FORUM

Chemical Ecology and Management of Lobesia botrana (Lepidoptera: Tortricidae)

C. IORIATTI,1,2 G. ANFORA, M. TASIN,1 A. DE CRISTOFARO,3 P. WITZGALL,4
AND

A. LUCCHI5

J. Econ. Entomol. 104(4): 11251137 (2011); DOI: 10.1603/EC10443

ABSTRACT The moth Lobesia botrana (Denis & Schiffermu ller) (Lepidoptera: Tortricidae) feeds on grapes (Vitis vinifera L.), reducing yield and increasing susceptibility to fungal infections. L. botrana is among the most economically important insects in Europe and has recently been found in vineyards in Chile, Argentina, and California. Here, we review L. botrana biology and behavior in relation to its larval host (the grapevine) and its natural enemies. We also discuss current and future control strategies in light of our knowledge of chemical ecology, with an emphasis on the use of the sex pheromone-based strategies as an environmentally safe management approach. Pheromone-mediated mating disruption is the most promising technique available on grapes and is currently implemented on 140,000 ha in Europe. Experience from several growing areas conrms the importance of collaboration between research, extension, growers, and pheromone-supply companies for the successful implementation of the mating disruption technique. In the vineyards where mating disruption has been successfully applied as an areawide strategy, the reduction in insecticide use has improved the quality of life for growers, consumers, as well as the public living near wine-growing areas and has thereby reduced the conict between agricultural and urban communities. KEY WORDS integrated pest management, natural enemies, pheromone mating disruption, plant volatiles

The moth Lobesia botrana (Denis & Shiffermu ller) (Lepidoptera: Tortricidae) is the major pest of grapes (Vitis vinifera L.) in the Mediterranean basin (Bovey 1966, Bournier 1977, Thie ry 2005). Damage by this pest is caused by larval feeding on grape clusters, which renders them susceptible to Botrytis cinerea (Persoon: Fries) (Sclerotiniaceae) in mid-season, leading to the development of primary and secondary rots at harvest. L. botrana is endemic in the Palearctic Region, where it is widespread in all wine-growing areas, but it is economically most important in southern Europe. In southern France, central and southern Spain, Portugal, Greece, Italy, and the islands of the Mediterranean basin, L. botrana is the only moth that has a signicant impact on grapevine production. L. botrana was recently found in the important South American and North American wine-growing regions of Argentina, Chile, and California (Gonzales 2010, Varela et al. 2010).

L. botrana biology, its impact on wine-table grapes, and various control strategies have been studied since the late 19th century. More recently, efforts have been made to increase the efcacy and to decrease the environmental impact of L. botrana management. In particular, L. botrana chemical ecology and behavioral physiology have been research foci over recent decades (Arn and Louis 1996, Maher et al. 2006, Anfora et al. 2009, Becher and Guerin 2009). We review L. botrana biology and behavior in relation to grapevines and its natural enemies, and we discuss current and future control strategies in light of our knowledge of its chemical ecology. Host Range and Life Cycle on Grapevines L. botrana was described in 1775 by Denis & Schiffermu ller as Tortrix and then redescribed by other authors and assigned to the genera Eudemis and Polychrosis. Currently, as Lobesia Guene 1845, it belongs to the family Tortricidae, subfamily Olethreutinae, tribe Olethreutini (Razowski 1995). The morphology of L. botrana was extensively described by Bovey (1966). Many studies have reported on the polyphagy of L. botrana. Its larvae feed on grapevines and up to 40 other plant species belonging to 27 families. These host plants, which generally grow in typical warm dry environments of the Mediterranean countries, include Olea europea L., Zizyphus vulgaris L., Rosmarinus ofcinalis L., Clematis vitalba L., Cornus spp., Lonicera

1 Fondazione Edmund Mach, Via E. Mach 1, I-38010 San Michele a/A (TN), Italy. 2 Corresponding author, e-mail: claudio.ioriatti@iasma.it. 3 Department of Animal, Plant and Environmental Sciences,University of Molise, Via De Sanctis, 86100 Campobasso, Italy. 4 Chemical Ecology Group, Swedish University of Agricultural Sciences, 23053 Alnarp, Sweden. 5 Department CDSL, Sect. Agricultural Entomology, University of Pisa, Via San Michele degli Scalzi, 2, 56124 Pisa, Italy.

