Drosophila (Sophophora) suzukii (Matsumura), new pest of soft fruits in Trentino (North-Italy) and in Europe

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1 Integrated Plant Protection in Soft Fruits IOBC/wprs Bulletin 70, 2011 pp Drosophila (Sophophora) suzukii (Matsumura), new pest of soft fruits in Trentino (North-Italy) and in Europe Alberto Grassi 1, Lara Giongo 2, Luisa Palmieri 2 Edmund Mach Foundation (FEM), 1 Technology Transfer Centre; 2 Research Centre, via Edmund Mach n 1, S. Michele all Adige, Trento, Italy Abstract: In September 2009, spotted wing drosophila (SWD), Drosophila (Sophophora) suzukii (Matsumura), was detected for the first time in Italy and Europe on raspberry (Rubus idaeus L.), highbush blueberry (Vaccinium corymbosum L.) and strawberry (Fragaria x ananassa Duch.) in several cultivated fields in Trentino (North-Italy). In 2010, an investigation was carried out with the aims to better understand the distribution of this species in the Province of Trento, to determine the hosts range (cultivated and spontaneous), to deepen the biology and behaviour of the pest and to set up a well-reasoned management plan. The results indicate that, in one year, D. suzukii colonised the whole territory. About 23,000 adults were caught from the beginning of July till the end of November in 82 apple cider vinegar traps placed in forest and cultivated sites located from 97 to 1458m a.s.l. Eggs and larvae were detected in fruits of sweet cherry, apricot, blueberry, strawberry, raspberry, blackberry, fig, wine grape and also in fruits of spontaneous hosts (Lonicera spp., wild blackberry, Sambucus nigra, Frangula alnus). Important crop losses (30-40%) were reported by Sant Orsola local soft fruit growers association especially on highbush blueberry and blackberry. The efficacy of some insecticides was evaluated in open field trials; amongst the few chemicals registered on soft fruits in Italy, lambda-cyhalothrin gave satisfying results and a moderate effectiveness was obtained with spinosad. A spinosad-bait spray formulation (Spintor Fly, Dow AgroSciences) was also tested and it achieved a modest efficacy. Severe damage might occur every season if insecticides and sanitation measures (removal and destruction of any overripe, rotting and infested fruit) are not applied during the ripening period. The increase in the use of pesticides might compromise the IPM on soft fruits (e.g. biological control of Tetranychus urticae on raspberry) and it is unsustainable over a long period for the negative impact on the environment. It is important to test as soon as possible alternative control methods (pheromones and other attractive substances, mass trapping, biological control methods, oviposition deterrents, physical barriers, etc.). Key words: Spotted wing drosophila (SWD), Drosophila (Sophophora) suzukii Matsumura, soft fruits, Trentino Introduction After the first report of Drosophila (Sophophora) suzukii in Trentino, the European Plant Protection Organization (EPPO) has included it in the Pest Alert List. In July 2010, a Pest Risk Analysis was performed, since spotted wing drosophila (SWD) was identified as a possible threat to all European and Mediterranean countries. During 2010, the pest has been officially recorded also in other regions of Italy (i.e. South Tyrol, Piedmont, Campania, Tuscany) and European countries (i.e. Spain and France, where it had been detected in traps respectively since 2008 and 2009). Drosophila suzukii is one of the two species of the genus Drosophila to lay eggs in healthy (whole) fruits instead of damaged or overripe ones (Sasaki & Sato 1995, 1996). It preferentially oviposits on mature fruits but can also lay eggs on immature and spoiled fruit of 121

