3
Host–Vector Interaction

Insect–plant interactions can range from associations that are highly detrimental to herbivores to those in which herbivores overexploit their plant hosts. In this chapter, the Committee on California Agricultural Research Priorities: Pierces’ Disease explores the naturally occurring mechanisms that control the outcome of insect–plant interactions that could be adapted to the management of the damage that attends pest–crop interactions. More specifically, the objective is to explore ways in which the links between the glassy-winged sharpshooter (GWSS), Homalodisca coagulata (Say), and its hosts, particularly its economically important crop hosts, can be eliminated, inhibited, or minimized; that is, to develop management strategies that reduce or impede this vector of the Xylella fastidiosa (Xf) bacterium. If management strategies are to be effective in sustainable pest management schemes they should include a cohesive, complementary, and coordinated set of tactics. Although discussions are provided on a variety of tactics, it is assumed that the overall approach to the resolution of the problem will involve implementation of an ecologically based pest management program.

Ecologically based pest management (EBPM) is “the release of living predatory, parasitic, pathogenic, or antagonistic organisms (biological control organisms), the deployment of biologically derived products, such as toxins or semiochemicals (biological control products), and the planting of resistant crop varieties (resistant plants)” (NRC, 1996). Thus, EBPM includes approaches that go beyond traditional biological control––the intentional use or manipulation of predators, parasitoids, pathogens, antagonists, or competitors (Van Driesche and Bellows 1996)––to control insects, weeds, or diseases. EBPM has been defined or described by a variety of names including biointensive integrated pest



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California Agricultural Research Priorities Pierce’s Disease 3 Host–Vector Interaction Insect–plant interactions can range from associations that are highly detrimental to herbivores to those in which herbivores overexploit their plant hosts. In this chapter, the Committee on California Agricultural Research Priorities: Pierces’ Disease explores the naturally occurring mechanisms that control the outcome of insect–plant interactions that could be adapted to the management of the damage that attends pest–crop interactions. More specifically, the objective is to explore ways in which the links between the glassy-winged sharpshooter (GWSS), Homalodisca coagulata (Say), and its hosts, particularly its economically important crop hosts, can be eliminated, inhibited, or minimized; that is, to develop management strategies that reduce or impede this vector of the Xylella fastidiosa (Xf) bacterium. If management strategies are to be effective in sustainable pest management schemes they should include a cohesive, complementary, and coordinated set of tactics. Although discussions are provided on a variety of tactics, it is assumed that the overall approach to the resolution of the problem will involve implementation of an ecologically based pest management program. Ecologically based pest management (EBPM) is “the release of living predatory, parasitic, pathogenic, or antagonistic organisms (biological control organisms), the deployment of biologically derived products, such as toxins or semiochemicals (biological control products), and the planting of resistant crop varieties (resistant plants)” (NRC, 1996). Thus, EBPM includes approaches that go beyond traditional biological control––the intentional use or manipulation of predators, parasitoids, pathogens, antagonists, or competitors (Van Driesche and Bellows 1996)––to control insects, weeds, or diseases. EBPM has been defined or described by a variety of names including biointensive integrated pest

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California Agricultural Research Priorities Pierce’s Disease management (IPM) and biorational IPM. EBPM is an IPM scheme that considers all possible management options and tactics that are complementary, effective, and sustainable with regard to the management of a pest and the quality of the environment. To be effective, EBPM tactics or agents might require environmental conditions that do not exist in agroecosystems. Reestablishing those conditions could require specific inputs or modifications of management tactics. EBPM typically requires more intensive management and planning and a fundamental knowledge of interactions among crops, pests, natural enemies, and the environment—requiring more time and record keeping. Some EBPM practices (such as augmentation biological control) could require an infrastructure that facilitates rearing, storage, and distribution of natural enemies (Neuenschwander et al., 1989). Unlike strategies that rely solely on the use of insecticides, most EBPM is either specific to a pest or nontoxic, so it is less likely to damage the environment. Although many natural enemies can be susceptible to insecticides used against target pests, the judicious use of selective or specific types of insecticides typically has been considered an important component of integrated or EBPM schemes. Because most EBPM practices do not result in toxicity or pathogenicity to mammals, particularly in comparison to the use of conventional pesticides, they are more acceptable in terms of public health and environmental safety. Furthermore, insect pests are less likely to develop resistance to biological agents or to ecologically based controls. If resistance does develop, it is likely to occur significantly more slowly than would be occasioned by the conventional use of pesticides. Nevertheless, EBPM could pose risks, as do most environmental manipulations. TACTICS AND STRATEGIES FOR ECOLOGICALLY BASED PEST MANAGEMENT Ecologically based pest management can involve the use of living natural enemies (biological-control organisms), resistant crop varieties, or any product derived from those and other organisms. The tactics are deployed in any fashion that enhances their effectiveness and sustainable use against pest species. Those tactics and management approaches include the following: host plant resistance (through conventional breeding or genetic modification) vegetation management (in- or off-crop field refuges, trap crops, alteration of refuge vegetation, plant barriers) traditional biological control (classical, augmentation, conservation) sterile male technique mass trapping using a compound derived from a living organism direct use of chemical agents (synthetic toxins, biorational insecticides, behavior-modifying chemicals, insect growth regulators) pheromone use and mating disruption

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California Agricultural Research Priorities Pierce’s Disease Although not all of those tactics are ready for implementation in the control of GWSS and Pierces disease, the tactics that could be used are reviewed below. HOST PLANT RESISTANCE Host plant resistance (HPR) is an important EBPM tool for minimizing crop damage caused by insect pests and diseases because it makes plants less suitable for or more tolerant of the pest. HPR has a long history of success in grape crops for management of phylloxera, grape leafhoppers, and various diseases (e.g., Granett et al., 1996; Jermini et al., 1996, Martinson and Dennehy, 1995; Walker, et al., 1994). HPR can be developed in three ways. Biosassays or direct observation in the field of apparent resistance or tolerance to a pest can be used to identify plant material for propagation. This has been the main approach to developing pest-resistant grapes because vegetative propagation is the norm, sexual reproduction delays the opportunity to perform crosses, and the value of the crop is directly related to its genetic pedigree (interspecific hybrids are not favored). Collecting and propagating resistant material can provide the quickest route to HPR, but the bases of resistance might not be known and resistance breakdown is common. HPR also can be developed from resistant or partially resistant plant material through standard breeding (crosses) if the plant’s biology is compatible (early sexual reproduction, outcrossing, compatible genotypes, inheritance relatively simple). The third way to develop HPR is to modify plant traits using direct molecular manipulation. Genetically transformed or genetically modified (GM) plants express naturally occurring resistance traits, but to different degrees or in different combinations than found normally, or they might express entirely novel traits (the protein toxins of Bacillus thuringiensis are an example). There is considerable debate about the risks, costs, and benefits of such approaches, especially for application in food crops. Resistance phenotypes can sometimes be manipulated through cultivation practices, such as fertilization. No matter how HPR to a given pest is developed, it is subject to periodic, repeated breakdown as a result of pest evolution or the introduction of new pest species or genotypes (e.g., Granett et al., 1996). HPR as a management tactic requires constant evaluation and modification for sustainability. Although constant searches for new plant material or germplasm could remain part of this process, common sense suggests that understanding the plant traits that do or can confer resistance would greatly accelerate HPR development. Successful HPR use in EBPM requires a detailed understanding of how the pest exploits the plant and how plant traits interfere with pests.