0022-0493/11/11251137$04.00/0 2011 Entomological Society of America

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xylosteum L., Viburnum lantana L, Ligustrum vulgare L., Ribes spp., and Hedera helix L. (Bovey 1966, Stoeva 1982, Coscolla ` 1997, Stavridis and Savopoulou-Soultani 1998, Thie ry 2005). The spurge ax Daphne gnidium L. (Thymelaeceae) is considered to be the original host of L. botrana (Bovey 1966), and its biology on D. gnidium was investigated in the early decades of the last century (Marchal 1912, Picard 1913). More recent research has demonstrated that L. botrana is exposed to a larger cohort of natural enemies on spurge ax than on surrounding grapevines (Nuzzaci and Triggiani 1982, Luciano et al. 1988). It is unclear whether this occurrence results from a lack of insecticide treatment, a greater attractiveness of natural enemies to D. gnidium, or a greater abundance of alternative hosts or prey for the natural enemies of L. botrana. In the Migliarino-San Rossore-Massaciuccoli National Park in Tuscany, Italy, where L. botrana feeds on D. gnidium, the insect life cycle is synchronous with that on grapevines in the vine-growing areas of coastal Tuscany (Lucchi and Santini 2011). On D. gnidium, larvae of the rst generation feed on leaves only, and the second and third generation larvae feed on leaves, owers, and fruit. On most of its host plants, L. botrana larvae feed on reproductive organs (ower buds, owers, and fruit). In a eld tunnel, however, young leaves and shoot tissues of grapevine allowed L. botrana larvae to develop, pupate, and produce fertile adult offspring in the absence of grapes (Lucchi et al. 2011). Host choice for L. botrana can sometimes be related to a particular location where the species adapts its behavior and life history to the local climate and ora. In Crete, for example, L. botrana acts as an itinerant grazer on several different host plants, i.e., its selection of host is closely linked to food availability such that it feeds on grapevines for only part of its annual life cycle. These alternative hosts include Olea europea L., Drimia maritima L., Lonicera etrusca G. Santi, Thymaelea hirsuta L., Erica manipuliora Salisb. Rubus idaeus L., Malva sp., and Rosmarinus ofcinalis L. (N. Roditakis, personal communication). L. botrana is a typical multivoltine species with facultative diapause and with two to ve annual generations on V. vinifera from northern Europe to the Mediterranean Basin. The number of generations depends on latitude, climate, and microclimate. Two generations per year are common in Germany, Switzerland, Austria, and northern France, whereas three generations (and sometimes four) occur in southern France, Spain, Portugal, Greece, and Italy (Roditakis and Karandinos 2001, Harari et al. 2007). In Israel, Egypt, and Crete, some populations do not diapause and instead spend the winter in the larval stage feeding on leftover grape clusters or on alternative hosts. The rst generation develops on inorescences (anthophagous); the larvae web together several prebloom owers to form the so-called glomerulus or nest. The following generations develop on berries (carpophagous). In vineyards, L. botrana hibernates at the pupal stage under exfoliating bark and in crevices and cracks of the trunk and cordons.

The spring generation of L. botrana usually has no direct economic importance, except on poorly fruiting wine cultivars. Larvae of carpophagous generations reduce berry production, but damage is mainly caused by the ensuing fungal and bacterial infections. Cultivars with compact grape clusters are more affected; the second generation is more harmful for early ripening varieties, whereas the third generation is more important for the late-ripening varieties. Insecticides and Integrated Pest Management (IPM) Wherever L. botrana is present, it has a great economic impact on grape production and requires control. The extent of the damage depends on a range of cultivar-specic factors and agronomical practices (i.e., grape cultivar, N fertilization, chemical thinning, training system, summer pruning), weather conditions, and number of generations (Vartholomaiou et al. 2008). Insecticides are applied according to the economic injury level, which can vary depending on the generation, the susceptibility of the cultivar to the subsequent infection by B. cinerea, as well as whether the grapes are produced for table fruit or wine. First generation larvae may not necessarily need to be controlled by chemical treatments, especially on cultivars with abundant inorescences. During the months between owering and harvest, reduction of owers and berries by L. botrana is compensated for by an increased size and weight of healthy berries. For these reasons, chemical control in the rst generation is exclusively applied when the pest population density reaches the injury thresholds (i.e., 50% of infested inorescences). For the following larval generations, the injury threshold ranges between 1 and 5% or 10 and 15% of injured clusters depending on the cultivar, bunch tightness, and harvest time (Ioriatti et al. 2008). An adequate sampling technique must be adopted to accurately determine the egg and larval population structure variability in space and time. Knowledge of the spatial distribution of L. botrana populations is important for developing efcient sampling programs that enable a more accurate assessment of the damage and the intervention threshold. Larvae are not randomly distributed in the eld (Badenhausser et al. 1999, Ifoulis and Savopoulou-Soultani 2006, Sciarretta et al. 2008) and are able to disperse from the original eclosion site; they can actively or passively disperse in all directions along the row (Torres-Vila et al. 1997). Dispersal capacity could modify the distribution of damage in the vineyard and must be considered in surveys. Geostatistical analysis has been used to characterize the spatial distribution of larval infestation, berry injury, and economic damage with the aim of developing accurate sampling plans for L. botrana (Ifoulis and Savopoulou-Soultani 2006). Insecticides applied in the past against L. botrana have been gradually replaced by materials that are more selective and less hazardous for human health. New neurotoxic insecticides (spinosyns and oxadiazines); chitin synthesis inhibitors; molting accelerat-