2 122 suitable varieties at lower rates (Kanzawa 1939, Mitsui et al. 2006). The larval feeding causes the fruit to collapse around the oviposition site. The oviposition scar exposes the fruit to secondary attack by pathogens and other insects (Hauser & Damus 2009). The damage caused by SWD larvae renders the fruit unmarketable (Bolda et al. 2010). Soft fruits and strawberry production is an important component of agriculture in Trentino, where these fruits showed a high intrinsic susceptibility to SWD infestations, probably because of their long harvest period, thin skin and sweet juicy pulp. In 2010, we conducted a monitoring study, field and lab surveys to better understand the distribution of the pest in Trentino, to deepen its biology and seasonal phenology, to determine the hosts range (cultivated and spontaneous). Two field trials were also carried out on highbush blueberry to evaluate the efficacy of insecticides in controlling SWD infestations. Molecular analyses were also performed on adult specimens sampled in different places, with the objective to confirm the species identification. Material and methods Monitoring of SWD adults flight activity To determine the distribution of this pest in Trentino and the seasonal adults flight activity, we used 82 apple cider vinegar traps. A trap consisted of a durable plastic bottle of ml capacity with a screw-top. Five to six mm diameter holes were drilled on the side and 200ml of apple cider vinegar was added as a bait. The traps (one per site, hung on shady side of the plant) were deployed in some woody areas, fields of highbush blueberry, raspberry, blackberry and strawberry and orchards of sweet cherry, apricot, plum, wine grape and apple. Some of the orchards and soft fruit fields were not mono-cropped. In most of the cultivated sites, traps were deployed before the fruits reddening and remained on place till the end of November (post-harvest period). The traps were replaced once a week, the solution was filtered in laboratory and males and females were counted under dissecting microscope. Fruits infestation assessment Samples of fruits ( soft fruits; cherries and apricots) at the right commercial ripening stage, were collected during the season from 22 of the monitored fields and orchards to estimate the infestation level. Infestation was also verified on fruit samples from spontaneous hosts in the boundaries of the plantations or in woody areas. Fruits were inspected under dissecting microscope to search for the eggs; these are inserted just below the skin and two white fine breathing tubes emerge from the oviposition scar. The fruits were then dissected to verify the presence of larvae inside the pulp. A small rearing of the pest was kept in laboratory and used to assess the susceptibility to SWD infestation of mature and immature (wild and cultivated) fruits. Evaluation of insecticides efficacy An experiment to evaluate the effectiveness of some insecticides in reducing fruits infestation, was carried out in a highbush blueberry plantation of cv. Brigitta located in Susà, Pergine Valsugana. Each treatment (Table 1) was applied to randomized unreplicated blocks of 40 bushes. A motorized knapsack sprayer (mod. SEH06/Italdifra, 7.5bar working pressure) was used to apply the insecticides at a water volume of 1700 l/ha. The insecticides were sprayed the 18 th of August. To assess the infestation, samples of 50 fruits/block at the right ripening stage were taken the day before the treatment as well as 2, 6, 9 and 13 days after. Each fruit was inspected to verify the presence of eggs and/or larvae.

3 123 Table 1. Details of the treatments for the evaluation of insecticides efficacy. Treatments (insecticide) Active ingredient and concentration Product dose rate/ha (l) check - untreated - - Calypso thiacloprid 40.4 % 0.34 Trebon etofenprox 30 % 0.85 Laser spinosad 44.2 % 0.34 Karate Zeon lambda-cyhalothrin 9.48 % 0.34 We evaluated the efficacy of a 0.024% spinosad bait spray commercial formulation (Spintor Fly, DowAgroscience) as well (Table 2). The product was applied in a 1400m 2 highbush blueberry plantation of cv Brigitta and Elliot, located in Samone, Valsugana. An untreated plantation in the same area, at a distance of about 100m, was used as a check plot. A hand-held sprayer was used to deliver the bait solution in spots of about 30cm diameter on bush canopy. A larger water volume was used after the first application, in order to improve the bait delivery and increase the number of spots. The fruits infestation in treated and untreated plots, was assessed on samples of 50 fruits at the right ripening stage, randomly collected the day before the first application and 7, 12 and 21 days after. Each fruit was inspected to verify the presence of eggs and/or larvae. Table 2. Details of the Spintor Fly treatments. application 1 application 2 application 3 Date of spray Water volume/ha (l) Spintor Fly dose rate/ha (l) Spinosad dose rate/ha (ml) Molecular analysis DNA was extracted from four Drosophila specimens sampled in four different places in Trentino (i. e. Pinè, Cembra valley, Valsugana, Vigolana plateau) using NucleoSpin Food II kit. The DNA integrity and quantity was evaluated using DNA-Chip (Biorad) on an Experion platform. PCR analysis was performed following the protocol by Calabria et al. (2010). PCR products were sequenced and these were compared with the ones present in NCBI database. Results and discussion Territorial monitoring and fruit infestation assessment Just one year after the first detection, SWD has colonised the whole territory of the Province of Trento (Figure 1). The insect was caught both in cultivations and in forests, from 97m a.s.l (Pratosaiano, Laghi Valley) to 1458m a.s.l (Redebus Pass, Mocheni Valley). This demonstrates the considerable abilities to spread, the rapid adaptability to different

