Executive Summary

Invasive species threaten agricultural ecosystems throughout the world. Within the United States, California has one of the most diverse and productive agricultural ecosystems. Because of its wealth of production systems, hospitable climate, and the ready movement of plants, animals, and microbes across its borders, California also is particularly vulnerable to invasive pests. Recent introductions of nonnative insect species into California, among them the olive fruit fly and the imported fire ant, are examples of invasive species that threaten ecosystems.

One significant threat to California agriculture in recent years has been the glassy-winged sharpshooter (GWSS) Homolodisca coagulata (Say) as a vector of Xylella fastidiosa (Xf), a bacterial pathogen that causes a range of diseases that threaten agricultural and horticultural crops. One disease is Pierce’s disease (PD) of grapevines, which affects wine, table, and raisin grape production. In California, grape production covers over 880,000 acres and represents $33 billion dollars in economic value.

Given the seriousness of the threat, the California Department of Food and Agriculture (CDFA), the U.S. Department of Agriculture (USDA), grape growers, and commodity and trade organizations have responded with directed efforts to slow the spread of the new insect vector and the disease. CDFA coordinates funding and provides oversight of the research effort through the Pierce’s Disease Control Program. In 2001, CDFA and the University of California’s Division of Agriculture and Natural Resources approached the National Research Council of the National Academies, requesting that the Council help monitor current and emerging issues in the state’s agricultural research agenda, particularly for PD. In response, the Board on Agriculture and Natural Resources convened an ad hoc committee, the Committee on California Agricultural Research Priorities: Pierce’s Disease, to address scientific and



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California Agricultural Research Priorities Pierce’s Disease Executive Summary Invasive species threaten agricultural ecosystems throughout the world. Within the United States, California has one of the most diverse and productive agricultural ecosystems. Because of its wealth of production systems, hospitable climate, and the ready movement of plants, animals, and microbes across its borders, California also is particularly vulnerable to invasive pests. Recent introductions of nonnative insect species into California, among them the olive fruit fly and the imported fire ant, are examples of invasive species that threaten ecosystems. One significant threat to California agriculture in recent years has been the glassy-winged sharpshooter (GWSS) Homolodisca coagulata (Say) as a vector of Xylella fastidiosa (Xf), a bacterial pathogen that causes a range of diseases that threaten agricultural and horticultural crops. One disease is Pierce’s disease (PD) of grapevines, which affects wine, table, and raisin grape production. In California, grape production covers over 880,000 acres and represents $33 billion dollars in economic value. Given the seriousness of the threat, the California Department of Food and Agriculture (CDFA), the U.S. Department of Agriculture (USDA), grape growers, and commodity and trade organizations have responded with directed efforts to slow the spread of the new insect vector and the disease. CDFA coordinates funding and provides oversight of the research effort through the Pierce’s Disease Control Program. In 2001, CDFA and the University of California’s Division of Agriculture and Natural Resources approached the National Research Council of the National Academies, requesting that the Council help monitor current and emerging issues in the state’s agricultural research agenda, particularly for PD. In response, the Board on Agriculture and Natural Resources convened an ad hoc committee, the Committee on California Agricultural Research Priorities: Pierce’s Disease, to address scientific and

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California Agricultural Research Priorities Pierce’s Disease technical issues surrounding new and potential challenges to California agriculture with respect to PD. The committee was asked to monitor scientific advances in the areas of economically and environmentally important agricultural diseases and pests, including their vectors; respond to requests; identify emerging issues; provide independent analyses of scientific information and of state, federal, and international activities; and submit a rigorous and timely evaluation of scientific issues in response to identified areas of concern. The specific charge to the committee was as follows: The area of proposed study for the committee will be the current outbreak of agricultural diseases caused by Xylella fastidiosa and the disease vector, the glassy-winged sharpshooter. The committee will review the state of California’s priorities for both short-term and long-term research and management efforts to control the glassy-winged sharpshooter, and identify a cure for Pierce’s disease. It is anticipated that the committee will help to identify research priorities and needs, and will assist the state in coordinating with national and international program efforts to address the disease. PIERCE’S DISEASE AND THE GLASSY-WINGED SHARPSHOOTER RESEARCH Pierce’s disease has affected grape production in California for more than a century, but until the introduction of GWSS in the past decade, neither the pathogen nor the insect stimulated significant and consistent research support. Because wine grape growers add significant value to their crops by making and selling wine, the wine industry has considerably greater resources than other agriculture commodity sectors do. The industry has been able to respond rapidly to the problems of PD–GWSS and to allocate significant resources for addressing the threat. The result is expanded research on the grape–PD–GWSS system and on identifying opportunities to control or manage the disease and vector. Over the past 3 years, nearly $20 million has been set aside to fund 125 completed and continuing research projects. Support is provided by the PD/GWSS Board, CDFA, the University of California Pierce’s Disease Research Grants Program, USDA’s Animal and Plant Health Inspection Service and its Agricultural Research Service, the American Vineyard Foundation, the California Competitive Grant Program for Research in Viticulture and Enology, the California Citrus Nursery Advisory Board, the Almond Board of California, and the California Department of Transportation. The research program that has emerged from the exchange of information, data, and experiences among growers, county and state officials, and academic researchers reflects the various interests of the stakeholders in the

