EPPO Datasheet: Drosophila suzukii
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Diptera: Drosophilidae
Common names in English: cherry drosophila, spotted-wing drosophila (US)
view more common names online...
Notes on taxonomy and nomenclature
In June 1916, maggots were found to be infesting cherries (Prunus avium) in Yamacho, Higashi Yamanashi County, Yamanashi Prefecture, Japan (Kanzawa, 1935). Infested fruits were collected and the adult flies that emerged were confirmed as a species of Drosophila (Kanzawa, 1935). The species was later described in 1931 by Dr Shounen Matsumura as Drosophila suzukii Matsumura, and he gave it the common name of cherry drosophila (Kanzawa, 1935). Little is known about its geographical origin; it is considered native to Far-East Asia (China, Japan and Korean Peninsula) but it was described also in the Kashmir region of India as the D. suzukii subspecies indicus (Parshad and Paika, 1965). D. suzukii belongs to the subgenus Sophophora, which is divided into several species groups. One of them, the melanogaster species group, also contains the famous species, extensively used in experimental biology and genetics, Drosophila melanogaster Meigen (Powell, 1997). The melanogaster group is further divided into species subgroups, one of which (the suzukii subgroup) comprises, together with 6 other subgroups, the ‘Oriental lineage’ (Kopp and True, 2002; Schawaroch, 2002; van der Linde et al., 2010). However, relationships between and within these subgroups are still far from being resolved, and the suzukii subgroup itself is commonly regarded as polyphyletic (Kopp and True, 2002). Recent papers suggested that D. biarmipes is a sister taxon of D. suzukii (Yang et al., 2011; Chiu et al., 2013; Ometto et al., 2013; Rota Stabelli et al., 2013), in accordance with previous findings (Kopp and True, 2002; Barmina and Kopp, 2007). However, other studies by Prud’homme et al. (2006) and van der Linde and Houle (2008) supported that D. subpulchrella is a sister species of D. suzukii (with D. biarmipes being the sister species of D. subpulchrella + D. suzukii).
EPPO Code: DROSSU
This species is predisposed towards infesting living material and prefers to infest, and subsequently develop in, slightly under ripe undamaged fruit. Fruits become susceptible to D. suzukii as they start to colour. D. suzukii has been shown to possess a broad host plant range, with thin-skinned berries (e.g. cranberries, blueberries, strawberries, raspberries) and stone fruits (e.g. cherries, peaches, plums) being particularly susceptible to infestation (Bellamy et al., 2013). Grapevine, Vitis vinifera, is also counted among the host plants of this pest. However, it has been shown that only some varieties, due to their chemical-physical characteristics, are susceptible to oviposition during the ripening phase (e.g. the "Schiava" variety) (Ioriatti et al., 2015; Baser et al., 2018). D. suzukii in fact prefers above all varieties with red fruits or berries, late harvest and less firm skin. The role of D. suzukii as a vector of microorganisms responsible for vine acid rot has been also demonstrated (Ioriatti et al., 2018). Differences in fruit susceptibility are present between species and also between varieties within the same fruit species (Lee et al., 2011). Fruit penetration force is one potential measure of host susceptibility, but host attractiveness will likely depend upon additional factors, such as soluble sugar content (Burrack et al., 2013; Ioriatti et al., 2015). If there are no healthy fruits available, D. suzukii is able to infest damaged fruits or rotten fruits (Kanzawa, 1935). Fallen fruits or the damaged areas of fruits of the following species have also been found to be infested: Prunus persica, Malus pumila var. domestica, Prunus triflora, Prunus armeniaca var. Anzu, Pyrus pyrifolia (Nakai, 1926), Pyrus sinensis, Eriobotrya japonica, Solanum lycopersicum (Kanzawa, 1939), Rubus microphyllus (Mitsui et al., 2010), as well as over-ripe figs (Ficus carica) still on the tree (Yu et al., 2013). Large numbers of D. suzukii were also reared from rotting strawberry guava fruits (Psidium cattleyanum) collected from trees and on the ground (Kido et al., 1996). It has been observed feeding upon injured or culled fruit including apple and oranges (Walsh et al., 2001). Some D. suzukii specimens emerged from fruits of Rubus crataegifolius, Alangium platanifolium, Cornus kousa, Torreya nucifera, Viburnum dilatatum. D. suzukii adults emerged from flowers of Styrax japonicus (Mitsui et al., 2010) and in early spring in southern Japan, the fly was also observed to breed on flowers of Camellia japonica (Nishiharu, 1980). During late winter and in early spring in Europe it has been shown that D. suzukii is able to develop in fruits of Viscum album subsp. laxum and Hedera helix (Briem et al., 2016; Grassi et al., 2018).