4 124 environments and the capability of food resources exploitation of this exotic pest. This species probably finds in Trentino optimal conditions for its development for many reasons: widespread cultivation of susceptible crops (mainly soft fruits and cherry), distribution of the cultivated land on different altitudes (offering a differentiated and extended fruit ripening period), and richness in forests, uncultivated and marginal areas (private gardens, urban public parks), often very close to the plantations. Figure 1. Map of Trentino and data of SWD catches in each of the monitored areas. Around 13% of the total number of adults was caught in traps deployed in woods. Eggs and larvae of SWD were detected in fruits of spontaneous hosts (Sambucus nigra, Lonicera spp., Frangula alnus, wild blackberry) in hedgerows. Moreover, the egg laying was documented in rearing conditions on berries of Morus nigra, Prunus laurocerasus and Vaccinium myrtillus. For most of the season, adults flight activity and attacks were concentrated in cultivated areas close to the forests, above m of altitude. SWD seems to have important relationships with the forest, where it might probably overwinter, to find suitable hosts on whom to begin its breeding and continue it till late autumn, and to find a refuge during the hottest periods of the summer. The variability in the total number of adults caught by the traps in the monitored areas (Figure 1) indicated a different development of local populations that might be associated with the microclimate and the diversity of the host species. The pest might have increased in geographically stable populations in those areas

5 125 where susceptible host species are more abundant and ripen in succession. Moreover, abundant adult catches occurred particularly in plantations where the harvest was rather incomplete and/or inaccurate and insecticides for the control of SWD were not applied. The insect appeared in the crops at the beginning of July and spread very fast; at the end of the same month it was already present in all the monitored valleys. A population outbreak occurred till the end of November (Figure 2). The pest developed on several fruits of spontaneous and cultivated hosts which ripe in succession in forests and plantations and that the adults found thanks to remarkable and frequent scouting flights in the territory. Probably 8-9 generations developed rapidly, overlapping during the season. The sex ratio of the adults caught in the traps was always slightly male predominant, except on very few occasions when females were more abundant. The adult catches peaked at the end of the season (October/November), in the post-harvest period; at this time, many adults were very active also on the bottom of the valleys, in search of the last cultivated or wild fruits for feeding and laying their last eggs. Apple cider vinegar traps were probably more attractive at the end of the season than during the fruiting period. 8 Development of SWD adults catches in apple cider vinegar traps in Trentino in mean n of adults/trap/day week number Figure 2. Apple cider vinegar trap catches of D.suzukii adults ( + ) in 2010 in Trentino. The first damages on cultivated fruits were recorded on sweet cherry in the second half of July. More than 90% of late harvested cherries in some orchards on Vigolana plateau and in Giudicarie Valley were infested by SWD eggs and larvae, even if the insecticides phosmet and acetamiprid had been sprayed at the reddening of the fruits for Rhagoletis cerasi control. Sweet cherry is a crop highly susceptible to SWD and a very important host for the seasonal development of its population and infestation. In August, from 20 to 50% of apricots sampled from orchards located in the same cherry production districts, resulted infested by SWD eggs detected also on hard and unripe (green/orange) fruits. About 32% of the total number of adults was caught in traps deployed in apricot orchards. Most of them were caught after the harvest time. Adults that emerged from infested fruits fallen from trees during the harvest and not removed, contributed to these high catches.

6 126 The damage on strawberry was negligible (2-3%) until the end of August. Probably, the frequent use of insecticides on this crop during the summer for the control of other important pests (e.g thrips, Lygus spp., Anthonomus rubi) contributed to limit SWD attacks. But a considerable damage (60-80%) was recorded in September on the last harvested fruits of late ripening strawberries (in Tesino and Vanoi sites), when the insecticides pressure was reduced. Severe infestations occurred in the middle of summer (July/August) on the early ripening cultivated blackberry of cv. Lochness. Sant Orsola local soft fruits growers association (APASO) reported a 30-40% loss of production on this crop. In September and October, from 60 to 100% of red raspberry fruits sampled at the right commercial ripening stage (pink/red colour) in some untreated plantations, were infested by eggs. Eggs were found till the beginning of November. One of the main reasons for this high susceptibility was the long harvest period, that unfortunately occured during the peaks of SWD adult flight in Trentino. Moreover, because of the presence of both flowers and fruits and the necessity to protect pollinators and respect the pre-harvest interval, there were difficulties in correctly timing the insecticide treatments against SWD. Highbush blueberry was one of the most damaged crop. In some sites (e.g Samone, in Valsugana South), % of the fruits were infested at the end of harvest. APASO reported a 30-40% loss of production due to SWD infestation. Additional severe losses occurred after a long fruit storage period, since during this time undetected eggs and very young larvae continued to develop inside the pulp. On blueberry, eggs were frequently recorded also on unripe fruits. Besides a very long harvest period, the high number of ripe fruits that fall on the ground or remain on the bushes during the harvest represented one of the main reasons for this high susceptibility. On soft fruits, the damage tended to increase from the beginning to the end of the picking period, since many adults concentrated their damage on few fruits. The highest levels of damage on cultivated fruits were observed where no insecticides for SWD control were applied and where the harvest was incomplete or sanitation measures (i.e. removal and destruction of any overripe, rotting and infested fruit) were not included. Adults were caught also in apple orchards and vineyards, but SWD eggs and larvae were detected in autumn only on over-ripe bunches of wine grapes. The damage on this crop was difficult to estimate. Many eggs had been counted on figs collected from a tree in Vigalzano, Pergine (Valsugana North). No damages were recorded on red currant. Insecticides efficacy assessment Results indicated a satisfactory efficacy of lambda-cyalothrin (Table 3) in reducing fruits damage. This pyrethroid showed a max. efficacy of 93% and quite a long persistence (at least 9-10 days). Unfortunately, it is only permitted on raspberry, with seven days of PHI. Also the effectiveness of spinosad was quite good (max 67%), but its persistence was less than 6-7 days. The performances of thiacloprid (neonicotinoid) and etofenprox were unsatisfactory. Spintor Fly (0.024% spinosad bait spray) achieved a modest efficacy, even if application rate/ha was increased after the first spray (Table 4). This compound might perform better in low pressure pest situations, starting the applications on a wide cultivated area before the beginning of the infestations, and in combination with other insecticide sprays.