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California Agricultural Research Priorities Pierce’s Disease Plant-Herbivore Interactions and Host Plant Resistance Insects have been consuming plants for 500 million years, and during that time diverse interactions between the two groups have evolved. As far as the committee knows, all plant species and all possible plant tissues are exploited as food, shelter, or reproductive sites by insects. Insect diets range from extremely narrow (limited to a particular tissue on a particular plant species) to very broad (feeding successfully on many plant species from several plant families). A striking feature of insects as herbivores is that relatively narrow diets (a single or a few plant species) are more common than are broader diets. Diet breadth is evolutionarily fixed; insects usually cannot broaden or narrow their diets during a lifetime, and often require significant genetic change (evolution) to switch or add host species to their diets. Identifying the proximate and ultimate factors that determine the structure of insect diets is an active area of in plant-herbivore research, and it is safe to say that a complex picture is emerging. Many factors can act as barriers to plant exploitation and thus are thought to influence the evolution and expression of insect host range. Plant chemistry is a crucial barrier to plant use and is thought to be an important influence on insect's host ranges. Plants are generally suboptimal food either because they contain low concentrations of critical nutrients such as nitrogen or protein or because they produce chemicals (allelochemicals or secondary metabolites) that deter feeding, inhibit digestion, or are toxic to the insect. Insects have developed specific adaptations that permit specialization on hosts that have particular chemistries, Those adaptations include the ability to avoid toxic tissues and a variety of biochemical traits that counter the negative effects of plant chemistry. Plant quality also can have indirect effects on herbivorous insects. Insect susceptibility to parasites, predators, disease, and insecticides has been shown to be influenced by the host plant (Wright and Verkerk, 1995). Nonlethal effects on fitness (those that reduce fecundity, for example) could influence insect population growth. It is likely that most aspects of insect performance are influenced by diet quality and that plant chemistry is a central factor in limiting consumption by insects. Although research on the effects of plant chemistry on insect herbivores originally focused on constitutive traits (those that are present constantly and encountered by an insect when it first goes to the plant), studies over the past two decades have shown that changes in plant chemistry that are induced by the feeding insects are at least as important (Karban and Baldwin, 1997). All plants so far studied alter the concentrations or composition of allelochemicals when attacked, sometimes in an insect-specific fashion. Those changes can reduce diet quality or enhance toxicity or deterrence in a matter of minutes or hours. Related changes are elicited in plants by pathogen attack, and there is evidence that the suitability of plants for insects could be influenced by plant responses to pathogenic and symbiotic microbes (Bostock, 1999). Most plants also emit volatile substances that attract the enemies of insect herbivores (parasitoids, predators) and could cue defense responses in

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California Agricultural Research Priorities Pierce’s Disease nearby plants (Dicke and Bruin, 2001). Those indirect effects on insect herbivores could be more influential in protecting plants from insects than are the more direct constitutive or inducible defense traits (Karban and Baldwin, 1997). Volatile substances also could have a direct effect by repelling or poisoning sessile, sucking insects such as aphids (Birkett et al., 2000). Recent research indicates that plants also emit complex volatile mixtures when they are attacked by microbes (J. Huang et al., 2003); one study suggests that such pathogen-elicited emissions could have an effect on insect vectors of plant diseases (Eigenbrode et al., 2002). Although the nutrient (protein, carbohydrate, fat, mineral) composition of plant tissues often is suboptimal for insect growth, it is assumed that all insects experience similar selection on their ability to extract sufficient nutrition from plants. Together with the need of plants to produce a minimal nutrient mix for their own functioning, the nutritional content of plants is rarely cited to explain evolution of insect host range. However, nutrition does shape insect adaptation and diet. It is true that even extremely nutrient-poor plant tissues are consumed by some insects, the insects that do so generally are limited to those tissues, presumably because adaptation comes at the cost of restricting the ability to use better tissues. The most germane example to the PD situation involves insects that feed on xylem, which generally is thought to contain extremely low concentrations of usable nutrients. Xylem also lacks or contains very low concentrations of allelochemicals (Rosenheim et al., 1996). Xylem-feeding insects usually consume large quantities to extract the limited nutrition (Brodbeck et al., 1993), and they generally cannot exploit other plant tissues, partly because of their specialized mouthparts, but also because they presumably are not adapted to the higher allelochemical concentrations found in more nutrient-rich portions of a plant. There are fewer examples of insect adaptation to physical deterrents. Plant tissue toughness is a trait that some insects have overcome in ways that sometimes lead to restrictions in host use (e.g., Howard and Giblin Davis, 1997). Surface hairs and trichomes can combine to form to form a physical and chemical barrier, particularly to small insects. The physical structure of some plants can offer unique opportunities for insects to escape predators or parasites, although the degree to which this influences the evolution of diet is debatable (Mira and Bernays, 2002; Scheirs and De Bruyn, 2002; Zangerl et al., 2002). It is generally easier to understand insect adaptation to plants and the reasons for using particular plant species on the basis of chemistry than it is to explain the adaptation on the basis of adjustment to the physical traits of the host plant. Insects do not always use the same plant species for food, shelter, and reproduction, so noncrop, alternative hosts might exert HPR-based effects on crop pests. There is long-standing controversy about the degree to which plant suitability for feeding adults is linked to suitability for offspring placed there (Wiklund, 1975). Plant traits that influence feeding might or might not be the same traits that influence oviposition or mating behaviors. When more than one plant species is exploited during the life cycle of an insect, each plant and its traits can make separate, significant contributions to the insect’s success.