A very wide range of additional host plants including several wild and ornamental non-crop species have been recently provided by both American and European researchers further showing the extremely high polyphagy of D. suzukii (Lee et al., 2015; Kenis et al., 2016; Poyet et al., 2016).Host list: Actinidia chinensis, Actinidia deliciosa, Arbutus unedo, Berberis aquifolium, Citrus sinensis, Cornus sp., Cotoneaster lacteus, Diospyros kaki, Elaeagnus umbellata, Eriobotrya japonica, Eugenia involucrata, Ficus carica, Fragaria x ananassa, Lindera benzoin, Lonicera caerulea, Malus domestica, Mangifera indica, Morella rubra, Morus sp., Phytolacca americana, Prunus armeniaca, Prunus avium, Prunus domestica, Prunus laurocerasus, Prunus lusitanica, Prunus persica, Pyrus pyrifolia, Rubus fruticosus, Rubus hedycarpus subsp. armeniacus, Rubus idaeus, Rubus laciniatus, Rubus microphyllus, Rubus sp., Rubus spectabilis, Rubus ursinus, Rubus x loganobaccus, Sambucus nigra, Sarcococca confusa, Solanum dulcamara, Solanum lycopersicum, Solanum villosum, Symphoricarpos albus, Vaccinium corymbosum, Vaccinium sp., Vitis vinifera
GEOGRAPHICAL DISTRIBUTION 2020-05-05
The species is endemic in Asia. It was first recorded as invasive in Hawaii in 1980 and then simultaneously in California and in Europe in 2008. In the following years, it rapidly spread throughout most of the temperate regions of Asia, Europe, North and South America. The use of predictive models has indicated that D. suzukii has the potential to further invade other areas in Africa and Australia (dos Santos et al., 2017).EPPO Region: Austria, Belgium, Bosnia and Herzegovina, Bulgaria, Croatia, Cyprus, Czech Republic, Finland, France (mainland, Corse), Georgia, Germany, Greece (mainland, Kriti), Hungary, Ireland, Israel, Italy (mainland, Sardegna, Sicilia), Montenegro, Morocco, Netherlands, Poland, Portugal (mainland, Madeira), Romania, Russia (Far East), Serbia, Slovakia, Slovenia, Spain (mainland), Sweden, Switzerland, Turkey, Ukraine, United Kingdom (England)
Africa: Morocco, Reunion
Asia: China (Anhui, Fujian, Guangdong, Guangxi, Guizhou, Hainan, Heilongjiang, Henan, Hubei, Hunan, Jiangxi, Jilin, Liaoning, Shandong, Shanxi, Sichuan, Yunnan, Zhejiang), India (Chandigarh, Jammu & Kashmir, Karnataka, Uttaranchal, Uttar Pradesh), Iran, Israel, Japan (Hokkaido, Honshu, Kyushu, Ryukyu Archipelago), Korea Dem. People's Republic, Korea, Republic, Myanmar, Pakistan, Taiwan, Thailand
North America: Canada (Alberta, British Columbia, Manitoba, New Brunswick, Newfoundland, Nova Scotia, Ontario, Prince Edward Island, Québec), Mexico, United States of America (Alabama, Arkansas, California, Colorado, Connecticut, Delaware, Florida, Georgia, Hawaii, Idaho, Illinois, Indiana, Iowa, Kansas, Kentucky, Louisiana, Maine, Maryland, Massachusetts, Michigan, Minnesota, Mississippi, Missouri, Montana, New Hampshire, New Jersey, New Mexico, New York, North Carolina, Ohio, Oklahoma, Oregon, Pennsylvania, Rhode Island, South Carolina, Tennessee, Texas, Utah, Vermont, Virginia, Washington, West Virginia, Wisconsin, Wyoming)
South America: Argentina, Brazil (Distrito Federal, Espirito Santo, Minas Gerais, Parana, Rio de Janeiro, Rio Grande do Sul, Santa Catarina), Chile, Uruguay
Oceania: French Polynesia
The first detailed information about the biology of D. suzukii is available in Kanzawa (1935) and reviewed by Cini et al. (2012) and Asplen et al. (2015). D. suzukii overwinters as adults in reproductive diapause (Wallingford et al., 2016). Flies emerge in spring, but some adults are active also during the winter when the day temperature is warm (Rossi Stacconi et al., 2016). A seasonal phenotypic plasticity has been observed in field populations in temperate regions, as overwintering populations show a different morph phenotype, characterized by darker pigmentation and larger body size, which is more resistant to cold conditions and thus has enhanced winter survival (Shearer et al., 2016). Eggs are laid in ripening fruits and the number of eggs per fruit ranges from one to several, scattered over the fruit. D. suzukii host selection under field conditions may differ among plant species and among varieties within a species, and laboratory observations suggest that fruit firmness may be one driver of this selection (Burrack et al., 2013; Ioriatti et al., 2015; Baser et al., 2018). Egg-laying lasts 10-59 days with 7-16 (but up to 38) eggs laid per day. Each female can lay 350-400 eggs during her lifetime (Kanzawa, 1939). It has been reported that within the first four weeks, a female lays between 85 and 148 eggs and that the number of eggs laid depends on the host plant. Eggs hatch in 1-3 days, larvae mature in 3-13 days and most of them pupate in the fruit, but some drop and creep into the soil. Pupation lasts between 4 and 15 days. Mating of new adults can happen any time of the day, but it can be observed more often during the day when the temperature is relatively high. Males are always active, but females are passive. Courtship is described by Kanzawa (1939) and Revadi et al. (2015) and role of the visual stimulus in the courtship was investigated by Fuyama (1979). Recently the crucial role of specific substrate borne vibrations during courtship in D. suzukii has been demonstrated (Mazzoni et al., 2013). The Drosophila pheromone cis-11-octadecenyl acetate (cVA) is used by many species belonging to the melanogaster group and plays a role in assessing sex mate quality, mating status, and social interactions. Surprisingly, D. suzukii does not produce cVA (Dekker et al., 2015) but intraspecific chemical communication at close range is mediated by changes in the quantity and quality of several cuticular hydrocarbons (Snellings et al., 2018). Females oviposit after mating and can repeat mating several days after but at a lower rate with respect to other drosophila species (Kanzawa, 1939; Krüger et al., 2019). Recently, the presence of a marking aggregation pheromone released by D. suzukii egg-laying females over the oviposition site has been reported (Tait et al., 2020). In the Northern hemisphere, oviposition generally occurs from April to November and Mitsui et al. (2010) reported that D. suzukii collected in autumn were reproductively immature. However, Grassi et al. (2018) found the first overwintered females with mature eggs as early as February suggesting its great potential for oviposition early in the season and the presence of winter/early spring host plants. No reproductive behaviour was observed during laboratory experiments where D. suzukii was kept for the entire life cycle at temperatures below 10°C (Dalton et al., 2011). The authors assumed that the males, which were emerging in those experimental conditions, were rendered sterile and were unable to mate successfully with emerged females. Sterility in males is also reported when temperatures are above 30°C (Walsh et al., 2011).