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California Agricultural Research Priorities Pierce’s Disease PD problem. Projects within the program can be classified into nine areas of basic research: crop biology and ecology basic biology of the vector insect–plant interactions and vector population ecology genetics of Xf Xf–host and plant–insect interactions epidemiology of Xf diseases vector monitoring and action thresholds Xf monitoring and action thresholds economics The program also supports applied research on management strategies for biologic and chemical control; cultural, physical, and behavioral control; and resistance to Xf diseases. The short-term objectives of the research are to produce tools and tactics that lead to methods of management of the bacterium and insect vectors; the long term goals are the prevention and cure of PD. This report is being released as the research efforts are just beginning to deliver results from the initial investment. Although in some instances a clearer understanding of the remaining challenges is emerging, in general, management efforts are hindered by a lack of understanding of the biology of the organisms and their mechanisms of interaction, and by a lack of information about the costs and benefits of different approaches. Setting priorities is difficult, and, as part of the discussion about different research avenues, the committee had to consider experience with other diseases in other contexts to judge the likelihood that one or more approach for addressing PD would prove useful. Nevertheless, the committee developed a clear picture of the foundation of information needed to build an effective response to PD–GWSS. The conclusion is that a well-conceived management program will be based on knowledge of the characteristics and interactions of the pathogen, the vector, and the host; the cultural and climate conditions under which the crop is grown; and the procedures available for disease control, including cultural, genetic, and chemical approaches. Management programs must be economically feasible, and their environmental and ecosystem effects must be kept to a minimum. In general, the breadth of topics included in the program appears appropriate for building the foundation needed to address PD–GWSS, but because the community is still at an early stage of understanding the various components of the epidemic, management strategies, policies, and research programs will need to be adjusted to maximize the investment of limited financial resources as new information evolves. Those adjustments will be achieved by recognizing the varying pace at which information will flow from different projects and by assessing the relative value and quality of different types of information in leveraging progress across all elements of the program, so that some subject areas or projects can be emphasized relative to others as the

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California Agricultural Research Priorities Pierce’s Disease overall research progresses over time. It also requires the selection of only those projects that meet the highest levels of scientific rigor. This strategic approach rests on the ability of the program to achieve significant coordination in project solicitation and selection and to maintain the flexibility to shift priorities as research results provide new information. The current process of selecting and supporting research might not be the best one for implementing such a framework. Not all research approaches are valued the same by the involved parties. Industry is searching for a solution to the problem faced by its commodities, and much of the research community is focused on uncovering the basic biology and epidemiology of PD–GWSS. There are good reasons to pursue research on both kinds of questions, but disjointed selection of projects could hinder the opportunities to create synergies or to implement a logical progression of research. The selection and design of basic and applied research should be at least complementary, and even integrative, if possible; the goal is to accumulate data that will advance progress on all fronts. The committee noted an absence of uniformity and communication in the process through which PD–GWSS research projects are selected, accepted, and funded. The greatest concern is that the scientific merit of the proposals is not receiving consistent scrutiny and attention. That could hinder the program’s ability to move forward, because decisions about priorities and direction need to be made using solid, reproducible results. Consequently, the committee makes the following recommendation: To ensure scientific rigor in and enhance coordination of the PD–GWSS research program, participating research sponsors should consolidate processes for proposal solicitation and review. Consolidation would facilitate the identification of strategically critical projects and of critical areas that are not receiving funding, avoid redundancy in the selection of projects, reduce costs, and distinguish projects for which teams or consortia should be established from those appropriate for one or two principal investigators. ESTABLISHING PRIORITIES The committee’s goal in providing advice on research priorities was to focus on strategies that would culminate in the development of effective control mechanisms. Several guiding themes emerged from deliberation on how to characterize the most desirable research outcomes. First, effective mechanisms can be defined as those that interfere with one or more of the three interactions involving PD–GWSS: between the host and the vector, between the vector and the pathogen, and between the host and the pathogen. Any successful “interference” could break the chain of events that ends with a plant succumbing to PD. By identifying a specific mechanism, researchers eventually could provide growers with tools or strategies to minimize the risks to or effects of the

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California Agricultural Research Priorities Pierce’s Disease disease in their agricultural production systems. (The concept of interference gave the committee a logical way to organize its work. In the report, separate chapters are dedicated to research on each of the three interactions.) A second guiding theme is that, because measures that keep the disease in check are more realistic than are attempts to cure or eradicate PD, it is better to focus on management strategies instead of cures, keeping in mind that different strategies will be useful for some parts of the grape industry and not for others and that management approaches will depend on the environment. Management tactics at the northern limit of the GWSS in California might be different from those used in the center. Third, although disease can be potentially controlled with one procedure, better management usually is achieved by means of a set of methods. Different measures are likely to provide incremental benefits; the goal should be to develop a complementary suite of approaches. Fourth, consideration should be given to the potential of any method to damage the environment and ecosystem; therefore, research that leads to ecologically based pest management (EBPM) strategies should be encouraged. Many board-spectrum synthetic chemical pesticides kill not only arthropod and pathogen pests but also beneficial organisms that serve as natural pest control systems. There also is a risk of dependence on chemical pesticides to which pests may eventually become resistant. EBPM systems are built on an underlying knowledge of the managed ecosystem, including the natural processes that suppress or augment pest populations. The practices will be supplemented by biological-control organisms and products, resistant plants, and narrow-spectrum pesticides. Evaluation Framework With the guiding principles in mind, the committee developed a framework for examining elements of the current and prospective PD–GWSS research program. The framework consists of two sets of evaluation criteria, and a system for grouping current and prospective research projects into categories that reflect differences in certainty, cost, and relative effectiveness. The first criterion assesses the ability of projects to achieve successful management of the PD–GWSS problem. The second addresses the important notion of sustainability of the strategies or products. Feasibility: Considering technical barriers and practical limits (including cost), what is the likelihood that the research will result in tools for effective management of PD–GWSS? Time: What period is required for the research to deliver an effective strategy, approach, or tool? Effectiveness: What is the likelihood that the research product will deliver a strategy that will improve the PD–GWSS situation? Because the degree to which a given strategy or product will change the situation will vary, it must be

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California Agricultural Research Priorities Pierce’s Disease determined whether the degree of change is better or worse than that achieved by other management measures and whether the strategy or product is sufficiently effective to warrant funding. Cost: What will it cost to accomplish the research objectives? Sustainability: Is the approach or product biologically adaptable and affordable? Will it remain useful? Efforts to manage disease or pest outbreaks in agriculture often promote research that results in effective short-term solutions, but because diseases and pests are dynamic and evolving, those control measures are often not sustainable solutions. What is the likelihood that the proposed research will lead to management strategies that can be affordably implemented over the long term? With information from the first criterion for any given research strategy, the committee classified each research strategy into one of four categories: Category 1: The research option holds reasonable promise of generating successful tools for management of PD–GWSS, either in the short term or in the long term. Category 2: The research approach looks promising, but either because of insufficient data or because of inconclusive results, it is difficult to predict whether it will lead to successful applications for management. Category 3: The research can produce data and results that are promising for successful management of PD–GWSS, but because of its complexity and the technology required, it would be prohibitively expensive for any one funding source to manage. Category 4: The research approach does not show promise, even in the long term, for PD–GWSS management. Assignment of projects to those categories provides a way to examine options for the research program as a whole. In considering how projects might be selected from several categories or within any particular category, the committee returned to the criterion of sustainability, concluding that, because many short- and medium-term control options are unlikely to be sustainable, a mixture of projects should be considered. Research priorities should be developed using the two criteria—the predicted feasibility that an approach will contribute to PD–GWSS management and its sustainability. The committee recommends a balance among short-, medium- and long-term research projects to ensure the development of sustainable management approaches.