7 127 Table 3. Efficacy of tested insecticides in controlling SWD infestation. Treatments % infested fruits T - 1 T + 2 % eff. T + 6 % eff. T + 9 % eff. T + 13 % eff. check plot thiacloprid etofenprox spinosad lambda cyhalothrin Table 4. Efficacy of spinosad bait spray Spintor Fly in controlling SWD infestation. % infested fruits Treatments after 1 appl. after 2 appl. after 3 appl. T -1 T+7 T+12 T ' ' ' '10 check plot - untreat.plantation Spintor Fly treated plantation % efficacy Molecular analysis DNA was extracted in good quantity from each of the samples. The PCR analysis gave the expected amplification profile (~700 bp) for each individual analyzed. The comparison of our sequences with the sequences present in the database, confirmed that all the analyzed samples were D. suzukii. Conclusions Just one year after its first record, SWD has become the major pest of soft fruits (but also of other fruits) in Trentino. It is evident that severe damage might occur every season if sanitation measures (removal and destruction of any overripe, rotting and infested fruit) and insecticides are not applied during the ripening period. It is urgent to provide growers with more efficient insecticides, possibly of different type and modality of action in order to avoid resistance problems in the SWD populations. The increase in the use of insecticides might compromise the IPM on soft fruits (e.g. biological control of Tetranychus urticae on raspberry) and it is unsustainable over a long period for the negative impact on the environment. It is important to test as soon as possible alternative control methods (pheromones and other attractive substances, mass trapping, biological control methods, oviposition deterrents, physical barriers, etc.). Acknowledgements We are grateful to all the advisors and colleagues of the Technology Transfer Centre at IASMA Foundation and to Dr. Frontuto Alessandro of the Regional Plant Protection Service of the Autonomous Province of Trento for their important contribution in the management of

8 128 the territorial monitoring plan. Many thanks also to Sant Orsola soft fruit growers association that provided us the plantations where to test insecticides and to Dr.Vaughn Walton (Oregon State University, Dept. of Horticulture) for his precious support and the exchange of technical information. References Bolda, M., Goodhue, R. E & Zalom, F. G. 2010: Spotted wing drosophila: potential economic impact of a newly established pest. Agric. Resource Econ. Update, Univ. Calif. Giannini Foundation Agric. Econ. 13(3): 5-8. Calabria, G., Máca, J., Bächli, G., Serra, L. & Pascual, M. 2010: First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. Journal of Applied Entomology. DOI: /j x Hauser, M., Gaimari, S. & Damus, M. 2009: Drosophila suzukii new to North America. Fly times no. 43: Kanzawa, T. 1939: Studies on Drosophila suzukii Mats. Kofu, Yamanashi Agric. Exp. Sta.: 49 pp. Abstract in Review of Applied Entomology 29: 622. Mitsui, H., Takahashi, K. H., & Kimura, M. T. 2006: Spatial distribution and clutch sizes of Drosophila species ovipositing on cherry fruits of different stages. Popul. Ecol. 48: Sasaki, M. & Sato, R. 1995: Bionomics of the cherry drosophila, Drosophila suzukii Matsumura (Diptera: Drosophilidae) in Fukushima prefecture (Japan). Annual report of the Society of Plant Protection of North Japan 46: Sasaki, M. & Sato, R. 1996: Bionomics of Drosophila pulcherella Tan, Hus et Sheng (Diptera: Drosophilidae) in Fukushima prefecture (Japan). Tohuku Agric. Res. 49: