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Pierce’s Disease and the Glassy-winged Sharpshooter: Their Biology and the Challenges of Their Management

In 2001, the California Department of Food and Agriculture (CDFA) approached the National Research Council of the National Academies, requesting that it help monitor current and emerging issues in the state’s agricultural research agenda, particularly for Pierce’s disease (PD), which threatens California’s wine, table, and raisin grape industry, and several other agricultural commodities. In response, the Board on Agriculture and Natural Resources convened the Committee on California Agricultural Research Priorities: Pierce’s Disease. 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 to submit a rigorous and timely evaluation of scientific issues in response to identified areas of concern.

The specific charge to the committee was the following: 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



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California Agricultural Research Priorities Pierce’s Disease 1 Pierce’s Disease and the Glassy-winged Sharpshooter: Their Biology and the Challenges of Their Management In 2001, the California Department of Food and Agriculture (CDFA) approached the National Research Council of the National Academies, requesting that it help monitor current and emerging issues in the state’s agricultural research agenda, particularly for Pierce’s disease (PD), which threatens California’s wine, table, and raisin grape industry, and several other agricultural commodities. In response, the Board on Agriculture and Natural Resources convened the Committee on California Agricultural Research Priorities: Pierce’s Disease. 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 to submit a rigorous and timely evaluation of scientific issues in response to identified areas of concern. The specific charge to the committee was the following: 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

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California Agricultural Research Priorities Pierce’s Disease priorities and needs, and will assist the state in coordinating with national and international program efforts to address the disease. In this report, the committee recommends ways to improve the development and implementation of a coherent research and management agenda to address Pierce’s disease. Chapter 2 discusses the issue of setting research priorities and the process of selecting the best science, emphasizing the need for economic analysis to enable more thoughtful decision-making. Chapters 3, 4, and 5 examine potential research and management approaches for protecting plants from the disease and for controlling the pathogen, Xylella fastidiosa (Xf) and its insect vector, the glassy-winged sharpshooter (Homalodisca coagulata [Say], GWSS). The remainder of Chapter 1 provides an introduction to the biology of the disease and the vector and offers estimates of the costs of their management. The chapter concludes with an overview of the organizational and institutional stakeholders who are responding to the threat of the disease and with a brief discussion of factors that could directly or indirectly influence the feasibility or effectiveness of proposed management strategies. PIERCE’S DISEASE In 1892, Newton B. Pierce, California’s first trained plant pathologist, characterized a disease that had been called “Anaheim disease” or “mysterious vine disease” that now bears his name. PD is caused by (Xf), a bacterial plant pathogen. Once transmitted to a plant by an insect vector, the bacteria multiply and generate a plaquelike substance within the xylem of the plant. Ultimately, water movement is blocked, and the plant dies. Pierce’s (1892) bulletin for the U.S. Bureau of Agriculture, The California Vine Disease, became the first comprehensive published description of the disease, which had caused significant problems for California agriculture up to that point and has continued to do so ever since: Between 1884 and 1900, PD destroyed more than 35,000 acres of grapevines in the Los Angeles basin (Gardner and Hweitt, 194). By 1921, the disease had become endemic throughout most of the grape-growing areas of California (Hewitt, 1970). It was observed in the Napa Valley in 1887, in the Livermore area in 1888, in the Sacramento and Santa Clara valleys in 1900, and in the San Joaquin Valley in 1921. Three major epidemics occurred in the twentieth century: Between 1914 and 1918, vineyards in the Santa Clara Valley were devastated. Then, between 1935 and 1940, more than 50,000 acres of grapevines in the San Joaquin and Napa valleys were destroyed (Gardner and Wewitt, 1974). The last major epidemic occurred in the Napa Valley between 1960 and 1962. Twentieth-century PD epidemics renewed interest in research. Throughout much of the century, PD generally was believed to be caused by a virus (Hewitt et. al., 1949) because no bacterial or fungal pathogens had been identified and because PD was known to be transmissible by grafting (Hewitt,

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California Agricultural Research Priorities Pierce’s Disease 1939) and by insect vectors (Hewitt et al., 1942). Researchers reported that numerous xylem-feeding insects could transmit the disease (Winkler, 1949) and that at least 76 species of plants in 28 genera were hosts of the pathogen (Freitag, 1951). In 1931, Weimer recognized alfalfa dwarf disease, which later was found to be caused by the same pathogen as PD. He demonstrated that alfalfa dwarf disease was graft-transmissible (Weimer, 1936), and he reported that the most consistent microscopic characteristic of alfalfa dwarf was the presence of “bacteria-like bodies” in xylem vessels. However, because Weimer observed bacteria in 75% of diseased plants, and because his bacterial isolations and subsequent inoculations failed to reveal a pathogen, he concluded that alfalfa dwarf most likely was a viral disease (Weimer, 1931). In 1941, Hewitt and Houston reported on the association of PD and alfalfa dwarf disease in adjacent plantings. Several years later Hewitt and colleagues (1946) demonstrated by grafting and by insect transmission that PD and alfalfa dwarf were caused by the same agent. In 1967, researchers (Doi et al., 1967; Ishie et al., 1967) reported that mycoplasma-like organisms, now known as phytoplasmas, were associated with several diseases that previously had been thought to be caused by unidentified viruses. That discovery stimulated renewed interest in the cause of numerous plant diseases of unclear etiology. In 1973 a xylem-inhabiting bacterium was described independently in Florida (Hopkins et al., 1973) and in California (Goheen et al., 1973) in association with PD. The xylem-inhabiting bacterium was described as “rickettsia-like” because of its small size, susceptibility to tetracycline antibiotics, peculiarly rippled cell wall, arthropod transmission, and apparent obligate parasitism (Hopkins, 1977). Because the bacteria were not readily cultured on conventional media, light and electron microscopy were used to reveal their existence in plants. That finding dispelled the assumption that a virus caused PD, but it did not entirely solve the mystery surrounding the etiology of the disease. Auger and colleagues (1974) reported isolation in culture of the bacterium associated with PD; the bacterium was later classified as Lactobacillus hordniae (Latorre-Guzman et al., 1977). Purcell and colleagues (1977) later determined that L. hordniae was not the cause of PD, but that it is commonly associated with an insect vector of PD (Purcell et al., 1977). Davis (1978) isolated the bacterium subsequently named Xylella fastidiosa (Wells et al., 1987) from grapevines with PD and conclusively proved that the Xf bacterium caused the disease. The PD bacterium was the first of numerous fastidious xylem-inhabiting bacteria to be isolated in special culture media that supports in vitro growth. Since that initial success, most of the known fastidious xylem-inhabiting bacteria have been cultured on the same or similar media derived from that media developed by Davis and colleagues, and in most cases the role of the bacteria as plant pathogens has been confirmed (Davis, 1991). Among the bacteria are numerous strains of Xf that cause “emergent” plant diseases (Hopkins and Purcell, 2002) (Table 1-1). Several of those diseases are found commonly from central Florida to the area near the Gulf of Mexico and the coastal plain of Georgia and South Carolina.