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California Agricultural Research Priorities Pierce’s Disease KEY RECOMMENDATIONS The research strategies recommended here are the result of the committee’s evaluation process, and are designated by category. Many potential research avenues are promising but lack the data required to inform a convincing prediction of success; those strategies fall into Category 2. The committee recommends that a mixture of projects be pursued, but above all that projects of the highest scientific quality in rationale, scope, and design be selected. A small number of research efforts are under way that the committee would assign to categories 3 and 4. They are discussed but not highlighted in the recommendations. Although in the full report the committee discusses the interactions of host, vector, and pathogen in two dimensions—that is, host–vector, host–pathogen, and pathogen–vector—it is important to recognize that the reality is a dynamic three-way interaction. Therefore, many of the recommendations in the report exhibit overlap in approach. To reflect the nature of these interactions, in this Executive Summary we consolidate several of the report’s recommendations. A full list is given at the end of the Executive Summary. Several factors, apart from purely scientific considerations, will influence the decision to pursue or implement a management strategy. For example, the cooperation of growers of unaffected crops might be required to implement some control measures; if those measures are to be effective, a continuing dialogue must be fostered about PD within agribusiness. Some factors that affect the pursuit of one or another management strategy are related to sustainability, which, in addition to scientific issues (such as the vector’s development of pesticide resistance), includes regulatory uncertainties or public acceptance, which could change. Some strategies will work in some cases and not others. For example, maintaining unique lineages of grapes results in the production of distinctive varieties of wine, such as chardonnay and cabernet sauvignon, which add value to grape production. But it also severely limits opportunities for crop improvement strategies that focus on breeding for disease or insect resistance by the conventional methods used for many other crop species. Breeding approaches might be useful for table grapes or raisins, however. Although the process of placing research options in categories focused on the potential effectiveness, time, and cost of a particular approach, the report mentions issues of sustainability and other factors when applicable. Interactions of Host, Pathogen, and Vector When this study began, the committee noted significant gaps in knowledge about the characteristics and biology of pathogen and insect and how they interact with each other and the host plant. Through the funding program coordinated by CDFA as well as other national and international institutions, significant, albeit in insufficient, strides are being made to remedy that lack of information. This is especially evident for Xf. The internationally coordinated

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California Agricultural Research Priorities Pierce’s Disease research effort that recently released the genome sequence for Xf provides fundamental information for development of testable hypotheses. For example, genes selected based on their relationships to genes with known functions in other pathogenic bacteria can be tested directly to determine whether they function in virulence to grapevine, survival in the environment, and interactions with the insect vector. Those hypotheses can now be accurately tested because of the development of standardized and reliable plant inoculation and molecular assays for measuring disease and defense responses and because of the development of new tools for genetic modification of the pathogen. The information will identify targets for interference, and thus for management. Therefore, the committee makes the following recommendations for research: Determine the genetic, biochemical, and physiologic base of Xf virulence, pathogenicity, transmission, and survival. This Category 2 research includes Xf colonization in grapevine and in GWSS and the production and delivery of Xf virulence factors in grapevine. The complex nature of the GWSS has hindered progress in the elucidation of its interactions with Xf and with the diversity of plants that can serve as hosts for the vector. Several aspects of the insect’s interactions with the pathogen and with plants need focused attention, including the biology of GWSS feeding, acquisition and transmission of Xf, host-finding behavior, host plant preferences, factors that influence reproductive success, and the importance of entomosymbionts (microbes that inhabit insects). To address those questions, the committee recommends the following research objectives: Determine genetic, biochemical, and physiologic basis for GWSS herbivory and disease vectoring. This Category 2 research includes GWSS feeding and host–finding behavior, host plant preference, performance on different hosts, and influences of natural enemies. Also included are the effects of Xf on GWSS behavior and on survivorship, fecundity, population growth rates. Knowledge of the host plant responses to GWSS feeding or to colonization by Xf could help guide breeding programs or vegetation management practices. Both Xf and GWSS target the plant xylem, so information about the composition of the xylem before, during, and after feeding or pathogen introduction is needed. Recent studies are beginning to unravel how GWSS feeds on xylem, and how, once introduced, Xf moves within and between vessels. However, little is known about how the xylem and surrounding tissues respond to insect feeding or to pathogen ingress or about whether modifications in the xylem structure or content enhance resistance or susceptibility. The committee makes the following research recommendations: Determine the genetic, biochemical, and physiologic basis for host plant factors that influence attraction, repulsion, survival, or inhibition of

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California Agricultural Research Priorities Pierce’s Disease GWSS or Xf. The studies must include an analysis of the criteria for assessing host plant responses and the means of Xf acquisition by GWSS from, and inoculation to, alternative hosts or dormant grapevines. This Category 2 research will benefit from a multifaceted approach, and it should include combinations of biochemical, physiologic, genetic, and genomic analyses. The analyses must be statistically rigorous so the results will be reliable. Host Plant Resistance to Pathogen and Pest Host plant resistance is a core element of disease–pest management strategies for many crop species, including grape, and it should be emphasized as a component of ecologically based management of PD–GWSS. Plants that are resistant either to GWSS or to Xf can be developed through selection and breeding for resistance or by transgenic technologies. Although the plants mechanisms of resistance to the pathogen or pest could differ, the strategies for mapping, cloning, and manipulating resistance or defense response genes are the same. The introduction of disease resistance in wine grapes by breeding is complicated by the complex and subtle gene combinations that contribute to grape quality and by the resistance of consumers, producers, and retailers to altering the genetic nature of the vines through the sexual process of breeding. One approach to reducing the disruption of complex trait combinations is to introduce useful genes by means of transgenic technologies. However, many consumers and producers are opposed to the use of transgenic technologies and there are significant regulatory requirements that must be met in introducing transgenic plants. Moreover, the assumption of introducing useful genes and minimizing disruption of desirable complex trait combinations currently is reasonable but can only be predicted, not assured. Thousands of transgenic plants will be discarded before one is found to have the desired traits. Nonetheless, the technology is a powerful research tool to further our understanding of the genes involved in pest and disease resistance. Although the transgenic plants might not be introduced into the field, the information gained through the research will be valuable. Regardless of the approach taken to develop it, the nature of resistance to GWSS or PD must be better understood. Therefore, the committee recommends the following research: Determine the genetic and mechanistic bases for grapevine resistance to Xf and GWSS. This Category 2 research would attempt to characterize the genetic loci and the biochemical and physiologic mechanisms responsible for host plant resistance to facilitate the development of resistant plants. Develop and improve methods for manipulating grapevine resistance to Xf and GWSS. This Category 2 research is necessary both for

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California Agricultural Research Priorities Pierce’s Disease experimental use (to identify and study resistance traits) and for possible commercial production. The methods should include various breeding practices and genetic transformation technologies. Transgenic approaches are essential to advancing our understanding of the genetic, biochemical, and physiologic bases for plant resistance to insects or pathogens. It is worth pointing out separately that some kinds of research—especially genome based projects—are very expensive and will require consortium efforts and investments. Funding of genome-based projects (particularly those involving hosts) by public agencies such as CDFA and private-sector stakeholders, such as the PD/GWSS Board, should be considered supplemental funding, and the investments should be made when the potential for solving specific commodity problems appears to be within reach. This is Category 3 research. Biological Control Biological control, or the use of living natural enemies to manage GWSS or Xf, is an appealing strategy because it is considered to be more environmentally benign than some other approaches. However, biological control must be rigorously evaluated to determine effectiveness in managing a pest or pathogen. Given approaches also must be proven to be environmentally benign and economically feasible. The focus of most current biological-control efforts for GWSS is on the use of native and introduced species of egg parasitoids (insect species that prey on the eggs). Although that strategy would prove useful in some environments and in combination with other management schemes (such as vegetation management), rigorous experimentation is needed to predict success. The experiments range from rearing and releasing natural enemies to those that examine the critical question of whether parasitoids can sufficiently reduce the abundance of GWSS. The latter point concerns the question of whether small numbers of GWSS can still transmit enough bacteria to cause economically significant disease. The committee makes the following recommendations: Research is needed to advance the use of classical biological control (predators and parasitoids) of the insect. Management will be particularly relevant in commercial vineyards where there is minimal use of insecticides, in vineyards where selective insecticides that are nontoxic to natural enemies are used, or where the timing of insecticide use is such that mortality to natural enemies is minimal. It also will be relevant in areas or habitats where insecticide use can be severely limited or eliminated. Areas for study would include riparian habitats, watershed areas, wetlands, and some urban and suburban green areas. The research is classified as Category 2, and includes the following:

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California Agricultural Research Priorities Pierce’s Disease Establishment of protocols for the effective selection of natural enemies Development of strategies that will increase the success of inoculative releases of parasitoids Rigorous evaluation of the effectiveness of the released natural enemies. Other biological-control strategies for GWSS management, including insect growth regulators, biorational pesticides, biological-control agents other than parasitoids, mating disruption, behavior-modifying chemicals, sterile-male techniques, and mass trapping are discussed in Chapter 3. However, it is not clear whether those strategies would be effective for managing GWSS and PD. For the pathogen, current research biological control is directed predominantly at identifying native endophytic (xylem inhabiting) or insect endosymbiotic (within insects) bacteria that might inhibit Xf or interfere with its interactions with the grapevine or the insect vector. Where limited control has been observed, it seems to be through competition for attachment sites in the hosts rather than through antibiosis. Thus, if any research is to be funded for biological control of Xf, it should be directed at identifying the factors involved in attachment and targeting organisms that compete for the same attachment sites. Such research elucidating the biology of the interactions between the target organisms could reveal important information about host–pathogen or host–vector interactions. However, biological-control strategies generally have not been highly effective for managing vascular pathogens (such as Xf), particularly in perennial crops such as grape. Thus, the committee views work involving biological control of the pathogen as Category 4 research. Because there is no way to confine an organism once it is released into the environment, no biological-control agent, whether to control the vector or to control the pathogen, should be considered for introduction without extensive study of its consequences for the ecosystem in general and more specifically for its effects on beneficial insects or microbes. Vegetation Management Vegetation management can be an important element in a comprehensive pest management system and has been effective for the control of insect-transmitted plant pathogens. Mixing host and non host species can lead to significant reductions in leafhopper abundance, which can also lead to lower prevalence of leafhopper-transmitted pathogens. Thus, GWSS populations, and therefore, the transmission of Xf, are likely to be influenced by the presence of ground covers in vineyards or through a mixture of plant species in riparian areas. However, the committee could not make clear recommendations for vegetation management to growers because information on leafhopper performance on, and preference for, a range of potential cover crops and alternative hosts is adequate, as is information on the potential of these

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California Agricultural Research Priorities Pierce’s Disease alternative hosts to develop epidemiologically significant populations of Xf. Thus, the committee provides the following recommendations: Research should advance the use of vegetation management to reduce populations of GWSS and Xf. This Category 2 research would involve determining the potential of ground cover crops to develop epidemiologically significant populations of Xf; determining leafhopper performance on (survivorship, fecundity, development time) and preference for a broad range of potential ground cover crops; and investigating the use of carefully selected cover crops in vineyards to reduce insect colonization of grape plants. Chemical Control Currently funded research encompasses a range of approaches for PD–GWSS management, some of which will require years of study and field verification before commercial acceptance is possible. Until then, growers face an expanding infestation that promises serious economic consequences. Research on the use of chemicals or biocides offers the most cost-effective near-term solution to managing GWSS in California vineyards. Many pesticides can be effective against GWSS eggs, nymphs, and adults. The insects predominate on different plants at different stages, so several types of pesticides with different application techniques or schedules are needed to effectively disrupt the their development. The best studied pesticides for control of GWSS include the systemic formulations, which move through the vascular system of the plant; the nonsystemics, which act after application to the surface of the plant; and inert compounds, which coat the plant surface to repel insects. Although insecticides offer reasonably good short term management for such control to remain economically feasible and environmentally acceptable, the committee urges research on improved application mechanisms that will reduce drift and thus exposure of nontarget organisms. The committee also recommends the pursuit of additional narrow-spectrum chemical controls. The determination of the social and environmental effects of any recommended compound and the rigorous economic assessments of insecticide effectiveness within an EBPM scheme are also recommended. In general, research should identify management strategies or approaches that minimize the use of insecticides or that promote the use of narrow-spectrum, sustainable pesticides. Research on chemicals should focus on the following areas: Identify and develop more efficient means of delivery of the chemical to the target. Identify novel pathogen targets for which highly specific chemicals can be identified or developed. Determine the social and environmental consequences of using these compounds.

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California Agricultural Research Priorities Pierce’s Disease Conduct an economic assessment of insecticide effectiveness within an ecologically based pest management scheme. Although effective for GWSS, research has demonstrated that existing chemical controls do not provide effective, economically feasible management of Xf or of any other bacterial pathogen of plant vascular systems. Although not all available chemicals have been rigorously tested, chemical control does not appear to be a promising area for short-term management of Xf. This class of controls includes chemicals that do not directly affect the pathogen but which induce systemic resistance in plants. Thus, the committee views this as Category 4 research. However, if research funding is directed at the study of chemical control the work should be directed toward the identification of novel targets in the bacteria for which highly specific chemicals can be identified or developed. Economic Feasibility The major factor driving research on PD–GWSS is the economic effect that results from the spread of the insect and pathogen in commercial agriculture but the true economic dimensions of the PD–GWSS problem are poorly defined. Economic analyses are needed in several areas, from studies of the relative cost of implementing control options to the prospective costs of management strategies currently in development. Because there is uncertainty about the spread of PD and GWSS to other parts of California, cost–benefit analyses of state policies on measures to control that spread should be undertaken. Taking these dimensions into consideration, the committee recommends examples of economic research projects needed. The first two are Category 1 projects: Assess the economic feasibility of specific biological and chemical control methods and strategies. In addition the cost of crop losses, grape production costs can be incurred through biological or chemical controls. Growers need decision and cost models to guide their implementation of specific control regimes. An economic analysis, including environmental impacts, should be for all potential management strategies and outcomes. There are no economic analyses of research-based management strategies and outcomes that address PD–GWSS. Such analyses are needed both to help determine the outcomes that will be most economically practical for growers and to inform the research agenda. The long-term research agenda should include economic analyses of policy regulations, incentives, and institutions to limit introduction and movement of PD vectors. The current concern with PD in California is attributable to the introduction of GWSS, which arrived in California and spread from a single location as a result of human activity. The need to

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California Agricultural Research Priorities Pierce’s Disease manage invasive species, such as GWSS and others that could emerge as PD vectors, could become more significant in the years ahead. This is classified as Category 2 research. SUMMARY Significant progress already has been made in elucidating the biology of the PD–GWSS problem. Plausible management strategies have been tested and either advanced to future studies or eliminated. However, there still are significant knowledge gaps in critical areas. This report identifies those gaps, provides guidance for setting priorities in the research needed to fill them, and describes mechanisms for improving funding and management. Areas that could benefit from research include economic feasibility; the biology of interactions among GWSS, Xf, and host plants; and various management strategies, including those that involve host plant resistance and biological and chemical controls. This and other reports, including those published by USDA’s Agricultural Research Service and the American Vineyard Foundation, provide stakeholders with guidance to take on the remaining challenges in managing the PD–GWSS problem. This report was developed early in the process of elucidating the mechanisms of GWSS–Xf–host interaction and early in the process of setting priorities for funding research. As new data emerge and as approaches and priorities are refined, research and management strategies will be adjusted. The process that has developed through this study can serve as a template for other emerging pest–pathogen problems not only in California, but in agricultural ecosystems in general. RECOMMENDATIONS (By Chapter) 2.1 To ensure scientific rigor and enhance the coordination of the PD–GWSS research program, participating research sponsors should consolidate the processes for proposal solicitation and review. 2.2 Research priorities should be developed according to their ability to meet two criteria: the predicted ability of the approach to contribute to PD–GWSS management and its sustainability. The committee recommends a balance among short-, medium-, and long-term research projects to ensure the development of sustainable management approaches are achieved. 2.3 An economic analysis including a study of environmental impacts should be conducted for all potential management strategies and outcomes (Category 1).

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California Agricultural Research Priorities Pierce’s Disease 2.4 The long-term research agenda should include economic analyses of policy regulations, incentives, and institutions to limit introduction and movement of PD vectors (Category 2). 3.1 Studies that provide more information about sharpshooter feeding, host-finding behavior, host plant preferences, and the factors that influence reproductive success and natural-enemy-caused mortality are needed. The potential effects of Xf infection on sharpshooter behavior and performance should be included in those studies. Those factors must be examined with statistical rigor so that the results are reliable (Category 1). 3.2 All the modern chemical, molecular, ecological, and statistical tools available to scientists should be used to identify mechanistic bases of grapevine resistance to xylem-feeding leafhoppers. Studies should be done in the ecosystem and consider multitrophic interactions among plants, insect pests, and natural enemies (predators and parasites), and they should include both insect-and Xf-induced changes in plant quality (Category 2). 3.3 Host–plant resistance should be emphasized as a component of ecologically based insect management strategies in the grapevine–sharpshooter–Xf system. Methods for manipulating grapevine resistance should be developed for experimental use to identify key resistance traits and with an eye toward eventual commercial deployment. The methods should allow work with genetically transformed plant material, use of chemical or other elicitors, and cultivation practices (Category 2). 3.4 Detailed, quantitative studies should examine leafhopper performance (survivorship, fecundity, development time) on and preference for a broad range of potential ground cover crops (Category 2). 3.5 The feasibility of using carefully selected cover crops in vineyards to reduce sharpshooter colonization to grape should be investigated (Category 2). 3.6 Potential ground cover crops should be screened for the capacity to develop epidemiologically significant populations of Xf (Category 2). 3.7 Detailed, quantitative studies should examine leafhopper preference for potential host plants in the context of natural assemblages of hosts in the field. Studies of leafhopper performance on a broad range of potential host plants are essential to elucidate host ranges (Category 2). 3.8 The plant-to-plant movement of GWSS at multiple scales should be examined throughout the year to identify long-range seasonal and “trivial” movements that lead to disease spread (Category 2).

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California Agricultural Research Priorities Pierce’s Disease 3.9 Sharpshooter host plants should be screened for their capacity to develop epidemiologically significant populations of Xf and examined for effective transmission rates from host to grape (Category 2). 3.10 After the epidemiologically important noncrop host plants of the vectors are identified, the ecological and socioeconomic barriers to removal of those plants from areas that influence disease prevalence in grapes should be explored (Category 2). 3.11 Basic and applied research should establish protocols for the effective selection of natural enemies, develop strategies to increase the success of inoculative releases of parasitoids, and rigorously evaluate the effectiveness of released natural enemies (Category 2). 3.12 Support for classical biological control (inoculative releases) is preferred over augmentation if inoculative releases result in self-sustaining populations and can be shown to be less costly than augmentation (Category 2). 3.13 Research should assess the economic feasibility of biological-control tactics and strategies (Category 2). 3.14 Biological-control tactics within EBPM schemes should be evaluated within the context of working economic thresholds (Category 2). 3.15 Research on the use of biological-control agents (predators and parasitoids) should be a priority in commercial vineyards where there is a minimal use of insecticides, the use of selective insecticides that are nontoxic to natural enemies are used, or where the timing of insecticide use is such that mortality to natural enemies is minimal. Similarly, research should be supported that advances the use of biological-control agents in areas and habitats where insecticide use can be severely restricted or eliminated. Areas for study could include riparian habitats, watershed areas, wetlands, and urban and suburban green areas (Category 2). 3.16 Control strategies should be pursued that limit the use of insecticides to sustainable formulations that are minimally incompatible with ecologically based approaches to pest management. A premium should be set on minimizing the negative consequences of pesticide use for human health and environmental quality. 3.17 Research should assess the economic feasibility of specific chemical control strategies and develop decision and cost models to guide growers in setting up chemical control methods for GWSS (Category 1).

