), university research, and forts on bioassay methodologies, conducting surveys, regulators—and to focus our limited resources on the and providing a coordinated response when resistance task. The other root cause is that there are too few first emerges. The IRAC has provided seed money to
120 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 121 start research programs but feels that this effort should continue to be dominated by land-grant universities and the USDA–ARS. The IRAC also has played a role in education by developing literature and videos, and by placing ads in the popular press. Edu- cation is the activity that can have the greatest im- pact. Historically, extension services have had the lead role, but they have struggled to take on new projects during a prolonged budget cutting era. The needs here should be assessed and perhaps ap- proached with more funding and partnerships on cer- tain aspects. It is generally known what we should do and not do to manage resistance, but the informa- tion is not well distributed and constant reinforce- ment is needed to change behavior from a short-term focus to a longer-term sustainable one. There are a few pest/crop situations for which there are too few tactics to keep pests off balance. Indus- try generally views these as economic opportunities and devotes resources to finding new tools, whereas the U.S. Environmental Protection Agency and the IR–4 have tried to decrease barriers to entry through preferred treatment for minor crops and vulnerable crops and through Section 18 justifications. All of these efforts should be reviewed with a longer-term approach rather than a crisis management ap- proach—the latter being all too common. Additional resources could be put to good use in many endeavors, but we believe that both current and additional resources should be focused on increased education and support of proactive local/regional pro- grams. Many educational efforts could be general in nature and combine efforts from insecticides, herbi- cides, fungicides, and general integrated pest manage- ment messages. The local/regional programs must be driven by the commodity groups and state extension services with support from industry, academia, and other stakeholders as needed. 122
6.2 How Can We Alleviate Barriers? Roger P. Kaiser
Introduction in their volatility, longevity, intrinsic activity, systemicity, and curative ability, but they all share The first ideas that come to mind when asked about the same mode of action. The limits of market size, “alleviating barriers” to implementing resistance the development of resistance, and the high cost of management are not solutions, but problems. Our completing the hundreds of tests necessary for regis- current economic system erects significant barriers to tration have cut the number of new product candi- cooperation between individuals and companies as we dates to a handful. Resistance always is considered compete in the marketplace. In the short term, one when evaluating new compounds for development. man’s gain is another man’s loss. When it comes to The net result with the QoIs is that more resources resistance management, however, the long-term loss are going into the development of chemistries with of any one class of chemistry or tool for controlling pest different modes of action and only a few QoIs will populations is a loss for everyone. reach the marketplace. Any discussions of resistance management must be With regard to fungicides, most new products have held against the background of our economic system. resistance management on the label. There is a rec- We operate within a system that values individual ognized procedure for establishing new “Working freedom, personal property, and patent rights. This Groups” within the North American Fungicide Resis- system is successful, and many alternatives are avail- tance Action Committee (NA-FRAC) and the Interna- able to our growers because of competition between tional FRAC organizations. Label changes are slow, companies. and sometimes the process is painful, but significant progress has been made in reaching agreement on label language and guidelines. Resistance manage- Current Efforts ment is just one aspect, just one small extension of integrated pest management. Good product steward- Although there is some benefit from identifying the ship rewards both the customer and the companies problems and defining exactly what is wrong with our selling the products. current resistant management strategy, I will begin People implement resistance management, not la- instead with a brief review of our current efforts and bels, laws, or educational programs. And people are successes. We must recognize that there are already strongly influenced by the culture that surrounds severe constraints on the selection and development them. Much like the movement against smoking, of new pest control products. Besides the basic hur- which has changed the culture from smoking as an dles of efficacy, environmental impact, and toxicolo- accepted practice to one of social disfavor, and like the gy, most companies monitor early-stage materials for “recycling” movement (though not as successful), loss of activity due to resistance. They may conduct which has made people aware of the limitations in “high pressure” trials in which materials are subject- resources and the need to reuse and conserve, resis- ed to intense selection and pests are monitored for tance management responds to our culture. resistance development. They may run models or lab- The best example of a cultural shift in the pathol- oratory trials that predict resistance. In all instanc- ogy area of the agricultural industry has been the es, resistance management is included when devel- fight against late blight of potatoes. Through educa- oping the business plan and estimating the market tional programs, grower meetings, and discussions size for a new product. over coffee at the local diner, late blight has become The Quinone outside Inhibitor (QoI) fungicide known as a “community disease.” Growers who do not chemistry is a good example. Tens of thousands of an- eliminate cull piles, plow down severely infected po- alogues were synthesized in this area; many could tatoes, or use clean seed and thereby introduce the have a unique fit into the marketplace. These differ pathogen into the township face irate neighbors and
122 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 123 public condemnation. We can do the same for resistance management; it can become a community issue with good stewardship as the goal.
Eliminating Barriers
How do we create this same feeling of community in the resistance management arena? What can we do to eliminate barriers to the adoption of resistance management? Education is key. We must change the culture so that good stewardship is a civic responsi- bility. We must establish resistance management as a community problem with a community solution. Within the pest control service sector this means a strict adherence to the resistance management guide- lines at all levels: the basic manufacturers, the deal- ers, the crop consultants, and the salespersons in the field. We must do what we can, working with the growers to eliminate off-label and nonrecommended uses. When we move the thought process from short- term solution and short-term goals to long-term think- ing, then we will have widespread resistance manage- ment in the field. What should be the role of government in this pro- cess? There is no question that the force of law and the threat of inspections can have a major impact on the adoption of specific behaviors. With resistance management, however, the issue is very complicated. Resistance management guidelines must be tailored to the local situation and the specifics of the pest and crop interaction. This is not an ideal environment for law and inflexible rules. There are certain actions that can help, however. First, the regulatory authorities could streamline the process for label changes. The PR Notice on resistance management gives guidelines for making label chang- es by “notification,” but the language is unacceptable for most pesticide labels. Next, because getting a new product onto the U.S. Environmental Protection Agency work plan has become a major issue, we should discuss adding resistance management as a critical factor for determining “Expedited Review” status. Finally, and this is already underway, we should establish uniform group names and codes for each specific mode of action or cross-resistance group. These actions, along with many of the other fine suggestions offered during this symposium, combined with an educational program and the efforts of our partners in extension and research, will shift the cul- ture of resistance management. Good resistance management will be the norm within the agricultur- al community. 124
6.3 Ways to Work Together Natalie DiNicola
Introduction terials that can be communicated by members of HRAC and by other interested stakeholders. When seeking ways to work together to improve im- A second stewardship goal is to continue to uphold plementation of weed resistance management strat- the transparency of scientific findings. In many cas- egies, there are some general principles that the Her- es, the HRAC members conduct research, either in- bicide Resistance Action Committee (HRAC) believes ternally or in collaboration with universities, to inves- need to be considered. First, it is critical to note that tigate the biochemical mechanism of resistance and herbicide resistance is an issue that affects all stake- to identify alternative control programs for resistant holders. Research- and development-based regis- weeds. This research is made available to the scien- trants, generic suppliers, retailers, growers, extension tific community and to other interested stakeholders agents, and other members of the agriculture commu- through scientific meetings or publications. The nity all have a stake in managing weed resistance. To HRAC will continue this practice to further increase that end, the HRAC believes that there is a benefit to our knowledge pool concerning the factors impacting all stakeholders to promote product stewardship, in- weed resistance. cluding the use of integrated weed management prac- Perhaps one of the greatest contributions the tices. Weed resistance is of concern to herbicide man- HRAC has made has been consistent funding of the ufacturers because it can impact the sales and International Survey of Herbicide-Resistant Weeds longevity of a product adversely if not managed prop- website (www.WeedScience.com) managed by Dr. Ian erly, and members of the HRAC take product stew- Heap. That website catalogues instances of weed re- ardship seriously. The HRAC believes that a balance sistance globally and tracks their trends according to of sound science, agronomic experience, and common mode of action class and weed species. The HRAC will sense should be used to manage herbicide resistance. continue funding this website to serve as a resource An effective resistance management strategy is one for numerous stakeholders worldwide. a grower will implement. The HRAC provides a fo- The HRAC will continue to encourage funding of rum for consideration of these principles and devel- basic research on herbicide resistance, both internally opment of consistent stewardship goals and best prac- and externally, to improve our understanding of the tice recommendations concerning herbicide-resistant resistance complex and to develop appropriate resis- weeds. tance management strategies and their proper imple- mentation. The HRAC will continue to encourage the develop- Goals ment of mode of action-specific resistance manage- ment plans that provide a balance of sound science, The HRAC is committed to a number of goals to agronomic experience, and common sense to manage promote product stewardship. A primary goal is the herbicide resistance. development of educational materials to be used by The HRAC has established regional working all stakeholders. The HRAC has developed a num- groups to focus needs at the local level. These regional ber of educational materials already, including a mode groups, in turn, often interact with an informal net- of action poster, a series of white papers on identify- work of national organizations. The HRAC will work ing, confirming, and managing weed resistance, and to ensure consistency of positions and communica- an HRAC website where interested parties can learn tions across these regional groups. more about herbicide resistance. The HRAC intends The HRAC also has identified certain key steward- to expand its educational efforts with additional ma- ship messages to communicate to growers as part of terials targeted more directly to the grower, such as its resistance management campaign: educational brochures, presentations, and other ma-
124 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 125
• Base weed control recommendations on local needs and use the tools necessary to obtain de- sired weed control. ° Use the RIGHT PRODUCT, at the RIGHT RATE at the RIGHT TIME! ° Use good agronomic principles such as cleaning equipment between fields, using certified seed, scouting, and monitoring. ° Adopt sound agronomic practices such as stra- tegic cultivation, narrow row spacings, multiple herbicides, and crop rotations, as appropriate. ° Do not allow weeds to reproduce by seed or to proliferate vegetatively. Mow or spray noncrop vegetation to prevent seed production.
• Report instances of unsatisfactory control to your company representative for investigation.
The HRAC will continue to implement these goals to foster cooperation among all stakeholders and to improve resistance management implementation in the field. 126
6.4 Eliminating Barriers Roger Carter
This paper represents the views of the membership distributors, and dealers), the U.S. Environmental of the National Alliance of Independent Crop Consult- Protection Agency, the U.S. Department of Agricul- ants. Eliminating the barriers to adopting, develop- ture, and university research and extension person- ing, and maintaining resistance management (RM) nel in each facet of RM is critical to the success of RM practices is paramount for the success of agriculture. programs. Increased communication among all stake- All stakeholders should increase industry and govern- holders is necessary. We should work first in small- mental support in all three phases: development, er units and then in larger ones to facilitate commu- adoption, and maintenance. Financial and technical nication. All information should be transferred in a support is needed. Development of more easily man- timely manner. ageable and profitable tools or alternative treatments Although it takes time and money, RM programs is of primary importance. should be developed as products are developed. Hav- Accepting the role of professional, scientifically ing RM programs in place before a product (includ- qualified, unbiased consultants as a medium to trans- ing transgenics) is marketed and selling that concept port the technology to the end users (growers) will im- as a “package deal” with that product will enhance prove both the flow and the credibility of the informa- acceptance. tion. Continuous training and education of Continuous communication among all stakehold- consultants and growers is necessary; having econom- ers is a must in development, adoption, and mainte- ic incentives for both is a must. The bottom line is nance. Currently there is little dialog among all that if it isn’t profitable for the grower, it won’t get stakeholders in the development stage; most dialog done. is between research and industry, with little input All stakeholders must work in unison. Including from others. growers, independent consultants, industry (majors,
126 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 127
6.5 Lessons Learned: Growers’ Perspective John Keeling
As the Executive Vice President and Chief Execu- • The advent of herbicide-resistant, genetically tive Officer of the National Potato Council (NPC), I modified organism grains has resulted in an exo- thank you for the opportunity to provide remarks to dus from herbicide development for major crops. the Pest Resistance Management Symposium on Because most minor crop chemicals are developed behalf of the National Potato Council and the potato based on research for major crops, this change will growers we represent. I have been asked to address provide additional disincentive for minor product briefly the significant barriers to the adoption development. of resistance management protocols by the potato • There are limited chemistries and modes of action industry. available to producers. Particular chemicals are The NPC believes that effective resistance manage- labeled for a variety of crops, likely giving pests ment is broadly dependent on two key components: some exposure before that product may even be grower education and the adequate availability of crop considered for use on a potato farm. The avail- protection chemicals or biologic agents capable of con- ability of fewer labeled products encourages re- trolling pests of concern. The NPC is strongly com- sistance development. mitted to delivering the education component to grow- • Producer groups lack the financial resources to de- ers. The obstacles to advancing grower education and velop and implement grower education programs. product availability are as follows: • Resistance management requires global planning and thinking. The efforts by an individual grow- • As a minor crop planted on slightly more than er will be insufficient if the grower’s neighbor is 405,000 hectares, potatoes offer relatively low re- not involved. Organizing more-widespread resis- turns to registrants and provide little incentive tance management efforts is difficult, and such to new product development. efforts typically do not have the overall incentives necessary for widespread adoption.
127 128
6.6 Stakeholder Roles in Resistance Management: Time to Get with the Program Charles Benbrook
Introduction Whose Job is Resistance Resistance management is like virtue—everyone Management? recognizes its importance yet it is largely dependent on the actions of others. Susceptible gene pools must Is it industry’s job? No—industry’s job is to discov- be looked at, and managed, as public goods that be- er and bring to market products that will earn a good long to and can benefit everyone. return on their shareholders’ investments. Market- When resistance moves through a population and ing goals almost always will trump the discipline an active ingredient or family of chemistry fails, it is needed for resistance management. Incentives in the important to ask why. Typically, all major players can pesticide industry are all volume and sales driven. argue with conviction that fault lies largely some- Plus, resistance can actually be good for business in where else: that it often renders older off-patent chemistry obso- lete and opens the market to newer, usually higher- • The U.S. Environmental Protection Agency (EPA) priced, proprietary chemistry and/or transgenic solu- was too slow in registering alternatives (especially tions. if a minor use crop); Does industry have a major role to play in manag- • The IR–4 program did not have the resources ing resistance? Absolutely. Their role, indeed their needed to get needed alternatives through the sys- responsibility, is to develop and share the knowledge, tem, or pursued inappropriate priorities; science, and information databases from which sound •A company pushed its product too hard, or a par- resistance management plans can be crafted, evalu- ticularly talented and motivated regional sales- ated, and as needed, upgraded. man was too successful; Companies also must bring into the public arena • Rotational product prices were set too high; the results of their annual monitoring of resistance • Growers were too eager for a simple solution; levels in key pest populations around the world. Some • Prevention-based integrated pest management king-size institutional innovation is going to be need- (IPM) takes too much time and effort because the ed to accomplish this goal, because some companies information needed to make it happen is hard to will resist sharing this data for liability and compet- compile and to interpret properly; itive reasons. But somehow, a safe and acceptable • Resistance pests moved into the area from else- mechanism must be discovered to make this critical where, or are the fault of neighbors who overused information accessible to those working at the front- the product; or, my personal favorite... lines of resistance management. • “I thought the company/extension/my applicator/ Company technical experts need to work more a local IPM scout was watching out for resis- openly with university specialists and IPM practitio- tance.” ners who are monitoring levels of resistance in local areas. The goal is simple and vitally important: cre- So the first barrier to resistance management is ation of accurate, up-to-date databases on resistance pretty obvious—we have to get it straight whose job levels in key target pests in all major production re- it is. We have to make sure that the people and play- gions. Such databases are an essential input in test- ers in the pest management community responsible ing and refining resistance management plans for resistance management (RM), or playing a sup- (RMPs)—what works, what doesn’t, why, and what portive role in RM, have the tools needed to tackle this more is needed? vital challenge realistically. The huge monitoring task looming before us can be accomplished only through teamwork within an area and through networks linking local and regional
128 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 129 teams so that “lessons learned” travel fast and new as well as definitive science showing that resistance insights are shared quickly. Our Wisconsin-Florida management is not necessary. biointensive IPM Risk Avoidance and Mitigation Pro- Are extension specialists and universities respon- gram (RAMP) project is working now to create such sible for resistance management? No—their role is a network focusing on the half-dozen reduce-risk to enable and support grower activity, not motivate chemistries that have made such a big difference in or compel compliance with needed RMPs. Their job vegetable pest management in the Central Sands re- is to generate, access, and integrate information need- gion of Wisconsin and in South Florida. ed to support sound resistance management. Our Is resistance management the EPA’s job? No—the RAMP project team senses that universities and ex- agency’s job is to assess the safety of pesticides as tension specialists need to be playing a more central proposed for use, and when needed, impose and as- role in two ways: (1) making sure that resistance sure compliance with risk mitigation measures. management plans are working, and (2) driving the By virtue of controlling the science that must sup- process of upgrading plans where resistance ratios are port registrations and what goes on pesticide labels, creeping upward. however, the EPA has important roles to play in mak- Universities and extension are the only players in ing sure that sound resistance management practic- the system that can work on behalf of the whole sys- es are identified and adhered to. The deep-set con- tem in defining how the efficacy of resistance man- cern over Bacillus thuringiensis (Bt) transgenics agement plans will be monitored and sustained. They triggering resistance forced the agency to develop should be given the responsibility of designing and technical expertise on resistance and IRM strategies. overseeing the implementation of mechanisms to de- It has also established a key precedence: When cir- tect and deal with resistance quickly and decisively, cumstances warrant, the EPA can and should request such that the integrity of the susceptible gene pool is data on resistance, including genetic and biochemi- protected. They must be the ones charged with blow- cal mechanisms, models, bioassays, discriminating ing the whistle when a train wreck appears imminent dose baselines, and RMP strategies. Such data can and should play a major, formal role in determining and should be assessed prior to approving registra- the scope of necessary additional resistance manage- tions; plus, the data can then be shared with the IPM ment practices. Others must shoulder the task of community in support of initial RM planning. making sure their recommendations are followed. The EPA also plays a key role as pesticide label Are farmers and field IPM practitioners responsi- gatekeeper. The agency deserves praise for recogniz- ble for resistance management? At the end of the day, ing the need to support resistance management yes, they are. through product labels; the joint EPA–Canada effort Only the people making day-to-day pest manage- leading to today’s voluntary labeling initiative start- ment decisions can make resistance management a ed more than 4 years ago. reality. Resistance management is going to take sys- On the topic of the EPA’s voluntary resistance tematic effort, focus, and resources. We cannot legis- management–mode of action labeling initiative, it is late it, mandate it, teach it, or pay for it. The steps worth noting that nearly two years after the policy needed to manage resistance successfully are too com- was finalized, only a few pesticide companies actual- plicated, variable across time and space, and dynam- ly have stepped up to the plate and placed revised ic to capture in laws, regulations, program rules, or labels on products. BASF has the coding scheme on incentives. This nut must be cracked in unconven- two pyraclostrobin (Cabrio, Headline) labels, Dow tional ways. AgroSciences has placed it on one spinosad label, and that’s it—out of more than 10,000 registered products. Three down; 9,997 to go. On the plus side, Syngenta Cracking the Resistance has voiced support for the initiative and expects to Management Nut have several products newly labeled this year. Hopefully one tangible outcome of this meeting will Teamwork in support of farm-level efforts and be a pledge from each of the major companies to add much more fluid generation of, and access to, infor- the coding scheme to all product labels by the end of mation are two essential ingredients in cracking this 2004. If adoption of the scheme remains spotty, the nut. Grower associations and other formal and infor- EPA should impose on the laggards a requirement to mal alliances across growers and their pest manag- submit to the agency all data on discriminating dos- ers are vitally needed to deal with an inescapable re- es and resistance ratios in the company’s possession, ality—human nature. Resistance management 130 6.6 Stakeholder Roles in Resistance Management: Time to Get with the Program requires collective action across landscapes. The re- Many experienced organic farmers have developed sistance management effort is like a chain, no stron- sophisticated, well-balanced cropping systems in ger than its weakest link. There must be a way for which pests simply are not as serious a problem as growers to work together to shore up weak links, and on other farms. For them, minimizing selection pres- sometimes those links will be growers with a noncha- sure to manage resistance is rarely an issue. But lant attitude about resistance. there are many farmers transitioning conventional Whether and how growers and the IPM communi- acreage to organic systems, and most of these grow- ty will deal with cowboys who choose to ignore RMP ers start the process with the substitution of organi- essentials is a major, unresolved issue. As long as it cally acceptable pesticides for synthetic pesticide remains unresolved, the inability to address weak products that are not allowed in organic farming. On links in the RM chain will loom as a major barrier to such farms, the temptation will be great to rely ex- successful, sustained resistance management. There cessively on cost-effective products such as spinosad are actually some useful ideas and mechanisms in the (SpinTor) or Bacillus subtilis (Seranade). In addition, Bt corn Insect Resistance Management (IRM) compli- these farmers will have far fewer chemical rotation ance and remedial action plans, including a process options, so their resistance management options will to prohibit further sales to growers not following IRM be curtailed. requirements, intensification of monitoring when a Consumers and environmental advocates who first case of resistance is found, and county- or region- want to see organic farming expand and thrive need wide suspension of sales and plantings (National Corn to focus attention on the need for targeted research Growers 2002). and education on resistance management practices Do consumers and environmentalists have a role? and strategies compatible with organic farming rules. Not directly, but they do have important supportive The organic farming community needs to quickly ad- roles. They need to help convince legislators to invest vise growers and certifiers of the risk of resistance and in biointensive IPM, which is, after all, the only sus- steps that are essential to avoid it. Without such an tainable way to decrease reliance on high-risk pesti- initiative, resistance to some important new reduced- cides. They need to keep the pressure on regulators risk chemistry likely will emerge from excessive use to identify and deal with high-risk pesticide uses, on a few organic farms, perhaps undercutting future while also working to streamline the registration of sales on both organic and conventional crops. If this reduced-risk and biopesticide products. They also happens, few companies will bother again to go need to recognize that when and how a pesticide is through the added effort and expense required to for- used determines risk outcomes and that resistance mulate a special product line for use on organic farms. management requires diversity in control measures, tactics, and products applied. Although it is simpler to run a campaign just to ban The Goal of Resistance all uses of a given pesticide, sometimes it is prudent Management to leave a few moderate-risk uses on the market, with labels limiting use to specific and narrow circumstanc- Our panel has been asked to address the goal of re- es consistent with recommended resistance manage- sistance management. This is a no-brainer—the goal ment plans. Pre-bloom stone and pome fruit uses of of RM must be to preserve the susceptible gene pool moderately toxic organophosphates are examples, to in target pest populations such that there is no mean- the extent that worker exposure and nontarget risks ingful erosion in pesticide efficacy. When lifeguards can be managed. are recruited and trained, their mission is not defined The public interest community has another key re- as managing the drowning process, their goal is pure sistance management responsibility that is barely on prevention. The same core goal should apply in man- their radar screen. As often-vocal advocates for or- aging resistance. ganic farming, these groups are promoting policy and What does “no meaningful erosion in pesticide ef- marketplace changes that will expand the acreage ficacy” mean in the field? Are we flirting with anoth- devoted to organic cropping systems. Pest managers er Delaney Clause? Pest managers can and should on organic farms have a far more narrow pesticide tool rely as heavily as possible on safe, effective products. kit to work with. As some of today’s most promising The only way a pest manager can tell where the line reduced-risk chemistries gain approval for use by cer- between sustainable use and resistance lies is to push tified organic farmers, resistance management risks limits, a process that will eventually lead to a mea- will be enormous and the challenge immediate. surable loss of efficacy. A “not meaningful,” and hence Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 131 acceptable “erosion of efficacy” is defined as an on prices. increase in resistance ratios that is contained and re- Over time, use of these materials