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California Agricultural Research Priorities Pierce’s Disease Table 1-1 Plant Diseases Caused by Different Strains of Xylella fastidiosa Host plant Strain and Disease Reference Almond (Prunus dulcis) Almond leaf scorch disease Davis et al., 1980; Goheen et al., 1973 Alfalfa (Medicago sativa) Alfalfa dwarf disease Mircetich et al., 1976; Thomson et al., 1978 Peach (Prunus persica) Phony disease of peach Davis et al., 1981; Hopkins et al., 1973; Goheen et al., 1973; Wells et al., 1981, 1983 Plum (Prunus domestica) Plum leaf scald disease French et al., 1978; Kitajima et al., 1975; Raju et al., 1982; Wells et al., 1981 Elm (Ulmus americana) Elm leaf scorch disease Hearon et al., 1980; Kostka et al., 1984; 1986a Mulberry (Morus rubra) Mulberry leaf scorch disease Kostka et al., 1986b Oak (Quercus spp.) Oak leaf scorch disease Chang and Walker, 1988; Hearon et al., 1980; Kostka et al., 1984 Periwinkle (Littorina vinca minor) Periwinkle wilt disease Davis et al., 1983; McCoy et al., 1978 Ragweed (Ambrosia trifida) Ragweed stunt disease Timmer et al., 1981 Red maple (Acer rubrum) Leaf scorch of red maple Sherald et al., 1987 Sycamore (Platanus occidentalis) Sycamore leaf scorch disease Hearon et al., 1980; Sherald et al., 1983 Oleander (Nerium oleander) Oleander leaf scorch Purcell et al., 1999 Coffee (Coffea spp.) Coffee leaf scorch De Lima et al., 1998 Citrus (Citrus aurantium) Citrus variegated chlorosis Chang et al., 1993; Hartung et al., 1994 Grape (Vitis vinifera) Pierce’s disease Davis et al., 1978; Goheen et al., 1973; Hopkins et al., 1973 Xylella fastidiosa is a Gram-negative bacterium—it contains a unit membrane as the surface of the cell wall—and the only species within the genus (Wells et al., 1987). A high degree of DNA homology sequence identity (75%–

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California Agricultural Research Priorities Pierce’s Disease 100%) exists between pathologically different strains of Xf, suggesting that the strains are indistinguishable at the species level (Kamper et al., 1985; Wells et al., 1987). Less than 5% DNA homology sequence identity was found between those strains and other strains representing different genera containing phytopathogenic bacteria and other Gram-negative bacteria. Phylogenetic analysis based on sequences of the 16S rRNA gene and the intergenic spacer region between the 16S and 23S rRNA genes indicates that—with the possible exception of one pear strain from Taiwan—Xf is a homogeneous species (Mehta and Rosata, 2001). Similarity and signature analysis of 16S rRNA sequences indicate that strains of Xf are most closely related to xanthomonads (Wells et al., 1987). Similar conclusions were drawn from phylogenetic analyses of DNA sequences (Mehta and Rosata, 2001). Although strains of Xf that cause PD in grapevines can colonize members of at least 28 families of monocotyledonous plants, recognizable disease symptoms are produced in only a few of those plants (Freitag, 1951; Hopkins and Adlerz, 1988; Raju et al., 1980, 1983). But Hopkins (1989) speculates that the list of natural hosts of all strains of Xf probably is limited more by the effort spent looking for other hosts than by the host specificity of the bacterium. Symptoms of PD in plants such as grape typically vary by season—most notably from spring to fall. Older leaves will exhibit non-uniform, often interveinal, chlorosis and then necrosis that usually starts at the leaf margins; the leaves turn yellow and then die. Fruit shrivels, and non-uniform wood maturity has been observed on grapevine canes. After winter dormancy in infected plants, delayed and stunted growth is exhibited in spring, as is erratic bud break, the emergence of smaller leaves, and chlorosis (American Vineyard, 2001). The appearance and severity of PD also varies with geography and regional factors such as climate contribute to proliferation. In the southeastern United States, for example, the occurrence of PD among wine grapes (Vitis vinifera) was so great and widespread that it always has been impractical to grow this crop in states of the Gulf Coastal Plains. The disease therefore has not been studied in that region, and no serious epidemiologic analysis of PD has been carried out in those states (Hopkins and Purcell, 2002). In contrast, the Mid-Atlantic states are experiencing only limited problems with PD; certainly not to the extent as found in Florida or Southern California. How, then, has the climate of the Gulf Plains states (particularly Florida) provided favorable conditions for PD? In Northern California and Virginia the disease has yet to proliferate. Evenings are cooler in Northern California and in Virginia than they are in Florida. More rain falls each year in Florida, and precipitation follows a different pattern in Florida than in California or Virginia. The Florida growing season is notably longer than is that of the other two states, so favorable conditions for Xf last longer and it more likely to that persistent infection will be established host plants. Hopkins and Purcell (2002) reported that “The only feasible control for PD in the southeastern United States… is genetically controlled plant resistance to X. fastidiosa.” An alternative to V. vinifera in the southeast is the natural muscadine grape (V.

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California Agricultural Research Priorities Pierce’s Disease rotundifol Michx). Although not well suited for winemaking, muscadine grapes are highly resistant to PD, and therefore have been grown as a (table) fruit in the southeastern United States for some time (Loomis, 1958). Thus far, alternatives to host plant resistance—such as control of the insect vector for PD—have not been successful at stopping the spread of the disease in that region (Hewitt, 1970; Hopkins and Purcell, 2002). Other states along the East Coast, including Virginia, are experiencing PD although not to the same extent as found in Southern California. The disease thus far, has been confirmed along the Eastern Shore of Virginia (in the Delmarva Peninsula and in Tidewater), but there is considerable uncertainty about the distribution of insect vectors throughout the state (Pfeiffer, 2002). Unlike the movement of PD in California, where the disease typically spreads from outside vegetation into vineyards (University of California, 2000), in the Southeast and the Mid-Atlantic, PD is more likely to spread by leafhoppers feeding between vines. Thus far, in the Eastern wine-producing states—such as Virginia—multifaceted approaches including integrated pest management (IPM), have been used to control the spread of PD and a variety of vectors, including leafhoppers (Pfeiffer, 2002). Much attention has been given to the general absence of vine-to-vine transmission of PD in California vineyards, although a transmission has been demonstrated in the laboratory (Purcell and Finlay, 1979). Such variables as environmental conditions and exposure time (the amount of time an insect vector spends feeding on a PD-infected plant, or the length of the season) also influence whether a pathogen will become established and spread from vine to vine. Purcell and Saunders (1999) note that “most PD strains do not move systemically in most symptomless [sic] hosts.” GLASSY-WINGED SHARPSHOOTER The glassy-winged sharpshooter (GWSS; Homalodisca coagulata [Say]) is a relatively new insect pest in California agriculture. It was introduced into the southern part of the state most likely through nursery plants transported from the southeastern United States (Cavanaugh, 1999). It is the primary vector of Xf in peach (it transmits phony peach disease; T.M.Perring et al., 2001) and grape in Georgia, Florida, and other southern states. A leafhopper (family Cicadellidae; sharpshooters are of the Cicadellinae subfamily), GWSS has been observed in high numbers in citrus along the of Southern California coast since the early 1990s. It is a close relative of the native smoke tree sharpshooter (H. lacerta [Fowler])—a pest also found in southern California. The leafhopper was identified as common to the southeastern states from Florida through eastern Texas, occurring as far north as Missouri. Early wine grape infestations of GWSS were noticed in 1996 in a chardonnay vineyard in Temecula Valley. The insect itself was discovered around 1989 on eucalyptus windbreaks in Ventura County and at a lemon grove near Santa Paula (Cavanaugh, 1999; Sorenson and Gill, 1996).

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California Agricultural Research Priorities Pierce’s Disease Over the past few years, GWSS has become locally abundant further inland in California, in Riverside and San Diego counties (Figure 1-1). Since the discovery of GWSS in the state, its abundance and distribution have increased. It can now can be found in Riverside County, and in areas of San Diego, Orange, San Bernardino, Los Angeles, Ventura, Santa Barbara, and Kern counties. Its range is continuing to spread northward, and recently it has been found in the San Joaquin Valley. In 1998 and 1999, high populations on citrus and adjacent vineyards were observed in southern Kern County. That county has been the site of a locally successful pilot program to control GWSS. GWSS is expected to spread north into the Central Valley citrus belt, and it could become a permanent part of various habitats throughout northern California. FIGURE 1-1 GWSS Distribution in California Several biological and cultural factors influence the spread and the effects of GWSS in California. Although it is active throughout each season (Blua et al., 1999) and has two generations per year (Blua et al., 2001), cooler temperatures seem to keep populations down (Morgan and Brennan, 2002). GWSS is larger and flies farther than other sharpshooters—such as the native blue-green sharpshooter (BGSS; graphocephala atropunctata [Signoret] )—it

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California Agricultural Research Priorities Pierce’s Disease presents a far greater threat to agricultural plants than do its relatives. The greater dispersal, longevity, and fecundity of GWSS relative to native sharpshooters are the primary causes of increased vectoring potential of PD. Moreover, it can fly as much as 4–5 m above the ground (Larsen, 2000a), so ground-based trapping is difficult. Unlike the native BGSS which feeds on young foliage, the larger GWSS can feed on basal, woody segments of stems, below the point at which annual pruning is done (Almeida and Purcell, 2003). This increases the probability that Xf infection will persist and spread systemically within the plant, rather than remaining peripheral where it might be pruned out or die out otherwise during winter. Late season (after May–June) infections introduced by GWSS are more likely to persist and become chronic than are those introduced by native sharpshooters. The ability of GWSS to feed on many different plant species also has important implications for Xf disease transmission. The CDFA Pierce’s Disease Control Program web site (www.cdfa.ca.gov/phpps/pdcp) lists more than 200 genera on which GWSS feeds, and it, and can consume as much as 10 times its body weight for each hour of feeding on plant xylem fluids (University of California Riverside, 2003). Thus, GWSS has numerous opportunities and great capacity for obtaining and transmitting Xf. Once insects begin to transmit the pathogen, the effects are progressive. Affected grapevines typically die within 1 or 2 years after infestation, and younger vines are especially susceptible. Purcell (1975) reported that the early-season distribution and infectivity of the BGSS sharpshooter in the Napa Valley coincided with the pattern of PD. Infection typically begins in April and May, when young shoots are susceptible (Adlerz and Hopkins, 1979). Left unchecked, Xf infestations carried by the BGSS typically spread at an annual rate of one-sixth of one percent of the total area of a vineyard. (Clarke, 2000). Adult sharpshooters that feed on plants infected by Xf transmit it to other plants, when the bacteria adhere to surfaces in their foreguts (Meadows, 2001). Chronic infections are likely to influence the epidemiology of PD in California, particularly by increasing the frequency of vine-to-vine spread of the disease by leafhoppers. Vine-to-vine spread is expected to result in an exponential—rather than linear—increase in the incidence of PD (Hashim, 2001). COSTS OF PIERCE’S DISEASE Relatively little in the literature discusses the economics of PD; only two reports have been published. The first is the work of Siebert (2001) on quantifying the economic effects of PD for wine grape growers; the second is a more specific study by Brown and colleagues (2002) on barrier crops for inhibiting GWSS movement. Drawing particularly on Siebert’s work, this section presents information related to grape growers’ costs attributable to PD, potential economic effects for citrus and almond production, and statewide costs of managing PD and GWSS.