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California Agricultural Research Priorities Pierce’s Disease 4.1 A systematic analysis of Xf pathogenicity should be accomplished with a combination of biochemical, genetic, and genomic analyses. Such research lends itself to a collaborative approach (Category 2). 4.2 As with the pathogen, systematic and global approaches to address host plant responses (disease or defense) to pathogen invasion are essential to identify important plant defense factors. However, until the sequence of the grape genome is available and until other tools, such as grapevine mutants for dissection of defense responses, are available, that approach should be viewed as a long-term and expensive effort (Category 3). 4.3 Host plant resistance to Xf, whether quantitative or qualitative, is important to long-term management of the disease. Immediate emphasis should be placed on identification and characterization of the genetic basis for resistance to Xf in host plants. Characterization of the genetic loci and biochemical mechanisms responsible for resistance will facilitate classical approaches (which use molecular markers) and transgenic breeding to create Xf-resistant plants (Category 2). 4.4 Improvements in tissue transformation systems and in the ability to regenerate plants from transformed tissue have made transgenic technology increasingly feasible, although the availability of genes of known function that could be introduced to target desired effects is limited. In the longterm, however, transgenic technology could hold promise for improving resistance to Xf (Category 2). 4.5 Long-term projects should focus on identification of pathogen targets for existing or novel chemical control approaches for means to stimulate or alter host defense response pathways (Category 2). 4.6 Research should determine the efficacy and the economic and environmental feasibility of manipulating alternative hosts for PD management (Category 2). 5.1 Research should be done on the transmission biology of the disease system, including acquisition from and inoculation to alternative hosts and acquisition from and inoculation to dormant grapevines (Category 2). 5.2 Research should be done on the determinants of transmission efficiency, including attachment and reproduction of Xf in GWSS (Category 2). 5.3 A subset of studies of the vector should explore the effects of Xf on vector survivorship, fecundity, and population growth rates (Category 2). 5.4 A subset of studies of the vector should explore the effects of Xf on vector behavior, including movement and attraction to infected hosts (Category 2).

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California Agricultural Research Priorities Pierce’s Disease Category 4 Research Chapter 4: With existing chemistries and approaches, chemical control of Xf is not promising for short- term disease management. However, the identification of new targets in the bacteria for which highly specific chemicals could be developed has not been explored. Chapter 4: Biological control of bacterial pathogens of plants’ vascular systems, particularly in perennial crops, has generally shown limited success. Naturally occurring endophytes or attenuated strains of Xf have not been effective in control of PD. However, better understanding of Xf and of the endophyte genes required for colonization, establishment, and virulence or antagonism through genome analysis could identify target genes that would allow development of effective biological-control agents. Chapter 5: It might be useful to consider the possibility of interference between two strains of Xf within the vector. Although that research is interesting from a biological perspective, the committee concluded that biological control of bacterial vascular pathogens, particularly in perennial crops, has generally shown little practical success. Chapter 5: Genetic engineering bacterial symbionts of vectors to express and release transgene products that can damage the pathogen (paratransgenesis) would clearly be a very long-term strategy for managing PD, and one in which the likelihood of success is limited. Research Lacking Sufficient Data to Categorize Chapter 3: Several research options could not be categorized because information associated with the techniques in the context of PD is so preliminary. They include the use of biological-control agents other than parasitoids, insect growth regulators, biorational insecticides, mating disruption, behavior-modifying chemicals, sterile male technique, and mass trapping using a compound from a living organism.

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California Agricultural Research Priorities Pierce’s Disease BOX ES-1 Framework for Evaluating Research and Management Strategies Category 1 The research holds reasonable promise of generating successful tools for short-term or long-term management of PD–GWSS. Category 2 The approach looks promising but either because of insufficient data or because of inconclusive results, it is difficult to predict whether it will lead to successful applications for management. Category 3 The research can produce data and results that show promise for successful management of PD–GWSS, but because of complexity and the technology required, the work will be prohibitively expensive for any one funding source to manage. Category 4 The approach does not show promise even in the long term for PD–GWSS management. Research also should be evaluated for its long-term sustainability and for nonscientific barriers to implementation.

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