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California Agricultural Research Priorities Pierce’s Disease Insect herbivores can become agricultural pests when conditions permit them to consume or destroy an economically significant fraction of the agricultural product. There are several HPR-based causes of this outcome. One is the tendency to eliminate chemical (or physical) deterrents from food products, because they can be distasteful or toxic to human consumers as well. Another is to bring plant and insect species together for the first time. A lack of coevolutionary history could mean that the plant has no viable defenses against a newly encountered insect. Because insect adaptation to host plants is continuous, uniform populations of crop plants that express the same resistance traits favor the rapid evolution of insects to overcome those traits. For this reason, and because ecosystem complexity itself interferes with finding and exploiting host plants, the simplification inherent to modern agriculture also contributes to the development of insect pest problems. Sharpshooters and Their Host Plants Sharpshooters Are Xylem-Feeding Leafhoppers Sharpshooters comprise a taxonomic subset of a family of insects (Cicadellidae) in the order Homoptera collectively called leafhoppers. All leafhoppers have piercing–sucking mouthparts, and they consume liquid from plants. Some species puncture individual cells or groups of cells, for example, the leaves; others penetrate xylem cells and consume the materials there. Sharpshooters are primarily xylem feeders, although some recent unpublished work suggests that they occasionally feed on cells that surround the xylem. Sharpshooters and other xylem-feeding leafhoppers have powerful cibarial pumps for extracting xylem contents (which are under negative pressure), and they consume large quantities of fluid, presumably to compensate for the low nutrient concentrations in xylem. There is some uncertainty about where on an individual plant sharpshooters prefer to feed. It is clear that tissues surrounding the xylem, a site of lignification, can become too tough for leafhoppers to penetrate; young tissues would be suggested as preferred feeding sites. Like many leafhoppers, sharpshooters, temporarily or permanently harbor microbes. They have a diverse assemblage of obligate symbiotic bacteria, the function of which is unknown (Moran et al., 2003). And of course, the plant-pathogenic bacteria they carry can be transmitted from plant to plant. There has been little work on host plant's influences on essential symbiotic microbes in insects or of plant responses to entomosymbionts. Sharpshooters Have a Broad Host Range All of the sharpshooter species involved in transmitting Xf appear at first to have large host ranges. They have been associated with many plant

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California Agricultural Research Priorities Pierce’s Disease species—native and introduced—including many that grow adjacent to vineyards. This could be important because Xf can be acquired from other plant species and transmitted to grape or citrus and because the abundance and fitness of the insect vector could be influenced by the availability of suitable host plants. The insect’s association with a plant species could mean that it feeds there, reproduces there, or both. There are examples of both types of association with various host plants, but the committee does not have a comprehensive picture of the associations between any of the Xf-transmitting sharpshooters and the host plant communities in their habitats. Indeed, the degree to which any of the sharpshooters actually feed, grow, or reproduce on the locally available plants has been established for relatively few plant species, and not always for plants found in or near California’s vineyards (Brodbeck et al., 1995). The literature evidences some confusion about which plants are suitable or preferred (Purcell, 1976, 1981; Purcell and Frazier, 1985), and the literature on host plant associations of insect herbivores is notoriously unreliable. An association is often assumed when an insect is found on a plant, although that says nothing about the insect’s performance or preferences. The concept of preference should comprise a quantitative measure of active choice (among equally available alternatives), of choice and performance (growth, reproduction), or at least of abundance on a plant in relation to that plant’s availability. None of those approaches appears to have been taken. Much of what is known about sharpshooters’ use of hosts consists of singular, isolated observations, often of a single insect on a plant. Despite numerous studies in which sharpshooters have been trapped as they move among or within crops and other communities (e.g., Blua et al., 2001), the degree to which the sharpshooters prefer grape or find it suitable for growth or reproduction compared with surrounding vegetation lacks quantitative confirmation. Factors Influencing Sharpshooter Plant Use To employ HPR, it is necessary to know what plant traits determine the pest's use of a plant. Few if any of the usual factors thought to influence host plant use have been investigated as barriers to sharpshooter feeding or oviposition on any plant species. There has been little work of this kind on xylem feeders in general, probably because of the difficulty in acquiring and analyzing xylem contents. Studies tend to focus on nutritional chemistry and mostly ignore putative defenses (allelochemicals; Brodbeck et al., 1990,1993,1995,1999; Ponder et al., 2002). Published work links sharpshooter growth to amino acid content and balance in xylem of Glycine max, Lagerstroemia indica and Euonymus japonica, a Vitis hybrid, and Catharanthus roseus (Andersen et al., 1992; Brodbeck et al., 1990,1993,1995,1999). Growth and selection of host plants by another leafhopper, Carneocephala floridana (Ball), was influenced by plant fertilization (Rossi et al., 1996). Grafting on rootstocks that alter xylem amino acid content can influence sharpshooter feeding and growth (Gould et al., 1991) but recent unpublished work failed to