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California Agricultural Research Priorities Pierce’s Disease Costs to Growers Pierce’s disease is expensive for grape growers, although the costs of production, income loss, and removal and replanting vary by location, grape variety, and vineyard age. Grower-added costs include removing and replanting parts of or entire vineyards; enhanced vineyard production management, including monitoring, replacement of diseased vines, and training new growth; vector management, including monitoring and application of vector controls such as pesticides; and GWSS host plant and riparian area management. Siebert (2001) developed hypothetical estimates of income lost to PD for a wine grape vineyard over a 5-year period (Table 1-2). That scenario depicts a vineyard so infested with PD that it must be completely replanted. Of course, replacement of a vineyard involves more than just replanting; it also entails lost yield and revenue. As Siebert (2001) notes, the estimated income loss to grape growers also could affect other aspects of California’s economy, such as employment and regional and state income, although those costs are not likely to have a large statewide effect. Siebert’s (2001) hypothetical example uses the costs for a Sonoma chardonnay vineyard (Table 1-2), and it assumes that the vineyard will suffer a 50 % loss in yield in the year before the vines are removed. Also assumed is a 7 ton/acre yield at the vineyard’s maturity and a price of $1,060/ton. The establishment of a new vineyard—as shown in Table 1-2—would cost $13,369, amortized over 22 years; the annual cost would be $1,227. Table 1-2 Hypothetical Cost and Revenue Scenario of Vineyard Replacement   Year 0 Year 1 Year 2 Year 3 Year 4 Yield (tons/acre) 3.5 0 0 3 7 Revenue $3,710 0 0 $3,180 $7,420 Revenue without PD $7,420 $7,420 $7,420 $7,420 $7,420 Revenue difference −$3,710 −$7,420 −$7,420 −$4,420 0 Replant cost   −$1,227 −$1,227 −$1,227 −$1,227   Source: Siebert, 2001 Table 1-3 estimates the cost of replanting a small percentage of the infected vines in a vineyard, by region and by grape variety (Siebert, 2001). The last two columns of the table present the cost of replanting a percentage of the

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California Agricultural Research Priorities Pierce’s Disease Table 1-3 Estimated Vineyard Establishment and Replanting Cost Area, Variety Variety Established Cost/Acre Cost/Vine Amortized Cost/Acre Vines/Acre Replanting Cost Vines Replanted San Joaquin Valley Wine $4,105 $7.27 $621 565 $18 2% Lodi Cabernet $5,949 $9.56 $381 622 $3 2% Sierra Nevada Zinfandel $10,173 $17.22 $1,013 622 $105 5% Sonoma Chardonnay $13,369 $14.72 $1,227 908 $103 4% Lake Sauvignon blanc $8,640 $15.27 $834 566 $47 2% Santa Maria Chardonnay $11,985 $11.01 $736 1,089 $256 5% San Luis Obispo Cabernet sauvignon $9,526 $10.94 $585 871 $64 2% San Joaquin Valley Thompson seedless $3,839 $7.40 $378 519 $22 5%   SOURCE: Siebert, 2001

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California Agricultural Research Priorities Pierce’s Disease vines in a vineyard; hence, for the San Joaquin Valley wine estimates, the cost is $18/acre to replant 2% of the vineyard. In this case, the cost reflects replanting 2% of 565 vines/acre, or approximately 11 vines/acre. In addition to the costs that are directly attributable to PD, grape production costs can involve controlling GWSS as a vector. Pest monitoring must be implemented, and that could involve the placement of traps or sweeping the edges of a vineyard with a net to quantify GWSS infestations. Economic information on the density and number of traps to be used and on the labor costs of monitoring are not available. Three pesticides generally are used in IPM programs for controlling sharpshooters. The formulations are chosen for their usefulness and efficacy on natural enemies. The first is imidacloprid (75% active ingredient [a.i.]), a foliar product that provides rapidly but short-term control (14 days). Imidacloprid is applied a rate of 0.75 oz/acre, but its use is limited to 2 oz/acre annually. The product costs $32 per ounce; so the cost per application is about $44/acre, assuming $20 to apply it. Another alternative is imidacloprid (21.4% a.i.) applied through an irrigation drip system at a rate of 16 oz/acre. The cost is $4.80/oz or $76.80/acre for one application. The third material is dimethoate, which is suggested for control of BGSS in coastal areas. Dimethoate is under a special-needs registration and no cost data are available (Siebert, 2001). Aggregate estimates of grower costs attributable to PD will depend on the spread of the disease. So far, there has been little investment in identifying the full current or potential economic costs of the disease to California agriculture or the state’s and economy. Although there are many host species that harbor GWSS, observations in Temecula, California, vineyards that are close to citrus groves show that vineyards are at greatest risk. Table 1-4 shows grape and citrus acreage by California county in 2001. The southern San Joaquin Valley has significant acreage in citrus in close proximity to vineyards. Vineyards in the rest of California would likely be likely to experience PD according to the presence of other habitats that harbor the vector, such as riparian areas. Considerable uncertainty exists about the potential for PD to spread significantly more than it has in the past. For example it is not known whether GWSS can survive in the cooler Northern California vineyards Potential Economic Effects on Almond and Citrus According to information reported to the committee, almond leaf scorch (a disease caused by Xf) has been identified in almond orchards; although neither BGSS nor GWSS has been identified as the vector. A concern is that another, as-yet-unidentified vector is contributing to the spread of almond leaf scorch (Gleeson et al., 2004). Almond growers have observed the spread of PD and worry about its implications for their crops. Management of almond leaf scorch consists of pruning the affected parts of the trees, and the economic consequences of the disease result from the increased pruning costs. Pruning a mature almond orchard currently costs about