surely will rise, versible through proven and practical resistance man- as will the importance and difficulty of managing re- agement plans. sistance. Charlie Mellinger, in his presentation, sum- In terms of monitoring resistance in the field, a marized our project’s most immediate concerns. Walt “meaningful loss of efficacy” occurs when a pesticide Stevenson outlined some of the steps extension needs must be applied at a higher rate of application to to take, and is taking in Wisconsin, to “ramp up” re- achieve a given level of control, and/or delivers accept- sistance management. Here I describe a new tool we able control over a shorter period of time. In the fu- are developing to support resistance management ture, crop consultants, experiment stations, and com- planning and practice. panies will need to carry out well-designed trials to determine use patterns that impose “over the line” levels of selection pressure. Establishing such resis- Next Generation RMPs tance-inducing use patterns in controlled, contained experiments is a logical way to alert field practitio- We are convinced that RMPs in intensive fruit and ners when it is time to diversify control tactics, as vegetable production regions must quickly evolve be- opposed to just ratcheting upward the intensity of yond alternating pesticide modes of action in a given pesticide use and waiting for growers to get ham- field. Mode of action rotation will remain an essen- mered by a newly resistant population. tial ingredient of resistance management, but will not be enough to sustain efficacy. This is because the movement of pests across landscapes can lead to Wisconsin-Florida RAMP multiple exposures to critical chemistries within a Project RM Goals matter of weeks, highlighting the need for areawide approaches and adherence to recommended RMPs. I am part of a biointensive IPM project focused on Our RAMP project team is developing “Resistance intensive vegetable production systems in Florida and Risk Profiles” that are region-crop-pesticide-pest spe- Wisconsin. Our team includes Charlie Mellinger, cific. Resistance Risk Profiles will be used in two Jerry Brust, Galen Frantz, and twenty-odd scouts ways: (1) to help determine the scope of the specific working for Glades Crop Care in South Florida, along practices and tactics that should be initially incorpo- with several of their grower-clients, and the Wiscon- rated in Resistance Management Plans, and (2) to sin potato IPM team and its grower-cooperators who monitor the efficacy of RMPs over time and help guide have worked together so well as part of the World the process of annually upgrading RMPs, when and Wildlife Fund, Wisconsin Potato and Vegetable Grow- as needed. ers Association, and the University of Wisconsin col- A Resistance Risk Profile will project the likelihood laboration. of resistance emerging based on a pesticide’s use pat- In both Florida and Wisconsin, the registration of tern, mode of action, the genetics of resistance (to the a number of low-impact, reduced-risk pesticides has extent known), and field studies where resistance has set the stage for progress in decreasing reliance on previously been monitored. Annual profile updates high-risk pesticides targeted by the Food Quality Pro- will track changes in discriminating doses and resis- tection Act (FQPA). In particular, rapid adoption of tance ratios. An upwardly trending resistance ratio, the nicotinoid insecticide imidacloprid (Admire, Pro- or evidence of resistance in some other production vado) in the mid-1990s and the strobilurin fungicide region around the world, will highlight the need for azoxystrobin (Quadris) in the late 1990s has greatly more sophisticated measures to further decrease se- and positively expanded biointensive IPM options. lection pressure. In this way, Resistance Risk Pro- Because these products have proved so effective, files and RMPs will evolve in tandem. Field experi- they are now bearing a major share of the control ence will sharpen both. burden for some major pests in both states. Indeed, Some of the information needed to complete a Re- selection pressure already is close to or exceeding the sistance Risk Profile is readily available, but other in- limits of sustainable use. Plus, additional active in- formation inputs will have to be generated through gredients in the nicotinoid and strobilurin families of laboratory research and/or field experience. Annual chemistry now have been registered, with several discriminating dose levels are clearly key data inputs, more coming. We expect even more intense market- and obtaining these data is a major technical and in- ing efforts in the years ahead and downward pressure stitutional challenge. It will require new investment, 132 6.6 Stakeholder Roles in Resistance Management: Time to Get with the Program infrastructure, and cooperation to monitor annual Literature Cited changes in discriminating doses on the scale needed. Our concept of resistance “risk” encompasses both National Corn Growers Association. 2002. Insect the prospect of a resistant phenotype emerging, as resistance management compliance assurance well as the additional pest management and pesticide- program,
Concluding Thoughts
The director of the IR–4 minor crop tolerance pro- gram in the United States, Dr. Bob Holm, has called this the “golden era of pest management” because of the proliferation of highly effective, lower-risk pesti- cides. Reduced-risk chemistries have indeed made enormous contributions in Florida and Wisconsin in lessening the adverse impacts of pesticide use. We are convinced that new resistance management tools and strategies are needed to sustain this golden era of pest management—and sooner rather than later. The tools must be locally adaptable, readily modified, widely used, and annually reviewed and updated. The scope of change must be driven by the rate of loss in the susceptible gene pool and projections of the con- sequences of resistance. New ways must be found to think through resis- tance management challenges on an areawide basis and to implement management interventions strate- gically across time and space, notwithstanding field borders and each grower’s unique perspective on what is really driving resistance, who is responsible for it, or changes needed to prevent it. Major changes in pesticide use patterns driven by exogenous factors such as FQPA implementation and phaseout of methyl bromide have the potential to trig- ger resistance management meltdowns. As a commu- nity, we have to pool resources, knowledge, and ex- periences to place resistance management innovation on the same timescale as that governing change with- in susceptible gene pools. I hope this symposium crys- tallizes our thinking on necessary first steps and re- inforces the need to get moving in building resistance management infrastructure with more than a hope and a prayer of meeting contemporary needs. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 133
6.7 Lessons Learned: Academic Research Perspective Thomas O. Holtzer
In the session on the role of stakeholders, I dis- ried the flour home. When she got there, she cussed barriers from the perspective of academic re- asked, “Who will help me make the flour into search, and my primary focus was on improving the dough?” “Not I,” said the duck. “Not I,” said the level of funding in support of research in the inter- goose. “Not I,” said the cat. “Not I,” said the pig. mediate area between narrow, product-oriented ef- “Then I will make the dough myself,” said the forts and very basic investigations. I suggested that Little Red Hen. And she did. So she put on a much could be accomplished by a partnership bring- white apron and mixed the dough. Soon the ing together the pesticide and genetically modified bread was ready to go into the oven. “Who will crop industries as well as the U.S. Department of Ag- help me bake the bread?” said the Little Red riculture’s Cooperative State Research, Education, Hen. “Not I,” said the duck. “Not I,” said the and Extension Service and the U.S. Environmental goose. “Not I,” said the cat. “Not I,” said the pig. Protection Agency. “Then I will bake it myself,” said the Little Red Clearly, forging such a partnership would benefit Hen. And she did. After the loaf had been tak- from many people and entities joining together in the en from the oven it was set on the table to cool. effort. But working together is much easier to talk “And now,” said the Little Red Hen, “who will about than it is to do. The folktale featuring the Lit- help me to eat the bread?” “I will!” said the duck. tle Red Hen offers some insights. “I will!” said the goose. “I will!” said the cat. “I will!” said the pig. “No, I will eat it myself!” said One summer day the Little Red Hen found a the Little Red Hen. And she did. grain of wheat. “A grain of wheat!” said the Lit- tle Red Hen to herself. “I will plant it.” She It is tempting when reading this tale to identify asked the duck, “Will you help me plant this with the title role. Surely we all want to see ourselves grain of wheat?” “Not I,” said the duck. She as the one who takes charge and persistently does asked the goose, “Will you help me plant this what needs to be done to reach the goal, even when grain of wheat?” “Not I,” said the goose. She we get no help. But implicit in the folktale is not just asked the cat, “Will you help me plant this grain the question of whether we fit the title role, but also of wheat?” “Not I,” said the cat. She asked the the question of how we will answer the call to become pig, “Will you help me plant this grain of involved when we are needed most. wheat?” “Not I,” said the pig. “Then I will plant it myself,” said the Little Red Hen. And she did. Soon the wheat grew tall, and the Little Red Hen knew it was time to reap it. “Who will help me reap the wheat?” she asked. “Not I,” said the duck. “Not I,” said the goose. “Not I,” said the cat. “Not I,” said the pig. “Then I will reap it myself,” said the Little Red Hen. And she did. So she reaped the wheat, and it was ready to take to the mill to be made into flour. “Who will help me carry the wheat to the mill?” she asked. “Not I,” said the duck. “Not I,” said the goose. “Not I,” said the cat. “Not I,” said the pig. “Then I will carry it myself,” said the Little Red Hen. And she did. So she carried the wheat to the mill and the miller made it into flour, and she car-
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6.8 Potential Resources to Address Resistance Management Eldon E. Ortman
Introduction and priorities, and address a broad range of IPM re- search, education, and outreach issues. This is a Sec- The U.S. Department of Agriculture’s Cooperative tion 406 national competitive grant program. State Research, Education, and Extension Service (CSREES) supports a broad portfolio of research, ed- ucation, and extension programs in integrated pest Regional Integrated Pest Management management (IPM). Resources are made available in Program (RIPM) two different modes. The CSREES and the Land- The RIPM Program is a regionally based program Grant Universities (LGU) are partners in program that supports development and implementation of development. To support that partnership, certain new and modified IPM tactics and systems, the vali- CSREES funds are made available to the LGUs on a dation in production systems, and the delivery of ed- formula basis. Those funds are matched by the LGU. ucational programs to pest managers, advisors, and The CSREES manages several competitive IPM grant producers. The program builds stakeholder partner- programs that have different goals and objectives. ships to address critical pest management needs in The Request for Applications (RFAs) for each program the region. This is a special research grant program are different and change over time. The RFAs for that is regionally competitive and will be managed by those competitive programs have not had a specific the Centers. line or created a unique identity for resistance man- agement. Within the context of several of the RFAs, however, there would be an opportunity to propose a Pest Management Alternatives Program project that is relevant to resistance management. (PMAP) Those persons interested in resistance management The program goal is to develop replacement tactics should review the grant program opportunities on the and technologies for pesticides undergoing regulato- CSREES website for specific RFA information. Fol- ry action for which there are no effective registered lowing is a brief description of the IPM programs in alternatives. This program funds short-term devel- which CSREES invests resources. opment and outreach projects aimed at adaptive re- search and implementation of tactics that have shown promise in previous studies. The focus of the program Regionally Focused Programs is on developing replacements for specific tactics. The intent is to continue current program goals and con- Regional IPM Centers (Centers) vert this program to a component managed by IPM Centers. This is a special research competitive grant Centers, through partnering with institutions and program. stakeholders, will facilitate the identification and prioritization of regional and multistate IPM re- search, extension, and education program needs. In Nationally Focused Programs fiscal year (FY) 2000, geographically based centers (Discovery to Implementation) were formed in the north central, northeastern, south- ern, and western regions of the United States prima- rily to establish a national pest management infor- Base Support to Land-Grant Universities mation network. Centers of the future will be the focal point for team building efforts, communication net- The underpinning of the national extramural ag- works, and stakeholder participation. Centers will ricultural research, education, and outreach capabil- bring together those with expertise, identify needs ity is accomplished through a federal/state
134 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 135 partnership with the LGU System. The CSREES Minor Crop Pest Management (IRÐ4) provides oversight for the federal annual base support that is provided through the Hatch, Smith-Lever, The IR–4 is the principal public program support- McIntyre-Stennis, and Evans-Allen Acts. The feder- ing the registration of pesticides and biological con- al funds are matched and multiplied by state and lo- trol agents for use on minor crops. This program pro- cal resources in support of the national agricultural vides coordination, funding, and scientific guidance research, education, and extension infra-structure. for both field and laboratory research to develop data This is a formula-based program. in support of registration packages to be submitted to the U.S. Environmental Protection Agency (EPA). IR–4 coordinates the cooperation of commodity pro- National Research Initiative (NRI) ducers, state and federal research scientists, and ex- The NRI pest management research program sup- tension specialists in identifying and prioritizing pest ports fundamental and mission-linked research on the control needs. This is a special research competitive biology of insects, microbes, nematodes, and invasive grant program, with additional support from CSREES plants. It also supports research on the interactions and the Agricultural Research Service base funds. among pest organisms, species of agricultural impor- tance, and their interaction with the environment. This research program is a foundation for the devel- Methyl Bromide Transitions Program (MBT) opment of the next generation of IPM tools, strategies, This program addresses the need to develop man- and systems. This is a national competitive grant agement technologies, systems approaches, and ex- program. tension delivery programs for methyl bromide uses that may be cancelled. This is a Section 406 national competitive grant program. Risk Avoidance and Mitigation Program (RAMP) The RAMP supports the development and imple- Organic Transitions Program (OTP) mentation of innovative IPM systems on an area or The goal of this program is the development and landscape basis. It is designed to maintain crop pro- implementation of biologically based pest manage- ductivity and profitability and, at the same time, to ment practices that mitigate the ecological, agronom- address environmental quality and human health is- ic, and economic risks associated with a transition sues. The program will involve major acreage crops from conventional to organic agricultural production as well as key fruit and vegetable production systems. systems based on national standards. This is a Sec- Projects funded by this program are long-term, involv- tion 406 national competitive grant program. ing systems approaches targeted at eliminating or minimizing pesticide residues in key foods, soil, and surface water. Funded projects tend to be multistate Extension IPM Implementation or regional in scale and typically involve multiple This is a base program in each state and territory cropping systems with emphasis on enhanced stabil- that facilitates the development and transfer of IPM ity and sustainability of IPM systems. This is a Sec- from researchers to implementation by farmers, crop tion 406 national competitive grant program. consultants, and other end users. Information out- reach occurs through consultations, clinics, work- shops, conferences, demonstrations, field days, and a Crops at Risk (CAR) wide variety of publications. This program provides The CAR program addresses intermediate-term, the scientific foundation for IPM. This is a Smith- applied research, education, and extension in IPM for Lever 3(d) program with funds distributed according crop and cropping systems. The goal of this program to a formula. is to develop or modify multiple-tactic IPM systems and strategies focused on specific crop production sys- tems. This is a Section 406 national competitive grant Pesticide Safety Education Program (PESP) program. The primary focus of this joint EPA/USDA program is to provide educational programs that support the proper use of pest management technologies. A cen- tral focus is to provide pesticide applicators with the 136 6.8 Potential Resources to Address Resistance Management knowledge and training needed to safely and effective- ly use pesticides. Education is provided by LGU ex- tension programs in conjunction with state regulato- ry agencies that certify and license applicators. The EPA provides funds (allocated on a formula basis) and the CSREES manages a national program connect- ing to the science education base in each state, the District of Columbia, and territories.
Biotechnology Risk Assessment Research Grant Program (BRARGP)
In addition to the IPM portfolio listed here, anoth- er potential source of competitive funds is the USDA Biotechnology Risk Assessment Research Grant Pro- gram (BRARGP), the purpose of which is to assist Federal regulatory agencies in making science-based decisions about the effects of introducing into the en- vironment genetically modified animals, plants, and microorganisms. In FY 2003, applications must ad- dress one of the following program areas or seek par- tial funding for a conference that addresses science- based risk assessment or risk management of genetically modified organisms released into the en- vironment:
• Research designed to identify and develop appro- priate management practices to minimize physi- cal and biological risks associated with genetically engineered animals, plants, and microorganisms. • Research designed to develop methods to moni- tor the dispersal of genetically engineered ani- mals, plants, and microorganisms. • Research designed to further existing knowledge with respect to the characteristics, rates, and methods of gene transfer that may occur between genetically engineered animals, plants, and mi- croorganisms, and related wild and agricultural organisms. • Environmental assessment research designed to provide analysis that compares the relative im- pacts of animals, plants, and microorganisms modified through genetic engineering to other types of production systems. • Other areas of research designed to further the purposes of the BRARGP. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 137
6.9 Lessons Learned: State Regulatory Perspective David Scott
In general, I believe we have learned that resis- I also believe that if the U.S. Environmental Pro- tance management is not a simple, one-size-fits-all, tection Agency and others feel that states do have a issue. While that idea is tempting to some people, I significant role to play in the issue of resistance man- do not believe that it is an issue for which there is a agement, the states must be more actively engaged simple regulatory fix. Even if regulation were the by those stakeholders relative to the issue. Waiting answer or part of the answer, most states would be to involve states, if truly needed, until the end of the required to work it into existing priorities. It would process will limit the support from state lead agen- not be a very high compliance priority for most states. cies.
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6.10 Public Sector Plant Breeding and Pest Resistance Management Margaret E. Smith
Introduction offer an economically viable level of pest control. De- signing for sustainability means that plant breeders A primary objective for many plant breeding pro- must seek ways to ensure long-term effectiveness of grams is improvement of pest resistance to produce pest control measures—in other words, ways to man- varieties that suffer less loss of yield and quality due age pest resistance effectively. Several possible ap- to pest damage. Not infrequently, such varieties have proaches to this challenge are discussed in the follow- provided the selection pressure that has led to evolu- ing sections. tion of resistance in pest populations (e.g., stem rust in small grains [Dyck and Kerber 1985], Hessian fly in wheat [Gallun and Khush 1980]). Judicious appli- Durable Resistance cation of plant breeding, however, also can contrib- ute positively to pest resistance management, as de- Much has been written about horizontal, broad scribed in the present paper. spectrum, or durable resistance (e.g., Gallun and Khush 1980, Simmonds 1999). Often it is equated with polygenic resistance, although this relationship Designing for Sustainability does not always hold true. There are some classic examples of single gene resistances that have proved A plant breeding approach that is designed for sus- durable over long time periods (e.g., Simmonds 1999). tainability of the agricultural system into which prod- Knowledge of pest biology often will suggest whether uct varieties will fit is most likely to be an approach single gene resistance might or might not hold up over that will contribute positively to pest resistance man- time. Highly mobile pests (e.g., airborne fungi) have agement. “Designing” implies an intentional ap- much greater potential to evolve to overcome a sin- proach, in which the goals and possible outcomes have gle gene resistance than less mobile pests (e.g., soil- been carefully considered in advance. “Sustainabili- living pathogens). ty” has been defined in many ways, but most defini- In most instances, resistance that is durable will tions incorporate certain common elements. Among be partial resistance rather than complete immuni- these are the ideas that sustainability is the capacity ty. Something short of immunity generally is suffi- over the long term to satisfy human food and fiber cient to avoid economic losses to pests, and certainly needs, enhance environmental quality and the natu- decreases the selection pressure experienced by the ral resource base upon which the agricultural econo- pest population. The plant breeding challenge inher- my depends, integrate (where appropriate) natural ent in this is that immunity is easiest to spot in large biological cycles and controls, and sustain the econom- breeding populations and simplest to select for. Se- ic viability of farm operations (U.S. Congress 1990). lection for partial resistance requires quantification Designing for sustainability, then, involves a thought- of relative levels of pest damage rather than simply ful, intentional approach to developing long-term ag- looking for the “clean” plants, and thus is more time ricultural productivity in a way that takes advantage consuming and complex. It also is impossible to do of biological cycles, enhances environmental and nat- in the presence of genes conferring immunity or near- ural resource quality, and is economically viable. immunity, because these genes mask any underlying As they relate to plant breeding, these principles variation in partial resistance. Nonetheless, pro- suggest that resistant varieties are a desirable option grams that have explicitly targeted partial resistance for pest management (because they take advantage generally have been quite successful. of natural biological controls and have few, if any, neg- Pyramiding multiple resistance genes was difficult ative effects on the environment), that such resistance or impossible to do based solely on phenotypic selec- must be long-standing or durable, and that it must tion approaches, but now may be achievable using
138 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 139 molecular genetic tools. Pyramiding can combine sev- beneficial, but yield or quality loss due to insect dam- eral different genes for resistance to provide polygenic age is undesirable (Losey, J. 2001. Personal commu- resistance based on multiple mechanisms of resis- nication). Tolerant varieties—those that support a tance—a combination much more likely to be dura- relatively large insect population but suffer little/no ble than single gene resistances. Molecular genetic yield or quality loss despite that—provide exactly markers also may allow combination of polygenic par- what is needed in a refuge. Tolerance often has been tial resistance with single genes conferring immuni- dismissed in developing resistant varieties, because ty, provided the markers can capture the majority of tolerant varieties can allow insect population build- the variation for the partial resistance trait. The abil- up over time to the point where the variety no longer ity to detect quantitative trait loci that explain most can withstand the insect pressure and yield or quali- trait variation still is limited, particularly for traits ty losses do occur. Tolerant varieties, however, should influenced by many loci each of which has a small ef- be optimal for use in refuge plantings. Plant breed- fect, which is the nature of most partial resistance. ers could certainly devote more attention to screen- With improved molecular genetic marker technology, ing for and/or breeding such varieties. this limitation should be overcome, and combining single gene immunities with a background of partial resistance should become possible. Heterogeneous Varieties
Host plant resistance is no different from other pest Background Resistance control tactics in that varying pest control measures Underlying Transgenes over space or time constitutes best integrated pest management practice. This is most apparent for those Some of the first transgenic crop varieties that have transgenic pest-resistant plants in which the resistant been successfully marketed carry transgenes that variety is simply a form of chemical control deployed confer near immunity to pests. These include the through the genetic machinery of the plant. We would Bacillus thuringiensis (Bt) crops for insect resistance not advocate pest control through repeated applica- and several disease-resistant horticultural crops. In tion of exactly the same chemical pesticide over large terms of selection pressure on the pest population, areas and multiple years. We should not fall into the transgenes are no different from genes native to a crop same trap with simple host plant resistance mecha- species—immunity still exercises strong selection nisms, whether transgenic or not. Heterogeneous pressure on pest populations. As discussed in the pre- varieties can provide diversity in pest resistance vious paragraph, the probability of pests evolving re- mechanisms in the spatial dimension. This is not a sistance to these transgenes would be decreased by new concept; the multiline approach was first suggest- incorporating them into varieties that carry partial ed fifty years ago by Jensen (1952), but it is still rele- resistance. This would enhance the lifetime of the vant and useful. Varietal mixtures including both resistant transgene by ensuring that the varieties resistant and tolerant components would have a sim- released with it had multiple mechanisms and mul- ilar effect and have been considered for providing the tiple genes for resistance, thus decreasing the likeli- required refuges for transgenic varieties in instanc- hood that a pest could evolve to overcome all of them es in which individual plants (as opposed to whole simultaneously. To my knowledge, this has not been fields) can constitute effective refuges. Such mixtures standard practice, but designing for sustainability have the advantage that by planting the seed, the suggests that it should be. farmer will automatically create a refuge. Knowledge about refuges and their management, agreement that refuges are important as a public good, and compli- Identifying Optimal Refuge ance all are taken care of as soon as the seed is pur- Varieties chased for planting. Heterogeneous varieties are probably an underutilized component for designing A tactic central to pest resistance management for sustainable pest resistance management systems. transgenic insect resistant varieties is the use of sus- ceptible refuge plantings. Little plant breeding effort has been devoted to identifying and/or developing optimal refuge varieties, but this could be done. In a refuge, adult insects that can mate are actually 140 6.10 Public Sector Plant Breeding and Pest Resistance Management
Novel Sources of Resistance Literature Cited Fundamentally, plant breeding contributions to Dyck, P. L. and E. R. Kerber. 1985. Resistance of the pest resistance management rely on the availability race-specific type. Pp. 469–500. In A. P. Roelfs and of multiple, diverse sources of resistance that differ W. R. Bushnell (eds.). The Cereal Rusts, Vol. II. Ac- in terms of their modes of action. Identifying such ademic Press, Orlando, Florida. sources has long been a goal of most breeding pro- Gallun, R. L. and G. S. Khush. 1980. Genetic factors grams, and this need will continue. Land races, old affecting expression and stability of resistance. Pp. varieties, local farmer varieties, and wild and weedy 62–85. In F. G. Maxwell and P. R. Jennings (eds.). crop relatives all may harbor useful resistance genes. Breeding Plants Resistant to Insects. John Wiley Although such varieties have been good sources of sin- & Sons, New York. gle, simply-inherited pest resistance genes in plant Jensen, N. F. 1952. Intra-varietal diversification in breeding programs, they generally have not been used oat breeding. Agron J 44:30–34. for extraction of the more complex, polygenic resis- Knight, J. 2003. Crop improvement: A dying breed. tances that are undoubtedly also present. Such use Nature 421:568-570. has proved difficult due to the unimproved and often Simmonds, N. W. 1999. Principles of Crop Improve- unadapted nature of the parent germplasm and hence ment. Blackwell Science, Malden, Massachusetts. the difficulty of phenotypically identifying desirable Tanksley, S. D. and S. R. McCouch. 1997. Seed banks individuals and maintaining multiple resistance and molecular maps: Unlocking genetic potential genes through a breeding process. Tanksley and Mc- from the wild. Science 277:1063–1066. Couch (1997) describe new molecular genetic ap- U. S. Congress. 1990. Farm Bill, Title 16, Subtitle proaches for more efficiently mining the genetic po- B—Sustainable Agriculture Research and Educa- tential of such varieties. Using these approaches, our tion—of the Food, Agriculture, Conservation, and gene banks could serve as a rich resource for design- Trade Act of 1990. Washington, D.C. ing more-sustainable pest-resistant varieties.