The life cycle from egg hatching to adult emergence ranges from about 9-10 days to 21-25 days at 25°C and 15°C, respectively (Kanzawa, 1939). Laboratory observations document development from egg to egg-laying female ranging from about a week to 12-15 days at 21.1°C and at 18.3 °C, respectively (Walsh et al., 2011: Wiman et al., 2014). Under laboratory conditions, D. suzukii can complete up to 15 generations per year. Observation across a wide geographical range in Asia indicated that the number of generations per year could range from 3 to 13 depending on the climatic conditions (Kanzawa, 1939). According to degree day models, it is estimated that D. suzukii can complete 3 to 9 generations per year in the Western United States, Canada and Northern Italy (Coop, 2010; Tochen et al., 2014; Wiman et al., 2014). The lifespan of adults is 20-56 days, but some overwintering adults lived for more than 200 days (Kanzawa, 1935). During experiments simulating winter conditions of the US Pacific Northwest, adult D. suzukii could survive up to 88 days at constant 10°C, with no marked change in mortality when flies were subjected to a 7 day freeze period; and adult longevity decreased progressively at constant temperature below 10°C. Adult longevity was estimated to be longer if adults emerge from pupae subjected to similar temperatures. These results suggested that acclimation may prolong survival of D. suzukii when later subject to cold temperatures (Dalton et al., 2011).
The D. suzukii genome is comparable in size and repeat content to other Drosophila species. Genome-scale relaxed-clock analyses indicate a late Miocene origin of D. suzukii, concomitant with paleo-geological and climatic conditions that suggest an adaptation to temperate climates.
DETECTION AND IDENTIFICATION 2020-05-05
The larval feeding causes the fruit to collapse around the oviposition site (Grassi et al., 2011). The oviposition scar exposes the fruit to secondary attack by pathogens and other insects (Hauser et al., 2009; Ioriatti et al., 2018).
A detailed morphological description of each stage is given by Kanzawa (1935), and it has recently been updated by Hauser (2011) and by Vlach (2010) who added morphological details and a dichotomous key, respectively. D. suzukii adults are drosophilid flies (2-3 mm long) with red eyes, a pale brown or yellowish-brown thorax and black transverse stripes on the abdomen. The antennae are short and stubby with branched arista. Sexual dimorphism is evident: males display a dark spot on the leading top edge of each wing, and females are larger and possess a large serrated ovipositor (Atallah et al., 2014). The dark spots on the wings together with two sets of black tarsal combs make the identification of the males relatively easy. However, males without wing dark spots can be present, because spots start to appear within 10 hours following emergence when the temperature is high, but it takes full two days before the spots become obvious. The eggs are oval (0.2 mm wide), milky white colour, with two filaments (aeropyle or spiracle) at one end whose length ranges from 0.4 to 0.6 mm. The maggot-like larvae are white with visible internal organs and black mouthparts. They grow throughout three larval stages and when fully-grown they can reach 5.5 mm in length and 0.8 mm in width. Distinguishing stages of instars can be estimated by the size of larvae, colour of mouthpart, but it is most accurately judged by pre-respiratory ducts (Kanzawa, 1935; Walsh et al., 2011). The pupae are spindle-shaped, reddish brown in colour and they bear two stalks with small finger-like projections (3.5 mm in length and 1.2 mm wide).
The distinguishing features of the two sexes (serrated ovipositor and black wing spots) are present in other 150 Drosophila species, thus making species identification difficult in areas where they are sympatric. An easy-to-use description of the combination of diagnostic characters that could be used for tentative identification of D. suzukii within the subgroup it belongs is given both by Hauser (2011) and Cini et al. (2012). Drosophila subpulchrella males’ black spots are very similar in shape and position to those of D. suzukii (Takamori et al., 2006). The possible lack of wing black spots in teneral specimens of D. suzukii could lead to misidentification with other closely related Drosophila species whose males do not present spots on the male wing: D. ashburneri, D. immacularis, D. lucipennis, D. mimetica, D. oshimai and D. unipectinata. Other characteristics may thus guide identification, such as the sex combs on the foretarsi; D. suzukii has one row of combs on the first and one row on the second tarsal segment while D. biarmipes has two combs on the first tarsomere. Similar problems arise with females. On the basis of the shape and length of the ovipositor, D. suzukii can be easily discriminated from related species, as for example D. biarmipes, but not easily from other species such as D. immigrans and D. subpulchrella (Takamori et al., 2006) which possess very similar ovipositors (Hauser, 2011; Atallah et al., 2014). In such cases, a final determination should rely on the relative size of spermatheca compared to ovipositor’s size: it is thus feasible only for the trained eyes of taxonomists (Hauser, 2011). The situation is complex also for immature stages (eggs, larvae and pupae), where no reliable morphological diagnostic features have been identified (Okada, 1968). The D. suzukii egg has two respiratory appendages but this character is not species-specific. Therefore, DNA barcoding is the only fully reliable identification (Freda and Braverman, 2013). Molecular identification is hence possible by amplification of the barcode COI gene with universal primers.
The EPPO diagnostic protocol on D. suzukii provides guidance on how to detect and identify the pest (EPPO, 2013).
Detection and inspection methods
The presence of adult flies in the field can be monitored by using traps baited with different attractants. Although field captures of D. suzukii in traps indicate its presence, trapping does not appear to provide good prediction of infestations in all crops. Any 250-750 mL plastic containers with closely fitting lids can be used as traps. Traps should have 0.5 – 1 mm diameter holes drilled on their sides to enable the flies to enter the trap. A variety of traps (i.e. prototypes made by researchers or traps sold by commercial companies) are available to monitor adult D. suzukii. Comparison among different trap design (size, colour, volatilization area, entry area) have been performed across different regions and crops (Lee et al., 2012; 2013; Renkema et al., 2014; Cha et al., 2018; Tonina et al., 2018). The number of captures increased with the size of the entry holes, but smaller holes slowed evaporation and increased selectivity (by preventing entry of larger insects). Red, yellow and black traps are preferable to clear or white, but there is an interaction between trap colour and crop type. Trap colour has no effect on the selectivity towards other drosophlids and traps integrating both visual and olfactory cues are better tools for monitoring D. suzukii (Lee et al., 2013; Kirkpatrick et al., 2017). Apple cider vinegar was one of the first baits used because of its efficacy and ease of use. This lure has been lately improved by adding wine (Landolt et al., 2012), or wine and sugar (Grassi et al. 2015; Rossi Stacconi et al., 2016). The fly response to the combination of vinegar and wine was greater than the response to acetic acid or the combination of acetic acid and ethanol, which are the principal volatile chemical components of vinegar and wine respectively (Landolt et al., 2012). This finding indicates that other volatiles emitted by vinegar and wine, in addition to acetic acid and ethanol, may also be attractive to male and female D. suzukii. A sugar-yeast bait has been used successfully and was found to outperform apple cider vinegar (Knight et al., 2013). A small drop of dish soap added to the liquid bait as a surfactant, or the placement of a sticky card within the trap, results in more fly captures. In term of sensitivity, the most effective traps are also the ones that catch the pest earlier in the season. Multi-component volatile blends have been identified (Cha et al., 2012; 2013; 2014; 2017) and may provide more selective lures and reduce the time for trap servicing. Improvement of the attraction efficiency of the available lure together with optimization of the trap design are major objectives of different research teams dealing with chemical ecology in order to set up effective tools for pest control (Cloonan et al., 2018, Landolt et al. 2012; Cha et al., 2013; Larson et al., 2020).
PATHWAYS FOR MOVEMENT 2020-05-05
Adults of D. suzukii can fly over short distances with the influence of biotic and abiotic factors such as the availability of cultivated and wild host plants and optimal temperature and humidity conditions (Tait et al., 2020). In addition, D. suzukii, as a fruit-specialist species among drosophilid flies, can seasonally migrate between low and high altitudes in mountain regions, probably exploiting the seasonal air currents along the valleys with high altitudinal gradient. It is assumed that during summer, adults are moving away from resource-poor conditions prevailing at low altitudes to exploit better resources at high altitudes (Mitsui et al., 2010; Tait et al., 2018).
Over long distances, it is considered that the main pathway for movement is the trade of potentially infested host fruit. Although, it has been observed that some flowers could also carry life stages of D. suzukii (see host plants section), cut flowers have been considered as presenting a very low risk (EPPO, 2011). The explosive dispersal worldwide of D. suzukii is partly due to the increasing global trade of fresh fruit and to the cryptic nature of larvae hidden inside the fruit, that are often undetected during and after transport (Cini et al., 2014). As a consequence, passive diffusion is likely the main cause of the spread of D. suzukii, as for many other invasive species (Westphal et al., 2008). Recent analyses indicate the presence of at most three D. suzukii genetic clusters in Europe, while North American populations are characterised by a larger genetic diversity (Adrion et al., 2014; Fraimout et al., 2017; Rota Stabelli et al., 2020). They have found that colonization events in the two continents were independent and demonstrated that reference American and European genomes lay in highly distant clusters. Invasion history shows that D. suzukii has a high dispersal ability and Calabria et al. (2012) could determine that D. suzukii was able to spread approximately 1400 km in one year, either actively through natural spread or passively through movements of infested fruits.
PEST SIGNIFICANCE 2020-05-05
D. suzukii infestations generate direct and indirect economic impacts, through yield losses, shorter shelf life of infested fruits, extra labour and material costs for monitoring, field sanitation and post-harvest handling (especially in organic production) as well as the closure of international markets in front of fruits produced in infested areas (Goodhue et al., 2011; Lee et al., 2011; DiGiacomo et al., 2019). In Europe, a yield loss of 30-40% of blueberry, blackberry and raspberry fruits, was observed in Italy (in 2011) and up to 80% of yield loss occurred in strawberry production in France in 2010. In addition to the loss of production, the increased costs for D. suzukii management have generated important revenue losses (Farnsworth et al., 2017; Mazzi et al., 2017). This pest caused a loss of 3.3 million EUR, in 2011, in small fruits cultivation, in Trento province (Northern Italy) (De Ros et al., 2015) and a total loss of 511 million USD, in strawberries, blueberries, raspberries, blackberries, and cherries in California, Oregon, and Washington states (Walsh et al., 2011). These losses can be reduced or mitigated by the introduction of Integrated Pest Management (IPM) strategies, based on insecticides, mass trapping, exclusion netting and field sanitation, which were proven to reduce economic losses, from 13% to 7%, in soft fruits production in Trento Province (De Ros et al., 2015; Del Fava et al., 2017).
Although various control approaches have been implemented to suppress D. suzukii populations and reduce crop damage (Haye et al., 2016), current programs still rely primarily on insecticides that target adult flies (Van Timmeren and Isaacs, 2013). Insecticides can be effective, but there is a restricted list of permitted active ingredients and increasing problems with fruit residues (Rodriguez-Saona et al., 2019). Insecticide applications may also negatively affect beneficial organisms, and lead to the development of resistance, which is of major concern over the longer term (Gress and Zalom, 2019). Therefore, given also the high polyphagy and mobility of the pest, only area-wide IPM strategies aimed at reducing population densities at the landscape level would be able to achieve sufficient levels of effectiveness. New IPM tools are hence under development including those based on semiochemicals (Cloonan et al., 2018; Alkema et al., 2019), cultural methods (Rendon and Walton, 2019), exclusion nets (Leach et al., 2016), sterile and/or incompatible insect techniques (Lanouette et al., 2017) possibly in combination with transgenic approaches (Ahmed et al., 2019). However, none of these methods alone or together has shown yet to significantly control D. suzukii populations on a large scale. In the light of these results, the method that seems most promising, suitable and durable over large areas is biological control. In this sense, many studies have been carried out and are at an advanced stage of application using both indigenous and non-indigenous arthropods, predators and microorganisms (Lee et al., 2019). Biological control in area-wide programs should be able to reduce pest populations in natural habitats, thereby reducing the number of flies that migrate into susceptible crops that, in turn, will improve the effectiveness of other control tools and lower damage (Rossi Stacconi et al., 2019).
D. suzukii was included in the EPPO A2 list of pests recommended for regulation as a quarantine pest in 2011. It has been declared a quarantine pest by New Zealand and Australia, and these countries have imposed restrictions on the importation of several cultivated fruit species from invaded areas. Even though successful eradication programs are not reported so far, due to the high reproductive capacity and dispersal abilities of this pest, early warning systems are vital in areas which are still free from D. suzukii, in case eradication is attempted.