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California Agricultural Research Priorities Pierce’s Disease RESPONSE TO PIERCE’S DISEASE AND THE GLASSY-WINGED SHARPSHOOTER During the summer of 1999, William J. Lyons Jr., who was secretary of CDFA, oversaw the creation of a task force to address the threat of GWSS. This culminated in the Pierce’s Disease Advisory Task Force, which counsels the Pierce’s Disease Control Program (CDFA, 2002a). In the spring of 2001, California Assembly member Patricia Wiggins (D-Santa Rosa) introduced legislation to raise $25 million for GWSS research. Her bill (Assembly Bill, or AB, 1394) proposed to secure $5 million annually for a period of 5 years. That funding would be obtained through an industry self-assessment on grapes grown for processing; producers would be charged a maximum of $3/$1,000 value of final purchase price. Moreover, AB 1394 would establish a PD/GWSS Board, which would collect the annual assessments. The bill also would allocate funds for research on IPM and other sustainable insect control practices. The law was to expire January 1, 2006, if not renewed. During the fall of 2001, the bill was signed into law by Governor Gray Davis, and it took effect immediately (State of California, 2001). An additional, $14 million was earmarked in the federal fiscal year 2002 agriculture appropriations bill for PD–GWSS research, to be divided between a U.S. Department of Agriculture–Agricultural Research Service (USDA–ARS) facility in Parlier, California; several state university research centers; and the USDA Animal and Plant Health Inspection Service (USDA–APHIS). The assessment on the grape growers’ profits subsequently was lowered to $2/$1,000 value (CDFA, 2002c). Diverse Community of Stakeholders A sophisticated community of stakeholders is involved in scientific, policy, industry, and agricultural responses to the threat presented by PD in California: local growers, nongovernmental organizations (NGOs), CDFA administrators, research scientists from the University of California (UC) and CDFA, and USDA–ARS and USDA–APHIS investigators. The affected industries, however, are not homogeneous in their perspectives on and approaches to the various agricultural, environmental, and economic problems caused by PD. Given the nature of the recent GWSS-mediated outbreak of PD in California, a list of research needs has emerged from the exchange of information and data among local growers, county officials, state officials, and academic researchers. Research on PD is coordinated broadly through the Pierce’s Disease Control Program [Figure 1-2]—an alliance consisting of CDFA, the agricultural commissioners of the various counties involved, researchers in the UC system and USDA, various state and local agencies, and several California agricultural organizations (CDFA, 2002a).

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California Agricultural Research Priorities Pierce’s Disease FIGURE 1-2 Research Coordination through the Pierce’s Disease Control Program. SOURCE: Adapted from CDFA, 2002a California Department of Food and Agriculture The California Department of Food and Agriculture coordinates research on PD. Its Advisory Task Force on Pierce’s Disease and that task force’s subcommittees assist in planning long-term research agendas and in identifying viable funding sources. The PD/GWSS Board and its subcommittees assist in the solicitation of new research projects, and in the scrutiny of funded projects. Members of the task force, the PD/GWSS Board, and their subcommittees serve as appointees; the California legislation (AB 1232 and AB 1394,1 respectively) that established those entities does specify term lengths. A science advisory panel of six experts advises CDFA on technical matters, such as trapping and other techniques, for responding to PD–GWSS. Each year, the Pierce’s Disease Control Program submits a report to the legislature that details the condition of the program and of the problem. The work of funded, continuing research projects for the Pierce’s Disease Control Program culminates in an annual Pierce’s Disease Program Research Symposium, where researchers and investigators present preliminary findings or data. Abstracts of that work are compiled and published in a set of proceedings that is available online to the public (CDFA, 2002b). University of California System Many researchers within the UC system are studying PD and GWSS. Because those investigators are familiar with the California agricultural landscape and because of their proximity to active PD–GWSS infestations and 1   AB 1394 was amended by AB 2890 in September 2002.

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California Agricultural Research Priorities Pierce’s Disease experimental sites and their access to the university system’s resources and experts, the UC system has become very involved in the Pierce’s Disease Control Program. But research on PD is by no means limited to the UC system. Many other researchers across the country (notably in the Southeast) are conducting high-quality, relevant work on the disease, its vectors, or other aspects of the problem that can be applied to the collective understanding of PD–GWSS. Some of those investigators receive support from the Pierce’s Disease Control Program. U.S. Department of Agriculture The U.S. Department of Agriculture works with institutions, including the UC system, on the challenges created by PD–GWSS. Through ARS, USDA conducts investigations on PD–GWSS, using, for example, scientists, university researchers and other experts who work in the Cooperative Extension. ARS—the internal biological-research unit of USDA—is distributed among various facilities throughout the United States. Its San Joaquin Valley Agricultural Sciences facility in Parlier, California is considered USDA’s headquarters for PD research. The Exotic and Invasive Diseases and Pests program was created at this facility and is overseen by a research leader. Updates and news concerning the facility are available from its Web site (USDA–ARS, 2002). USDA–APHIS also has been assessing the PD–GWSS problem in California, through surveys to assist CDFA in mapping GWSS movement throughout the state (USDA-APHIS, 2002). County Departments of Agriculture In light of the uneven distribution of PD and GWSS throughout California, the state relies heavily on county-administered programs to monitor and manage the problem. Given the dynamics of PD–GWSS infestation, county departments of agriculture implement programs and apply experimental techniques based on specific needs, many of which are determined by the production and flow of agricultural commodities within and across political boundaries. Thus, the counties are important stakeholders in coordinating responses to PD–GWSS. The counties also provide a central point of contact for government, university researchers, producers, and other counties. In Kern County, for example, Cooperative Extension specialists, CDFA, industry, and other associations of producers have converged to address GWSS management and control (University of California Cooperative Extension, 2003b). Kern and Tulare counties have created a Kern–Tulare GWSS Task Force.