The Need for Public Sector Plant Breeding Breeding and selection of polygenic or durable host plant resistance usually is a lengthy, gradual process. As described in this paper, it provides products that are clearly in the public interest to have available. But the paybacks to such research (e.g., profits) are not immediate. This is the classic description of the type of plant breeding that will most likely be done in the public sector—longer-term projects with un- clear short-term profit potential, but that serve the public’s interests. Unfortunately, as noted recently by Knight (2003, p. 568), “All over the world, conven- tional plant breeding has fallen on hard times, and is seen as the unfashionable older cousin of genetic engineering...Government funding of plant-breeding research has all but dried up....” If plant breeding is to continue to make significant contributions toward sustainable design for pest resistance management, this is a trend that clearly must be reversed—soon, and strongly so. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 141
6.11 Working Together to Remove Resistance Management Barriers and to Adopt Proactive Resistance Management Strategies: A U.S. Perspective Sharlene R. Matten
Introduction likely to facilitate development of consensus are pub- lic workshops, grower meetings, and scientific meet- The mission of the U.S. Environmental Protection ings. Agency (EPA) is to protect human health and the It also is important to have transparent and con- environment. Part of this mission can be accom- sistent regulatory processes, policies, regulations, and plished through the adoption of proactive resistance requirements that are cost-effective and based on management strategies. The EPA has worked with sound science. There should be clear economic advan- all stakeholders to achieve proactive resistance man- tages and incentives for the adoption of resistance agement. This has primarily been done on a volun- management strategies. There also should be volun- tary basis, except for the case of specific resistance tary programs that promote the use of pesticide re- management requirements for Bacillus thuringiensis sistance management strategies. (Bt) plant-incorporated protectants (Bt crops). To Whenever possible, all stakeholders should work promote greater success in implementation of long- toward obtaining the necessary research funding to term, proactive resistance management strategies, support the development, implementation, and adop- however, there should be more emphasis on determin- tion of proactive resistance management strategies. ing common resistance management objectives and There should be a strong financial incentive to main- goals. This requires more intensive and iterative com- taining long-term resistance management programs munication among stakeholders. as part of an overall integrated pest management program. All stakeholders must share in the common goal of proactive resistance management. Removing Barriers and Working Together to Achieve Proactive Summary Resistance Management The EPA believes that proactive resistance man- The following goals, objectives, and activities can agement is important to its overall mission of protect- remove barriers to developing and adopting proactive ing human health and the environment. There are resistance management strategies. All of these activ- many steps available to achieve successful proactive ities involve extensive and intensive stakeholder par- resistance management provided there are agreed- ticipation and commitment to achieve success. upon common goals and objectives. Whenever possi- First, there must be a determination of common re- ble, all stakeholders must reach a consensus as to sistance management objectives and goals among these common goals and objectives to remove resis- stakeholders through both iterative and interactive tance management implementation barriers and to processes. This common set of objectives will allow work together more productively. every stakeholder to participate in a “win-win” situ- ation to achieve proactive resistance management. To create a common set of objectives and goals, all stake- holders must work toward consensus and motivate cultural changes that will allow full participation in the development and implementation of proactive resistance management. This interaction will allow more fully the development of positive relationships among stakeholders based on mutual respect and trust. Examples of processes and frameworks that are
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6.12 Working Together to Remove Resistance Management Barriers and to Adopt Proactive Resistance Management Strategies: A Canadian Perspective Pierre Beauchamp
Introduction In October 2001, 2 years after publication of the DIR99-06, only 30 labels contained the new resistance The Canadian Pest Management Regulatory Agen- management statements. Following that finding, a cy’s (PMRA) primary goal is to protect human health decision was taken to incorporate in each letter of and safety and the environment while enabling access registration a paragraph asking the company to to effective pest management tools. Part of this goal amend the label at next printing. For new active in- can be accomplished through delaying the loss of pes- gredients, the labeling changes were requested at first ticide effectiveness due to the development of resis- label printing. tance by pests. The PMRA, in concert with the U.S. As of January 2003, 288 products, or approximately Environmental Protection Agency (EPA) has devel- 18% of eligible products, incorporate resistance man- oped specific resistance management labeling as a tool agement statements in their labels. It is expected that for growers in their day-to-day resistance manage- less than 40% of eligible products will have resistance ment activities. management statements by the target date of Janu- ary 1, 2004. At that time, an assessment of the progress will be made and a new approach to resis- tance management labeling may be considered. Removing Barriers and Working Together to Achieve Proactive Summary Resistance Management The PMRA believes that resistance management The Regulatory Directive 99-06 “Voluntary Pesti- labeling is essential to delay resistance development. cide Resistance Management Labeling Based on Tar- The PMRA, in conjunction with the EPA and in dis- get Site/Mode of Action” was published in October cussion with industry, is hopeful that greater partic- 1999. The Directive was made available to the indus- ipation by registrants will be forthcoming. Voluntary try through mailings, the Internet, presentations at resistance management labeling has been less suc- scientific and regulatory meetings, and personal con- cessful than hoped and new approaches (e.g., manda- tacts. Unlike the EPA PR Notice 2001-05, DIR99-06 tory statements) may be necessary after January 1, specifically mentions a target date of January 1, 2004 2004. for full implementation of the label changes. The new label statements proposed in the DIR99- 06 can be separated into two parts: (1) assignment of each product to a standard group based on the target site/mode of action of the active ingredient; (2) spe- cific recommendations on how to prevent the devel- opment of resistance. These label statements are con- sidered to be the basic information needed by the growers to make the link between resistance manage- ment education/recommendation and how to choose and use products to delay resistance development in the field. This is why the addition of the resistance management statements on all Agricultural/Commer- cial products has been the main goal of PMRA since publication of DIR99-06.
142 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 143
7.1 Herbicide Resistance Management Strategies for Weeds Dale L. Shaner
Introduction farmers who were early adapters of resistance management versus late adapters. Hence there is lit- Herbicide-resistant weed populations have been se- tle economic incentive for farmers to practice proac- lected at a relatively steady rate of nine new biotypes tive resistance management. per year for the last 30 years with no indication that American Cyanamid introduced a program that at- this rate is decreasing (Heap 2003). This increase has tempted to manage proactively the selection of resis- occurred in spite of the fact that resistance manage- tance to the imidazolinones (Shaner, Feist, and Retz- ment guidelines have been available and have been inger 1997). The program contained multiple taught to growers beginning in the 1970s. The con- elements including education of sales staff, distribu- tinued rise in herbicide-resistant weed populations tors, and users on herbicide resistance; recommenda- indicates that there is some problem either with the tions for effective herbicide mixtures or sequential resistance management guidelines or in our efforts to programs for resistance management; and incentives educate the farmer in how to use them or the ability for farmers to implement these programs. The pro- of farmers to implement resistance management. gram was not very successful for various reasons. A survey of farmers indicated that they did not have a clear understanding of how resistance develops or on Proactive Versus Reactive herbicide mechanisms of action. Their major concern, Herbicide Resistance however, was the cost of implementation of resistance management. Management What are consequences of this lack of proactive re- sistance management? One is that educational efforts Although it seems that it is better to manage re- to change farmer practices proactively are probably sistance proactively rather than reactively, most going to be unsuccessful. That does not mean that the farmers do not change their weed management prac- farmers do not need to be informed on effective resis- tices until after a resistance problem has developed tance management practices because they will need on their farm. One difference between herbicide use to know what to do when the problems occur. A sur- and either insecticide or fungicide use is the frequen- vey conducted in Western Australia found that grow- cy of applications during a growing season. Insecti- ers were more likely to implement a herbicide resis- cides and fungicides often are applied 4 to 10 times tance management system if they had resistance on per season, whereas herbicides are applied only once their farms and if they had easy access to informa- or twice. Thus it may be easier to practice proactive tion on resistance management (Llewellyn et al. resistance management for insects and diseases be- 2002). Thus, the aim of educational programs may cause there are more opportunities to use multiple have to change from proactive management tech- mechanisms of action of insecticides or fungicides per niques to helping farmers recognize when resistance season on the pest population. has been selected on their farms and giving them Another reason for the lack of proactive herbicide guidelines on what to do once it has occurred to pre- resistance management is that the resistance man- vent the problem from spreading. agement program will be more complicated and ex- pensive than a program that depends on one highly effective herbicide or herbicide class (Peterson 1999). Role of Resistance Monitoring Furthermore, the cost of the cure for herbicide resis- tance is the same as the cost of prevention. An eco- There are key technical and managerial elements nomic analysis by Pannel and Zilberman (2001) involved in all antiresistance strategies (Schwinn and showed that there was no economic advantage for Morton 1990). The key technical elements include the
143 144 7.1 Herbicide Resistance Management Strategies For Weeds following: for a change in herbicide usage that would slow the spread of resistance. • Early evaluation of the inherent risks of select- An example is the introduction of glyphosate-resis- ing for resistance tant crops. Shaner (2000) proposed that there would • Establishment of baselines of resistance in weed be an increase in certain weed species once glypho- populations and development of methods to detect sate became the primary herbicide used. Conyza ca- resistance nadensis (horseweed) was identified as one of the spe- • Determination of specific use parameters of the cies that could act as an early indicator of shifts in herbicide based on cropping patterns, product per- weed populations once glyphosate became the prima- formance, and weed spectrum ry herbicide used for weed management in glypho- • Development of programs for detecting and mon- sate-resistant crops. It has now been documented itoring resistance under practical conditions that this shift is occurring (Van Gessel 2001), and gly- phosate-resistant C. canadensis has spread to large The managerial elements include the following: regions of the Southeast and East Coast in no-till gly- • Determination of use recommendations for the phosate-resistant cotton and soybeans (Mueller et al. herbicide (i.e., dosage, proportion of area treated, 2003). Although this weed is not a particularly hard persistence, etc.) problem to control with alternative herbicides, it • Integration with other weed control methods should act as an early indicator of potential problems • The ability to enforce recommendations we may face in the future and a reminder that now is • Acceptance of recommendations by other compa- the time to change farming practices to decrease reli- nies, academia, and users ance on glyphosate for weed management. •Coordination of recommendations with manufac- turers of herbicides with the same mode of action or herbicides used on the same crop Strategies for Herbicide • Implementation of recommendations before resis- Resistance Management tant weeds develop What practices have been shown to be the most ef- Based on these key elements for resistance man- fective in herbicide resistance management? Certain agement, companies need to have a resistance man- procedures that are effective in insect resistance man- agement program in place so they can give farmers agement, such as providing refugia for susceptible the answers they need when resistance occurs. This weed biotypes, have not been shown to be an effective program should be established during the develop- strategy. Unlike insects, weeds are not mobile and ment phase of a new compound and should include pollen flow may not occur at high enough rates to keep diagnostic tests as well as resistance management susceptibility in the populations. In addition, in many practices. Resistance monitoring plays a vital role in instances, the resistant trait is dominant or semi- determining when and where resistance is occurring dominant and heterozygous resistant plants will sur- and should be part of a herbicide marketing program vive and set seed after treatment with a full-use rate so that the problem can be detected early before it has of the herbicide. Therefore it is difficult to keep the spread too far. In Europe, one requirement of regis- resistant trait as a recessive trait within a population. tration for a new pesticide consists of an estimate of Farmers also are reluctant to allow unfettered weed the risk for selecting resistance, and the establish- growth in even part of the field, because this location ment of a monitoring system for resistance as well as will act as a seed source for the rest of the field and a mitigation program for managing resistance (Shan- the weed population can spread rapidly. er and Leonard 2001). But it is difficult to conduct a monitoring program, The generally accepted guidelines for herbicide re- particularly for a herbicide with a new mechanism of sistance management are the following: action and for which resistance has not yet occurred. • Avoid continuous use of same herbicide or mech- Modeling, although imperfect, can be a means to rank anism of action (MOA) weed species according to their probability of becom- •Use other methods of weed control (e.g., physical) ing resistant. Those species that appear to be the in addition to herbicides most vulnerable can act as the “canary test” for the • Rotate herbicide MOAs selection of resistance and could possibly allow time • Use mixtures of herbicides with different MOAs Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 145
• If possible, rotate herbicide mixtures to be well educated on resistance management and on the mechanism of action of the herbicides they are Two of the most widely used methods for herbicide currently using. Placing the mechanism of action on resistance management are rotating herbicides and the label, which is currently done on a voluntary ba- using tank mixtures of herbicides with different mech- sis, should act as a good educational tool and help anisms of action. The reason for this is that there is farmers make more informed choices (Beckie, Chang, a very low probability of resistance being selected to and Stevenson 1999; Mallory-Smith 1999). two different mechanisms of action. But there are Ultimately, resistance management comes down to problems with this approach because both herbicide implementation at the farm level. The methods for classes must be active on the same weed species in management are straightforward and, in most cases, order for this to be an effective management strate- relatively easily done. Farmers, however, will change gy. In addition, the use of mixtures often increases their practices when they see value in the changes or the cost to farmers and they are reluctant to add the they are forced to make changes due to a resistance additional cost until after resistance has occurred, at problem. Strategies need to be in place to provide an- which time the mixture is no longer effective as a pre- swers to these problems as they arise and methods ventive strategy. need to be developed to allow detection of the prob- One criticism of the use of tank mixtures is that lem as early as possible, so that resistance does not there is an increased potential that resistance will be spread. selected to both herbicides. Although this has not yet occurred, it is a possibility. A way to avoid selecting for resistance to two mechanisms of action simulta- Literature Cited neously is to rotate tank mixtures rather than just ro- tating single mechanisms of action herbicides. These Beckie, H. J. and K. J. Kirkland. 2003. Implication mixtures may not be available, however, and the cost of reduced herbicide rates on resistance enrichment will increase. In addition, it is unlikely farmers will in wild oat (Avena fatua). Weed Tech 17:138-148. adopt this practice until after resistance has occurred Beckie, H. J., F. Chang, and F. C. Stevenson. 1999. on their farm. The effect of labeling herbicides with their site of It is important to note that herbicide resistance action: A Canadian perspective. Weed Tech 13:655– management is a multiyear process. It has to be part 661. of an integrated system and cannot be done on a year- Buhler, D. D. 2002. Challenges and opportunities for to-year basis. Weed scientists have been seeking ac- integrated weed management. Weed Sci 50:273– ceptance of integrated weed management (IWM) by 280. farmers for many years (Buhler 2002). In Australia, Heap, I. 2003. The International Survey of Herbi- herbicide resistance has been one of the key reasons cide Resistant Weeds,
Peterson, D. 1999. The impact of herbicide-resistant weeds on Kansas agriculture. Weed Tech 13:632– 635. Schwinn, F. J. and H. V. Morton. 1990. Antiresis- tance strategies: Design and implementation in practice. Pp. 170–183. In M. B. Green, H. M. LeB- aron, and W. K. Moberg (eds.). Managing Resistance to Agrochemicals. American Chemical Society, Washington, D.C. Shaner, D. L. 2000. The impact of glyphosate-toler- ant crops on the use of other herbicides and on re- sistance management. Pest Manag Sci 56:320–326. Shaner, D. L. and P. Leonard. 2001. Regulatory as- pects of resistance management for herbicides and other crop protection products. Pp. 279–294. In S. B. Powles and D. L. Shaner (eds.). Herbicide Resis- tance and World Grains. CRC Press, Boca Raton, Florida. Shaner, D. L., D. A. Feist, and E. J. Retzinger. 1997. SAMOATM: One company’s approach to herbicide- resistant weed management. Pestic Sci 51:367–370. VanGessel, M. J. 2001. Glyphosate-resistant horseweed in Delaware. Weed Sci 49:703–705. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 147
7.2 Pest Resistance Management Goals: Monitoring Insects D. D. Hardee
Introduction al. 2001). Genes from the bacterium, Bacillus thuringiensis From 1996 to the present, the U.S. Department of Berliner, for the production of the insecticidal protoxin Agriculture–Agricultural Research Service (USDA– (Cry1Ac δ-endotoxin, or Bt) have been inserted into ARS) at Stoneville, Mississippi has provided the only the genome of several crops, including cotton and corn, program for the U.S. cotton industry designed to mon- to control certain pests. The development of resis- itor bollworm (Helicoverpa zea [Boddie]) and tobacco tance to Cry1Ac in Bt cotton has been a major con- budworm (Heliothis virescens [F.]) for possible devel- cern, because all parts of the cotton plant contain the opment of resistance to the Cry1Ac δ-endotoxin (Ba- toxin all season, and thus potentially resistant pests cillus thuringiensis [Bt]) in transgenic cotton. To date, are afforded a greater opportunity to survive and to no significant and recurring changes in tolerance have produce resistant populations (Gould 1998). Current been detected, nor have any field control failures due resistance management plans for Bt cotton have the to such tolerance been reported. As novel proteins are signal feature of relying on the “refuge/high dose” introduced into Bt cotton for commercial use in the strategy that combines transgenic plants delivering future, monitoring will of necessity be more complex, very high doses of toxin, supported by the nearby pres- detailed, and expensive. The ARS, consultants, cot- ence of non-Bt plants, or refuges. A high-dose strate- ton producers, and state experiment stations are ini- gy based on simple models that used mostly results tiating proactive programs to improve the reliability from laboratory studies (Gould 1986) and the require- of the monitoring program to ensure long-term effec- ment of plantings of non-Bt cotton as refuges to pro- tiveness of this valuable technology. duce susceptible insects for mating with surviving resistant individuals have been mandated by the U.S. Environmental Protection Agency to retard total pop- Pests in Cotton ulation resistance. Growers may choose one of the following refuge types for 2003: Worldwide, cotton (Gossypium hirsutum L.) is a pleasing target for insects of all types. United States 1. Plant an external refuge of at least 20 acres (a.) cotton is no exception—at least 15 insect species in of non-Bt cotton for every 80 a. of Bt cotton with- some years and in some parts of the U.S. Cotton Belt in 1.0 mile of the farthest Bt cotton to provide Bt- can cause moderate to extensive damage (Williams susceptible moths; refuges can be treated with 2002). Insecticides remain the solution of choice for any non-Bt insecticide for any insect most of these pest problems in cotton fields. One of 2. Plant at least 5 a. of non-Bt embedded refuge at these pests, the boll weevil, Anthonomus grandis least 150 feet (ft) wide for every 95 a. of Bt cotton grandis Boheman (Coleoptera: Curculionidae), is on as a contiguous block within the Bt field; the ref- the verge of total elimination from the United States uge may be treated with any insecticide applied with the aid of a combination of insecticides, cultural to the Bt cotton control, and traps and lures (Hardee and Harris 3. Plant at least 5 a. of non-Bt cotton for every 95 a. 2003). Need for insecticides to manage three other of Bt cotton; this acreage may not be treated with major pests, pink bollworm, Pectinophora gossypiel- any insecticide labeled for bollworm (BW) and to- la (Saunders) (Lepidoptera: Gelechiidae), tobacco bud- bacco budworm (TBW) and must be at least 150 worm, Heliothis virescens (F.) (Lepidoptera: Noctu- ft wide and within 0.5 mile of Bt cotton. idae), and bollworm Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), has declined in some pro- Depending on results from 2002–2003 alternate duction regions since 1996 because of the commercial host studies, some of these options may be subject to introduction and use of transgenic cotton (Hardee et change for the 2004 crop year.