PHYTOSANITARY MEASURES 2020-05-05
In order to reduce the risk of introducing D. suzukii into new areas, countries have been advised to require that fruit are coming from areas that are free from the pest, or produced under specific conditions to prevent fruit infestations (e.g. by growing plants under a net or in screened greenhouses with trapping to verify pest absence). Fruit treatments may also be used (EPPO, 2011). For example, cold storage or cold treatments can reduce survival and increase development time of D. suzukii larvae infesting fruits (Aly et al., 2017; Saeed et al., 2020). In countries outside the EPPO region, fumigation or irradiation treatments have been recommended (Walse et al., 2012; DAFF, 2013; Follett et al., 2014).
Adrion JR, Kousathanas A, Pascual M, Burrack HJ, Haddad NM, Bergland AO, Wegmann D (2014) Drosophila suzukii: the genetic footprint of a recent, worldwide invasion. Molecular biology and evolution 31(12), 3148-3163.
Ahmed HM, Hildebrand L, Wimmer EA (2019) Improvement and use of CRISPR/Cas9 to engineer a sperm-marking strain for the invasive fruit pest Drosophila suzukii. BMC Biotechnology 19(1), 1-14.
Alkema JT, Dicke M, Wertheim B (2019) Context-dependence and the development of push-pull approaches for integrated management of Drosophila suzukii. Insects 10(12), 454.
Aly MF, Kraus DA, Burrack HJ (2017) Effects of postharvest cold storage on the development and survival of immature Drosophila suzukii (Diptera: Drosophilidae) in artificial diet and fruit. Journal of Economic Entomology 110(1), 87-93.
Asplen MK, Anfora G, Biondi A, Choi DS, Chu D, Daane KM, Gibert P, Gutierrez AP, Hoelmer KA, Hutchison WD, Isaacs R, Jiang ZL, Kárpáti Z, Kimura MT, Pascual M, Philips CR, Plantamp C, Ponti L, Vétek G, Vogt H, Walton VM, Yu Y, Zappalà L, Desneux N (2015) Invasion biology of spotted wing drosophila (Drosophila suzukii): a global perspective and future priorities. Journal of Pest Science 88, 469-494.
Atallah J, Teixeira L, Salazar R, Zaragoza G, Kopp A (2014) The making of a pest: the evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species. Proceedings of the Royal Society B: Biological Sciences 281(1781), 20132840.
Barmina O, Kopp A (2007) Sex-specific expression of a Hox gene associated with rapid morphological evolution. Developmental Biology 311, 277-286.
Baser N, Broutou O, Verrastro V, Porcelli F, Ioriatti C, Anfora G, Mazzoni V, Rossi Stacconi MV (2018) Susceptibility of table grape varieties grown in south-eastern Italy to Drosophila suzukii. Journal of Applied Entomology 142, 465-472.
Bellamy DE, Sisterson MS, Walse SS (2013) Quantifying host potentials: indexing postharvest fresh fruits for spotted wing drosophila, Drosophila suzukii. PLoS ONE 8(4), e61227.
Briem F, Eben A, Gross J, Vogt H (2016) An invader supported by a parasite: Mistletoe berries as a host for food and reproduction of spotted wing drosophila in early spring. Journal of Pest Science 89(3), 749-759.Calabria G, Maca J, Bachli G, Serra L, Pascual M (2012) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. Journal of Applied Entomology 136, 139-147.
Cha D, Adams T, Rogg H, Landolt PJ (2012) Identification and field evaluation of fermentation volatiles from wine and vinegar that mediate attraction of spotted wing drosophila, Drosophila suzukii. Journal of Chemical Ecology 38, 1419–1431.
Cha DH, Adams T, Werle CT, Sampson BJ, Adamczyk Jr JJ, Rogg H, Landolt PJ (2014) A four-component synthetic attractant for Drosophila suzukii (Diptera: Drosophilidae) isolated from fermented bait headspace. Pest Management Science 70, 324-331.
Cha DH, Hesler SP, Cowles RS, Vogt H, Loeb GM, Landolt PJ (2013) Comparison of a synthetic chemical lure and standard fermented baits for trapping Drosophila suzukii (Diptera: Drosophilidae). Environmental Entomology 42(5), 1052-1060.
Cha DH, Landolt PJ, Adams TB (2017) Effect of chemical ratios of a microbial-based feeding attractant on trap catch of Drosophila suzukii (Diptera: Drosophilidae). Environmental Entomology 46(4), 907-915.
Cha DH, Hesler SP, Wallingford AK, Zaman F, Jentsch P, Nyrop J, Loeb GM (2018) Comparison of commercial lures and food baits for early detection of fruit infestation risk by Drosophila suzukii (Diptera: Drosophilidae). Journal of Economic Entomology 111, 645-652.
Chiu JC, Jiang X, Zhao L, Hamm CA, Cridland JM, Saelao P, Hamby KA, Lee EK, Kwok RS, Zhang G, Zalom FG, Walton VM, Begun DJ (2013) Genome of Drosophila suzukii, the spotted wing drosophila. G3: Genes|Genomes|Genetics 3, 2257-2271.
Cini A, Ioriatti C, Anfora G (2012) A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for Integrated Pest Management. Bulletin of Insectology 65 (1), 149-160.
Cini A, Anfora G, Escudero-Colomar LA, Grassi A, Santosuosso U, Seljak G, Papini A (2014) Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe. Journal of Pest Science 87, 559-566.
Cloonan KR, Abraham J, Angeli S, Syed Z, Rodriguez-Saona C (2018) Advances in the chemical ecology of the spotted wing drosophila (Drosophila suzukii) and its applications. Journal of Chemical Ecology 44(10), 922-939.
Coop L (2010) Online phenology and degree-day model for agricultural and decision-making in the US. Integrated Plant Protection Center, Botany & Plant Pathology Dep. Oregon State University, Corvallis, Oregon. (http://uspest.org/risk/models?spp_swd).