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California Agricultural Research Priorities Pierce’s Disease show similar differences in Vitis grafts. Compensatory feeding can confuse interpretation of results in studies like these: Insects can appear to consume more of an unsuitable plant to compensate for its low quality nutrition. If Xf transmission by sharpshooters is linked to time spent feeding, low-quality plants (from the insect’s point of view) could be more likely to become inoculated. The assumption that sharpshooters can exploit many plant species makes evolutionary sense if the assertion that biochemical challenges (such as defenses) in xylem are few, because host specificity often is assumed to be a product of adaptation to plant exploitation barriers (for example., biochemical defenses, above). Xylem-feeding leafhoppers appear to have adapted to the low nutrient concentrations typical of most xylem, and if there are no other chemical influences, one plant’s xylem thus could be as suitable as another’s. Some xylem-feeding leafhoppers do exhibit relatively low activity of enzymatic detoxification systems and comparatively high susceptibility to chemical pesticides, an observation taken to indicate that they do not typically encounter substances that cause toxic reactions (Rosenheim et al., 1996). Despite the attractiveness of this logic, there are few studies of xylem chemistry or xylem-feeding leafhopper performance to support it. It could be that physical toughness, not chemistry, is the major barrier to leafhopper feeding (Brewer et al., 1986). But the observations that sharpshooters apparently avoid or perform differently on various plant species (Brodbeck et al., 1992, 1995; Purcell and Frazier, 1985) and that various plant species exhibit genotypic resistance to xylem-feeding and other leafhoppers (Elden and Lambert, 1992; Kornegay et al., 1989; Martinson and Dennehy, 1995; Sanford et al., 1990; Tingey and Laubengayer, 1981) suggest that plant traits do influence sharpshooter attack. Leafhoppers must locate plants or suitable habitats from a distance, determine a plant’s suitability, upon contact, penetrate tissues to get to the xylem, and grow and reproduce adequately as a result of feeding on the xylem. Plant odors, the taste and texture of tissues superficial to xylem, xylem toughness and xylem allelochemistry could produce the observed preferences and hence could be employed in HPR strategies. None of those possibilities has been investigated in any systematic way for Xf-transmitting sharpshooters, although trichomes have been found to constitute barriers to feeding by leafhoppers in several plant species (Elden and Lambert, 1992; Shockley and Backus, 2002; Tingey and Laubengayer, 1981) as has xylem lignification toughness (Brewer et al., 1986). Plant xylem can include allelochemicals and can express enzyme activity that could influence sharpshooters and provide bases for HPR in grapes. In other plants, alkaloids and other allelochemicals that are toxic to leafhoppers (Sanford et al., 1996) and synthesized in roots are translocated to shoots and leaves in xylem, often in response to aboveground insect attack (Baldwin et al., 1994). Phytoalexins have been found in xylem of several plant species (Kragh et al., 1995; Resende et al., 1996). Xylem of some plants contains phenolics and oxidative enzymes (e.g., Kpemoua et al., 1996; Young et al., 1995). Many authors assume that the presence of those compounds is related to xylem lignification (Kpemoua et al., 1996), but phenolics can be toxic; inhibit enzymes (including digestive enzymes); and could bind to cations, proteins, and amino

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California Agricultural Research Priorities Pierce’s Disease acids, especially when activated by peroxidases or other enzymes (Appel, 1993; Morales and Ros-Barcelo, 1997). Phenolic production and activities of oxidizing enzymes can be induced by insect signals (Kruzmane et al., 2002) and could be elevated during pathogen infection in xylem (Kpemoua et al., 1996; Young et al., 1995). Peroxidase activity and phenolic accumulation have been associated with the stylets of feeding insects as they penetrate the plant (Crews et al., 1998) and oxidized allelochemicals form a basis of resistance to leafhoppers in corn (Dowd and Vega, 1996). The discovery of proteases in the saliva of other xylem feeders (Foissac et al., 2002) and unpublished work finding the same in sharpshooters suggests that digestive activity (not just uptake) could occur and could be inhibited by xylem chemistry. Recent work in grapes suggests that rootstock identity—which one might expect to influence xylem chemistry—has little or no effect on aboveground sharpshooter feeding. The xylem chemistry arising from various grafts in Vitis has not been examined. A promising form of HPR that is consistent with EBPM and IPM is the emission of volatile compounds that attract pest-consuming predators and parasites. There are no studies of grape plant (or other host plant) volatile substances on sharpshooters or their parasitoids, despite the indication that grape leaves produce ample volatile signals when they are wounded by insects (Loughrin et al., 1996, 1997) and that some leafhoppers are responsive to leaf volatiles in other plant species (Saxena and Basit, 1982; Shockley and Backus, 2002; Todd et al., 1990). Recent studies suggest that plants infected by insect-vectored pathogens emit volatile substances that attract the insect vectors (Eigenbrode et al., 2002). There are no studies of the effect of Xf (or other pathogens) on sharpshooter host plant use, or vice versa. HPR has been developed against several pests in wine grapes, largely by trial and error, by locating apparently resistant material in the field. Vines that are apparently resistant to Xf or sharpshooters and also compatible with producing high-quality wine have not yet been identified by this method. Identifying resistant plants and useful HPR traits would be accelerated and enhanced by understanding how plant and pest interact. A library of phenotypic and genetic resistance traits is needed for effective use of HPR, but few resistance traits have been identified because too little is known about how the insects and plants interact. Although each of the Xf-transmitting sharpshooter species can be found on and could feed on a large number of plant species, the insects’ preferences for those plants and the suitability of various plants and plant tissues for insect performance have not been determined. It is evident that transmission of Xf to grapevines is linked to insect and disease presence in surrounding vegetation, so it is important to identify with confidence the relative importance of individual plant species in the system. All plants express heritable, phenotypically plastic “defense” traits thought or known to influence their susceptibility to insects. Sharpshooters and their hosts should be no exception, and the fact that some plants clearly seem unacceptable to them supports this view. Comparisons of plant species’ suitability can provide rough clues about important resistance traits, but similar

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California Agricultural Research Priorities Pierce’s Disease comparisons must be made within plant species, because intraspecific variation in resistance provides the raw material for developing resistant plants. And there is informal evidence that such variation exists in Vitis vinifera. But because the basic studies of factors that could influence plant suitability have not been done for sharpshooters, it is difficult if not impossible to guess what sort of plant traits might be useful in developing resistant cultivars or grafts, or in instituting cultivation practices to maximize plant resistance. Recommendation 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). Recommendation 3.2. All the modern chemical, molecular, ecological, and statistical tools available to scientists should be used to identify the mechanistic bases of grapevine resistance to xylem-feeding leafhoppers. Studies should be done in the ecosystem context and consider multitrophic interactions among plants, insect pests, and natural enemies (predators and parasites), and they should include insect- and Xf-induced changes in plant quality (Category 2). Recommendation 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 deployment. The methods should allow work with genetically transformed plant material, use of chemical or other elicitors, and cultivation practices (Category 2). MANAGEMENT OF VEGETATION Research on plant resistance to insect feeding is complementary to studies of how crop and noncrop components of an agricultural landscape influence the population dynamics and movement of herbivorous insects that attack crops (Gurr et al., 2003) and, if the insects are vectors of plant pathogens, to studies of the epidemiology of those pathogens (A.G. Power, 1990). 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 (Wisler and Duffus, 2000). Insects and pathogens respond to vegetation structure and diversity both inside the agroecosystem itself and in the surrounding landscape.

