Bulletin of Insectology 65 (1): 149-160, 2012 ISSN 1721-8861

A review of the invasion of suzukii in and a draft research agenda for integrated pest management

1,2 1 1 Alessandro CINI , Claudio IORIATTI , Gianfranco ANFORA 1Research and Innovation Centre, Fondazione Edmund Mach, San Michele all’Adige (TN), 2Laboratoire Ecologie & Evolution UMR 7625, Université Pierre et Marie Curie, Paris,

Abstract

The vinegar (Matsumura) (Diptera ), spotted wing drosophila, is a highly polyphagous inva- sive pest endemic to South East Asia, which has recently invaded western countries. Its serrated ovipositor allows this fly to lay eggs on and damage unwounded ripening fruits, thus heavily threatening fruit production. D. suzukii is spreading rapidly and eco- nomic losses are severe, thus it is rapidly becoming a pest of great concern. This paper reviews the existing knowledge on the pest life history and updates its current distribution across Europe. D. suzukii presence has now been reported in nine European coun- tries. Nonetheless, several knowledge gaps about this pest still exist and no efficient monitoring tools have been developed yet. This review is aimed at highlighting the possible research approach which may hopefully provide management solutions to the expanding challenge that D. suzukii poses to European fruit production.

Key words: spotted wing drosophila, cherry fruit fly, invasive species, berry fruit, control.

A new pest is threatening European fruit pro- in Kanzawa (1935; 1936; 1939), while more recent bio- duction logical data in English are available in Walsh et al. (2011) and Lee et al. (2011b). We then provide an up- On the 2nd of December 2011 about 180 people attended dated overview of its distribution across Europe. The the international meeting “Drosophila suzukii: new understanding of basic biology, ecology and distribution threat for European fruit production” in Trento. The is crucial for development of efficient management meeting represented a unique occasion to exchange in- strategies. The presence of multiple gaps in the present formation about the spread and impact of Drosophila knowledge was indeed clear in the aforementioned suzukii (Matsumura) (Diptera Drosophilidae), a new meeting, and only an integrated and multidisciplinary fruit pest which is invading Europe. Researchers, pro- approach can face the challenge of understanding and ducers, representatives of local institutions and phyto- ultimately controlling this pest. Efficient and rapid solu- sanitary services from ten European countries attended tions will only arise from a coordinated network of di- the meeting, shared ideas, identified needs and tried to verse expertises, from molecular biology and neuro- elaborate strategies for the near future. The fly D. su- physiology to pest management techniques. The main zukii (also known as spotted wing drosophila, SWD, in focus of this review will thus be the possible research the USA) is an invasive pest endemic to South East Asia lines able to provide management solutions to the chal- which recently invaded western countries where it is lenge D. suzukii poses to European fruit production. We now threatening both the European and the American draw up a draft research agenda in the hope that it will fruit industry, due to its egg laying and feeding on un- guide future research. wounded ripening fruits of many plant species. D. suzukii has been reported so far in most of the Mediterranean countries in Europe and is rapidly Where does the pest come from and where spreading toward north and east. In most attacked coun- will it go? tries D. suzukii caused extensive economic damage to small fruits (Goodhue et al., 2011); for this reason, and What does D. suzukii look like? because efficient monitoring and control tools are not D. suzukii adults are drosophilid (2-3 mm long) yet available for this species, growers and producers at with red eyes, a pale brown or yellowish brown thorax the Trento meeting pushed for immediate and efficient and black stripes on the abdomen. Sexual dimorphism is solutions. The European and Mediterranean Plant Pro- evident: males display a dark spot on the leading top tection Organization (EPPO) recently presented a pest edge of each wing and females possess a large serrated risk assessment (PRA), in which it was concluded that ovipositor (Kanzawa, 1939; Walsh et al., 2011). Despite D. suzukii is a threat for most parts of the EPPO region, these evident features, the identification of D. suzukii where the pest will likely spread further, and that com- presents several challenges: adults can be easily mis- plete eradication is unfeasible and management difficult identified, as it occurred for example in California, (information available at www.eppo.org). where it was initially erroneously identified as Droso- Inspired by the meeting, we review the knowledge phila biarmipes Malloch (Hauser, 2011). gained so far about D. suzukii life history traits in a The distinguishing features of the two sexes (serrated European context. Extensive information can be found ovipositor and black wing spots) are present in other