DAFF (2013) Final pest risk analysis report for Drosophila suzukii. Australian Government, Department of Agriculture, Fisheries and Forestry Biosecurity. https://www.agriculture.gov.au/sites/default/files/sitecollectiondocuments/ba/plant/2013/drosophila-suzukii-pra/BA2013-09-final-Drosophila-suzukii-PRA.pdf
Dalton DT, Walton VM, Shearer PW, Walsh DB, Caprile J, Isaacs R (2011) Laboratory survival of Drosophila suzukii under simulated winter conditions of the Pacific Northwest and seasonal field trapping in five primary regions of small and stone fruit production in the United States. Pest Management Science 67, 1368-1374.
Dekker T, Mansourian S, Revadi S, Lebreton S, Becher P, Angeli S, Rota-Stabelli O, Anfora G (2015) From pheromone to antagonist: cis-vaccenyl acetate loss in Drosophila suzukii reverses its role in sexual communication. Proceedings of the Royal Society B 282, 20143018.
Del Fava E, Ioriatti C, Melegaro A (2017) Cost–benefit analysis of controlling the spotted wing drosophila (Drosophila suzukii (Matsumura)) spread and infestation of soft fruits in Trentino, Northern Italy. Pest Management Science 73(11), 2318-2327.
De Ros G, Conci S, Pantezzi T, Savini G (2015) The economic impact of invasive pest Drosophila suzukii on berry production in the Province of Trento, Italy. Journal of Berry Research 5(2), 89-96.
DiGiacomo G, Hadrich J, Hutchison WD, Peterson H, Rogers M (2019) Economic impact of spotted wing drosophila (Diptera: Drosophilidae) yield loss on Minnesota raspberry farms: A grower survey. Journal of Integrated Pest Management 10(1), 11.
Dos Santos LA, Mendes MF, Krüger AP, Blauth ML, Gottschalk MS, Garcia FRM (2017) Global potential distribution of Drosophila suzukii (Diptera,Drosophilidae). PLoS ONE 12(3), e0174318.
EPPO (2011) EPPO Pest Risk Analysis on Drosophila suzukii. https://pra.eppo.int/organism/DROSSU
EPPO (2013) EPPO Standards. Diagnostics. PM 7/115 (1) Drosophila suzukii. EPPO Bulletin 43(3), 417-424.
Farnsworth D, Hamby KA, Bolda M, Goodhue RE, Williams JC, Zalom FG (2017) Economic analysis of revenue losses and control costs associated with the spotted wing drosophila, Drosophila suzukii (Matsumura), in the California raspberry industry. Pest Management Science 73(6), 1083-1090.
Follett PA, Swedman A, Price DK (2014) Postharvest irradiation treatment for quarantine control of Drosophila suzukii (Diptera: Drosophilidae) in fresh commodities. Journal of Economic Entomology 107(3), 964-969.
Fraimout, A., Debat, V., Fellous, S., Hufbauer RA, Foucaud J, Pudlo P, Deprá M (2017) Deciphering the routes of invasion of Drosophila suzukii by means of ABC random forest. Molecular Biology and Evolution 34(4), 980-996.
Freda PJ, Braverman JM (2013) Drosophila suzukii, or spotted wing drosophila, recorded in southeastern Pennsylvania, USA. Entomological News 123(1), 71-75
Fuyama Y (1979) A visual stimulus in the courtship of Drosophila suzukii. Experientia 35(10), 1327-1328.
Goodhue RE, Bolda M, Farnsworth D, Williams JC, Zalom FG (2011) Spotted wing drosophila infestation of California strawberries and raspberries: economic analysis of potential revenue losses and control costs. Pest Management Science 67(11), 1396-1402.
Grassi A, Palmieri L, Giongo L (2011) Drosophila (Sophophora) suzukii (Matsumura), new pest of soft fruits in Trentino (North-Italy) and in Europe. IOBC/wprs Bulletin 70, 129-136.
Grassi A, Anfora G, Maistri S, Maddalena G, De Cristofaro A, Savini G, Ioriatti C (2015) Development and efficacy of Droskidrink, a food bait for trapping Drosophila suzukii. IOBC Bulletin 109, 197-204.
Grassi A, Gottardello A, Dalton DT, Tait G, Rendon D, Ioriatti C, Walton VM (2018) Seasonal reproductive biology of Drosophila suzukii (Diptera: Drosophilidae) in temperate climates. Environmental Entomology 47(1), 166-174.
Gress BE, Zalom FG (2019) Identification and risk assessment of spinosad resistance in a California population of Drosophila suzukii. Pest Management Science 75, 1270-1276.
Hauser M (2011) A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Management Science 67, 1352-1357.
Haye T, Girod P, Cuthbertson AGS, Wang XG, Daane KM, Hoelmer KA, Baroffio C, Zhang JP, Desneux N (2016) Current SWD IPM tactics and their practical implementation in fruit crops across different regions around the world. Journal of Pest Science 89, 643-651.
Krüger A P, Schlesener DC, Martins LN, Wollmann J, Deprá M, Garcia FR (2019) Radiation effects on Drosophila suzukii (Diptera: Drosophilidae) reproductive behaviour. Journal of Applied Entomology, 143, 88-94.
Ioriatti C, Walton V, Dalton D, Anfora G, Grassi A, Maistri S, Mazzoni V (2015) Drosophila suzukii (Diptera: Drosophilidae) and its potential impact to wine grapes during harvest in two cool climate wine grape production regions. Journal of Economic Entomology 108(3), 1148-1155.
Ioriatti C, Guzzon R, Anfora G, Ghidoni F, Mazzoni V, Roman Villegas T, Dalton DT, Walton VM (2018) Drosophila suzukii (Diptera: Drosophilidae) contributes to the development of sour rot in grape. Journal of Economic Entomology 111(1), 283-292.
Landolt PJ, Adams T, Rogg H (2012) Trapping spotted wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), with combinations of vinegar and wine, and acetic acid and ethanol. Journal of Applied Entomology 136, 148-154.
Larson NR, Strickland J, Shields VD, Zhang A (2020) Controlled-release dispenser and dry trap developments for Drosophila suzukii detection. Frontiers in Ecology and Evolution 8, p 45.