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California Agricultural Research Priorities Pierce’s Disease Vegetation Management within the Cropping System Although the response of individual herbivores to particular cropping patterns varies, crop diversification within an agroecosystem often leads to reductions in herbivorous insect populations (for reviews, see Andow, 1991; Tonhasca and Byrne, 1994; Hooks and Johnson, 2003) and in the pathogens that they transmit to plants (A.G. Power, 1990). The effect of increasing diversity can result either from “bottom up” effects (the effects of the host plants themselves on herbivore population dynamics and behavior) or from “topdown” effects (enhancement of natural enemy populations or behavior). That range of processes which might explain lower herbivore abundance in diverse systems, was first described by R. B. Root (1973) when he posed the resource concentration hypothesis and the enemies hypothesis. The first predicts that herbivores, particularly specialists, in pure, dense host plant stands will be more likely to find their hosts and more likely to survive and reproduce. In contrast, herbivores in less dense or more host-plant-diverse stands should be less likely to find their hosts and more likely to lose them. Although the details of herbivore–host interactions vary considerably, subsequent experimental tests of this hypothesis generally have supported it with respect to the effects of diversity, especially for specialist herbivores. Host-finding behavior and insect colonization and emigration appear to be important in the response of herbivorous insects to agroecosystems. Densities of specialists could be lower in diverse systems because they have difficulty locating hosts, because of interference with olfactory or visual cues; or because they leave hosts more often because of lower plant quality and then have difficulty relocating the hosts. Those behaviors are significantly affected by the chemical, nutritional, and structural diversity that accompanies crop diversity. Although the predicted effects of plant diversity on insect herbivores with narrow host ranges are reasonably straightforward, predictions for herbivores with broad host ranges are less clear. The determining factors for insect response are the distribution of host and nonhost plants in the system and the preferences of the herbivore. The expectation of lower abundance in diverse systems attributable to effects on host finding and “host losing” (Kareiva, 1985) is predicated on the existence of nonhost or nonpreferred plants in the system. The enemies hypothesis predicts that the diverse systems will have higher densities of herbivore natural enemies (predators and parasites) because they provide more resources for those natural enemies, such as alternative prey or hosts, nectar, pollen, and refuge. The hypothesis also has largely been supported in experimental studies, particularly for parasitoids (Andow 1991; Russell, 1989). Compared with monocultures, diverse systems are likely to have higher rates of predation, higher rates of parasitism, and higher ratios of natural enemies to herbivores, all of which can contribute to lower pest densities of specialist and generalist herbivores.

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California Agricultural Research Priorities Pierce’s Disease native parasitoids are species that occur in affected areas but have not provided the necessary amount of control, enhancing their effectiveness is likely to depend on the development of conservation strategies that improve their habitat and provide missing or limited requisites. The habitats to which they are introduced might not be optimal for the natural enemies’ survival and effectiveness and thus, where possible, those conditions should be altered or manipulated to conserve natural enemies, through provision of sugar or nectar sources for adult natural enemies, introduction of alternate hosts or prey, or maintenance of a toxin-free habitat, for example. Similarly, any manipulation, including alterations in viticulture practices, that enhances overwintering survival of natural enemies can be important, particularly because mortality imposed by parasitoids in the spring generation of the GWSS appears to be lower than in summer. Nevertheless, the rigorous experimental confirmation of the importance of such manipulations in agroecosytems has only recently been undertaken, and if manipulations are found to be practical for that agroecosystem, they too should be evaluated experimentally. Environmental Impact of Biological Control Many of the consequences of EBPM are unknown. The use of introduced natural enemies, sterile insects, microbial pesticides, and pheromones has sometimes directly or indirectly affected not only the targeted pest species but nontarget plants or other insects. The release of biological-control agents raises ecological concerns, particularly when natural enemies have relatively broad host ranges, as do many of the parasitoids being considered for the use against the GWSS (Triaptisyn et al., 2003). Because many of the parasitoids will parasitize the eggs of other leafhoppers (in the tribes Proconiini, Athysaniini, and others), the effect on leafhopper biodiversity is a valid area of concern that merits investigation. However, important risks also are associated with the failure to control the pests. Thus, concern about the consequences of releasing natural enemies must be balanced against the effect of outbreak levels of GWSS on leafhopper biodiversity or in biodiversity in general. A pest species such as GWSS, which, in California, is a nonindigenous disease vector with a broad hostplant range, can significantly alter unmanaged native ecosystems. The use of introduced biological-control agents has provided significant benefits and fewer risks than have most other control tactics and approaches, although the environmental consequences of biological control are still the subject of considerable debate (Howarth, 1991; Wajnberg et al., 2001). Human exposure to agents or products used in EBPM can occur at many stages of the production and release of natural enemies. Employees of the facilities in which natural enemies are reared can be exposed to the organisms or to materials used in their rearing. Farm personnel and residents of nearby communities also risk exposure. Although perhaps unlikely, consumers might unknowingly consume microbial pesticides or fragments of arthropod natural enemies in foods. Despite that, few human health effects—with the exception of

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California Agricultural Research Priorities Pierce’s Disease allergic reactions—or risks attributable to EBPM agents or products have been reported in the literature. Health concerns arise more often from the use of microbial pesticides. OTHER OPTIONS The recommended incorporation of some tactics and approaches into an EBPM scheme does not mean that other tactics will not be shown to be effective as more research is done. However, available information on leafhoppers in general and on GWSS and its host plants in particular, suggests that the potential of some approaches to the management of the PD–GWSS is highly questionable. In some cases, the absence of data makes an approach impossible to evaluate. Insect Growth Regulators Formulations of chitin inhibitors that affect an insect’s ability to develop from one instart to the next have been evaluated. Buprofezin, diflubenzuron and benzoylphenyl were evaluated by Akey and colleagues (2002), and Toscano and colleagues (2002) have studied buprofezin and pyriproxyfen. The chitin inhibitors are applied using standard air blast field sprayers. Akey and colleagues reported that buprofezin controlled eggs and nymphs at a rate of 90–100%, and produced 70% control of adults. Diflubenzuron was nearly as effective, and benzoylphenyl was less effective than the other two inhibitors. Toscano and colleagues reported that buprofezin was effective against first-instar GWSS but that higher doses were required to control third and fourth instars. Pyriproxyfen was effective against GWSS eggs but not against nymphs (Toscano et al., 2003). The effects of chitin inhibitors on beneficial insects were not reported. One or two formulations that restrain development of chitin have been reported to be effective in preventing nymphs from advancing to the adult stage. Because the nymphs tend to reside on the underside of leaves to avoid predators some new application technology would be required to deposit the spray on those surfaces. Charging fine spray particles can enhance such deposition. However, there are still questions to answer about the amounts of inhibitors required for field control and about the means of application. Biorational Insecticides Sugar esters, insecticidal soap and neem oil derivatives constitute a new class of insecticides that is being evaluated by organic growers for GWSS control. In one study, sucrose octoanate, sorbitol octoanate, and insecticidal soap were applied with a hand gun sprayer. Several neem derivatives were applied by air blast sprayer. Those materials are being investigated as a means for GWSS