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ing compounds; microbial insecticides; and more recently, some avermectins and anthranilic diamides have been introduced into IPM strategies. To be effective, many of these substances must be applied when the pest is at its most susceptible stage, and so prediction of the moth development cycle is critical for determining an optimal treatment schedule. Selective insecticide programs supported by population monitoring using pheromone traps and egg scouting in the eld usually provide adequate control. Improvement in IPM is expected by the modeling of the developmental cycle (Moravie et al. 2006 and references therein). Alternative forecasting techniques are currently under development and include the evaluation of larval age distribution of the previous generation to predict the distribution of female emergence (Delbac et al. 2010). Use of Pheromones for Direct Control The rst evidence of an intra-specic olfactory communication in L. botrana dates back to eld observations by Feytaudt (1917). The structure and the behavioral activity of the female sex pheromone were identied in the 1970s and 1980s. The discovery of the main compound (E,Z)-7,9-dodecadienyl acetate (Roelofs et al. 1973, Buser et al. 1974) was followed by a more detailed characterization of the sex pheromone gland extracts, which identied at least 15 straightchain alcohol and acetate compounds, three of which are behaviorally active (Arn et al. 1988). Indeed, the addition of small amounts of (E,Z)-7,9-dodecadien1-ol and (Z)-9-dodecenyl acetate to (E,Z)-7,9-dodecadienyl acetate dramatically improved attraction of males to synthetic pheromone sources in a wind tunnel. According to El-Sayed et al. (1999), the optimum release rate of the main pheromone component based on the ight of males in a wind tunnel was 10 pg/min (i.e., 0.6 ng/h), and the optimum ratio of the minor compounds (E,Z)-7,9-dodecadien-1-ol and (Z)-9-dodecenyl acetate was 5 and 1%, respectively. Addition of 1 and 10% of (E)-9-dodecenyl acetate and 11-dodecenyl acetate to the three-component blend further enhanced male attraction in terms of the number of males reaching the source, straightness of the ight path, linear velocity, and decreased track angle of upwind ight. However, upwind ights were straighter and faster to natural sex pheromone (i.e., to calling females) than to the ve-component blend (El-Sayed et al. 1999). Recent chemical and electrophysiological analysis of gland extracts of L. botrana virgin females revealed the presence of three additional compounds not reported by Arn et al. (1988): (E)-7-dodecenyl acetate and the (E,E)- and (Z,E)-isomers of 7,9,11-dodecatrienyl acetate. These three compounds had a strong synergistic effect when added in small amounts to the main component. Interestingly, (E)-7-dodecenyl acetate was found only in gland extracts of L. botrana populations from southern Europe, whereas it was not detected in insects from north of the Alps, suggesting the occurrence of geographical pheromone races of L.

botrana (Witzgall et al. 2005). Although some of the minor components of the natural blend improve levels of attraction in wind-tunnel assays, only the main component, (E,Z)-7,9-dodecadienyl acetate, is used in the eld for both monitoring and pheromone-mediated control strategies. The pheromone gland is located on both the dorsal and the ventral side of the intersegmental membrane, between the eighth and ninth abdominal segments (Lalanne-Cassou et al. 1977; El-Sayed et al. 1998). This gland contains 1 ng of (E,Z)-7,9-dodecadienyl acetate (Buser et al. 1974), and during the peak of the female calling behavior, which occurs in the rst hour of the scotophase, females release 0.3 ng/h (Anfora et al. 2005). Recordings from single olfactory receptor neurons housed in sensilla trichodea of L. botrana male antenna showed the presence of a cell population primarily tuned to (E,Z)-7,9-dodecadienyl acetate (De Cristofaro et al. 2008). Moreover, as shown by electroantennogram measurements, L. botrana male antennae are responsive over a wide range of (E,Z)7,9-dodecadienyl acetate concentrations (from 0.1 to 2,500 ng), whether this compound is supplied on rubber septa or in lter paper (Schmitz et al. 1997b, Vitagliano et al. 2005). Once received by the male, the pheromone signal is transmitted by the olfactory receptor neurons to the antennal lobes, the primary olfactory center in the brain. As with other Lepidoptera, there is a large sexually dimorphic glomerulus in the antennal lobe of grapevine moth males that seems to be dedicated to the processing of the main pheromone compound (Masante-Roca et al. 2005). Knowledge of the sexual behavior of adults under natural conditions is essential for the purpose of manipulating their behavior with semiochemicals for population management. An important nding with respect to pheromone-based control strategies is that even delayed mating of females signicantly reduces their fecundity and fertility (Torres-Vila et al. 2002). The efcacy of pheromone-based control strategies also depends on the ability of moths to move through space. Field observations performed with marked insects subsequently captured with food traps showed that L. botrana is rather sedentary in comparison with other tortricids (Hughes and Dorn 2002). Although males can y a few meters over the vegetation to exploit air streams for longer distance migrations, females are generally less dispersive, and have not been observed to y further than 100 m (Roehrich and Carles 1981, Schmitz et al. 1996). Besides sex pheromones, intraspecic communication also is apparently mediated by semiochemicals present on the egg surface. Oviposition site selection may be regulated by an oviposition-deterring pheromone, which would explain the female behavior of laying isolated eggs on V. vinifera owers and grapes (Gabel and Thie ry 1992). Mating Disruption (MD). MD with hand-applied dispensers is the most well-studied and widely applied pheromone-mediated control technique used against L. botrana in the European wine-growing areas. Other pheromone techniques such as autoconfusion, lure-