Leach H, Van Timmeren S, Isaacs R (2016) Exclusion netting delays and reduces Drosophila suzukii (Diptera: Drosophilidae) infestation in raspberries. Journal of Economic Entomology 109(5), 2151-2158.
Lee JC, Bruck DJ, Dreves AJ, Ioriatti C, Vogt H, Baufeld P (2011) In Focus: Spotted wing drosophila, Drosophila suzukii, across perspectives. Pest Management Science 67(11), 1349-1351.
Lee JC, Burrack HJ, Barrantes LD, Beers EH, Dreves AJ, Hamby KA, Haviland DR, Isaacs R, Richardson TA, Shearer PW, Stanley CA, Walsh DB, Walton VM, Zalon FG, Bruck D (2012) Evaluation of monitoring traps for Drosophila suzukii (Diptera: Drosophilidae) in North America. Journal of Economic Entomology 105(4), 1350-1357.
Lee JC, Shearer PW, Barrantes LD, Beers EH, Burrack HJ, Dalton DT, Dreves AJ, Gut LJ, Hamby KA, Haviland DR, Isaacs R, Nielsen AL, Richardson T, Rodriguez-Saona CR, Stanley CA, Walsh DB, Walton VM, Yee WL, Zalom FG, Bruck DJ (2013) Trap designs for monitoring Drosophila suzukii (Diptera: Drosophilidae). Environmental Entomology 42(6), 1348-1355.
Lee JC, Dreves AJ, Cave AM, Kawai S, Isaacs R, Miller JC, Bruck DJ (2015) Infestation of wild and ornamental non-crop fruits by Drosophila suzukii (Diptera: Drosophilidae). Annals of the Entomological Society of America 108(2), 117-129.
Lee JC, Wang X, Daane KM, Hoelmer KA, Isaacs R, Sial AA, Walton VM (2019) Biological control of spotted-wing Drosophila (Diptera: Drosophilidae)—current and pending tactics. Journal of Integrated Pest Management 10(1), 13.
Kanzawa T (1935) Research into the fruit-fly Drosophila suzukii Matsumura (Preliminary Report). Yamanashi Prefecture Agricultural Experiment Station Report. Japan.
Kanzawa T (1939) Studies on Drosophila suzukii Mats. Kofu, Yanamashi Agricultural Experimental Station, Japan.
Kenis M, Tonina L, Eschen R, van der Sluis B, Sancassani M, Mori N, Helsen H (2016) Non-crop plants used as hosts by Drosophila suzukii in Europe. Journal of Pest Science 89(3), 735-748.
Kirkpatrick D M, McGhee PS, Gut LJ, Miller JR (2017) Improving monitoring tools for spotted wing drosophila, Drosophila suzukii. Entomologia Experimentalis et Applicata 164(2), 87-93.
Knight A, Yee W, Hilton R (2013) Developing a new bait for spotted-wing drosophila in organic cherry production. Proceedings of the 2nd International Organic Fruit Symposium. Acta Horticulturae 1001, 147-152.
Kopp A, True JR (2002) Phylogeny of the oriental Drosophila melanogaster species group: a multilocus reconstruction. Systematic Biology 51, 786-805.
Mazzi D, Bravin E, Meraner M, Finger R, Kuske S (2017) Economic impact of the introduction and establishment of Drosophila suzukii on sweet cherry production in Switzerland. Insects 8(1), 18.
Mazzoni V, Anfora G, Virant-Doberlet M (2013) Substrate vibrations during courtship in three Drosophila species. PLoSONE 8, e80708.
Mitsui H, Kimura MT (2010) Distribution, abundance and host association of two parasitoid species attacking frugivorous drosophilid larvae in central Japan. European Journal of Entomology 107(4), 535-540.
Nikolouli K, Sassù F, Mouton L, Stauffer C, Bourtzis K (2020) Combining sterile and incompatible insect techniques for the population suppression of Drosophila suzukii. Journal of Pest Science 93(2), 647-661.
Nishiharu S (1980) A study of ecology and evolution of drosophilid flies with special regard to imaginal and larval feeding habits and seasonal population fluctuations. PhD Thesis, Tokyo Metropolitan University.
Okada T (1976) New distribution records of the Drosophilids in the oriental region. Makunagi 8, 1-8 (in Japanese).
Ometto L, Cestaro A, Ramasamy S, Grassi A, Revadi S, Siozios S, Moretto M, Fontana P, Varotto C, Pisani D, Dekker T, Wrobel N, Viola R, Pertot I, Cavalieri D, Blaxter M, Anfora G, Rota-Stabelli O (2013) Linking genomics and ecology to unveil the complex evolution of an invasive Drosophila pest. Genome Biology and Evolution 5(4), 745-757.
Parshad R, Paika IJ (1965) Drosophilid survey of India II. Taxonomy and cytology of the subgenus Sophophora (Drosophila). Research Bulletin of the Panjab University 15, 225-252.
Poyet, M, Le Roux V, Gibert P, Meirland A, Prevost G, Eslin P, Chabrerie O (2015) The wide potential trophic niche of the Asiatic fruit fly Drosophila suzukii: the key of its invasion success in temperate Europe? PLoS ONE, 10(11).
Powell JR (1997) Progress and prospects in evolutionary biology: The Drosophila model. Oxford University Press, Inc. New York, USA.
Prud’homme B, Gompel N, Rokas A, Kassner VA, Williamst M, Yeh SD, True JR, Carroll SB (2006) Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 440, 1050-1053.
Rendon D, Walton VM (2019) Drip and overhead sprinkler irrigation in blueberry as cultural control for Drosophila suzukii (Diptera: Drosophilidae) in Northwestern United States. Journal of Economic Entomology 112, 745-752.
Renkema JM, Buitenhuis R, Hallett RH (2014) Optimizing trap design and trapping protocols for Drosophila suzukii (Diptera: Drosophilidae). Journal of Economic Entomology 107(6), 2107-2118.
Revadi S, Lebreton S, Witzgall P, Anfora G, Dekker T, Becher PG (2015) Sexual behavior of Drosophila suzukii. Insects 6, 183-196.