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California Agricultural Research Priorities Pierce’s Disease control that circumvents conventional chemical insecticides. Depending on the rate of application, the sucrose materials produced about 98% adult mortality; the insecticidal soap produced 97% mortality rates (Paterka, 2001). The neem derivatives resulted in 33–48% mortality of eggs, 62–78% in nymphs, and 16–50% in adults (Akey, et al., 2002). All of those biorational insecticides are nontoxic to humans and believed to be environmentally neutral. Research results for biotrational insecticides indicate acceptable control provided by sugar esters and possibly by insecticidal soaps. This is a recent area of research and additional studies would be useful to more clearly develop the application process for such materials. Important questions must be answered: What amounts of these materials should be applied? Do any of them harm beneficial insects? Biological-Control Agents other than Parasitoids Biological-control agents of equal or greater effectiveness, such as entomopathogenic fungi, predators, and parasites, could still be developed. The use of entomopathogens such as Hirsutella, a fungus that is known in the southeastern United States to affect sharpshooters, is being explored. However, abiotic constraints, including the need for high humidity, can hamper the use of fungi in many agroecosystems (Soper, 1985). Other options will require considerable basic and applied level research. For example, many of the potentially useful GWSS predators are generalists, and although some of those species have been identified, not all are known. The species that actively feed on GWSS would need to be identified, but more important, their influence on the survival and numerical increase of GWSS would need to be determined. Although many management innovations have resulted from similar research and thus should be encouraged and funded, generalist natural enemies could dramatically affect other indigenous species so it will be important also to study their ecological consequences. Mating Disruption It is not currently practical to use pheromones to cause GWSS mating disruption as part of an EBPM strategy. Although sex pheromones have been used to manage other pests, there is no empirical evidence of pheromone-mediated sexual communication in leafhoppers. Available evidence suggests that mating in most leafhoppers, including species that vector plant pathogens (Claridge, 1985) is mediated by substrate-borne vibrations (R. E. Hunt et al., 1992; R. H. Hunt and Morton, 2001).

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California Agricultural Research Priorities Pierce’s Disease Behavior-Modifying Chemicals Relatively little is known about the host plant chemical compounds that influence the way pest insects find them, begin to feed on them, or initiate other behaviors. The use of behavior-modifying chemicals as attractant lures or repellant sprays is unlikely to result in the effective control of PD–GWSS. As plant and other influences on GWSS host preferences are uncovered, compounds might be identified that could make it practical to use synthesized or natural compounds. Sterile Male Technique The sterile male technique has been used to manage pest insects; such as medflies, tsetse flies, and screwworms. Factory-reared flies that have been sterilized, usually by exposure to gamma radiation, are released into a natural population. The males are expected to mate with feral females, thus inhibiting the females’ ability to reproduce. The approach works only if the females mate once, if the released males are competitive with feral males, and if the number of released males at least matches that of feral males. The use of the sterile male technique has been applied against few pest species, in part because of the technique’s biological and ecological requirements. Substantial financial and infrastructure resources also are required to rear and sterilize the millions of individuals generally required. To achieve control, the total pest population in a region must be targeted. Reinfestation of individuals from adjacent areas often interferes with the technique and thus must be prevented with quarantines, insecticidal sprays, or continued releases of sterile males to create a barrier zone that is wider than the flight range of the insect pest. Research has been insufficient, but at present the sterile male technique does not seem to be a useful approach for GWSS management. Mass Trapping The use of mass trapping generally involves traps that are baited with an attractant chemical derived from a living organism. Traps must be distributed over a large area, in a specific pattern. The traps and chemicals are expensive, however, and the need for formulations that are more attractive than are compounds that occur in the ecosystem and the difficulty with the deployment of traps limit the usefulness of the approach. Because there are not data on the use of this approach to control GWSS, the method is not recommended.

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California Agricultural Research Priorities Pierce’s Disease INSECTICIDES Although studies of EPBM techniques could eventually lead to control of PD, it is probable that several years of study with field verification will be required before they are accepted commercially. Until then, grape growers are faced with an expanding infestation that portends serious economic consequences. Research that addresses the use of chemical or biological pesticides offers the most near-term solution to controlling and possibly eliminating the GWSS population in California vineyards and orchards. Many pesticides can be effective against GWSS eggs, nymphs, and adults (Akey et al., 2002; Toscano and Castle, 2002). GWSS eggs, nymphs, and adults prefer different plants at different stages (Daane and Johnson, 2002). Citrus and grape are highly preferred for egg masses. Oleander and grape are preferred by the nymphs and adults, and adults also favor Agapanthus (African lily). Two peak periods of GWSS egg density on citrus have been identified, one in March and April and the other in July and August (Coviella and Luck, 2003). Coviella and Luck (2003) reported a single peak of nymph activity in May and June and an adult activity in June and July. T. M. Perring and Gispert (2002) reported a peak in adult activity on grape and citrus in June and July. Knowing the preferred locations of eggs, nymphs, and adults and the time of their peak presence can help inform the choice of a control strategy. Several pesticides have been studied for their effectiveness against GWSS at different stages of development. They are discussed by class in the following sections. Systemic Formulations Systemic pesticides act through a plant’s vascular system. Neonicotinoids, for example, are introduced into the plant either through the root system or through the leaf cuticle. The pesticides kill the GWSS nymph or adult as it feeds on the xylem fluids. When applied through drip irrigation, the pesticide is taken up by the root tips and transported through the xylem tissue throughout the plant. It takes about 10 days for the compound to reach all parts of a grapevines and about 6 weeks for a citrus tree to become infused (Toscano and Castle, 2002). When applied as a foliar spray, the pesticide diffuses through cell walls and is ingested by GWSS during feeding. There is some evidence that systemics applied to leaves can be diluted by sprinkler irrigation, so that there is incomplete penetration or diffusion (Grafton-Cardwell, 2002). Applying systemics through drip irrigation systems is an efficient way to treat the whole plant. There would be some loss in the root zone, but worker exposure and drift are minimized. Mortality of 99% of small and large nymphs and 74–79% of adults can be achieved by this method (Akey et al., 2002). Pesticide retention is significant, and data indicate that imidacloprid remains effective in a plant for 1 year (Toscano and Castle, 2002). Foliar application of systemics can be done by aircraft, by air blast sprayers or by hydraulic sprayers. Aircraft spraying is quick, but it results in

