CALIFORNIA AGRICULTURAL RESEARCH PRIORITIES PIERCE’S DISEASE

Committee on California Agricultural Research Priorities: Pierce’s Disease

Board on Agriculture and Natural Resources

Division on Earth and Life Studies

NATIONAL RESEARCH COUNCIL OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS
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California Agricultural Research Priorities Pierce’s Disease CALIFORNIA AGRICULTURAL RESEARCH PRIORITIES PIERCE’S DISEASE Committee on California Agricultural Research Priorities: Pierce’s Disease Board on Agriculture and Natural Resources Division on Earth and Life Studies NATIONAL RESEARCH COUNCIL OF THE NATIONAL ACADEMIES THE NATIONAL ACADEMIES PRESS Washington, D.C. www.nap.edu

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California Agricultural Research Priorities Pierce’s Disease THE NATIONAL ACADEMIES PRESS 500 Fifth Street, N.W. Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance. This study was supported by Agreement No. SA6646 between the National Academy of Sciences and the University of California. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the views of the organizations or agencies that provided support for the project. This report was prepared as a result of work sponsored through the University of California by the California Department of Food and Agriculture Agreement Number 02-0376. It does not necessarily represent the views of the Agency, its employees or the State of California. Neither the Agency, nor any of its employees, contractors or subcontractors, nor the Regents of the University of California: (A) Make any warranty or representation whatsoever regarding the report, express or implied, with respect to the merchantability or fitness for any particular purpose of the report, or freedom from contamination by computer viruses with respect to the report, or (B) Assumes any liability whatsoever, direct or indirect with respect to any use of the report or any portion thereof, or for the accuracy or validity of the information contained in the report. The National Academy of Sciences is an Equal Opportunity service provider. International Standard Book Number 0-309-09289-2 (Book) International Standard Book Number 0-309-54493-9 (PDF) Library of Congress Control Number 2004114396 Additional copies of this report are available from the National Academies Press, 500 Fifth Street, N.W., Lockbox 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu Copyright 2004 by the National Academy of Sciences. All rights reserved. Printed in the United States of America

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California Agricultural Research Priorities Pierce’s Disease THE NATIONAL ACADEMIES Advisers to the Nation on Science, Engineering, and Medicine The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Bruce M. Alberts is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Wm. A. Wulf is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Bruce M. Alberts and Dr. Wm. A. Wulf are chairman and vice chairman, respectively, of the National Research Council

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California Agricultural Research Priorities Pierce’s Disease COMMITTEE ON CALIFORNIA AGRICULTURAL RESEARCH PRIORITIES: PIERCE’S DISEASE JAN E. LEACH, Chair, Kansas State University, Manhattan PEDRO BARBOSA, University of Maryland, College Park MICHAEL J. DAVIS, University of Florida, Homestead DAVID G. HOEL, Medical University of South Carolina, Charleston L. JOE MOFFITT, University of Massachusetts, Amherst ALISON G. POWER, Cornell University, Ithaca TERRY L. ROOT, Stanford University, Stanford JACK SCHULTZ, The Pennsylvania State University, University Park WILLIAM E. SPLINTER, University of Nebraska, Lincoln BRIAN J. STASKAWICZ, University of California, Berkeley MARIE-ANNE VAN SLUYS, University of São Paolo, Brazil T. ULF WESTBLOM, Central Texas Veterans Health Care System, Texas A&M University, Temple Staff KIM WADDELL, Study Director (through March 2004) ROBIN SCHOEN, Senior Program Officer MICHAEL KISIELEWSKI, Research Associate DONNA WILKINSON, Research Intern PETER ROGERS, Research Intern CINDY LOCHHEAD, Project Assistant JULIE COFFIN, Project Assistant