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and-kill, false-trail following, aerosol puffers, and microencapsulated sprayables and nanobers (Underwood et al. 2002, Charmillot et al. 2005, Nansen et al. 2007, Anfora et al. 2008, Hein Detlef et al. 2011) are still under development and registration. The rst eld experiments to control L. botrana with MD were carried out in France (Roehrich et al. 1977) but inconsistent results and insufcient quantities of pheromone due to the difculties of large-batch synthesis (Descoins 1990) prevented full development of the control technique at that time. Field trials were restarted 10 yr later in France as well as in Switzerland, Germany, Spain, and Italy (Ioriatti and Vita 1990, Charmillot 1992, Louis and Schirra 1992, Perez Marin 1992, Stockel et al. 1992, Neumann et al. 1993, Kast 2001). This renewed interest resulted from favorable results obtained in MD control of Eupoecilia ambiguella (Hu bner), a species closely related to L. botrana (Charmillot et al. 1987, Neumann 1987). Currently, MD is applied against both species on 140,000 ha in European vineyards (3 4% of the total grape growing area in European Union). Recent MD area-wide applications have been carried out in Chile and California where L. botrana was accidentally introduced (Witzgall et al. 2010). The most commonly used hand-applied dispensers for MD of L. botrana in Europe are Shin-Etsu twist tie ropes (Isonet L, Isonet LE, Tokyo, Japan), the BASF twin ampoules (RAK 2, RAK 2R, RAK 1 2, Ludwigshafen, Germany), and the Suterra LLC membranes (Checkmate, Bend, OR). The active ingredient in these dispensers is the main pheromone component (E,Z)-7,9-dodecadienyl acetate, and the release rate for each dispenser is 50 60 g/h (Pasquier and Charmillot 2005). When aged for 1 yr in the eld, Isonet LE dispensers release a much higher amount of active ingredient per hour than a calling L. botrana female but are signicantly less attractive than a calling female in wind-tunnel assays (Anfora et al. 2005). Nevertheless, the same eld-aged Isonet LE dispensers exert a similar attraction to males as a freshly prepared rubber monitoring septa, both in the wind tunnel and in the eld. Apart from the active ingredient, which is represented by (E,Z)-7,9-dodecadienyl acetate, there is a large variation in the load as well as in the physical and chemical features of the dispensers, including size, shape, and thickness of the dispenser walls, leading to differences in release rates and dispenser life. As with MD of other moths, MD of L. botrana is the result of physiological and behavioral effects that can be classied as sensory adaptation, competition, and camouage (Carde 2007, and references therein). The relative importance of these three mechanisms and their role in reducing the location of females by males has been discussed by several authors. According to Bartell (1982), the prevailing mechanism depends on the technology for the distribution of pheromone, whereas according to Campion (1986), a combination of the three mechanisms occurs in the eld. Weatherston (1990) suggested that the three mechanisms could act in a sequential manner depend-

ing on environmental conditions and application procedures. More recently, Miller et al. (2006) demonstrated that the prevailing mechanism depends on the target species. In the vineyard, all the factors that inuence concentration, homogeneity, and atmospheric distribution of synthetic pheromone greatly affect the behavioral mechanisms of MD; these factors include plant spacing, training system, plant canopy, and leaf density according to the vine phenological stage. This is mostly due to the ability of foliage to absorb and release pheromone and to mitigate the effect of wind (Schmitz et al. 1997a, Sauer and Karg 1998). However, the specic mechanisms underlying MD against L. botrana are still debated, and different hypothesis have been proposed. Karg and Sauer (1997) hypothesized that, during the summer in vineyards with dense canopies, adaptation of the moth sensory system, habituation, or both of behavioral response are likely to occur. In contrast, Schmitz et al. (1995, 1997b) argued that sensory adaptation could not be important because such adaptation would require that the moths be exposed to much higher concentrations of sex pheromone than typically occurs in vineyards treated with MD dispensers. Camouage is also unlikely to be an important contributing mechanism because of the difculty in evenly permeating a vineyard with synthetic sex pheromone, particularly with individual point sources of sex pheromone; MD activity may be best explained by the mechanism of competition (Schmitz et al.1995, Miller et al. 2010). This mechanism also is enhanced by the grape leaves, which act as point sources of pheromone in vineyards treated with high doses of pheromone (Schmitz et al. 1997a, Sauer and Karg 1998). Population Density and MD Application Protocols. Population density is a key factor for MD success: above a certain population density, matings are not disrupted, regardless of ambient pheromone concentrations. For L. botrana, 4,000 pairs/ha is the critical density above which the efcacy of MD is dramatically reduced (Feldhege et al. 1995). Tethered females (Charmillot et al. 1987), eld cages (Doye and Koch 2005), and food traps (Thie ry et al. 2006) can be useful research tools to estimate the efcacy of the MD, but these methods are too labor-intensive for practical use. Pheromone traps are inefcient for this purpose because they do not capture males in pheromonepermeated vineyards. For these reasons, predictions of MD efcacy are usually based on quantifying eggs and larvae rather than adults. L. botrana numbers also can be assessed based on the percentage of infested clusters, and according to Stockel et al. (1992) and Charmillot and Pasquier (2000), a 510% cluster infestation during the rst generation considerably reduces the efcacy of MD in the following generations. The percentage of cluster infestation, however, depends on the training system (which determines the number of clusters per ha) and on pruning and other agronomical practices that affect egg, larval, and pupal mortality. These contributing factors vary widely among vineyards and cultivars. Because larvae are