147 148 7.2 Pest Resistance Management Goals: Monitoring Insects
Monitoring Program effective is based mostly on theory, not fact. Another criticism of the refuge concept currently in place is In addition, the USDA–ARS at Stoneville, Missis- that all sections of the Cotton Belt, regardless of ag- sippi was selected in 1995 to initiate and continue a ricultural practices and pest complex, have the same U.S. Cotton Beltwide monitoring program to detect refuge requirements. To obtain more defensible in- any changes in resistance or tolerance levels from year formation on the production of susceptible populations to year. Such changes in tolerance would then be used of pest insects by other host crops, the ARS in Mis- to recommend resistance management procedures sissippi, Monsanto Ag, and cotton entomologists from and remedial action plans if levels of tolerance and/ Arkansas, Georgia, Louisiana, and North Carolina or resistance were detected. Since the 1996 crop year, have just completed the first year of a 2-year study to the ARS’s Southern Insect Management Research determine the number of BW produced by corn, grain Unit (SIMRU), in cooperation with farmers, consult- sorghum, peanuts, and soybeans in an agricultural ants, and state experiment stations and extension environment. Preliminary results indicate that high- services across the southern United States, has con- er numbers of BW than expected were produced in ducted a monitoring program to compare colonies of most of these crops (refuges). This is an important TBW and BW collected in various states to highly sus- finding because BW is less susceptible to Cry1Ac than ceptible, laboratory-reared colonies of both species TBW, Cry1Ac in Bt cotton is not considered high dose (Hardee et al. 2002). These procedures have changed for BW, and this insect is predicted to be the most like- over the years but essentially consist of a larval bio- ly to develop resistance to Cry1Ac. Pyramiding genes assay in which insects are fed on an artificial diet con- for a two-toxin system to be introduced to the grower taining a small dose of Cry1Ac found in a foliar Bt in 2003 in transgenic cotton (Adamczyk, Adams, and product, MPVII. This dose is similar to the concen- Hardee 2001; Sachs et al. 1996; Tabashnik 1994) may tration found in Bt cotton. overcome the challenge to decreased susceptibility in Fortunately for the entire cotton industry, with the BW, but the effect of dual-toxin Bt cotton on increased exception of a slight but as yet unexplained increase potential for cross-resistance is yet to be determined. in tolerance of BW in 1998 (Hardee et al. 2002), no Skeptics of the monitoring program through 2002 changes in overall susceptibility in both species had have stated that we are not sampling a large enough been detected through 2002. Multiple reasons for the field population to detect low levels of tolerance, and continuing effectiveness of Bt cotton with no sign of our use of moths from pheromone traps fails to test change in susceptibility have been suggested. Some the possible presence of recessive resistant genes in of these include effectiveness of the refuge concept, the native population. Both of these concerns have higher than expected contribution of susceptible in- merit. In order to test the numbers of insects suggest- sects from alternate crops and weed hosts, small per- ed as being needed would require considerably more centages of Bt cotton planted in many locations, and collective manpower and funds than currently are greater susceptibility of resistant BW and TBW to available for this program, even though we have con- other factors such as winter kill, application of insec- sistently increased and improved our effort since ticides for other pests, and biological control agents. 1996. While with the ARS at Stoneville, D. V. Sum- A combination of these reasons, and perhaps other un- erford (unpublished) attempted to detect recessive knowns, may be contributing factors. Regardless of resistance through an F2 screen (Andow and Alstad the reason(s), we can state with confidence that 1998; Andow et al. 1998; Venette, Hutchison, and through the 2002 growing season, no tolerance had Andow 2000) but was unable to show conclusively that been noted at a high enough level to cause control fail- any existed. In 2003, the ARS is taking proactive ures in the field. steps to study the possibility of recessive resistance It is not surprising that the refuge concept and genes by cooperating with entomologists in states and monitoring program have both had their share of chal- locations growing a high percentage of Bt cotton an- lenges and critics. The requirement of non-Bt refug- nually since 1996. These studies will include season- es, regardless of the option chosen, has been met with long collection of eggs from moths captured in light considerable skepticism by growers, consultants, and traps, followed by extensive bioassays and cross mat- certain cotton entomologists and geneticists, especial- ing. In addition, we will increase our general moni- ly because certain assumptions of the models used to toring program by at least 50% in 2003 to include predict refuge needs are not met (Peck, Gould, and Ell- more states and cotton-producing regions. ner 1999), and no data exist supporting the efficacy Bt resistance monitoring in the future undoubted- of the refuges. Thus, the assumption that refuges are ly will increase in importance and complexity. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 149
For example, in 2003 alone there will be two dual-tox- Department of Agriculture-Agricultural Research in systems introduced. These will involve the need Service-154, Washington, D.C. 37 pp. to bioassay populations for susceptibility to not only Hardee, D. D., L. C. Adams, W. L. Solomon, and D. Cry1Ac, but also Cry2Ab, Cry1F, and possibly their V. Sumerford. 2002. Tolerance to Cry1Ac in pop- combinations. These make up the transgenic cottons ulations of Helicoverpa zea and Heliothis virescens known as “Bollgard II” (Monsanto Ag) and “Wide (Lepidoptera: Noctuidae): Three year summary. J Strike” (Dow Agrosciences). In addition, on the hori- Agric Urban Entomol 18:187–197. zon are other products such as “Vip” (Syngenta’s Veg- Peck, S. L., F. Gould, and S. P. Ellner. 1999. Spread etative Insecticidal Protein). All of these new prod- of resistance in spatially extended regions of trans- ucts offer a wide range of effectiveness against many genic cotton: Implications for management of He- other lepidopteran pests of cotton that may lead to the liothis virescens (Lepidoptera: Noctuidae). J Econ need for monitoring programs for other insects. Entomol 92:1–16. At the moment, Mid-South and Southeastern cot- Sachs, E. S., J. H. Benedict, J. F. Taylor, D. M. Stel- ton entomologists are drafting a resistance mitigation ly, S. K. Davis, and D. W. Altman. 1996. Pyramid- plan for BW and TBW in Bt cotton. Because of the ing Cry1A(b) insecticidal protein and terpenoids in dual insect and multiple host situations in the Mid cotton to resist tobacco budworm (Lepidoptera: South and Southeast as opposed to the single host Noctuidae). Environ Entomol 25:1257–1266. pink bollworm in the arid Southwest, an acceptable Tabashnik, B. E. 1994. Evolution of resistance to plan of mitigation will require the collective thinking Bacillus thuringiensis. Annu Rev Entomol 39:47– of the entire cotton and chemical industries. 79. Venette, R. C., W. D. Hutchison, and D. A. Andow. 2000. An in-field screen for early detection and Literature Cited monitoring of insect resistance to Bacillus thuring- iensis in transgenic crops. J Econ Entomol Adamczyk, J. J., Jr., L. C. Adams, and D. D. Hardee. 93:1055–1064. 2001. Field efficacy and seasonal expression pro- Williams, M. R. 2002. Cotton Insect Losses 2001. files for terminal leaves of single and double Ba- Proc 2002 Beltwide Cotton Conf,
Andow, D. A. and D. N. Alstad. 1998. F2 screen for rare resistance alleles. J Econ Entomol 91:572– 578. Andow, D. A., D. N. Alstad, Y.–H. Pang, P. C. Bolin,
and W. D. Hutchinson. 1998. Using an F2 screen for resistance alleles to Bacillus thuringiensis tox- in in European corn borer (Lepidoptera: Pyralidae). J Econ Entomol 91:579–584. Gould, F. 1986. Simulation models for predicting durability of insect-resistant germplasm: A deter- ministic diploid, two-locus model. Environ Ento- mol 15:1–10. Gould, F. 1998. Sustainability of transgenic insecti- cidal cultivars: Integrating pest genetics and ecol- ogy. Annu Rev Entomol 43:701–726. Hardee, D. D. and F. A. Harris. 2003. Eradicating the boll weevil, Anthonomus grandis grandis (Co- leoptera: Curculionidae): A clash between a high- ly successful insect, good scientific achievement, and differing agricultural philosophies. Amer En- tomol 49:82–97. Hardee, D. D., J. W. Van Duyn, M. B. Layton, and R. D. Bagwell. 2001. Bt cotton and management of the tobacco budworm/bollworm complex. U.S. 150
7.3 Resistance Management Strategies for Plant Pathogens Barry J. Jacobsen
Introduction strategies. Assessment of risk relative to fungicide resistance has been reviewed by Brent and Holloman Plant protection pesticides have played and will (1998). Critical factors identified by these authors continue to play a critical role in integrated disease include mode of action(s) of fungicides, site specifici- management strategies for the foreseeable future. ty in the pathogen, genetic variability in pathogen Until the 1970s, plant pathologists did not have to populations, factors involved in cross-resistance, and consider pathogen resistance to fungicides (Brent factors involved in the selection and survival of resis- 1995), bactericides (McManus and Stockwell 2001) or tant individuals in pathogens. These authors devel- nematicides. Today this is a major consideration oped estimates of inherent risk of failure or diminu- when developing integrated disease management tion of control based on structural classes of fungicides strategies that incorporate modern fungicides and and mode of action of fungicides. Based on field ex- bactericides. Resistance of nematodes to nematicides perience to date, the authors have estimated failure has not yet become more than a conceptual problem relatively accurately. Factors included primary and (Moens and Hendrickx 1998), whereas bacterial re- secondary mode(s) of action; site specificity and inten- sistance to streptomycin and fungal resistance to ben- sity of use of the fungicide; and characteristics of the zimidazole, phenylamide, sterol demethylation inhib- causal agents of disease such as whether the patho- itors, and quinine outside inhibitors (strobilurin) gen is mono or polycyclic, capacity of the pathogen to fungicides have caused significant losses to farmers. produce and retain resistant individuals in the popu- Prevention of further losses and maintenance of the lation, the isolation of the pathogen population, and use of these valuable crop protection tools will require implementation of other control strategies. understanding of the scientific basis for development The Fungicide Resistance Action Committee of resistance in plant pathogen populations, strate- (FRAC) has classified fungicide classes as having gies for prevention, and a commitment to stewardship high, moderate, or low risk potential for performance by manufacturers, dealers, extension educators, con- failure (FRAC 2003 a,b). Those with high risk are sultants, farmers, and federal and state regulatory characterized by having highly specific sites of action, agencies. Support for basic scientific research by both use as eradicants, persistence, high dose strategies the public and private sectors dealing with develop- and intensive use without other effective tools being ment and persistence of resistance in plant pathogen used for disease control. Those with low risk poten- populations is critical to developing appropriate strat- tial are characterized by having multiple modes of egies and regulation. action, important secondary modes of action, lack of Plant pathogen resistance to transgenic events that eradicant activity, and lack of observed cross resis- provide host plant resistance have not yet been iden- tance. Pathogen characteristics that create high risk tified, but there is reason to expect that pathogens will are multiple cycles of infection on a crop, fast genera- express genes that allow them to attack these trans- tion time, high level of reproduction, high potential genic plants. It is critical that the risk of pathogen for genetic variation due to sexual recombination, the resistance to both transgenic plant protection events parasexual cycle, or high mutation rate, high fitness and to plant protection pesticides be assessed and of resistant individuals, isolated nonmigratory popu- strategies be developed to retain these valuable dis- lations, and an obligate nature of parasitism. Another ease management tools. significant factor is the use or nonuse of integrated disease management strategies wherein the more diverse the management tools used, the lower the risk Risk Assessment of development of resistance. The lack of basic infor- mation on pathogen genetic variability, inheritance, The assessment of risk of pathogen resistance must and fitness as well as on secondary modes of action of serve as the basis for development of management
150 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 151 fungicides are significant obstacles to predicting risk more stable than those dependent on a single fac- with greater reliability. The considerations previous- tor. Disease control products should be used with ly described for fungicides also are important for risk other tactics such as traditional host plant resis- assessment for bactericides, nematicides, and trans- tance, crop rotation, biological control, cultural genic pathogen control events. and regulatory controls, and with other strategies such as induced host resistance. Any factor that decreases pathogen populations and their surviv- Management of Plant al will decrease the risk of pathogen resistance de- Pathogen Resistance velopment. Fungicide resistance management has been re- viewed by Brent (1995) and Brent and Holloman Creating the Environment for (1998). The following key points are made by these Management of Plant Pathogen authors, proved with field experience, and appropri- ate to all plant pathogen management tools: Resistance
1. Do not use products with high or moderate risk Critical to the implementation of these manage- in isolation. Use two or more modes of action in ment concepts is the availability of diverse types of combination or alternation in control programs. pathogen management tools. This means continued Specifically, integration of products with low risk registration of existing products with low risk for re- potential with those of higher risk is desirable. sistance development and registration of new prod- Generally this has meant using high risk products ucts with different modes of action. New registrations with low risk ones either in combination or in al- must address the full range of disease control prod- ternation. In practice this has been relatively ef- ucts including biological controls, pesticides, trans- fective; however, the use of a protective contact genic crops, and products that induce systemic resis- material in combination with a systemic materi- tance in plants. Equally important is development of al does not prevent selection of resistant individ- a stewardship ethic by all stakeholders. Manufactur- uals by systemic materials inside the plant. The ers and their marketing groups must take a long-term concept of combinations of protective contact ma- view of sales of moderate or high risk products. Con- terials and systemics for resistance management sultants, food company pest control managers, exten- is weakened when the protective contact materi- sion educators, and farmers should emphasize inte- al has markedly shorter effective residue periods. grated strategies based on sound science. Finally, Only the use of two systemic materials with dif- private and public support for pathogen population ferent modes of action will decrease the probabil- resistance monitoring programs, basic science, regu- ity of selection of resistant individuals within latory programs, and educational programs that sup- plant tissues. port pathogen resistance management must be in 2. Restrict the number of treatments of high risk place. products per season and avoid eradicant use. In- tensity of selection pressure is clearly a factor in development of significant populations with resis- Literature Cited tance. Disease prediction and action thresholds clearly must take this into consideration. Brent, K. J. 1995. Fungicide Resistance in Crop Patho- 3. Use full manufacturers’ recommended dose. gens: How It Can Be Managed? FRAC Monograph Clearly, that is the preferred strategy where ma- No.1. Global Crop Protection Federation, Brussels. jor gene resistance is anticipated; however, where 49 pp. multistep resistance is anticipated, lower-than- Brent, K. J. and D. W. Holloman. 1998. Fungicide recommended dose strategies may not lead to Resistance: The Management of Risk. FRAC Mono- buildup of highly resistant populations. This lat- graph No.2. Global Crop Protection Federation, ter point is not completely clear and more basic Brussels. 48 pp. scientific information is needed. Fungicide Resistance Action Committee. 2003a. 4. Use disease control products integrated with oth- FRAC Fungicide List (1) Arranged by FRAC Code. er pathogen control strategies. Integrated or di-
Fungicide Resistance Action Committee. 2003b. FRAC Fungicide List (2) Sorted by mode of action.
7.4 The Use of Information Technology in Resistance Management and Refuge Compliance Dennis D. Calvin and Joseph M. Russo
Introduction ly, however, between studies and across hybrids (Dillehay 2003). Hyde and colleagues (1999) provid- Information technology provides a framework to ed an economic assessment of the Bt corn technology analyze complex problems and provide crop and pest for European corn borer protection for several states management guidance. Managing resistance within based on published yield impacts of the pest. Little pest populations against control technologies is a topic yield information currently is available for the corn of increasing importance and one for which informa- rootworm material, but it is likely to provide signifi- tion technology can provide help (Ffrench-Constant cant yield protection. and Roush 1990; Marcon et al. 2000). This paper is The adoption rates of the Bt corn for ECB protec- designed to show how information technology can (1) tion currently are being driven by both the perceived provide a valuable framework to analyze the need for and actual value of the technology at a given geo- using a pest management technology and (2) provide graphic location. The actual value is determined by refuge compliance guidance. Before discussing the use climatic factors that influence the synchrony of crop of information technology in resistance management growth stage and timing of stalk tunneling by third and refuge compliance, it may be instructive to dis- instars (Bode and Calvin 1990; Calvin et al. 1988). cuss the value of Bacillus thuringiensis (Bt) corn hy- The synchrony is a function of planting date, relative brids today. maturity group of a hybrid, and weather conditions during a year. Other factors that contribute to im- pact on value include hybrid sensitivity to the pest and Value of Bacillus thuringiensis frequency of an infestation level. Geographically, the Corn Hybrids value of the technology can vary from negative net returns to significant positive returns for farmers (un- In 1996, the first transgenic corn hybrids that pro- published simulations for Risk Assessment and Mit- duced the insecticidal protein Cry I A(b) were released igation Program project [RAMP] (Figure 7.4.1). commercially to protect against European corn borer The first objective of this paper is to report on the (ECB) and several other Lepidopteran pests. These design and capability of a high-resolution landscape hybrids were the result of biotechnology methods used ECB management model to predict average net to transfer the gene that codes for Cry A(b) from Bt returns to a technology and the frequency of fields that ssp. kurstaki into the corn plant genome. Since their can economically benefit from the same technology. initial introduction, Bt corn hybrids have captured The model provides a mechanism to assess the local approximately 22% of the corn market (National Corn need for Bt corn technology. Limiting the use of Growers Association, 2003). The U.S. Department of Bt corn or any other technology use only to fields Agriculture (USDA)–Economic Research Service that will economically benefit from the technology is (ERS) estimated that about 19% of the corn acreage the first line of defense in a resistance management in 2001 was planted to Bt corn hybrids, with use peak- program. ing in 1999 at about 26% of corn acreage (USDA–ERS 2003). Certain counties in the United States have adoption rates as high as 70 and 80%. In 2003, corn Effective Resistance hybrids that code for the Cry 3B(b) protein were re- Management Programs leased commercially to protect against corn rootworm. Bt corn hybrids designed to protect against ECB The second line of defense is the implementation feeding have resulted in an average yield advantage of an effective resistance management program, par- of between 20 to 30 bushels per hectare over their near ticularly in high-adoption regions. Genetic models isolines. This value or yield protection varies great- suggest that at least 20% of corn acreage should be
153 154 7.4 The Use of Information Technology in Resistance Management and Refuge Compliance
Figure 7.4.1. High-resolution landscape map of projected economic value of a 100-day Bt corn hybrid planted on May 1, 2002 using the European corn borer management model (map created by ZedX, Inc., Bellefonte, Pennsylvania). planted to a non-Bt corn refuge to maintain suscepti- fate of the remaining 95 to 99% of the population. bility of ECB in the population. These fields also must Regardless of the scientific understanding behind be planted within 0.5 mile of the Bt corn field to as- the resistance management requirements, they will sure close to random mating, and the field preferably not be effective unless growers adopt them. Lack of should be planted on about the same date and be of adoption or improper adoption will lead to rapid evo- the same relative maturity. Resistance management lution of resistance and the loss of a highly effective programs for transgenic crops represent the first time pest management tactic. Therefore, it is imperative that the U.S. Environmental Protection Agency (EPA) that growers do the best they can to accomplish the has made resistance management a mandatory re- mandatory resistance management requirements quirement for using a technology. Although the rules when using the technology. The second objective of may change in the near future, traditional pesticide this paper is to illustrate how information technolo- technologies have not had mandatory resistance man- gy can assist growers, crop consultants, seed indus- agement programs. Resistance management was try personnel, and government agencies in planning adopted in an attempt to preserve new products for and implementing resistance management plans. insects that are known to develop resistance rapidly. The EPA rules to minimize the evolution of resistance when using Bt hybrids are the culmination of discus- Predicting the Value sion among research scientists, government, indus- of a Technology try, special interest groups, and the general public. The rules are based in part on science, but also on The High-Resolution European Corn Borer Man- compromise. For instance, it is not known scientifi- agement Model has four major components: (1) weath- cally whether 0.5 mile is the appropriate maximum er, (2) corn development,(3) ECB phenology, and (4) distance for the resistance management program. economic analysis. The weather component is provid- This is because scientific methods to quantify insect ed by ZedX, Inc. of Bellefonte, Pennsylvania in the movement are crude and typically are based on mark/ form of spatially interpolated 1-hour temperature pre- recapture studies that only recover 1 to 5% of the re- dictions at a 1-km2 resolution. These temperature leased individuals. The researchers do not know the predictions are fed into both the corn development and Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 155
ECB phenology components of the model. The tem- with an on-line tool to assess the value of Bt corn on perature predictions can be 30-year historic values, their farm. It also will provide an interactive inter- individual year, or real-time predictions (current face that will allow growers to modify values in the year). Additional inputs for the corn development economic equations to better reflect their individual model are planting date and relative maturity of a field or farm conditions. The major advantage of this hybrid. The output of this component is a day-by-day information technology is that it is the first tool for prediction of the proportion of corn development re- farmers and crop advisors to assess whether Bt corn maining to physiological maturity. The ECB phenol- should be grown in a field or on a specific farm. In ogy component is driven by the weather inputs, and locations where the frequency of fields that will ben- it outputs the proportion of the population entering a efit from the technology is low, there is little need for particular life stage on a given day. By overlaying the high levels of technology adoption. If the model’s pre- predicted proportion of corn development remaining dictions are followed, then there also will be a de- to physiological maturity with the predicted propor- creased likelihood of resistance evolution there. In tion of the ECB population entering the third instar, locations where the model predicts that a high per- the daily contribution of the ECB population to yield centage of fields will benefit from the technology, then loss per larva is calculated. By summing the daily adoption of a resistance management program will be contributions to loss per larva, the weighted average essential to prevent resistance evolution. loss per ECB larva is calculated for each geographic grid. For a given geographic grid (1 km2), the weight- ed average loss per ECB larva is calculated for each Information Technology Tools for planting date by relative maturity group grown at the Refuge Compliance location for 30 years of individual weather profiles. This provides a probability distribution of possible A web-based crop management database system losses per ECB larva for each relative maturity and has been developed by ZedX, Inc. that allows consult- planting date combination to feed into the economic ants to input directly Global Positioning System analysis component. (GPS) coordinated field-specific information for pest The basic structure of the economic analysis com- and crop management (Figure 7.4.2). The consultants ponent is a cost/benefit ratio. Benefit of a technology collect and input field data from a remote setting onto is calculated using the following formula: the ZedX, Inc. server in Bellefonte, Pennsylvania. Benefit of the Technology = MV X EY X There the GPS data can be analyzed and a report re- NIPP X PLPI X PC turned to the consultants to help their clientele plan where MV = expected market value of the crop; EY = crop management. This system offers a mechanism expected yield of the crop; NIPP = number of insects to provide growers with assistance in developing a per plant; PLPI = predicted loss per larvae per plant; resistance management program for their farm and and PC = expected proportional control from the tech- to help the seed industry and the EPA monitor com- nology. pliance. The cost of the technology is calculated using the Currently, farmers provide to their consultant in- following formula: formation on corn hybrids that includes planting date, Cost of Control = NA (MC X AC) maturity group, and GPS position. The GPS position where NA = number of applications; MC = material may be for a field or a subfield location where the cost; and AC = application cost. For transgenic corn hybrid was planted. Using these GPS locations, math- hybrids, the cost of control simply is the technology ematical formulas can be employed to measure loca- fee because it is applied only once a season at the time tion and distances between the Bt corn and its non- of planting. Therefore, a second trip across the field Bt refuge. The database system can be used to is not needed. The outputs of the model are colored calculate whether individual fields are in compliance maps of the average net return of Bt corn for each 1 and the degree to which a farm is in compliance. If km2 across North America and the frequency of corn- adequate numbers of farms within a county or region fields likely to benefit from the technology. are in the database, then the percentage of compli- The high-resolution ECB management model is an ance for the region can be calculated and made avail- information technology that integrates all relevant able to industry or to the EPA (with permission of the biological knowledge necessary for an economic as- consultant’s farmer clientele). The key, however, is sessment of a technology to manage the pest. These cooperation of the farmers with industry and the EPA. maps will provide growers and their crop advisors The technology is available to check compliance, but 156 7.4 The Use of Information Technology in Resistance Management and Refuge Compliance
Figure 7.4.2. Example of how fields, bounded with GPS coordinates, can be used for hybrid location and the calculation of resistance management compliance (screen shot provided by ZedX, Inc., Bellefonte, Pennsylvania). The map background is a U.S. Geographical Sur- vey orthodigital quarter quad. it will require trust among farmers, industry, and the Ffrench-Constant, R. H. and R. T. Roush. 1990. Re- EPA. Without this trust and cooperation, the only sistance detection and documentation. Pp. 4–38. In mechanisms are to help farmers with planning ref- R. T. Roush and B. E. Tabashnik (eds.). The Rela- uge compliance and to implement an educational pro- tive Roles of Pesticidal and Biochemical Assays. gram through crop consultants and extension. No Pesticide Resistance in Arthropods. Chapman and matter what the mechanism for monitoring compli- Hall, New York, New York. ance, the industry still is responsible for assuring that Hyde, J., M. A. Martin, P. V. Preckel, and C. R. Ed- farmers who purchase their seed comply with man- wards. 1999. The economics of Bt corn: Valuing pro- datory resistance management. tection from the European corn borer. Rev Ag Econ 21:442–454. Marcon, P. C. R. G., B. D. Siegfried, T. Spencer, and Literature Cited W. D. Hutchison. 2000. Development of diagnos- tic concentrations for monitoring Bacillus thuring- Bode, W. M. and D. D. Calvin. 1990. Yield-loss rela- iensis resistance in European corn borer (Lepi- tionships and economic injury levels for European doptera: Crambidae). J Econ Entomol 93:925–930. corn borer (Lepidoptera: Pyralidae). J Econ Ento- National Corn Growers Association. 2003. The World mol 84:1595–1603. of Corn Production 2003,
7.5 Resistance Management Education and Communication: Weeds in Vegetable Crops Michael D. Orzolek
Introduction and can be applied either pre- or postemergence, almost all corn growers (those raising field, sweet, Weed management in vegetable crops, and in hor- pop, and ornamental corn) in Pennsylvania make one ticultural crops generally, presents many challenges, application/acre/year. Thus, the challenge for Exten- the least of which is that vegetables are classified as sion is to provide viable, efficient method(s) of control- minor crops and have few labeled herbicides compared ling weeds in vegetables by chemical and/or cultural with agronomic crops. Also, there are no weed-resis- means and to encourage the decrease or elimination tant vegetable varieties like there are disease-resis- of atrazine use in the state while using IPM methods tant and, to some extent, insect-resistant varieties. for weed control in vegetables. Out of necessity vegetable growers have had to prac- tice integrated weed management, but many have adopted only a partial list of integrated pest manage- Cultural Controls ment (IPM) practices, assuming that weed resistance to current herbicides will not occur in their fields or Cultural controls can help to decrease problem pop- during their lifetime (growers in the age group over ulations and resistant weed populations in many 50). fields by at least 50% a year. Monitoring fields and identifying the different type of weeds and population Weed Management Programs changes that take place each year will help growers decide what crop(s) to plant in each of the fields, de- pending on weed demographics. In addition, some All vegetable weed management presentations in vegetable crops, when grown in a no-till system, are Pennsylvania have emphasized an IPM approach. more competitive than the weeds and compete rath- The presentation is divided into two segments: cul- er effectively from establishment through harvest. tural controls and chemical controls. Cultural con- trols include tillage methods, liming and soil pH man- • Crop rotation. Use of legume cover crops (hairy agement, banding fertilizer, crop rotation, cultivation, vetch, clovers, etc.) or small grain in a crop rota- crop density, identifying and treating hot spots of tion program will provide effective weed control weeds in the field with nonselective herbicides, elim- of most annual broadleaf weeds such as ragweed, inating weed seed production in the crop, and using jimsonweed, and galinsoga. Because most minor plastic mulch, raised beds, and drip irrigation. Chem- crops have few labeled herbicides, rotating minor ical control methods include proper identification of crops (horticultural crops) with corn and soybeans the problem weed, treatment of actively growing will increase the number of labeled herbicides weed(s), correct choice of herbicide and rate, correct available that will control both annual and peren- application technique, and uniform application in the nial weeds. This practice also will enable the field. grower to choose from more herbicide families and A Resistance Management Education program has to decrease the potential for resistance in weed been part of my Integrated Weed Management Exten- populations. sion program for the last 10 years in Pennsylvania. • Tillage. The use of a moldboard plow in alternate Weed resistance is a critical concern to both educa- years or at least every third year will provide gen- tors and regulators in Pennsylvania because there are erally better perennial weed control (for weeds currently two widespread weeds resistant to atrazine: such as Canada thistle and horsenettle) than chis- common lambsquarters and redroot pigweed. Be- el plowing. Moldboard plowing will bring to the cause atrazine is an inexpensive herbicide to apply, soil surface and expose the large storage organ controls a large number of grass and broadleaf weeds, (root) of many weeds so that over time the
157 158 7.5 Resistance Management Education and Communication: Weeds in Vegetable Crops