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California Agricultural Research Priorities Pierce’s Disease BOARD ON AGRICULTURE AND NATURAL RESOURCES MAY BERENBAUM, Chair, University of Illinois, Urbana SANDRA BARTHOLMEY, University of Illinois, Chicago DEBORAH BLUM, University of Wisconsin, Madison H. H. CHENG, University of Minnesota, St. Paul W. R. (REG) GOMES, University of California, Oakland ARTURO GOMEZ-POMPA, University of California, Riverside PERRY R. HAGENSTEIN, Institute for Forest Analysis, Planning, and Policy, Wayland, Massachusetts JEAN HALLORAN, Consumer Policy Institute/Consumers Union, Yonkers, New York JANET C. KING, Children’s Hospital Oakland Research Center, California DANIEL P. LOUCKS, Cornell University, Ithaca, New York WHITNEY MACMILLAN, Cargill, Inc., Minneapolis, Minnesota BRIAN MCBRIDE, University of Guelph, Ontario, Canada TERRY L. MEDLEY, DuPont de Nemours & Co., Wilmington, Delaware OLE NIELSEN, Ontario Veterinary College, Canada ROBERT PAARLBERG, Wellesley College, Massachusetts ALICE N. PELL, Cornell University, Ithaca, New York BOBBY PHILLS, Florida A&M University, Tallahassee SHARRON S. QUISENBERRY, Virgnia Polytechnic Institute and State University, Blacksburg SONYA B. SALAMON, University of Illinois at Urbana-Champaign JACK WARD THOMAS, University of Montana, Missoula B. L. TURNER, Clark University, Worcester, Massachusetts JAW KAI WANG, University of Hawaii, Manoa Staff CHARLOTTE KIRK BAER, Director KAREN L. IMHOF, Administrative Assistant

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California Agricultural Research Priorities Pierce’s Disease Reviewers This report represents the integrated efforts of many individuals. The committee thanks all those who shared their insight and knowledge to bring the document to fruition. We also thank all those who participated in our public sessions. The committee is grateful to members of the National Research Council (NRC) staff who worked diligently to maintain progress and quality in its work. This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the National Research Council’s Report Review Committee. The purpose of this independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberative process. We wish to thank the following individuals for their review of this report: Paul E. Read, University of Nebraska, Lincoln John S. Hartung, USDA-ARS, Beltsville, Maryland Lori Ann Thrupp, Fetzer Vineyards Donald L. Hopkins, University of Florida, Apopka

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California Agricultural Research Priorities Pierce’s Disease Carole Meredith (Emeritus), University of California, Davis Gregory English-Loeb, Cornell University, Ithaca, New York George W. Norton, Virginia Institute of Technology, Blacksburg Jerome B. Siebert, University of California, Berkeley Andrew J.G. Simpson, Ludwig Institute for Cancer Research, New York, New York Ann Vidaver, University of Nebraska, Lincoln Frank H. Stillinger, Princeton University, New Jersey Although the reviewers listed above have provided many constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations nor did they see the final draft of the report before its release. The review of this report was overseen by R. James Cook, Washington State University. Appointed by the National Research Council, they were responsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the authoring committee and the institution.

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California Agricultural Research Priorities Pierce’s Disease Preface Although Pierce’s disease (PD), caused by the bacterial pathogen Xylella fastidiosa (Xf), has been present in California vineyards for more than a century, it has not been considered a major problem for more than 40 years. The situation changed dramatically with the introduction of a new more aggressive vector, the glassy-winged sharpshooter (GWSS) Homalodisca coagulata (Say), a leafhopper of the Cicadellidae family. By the end of 2003, 15 counties in California were infested with this new vector, and in Riverside County alone PD damage estimates approached $13 million. Because of the high potential for GWSS to continue to move and transmit the pathogen within the state—and because of the tremendous value of grapes and grape products to California—this situation, understandably, created great concern. That worry is exacerbated by the facts that other strains of Xf can cause disease in other economically important crops, such as citrus and almond, and that GWSS is a voracious feeder, with tastes for a broad range of plants. I can only imagine the frustration when this disease that historically had been confined to a relatively limited area of California first began to be spread farther and faster by the new vector. The old management strategies were insufficient by themselves, and it was not clear whether components of those strategies could provide some relief from the emerging problem, or whether entirely new paradigms for management of the disease and pest would be needed. Although pockets of solid and excellent research on PD, GWSS, and