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easily counted, predictions of MD efcacy with respect to L. botrana population density are usually based on larval numbers in commercial vineyards. Estimates of population density for predicting MD efcacy can be strongly inuenced by L. botrana distribution within the vineyard. Larval aggregations may lead to critical adult densities in parts of the vineyard, affecting the efcacy of MD (Badenhausser et al. 1999). Moreover, lower pheromone concentrations along borders combined with increased population densities there (Louis et al. 1997) account for difculties in obtaining satisfactory results along vineyard edges (Charmillot and Pasquier 2000, Varner et al. 2001). Border effects are obviously much reduced when MD is applied to wide areas, as is done in Northern Italy (Trentino, South Tyrol), Germany, Switzerland, and in certain growing areas in Spain (Ioriatti et al. 2008). Additional insecticide treatments may become necessary when population densities exceed the estimated efcacy thresholds of MD; these insecticides can be applied to the entire vineyard or to the borders or other possible hot spots. For MD to be effective, 500 hand-applied dispensers per ha must be installed in the vineyards before the onset of the rst seasonal ight; later applications will likely result in MD failure. Dispensers must be evenly distributed in the vineyard and should be attached to vine shoots so that the foliage protects them from direct exposure to sun and high temperatures. To compensate for atmospheric pheromone dilution along the plot perimeter, twice the number of dispensers must be applied along the borders (Descoins 1990). According to vine spacing, it may be possible to apply dispensers on alternate rows to reduce application cost. Estimated application time varies from 1.5 to 3.0 h/ha, depending on vineyard layout and work rate (Ioriatti et al. 2004). Efcacy Evaluation. MD efcacy evaluation is carried out by assessing the presence of adults and larvae by monitoring and eld scouting. Male captures in pheromone traps is considered the easiest way to evaluate MD efcacy. Zero captures in the traps is considered a necessary but insufcient indicator of effective MD because the amount of pheromone needed to disrupt male orientation to traps baited with synthetic lures is lower than the amount needed to disrupt mating, as is also the case for other tortricids. For this reason, the capture of even a few males in the same trap indicates a high risk of MD failure. The dependability of traps for monitoring adults might be increased by the use of high-dose lures; for example, such high-dose lures trapped codling moths, Cydia pomonella (L.), in pheromone-treated plots when standard lures did not (Charmillot and Bloesch 1987); the use of high-dose lures for monitoring MD of L. botrana in vineyards has not been sufciently investigated. A direct but more time-consuming method of monitoring L. botrana in MD-treated vineyards is to count preimaginal stages. For quantifying infestation rate, the following variables should be considered: percentage of infested clusters, number of larvae per inorescence, number of eggs and larvae per cluster,

and number of injured berries per cluster. The average number of larvae per cluster provides the most accurate assessment of MD efcacy. Whereas the number of larvae per inorescence (i.e., the number of rst generation larvae) is very quickly assessed in the eld, the accurate estimation of the larval population during the second and third generation requires destructive sampling and time-consuming dissection, particularly for varieties with compact grape bunches. Evaluations of MD based on the nal damage at harvest can be misleading because such damage, primary and secondary rots in particular, can result from factors in addition to larval feeding. Despite intensive research and substantial experience gained during the past two decades, the number of hectares of vineyard under pheromone-mediated MD against L. botrana is still limited. However, increasing quality standards for wine and table grapes, with respect to both larval injury and pesticide residues, are opening new opportunities for the adoption of MD in IPM programs. Areawide Use of MD: A Case Study. The main factors limiting the adoption of MD are socio-economic. Grower interest in innovative methods is often low, and participation is deterred because of a lack of information about how to implement MD, higher short-term costs, and fear of failure that is typically elicited by any new technique. L. botrana management by MD has been successfully implemented in the province of Trento (northern Italy) since 1998, when the local government decided to subsidize the areawide application of MD. A main aspect contributing to the success of this program was the tight interconnection between research scientists, extension entomologists, grower associations, and pheromone supply companies. The objectives of the MD program in the province of Trento (Trentino) were to 1) promote the image of clean agriculture that recognizes the value of environmental protection for tourism; 2) promote grape and wine production by enforcing high consumersafety standards; 3) replace neurotoxic pesticides with safer techniques; 4) reduce public and worker exposure to insecticides, including residential areas adjacent to vineyards; and 5) improve the professional skill of growers and consultants (Ioriatti et al. 2008). To convince farmers to join the project, the local government initially subsidized part of the dispenser cost. From 1998 to 2001, the public subsidy covered up to 50% of the cost of the dispensers for conventional farms and 100% for certied organic farms. Consultants and grower associations worked together in promoting MD and in organizing the eld application of the dispensers (Varner and Ioriatti 1992). Over 4 yr, the pheromone-treated area increased from 700 to 5,500 ha, and MD became the standard technology for the control of L. botrana in the region. From 2002 onward, the public subsidy gradually decreased while the MD area further increased to 9,000 ha in 2010, accounting for 90% of the grape-growing area in the province of Trento.