storage root desiccates and/or rots. populations of a weed. • Cultivation. Timely cultivation can control many • Use of plasticulture systems for vegetable produc- annual weeds effectively, especially weed popu- tion. Many vegetables benefit from being grown lations that have acquired resistance to on raised beds covered with plastic mulch and drip herbicide(s) or have a very narrow genetic base irrigation tape buried beneath it in the bed. The or variation. Generally, cultivating several times plastic film generally is black but can be other during the growing season in specific crops grown colors; it not only eliminates weed growth in the in fields with low weed seed populations will pro- 28" to 30"-wide top of the 6" to 8"-tall bed but also vide effective weed management during the en- increases soil temperature, maintains higher tire growing season. The one drawback of rely- soil moisture levels, decreases leaching of ing solely on cultivation for weed control during nutrients and other pesticides applied to the bed, the growing season, however, is rainfall and wet and retains soil structure throughout the soils. Extended wet periods can eliminate the growing season. use of a cultivator in the production field for several weeks while young weeds still are If populations of volunteer weeds are still growing growing actively. after the grower has used several of the cultural con- • Banding or injecting fertilizer. Application of fer- trols available for weed management in vegetables, tilizer as a band next to the crop provides nutri- then the use of herbicides should be considered. Be- ents to the crop but not to the weeds, especially fore applying the herbicide on the problem weed(s), between crop rows. Likewise, injecting fertilizer however, the grower needs to make several decisions: in drip irrigation tapes will provide nutrients for (a) is the herbicide labeled for that particular crop use? the crop but not for the weeds. Banding also helps (b) will the herbicide provide effective control of the to decrease the total cost of nutrient application problem weed in the crop? (c) what rate should be for a vegetable crop. applied and what method of application should be • Plant populations. The higher the plant popula- used? (d) are there any sensitive crops being grown tion per acre, the greater the canopy of the vege- near the field where the herbicide will be applied? and table crop and the decrease in the number of (e) what is the half-life of the herbicide and how long weeds that are competitive with the crop due to will it last in the field after application? If a grower lack of or decrease in photosynthetic active radi- has answered all these questions to his or her satis- ation. Plant populations can be increased within faction, then applying a specific herbicide to a specif- limits to enhance canopy development of the crop ic vegetable crop to control specific weeds should be without compromising crop yield or quality. the choice that is made. Of course, it is assumed that •Eliminating weed seed production. This is the (1) there is negligible wind during application, (2) the most significant cultural practice that will reap sprayer has been calibrated correctly, (3) all nozzles rewards for years. The elimination of viable weed tips and screens have been checked for wear and seed and/or reproductive structures by either me- blockage, and (4) both the crop and weed populations chanical or chemical means will, over time, result are actively growing and not under stress. in much smaller weed seed populations in the soil After presenting this material to grower/producer bank that can actively compete with vegetable clientele at local and statewide meetings during the crops in the future. Simply mowing weeds and winter, I am amazed, even after 29 years as an Ex- eliminating immature flowers on the weeds is tension Educator, at the number of growers who con- very effective. Some weeds when mature can sup- tact me during the growing season to ask why there ply thousands of weed seeds per plant back into are still volunteer weeds in their vegetable crop or the soil bank and be problems for many years to why their vegetable crop appears stunted, discolored, come. or necrotic. Even though the information on herbi- • Treating hot spots. Many weed problems origi- cide application presented to the growers is current nate in fencerows near the field with only a few and up-to-date, as growers become busier tilling their plants or even one. Treating and eliminating fields, planting crops, and monitoring pests in the weeds, even if only one or two that seem insignif- field, they invariably will take short cuts to use their icant at the time, in fencerows will help to elimi- time more efficiently and to maintain a production nate future problem weeds in the field. Also, elim- plan for the year. But short cuts lead to mistakes and inating hot spots in a production field as they mistakes can result in the decrease of both yield and become apparent will prevent future large-scale quality of most vegetable crops. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 159
Sweet Corn: A Case Study Weed control in the 9,700 hectares of sweet corn in Pennsylvania is important to ensure timely har- vest, maximum yield, and quality of the sweet corn crop. Early weed infestation in sweet corn decreases both early and total marketable yield and quality because of competition for both water and nutrients and may serve as a reservoir for other sweet corn in- sect pests. Although there are several herbicide op- tions for use in sweet corn, maturity of the variety, production system, and date planted will influence the choice of herbicide and other weed management prac- tices. Soil temperature will generally determine when sweet corn is planted (minimum soil temperature for sweet corn germination and emergence is 50°F) throughout the state. For very early sweet corn (be- fore July 4), most growers will plant sweet corn seed in furrows and cover the double rows with clear poly- ethylene mulch in mid- to late April. The clear poly- ethylene mulch will warm the soil and maintain a higher level of soil moisture compared with bare ground. Plastic is not selective, however, so weed seed will have the same advantage as sweet corn seed for early germination and soil emergence. Weed manage- ment in this instance could be as simple as field se- lection and crop rotation or as intense as preplant- incorporated and preemergence herbicide applications. Currently there are only 3 labeled her- bicides for preplant-incorporated or preemergence weed control in sweet corn: atrazine, metoachlor, and alachlor. One immediate concern for continued use of these materials, especially atrazine, is the devel- opment of weed resistance. Currently, both atrazine- resistant pigweed and lambsquarters can be found in Pennsylvania. In addition, many vegetable crops are extremely sensitive to atrazine residues, especially from application rates in excess of 1.4 kilograms/hect- are from the previous year. Because sweet corn can be planted continually from April through August, ap- plication of atrazine can result in buildup of atrazine residue in soil and the potential for additional weed resistance development. How can this problem with atrazine and other herbicides be avoided in the fu- ture? The answer may be using more cultural weed management techniques including (a) scouting the field in which sweet corn will be planted the follow- ing year, (b) avoiding fields with serious weed prob- lems, especially high populations of perennial weeds, (c) effective crop rotations programs including the use of cover crops, (d) use of higher plant population pro- grams (39,500 vs. 54,300 plants per hectare), and (e) using different families of herbicides to control weeds in sweet corn. 160
7.6 The Resistant Pest Management Newsletter and Resistant Arthropods Database Mark E. Whalon and Erin Gould
Introduction Features of the RPM News include the following: The Resistant Pest Management Newsletter (RPM • Letter from the Editors / Editorials News) is international in scope with worldwide circu- • Resistance Management Reviews: Summaries lation to approximately 3,000 resistance workers in and analyses of important resistance manage- academia, industry, and government. The newslet- ment topics geared toward a general reader au- ter provides information on the ongoing changes and dience advances in the field of resistance management. The • Resistance Management from Around the World: RPM News is a biannual publication of the Center for Articles highlighting resistance issues from glo- Integrated Plant Systems (CIPS) in cooperation with bal localities the Insecticide Resistance Action Committee (IRAC) •Research in Resistance Management: The fea- and the Western Regional Coordinating Committee ture article—an exhibition of research in the field (WRCC-60). We are proud to introduce the first elec- that leads toward an advanced understanding of tronic version of the RPM News during this, the tenth issues while providing practical applications year of publication. With the new electronic format, • Resistance Management News: Briefings (new the RPM News endeavors to provide an accurate, in- findings, recommendation, etc.) and industry formative, and useful resource to our readers while news (new products, label changes, etc.) enhancing the communication of ideas among col- •Abstracts leagues worldwide. • Symposia Information: Meetings, forums, confer- The electronic format allows us greater facility to ences of interest serve our readers through the rapid publication of • Readers’ Response: Letters and comments from breaking events in resistance development and man- our readers agement. Our hope is that there will be decreased • Announcements and Submission Information: time between the availability of issues as well as in- Corrections, reminders, calls for papers creased access, leading to a more informative and • E-mail Notification of New Issues complete reporting process for resistant pest manage- •A Link to the Resistant Arthropods Database ment globally. In addition, we intend to publish up- • An Archive of Past Issues dated lists and other relevant information from our • Ask an Expert: A listserv of international profes- sister website, the Resistant Arthropod Database. We sionals in various fields willing to give expert ad- trust that you will find many of the articles, abstracts, vice related to resistance management. and other information in our newsletter useful and informative. The Resistant Arthropods Database is the accumu- lation of resistance data published on the Internet as RPM News a public service, for use by resistance management practitioners around the world. This database reports instance of resistance from 1914, when resistance was The editorial staff of RPM News is excited about first discovered for a specific time and place, to the our new web venue and hope that it will serve read- present. Pesticide resistance is a dynamic, evolution- ers’ resistance information needs effectively. The ary phenomenon and a record in this database may website is available at
160 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 161
Resistance Database There is a worldwide need for accurate, easily ac- cessible pest resistance information—information that will be used by numerous stakeholders in agri- culture, human health, and animal protection as well as those in structural, ornamental, and other pest management arenas. In addition, regulatory, struc- tural, and evolutionary pressures surrounding resis- tance development illustrate the need to document, understand, and manage resistance more effectively. In order to manage resistance effectively there is a clear need for access by decision makers to appropri- ate and critical information. Our goal in implement- ing a resistance database is to help address arthro- pod resistance by evolving an integrated, cooperative system to deliver resistance information efficiently. Currently, our information resides in an electronic database at Mark Whalon’s laboratory at Michigan State University’s Center for Integrated Plant Sys- tems and is available through the Internet at
7.7 Resistance Management Education and Communication Ronald E. Stinner
Introduction • Insecticide Resistance Action Committee (IRAC) website. Approximately 5 years ago, the CIPM By way of introduction, a brief description of the was approached by the IRAC to see if we would Center for IPM (CIPM) and our focus is needed to put be willing to set up a small website for IRAC, con- our efforts with resistance management information sisting primarily of a PowerPoint presentation in context. The Center for IPM is a National Science explaining the issue of Insecticide Resistance and Foundation-founded Industry/University/Govern- the role of IRAC. The site has expanded greatly ment Cooperative Research Center that both funds since then in size, types of content, and technolo- projects throughout the United States with member- gy. The site is now a complex, database-driven, ship fees and competes for funding in the sectors of international source of information from IRAC. It information dissemination and cooperative manage- includes information on resources, education, ment of integrated pest management (IPM) programs. current events, and news. It also has project fund- The Center was started in 1991. To avoid potential ing reports and a members’ section for internal conflict of interest, the Center engages in no propri- use. News is maintained in a database and shown etary research and all programs are approved, and dynamically on the first page. Current literature results shared, by the Center members through an citations are available along with a calendar of Industry Advisory Board. events. Of course, the site maintains the origi- Because many of our members are national and in- nal educational slide shows and knowledge quiz ternational companies and organizations, the CIPM for students. A unique feature is that all of the has maintained a national and international focus. site’s content is written and controlled from the With the geographic diversity in our membership and United Kingdom through a secure back-end da- the nature of IPM, we were forced early on to invest tabase that allows immediate updating. heavily in information systems. With the public ad- • HRAC website. The CIPM also has maintained vent of the World Wide Web in 1993, one of our pri- the HRAC website for several years. The site fea- mary tasks became the dissemination of current, ac- tures a number of reports and the Mode of Action curate, and unbiased information needed in the IPM (MOA) Classification, including downloads of community. Because we have been a member-based large posters displaying the chemical structures organization, we have focused on cooperative efforts involved. The HRAC also has developed a num- with many diverse organizations to provide IPM in- ber of their documents in Spanish and these are formation electronically. available on the site. This is a more traditional site, with updates e-mailed from the chairman of the communications committee in Germany, but Four Cooperators to a CIPM employee now living in Kansas for post- ing on the server located in North Carolina. In this paper, I would like to describe our efforts • Insecticide Resistance Management (IRM) train- with four cooperators. Two are funded through our ing website. The third site provides on-the- membership account; one is a funded U.S. Depart- ground information to consultants and farmers on ment of Agriculture–Cooperative State Research, their choices for IRM with genetically modified Education, and Extension Service (USDA–CSREES) crops, specifically Bacillus thuringiensis (Bt) cot- program (USDA Pest Management Centers); and one ton and corn. The site has been funded from our is not funded, but supported internally, simply be- Center membership account, at the request of cause the information needed to be made available Monsanto, but with the approval and review of and we could provide the technology (Herbicide Re- our full Industry Advisory Board. With the U.S. sistance Action Committee [HRAC]). Environmental Protection Agency (EPA) 162 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 163
requirements for management plans, the use of industry and other organizations that have an inter- online training and management plan explana- est in public exchange of data. tions makes both components easy and accessi- In closing, I would expand on the CIPM’s desire to ble. For these management plans to work, grow- cooperate with other organizations, both public and ers, extension personnel, crop consultants, and private. The CIPM has national and international industry all must use the same information. Com- information dissemination as a core function. We munity plans can be complex and the rules can have the infrastructure in terms of personnel and change, as we have already seen with Bt cotton. commercial servers, and we have public interest— Where numerous choices in refuge design exist, with more than 2.5 million hits per month. If you have as is the case with Bt corn, graphics of the choic- valid and current IRM data, and you want to share es make choice selection easier. With a web for- it, we will work with you. mat, updates in information are easy and down- loadable agreement forms can even be provided. The site is relatively small, easy to navigate, and provides the essentials needed for planning deci- sions. •PM Centers. The CIPM is the management enti- ty for the National Information System of the USDA Regional IPM Centers. Much of the focus of this system deals with pesticides and pesticide use in the context of PM. To that end, the CIPM currently maintains databases for the National Agricultural Statistics Service (NASS) pesticide use data, IR–4 and Office of Pest Management Policy (OPMP) new technology data, and the EPA crop activity timelines. We also maintain dynam- ic searching and links among some of these data- bases as well as with the EPA Pesticide Label System. At present we do not have resistance data, but we see some new technologies as the key to integrating the information we maintain with that available or being developed by others. There is a crucial need for this integration. The MOA classifications change, new resistance problems emerge, the EPA continues to require more plan- ning and data, and much of the information is text-based rather than part of a formal database structure.
Because of this, the CIPM has been drawn into the mysterious world of Extensible Markup Language (XML), or data-sharing on the Web. Without a disser- tation on XML, suffice it to say that this technology for data sharing requires a formal set of standards that define terminologies and structure called a DTD (Data Type Definition). Groups such as RAPID and C&P Press already have developed Pesticide DTDs, but these are proprietary and not available in the public domain. The CIPM, through the USDA Region- al Pest Management Centers and cooperating with representatives from IR–4, NASS, OPMP, and the EPA, has begun the process of developing and pub- lishing a DTD. We would welcome involvement from 164
7.8 A Producer’s View of Managing Bacillus thuringiensis Technology Thomas Slunecka
Introduction Compliance Assurance Program (CAP) was expand- ed, outlining how registrants of Bt corn are required In the practice of producing high-quality corn at to monitor, assist, and deal with growers who do not minimum expense, each percentage increase is cru- follow IRM requirements. cial. Bacillus thuringiensis (Bt) corn has proved to be With the advent of rootworm-resistant corn, the an important technology to help corn growers control rules are changing. Insect resistance management re- damaging insect pests and produce higher yields and quires corn borer-resistant-corn growers to plant at better-quality grain. For many producers, the consis- least 20% of their acreage to a non-Bt corn refuge. In tency of control far outweighs up-front seed purchase certain cotton-growing regions where both Bt corn and costs. But the cost/benefit ratio of the technology is Bt cotton are planted, growers must plant a 50% non- not calculated easily. Complications in this calcula- Bt corn refuge. The Bt corn must be located within tion result from added production costs of planting to 0.5 mile of the refuge (0.25 mile is preferred). When meet insect resistance management (IRM) require- using strip methods, the refuge must be at least four ments and variations of hybrid maturity. In addition rows wide. Rootworm-resistant corn has the same to these agronomic differences, we need to add man- refuge requirements; however, those refuges must be agement costs of hybrid selection and marketing re- adjacent and at least six rows wide. The differences striction. in product IRM requirements can create confusion, According to a survey of growers who planted Bt which further illustrates the need for a consistent corn in the 2002 season, the majority of Bt corn grow- source of information for all stakeholders. ers understand the importance of IRM; awareness has risen to 81% in 2002 from 58% 2 years earlier (Agri- cultural Biotechnology Technical Committee 2002). Role of the National Corn Compliance to IRM requirements still is not at 100%, Growers Association however. According to that same survey, the majori- ty of Bt corn growers (86%) planted at least the min- One of the NCGA’s main roles is to serve as the imum required refuge size in 2002, remaining fairly leading voice for corn growers in the promotion of IRM constant over the previous year. From the National to U.S. corn growers. The NCGA advocates the con- Corn Growers Association’s (NCGA) perspective, tinued availability of federally regulated and ap- reasons for noncompliance include several economic proved seed and crops produced through biotechnol- factors; yield concerns; convenience factors; available ogy. The NCGA supports the science-based hybrid selection; information flow; and the key mes- regulatory process and stands behind the system that sages being presented to producers, the media, and approves these new tools for agriculture and food pro- influencers. tection. Through its educational program, the NCGA has instituted a multifaceted approach that includes the Insect Resistance Management following: Requirements • Insect Resistance Management Logo. The NCGA The Bt corn industry has been operating under the was instrumental in the development of the IRM “unified plan” for IRM since it was accepted by the logo, which has been adopted by government and U.S. Environmental Protection Agency (EPA) in 2000. industry in IRM awareness campaigns. The unified plan was developed by the Agricultural • “Know Before You Grow” Program. This program Biotechnology Stewardship Technical Committee includes a comprehensive, dynamic database of (ABSTC) in cooperation with the NCGA. In 2003, the commercially available hybrids as well as their
164 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 165
approval status, allowing growers to make in- Literature Cited formed decisions that will affect them not only at planting, but also at harvest when the grain is to Agricultural Biotechnology Technical Committee. be marketed. This database is accessible at the 2002. Insect Resistance Management Grower NCGA’s website,
The challenge to the Bt corn industry will be to use this recognition of value as a means of improving growers’ appreciation for the importance of IRM as the best way to preserve the technology over the long term. Certain elements of the CAP, such as the phased compliance approach, combined with the industry’s ongoing educational plan, should strength- en growers’ stewardship of this technology in the future. Producers understand and take very seriously their role in the technology community. This is a steep learning curve, but U.S. farmers have proved time after time their willingness to do the right thing for the environment, their trade, and their own well-being. 166
Conclusions and Recommendations
Conclusions the presentations, papers, and discussions during the symposium. The Council for Agricultural Science and Technol- ogy’s Pest Resistance Management Symposium was • Pest resistance is a genetically based decrease in the first U.S.-based multidisciplinary stakeholder susceptibility in a pest species. meeting on pest resistance management (PRM) since • Pest resistance results in control failures and can the 1995 American Chemical Society meeting on lead to disrupted pest management systems, mechanisms of pest resistance and the 1984 Nation- higher costs of pest control, and use of more pes- al Research Council meeting on pest resistance. The ticides that may pose higher risks to human Symposium provided the opportunity for all stake- health and the environment. (Even organic pro- holders involved in insect, weed, and pathogen pest duction can be affected by pest adaptation to management to come together in a fruitful discussion management practices, although pest resistance of the issues, laying the foundation for future collab- is not considered to be a major issue.) Therefore, orations addressing PRM. pest resistance is identified as a growing chal- The coverage of different classes of pesticides (her- lenge to sustainable agriculture both in the Unit- bicides, fungicides, and insecticides) made evident the ed States and in other countries throughout the important differences among and within these class- world. es in terms of resistance management (RM) needs and • Understanding the scientific basis for why a strat- highlighted the necessity of addressing these needs egy will work is fundamental to the success of ef- on a case-by-case basis. At the same time, a number fective, preventive RM strategies. of general conclusions emerged. • Resistance management is a key component of in- The overall conclusion of the meeting was that tegrated pest management (IPM). PRM is very important to the sustainability of agri- • Successful RM requires a long-term vision. cultural production systems. Achieving proactive or • Proactive or preventative RM generally is prefer- preventive RM is a desirable goal, but how to achieve able to reactive RM, but is more complex. If pre- it is a complex process that requires extensive input ventative measures are expensive and of uncer- and commitment by all stakeholders. The keys to ef- tain value, and the evolution of resistance does not fective RM are strong science; environmentally be- impact the value of the product significantly, then nign, feasible, and cost-effective strategies; and edu- preventative management may not be cost effec- cation about the benefits of implementation. In tive. It is desirable to formulate RM plans before addition, multiple pest control tactics, including cul- commercialization of a new chemical active ingre- tural practices, biological control, transgenic plants dient. producing pesticidal substances (such as Bacillus thu- • Successful RM requires input and collaboration ringiensis [Bt] insecticidal endotoxins), and chemical by all stakeholders. The goals and objectives of pesticides (with different modes of action), can help RM must be clear, and support should be sought decrease selection pressure for the evolution of pest from all parties. resistance. That is, to most effectively curtail resis- • Education and training are fundamental to the tance, nonchemical pest control practices should be implementation and adoption of RM strategies. augmented with different pesticide modes of action in- •Resistance management benefits must be demon- cluding biological control. Lastly, further research strated to growers. Successful RM should be into the development, implementation, and adoption profitable, sustainable, and environmentally ben- of RM is necessary. eficial. Several specific conclusions were identified from • Federally funded RM research is important to the successful development and implementation of
166 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 167
effective RM strategies and should be a compo- • Resistance monitoring plays an important role in nent of federally funded IPM grant programs. surveillance and detection of resistance prior to • The U.S. Department of Agriculture (USDA) and field failure where suitable tools are available the U.S. Environmental Protection Agency (EPA) (e.g., many insecticides). It can be an expensive play important roles in PRM and pesticide regu- proposition to find a rare event, however. New lation. The Interregional Research Project–4 (IR– developments using biotechnology and high- 4) plays a particularly important role in register- throughput engineering could increase signifi- ing new pesticide uses and biopesticides, cantly the effectiveness and timeliness of moni- especially for minor crops. The USDA–Natural toring, while decreasing the cost. Homeland Resources Conservation Service (NRCS) could be Security funding may be appropriate both in re- engaged by identifying RM programs as conser- sistance detection/monitoring and resistance re- vation practices within the Farm Bill Environ- mediation to enhance food security. mental Quality Incentives Program (EQIP) and • Plant breeding can be an important component Conservation Security Program (CSP) titles. in successful implementation of effective RM and • Central and permanent databases of pest and pes- should be encouraged in this context. ticide resistance information are important and • In organic production of short-term annuals, pest need continued funding. Two such databases ex- resistance has not been a big issue because of the ist: one for herbicides and resistant weed biotypes extensive focus on crop rotation and other cultural (WeedScience 2003) and one for insecticides and management practices, soil management, and the resistant insects (Michigan State University– use of biological pesticides. Organic production Center for Integrated Plant Systems 2003). of perennial crops, however, has not always suc- • Dissemination of pest and pesticide resistance in- cessfully managed resistance (e.g., diamondback formation is necessary to determine the extent of moth resistance to Bt microbial pesticides used in resistance. Such information also is needed to de- Hawaiian watercress production, and tetranychid velop RM strategies in locations where resistance mite, Bryobia sp., resistance to sulfur). to the same or related mode of action has not oc- curred but is likely to occur in the future. • Agricultural information technology provides a Recommendations mechanism for disseminating forecast tools to and Suggestions know where and when to use a pest control tech- nology. Use of this information may decrease the Participants made several RM recommendations selection pressure on any one pest control tactic and suggestions in a discussion held at the end of the and increase its efficiency and effectiveness. symposium. These recommendations focused on four • Barriers that impede the development of effective areas: (1) Science, (2) Research and Extension, (3) RM strategies do exist and include the following: Education, and (4) Policy. ° limited understanding of the factors affecting resistance evolution, Science Recommendations ° limited product availability, ° economic factors, • Resistance management strategies should be de- ° short-term solutions, veloped on a case-by-case basis, considering char- ° focus on individual crops/pests rather than acteristics of the chemistry, the target pests, and a holistic-systems approach for the agroecosys- the management system using certain guiding tem, principles. ° lack of clear goals and objectives, • Guidance and direction are needed in developing ° lack of clear RM regulatory policy, resistance monitoring programs for new technol- ° limited federally funded and industry-funded ogies including establishment of baseline suscep- RM research, and tibility, detection techniques, and sampling strat- ° competitive marketing practices within indus- egies. try that discourage proactive, preventive RM. • Resistance management strategies should be flex- ible to allow changes over time due to the tempo- • Predictive models are useful for comparing RM ral and spatial variation in the pest/crop/pesticide options and identifying key data gaps, but they situation. Databases can be used to measure the offer a simplified reality. extent of resistance both temporally and 168 Conclusions and Recommendations
spatially. Further funding of resistance databas- Education Recommendations es is recommended. • Standard definitions of resistance should exist for • Resistance management education programs pest/pesticide combinations and methods of doc- should continue to be developed and implement- umentation and validation (e.g., field failure, bio- ed as part of ongoing pesticide education pro- assay [dose response, discriminating or diagnos- grams. The support of the EPA and the USDA
tic dose concentration], tenfold LD50, DNA for RM, as part of a pesticide education program, markers, change in resistance allele frequency). is important. More educational materials are • Economic benefits and costs of effective RM needed in relation to PR Notice 2001-5, including should be developed, identified, and described voluntary RM labeling based on mode of action. better. One suggestion was to develop an issue The USDA/Cooperative State Research, Educa- paper on the economic impacts of resistance and tion, and Extension Service should improve their RM. coordination of education programs. • Consumer education programs should include the cost of producing “blemish-free” food in the mar- Research and Extension Recommendations ketplace and the use of reduced-risk pesticides. • There should be explicit RM priorities within the federal government. Policy Recommendations ° One suggestion was to create a new competitive grants program to focus on RM. • The USDA grading (marketing) standards and ° Other suggestions involved strengthening exist- the marketing of food internationally should be ing USDA competitive grants research pro- examined for their impact on RM. grams to provide more explicit priorities with- • Although all stakeholders noted the EPA’s role in in the Request for Applications (RFAs) to fund RM as important, there was disagreement about RM research. These include the National Re- the scope and regulatory nature of this role. search Initiative programs and the following ° Some participants recommended a mandatory Section 406 programs: Risk Avoidance Mitiga- role for the EPA in RM, but consensus was not tion Program, Crops at Risk, Extension Inte- achieved in the limited time available. grated Pest Management Implementation, Me- ° Others noted that the rigid nature of mandato- thyl Bromide Transition Program, Organic ry regulations could impact negatively the effec- Transitions Program, Pesticide Safety Educa- tiveness of RM, as well as industry investment tion Program, and the Biotechnology Risk As- in product development and the diversity of con- sessment Research Program. For all programs trol options available. cited here (or others to be developed), research ° The Fungicide Resistance Action Committee rec- efforts should be prioritized to make best use of ommended that the mode of action guidelines de- available resources. This process should involve scribed in PR Notice 2001-5 (EPA) and DIR 99- all stakeholders in the RFA development. 06 (Canada) become mandatory to provide ° IR–4 funding should include RM research for uniformity within fungicide classes. The other minor crops. Resistance Action Committees (herbicides and ° Resistance management research should be part insecticides) did not support such a move. of the mission of the Regional Integrated Pest ° The EPA’s regulatory process for RM should be Management Centers. more transparent and be made clearer (e.g., ° Research efforts should be multidisciplinary and what constitutes a “public good” or pesticides de- collaborative. serving of regulation). ° The EPA’s Section 18 (Emergency Exemption) • One suggestion was to create an RM research process should allow for the use of reduced-risk initiative supported jointly by funds from a user pesticides with alternative modes of action in fee associated with pesticide sales and funds from crops and on pests where resistance has been a the federal government. Some grower groups chronic problem. noted that this could be a significant burden on ° There should be mechanisms to provide incen- growers. tives and/or rewards for good RM and environ- mental stewardship by industry and pest managers. Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 169
• Several suggestions were made that Farm Bill priorities should be changed to better fund RM re- search and education. Specifically, The NRCS should recognize RM as a conservation practice under the EQIP and CSP Titles.