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California Agricultural Research Priorities Pierce’s Disease significant drift. Air blast sprayers require a large amount of power, are very inefficient, and produce drift—as much as 256 m after spraying through a canopy in a calm wind (Derksen et al., 2000; Fox et al., 1993). Foliar application of neonicotinoids (where they are translaminar) is effective for a shorter period—3–4 weeks—than is application by drip irrigation, which remains effective for 8–11 weeks (Grafton-Cardwell, 2002). Research comparing the use of air blast spraying with air-assisted electrostatic charging of a fungicide indicated that the dislodgeable foliar residue from grapevines was 68% less with the air blast sprayer, even though the application rate for the electrostatic sprayer was a tenth that of the air blast sprayer (Welsh et al., 2000). This suggests that research should be done to determine whether some of the problems accompanying foliar application of the neonicotinoids can be reduced with a more efficient application technology. Systemic application is better than foliar application because it requires a smaller amount of the substance to achieve the same plant protection—although that needs verification—because worker exposure and drift are minimized. Research on efficient spray application technologies could lead to reduction in drift for spray applications with ground equipment. Several questions about the use of the compounds themselves remain, including the quantification of the efficiency of transport into the plant root system and its persistence in the soil after drip irrigation. There also have been reports that repeated use of neonicotinoids, in this case, Assail causes flare-ups of infestatation by spider mites (Michigan State University, 2002). More serious questions concern the presence of systemic compounds in harvested grapes and their possible consequences for human health. Where systemic pesticides are applied to the surfaces of leaves, what is the role of absorption and adsorption through the cuticle? Their apparently longer term effectiveness warrants intensification of research into the mechanisms of their uptake and movement through the xylem of the plant. More information is needed about their residual presence in the xylem and any effect that might have on grape quality and safety for consumption. Finally, there is some evidence that sprinkler irrigation can dilute or wash out or off systemic formulations. Does this pose a hazard to vineyard workers? When applied by aircraft or air blast sprayers is there a chance that the material will drift into adjacent areas and affect human or animal health? Animal studies have shown neonictinoids are likely to be moderately toxic to humans. They can be highly toxic to birds and bees, although studies show that birds can learn to avoid seeds treated with neonictioids (EXTOXNET, 2004). Nonsystemic Insecticides Pyrethroids, organophosphates, and carbamates generally are effective but for a shorter period than systemic compounds––3–4 weeks compared with almost 3 months after application (Grafton-Cardwell, 2002). Nonsystemic insecticides are commonly applied by air blast sprayers. Where they are used to

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California Agricultural Research Priorities Pierce’s Disease kill GWSS eggs or nymphs it is desirable to place the compound on the underside of the leaves, where the eggs and nymphs reside to avoid predators. Charging small droplets can significantly increase deposition on lower leaf surfaces (Splinter 1968a, b, c). Manufacturers of air-assisted electrostatic sprayers usually recommend application at one-half the rate of active ingredient. There are no reports of spray application equipment used by any of the researchers funded by the PD program other than the air blast sprayers in the sponsored research program reports. Pyrethroids, organophosphates, and carbamates provide close to nearly 100% kill rates for eggs and nymphs and 70%–80% kill rates for adult GWSS (Akey et al., 2002). The are reported to last 2–3 weeks for adults but less than 2 weeks for eggs. Several nonsystemic chemical insecticides have been shown control nymph and adult GWSS, but their effectiveness generally lasts only a few days. In contrast, the systemics show persistence over a growing season. The most effective use of nonsystemic insecticides therefore would be as a rapid response to an invasion of GWSS from adjacent host plants. Most of those chemicals have exposure limits for field workers and dissipation times before human consumption. There is evidence that carabaryl (Sevin) residue can be dissipated with repeated sprinkler irrigation (Grafton-Cardwell, 2002). Some compounds in the organophosphates group are highly toxic; and chlorpyrifos and dimethoate have been found to be moderately toxic to humans (EXTOXNET, 2004) so there is concern about drift into adjacent residential areas, pasture, or croplands. Organophosphates are readily absorbed by humans and can affect the nervous system through the inhibition of acetylcholinesterase (IOM, 2003; Michigan DNR, 2004). In addition to determining the toxic effects of those compounds, research should be done to find ways to reduce the amount applied and minimize drift from the point of application. As with any pesticide, efficient application is essential to minimizing the amount of material applied. Conventional application technology—which used air blast sprayers or aircraft—poses inherent problems with the unintentional drift of toxic substances. Commercial application equipment (Law, 1978) is available that effectively charges fine spray particles. The question of whether the amount of pesticide can be reduced through more efficient application methods—while retaining the desired GWSS control level—could be worth investigating. Inert Materials Finely divided kaolin, marketed as Surround, has been found to repel GWSS nymphs and adults to the extent that they refuse to remain on the plant or to feed (Paterka, 2002; Paterka and Reinke, 2003). A fine coating of this material deters GWSS from settling on treated plants and therefore from oviposition. The material is applied biweekly using air blast sprayers. Kaolin clay has no adverse effects from contact or ingestion.