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Before MD was used, 60% of the growers controlled vine moths with two insecticide treatments per year, 31% treated only once, and 9% did not treat at all. Chlopyrifos methyl was the most widely applied insecticide, and 17 metric tons of the commercial formulation Reldan (Dow AgroScience, Indianapolis, IN) (recommended eld dose, 2 kg/ha) were sprayed every year in the vineyards of Trentino (Ioriatti et al. 1993). At present, after 12 yr of MD, insecticides are no longer needed for grape moth control in most of the area. Sporadic chemical treatments are applied only in small and isolated vineyards during the years more favorable for pest development. The risk of negative side effects of the pesticides on crops as well as on human beings is generally avoided (Ioriatti et al. 2007). The benet of MD technology results not only from its higher efcacy relative to insecticide sprays but also in its acceptance by the public. The withdrawal of chlorpyrifos methyl in summer, when public awareness is particularly high because of the increase in outdoor activities, has reduced the conict between the agricultural and the nonagricultural world. This is extremely important in a region like Trentino, where tourism is a key economic industry (Ioriatti et al. 2008). MD Efcacy: Complementary Elements Apart from all the above-mentioned elements, successful application of MD depends on other important factors that must be carefully considered for each area: these include natural biological control and the different susceptibility of diverse grapevine cultivars to L. botrana. The existing pheromone-based IPM programs can be strengthened by the implementation of natural biological control. Indeed, the effects of MD and L. botrana parasitoids and predators can be synergistic (Louis et al. 1997). For this reason, natural enemies must be properly protected and enhanced through the implementation of viable and environmentally friendly IPM strategies, including the use of ecological infrastructures in the vineyard (Boller et al. 2004) and, potentially, by the use of semiochemicals that modify parasitoid behavior (Chuche et al. 2006). Although grape cultivar susceptibility cannot be manipulated for pest control in established vineyards, the diverse tness of L. botrana on a given cultivar (Moreau et al. 2007) and the cultivars potential for incurring injury (Fermaud 1998) must be carefully considered in evaluating MD potential. Natural Enemies. The cohort of L. botrana natural enemies varies considerably both in time and space (Coscolla ` 1997, Marchesini and Dalla Monta ` 1994, Thie ry et al. 2001, Thie ry and Xuereb 2004, Bagnoli and Lucchi 2006, Chuche et al. 2006). Entomopathogenic fungi of the genera Spicaria, Beauveria, Paecilomyces, Aspergillus, Cephalosporium, Cladosporium, Penicillium, Citromyces, and Stemphylium can infect a large percentage of overwintering pupae (Coscolla ` 1997). The bacteria Bacillus thuringiensis Berliner ssp. kurstaki and aizawai are still effectively and exten-

sively used against L. botrana (Scalco et al. 1997, Shahini et al. 2010). Baculovirus orana was applied to grapes in Georgia and France some decades ago, but its further use has been limited by its slowness of action on L. botrana larvae (Chkhubianishili and Malaniya 1986). Arthropods associated with L. botrana include predators such as spiders (Clubionidae, Theridiidae, Tomisidae, Linyphiidae, and Salticidae), mites (Thrombididae), and insects belonging to the Dermaptera, Hemiptera, Neuroptera, Diptera, and Coleoptera (Marchesini and Dalla Monta ` 1994). Among insect parasitoids, the complex of species associated with L. botrana in Europe includes mainly Hymenoptera Ichneumonoidea (Ichneumonidae and Braconidae), Chalcidoidea (Chalcididae, Pteromalidae, Eulophidae, Elasmidae, and Trichogrammatidae), and one species belonging to Diptera (Tachinidae) (Bagnoli and Lucchi 2006). As for most natural enemies of L. botrana, the role played in natural control by each species of parasitoid is greatly variable in space and time; under the most favorable conditions, the percentage of parasitism can reach 80% (Thie ry and Xuereb 2004). Typically, the frequency of egg and larval parasitoids is high in the rst two generations and decreases drastically in the overwintering generation, which is mainly affected by larvalpupal and pupal parasitoids. Regardless of the extensive scientic effort to apply biological control against L. botrana, an effective method for a practical use in the eld is still lacking. Egg parasitoids of the genus Trichogramma have been articially released against L. botrana according to the inundative strategy but with inconsistent results (Stellwaag 1929, Ibrahim 2004). The pteromalid Dibrachys afnis Masi was employed 15 yr ago in the Russian vineyards (Dergachev 1995). This species and Dibrachys cavus (Walker) are gregarious generalist larvalpupal parasitoids of Lepidoptera, Diptera, and Hymenoptera and are quite easily raised in the laboratory. Because they have low host selectivity and are prone to act as hyperparasites, applied entomologists have not attempted to use them for biological control of L. botrana. The most active, frequent, and efcient parasitoid in European vineyards is the larval parasitoid Campoplex capitator Aubert (Hymenoptera: Ichneumonidae). In a 2-yr study in French vineyards, this species had an average parasitism rate of 40% (Xuereb and Thie ry 2006). C. capitator is still regarded as the best candidate for L. botrana biological control, but its application in the open eld has been prevented by difculties in its mass rearing (Thie ry and Xuereb 2004). Effect of Food Quality on Life-History Traits. L. botrana time of development, mating success, fecundity, egg size, and fertility are affected by the grapevine cultivar that the larvae feed on (Moreau et al. 2006a,b; Moreau et al. 2007). Additional factors such as nutritional quality of different parts of V. vinifera berries (Moreau et al. 2006c) or phenological stage of vine during larval feeding (Torres-Vila 1999) signicantly inuence male and female performance. Larval food also can affect L. botrana preference for oviposition