Literature Cited
Michigan State University–Center for Integrated Plant Systems. 2003. The Database of Arthropods Resistant to Pesticides,
WeedScience. 2003. International Survey of Herbicide Resistant Weeds,
Appendix A: Abbreviations and Acronyms
µg microgram EUP Experimental Use Permit a. acre FAOSTAT Food and Agricultural Organization AAFC Agriculture and Agri Food Canada of the United Nations, Statistical ABSTC Agricultural Biotechnology Steward- Database ship Technical Committee FIFRA Federal Insecticide, Fungicide, and ACCase acetyl-CoA carboxylase Rodenticide Act AHAS acetohydroxyacid synthase FQPA Food Quality Protection Act ALS acetolactate synthase FRAC Fungicide Resistance Action ARS Agricultural Research Service Committee ASTA American Seed Trade Association ft feet BRARGP Biotechnology Risk Assessment FTE full time equivalent Research Grant Program FY fiscal year Bt Bacillus thuringiensis GE genetically engineered BW bollworm GMO genetically modified organism CAP Compliance Assurance Program GPS Global Positioning System CAR Crops at Risk ha hectare CAST Council for Agricultural Science and HPPD hydroxyphenyl-pyruvate- Technology dioxygenase CBI Council for Biotechnology HRAC Herbicide Resistance Action Information Committee CIPM Center for Integrated Pest ICM integrated crop management Management IGR insect growth regulator CRW corn rootworm IMI imidazolinones CSP Conservation Security Program IPM integrated pest management CSREES Cooperative State Research, IR–4 Interregional Research Project Education, and Extension Service Number 4 DBM diamondback moth IRAC Insecticide Resistance Action DMI dimethylation inhibitor Committee DPE diphenyl ethers IRM insect resistance management DSMA disodium methanearsonate IWM integrated weed management
DTD Data Type Definition KD50 median knockdown EBDC ethylenebisdithiocarbamates LC50 median lethal concentration ECB European corn borer LD50 median lethal doses ED effective dose LGU Land-Grant Universities
EPA U.S. Environmental Protection LT50 median lethal time Agency MBT Methyl Bromide Transitions Program EPPO European and Mediterranean Plant ml milliliter Protection Organization MOA mode of action EPSPS 5-enolpyruvylshikimate-3-phosphate MSMA monosodium methanearsonate synthase MSU Michigan State University EQIP Environmental Quality Incentives MSU–CIPS Michigan State University–Center Program for Integrated Plant Systems ERS Economic Research Service NA-FRAC North American Fungicide EU European Union Resistance Action Committee
170 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 171
NAFTA North American Free Trade USDA–ARS U.S. Department of Agriculture– Agreement Agricultural Research Service NASS National Agricultural Statistics USDA–ERS U.S. Department of Agriculture– Service Economic Research Service NCC National Cotton Council WCRW Western corn rootworm NCGA National Corn Growers Association WHO World Health Organization NPC National Potato Council WSSA Weed Science Society of America NRI National Research Initiative XML Extensible Markup Language OECD Organisation for Economic Co-Operation and Development OP organophosphate OPMP Office of Pest Management Policy OTP Organic Transitions Program PAMS prevention, avoidance, monitoring, suppression PEP phosphoenolpyruvate PESP Pesticide Environmental Steward- ship Program PSEP Pesticide Safety Education Program PIP plant-incorporated protectant PM pest management PMAP Pest Management Alternatives Program PMRA Pest Management Regulatory Agency PPDC Pesticide Program Dialogue Committee PPO protoporphyrinogen oxidase PRM pesticide resistance management PSEP Pesticide Safety Education Program PTB pyrimidinyl-thio-benzoates QoI Quinone outside Inhibitor RAC Resistance Action Committee RAMP Risk Avoidance and Mitigation Program RFA Request for Application RM resistance management RMP resistance management plan RPS resistant pest management RR resistance ratio SCN soybean cyst nematode SCT sulfonylamino-carbonyl-triazolinones SIMRU Southern Insect Management Research Unit SLA state lead agency SRI Stanford Research Institute SU sulfonylurea TBW tobacco budworm TP triazolopyrimidines UN FAO United Nations Food and Agriculture Organization USDA U.S. Department of Agriculture 172
Appendix B: Glossary
ALS inhibitor. Herbicides designed to inhibit the group of individuals within a population. A decline plant (weed) enzyme, acetolactate synthase (ALS). in any of these heritable traits can result in a re- Bacillus thuringiensis (Bt). A naturally occurring productive disadvantage and is termed a fitness bacterium found worldwide in soil and on the sur- cost. faces of plants. Bt produces proteins toxic to cer- Fungicide. An agent that destroys fungi or inhibits tain insect groups (e.g., caterpillars, beetles, and their growth. blackfly and mosquito larvae). Different strains of Fungicide resistance. The evolved capacity of a Bt have been registered as insecticides but have previously fungicide-susceptible fungal population had limited use. Genes from Bt have been geneti- to survive a fungicide. cally engineered into crop plants (Bt plants) to pro- Genetically engineered crop. See Transgenic tect the plants from certain insect species. crop. Baseline population. A pest population that has Herbicide. An agent used to kill plants or inhibit not been exposed to a particular selective agent, plant growth. such as a pesticide, and thus can be used as repre- Herbicide mixtures. A combination of herbicides sentative of unselected pest populations. with different modes of action used to control a set Biointensive IPM. A range of preventative tactics, of weed species. such as cultural practices and biological controls, Herbicide resistance. The evolved capacity of a pre- used to confine pest populations below economically viously herbicide-susceptible weed population to damaging limits. survive an herbicide application. Biopesticide. A living organism, or a product de- Herbicide rotation. Rotating between herbicide rived from a living organism, that functions as a modes of action from year to year or within a sea- pesticide. Examples are parasites, microorgan- son. This technique is used to delay resistance de- isms, plant metabolites, and plant-incorporated velopment. protectants. Insecticide. An agent that kills, repels, or otherwise Bt crops. Crops that have been genetically engi- controls insects. neered to express proteins from the soil bacterium, Insecticide resistance. The evolved capacity of a Bacillus thuringiensis (Bt) to control insect pests. previously insecticide-susceptible insect population Cross-resistance. A situation in which a single re- to survive an insecticide. sistance mechanism confers resistance to two or Integrated pest management. A strategy that uses more pesticides. A pest with that resistance may combinations of biological, chemical, and cultural be resistant to multiple chemistries without being practices (including crop rotation and host-plant re- exposed to all of them. sistance) for the satisfactory control of pests and Dose-mortality. The mortality of a pest strain at a to keep pests below economically damaging levels. specific dose of the toxin, often expressed as the Mode of action. The biochemical mechanism by LD50, which means the lethal dose required to kill which a pesticide kills a pest. 50% of the population. Multiple resistance. A situation in which more than Environmentalism. Advocacy for the preservation one resistance mechanism is present within the or improvement of the natural environment. same individuals of a pest population. Evolved capacity. Resistance caused by a herita- Organically grown food. Food grown under a set ble change (mutation) in the genetic makeup of the of standards set by the National Organic Program pest that confers the ability to withstand a pesti- governed by the United States Department of Ag- cide. riculture, Agricultural Marketing Service (Final Fitness. A measure of the behavior, developmental Rule, 7 CFR Part 205, Federal Register, Vol. 65, No. time, fecundity, and fertility of an individual or 246, Dec. 21, 2000).
172 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 173
Organophosphate. A chemical class of insecticides Resistance Risk Profile. The likelihood of resis- that operates by blocking the enzyme acetylcho- tance evolving to a particular pesticide based on its linesterase, interrupting the transmission of nerve use pattern, mode of action, the genetics of resis- impulses and leading to insect death. tance (to the extent known), and field studies. Pest. Any insect, mite, fungi, bacteria, virus, weed, Selectivity. The breadth of species affected by the nematode, or mammal that poses a threat to hu- pesticide. man activities such as agriculture. Single-site inhibitor. A pesticide that targets only Pest complex. A combination of diseases, insects, one enzymatic site of action. or weeds targeted by pest control practices. Spatial model. A mathematical simulation model Pesticide resistance. The evolved capacity of a pest that explicitly considers spatial variation. population to withstand exposure to a pesticide. Target site. The biochemical site of action of a pes- The evolution of resistance occurs through a pro- ticide (e.g., the specific enzyme that the pesticide cess of natural selection whereby a population be- affects). comes less sensitive to a pesticide. Resistance may Target-site specificity. The degree to which a pes- develop in insects, weeds, or pathogens. ticide targets only one specific site of action. Pyrethroid. A chemical class of insecticides that af- Tolerance. The ability of a pest to withstand expo- fects sodium channels in both the peripheral and sure to a particular pesticide. This ability need not central nervous system of insects, stimulating re- be heritable, or related to exposure to that pesti- petitive nervous discharges leading to insect paral- cide. ysis and death. Transgenic crop. A crop modified through genetic Quinone outside inhibitor. A chemical class of fun- engineering to contain one or more genes from an gicides that acts at the Quinone “outside” (Qo) bind- unrelated species to provide the crop with a desired ing site of the cytochrome bc1 complex. trait, such as pest resistance. Reduced-risk pesticide. An EPA definition used Transgenic technology. A set of technologies by to designate certain lower-risk pesticides (as com- which a plant, animal, or microorganism may be pared with the registered alternatives) that pass genetically introduced into an unrelated species a reduced-risk screening process (see Pesticide (e.g., Agrobacterium tumefaciens-mediated trans- Registration Notices 97-2 and 98-7). Reduced-risk formation, biolistic bombardment). pesticides also include all biopesticides. Varietal selection. The genetic breeding process for Redundant killing. The use of two pesticides with selecting specific agronomic or genetic traits of in- different modes of action to effectively kill suscep- terest in a plant, animal, or microorganism. tible individuals more than once because each mode of action is lethal by itself. Refuge. An area in which a pesticide is not applied against a pest population and hence susceptible al- leles to the pesticide can remain abundant. In terms of insect resistance management for Bt crops, an area planted to non-Bt varieties or alternative hosts where susceptible pests can survive and pro- duce a local population capable of mating with any possible Bt-resistant insects that developed on the Bt crop. Resistance. The evolved capacity of an organism to survive exposure to a selective agent (e.g., pesti- cide). Resistance management strategy. A strategy that can be employed to delay the onset of resistance. For insect resistance management, this may in- clude the use of a “refuge” area. Resistance ratio. A measure of resistance defined by the ratio of dose-mortality of the tested strain over the dose-mortality of the susceptibility strain. 174
Appendix C: Symposium Agenda CAST Symposium Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides April 10-11, 2003 Indianapolis, Indiana AGENDA
Thursday, April 10, 2003
1:00 P.M. Welcome and Introduction to the Workshop Teresa A. Gruber, Council for Agricultural Science and Technology (CAST) and Barry J. Jacobsen, Montana State University
1:10 P.M. Session I: Scope of North American Pest Resistance Problems in 2003
Each speaker will summarize the scope and magnitude of pest/pesticide resistance problems in North America. A.Overview: Mark E. Whalon, Michigan State University B.Insects: Mark E. Whalon, Michigan State University C.Weeds: Ian M. Heap, Weed Smart LLC D.Pathogens: Wolfram Koeller, Cornell University
2:05 P.M. Session II: Issues in Pest Resistance Management Moderator: Sharlene R. Matten, United States Environmental Protection Agency
For each crop/pest(s) situation, each speaker will address the following: 1. the pest/pesticide resistance issues. 2. what is/was done to manage the resistance problems (or potential problems). 3. the barriers to pest resistance management.
A. Fruits and vegetables: Charles Mellinger, Glades Crop Care B. Cotton: Patricia F. O’Leary, Cotton Incorporated C. Potato: John Keeling, National Potato Council D. Corn/soybean cropping system: Kevin L. Steffey, University of Illinois E. Turf/ornamental: Larry Stowell, PACE Turfgrass Research Institute F. Organic cropping systems: Kevin Brussell, Midwest Organic Farmers Cooperative G. Panel discussion/Q & A
3:45 P.M. BREAK
4:00 P.M. Session III: Lessons Learned I: Balance between Industry, Academia, Users, and Regulators [Case Studies] Moderator: Tony Shelton, Cornell University
For each case study, each speaker will address the following: 1. the particular pest/pesticide resistance problem (scope and extent in the U.S. and worldwide). 2. what is/was done to manage the resistance problem (or potential). 3. the barriers to pest resistance management.
174 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 175
A. Triazine, Acetolactate synthase (ALS) inhibitor, Protoporphyrinogen oxidase (PPO) inhibitor resistance: Les Glasgow, Syngenta B. Glyphosate resistance: David Heering, Monsanto Company C. Cotton pest (insects, weeds, pathogen) resistance in the Midsouth: Ralph Bagwell, Louisiana State University D. Fungicide resistance in fruit crops: Wayne F. Wilcox, Cornell University E. Diamondback resistance in crucifers: Anthony M. Shelton, Cornell University F. Cotton/vegetable crop insect resistance in the Southwest: Timothy J. Dennehy, University of Arizona G. Bt Crop insect resistance management: Graham P. Head, Monsanto Company H.Panel discussion/Q&A
5:30 P.M. DINNER ON YOUR OWN
7:30–9:30 P.M. Session IV: Lessons Learned II: Have Models Helped? Moderator: Wolfram Koeller, Cornell University
For insect, weeds, and pathogens, each speaker will address the following: 1. the predictive role models have played in pest resistance management. 2. how models have been used to identify data gaps/needs. 3. the uncertainty associated with input parameters in various models. 4. the validation of models.
A. Insects: Nicholas P. Storer, Dow AgroSciences B. Insects: Richard Roush, University of California–Davis C. Weeds: Carol Mallory-Smith, Oregon State University D. Pathogens: Hendrik L.Ypema, BASF E. Panel discussion/Q & A
Friday, April 11, 2003
8:00 A.M. Session V: Role of Stakeholders Moderator: Carol Mallory-Smith, Oregon State University
For each stakeholder, each speaker will address the following: 1. the goals of RM implementation. 2. the barriers/challenges to resistance management (RM) implementation. 3. the goals of others in pest resistance management.
Session V, Part I: Consumers, Producers, and Distributors
A. Consumer/public interest communities: Doug Gurian-Sherman, Center for Science in the Public Interest (CSPI) B. Crop consultants: Roger Carter, National Alliance of Independent Crop Consultants (NAICC) C. Grower organizations: Frank L. Carter, National Cotton Council D. Pesticide manufacturers: Caydee Savinelli, Syngenta, Insecticide Resistance Action Committee (IRAC); Gilberto Olaya, Syngenta, Fungicide Resistance Action Committee (FRAC); and Marvin Schultz, Dow AgroSciences, Herbicide Resistance Action Committee (HRAC) E. Pesticide dealers and distributors: Scott Pace, Helena Chemical Company, Chemical Producers and Distributors Association (CPDA)
Session V, Part II: Regulation, Research, Education, and Funding 176 Appendix C: Symposium Agenda
F. Federal pesticide regulation: Sharlene R. Matten, USEPA and Pierre Beauchamp, Canada/ Pest Management Regulatory Agency G. Federal cooperative research: Eldon E. Ortman, U.S. Department of Agriculture (USDA), Cooperative State Research, Extension, and Education Service (CSREES) H.Minor crops (IR–4 Project): Michael P. Braverman, Rutgers, The State University of New Jersey I. Pesticide education and training programs: Monte P. Johnson, USDA/CSREES J. State pesticide regulation: David Scott, Office of the Indiana State Chemist K. Extension: Walter R. Stevenson, University of Wisconsin L. Academic research: Thomas O. Holtzer, Colorado State University
10:15 A.M. BREAK
10:30 A.M. Session VI: Lessons Learned III: How Can We Work to Alleviate Barriers to Comprehensive RM Implementation? How Can We Work Together Better? Moderator: Barry J. Jacobsen, Montana State University
Each speaker will address the following questions: 1. What are the possible tactics/solutions that can/should be used to alleviate barriers to com prehensive resistance management implementation? 2. How should organizations work together to address proactively potential resistance issues?
Session VI, Part I: Consumers, Producers, and Distributors A. Pesticide manufacturers: Gary D. Thompson, Dow AgroSciences, IRAC; Roger P. Kaiser, Bayer, FRAC and Natalie DiNicola, Monsanto Company, HRAC B. Crop consultants: Roger Carter, National Alliance of Independent Crop Consultants C. Growers: John Keeling, National Potato Council D. Public interest consultants: Charles Benbrook, Benbrook Consulting Services
Session VI, Part II: Regulation, Research, Education, and Funding E. Academic research: Thomas O. Holtzer, Colorado State University F. Federal research: Eldon E. Ortman, USDA/CSREES G. State regulatory: David Scott, Office of the Indiana State Chemist H.Plant breeding research: Margaret E. Smith, Cornell University I. Federal pesticide regulation: Sharlene R. Matten, USEPA J. Canadian pesticide regulation: Pierre Beauchamp, Canada/PMRA K. Panel Discussion/Q & A
12:00 P.M. LUNCH ON YOUR OWN
1:00 P.M. Session VII: Pest Resistance Management Goals Moderator: Cindy Lynn Richard, Council for Agricultural Science and Technology
Session VII, Part I: Resistance Management Strategies Each speaker will address the following: 1. the goals of pest resistance management: proactive versus reactive resistance management. 2. the role of resistance monitoring in managing pest resistance. 3. the strategies/tactics that should be used to limit selection pressure (e.g., mode of action rotation, limiting number and frequency of applications, timing of application, high dose/ refuge, crop rotation, biological control etc.). 4. the use of forecasting and diagnostic tools in aiding resistance management?
A. Weeds: Dale L. Shaner, USDA/Agricultural Research Service Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 177
B. Insects: D. D. Hardee, USDA/Agricultural Research Service C. Pathogens: Barry J. Jacobsen, Montana State University D. Agricultural information technology: Dennis D. Calvin, Pennsylvania State University (& ZedX) E. Discussion/Q & A
Session VII, Part II: Resistance Management Education and Communication Each speaker will describe the education and communication efforts used to improve the effec- tiveness of long-term pest resistance management.