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California Agricultural Research Priorities Pierce’s Disease Industry Several California agricultural commodities are affected by PD–GWSS. Although the table grape and wine industries are most threatened they are by no means the only industries at risk. Almond, alfalfa, citrus, oleander, are among other plants affected by GWSS (see Table 1-1). Nor is there a single industry perspective on how to respond to the problem (see Box 1-1). There are many viewpoints about how the disease and its vector should be treated. Some perspectives are based on geography: Grape growers in Southern California—especially in areas affected most by PD, such as Temecula Valley—perceive the problem as being one of greater severity than do some growers in the north, where PD has not been established by GWSS. However, other growers from the north might perceive the appearance of PD in the south as an indication of an impending threat because of expansion of GWSS host range, thus calling for the application of resources and attention to managing what could be an eventual emergence of the disease in the north. There are several industry perspectives concerning the breadth and quality of existing research programs on PD–GWSS. Some manifest themselves in the positions taken by agricultural associations (the Almond Board of California, the American Vineyard Foundation). In one respect, there is unity among industry representatives: Many of them acknowledge the significant improvement in basic and applied research over the past 5 years, noting that a concerted public- and private-sector research effort largely was missing until BOX 1-1 Who Should Implement Control Strategies? The diversity of California’s agricultural landscape makes it difficult to place the perspectives of commodity producers into a single “industry” viewpoint. The agricultural threat created by PD–GWSS highlights the point. In its consultation with various representatives of industry, the committee learned of potentially growing frustrations among representatives of various industries, such as growers and nursery operators. The frustrations have emerged from questions about who should be held accountable and who should be responsible for implementing strategies for managing GWSS populations. Should individual nurseries bear prime responsibility for ensuring that their ornamental plants are GWSS- or pathogen-free? If so, how should the assortment of costs associated with implementing various strategies be shared? Should the responsibility of implementing management strategies be delegated more evenly throughout industry to lessen the tremendous burden placed on nursery owners who must serve as the first line of GWSS or pathogen screening? If so, how?

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California Agricultural Research Priorities Pierce’s Disease then (unpublished data submitted to committee, 2002). Industry representatives also must contend with the temporal element of responding to emerging pest problems. There is understandable frustration in the fact that the knowledge that is provided by research and that is needed for sustainable solutions lags behind the perceived need to solve the problem immediately. There is also a perception among some industry representatives that returns on their investments in research and management of PD–GWSS are marginal. Another area of concern is related to the transparency of communication between researchers and the lay community. Industry is positioned to act on research recommendations for responding to PD–GWSS, so there is concern that the often highly technical nature of research projects will make it difficult to implement new management strategies. Another difficulty faced by industry is the call for widespread replanting of affected crops—an expense that growers want to avoid, given the time that it takes for plants to yield fruit. According to one industry representative, replanting is occurring at a fraction of the rate needed to replenish the acreage so far affected by PD. Mature vineyards are also popular among tourist attractions and tourism is a significant source of revenue for the wine industry. Nongovernmental Organizations The group of NGOs that has responded to the PD–GWSS threat is heterogeneous. Agricultural commodity groups, such as commodity boards, could be classified as NGOs, despite their affinity for industry objectives. Environmental watchdog groups also qualify as actors in the response to PD–GWSS, and many in those organizations are concerned about aerial spraying of pesticides. In 2000, the Northern California River Watch threatened to sue growers who used aerial sprays to control GWSS (CAWG, 2000), and in 2003, a coalition of NGOs filed suit in California Superior Court in defense of greater measures for protecting the environment and against the use of pesticides for managing GWSS (CATS, 2003). OVERVIEW OF APPROACHES The spread of PD–GWSS has elicited multifaceted responses. There is no exclusive, comprehensive means by which the spread of PD–GWSS can be inhibited. Some experts emphasize the need to focus on one element, the insect vector, the disease, the host plant; others would incorporate several techniques and strategies to respond to the problem (Meadows, 2001). Although long-term, advanced research on PD has given primacy to the development of grapevines that have improved disease resistance, several immediate management strategies are emerging or are being implemented. The use of the term “management,” in contrast to “control” is deliberate. There are distinct philosophical and practical differences between the two concepts.