Rodriguez-Saona C, Vincent C, Isaacs R (2019) Blueberry IPM: Past successes and future challenges. Annual Review of Entomology 64, 95-114.
Rossi Stacconi MV, Kaur R, Mazzoni V, Ometto L, Grassi A, Gottardello A, Rota-Stabelli O, Anfora G (2016) Multiple lines of evidence for reproductive winter diapause in the invasive pest Drosophila suzukii: useful clues for control strategies. Journal of Pest Science 89, 689-700.
Rossi Stacconi MV, Grassi A, Ioriatti C, Anfora G (2019) Augmentative releases of Trichopria drosophilae for the suppression of early season Drosophila suzukii populations. BioControl 64, 9-19.
Rota-Stabelli O, Ometto L, Tait G, Ghirotto S, Kaur R, Drago F, González J, Walton VM, Anfora G, Rossi Stacconi MV (2020) Distinct genotypes and phenotypes in European and American strains of Drosophila suzukii: implications for biology and management of an invasive organism. Journal of Pest Science 93, 77-89.
Saeed N, Tonina L, Battisti A, Mori N (2020) Postharvest short cold temperature treatment to preserve fruit quality after Drosophila suzukii damage. International Journal of Pest Management 66(1), 23-30.
Schawaroch V (2002) Phylogeny of a paradigm lineage: The Drosophila melanogaster species group (Diptera: Drosophilidae). Biological Journal of the Linnean Society 76, 21-37.
Shearer PW, West JD, Walton VM, Brown PH, Svetec N, Chiu JC (2016) Seasonal cues induce phenotypic plasticity of Drosophila suzukii to enhance winter survival. BMC ecology 16(1), 11.
Snellings Y, Herrera B, Wildemann B, Beelen M, Zwarts L, Wenseleers T, Callaerts P (2018) The role of cuticular hydrocarbons in mate recognition in Drosophila suzukii. Scientific reports 8(1), 1-11.
Takamori H, Watabe HA, Fuyama Y, Zhang YP, Aotsuka T (2006) Drosophila subpulchrella, a new species of the Drosophila suzukii species subgroup from Japan and China (Diptera: Drosophilidae). Entomological Science 9(1), 121-128.
Tait G, Park K, Nieri R, Crava MC, Mermer S, Clappa E, Boyer G, Dalton DT, Carlin S, Brewer L, Walton MW, Anfora G, Rossi Stacconi MV (2020) Reproductive site selection: evidence of an oviposition cue in a highly adaptive dipteran, Drosophila suzukii (Diptera: Drosophilidae). Environmental Entomology. DOI: 10.1093/ee/nvaa005
Tait G, Cabianca A, Grassi A, Pfab F, Oppedisano T, Puppato S, Mazzoni V, Anfora G, Walton VM (2020) Drosophila suzukii daily dispersal between distinctly different habitats. Entomologia Generalis 40, 25-37.
Tait G, Grassi A, Pfab F, Crava CM, Dalton DT, Magarey R, Ometto L, Vezzulli S, Rossi-Stacconi MV, Gottardello A, Pugliese A, Firrao G, Walton VM, Anfora G (2018) Large-scale spatial dynamics of Drosophila suzukii in Trentino, Italy. Journal of Pest Science 91, 1213-1224.
Tonina L, Grassi A, Caruso S, Mori N, Gottardello A, Anfora G, Giomi F, Vaccari G, Ioriatti C (2018) Comparison of attractants for monitoring Drosophila suzukii in sweet cherry orchards in Italy. Journal of Applied Entomology 142, 18-25.
Van der Linde K, Houle D (2008) A super-tree analysis and literature review of the genus Drosophila and closely related genera. Insect Systematics and Evolution 39, 241-267.
Van Timmeren S, Isaacs R (2013) Control of spotted wing drosophila, Drosophila suzukii, by specific insecticides and by conventional and organic crop protection programs. Crop Protection 54, 126-133.
Vlach J (2010) Identifying Drosophila suzukii. Oregon Department of Agriculture http://www.oregon.gov/ODA/PLANT/docs/pdf/ippm_d_suzukii_id_guide10.pdf
Wallingford AK, Lee JC, Loeb GM (2016) The influence of temperature and photoperiod on the reproductive diapause and cold tolerance of spotted‐wing drosophila, Drosophila suzukii. Entomologia Experimentalis et Applicata 159(3), 327-337.
Walse SS, Krugner R, Tebbets JS (2012) Postharvest treatment of strawberries with methyl bromide to control spotted wing drosophila, Drosophila suzukii. Journal of Asia-Pacific Entomology 15(3), 451-456.
Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee J, Bruck DJ, Walton VM, O’Neil SD, Zalon FG (2011) Drosophila suzukii (Diptera; Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. Journal of Integrated Pest Management 2(1), G1-G7
Westphal MI, Browne M, Mackinnon K, Noble I (2008) The link between international trade and the global distribution of invasive alien species. Biological Invasions 10, 391-398.
Wiman NG, Walton VM, Dalton DT, Anfora G, Burrack HJ, Chiu JC, Daane KM, Grassi A, Miller B, Tochen S, Wang X, Ioriatti C (2014) Integrating temperature-dependent life table data into a matrix projection model for Drosophila suzukii population estimation. PLoS ONE 9(9), e106909.
Yang Y, Hou ZC, Qian HY, Kang H, Zeng QT (2011) Increasing the data size to accurately reconstruct the phylogenetic relationships between nine subgroups of the Drosophila melanogaster species group (Drosophilidae, Diptera). Molecular Phylogenetics and Evolution 62, 214- 223.
Yu D, Zalom FG, Hamby KA (2013) Host status and fruit odor response of Drosophila suzukii (Diptera: Drosophilidae) to figs and mulberries. Journal of Economic Entomology 106(4), 1932-1537.
CABI resources used when preparing this datasheet
CABI (2020) Invasive Species Compendium. Datasheet on Drosophila suzukii (spotted wing drosophila). https://www.cabi.org/isc/datasheet/109283
This datasheet was prepared in 2020 by Gianfranco Anfora. His contribution is gratefully acknowledged.