A. Michael D. Orzolek: Pennsylvania State University B. Mark E. Whalon: Michigan State University C. Ronald E. Stinner: North Carolina State University D. Thomas Slunecka: National Corn Growers Association E. Discussion/Q & A
2:45 P.M. BREAK
3:00 P.M. Session VIII: Symposium Recommendations for Pest Resistance Management— Where to Now? Moderator: Teresa A. Gruber, Council for Agricultural Science and Technology
4:00 P.M. Symposium Adjourns 178
Appendix D: Symposium Attendees
John E. Ayers Tel: 208-263-5236 Kevin Brussell Penn State University E-mail: [email protected] Rainy Creek Farms 114 Backhout Lab 572 County Road University Park, PA 16802 Rachel Binning 2100 East Tel: 814-865-7776 Pioneer Hi-Bred International Casey, IL 62420 E-mail: [email protected] 7250 NW 62nd Ave. Tel: 217-923-5190 Johnston, IA 50131-0552 E-mail: [email protected] Ralph Bagwell Tel: 515-270-3332 Louisiana State University E-mail: Dennis D. Calvin Cooperative Extension Service [email protected] Department of Entomology 212 Macon Ridge Road The Pennsylvania State Univer- Winnsboro, LA 71295 Karen R. Blundell sity Tel: 318-435-2908 BASF Corporation 509 Agriculture Science and E-mail: [email protected] PO Box 13578 Industry Building Research Triangle Park, NC University Park, PA 16802 Sarah Bates 27709 Tel: 814-863-4640 Cornell University Tel: 919-547-2979 E-mail: [email protected] Dept. of Entomology E-mail: [email protected] 630 W. North St. Frank L. Carter Geneva, NY 14456 Michael P. Braverman Manager, Pest Management/ Tel: 315-787-2343 Biopesticide Coordinator Regulatory E-mail: [email protected] IR-4 Project National Cotton Council of Center for Minor Crop Pest America Pierre Beauchamp Management 1918 No. Parkway Acting Section Head Technology Center of New Box 12285 Health Canada, Pest Manage- Jersey Memphis, TN 38182 ment Regulatory Agency Rutgers, The State University of Tel: 901-274-9030 Efficacy and Sustainability New Jersey E-mail: [email protected] Assessment Division 681 U.S. Highway No. 1, South Sir Charles Tupper Building North Brunswick, NJ 08902- Roger Carter Room E749 3390 President 2720 Riverside Drive (Mail Tel: 732-932-9575, Ext. 610 AMS Incorporated code: 6607E) E-mail: Rt. 1, Box 45 Ottawa, Ontario K1A 0K9 [email protected] 178 Carter Loop CANADA Clayton, LA 71326 Tel: 613-736-3756 Mike Bruer Tel: 318-389-4411 E-mail: Pierre_Beauchamp@hc- National Association of Wheat E-mail: [email protected] sc.gc.ca Growers RR1, Box 71 Charles Benbrook Alberta, MN 56207 Benbrook Consulting Services Tel: 320-324-7577 5085 Upper Pack River Road E-mail: [email protected] Sandpoint, ID 83864
178 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 179
Harold Coble John Dunley Les Glasgow USDA/ARS/OPMP Washington State University- R&D Weed Control Group 320 Scott Hall, Box 7608 TFREC Leader North Carolina State University 1100 N. Western Ave. Syngenta Crop Protection Inc. Raleigh, NC 27695-7608 Wenatchee, WA 98801 Vero Beach Research Center Tel: 919-513-2124 Tel: 509-663-8181 7145 58th Avenue E-mail: [email protected] E-mail: [email protected] Vero Beach, FL 32967 Work: 772-567-5218, ext. 170 Paula Davis Gary L. Eilrich E-mail: Pioneer ISK Biosciences Corporation [email protected] 7100 N.W. 62nd Ave. 7470 Auburn Rd., Suite A PO Box 1150 Concord, OH 44077 Barb Gradin Johnston, IA 50131-1150 Tel: 440-357-4656 Pest Management Regulatory Tel: 515-334-6994 E-mail: [email protected] Agency E-mail: 2720 Riverside Dr. [email protected] Chuck Foresman Ottawa, Ontario K1A 0K9 Syngenta Crop Protection Canada Timothy J. Dennehy 410 Swing Rd. Tel: 613-736-3805 Integrated Pest Management Greensboro, NC 27419 E-mail: Barbara_Gradin@hc- Extension Specialist/Research Tel: 336-632-7176 sc.gc.ca Scientist E-mail: Department of Entomology [email protected] Elizabeth Grafton-Cardwell University of Arizona University of California–River- Tuscon, AZ 85721 Raymond Forney side Tel: 520-621-7124 DuPont Company Kearny Agriculture Center E-mail: PO Box 80705 9240 S. Riverbend Ave. [email protected] CRP/Laurel Run 1N13 Parlier, CA 93648 Wilmington, DE 19880 E-mail: [email protected] Natalie DiNicola Tel: 302-999-5407 Monsanto Company E-mail: Mary Grodner Regulatory Affairs [email protected] Louisiana State University 800 North Linbergh Blvd. Dept. of Entomology St. Louis, MO 63167 Lorianne Fought 404 Life Science Bldg. Tel: 314-694-3195 Bayer CropScience Baton Rouge, LA 70873 E-mail: PO Box 12014 Tel: 225-578-2180 [email protected] Research Triangle Park, NC E-mail: [email protected] 27709 Jerry Doll Tel: 919-549-2952 Teresa A. Gruber University of Wisconsin E-mail: Executive Vice President Department of Agronomy [email protected] CAST 1975 Linden Dr. 505 Capitol Court, NE, Suite Madison, WI 53706 John Glaser 200 Tel: 608-263-7437 U.S. Environmental Protection Washington, D.C. 20002-4937 E-mail: [email protected] Agency Tel: 202-675-8333, ext. 11 26 W. Martin Luther King Drive E-mail: tgruber@cast- John Dunbar (MS498) science.org University of California Cincinnati, OH 45268 Dept. of Animal Science Tel: 513-569-7568 2211 Meyer Hall E-mail: [email protected] Davis, CA 95616 Tel: 916-752-0525 180 Appendix D: Symposium Attendees
Doug Gurian-Sherman David C. Heering Madan M. Joshi Co-Director, Biotechnology Monsanto Company DuPont Crop Protection Project Roundup Technical Lead Chestnut Run Plaza Center for Science in the Public 800 North Linbergh Blvd. P.O. Box 80705 Interest St. Louis, MO 63167 Wilmington, DE 19880-0705 1875 Connecticut Ave., NW, Tel: 314-694-6698 Tel: 302-999-5888 #300 Email: E-mail: Washington, DC 20009 [email protected] [email protected] Tel: 202-332-9110 Ext. 377 E-mail: dgurian- Richard Hellmich Roger P. Kaiser [email protected] USDA/ARS Early Development Manager, Corn Insects and Crop Genetics Fungicides & SAT D. D. Hardee Research Unit and Department Bayer CropScience, USA Research Leader of Entomology P.O. Box 12014 USDA/ARS Genetics Laboratory, c/o Insecta- 2 T.W. Alexander Dr. Southern Insect Management ry RTP, NC 27709 Research Unit Iowa State University Tel: 919-549-2188 P.O. Box 346 Ames, IA 50011 E-mail: Stoneville, MS 38776 Tel: 515-294-4509 [email protected] Tel: 662-686-5231 E-mail: [email protected] E-mail: [email protected] John Keeling Thomas O. Holtzer Executive Vice President and Craig K. Harris Department Head CEO Michigan State University Department of Bioagricultural National Potato Council 429b Berkey Hall Sciences and Pest Management 1300 L St., NW Suite 910 East Lansing, MI 48824-1111 Colorado State University Washington, D.C. 20005 Tel: 517-355-5048 Fort Collins, CO 80523-1177 Tel: 202-682-9456 E-mail: Tel: 970-491-5261 E-mail: [email protected] E-mail: [email protected] [email protected] Graham P. Head Gregory Kemmitt Research Entomologist Barry J. Jacobsen Dow Agro Sciences Monsanto Department of Plant Science 9330 Zionsville Rd. 700 Chesterfield Parkway North and Plant Pathology Indianapolis, IN 46268 Mail Zone: GG3E Montana State University Tel: 317-337-4575 St. Louis, MO 63198 P.O. Box 1733150 E-mail: [email protected] Tel: 636-737-7554 Bozeman, MT 59717-3150 E-mail: Tel: 406-994-5161 John Kiser [email protected] E-mail: [email protected] Verdia Inc. 3208 Curvew St. Ian M. Heap Monte P. Johnson Davis, CA 95616 Organizer of the International National Program Leader Tel: 530-750-3776 Survey of Herbicide Resistant USDA/CSREES E-mail: [email protected] Weeds Stop 2220 Weed Smart LLC 1400 Independence Ave., SW Wolfram Koeller P.O. Box 1365 Washington DC 20250-2220 Department of Plant Pathology Corvallis, OR 97339 Tel: 202-401-1108 Cornell University Tel: 541-929-6639 E-mail: Box 15 Roberts Hall E-mail: [email protected] Geneva, NY 14456-0462 [email protected] Tel: 315-787-2375 E-mail: [email protected] Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 181
Fritz Koppatschek Carol Mallory-Smith Madeline Mellinger AgriBusiness Group Oregon State University Glades Crop Care, Inc. 3905 Vincennes Road, Ste. 402 Department of Crop & Soil 949 Turner Quay Indianapolis, IN 46268 Sciences Jupiter, FL 33458 Tel: 1-800-285-8859 Crop Science Bldg. 107 Tel: 561-746-3740 Corvallis, OR 97331-3002 E-mail: [email protected] Larry L. Larson (Deceased) Tel: 541-737-5883 Dow Agro Sciences E-mail: carol.mallory- William J. Moar 9330 Zionsville Rd. [email protected] Auburn University Indianapolis, IN 46268 Department of Entomology Tel: 317-337-3099 Sharlene R. Matten 301 Funchess Hall E-mail: [email protected] U.S. EPA Auburn, AL 36849 Office of Pesticide Programs Tel: 334-844-2560 Steve Lefko Biopesticides and Pollution E-mail: [email protected] Pioneer Hi-Bred Prevention Division (7511C) 7250 NW 62nd Ave. 1200 Pennsylvania Ave., NW Walt Mullins P.O. Box 552 Washington, D.C. 20460 Monsanto Company Johnson, IA 50131 Tel: 703-605-0514 3175 Lenox Park Blvd., Suite Tel: 515-253-2137 E-mail: 110 E-mail: [email protected] [email protected] Memphis, TN 38115 Tel: 901-375-5643 Frank Lichtner Ronald Mau E-mail: DuPont Crop Protection University of Hawaii [email protected] 131 Foxfire Drive 3050 Maile Way Newark, DE 19711 Honolulu, HI 96822 Fred Musser Tel: 302-999-5891 Tel: 808-956-7063 Cornell University, NYSAES E-mail: E-mail: [email protected] Dept. of Entomology [email protected] 630 W. North St. Margaret Tuttle McGrath Geneva, NY 14456 Julio Lopez Department of Plant Pathology Tel: 315-787-2453 Zamorano Cornell University E-mail: [email protected] Costado Noreste Catedral 3C. Al Long Island Horticultural Este. Esteli Research & Extension Center Robert L. Nichols Apartado Postal 0014 3059 Sound Ave. Cotton Incorporated Tel: 00-505-713-2226 Riverhead, NY 11901-1098 6399 Weston Parkway E-mail: [email protected] Tel: 631-727-3595 Cary, NC 27513 E-mail: [email protected] Tel: 919-678-2371 Charles Luper E-mail: [email protected] Oklahoma State University Lance J. Meinke 127 NRC University of Nebraska Scott Nissen Stillwater, OK 74078 Dept. of Entomology Colorado State University Tel: 405-744-5808 Lincoln, NE 68583-0816 115 Weed Research Lab E-mail: [email protected] Tel: 402-472-8707 Ft. Collins, CO 80523 E-mail: Tel: 970-491-3489 Randall G. Luttrell [email protected] E-mail: Department of Entomology [email protected] University of Arkansas Charles Mellinger Agri 319 Glades Crop Care Robert Nowierski Fayetteville, AR 72701 949 Turner Quay USDA/CSREES Tel: 479-575-4433 Jupiter, FL 33458 1400 Independence Ave. SW E-mail: [email protected] Tel: 561-746-3740 Washington, DC 20250 E-mail: [email protected] Tel: 202-401-4900 E-mail: [email protected] 182 Appendix D: Symposium Attendees
Patricia F. O’Leary Scott Pace Richard Roush Director Manager of Registration and Director Agricultural Research Marketing Statewide IPM Program Cotton Incorporated Helena Chemical Company University of California–Davis 6399 Weston Parkway 7664 Moore Road 1 Shields Ave. Cary, NC 27513 Memphis, TN 38119 Davis, CA 95616 Tel: 919-678-2366 Tel: 901-752-4410 Tel: 530-752-8350 E-mail: [email protected] E-mail: E-mail: [email protected] [email protected] Gilberto Olaya Alan P. Rudy Fungicides Kevin Perry Sociology-Michigan State Syngenta Crop Protection, Inc. Valent USA Corporation 316 Berkey Hall Vero Beach Research Center 1898 W. U.S. 40th East Lansing, MI 48824 7145 58th Avenue Greenfield, IN 46140 Tel: 517-353-0745 Vero Beach, FL 32967 Tel: 317-467-4942 E-mail: [email protected] Work: 772-567-5218, ext. 149 E-mail: [email protected] E-mail: Alfredo Rueda [email protected] Mark Powell Zamorano USDA Escuela Agricola Panamericana Eldon E. Ortman 1400 Independence Ave., SW P.O. Box 93 Plant and Animal Systems Rm. 5248 South Ag. Bldg. El Zamorano, Honduras USDA/CSREES Washington D.C. 20250 Tel: 00-504-776-6140 Waterfront Centre, RM. 3471 Tel: 202-720-8022 E-mail: [email protected] Stop 2220 E-mail: [email protected] 800 9th Street, SW Charlotte Sanson Washington DC 20250-2220 Cindy Lynn Richard BASF Corporation Tel: 202-401-5804 Program Coordinator P.O. Box 13528 E-mail: [email protected] CAST Research Triangle Park, NC 505 Capitol Court, NE, Suite 200 27709 Michael D. Orzolek Washington, D.C. 20002-4937 Tel: 919-547-2983 Department of Horticulture Tel: 202-675-8333, ext. 12 E-mail: [email protected] The Pennsylvania State Univer- E-mail: crichard@cast- sity science.org David Saunders 203 Tyson Building DuPont University Park, PA 16802 David Rogers 2401 230th St. Tel: 814-863-2251 Bayer Crop Science Dallas Centre, IA 80063 E-mail: [email protected] P.O. Box 12014 Tel: 515-334-4485 Research Triangle Park, NC E-mail: Elizabeth Owens 27709 [email protected] Pioneer Hi-Bred Int’l Inc. Tel: 919-549-2738 7250 NW 62nd E-mail: Caydee Savinelli Johnston, IA 50131 [email protected] Technical Brand Manager, In- Tel: 515-270-4083 secticides E-mail: George L. Rolofson Syngenta Crop Protection, Inc. [email protected] Crop Life America Post Office Box 18300 1156 15th St. NW Suite #400 Greensboro, NC 27419-8300 Washington, D.C. 20005 Tel: 336-632-2283 Tel: 202-872-3896 E-mail: E-mail: [email protected] [email protected] Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 183
Marvin Schultz Burleson Smith Uwe Stolz Dow AgroSciences USDA U.S. EPA 9330 Zionsville Rd. 8705 Prudence Drive 26 Martin Luther King Dr. Indianapolis, IN 46268 Annandale, VA 22003 Cincinnati, OH 45268 Tel: 317-337-3981 Tel: 202-720-2889 Tel: 574-569-7290 E-mail: [email protected] E-mail: E-mail: [email protected] [email protected] David Scott Nicholas P. Storer Office of the Indiana State Margaret E. Smith Research Biologist Chemist Department of Plant Breeding Dow AgroSciences LLC Purdue University Cornell University 9330 Zionsville Rd. 175 S. University St. 252 Emerson Hall Indianapolis, IN 46268 West Lafayette, IN 47907-2063 Ithaca, NY 14853 Tel: 317-337-5138 Tel: 765-494-1585 Tel: 607-255-1654 E-mail: [email protected] E-mail: [email protected] E-mail: [email protected] Larry Stowell Dale L. Shaner Charles Staetz PACE Turf Grass Research USDA/ARS FMC Corp. Institute Water Management Research P.O. Box 8 1267 Diamond St. AERC-CSU Princeton, NJ 08543 San Diego, CA 92109-2645 Ft. Collins, CO 80523-1325 Tel: 609-951-3611 Tel: 858-272-9897 Tel: 970-491-8263 E-mail: [email protected] E-mail: [email protected] E-mail: [email protected] Kevin L. Steffey Kenji Takama Extension Entomologist K-I Chemical USA Anthony M. Shelton University of Illinois at Urbana- 11 Martine Ave, 9th Floor, Suite Department of Entomology Champaign 970 Cornell University Department of Crop Sciences White Plains, NY 10606 416 Barton Lab S-322 Turner Hall Tel: 914-682-8934 630 W. North Street 1102 S. Goodwin E-mail: [email protected] Geneva, NY 14456-0462 Urbana, IL 61801 Tel: 315-787-2352 Tel: 217-333-6652 Tina Gray Teague E-mail: [email protected] E-mail: [email protected] University of AR-ASU-AES P.O. Box 2340 Blair Siegfried Walter R. Stevenson State University, AR 32467 University of Nebraska Department of Plant Pathology Tel: 840-972-2043 202 Plant Industry Building University of Wisconsin-Madi- E-mail: [email protected] Lincoln, NE 41687 son Tel: 402-472-8714 1630 Linden Drive Gary D. Thompson E-mail: [email protected] Madison, WI 53706-1598 Insect Management Global Tel: 608-262-6291 Dow AgroSciences LLC Thomas Slunecka E-mail: [email protected] 9330 Zionsville Rd. Director, Development Indianapolis, IN 46268 National Corn Growers Associa- Ronald E. Stinner Tel: 317-337-4579 tion Director of Center for IPM E-mail: [email protected] 632 Chesterfield, MO 63005 1017 Main Campus Drive, Tel: 636-733-9004, ext. 114 Suite 1100 E-mail: [email protected] Raleigh, NC 27606 Tel: 919-515-1648 E-mail: [email protected] and [email protected] 184 Appendix D: Symposium Attendees
Rogelio Trabanino Wayne F. Wilcox Zamorano Department of Plant Pathology Escuela Agricola Panamericana Cornell University P.O. Box 93 104 Barton Laboratory El Zamorano, Honduras Geneva, NY 14456 Tel: 00-504-776-6140 Tel: 315-787-2335 E-mail: E-mail: [email protected] [email protected] Yoshihiro Yamaji Barbara VanTil Kumiai Chemical U.S. EPA 11 Martine Ave. 9th Floor, Suite 77 West Jackson Blvd. 970 Chicago, IL 60604 White Plains, NY 10606 Tel: 312-886-3164 Tel: 914-682-8934 Ext: 105 E-mail: [email protected] E-mail: y-yamaji@kumiai- chem.co.jp Richard D. Voth Monsanto Len Yourman 700 Chesterfield Pkwy West EPA/OPP/BEAD BB1E 1200 Pennsylvania Ave., NW Chesterfield, MO 63017 7503C Tel: 636-737-6194 Washington, D.C. 20460 Tel: 703-308-8151 Rick Weinzierl E-mail: University of Illinois [email protected] 1102 S. Goodwin Ave. Urbana, IL 61801 Hendrik L. Ypema Tel: 217-333-6651 Biology Project Leader–Fungi- E-mail: [email protected] cides BASF Corporation Jerry Wells 26 Davis Drive Syngenta Crop Protection Research Triangle Park, NC P.O. Box 18300 27709 Greensboro, NC 27419-8300 Tel: 919-547-2283 Tel: 336-632-6324 E-mail: [email protected] E-mail: [email protected] Jianzhou (Joe) Zhao Cornell University Mark E. Whalon Dept. of Entomology, NYSAES Pesticide Research Center 630 W. North St. Michigan State University Geneva, NY 14456 B11 Pesticide Research Center Tel: 315-787-2953 East Lansing, MI 48824 E-mail: [email protected] Tel: 517-353-9425 E-mail: [email protected] Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 185
Index
A Bacillus thuringiensis applications of, 22, 23, 27, 70 ACCase. See Acetyl-CoA carboxylase corn, 34, 66–68, 69, 130, 153–156, 162–163, 164–165 Acephate, 25 cotton, 27, 66, 67–68, 69, 92, 93, 162–163 Acetamiprid, 20 crops, 1, 66–68, 74–75, 87, 92, 110, 139, 141, 147–149 Acetochlor, 54 with diamondback moth, 62–64, 73 Acetohydroxyacid synthase enzyme, 46 insecticidal endotoxins, 166 Acetolactate synthase insecticidal proteins, 4 herbicide, 26, 54 microbial, 86 inhibitor, 12, 13–15, 26, 36, 44, 45–47, 48, 51, 53, 112 and Monarch butterflies, 85 resistance, 1, 5, 15, 21–22, 36, 53, 54, 78 plant-incorporated protectants, 104 Acetyl-CoA carboxylase regulation of, 108 inhibitor, 12–15, 26, 53 resistance management in, 1, 2, 66–68 Acifluorfen, 47 technology, 164–165 Agri Food Canada, 105 in turf management, 41 Agricultural Biotechnology Stewardship Technical Committee, 164 Bacillus thuringiensis ssp. aizawai, 62 Alachlor, 54, 159 Bacillus thuringiensis ssp. kurstaki, 62, 153 Aldicarb, 28 Bacteria, 4, 21, 85, 150 Alopecurus myosuroides Huds., 12 Bactericides, 151 ALS. See Acetolactate synthase Banding, 158 Amaranthus palmeri, 26 Baseline population, 56 Amaranthus rudis, 44, 46 BASF Corporation, vi, 129 Amaranthus spp., 13 Basidiomycetes, 98 American Chemical Society, 1, 166 Bayer Crop Science, vi American Seed Trade Association, 165 Beet armyworms, 22 Anthonomus grandis grandis, 147 Bemisia argentifolii, 26 Anthracnose, 35 Benzimidazoles, 17, 18, 56, 81, 150 Antiresistance strategies, 18–19, 143–144 Berries, 17 Aphids Biointensive IPM, 10, 23, 86, 87, 129–131 in cotton, 25, 27 Biopesticides, 7, 86, 87, 102, 105, 109–112, 130, 167 in potatoes, 30–31 Biotechnology Risk Assessment Research Program, 118, 136, 168 resistance in, 20 Bioterrorism, 8 in soybeans, 34 Birdsfoot trefoil, 14 Aphis gossypii, 25 Black cutworm, 33 Apples, 17–18, 56, 58, 81 Boll rots, 92 Apple scab, 17–18, 56, 58, 81 Boll weevil, 28, 92, 147 Armyworm, 22, 33 Boll Weevil Eradication Program, 28 Aromatic hydrocarbons, 17–18 Bollworm, 25–27, 28, 68, 75, 147, 149 Arthropods, 7, 8, 9–10, 160–161 Botrytis spp., 80 Ascomycetes, 99 Broadleaf weeds, 46, 48, 158 Atrazine Broccoli, 61, 63, 64 effect of on frogs, 85 Brown stinkbug, 89 introduction of, 44 Bryobia spp., 167 resistance, 44, 157 Bt. See Bacillus thuringiensis use of in corn, 54, 159 use of by farmers, 45, 47 C Avermectin, 20, 23 Azoxystrobin, 35–36, 97, 109, 131, 132 Cabbage, 61, 62 Canada thistle, 157 B Canadian Pest Management Regulatory Agency, 142 Captan, 17, 58 B2-carcinogen classification, 17 Carbamate, 20–21, 23, 25, 35, 61–63, 102 Bacillus subtilis, 130 Carbaryl, 34