Drosophila species, thus making species identification D. suzukii is rapidly spreading across Europe difficult in areas where they are sympatric. For example, If phylogenetic relationships of D. suzukii have not Drosophila subpulchrella Takamori et Watabe males’ been resolved yet, little is known about its geographical black spots are very similar in shape and position to origin either. It was firstly described in in 1916, those of D. suzukii (Takamori et al., 2006). Moreover, where it was found to attack cherries, but it is still un- small or young D. suzukii males sometimes lack the certain whether it is native to this area or possibly intro- wing spot, which becomes clearly visible circa two days duced around the turn of the last century (Kanzawa, after emergence (Hauser, 2011), which could lead to 1936). The fly is also present in the eastern part of misidentification with other Drosophila males. Other (Peng, 1937), Taiwan (Lin et al., 1977), North characteristics may thus guide identification, such as the and South (Chung, 1955; Kang and Moon, 1968), sex combs on the foretarsi (D. suzukii has one row of Pakistan (Amin ud Din et al., 2005), Myanmar (Toda, combs on the first and one row on the second tarsal seg- 1991), Thailand (Okada, 1976), the Russian Far East ment) (Kikkawa and Peng, 1938; Parshad and Paika, (Sidorenko, 1992) and India (Kashmir region, Parshad 1965; Bock and Wheeler, 1972). Therefore, in many and Duggal, 1965), where it was described as the D. su- cases, only analyses of a full set of features, also in- zukii subspecies indicus (Parshad and Paika, 1965). cluding male genitalia (Hsu, 1949; Okada, 1954; Par- D. suzukii is currently spreading in many areas, such shad and Paika, 1965; Bock and Wheeler, 1972), enable as the USA (West and East coast), Canada, Mexico and a reliable identification. Similar problems arise with Europe (a history of the introduction in females. On the basis of the shape and length of the is reviewed by Hauser, 2011). A key feature of its rapid ovipositor, D. suzukii can be easily discriminated from spread was the initial lack of regulation over the spread related species, as for example D. biarmipes, but not of any Drosophila. In Europe it was first reported in au- easily from other species such as Drosophila immi- tumn 2008 in (Rasquera Province) (Calabria et grans Sturtevant and D. subpulchrella (Takamori et al., al., 2012), although a recent publication offers an up- 2006) which possess very similar ovipositors (Hauser, date of its first findings in Europe. Malaise traps de- 2011). In such cases, a final determination should rely ployed in Tuscany (San Giuliano Terme, Pisa, Italy) in on the relative size of spermatheca compared to ovi- 2008, whose catches were examined only recently, positor’s size: it is thus feasible only for the trained caught D. suzukii adults contemporaneously with those eyes of taxonomists (Hauser, 2011). The situation is deployed in Spain (Raspi et al., 2011). complex also for immature stages (eggs, larvae and pu- In 2009 D. suzukii adults were recorded in traps in pae), where no reliable morphological diagnostic fea- other regions of Spain (Bellaterra, near Barcelona) tures have been identified (Okada, 1968). The D. su- France (Montpellier and Maritimes Alpes) and Italy zukii egg has two respiratory appendages but this char- (Trentino) (Grassi et al., 2009; Calabria et al., 2012). In acter is not species-specific. Therefore, DNA barcoding Trentino, both first oviposition on wild hosts (Vaccin- is the only fully reliable identification tool (Doczkal D., ium, Fragaria and Rubus spp.) and economically impor- http://barcodenews.net/2012/02/22/). tant damage on several species of cultivated berries were reported (Grassi et al., 2009). A difficult tree for a fruit pest By 2010-2011, the range of D. suzukii was further D. suzukii belongs to the subgenus , which enlarged. In Italy it was reported in several other re- is divided into several species groups. One of them, the gions: Piedmont, Aosta Valley, Lombardy, Veneto, melanogaster species group, also contains the famous Emilia Romagna, Liguria, Marche and Campania (Fran- “workhorse” of experimental biology and genetics, chi and Barani, 2011; Pansa et al., 2011; Süss and Co- Meigen (Powell, 1997). The stanzi, 2011; Griffo et al., 2012) and in France it was melanogaster group is further divided into species sub- found from Corsica up to Ile de France (Mandrin et al., groups, one of which (the suzukii subgroup) composes, 2010; Weydert and Bourgouin, 2011). Then, many other together with 6 other subgroups, the “oriental lineage” European countries made their first record: Switzerland (Kopp and True, 2002; Schawaroch, 2002; van der (Baroffio and Fisher, 2011), Slovenjia (Seljiak, 2011), Linde et al., 2010). Croazia (Masten Milek et al., 2011), Austria (Leth- However, relationships between and within these sub- mayer, 2011), Germany (Vogt et al., 2012) and groups are still far from being resolved, and the suzukii (EPPO Website). subgroup itself is commonly regarded as polyphyletic The data presented and summarized in figure 1 reflect (Kopp and True, 2002). A recent paper suggested the current known distribution of D. suzukii in Europe. D. biarmipes as the sister species of D. suzukii (Yang et It appears to be spreading rapidly and all of continental al., 2011), in accordance with previous findings (Kopp Europe is at risk for invasion. We advocate an inte- and True, 2002; Barmina and Kopp, 2007), but in con- grated, precise and area-wide monitoring network. It is trast with Prud’homme et al. (2006) and van der Linde worthwhile to note that the lack of reports from several and Houle (2008), which instead supported D. subpul- areas is probably due to a lack of monitoring rather than chrella as the sister species of D. suzukii (with D. biar- to an actual absence of D. suzukii. Thus, the history of mipes being the sister species of D. subpulchrella + reports might reflect differences in the sampling effort D. suzukii). Conflicting results could be due to inade- and/or problems of awareness rather than the true D. quate sampling of taxa and characters, as well as being suzukii distribution. due to the complex phylogenetic signal residing in dif- Considering the recent reports together with the out- ferent genes (Rota Stabelli, unpublished data). puts of the available degree-day phenological models