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California Agricultural Research Priorities Pierce’s Disease their interactions with grapevine existed, none were sufficient to provide conclusive answers to those questions. Faced with this crisis, the relevant industry, university, and government groups rapidly established a funding program that solicited the badly needed research. The initial net cast for research projects was very broad and inclusive. Now, with the accumulation of several years of data, the funding network has realized the need to review research progress and to focus efforts in areas that are most likely to lead to management of the PD–GWSS problem. Identifying research areas with the most promise was the major challenge presented to the Committee on California Agricultural Research Priorities: Pierces’ Disease, which has produced this report. Although tragic in and of itself, the positive aspect of the PD–GWSS situation is that it calls attention to the need for models for coping with other emerging or introduced disease and pest problems of agronomic importance. Although the focus of the report is on PD–GWSS in grape in California, during its deliberations, the committee considered operational and research strategies in a much broader context. The intent is that the ideas and suggestions provided here will serve as a foundation for responses to future outbreaks. Most of my career as a plant pathologist has been spent studying an annual crop species, where breeding for resistance is the most economically feasible and environmentally sound approach to disease management. Understanding the many complex facets of the PD–GWSS problem on grape was a particularly intriguing exercise. Breeding for resistance to PD in grapevine is not trivial for many reasons, not the least of which is the importance of the genetic identity of traditional cultivars used for wine making. The current social and political landscape in California restricts consideration of other options for disease management that might be acceptable elsewhere, including the use of transgenic varieties. These and many other considerations made for lively and thought-provoking discussions during committee meetings. I particularly want to thank the committee members for their hard work in drafting, reviewing, and revising the document. It is particularly satisfying that the diverse expertise of the committee is positively reflected in the document, and I truly appreciate each member’s willingness to consider and discuss freely the perspectives of others. The PD–GWSS research community was particularly helpful to our deliberations; they patiently answered our many questions and frequently provided unpublished information for our education and consideration. Special thanks are extended to the staff of the Board on Agriculture and Natural Resources of The National Academies, including Michael Kisielewski, Donna Wilkinson, Julie Coffin, Cindy Lochhead, Peter Rodgers, and Tanja Pilzak. I thank Dr. Kim Waddell, the study director, for his essential scientific insights, his tremendous tact and patience, and his tireless efforts. Finally, I thank Robin Schoen, who, due to changes in staffing, was brought into the preparation of this report just before the review process. Her

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California Agricultural Research Priorities Pierce’s Disease fresh perspective, sound judgment, and superb organizational skills were critical in completing the document. Jan E. Leach Chair, Committee on California Agricultural Research Priorities: Pierce’s Disease

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California Agricultural Research Priorities Pierce’s Disease Contents     EXECUTIVE SUMMARY   1      Pierce’s Disease and Glassy Winged Sharpshooter Research   2      Establishing Priorities   4      Key Recommendations   7      Summary   14      Recommendations (By Chapter)   14 1   PIERCE’S DISEASE AND THE GLASSY-WINGED SHARPSHOOTER: THEIR BIOLOGY AND THE CHALLENGES OF THEIR MANAGEMENT   21      Pierce’s Disease   22      Glassy-winged Sharpshooter   26      Costs of Pierce’s Disease   28      Response to Pierce’s Disease and the Glassy-winged Sharpshooter   34      Overview of Approaches   38      Acceptance of Management Strategies   41 2   DEVELOPING PRIORITIES FOR RESEARCH   45      Current Research   46      Evaluation Framework   50 3   HOST–VECTOR INTERACTION   55      Tactics and Strategies for Ecologically Based Pest Management   56      Host–Plant Resistance   57      Management of Vegetation   64      Biological Control   70

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California Agricultural Research Priorities Pierce’s Disease      Current Tactics and Strategies in Biological Control   72      Other Options   78      Insecticides   81      Economic Control Strategy   84 4   PLANT–PATHOGEN INTERACTION   88      Analyzing Virulence   89      Toward Host Plant Resistance   92      Chemical Control   98      Cultural Methods to Reduce Bacterial Inoculum   100      Biological Control   102      Summary   104 5   VECTOR–PATHOGEN INTERACTION   105      Strategies of Interference   106      Pathogen Transmission   106      Pathogens and Vector Fitness   110      Infection and Vector Behavior   111     REFERENCES   114 APPENDIX A:   COMMITTEE BIOGRAPHIES   153     BOARD ON AGRICULTURE AND NATURAL RESOURCES PUBLICATIONS   158

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California Agricultural Research Priorities Pierce’s Disease Tables, Figures, and Boxes TABLES 1-1   Plant Diseases Caused by Different Strains of Xylella fastidiosa   24 1-2   Hypothetical Cost and Revenue Scenario of Vineyard Replacement   29 1-3   Estimated Vineyard Establishment and Replanting Cost   30 1-4   Grape Acreage by End Use, Citrus Acreage, Almond Acreage in California Counties, 2001   32 FIGURES 1-1   GWSS Distribution in California   27 1-2   Research Coordination through the Pierce’s Disease Control Program   35 BOXES ES-1   Framework for Evaluating Research and Management Strategies   19 1-1   Who Should Implement Control Strategies?   37 2-1   Ensuring High Scientific Standards in Proposal Selection   49 5-1   Pathogen Effects on Vector Survivorship and Reproduction   110 5-2   Vector Attraction to Infected Plants   112 5-3   Implications for Epidemiology   113

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