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substrate. Females raised as larvae on grapes preferred to lay eggs on the cultivar that they had experienced (Moreau et al. 2008). The total number of spermatophores produced by L. botrana males as well as the volume of the rst spermatophore were dependent on the vine cultivars that they had fed upon in the laboratory (Torres-Vila et al. 1999). Within the same cultivar, the phenological stage could be a potential factor affecting development, insect size, and male reproductive performance. L. botrana larvae fed on ripe grape berries produced larger adults than larvae fed on unripe fruit and inorescences. At the same time, the number of spermatophores transferred was two-fold higher in males reared on ripe berries than in males reared on inorescences, probably because of differences in the protein/sugar ratio of the ingested food (Savopoulou-Soultani et al. 1994, Torres-Vila et al. 1999). Improvement in the reproductive performance (reduced larval mortality, shortened development time of the larvae, and increased pupal weight, female longevity, female fecundity, laying duration, and mating success) was obtained when a laboratory strain of L. botrana was reared on alternative host plants to Vitaceae (Thie ry and Moreau 2005). In Greece, a natural population of L. botrana larvae developed 23 d faster on olive (Olea spp.) owers than on grapevine inorescences (Savopoulou-Soultani et al. 1990). In France, L. botrana tness was higher on D. gnidium and O. europaea than on the vitaceous plants V. vinifera or Ampelopsis brevipedunculata (Maximowicz) (Thie ry and Moreau 2005). Some innovative studies on the interaction between L. botrana and the phytopathogenic fungus B. cinerea have demonstrated a mutualistic relationship between these two organisms. The positive effect of the fungus on insect development and oviposition behavior was directly correlated to the presence of fungal sterols in the diet (Mondy et al. 1998). The oviposition preference for grapes inoculated with a pool of grape-borne yeast was reported in a recent study (Tasin et al. 2009). Host Preference and Plant External Features. The number of eggs laid by L. botrana females and the survival of neonate larvae can be affected by the grapevine cultivar (Fermaud 1998, Sharon et al. 2009). During the rst ight of L. botrana, females strongly prefer smooth surfaces for oviposition and avoid owers that are hairy (Geisler 1959, Galet 1982, Maher and Thie ry 2004, Pavan et al. 2009). In addition, survival of larvae is greatly inuenced by phenological changes of the inorescences. According to Torres-Vila et al. (1992) and Gabel and Roehrich (1995), the mortality of newly hatched larvae is high until fructiferous organs differentiate, and mortality decreases to the lowest level just before blooming. The lack of synchrony between the most sensitive phenological stages of the vine, i.e., no. 15 and 17 according to Eichhorn and Lorenz (1977), and the peak of eggs eclosion can account for a pseudo-resistance. This varies according to latitude and climate. Anthesis was conrmed as an important mechanism reducing the establishment of larvae (Torres-Vila et al. 1992). Physiological thinning of the infested grape, rapid grape development, as well

as rigidity of the peduncle that impedes the larval nest formation also are reported as factors that can affect larval survival (Coscolla ` 1997). Moreover, cultivars with tight grape bunches are much more susceptible to L. botrana infestation (Bagnoli 1990). Chemical Interaction With the Host Plant Role of Olfactory Cues in Host Finding. L. botrana females are attracted by grape odor for egg-laying on ower buds and berries at different phenological stages (Tasin et al. 2005, Masante-Roca et al. 2007). Studies on the perception and the processing of plant volatiles in L. botrana at the level of both the central and peripheral nervous system led to the identication of a number of physiologically active compounds, and wind tunnel bioassay enabled the determination of the behavioral relevance of these compounds (MasanteRoca et al. 2002; Masante-Roca et al. 2005; Tasin et al. 2005, 2010). Female attraction to plant volatiles also has been found in the North American grape berry moth, Paralobesia viteana (Clemens) (Cha et al. 2008a, Cha et al. 2011). Based on the analysis of the shoots of Vitis riparia Michx, a synthetic blend was formulated that, when used as bait in traps, caught females of P. viteana in a vineyard (Cha et al. 2008b). In L. botrana females, synergism and redundancy of the attractive olfactory signal has been demonstrated for a number of compounds. This response may reect the behavioral plasticity of L. botrana, which oviposits on a large number of host plants with a different volatile proles, including the ax-leaved daphne, D. gnidium (Tasin et al. 2006b, 2007, 2010). In addition, attraction of L. botrana females to a blend composed of a few synthetic grapevine volatiles is ratio-dependent (Tasin et al. 2006a, Anfora et al. 2009), but this is not the case for blends of a large number of compounds (Tasin et al. 2010). In wind tunnel experiments, Tasin et al. (2010) reported that L. botrana females discriminated among host plants, and attraction was greater for plants with a higher suitability for the development of offspring (D. gnidium versus V. vinifera). A highly complex odor (a blend of 11 compounds) was identied from the most attractive plant. Volatiles from grape also have recently been found to be behaviorally active on L. botrana larvae (Becher and Guerin 2009). L. botrana females also are capable of detecting the odor of naturally occurring microorganisms that increase the food quality of the host plant for larvae (Mondy et al. 1998). In vineyards, L. botrana females were observed to y not only to grapevines but also to the nonhost plant tansy (Tanacetum vulgare L.), probably for nectar foraging (Gabel 1992). Nonhost volatiles from tansy owers did not affect the ight behavior of virgin females in the wind tunnel but it increased the proportion of mated females that initiated ight (Hurtrel and Thie ry 1999). The steam distillate of tansy as well as a synthetic blend of electrophysiologically active compounds released by this plant elicited attraction in a eld cage (Gabel et al. 1992). Nonetheless, the attraction to owers or leaves