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California Agricultural Research Priorities Pierce’s Disease Quarantine The state of California classifies GWSS as a Category B pest, so individual counties can implement controls or quarantine measures on agricultural products that are found to harbor the insect. (Category A pests must be eradicated wherever found; Category C pests do not warrant immediate action.) More than 10 counties in California have instituted the Blue Tag protocol, which requires the return of the entire shipment of plants (ornamentals, for example) to the place of origin if the plants are found to carry GWSS. It is permissible, however, to send shipments to counties that have not yet adopted the protocol (Cavanaugh, 2000). GWSS has settled into various settings, including farmland and urban areas. When GWSS egg masses are found on the rinds of citrus fruits, the fruits no longer are marketable. Consequently, some representatives of industry have expressed interest in seeing GWSS upgraded to Category A (Meadows, 2001). Treatment at the Nursery More than half of California’s nurseries are in counties where GWSS infestations have been found, most commonly as egg masses on nursery stock (CDFA, 2002a). Because some nurseries ship their stock to counties that are not infested with GWSS, the importance of having nurseries monitor for and treat GWSS infestation is significant. Surveys entail setting traps at retail and wholesale nurseries and treatment commonly involves the application of ovicides or other chemical compounds to kill sharpshooter egg masses. Although chemical pesticides do not provide a comprehensive approach to treating sharpshooters that have infested nursery stock, it is suspected that older insects are more vulnerable to them (Akey et al., 2001). Current California law requires preshipment inspection of nursery stock that is to be shipped from an infested area to an uninfested one. Nurseries that receive stock must be notified to hold it for inspection (CDFA, 2002a). Biological Control: Parasitoid Wasps In September 2000, it was announced that a parasitoid wasp from Mexico (Gonatocerus triguttatus Girault) would be released in Fresno, Kings, and Tulare counties to control GWSS populations. This method of biological control (see Chapter 3) is being explored further with the parasitoid wasp G. ashmeadi Girault, which is lethal to sharpshooters that hatch during the summer. A wasp oviposition (egg laying) rate on the sharpshooters of about 90% effectiveness has been recorded. Unfortunately, the oviposition rates are much lower on sharpshooters that hatch during spring (Larsen, 2000a), the first

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California Agricultural Research Priorities Pierce’s Disease generation of the season. The number of spring-hatching sharpshooters influences the number of sharpshooters in subsequent generations and thus their effects on vineyards and orchards. Vegetation Management Removing plants that serve as sharpshooter hosts outside of vineyards could help disrupt GWSS populations and thereby reduce the number of insects feeding on vines. However, when those plants are removed, many growers have replanted them, thereby introducing new host plants because many of those plants also are habitat for beneficial insect species and other wildlife. Border “trap crops” have been planted around vineyards to create protective buffers (University of California, 2000). It now is quite apparent that the distance between the insect vector and its host plant is crucial to managing the spread of PD. As Purcell and Saunders (1999) noted, along the California coast, PD generally is highest on the outskirts of vineyards “adjacent to riparian habitats that harbor overwintering vector populations”. Because GWSS flies relatively low (typically below 15 ft. above the ground; Larsen, 2000a), some growers place barriers (mesh screens with sticky traps) between GWSS habitats such as orange groves and their feeding areas (vineyards). Nevertheless, without a better understanding of spatial relationships between vineyards and sharpshooter reproductive-breeding grounds, such as citrus groves, it will not be possible to prevent PD simply by adopting management practices “within a single vineyard” (T.M. Perring et al., 2001). Other Pesticides and Insecticides In addition to potential chemical treatments used against sharpshooter egg masses other pesticides and insecticides for managing GWSS populations are being tested or are in use (Akey et al., 2001; Extension Toxicology Network, 2003). However, no single pesticide or insecticide can solve the PD problem. For example, Provado kills the sharpshooter, but not quickly enough to prevent transmission of Xf to grapevines. The amount of time it takes an insecticide to inhibit the sharpshooter is pivotal to its effectiveness (the optimal situation would be one in which sharpshooters are killed before they can transmit Xf; USDA–ARS, 2001). Growers who apply pesticidal chemical formulations often look for products that offer long-term effectiveness, so as to increase the amount of time between chemical treatments and thereby to decrease the cost because fewer applications are required. The use of pesticides does not constitute a comprehensive strategy for responding to the threat of PD–GWSS. Often, an area must be sprayed more than once, because the sprays do not kill sharpshooter egg masses. Spraying tends to offer local results, but not much widespread success (Larsen, 2000b). Spaying does not constitute a means of eradicating GWSS—and it is not known

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California Agricultural Research Priorities Pierce’s Disease whether eradication can be achieved. Moreover, the acceptability of continual pesticide applications has social, environmental, and human health implications. If pesticide compounds are to be used in an environmentally safe way, they must be deployed within the context of IPM strategies (Akey et al., 2001). Genetic and Genomic Strategies: Management Tools of the Future? The genetic approach to controlling PD–GWSS will be a long-term endeavor. Muscadine grapes, which are native to the Southeastern United States are resistant to PD, but they are not well suited for winemaking. Scientists are exploring the possibility of transferring the genes that confer resistance in muscadine grapes to wine grapes. This is a goal of long-term research that targets PD (Cavanaugh, 1999). Some genetic studies of Xf have focused on the diverse strains of the bacterium with the goal of preventing the emergence of new Xylella-based diseases. As Chen and colleagues (2002) noted, inhibiting the development of new Xylella-based diseases calls for an understanding of how strains of the bacteria “select their hosts, and their ecological roles in the native vegetation.” Those researchers point out that the strains of Xf that have been studied carefully are from “economically important hosts,” but strains from less important hosts could become reserves for the onset of new diseases (Chen et al., 2002). Hence, the less well known strains merit greater attention. Over the past few years, genomic analyses of Xylella strains have received a good deal of attention from the scientific community. The availability of completely sequenced genomes of more than one strain of Xf (Simpson et al., 2000; Van Sluys et al., 2003) and the development of microarrays (de Oliveira et al., 2002) provide the means to identify the genes involved in transmission, pathogenicity, and survival. In 2000, Simpson and colleagues reported the genome sequence of a citrus variegated chlorosis (CVC) strain of Xf. Recently, the completion of the genome sequencing of the Temecula PD strain of Xf was announced by Van Sluys and colleagues. (2003). Comparative analyses between the two Xf strains and among Xf and other sequenced plant-pathogenic bacteria reveal similarities and differences that could provide clues about the diverse biology of those bacteria (Bhattacharyya et al., 2002; da Silva et al., 2002; Van Sluys et al., 2003). ACCEPTANCE OF MANAGEMENT STRATEGIES It is important for all of the stakeholders involved in PD–GWSS research to consider several factors that will influence the acceptance and effectiveness of the research efforts and the management strategies that are developed for combating PD. Because of the diverse host range and dispersal abilities of GWSS, cooperation and coordination among grape, citrus, and nursery plant growers and their neighbors in rural, suburban, and urban areas