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California Agricultural Research Priorities Pierce’s Disease However, Grafton-Cardwell and Reagan (2003) found that the kaolin coating also repelled the parasitic wasps Aphystus melinus and Comperiella bifasciata and prevented them from attacking California red scale, an unintended consequence to the use of kaolin in citrus. California red scale is not a problem for grapes. The white coating on the leaves, although harmless, raises esthetic concerns that the clay on the grapes could be visually disconcerting to tourists––a major source of revenue for the vineyards––and could taint wine produced from them. Applying a coating of finely divided kaolin clay has been found to effectively repel both GWSS nymphs and adults. However, the mechanism for this response is poorly understood and the indirect effects (e.g., the impacts on beneficial insects) are also unknown. ECONOMIC CONTROL STRATEGY In the short-term, the management of PD is likely to focus on the control of GWSS by pesticides, despite their hazards. The economic sustainability and effectiveness of pesticide use is closely tied to how, when, and where pesticides are applied in the field. For acceptable economic control of GWSS, and to minimize workers’ exposure to the pesticides a precise amount must be applied at the best time, in the correct locations, and for the lowest cost. The factors involved in understanding how pesticides can be used most cost efficiently represent a good case study for the economic analyses needed for all prospective management tools. Amout of Pesticide Applied Pesticides are chemical formulations that are intended to kill insects or plant pathogens. Their toxicity to humans is always a concern; even sulfur, which has had a long history of use used to control mildew is being challenged because of its possible allergenicity. And there is always the potential for unintended consequences, as is classically illustrated by the effect of dichlorodiphenyl-trichloroethane (DDT) on the eggshells of birds. Even the inert clay kaolin has met resistance because it whitens grape leaves and because of the concern that it could alter wine flavors. All pesticides carry costs of application, and they all have costs of acquisition. Therefore fewer applications are better, but the challenge is to determine the minimum amount that will provide acceptable control. The 2002 volume of the Proceedings of the Pierce’s Disease Research Symposium (CDFA, 2002b) contains reports of several studies that evaluate lethal doses for GWSS in a spectrum of pesticides. The work of Blua and Walker (2002), for example, who investigated sublethal doses of neonicotinoids, provides an excellent regression of dose to mortality. That type of study should lead to a rational basis for setting acceptable rates of application.

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California Agricultural Research Priorities Pierce’s Disease Timeliness of Application The best time to control GWSS is before it reaches the adult stage, when it becomes more mobile and can spread the PD as it feeds. Daane and Johnson (2002) reported significant differences in the locations of eggs, nymphs, and adults on host plants. Citrus, gardenia, grape, and hibiscus were preferred for egg laying; oleander and grape were preferred sites for nymphs. Grape and citrus were the primary host plants for adults. T.M. Perring and Gispert (2002) reported a peak in adult GWSS trap catches in July. If GWSS primarily overwinters as adults, and there appears to be a small population peak in February and March, it would be efficient to schedule a control application with the emergence of the adults at the location of first egg laying on neighboring host plants, such as gardenia and citrus. Grape will be dormant at this time. After the eggs hatch, another application on oleander, hibiscus, and euonymus would target nymphs. Adults should then be targeted in citrus. A second control sequence before the peak in June and July would be indicated, and grapes should be included at this point. Discussions with the research scientists who provided background information to the committee indicate that feeding by GWSS on grapevines after July can infect plants, but that the effect is minimal because the infected stems are pruned. This is reinforced by studies by Coviella and Luck (2003), who reported peaks in egg densities in citrus in March and in August; a peak in the nymph population in citrus was found in June and a peak in the adult population was found in August. They observed high egg mortality during the August in egg density. Location of Pesticide Application Conventional application of pesticides has been found to be only 1%–2% efficient for delivering the active material to the effective site (F.R. Hall, 1985; Pimental and Levitan, 1986). This clearly is an area for improvement. Egg masses generally occur on the bottom surfaces of the host plant leaves. Nymphs also hide on lower leaf surfaces. Mature GWSS evidently feed on larger stems than do smaller leafhoppers. This information should dictate the target area for control. Toscano and colleagues (2002) reported on simple and effective means of GWSS control that used systemic application of imidacloprid (Admire) through the root system of grapes and citrus. Nymphs and adults were controlled with a single application per season for areawide management programs. The best control was achieved with the application of the pesticide at a rate of 32 oz/acre. The researchers also tested rates of 20 oz and 16 oz/acre. The pesticide moved through the vascular system in 10 days but required about 6 weeks for citrus. Because imidacloprid can be applied through drip irrigation, it has major advantages as a potential control method. Systemic pesticides can also be applied by aerial or conventional ground rig spraying equipment, requiring only that the active ingredient be

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California Agricultural Research Priorities Pierce’s Disease applied to the leaf surface where it can be absorbed. This allows the formulation to be introduced more quickly into the vascular system where GWSS feeds, but one would expect drift losses because vineyards and orchards have large cross-sectional areas that are not occupied by fruit crops. Many pesticides are applied by air blast sprayers, at 80–100 gal/acre at velocities up to 60 mph. Drift can be measured as far as 100 yd away after spraying through a tree canopy in relatively calm wind (Derksen et al., 2000 Fox et al., 1994). The air blast system uses a large amount of energy, requires the transport of large amounts of solution, and presents obvious concern about drift. Welsh and colleagues (2000) compared the results from an application of fungicide to grape by air blast sprayer at a rate of 80–100 gal/acre with results from application by electrostatic-spray-charging nozzles at 8–10 gal/acre. They measured dislodgeable foliar residue because they were interested in determining exposure of workers to fungicide. They reported that, at an application of 4 oz/acre a.i., leaf deposition for the air blast sprayer was 68% of that provided by the electrostatic sprayer, as indicated by dislodgeable foliar residue, even though the electrostatic application was one-tenth the volume. Economic Research Several current research projects are addressing the effectiveness of a spectrum of GWSS control strategies. The commonly accepted method for pesticide application—the air blast spray system—is inefficient, uses an excessive amount of energy, and creates problems with drift. Newer methods—such as drip irrigation application of systemic pesticides—offer several advantages. The use of air-assisted electrostatic sprayers should be evaluated for application efficiency and drift. Development of that technology for citrus orchards would be appropriate because citrus hosts all GWSS stages. There have been no engineering studies to evaluate the potential for reduction in pesticide application rates or for reduction in drift. Minimizing application rates produces concomitant reductions in cost. Reducing drift addresses a sensitive issue, especially in residential areas. Research is needed to assess the feasibility and effectiveness of methods other than air blast or aircraft spraying, including recirculating tunnel sprays and the charging of fine sprays—as means for improving deposition efficiency and decreasing pesticide drift. Any new pesticide offers the potential for undesirable or unanticipated consequences. Therefore the potential risk to agricultural workers, to wildlife, to the environment, and to crop quality must be determined as soon as a new control technology is identified. The committee, therefore, makes the following recommendations: Recommendation 3.16. Control strategies should be pursued that limit the use of insecticides to narrow-spectrum, sustainable formulations that are minimally incompatible with ecologically based approaches to pest

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California Agricultural Research Priorities Pierce’s Disease management. A premium should be set on minimizing the negative consequences of pesticide use for human health and environmental quality. Recommendation 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).