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of tansy could not be conrmed in the wind tunnel study reported by Masante-Roca et al. (2007). Fermenting apple juice was assessed as a potential bait to trap L. botrana adults and to predict oviposition dynamics in the eld (Thie ry et al. 2006), but its wide use as monitoring tool for consultants and farmers is hampered by time-consuming maintenance and low selectivity. In contrast to mated females, males and virgin females are not responsive to volatile plant compounds alone (Masante-Roca et al. 2007). When presented in mixtures with the main component of the female sex pheromone (E,Z)-7,9-dodecadienyl acetate, however, plant volatiles signicantly enhanced the attractiveness of males to the pheromone (Sharon et al. 2009), which also has been documented for E. ambiguella (Schmidt-Busser et al. 2009) and a number of other moths (Reddy and Guerrero 2004). That olfactory receptor neurons on the antennae of L. botrana respond to both the main pheromone component and plant volatiles further supports the hypothesis of a physiological interaction between these two categories of compounds (De Cristofaro et al. 2008). Role of Volatile and Nonvolatile Stimuli on Oviposition. Berry extracts of V. vinifera and leaf and berry extracts from D. gnidium triggered oviposition in L. botrana females (Maher 2002). Polar surface compounds of grape berries acted as dose-dependent oviposition stimulants (Maher and Thie ry 2004). The response varied according to the plant part and its phenological stage (Maher and Thie ry 2006, Maher et al. 2006). For example, an extract from D. gnidium stems was repellent, whereas an extract from D. gnidium berries triggered oviposition. Chemical analysis of the active extract from these berries showed the presence of several compounds that trigger oviposition. When an extract from D. gnidium berries was sprayed on grape berries and the sprayed and unsprayed grapes were compared in a choice test, L. botrana females laid signicantly more eggs on the sprayed grapes (Maher and Thie ry 2006). Tarsal contact-chemoreceptor sensilla are sensitive to fructose and sucrose, and they may be of special importance for exploiting fruit as an oviposition site (Maher et al. 2006). The effect of plant volatiles on oviposition was investigated by Anfora et al. (2009). In a laboratory assay, volatiles released from a grape bunch signicantly triggered L. botrana oviposition. A blend of synthetic compounds identied from grape produced the same effect, indicating a role of volatile compounds in the oviposition response. In a eld experiment, synthetic grape volatiles released from a septum both attracted mated females and stimulated oviposition on vegetation near the lure (Anfora et al. 2009). Savopoulou-Soultani and Tzanakakis (1981) reported a signicant increase in the fecundity of laboratoryreared L. botrana females (from 72 to 118.8 eggs per female) by the introduction of vine leaves and grapes into the oviposition cups containing the adults. Given the importance of both contact and olfactory chemoreception in L. botrana, the behavioral response of the egg-laying female may thus be the outcome of a mul-

tisensory modality. Accordingly, a recent study by Tasin et al. (2011) determined that although L. botrana female behavior in response to plants was largely based on olfaction, olfaction showed strong synergistic interactions when co-occurring with vision or with vision and contact. This emphasizes the necessity of additional research on the interaction between different sensory cues during oviposition. Future Directions in Research and IPM Pheromone-mediated mating disruption and other pheromone techniques are most effective at low population densities and are therefore powerful tools for the management of and even the eradication of insect invasions (El-Sayed et al. 2006, 2009; Liebhold and Tobin 2008). Insecticides, however, are required for the management of high densities of established insect populations in agricultural or horticultural crops. As discussed earlier, high populations must be brought to threshold levels by insecticide sprays before pheromones can be used efciently. One future research challenge is to determine whether female attractants, for example host plant volatiles (Tasin et al. 2010), in combination with mass trapping or lure-and-kill techniques might become an alternative to curative insecticide treatments. It is, however, still unclear whether plant volatiles can be as attractive to females as sex pheromones are to males. One main drawback in the search for plant volatile lures is the lack of a correlation between the production of these plant signals and their behavioral relevance, which is contrary to the case with insect pheromones. Because L. botrana feeds on many plants, several different blends of plant volatiles can stimulate oviposition (Tasin et al. 2010). Volatiles from plants other than grape would likely be more suitable than volatiles from grape for eld trapping in vineyards because the background vine odor is likely to interfere with attraction to lures containing synthetic vine odors (Knudsen et al. 2008). The most powerful plant volatile lure for codling moth, a pest of apple (Malus spp.), is derived from its alternative host, the pear (Pyrus spp.) (Light et al. 2001). The effort required to identify behaviorally active plant volatiles through chemical headspace analysis, followed by behavioral studies of multicomponent volatile blends, is substantial (Tasin et al. 2005, 2007), and this approach is hardly feasible for screening several L. botrana host plants for attractant compounds. Instead, molecular tools now offer the opportunity to accelerate the search for novel attractants via identication of odorant receptor genes and characterization of their ligand specicity (Jacquin-Joly and Merlin 2004). The feasibility of this approach has been demonstrated with pheromone receptors in the silkworm, Bombyx mori L. (Krieger et al. 2004, Sakurai et al. 2004), and more recently with plant volatile receptors in the light brown apple moth, Epiphyas postvittana (Walker) (Jordan et al. 2009). Identied ligands can then be further assayed in vivo by peripheral antennal recordings and by intracellular recordings from individual projection neurons in the antennal

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lobe, the olfactory center of the insect brain. Intracellular recordings have been established in tortricids including the L. botrana and codling moth (MasanteRoca et al. 2005, Trona et al. 2010). Further research on behavior-modifying chemicals and L. botrana behavioral and chemical physiology and ecology will enhance management of this pest provided that concurrent efforts are made to improve communication between research institutes, extension services, grower associations, and plant protection industries. This interface between research and the end user, or the lack of it, accounts for the tremendous geographical variation in the application of biorational control techniques in European winegrowing areas.

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