185 186 Index
CAST. See Council for Agricultural Science and Technology Cross-resistance, 15, 42, 44, 46–48, 63, 70, 79, 97–98, 114, 123, 148, Center for Integrated Pest Management, vi, 160, 161, 162 150 Center for Integrated Plant Systems, 160, 161 Crucifers Center for Science in the Public Interest, 85 diamondback moth resistance in, 61–64 Chloracetanilides, 45, 47 insecticide resistance in, 1–2, 5 Chlorinated hydrocarbons, 25, 34 Cultivation, 15, 45, 49, 125, 158 Chlorophyll biosynthesis, 48 deep, 38 Chlorothalonil, 17, 21, 39, 58 mechanical, 36 Chlorsulfuron, 45 Cultural practices, 2, 39, 54, 100–101, 109, 111, 166 Citrus rot, 18 Cypermethrin, 25, 28 Citrus rust mites, 20, 23 Cytochrome P450 monooxygenase activity, 12 Clothianidin, 34 Clover, 157 D Cocklebur, 26, 36 Colorado potato beetle, 9, 20, 30, 31 Daucus carota, 44 Common cocklebur, 36 DDT, 61, 85 Common groundsel, 44 Demethylation inhibitors, 17, 56–59, 81, 150 Common lambsquarters, 36, 53, 157 Diadegma insulare, 61 Common ragweed, 36 Diamondback moth, 20, 61–64, 73, 167 Compliance assurance programs, 104, 164–165 Dicamba, 45, 47, 54 Congressional Research Service, xvii Dicofol, 120 Conservation Security Program, 167, 169 Difenconazole, 58 Consumerism, 6 Dinitroaniline, 12, 26 Conyza canadensis, 14, 26, 36, 51, 144 Diphenyl ethers, 47 Cooperative State Research, Education, and Extension Service. See Diquat, 52 U.S. Department of Agriculture, Cooperative State Research, DNA markers, 168 Education, and Extension Service Dodine, 18, 57, 58 Coppers, 21 Dose-mortality, 10 Copper fungicides, 17 Dow AgroSciences, vi, 129, 149 Corn Downy mildew, 80 Bt. See Bacillus thuringiensis, corn Dupont Agricultural Products, vi effectiveness of triazines in, 44, 45 field, 66, 158 E genetically modified, 86, 147, 153 insecticidal proteins in, 66–68 EBDC. See Ethylenebisdithiocarbamantes pop, 157 Eleusine indica, 14, 36, 51 resistance management in, 1, 4, 5, 17, 33, 35, 44–45, 47, 86, Emamectin benzoate, 63 157–159 Environmentalism, 6–8 retail values in 1994 of, 38 EPA. See U. S. Environmental Protection Agency /soybean cropping system, 5, 14, 33–37, 45, 54 EPSPS. See 5-enolpyruvylshikimate-3-phosphate synthase sweet, 64, 157–159 Ethylenebisdithiocarbamates, 17, 21, 105 Corn borer, 33, 34, 43, 67 European corn borer, 33, 34, 43, 67, 153–154 Corn earworm, 33 European Union, 7, 19, 36 Corn rootworm, 4, 7, 33, 34, 35, 107 Evolved capacity, 12 Corn rust, 35 Experimental Use Permit, 7, 117 Cotton Extensible Markup Language, 163 aphids, 25 Extension bollworm, 25, 27, 28 efforts of, 398, 45, 49, 129, 148, 150–151 Bt. See Bacillus thuringiensis, cotton programs, 39, 43, 103, 105, 114, 121, 123, 133, 134–136, 156 pyrethroid resistance in, 28, 96 recommendations for, 1, 4–5, 90, 93, 97–99, 101, 116–117, 124, resistance management in, 1 , 25–28, 92–94, 95, 112, 144, 126, 129, 131, 157, 163, 167–169 147–149 retail values in 1994 of, 25, 39 sticky, 26 F transgenic, 27, 147, 149, 162–163, 164 Cotton Incorporated, vi, 27, 112 Fall armyworms, 33 Coumaphos, 111 Farm Bill, 3, 169 Council for Agricultural Science and Technology, vi, vii, xvii, 1, Farm Bill Environmental Quality Incentives Program, 167 4, 12, 32, 120, 166 Federal Insecticide, Fungicide, and Rodenticide Act, 102–104, 115 CropLife, vi, 100, 120 Fenarimol, 57, 58 Crop grouping, 109, 111–112 Fenvalerate, 63 Crop rotation, 2, 7, 15, 38, 43, 45, 47, 49, 54, 125, 151, 157, 159, Ferbam, 58 167 Fitness, 10, 44–45, 46, 48, 51, 70, 73, 77–78, 80, 81, 82, 150 Crops at Risk, 135, 168 5-enolpyruvylshikimate-3-phosphate synthase, 12, 51, 52 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 187
Flusilazole, 58 Honeybees, 111 Fluvalinate, 111 Honeydew, 26 Foliar fungicides, 17–18, 35, 97 Horsenettle, 157 Foliar herbicides, 47, 48 Horseweed, 26, 36, 144 Foliar insecticides, 34, 67, 148 Fomesafen, 47 I Food, Agriculture, and Trade Act, 10 Food Quality Protection Act. See U.S. Food Quality Protection Act Imidacloprid, 20, 23, 34, 42, 131, 132 Fungal leaf blight, 35 Imidazolinones, 45, 51, 78, 143 Fungi, 4, 30, 35–36, 80–81, 86, 97, 98, 138 Indoxacarb, 63 Fungicide resistance. See under Fungicides Industry Advisory Board, 162 Fungicide Resistance Action Committee, vi, 42, 93, 98, 122, 150, Insect growth regulators, 20, 27 168 Insect resistance management, 1, 5, 70–73 Fungicides, 2, 5, 7, 8, 17, 27, 33, 39–42, 74, 86, 97, 98–99, 101, 112, Insect Resistance Management Learning Center, 165 116, 143, 150–151, 166 Insecticidal proteins, 4, 7, 27, 66–67, 85, 153 antiresistance strategies with use of, 21, 121 Insecticide resistance. See under Insecticides resistance to, 1–2, 5, 6, 7, 8, 18–19, 35–37, 56–59, 80–82, 151 Insecticide Resistance Action Committee, vi, 25, 28, 42, 92–93, types of, 17, 21, 33, 39, 41, 104, 110, 122, 131, 168 120–121, 160–161, 162 Insecticides, 2, 6, 9, 20–23, 69–71, 112, 143, 166–168 G resistance, 2, 25, 66, 74, 112, 120, 167 safety of, 87 Galinsoga, 157 types/classes of, 2, 7, 9, 20, 21, 25, 27, 33, 34, 61, 74, 86, 101– Gene migration, 78 102, 121, 131, 166 Genetically engineered/modified animals/crops/foods, organisms, use of in Bt crops, 66–68, 86, 147–148 plants, 7, 8, 108, 118, 127, 133, 136, 162 use of with corn, 34–37 Giant foxtail, 36 use of with cotton, 28, 92–94, 147 Giant ragweed, 36, 37, 53 use of with diamondback moth, 61–64 Glades Crop Care, 22, 132 use of with peppers, 22 Glassy winged sharpshooters, 111 Integrated crop management, 90 Global Herbicide Resistance Action Committee, vi Integrated pest management, 9, 17, 27, 40, 59, 87, 89, 105, 111, Global Positioning System, 155 121, 128, 134, 139, 162 Glutamine synthetase, 52 in Bt crops, 34 Glyphosate, 1, 5, 14, 26, 36–37, 47, 48, 51–54, 78, 92, 109, 112, 144 and consumers, 84–88 Golf course turf, 38–42 in potato industry, 30 Goosegrass, 36, 51 role of resistance management in, 4, 67, 84, 103, 107, 115, 122, Gossypium hirsutum, 25, 147 141, 166 Graminicides, 26 in sweet corn, 159 Grapes, 17, 56, 58 in vegetable crops, 157–159 Grapevine powdery mildew, 57 Integrated weed management, 124, 145, 157 Gray leaf spot, 35 Integrated Weed Management Extension program, 157 International Survey of Herbicide-Resistant Weeds, 13–14, 124 H Interregional Research Project No. 4. See U.S. Department of Agriculture, Interregional Research Project Number 4 Hairy vetch, 157 IPM Risk Avoidance and Mitigation Program, 129 Halofenozide, 42 IR–4. See U.S. Department of Agriculture, Interregional Research Hawaiian watercress, 167 Project Number 4 Helicoverpa armigera, 68 Isoleucine, 46 Helicoverpa zea, 25, 147 Italian ryegrass, 36, 51 Heliothis armigera, 27 Heliothis virescens, 25, 69, 147 J Heme biosynthesis, 48 Herbicide resistance. See under Herbicides Jimsonweed, 157 Herbicide Resistance Action Committee (HRAC), 15, 26, 93, Johnsongrass, 26 100–101, 124–125, 162 Herbicides, 1, 2, 7, 21–22, 26, 33, 36, 44–49, 51–54, 86, 114, 116, K 121, 157–159, 166, 167–168 antiresistance strategies with use of, 26–27, 30, 36–37, 51–54, Kaolin, 111 101, 112 Kelthane, 120 resistance to, 5, 6, 74, 77–79, 100–101, 124–125, 127, 143–145 Kochia, 36, 46 Hessian fly, 75 Kochia scoparia, 44, 46 Heterogeneous varieties, 139 Heterozygotes, 73–75 High-Resolution European Corn Borer Management Model, 154–155 188 Index
L Natural Resources Conservation Service. See U.S. Department of Agriculture, Natural Resources Conservation Service. Lactuca serriola, 46 Nematicides, 28, 150–151 Ladybugs, 86 Nematodes, 4, 21, 28, 33, 34–35, 92, 135, 150–151 Late blight, 30, 122 Neonicotinoids, 9 Leaf dip assay, 61 Nicosulfuron, 54 Leafminer, 20 Nicotinoids, 20–21, 23, 24, 131 Lentils, 43 Nightshade, 22 Lepidoptera, 33, 66–68, 147, 149, 153 Non-Bt Leptinotarsa decemlineata, 9 corn, 33–34, 153–154, 164 Leucine, 46 cotton, 147 Lolium multiflorum, 14, 36, 51 crops, 70 Lolium rigidum, 12, 14, 36, 51 refuges, 87, 147–148, 154, 164 Lotus corniculatus, 14 Nontransgenic crops, 64, 75 Lygus hesperus, 25 North America QoI subgroup of the Fungicide Resistance Action Lygus lineolaris, 25–26 Committee, 98 Lygus spp., 25 North American Free Trade Agreement, 102–103 North American Fungicide Resistance Action Committee, 122 M North Central Weed Science Society, 47
Malathion, 28 O Mancozeb, 39, 57, 58, 104 Maneb, 104 Office of Pest Management Policy, 163 Marestail, 36, 51 Office of Pesticide Program Dialogue Committee, 104 Mechanism of action, 48, 144–145 Oilseed rape, 47 Methamidophos, 20, 61 Oklahoma State University, “Cotton Aphid Resistance Methomyl, 21, 22, 61–63 Management Guidelines,” 27 Methyl bromide, 20, 21, 132, 135 Old World bollworm, 68 Methyl Bromide Transitions Program, 135, 168 Oomycetes, 98 Methyl parathion, 34, 89 Organic Metoachlor, 54, 159 agriculture, 114 Metriam, 104 crops, 130 Michigan State University database, 9–11 farming/systems, 130, 135, 166–167 Minor Crop Pest Management, 135 Organic Transitions Program, 135, 168 Mites, 4, 20, 23, 31, 74, 111, 120, 167 Organoarsenical herbicides, 26 Mode of action, 13, 20, 26, 27, 40, 47, 49, 80, 95, 97–98, 103, 105, Organophosphates, 7, 8, 20, 25–26, 35, 61, 63, 86, 102, 111, 130 110, 111, 114, 117, 122–123, 124, 129, 131, 142, 144, 150, Ornamental crops, 1, 5, 114, 157, 161 167–168 Ostrinia nubilalis, 67 glyphosate, 51–54 Oxadiazoles, 47 nonspecific, 17 Oxamyl, 21, 255 novel, 63 Oxazolidinediones, 47 and QoI fungicides, 81 rotation of herbicide, 22, 30, 48, 102, 106, 130 P specific, 18, 117, 125 Mode of Action Classification System, 103, 162, 168 PACE Turfgrass Research Institute, 39, 41 Monarch butterflies, 85 Palmer amaranth, 26 Monocropping, 43 Paraquat, 22, 45, 52 Monsanto, 51, 54, 148, 149, 162–163 Pear psylla, 111 Mosaics, 74–75 Pectinophora gossypiella, 147 Multiple resistance, 12, 18, 47, 48, 78, 111, 114, 138–139, 140 Peking resistance, 35 Myclobutanil, 55, 58 Pendimethalin, 54 Penicillium, 18 N Peppers, 20–22 Performance Planning and Reporting System, 114 N-phenylphthalimides, 47 Permethrin, 61–63 Nabam, 104 Pest complex, 21, 38, 90, 148 NAFTA Technical Working Group on Pesticides, 102 Pest Management Alternatives Program, 134, 161 National Alliance of Independent Crop Consultants, 126 Pest Management Regulatory Agency of Canada, 102–106, 142 National Corn Growers Association, vi, 164–165 Pesticide Environmental Stewardship Program. See U.S. National Cotton Council, 92 Department of Agriculture, Pesticide Environmental Steward- National Potato Council, 30, 127 ship Program National Research Council, 1, 7, 10, 59, 166 Pesticide resistance. See under Pesticides National Research Initiative, 59, 118, 135, 168 Pesticide Safety Education Program, 114, 135–136, 168 National Science Foundation, vi, 162 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 189
Pesticides, 7, 9–11, 38, 84–88, 92, 111, 134, 150, 151, 154, 163 Request for Application, 134, 168 effect of on arthropods, 9–11 Resistance Action Committees, 1, 4, 120, 134 classes/types of, 2, 31, 33, 59, 74, 103–106, 107, 119, 129, 130, Resistance management 160, 166 education, 3, 123, 142, 157–159, 162–163, 168 in cotton, 25, 27 evolution of, 46–47 distributors/manufacturers of, 1, 5, 97–99, 105, 114, 117–118 monitoring, 2, 3, 6–8, 10, 17, 19, 21, 23, 27, 28, 37, 48, 56, 66, 67, economic impact of, 9 89, 98, 104, 107, 125, 128, 131, 143–144, 147–149, 151, 157, Education Safety, 114 167, 168 in fruits and vegetables, 20–23 ratio, 10, 21, 23, 61, 129, 131 resistance management of, 1, 2, 3, 4–5, 6, 8, 17, 28, 30, 38–42, research program, 89, 119, 120–121, 135, 168 77, 84–88, 102–106, 109, 115, 116–117, 130–131, 135, 141, 160– risk profile in, 117, 131–132 161, 166–169 strategy, 2, 9, 14–15, 18, 22, 36, 39, 53, 63–64, 66, 67, 69, 74, 79, and transgenic crops, 73 97, 98, 100, 103, 107, 109, 122, 124, 144, 145, 151, 166 Phenylamides, 17, 81, 150 Resistant Arthropods Database, 160–161 Phenylpyrazoles, 47 Resistant Pest Management Newsletter, 160–161 Phosphinothricin, 52 Rhizoctonia solani, 27 Phosphoenolpyruvate, 51 Rice, 46, 47 Phytophthora sojae, 35 Rigid ryegrass, 36, 44 Pink bollworm, 75, 147, 149 Risk assessments, 153 Pioneer Hi-Bred International, Inc., vi Risk Assessment and Mitigation Program, 153 Pistachios, 97 Risk Avoidance and Mitigation Program, 129, 131, 135, 153 Plasticulture, 158 Rodents, 4 Plodia interpunctella, 71 Root rot, 35, 92 Plutella xylostella, 61, 71 Rootworm-resistant corn, 164 Pod/stem blight, 35 Rotylenchulus reniformis, 28 Polygenic resistance, 74, 78, 138–139, 140 Pome fruits, 130 S Popcorn, 157 Portulaca oleracea, 44–45 Scab, 17–18, 56, 58, 81 Potato, 1, 3, 5, 9, 66, 122, 127, 131, 132 Seedbank longevity, 79 beetle, 9, 20, 30, 31 Selection pressure, 79, 82, 84, 95, 98, 102, 103, 110–112, 130–131, blight, 22 138, 139, 151, 166, 167 fungicide use on, 17, 30–31 Selectivity, 9–10, 45–46, 112 leafhoppers, 32 Senecio vulgaris, 12 resistance issues in, 30, 32 Silverleaf whitefly, 26, 27 spot, 21 Simazine, 12, 44 Powdery mildew, 18, 56–57, 80, 81 Single-site inhibitor, 80–81 Prickly lettuce, 46 Smooth pigweed, 36 Protoporphyrinogen inhibitors, 36, 47–49 Soil residual activity, 14, 53 Protox inhibitors, 47–49 Sorbitol octanoate, 111 Public sector plant breeding, 138–140 Sorghum, 44, 45, 148 Pyraclostrobin, 129 Sorghum halepense, 26 Pyramiding, 64, 66, 74–75, 138–139, 148 Southern Insect Management Research Unit, 148 Pyrethroid, 23, 34, 61, 62–63, 86 Southwestern corn borer, 33 -organophosphate combination, 26 Soybeans, 1, 4, 14, 17, 26, 33–37, 38, 45, 46, 47, 48, 54, 89, 107, resistance, 25–26, 27, 95, 111 112, 144, 148, 157 synthetic, 20, 86 Soybean/corn crop rotation, 1, 4, 5, 14, 33–37, 54 Pyrimidinediones, 47 Soybean cyst nematode, 34–35 Pyrimidinyl-thio-benzoates, 45–46 Spatial models, 70 Pythium spp., 27 Spider mites, 20, 31 Spinosad, 20, 63, 109, 129, 130 Q State lead agencies, 115, 137 Stem rust, 138 QoI. See Quinone outside Inhibitor fungicides Sterol inhibitors, 17, 56, 81, 150 Quinone outside Inhibitor fungicides, 41, 58, 59, 81–82, 98, 122 Sticky cotton, 26 Stone fruits, 130 R Streptomycin, 150 Strobilurins, 17–18, 19, 21, 35–36, 81, 97, 110, 131, 150 Ragweed, 36, 37, 53, 157 Strobilurus tenacellus, 81 Rapeseed/canola, 61 Strobilus, 87 Redroot pigweed, 157 Sucrose octanoate, 111 Redundant killing, 74 Sugar esters, 111 Regional Integrated Pest Management Centers, 3, 134, 163 Sugarcane, 44, 45 Sulfony-lamino-carbonyl-triazolinones, 46 190 Index
Sulfonylurea herbicides, 21–22, 45, 46, 51, 78, 112 programs of, 3, 110, 118, 136, 148, 161, 168 Sulfur, 17, 57, 167 resistance management programs/centers, 2–3, 90–91, 105, 106, Sunflowers, 43 111, 118, 119, 120, 126, 137, 148, 162–163, 167, 169 Syngenta, 45–46, 47, 48, 129, 149 role of in pest resistance management, 2–3, 90–91, 105, 126, 167, Synthetic pyrethroid insecticides, 20, 86 169 Symposium proceedings to inform, xvii, 1, 4 U. S. Environmental Protection Agency, vi T Bacillus thuringiensis regulations, 33, 154, 164–165 Biopesticides and Pollution Prevention Division, 112 Target site, 12, 51, 102, 142 and Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA), insensitivity, 46 102–104 mutations, 18, 19, 52, 81 and Food Quality Protection Act, 7 plasticity, 46 goals and challenges of, 31, 102–106, 116, 118–119, 121, 126, 133, resistance, 12, 15, 44, 46, 51, 97 141 specificity, 51–53 and IR–4 Program, 109–112 Tarnished plant bug, 27 nicotinoid seed treatment regulations, 34 Tetranychid mite, 167 Notice of Pesticide Registration, 34 Thiacloprid, 20 and Pest Management Regulatory Agency of Canada, 102–106, Thiadiazoles, 47 142 Thiamethoxam, 20, 34 and Pesticide Environmental Stewardship Program, 30–32, 114, Thrips, 20, 23 135–136 Thrips palmi, 21 reduced-risk pesticides registered by, 59, 86, 87 Thymol, 111 role of in pesticide resistance management, 2–3, 21, 31–32, 89– Tillage, 30, 43, 44, 45, 47, 92, 157 90, 96, 99, 109–112, 129, 137, 154–156, 162–163, 167–168 Tobacco budworm, 25, 27, 69, 147 state lead agencies and, 115 Tolerance, 28, 35, 53, 110, 111, 132, 139, 147, 148 Symposium proceedings to inform, xvii, 1, 4 Tomato, 20, 21, 23, 46, 64 thymol regulation, 111 Transgenic U.S. Food and Drug Administration, xvii corn, 33, 70, 153 U.S. Food Quality Protection Act, 6, 7, 10, 17, 20–21, 58, 102, 105, cotton, 27–28, 147–149, 155 109, 116, 131–132 plants/crops, 2, 4, 34, 63–64, 66–68, 69, 73, 74, 86, 95, 102, 104, Uncinula necator, 56–58 114, 126, 129, 139, 150–151, 154, 166 United Nations, 4, 10 soybeans, 33, 36 University of California, “Herbicide Resistance—How to Delay or technology, 28 Prevent Problems,” 27 Triazines, 12–13, 36, 44–45, 48, 49, 54, 77, 78 Triazolinones, 47 V Triazolopyrimidines, 45 Trifloxistrobin, 35 Valine, 46 Trifluralin, 54 Varietal selection, 109 Tropical fruit, 111 Varroa mites, 111 Turf/Turfgrass, 1, 5, 17, 38–42, 114 Vascular wilts, 92 2,4–D, 12, 44, 45, 47, 54, 78 Velvetleaf, 44 Venturia inaequalis, 56–59, 81 U Vero Beach Research Center, 45 Viruses, 4 U.S. Board on Agriculture of the National Research Council, 7, 10 U.S. Centers for Disease Control, 7 W U.S. Cotton Beltwide Monitoring Program, 148 U.S. Department of Agriculture Waterhemp, 36–37, 46, 47, 48, 54 –Agricultural Research Service, 120–121, 135, 147, 148 Weeds Agriculture and Agri Food Canada Program, 105 in corn/soybean crops, 33, 36–37, 92 –Cooperative State Research, Education, and Extension Service, in cotton, 26, 92 vi, 118–119, 133, 134–136, 161, 162, 168 and fungal plant pests, 17 –Economic Research Service, 153 glyphosate-resistant, 51, 53–54, 111–112 grading standards, 3, 168 herbicide-resistant in North America, 1, 4, 12–15, 22, 45–49, 74, Interregional Research Project Number 4, 32, 109–112, 119, 121, 77–79, 114, 124–125, 143–145 128, 132, 135, 163, 167, 168 management of, 1, 4–5, 36–37, 43, 49, 90, 100–102, 116, 124, marketing standards, 168 148, 166–167 –National Agricultural Statistics Service, 163 in organic crops, 43 –Natural Resources Conservation Service, 3, 167, 169 pest resistance in, 4, 8, 20, 27, 61, 73–74, 100, 112, 114 organic foods and, 85, 167 in potatoes, 30–31 Pest Management Centers, 162–163 strategies for herbicide resistance in, 143–145 Pesticide Environmental Stewardship Program, 30–32, 115, in turfgrass, 38 135–136 in vegetable crops, 157–159 Management of Pest Resistance: Strategies Using Crop Management, Biotechnology, and Pesticides 191
Weed Science Society of America, 15, 26 Weevil, 22, 28, 92, 147 Wegman IPM Program, 85 West Nile virus, 7 Western corn rootworm, 33, 34, 107 Western cotton, 92 Western flower thrips, 20 Western Regional Coordinating Committee, 160 Wheat, 17, 38, 43, 46, 108, 138 Wheat stem sawfly, 43 White grubs, 34 White mold, 35 Whiteflies, 20, 23, 26, 27, 93, 132 Wild radish, 36 Windows approach, 27 Wireworms, 31, 34 Wisconsin-Florida RAMP, 129, 131 Wisconsin Potato and Vegetable Growers Association, 131 World Health Organization, 7, 9–10 World Wildlife Fund, 86, 131
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Xanthium strumarium, 26 XML. See Extensible Markup Language