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California Agricultural Research Priorities Pierce’s Disease will be essential for any successful strategy. Fortunately, because CDFA and the other research and regulatory entities are well aware of this need they have made considerable effort to promote cooperation. The discussion that follows highlights a few categories and a few examples of factors already identified as important. Cultural Factors Management strategies for PD–GWSS could influence crop production practices. Given the diversity and distribution of fruit, vegetable, tree nut, and grain production in California, any decision to pursue research that leads to new management strategies must account for those potential influences to ensure that practical management strategies result. For example, a PD–GWSS management strategy emerging from research that calls for chemical control of GWSS in citrus groves could conflict with current IPM practices for citrus, and citrus growers who are not involved in grape production might be reluctant to change their IPM practices for the sake of PD–GWSS management in grapes. Consequently, the likelihood of successful implementation of that strategy could be low unless incentives are provided or value is demonstrated to the citrus growers. One incentive for citrus growers would be the chance to reduce the amount of water used in citrus production because of the reduction in GWSS feeding. The committee was presented with evidence that GWSS infestations in citrus groves could significantly increase requirements for irrigation water and reduce the quality of fruit harvested. In view of the critical water use priorities in California, that could be a serious economic issue for citrus growers to consider. Environmental Factors PD–GWSS management strategies could have environmental implications that require careful consideration. A research priority that ultimately leads to areawide management of GWSS and other PD vectors by use of pesticides, for example, will likely affect IPM programs as well as the air, soil, and water where spraying takes place. There are several formulations in evaluation that are not yet labeled for use on GWSS. Some—including most of the systemic neonicotinoids (see Chapter 3)—show considerable promise. Recent study results reported no residue of neonicotinoids in mammalian tissue, suggesting that it is safe for humans to consume grapes treated with those compounds (Tomizawa and Casida, 2003). The effect of those and other chemicals on exposed workers and in others who consume fruit or wine, and the unintended consequences relative to other plant diseases must still be determined. Grafton-Cardwell (2003) reported that applications of Surround (a finely divided inert kaolin clay) on citrus for GWSS control, also disrupted the parasitic wasps that control California red scale in citrus, resulting in an increase in scale infestation of the

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California Agricultural Research Priorities Pierce’s Disease fruit. That finding is of particular concern because red scale infestations, left unchecked, can lead to the premature death of a citrus tree that might otherwise yield fruit for 40–80 years. Management strategies for BGSS, another PD vector, entail modification of riparian areas and other habitats where the adults reside. Such modifications include the removal of BGSS-preferred host plants. The environmental repercussions could be substantial, affecting many other species: fish, birds, mammals, and pollinating insects. Public concern about habitat modification is significant, and a legal challenge to the statewide CDFA vector management program has been brought by environmental groups (CALTOX v. CDFA, 2003). That litigation alone suggests that research-based PD management strategies must consider environmental issues and concerns. Regulatory Factors Because crop production practices can be influenced by PD management strategies, those that are consistent with a variety of research priorities research priorities considered in subsequent chapters of this report could require additional regulatory control. For example, orchard sanitation in citrus could be required to reduce GWSS populations to protect neighboring vineyards. In some cases, grower cooperation could meet that need, but new regulations could be required to overcome resistance from some sectors of the California agricultural community; those whose crops are not directly affected by PD but that contribute to the spread of the disease (see Box 1-1). Several new regulations govern shipment of nursery stock and of citrus fruit from infected areas to noninfected areas in California. Those measures further limit the spread of PD. Thus, PD research priorities must admit the possibility of additional regulation. Social Factors Social factors are diverse and can reflect a broad set of concerns and perspectives, including some mentioned above. For example, environmental concern regarding pesticide use is greater in some communities than in others, and it can result in political pressure that leads to regulatory restrictions. The choice of chemical controls is likely to reflect human and environmental safety requirements and economic thresholds, such as the per-acre cost of pesticide application for growers. Public acceptance is never guaranteed for new formulations or procedures that can result in effects on neighboring areas through drifting sprays or movement of a compound through surface runoff or seepage into groundwater. Several studies have shown that conventional air-blast spraying and aircraft application of pesticides can result in measurable drift. The encroachment of urban development into agricultural areas means that exposure to drift often is not acceptable, and conflicts can arise between

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California Agricultural Research Priorities Pierce’s Disease agricultural operators and their residential neighbors. That situation warrants the reduction of exposure, and it highlights the need to avoid the imposition of rules and regulations that reduce flexibility in controlling agricultural pests. It is clear that PD–GWSS research priorities must reflect awareness of the social milieu in which management strategies will be implemented. Economic Factors Pierce’s disease is not new to California, but concern about it has increased since the introduction of GWSS (Office of the President, 1999). Clearly, the scale of the recent investment into PD–GWSS research indicates the potential economic consequences for California’s agriculture and economy. Large-scale factors, such as the current supply of and demand for grapes and the resulting effects on prices, will influence the ability of the industry to respond to the threat. For individual growers and producers, options and approaches for PD–GWSS management will be influenced by perceived and actual costs, risks, and benefits. Recent trends in the market indicate an oversupply of California grapes, and that could influence the concern about yield loss attributable to PD, and dampen enthusiasm for PD–GWSS research (Murphy, 2003). Economics is important in all aspects of the PD problem, from estimating current and future losses, to understanding how existing control strategies might be implemented most economically, to evaluating which management strategies still in development might realistically be adopted by growers and producers. One difficulty is that not much economic information has been collected on the PD problem.