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Figure 1. The escalating outbreak of D. suzukii in Europe. European countries and Italian regions are represented by different colours on the maps according to the year of the first finding. The fly drawings are placed in the areas of the first record.

(Damus, 2009; Coop, 2010) and analysis of D. suzukii ondary infections of pathogens - such as filamentous host plants distribution (EPPO website), it is very likely fungi, yeasts and bacteria - that may cause faster deterio- that D. suzukii will spread all over Europe. Indeed, eco- ration and further losses. Additional costs are related to logical simulations indicate the northern humid areas as increased production costs related to pest control (moni- more suitable ecosystems compared to the Mediterra- toring and chemical input costs, increased labour and fruit nean drier environments, especially because desiccation selection, reduction of the fruit shelf life, storage costs) seems to be a limiting factor for drosophilids (Walsh et and to the decrease of foreign market appeal for produc- al., 2011). If the current climate changes are taken into tion from contaminated areas (Goodhue et al., 2011). account, even Scandinavian countries can not be con- However, the oviposition habit itself is not enough to sidered exempt from these risks of invasion. On a wider explain the dramatic impact of D. suzukii on production. geographic perspective, according to D. suzukii biology, In the next sections we show the main features making the global expansion in regions with climatic conditions D. suzukii a threat of high concern for the European spanning from subtropical to continental is highly likely fruit production. to happen (Walsh et al., 2011). Furthermore, niche shifts, as occurred for other pests (e.g. in- Extreme fecundity dianus Gupta, Da Mata et al., 2010), should not be ex- Adults of D. suzukii reach maturity one or two days cluded (Calabria et al., 2012), which suggests that after emergence (during the warm season). Mating oc- D. suzukii could become a global problem for fruit pro- curs from the first days of life and females start to lay duction. It has yet to arrive in South America or Africa, eggs already from the second day from emergence. Fe- but seems likely to reach there in the future. males typically lay 1-3 eggs per fruit in up to 7-16 fruits per day; since they are able to oviposit for 10-59 days, they can lay up to a total of 600 eggs during their life- Why is D. suzukii a threat for fruit production? time (around 400 eggs on average). Eggs hatch within 2 to 72 hours after being laid inside fruits, and larvae ma- Unlike most other Drosophilidae, possibly exempting ture (inside the fruit) in 3 to 13 days. Pupae reside inside D. subpulchrella, D. suzukii is able to lay eggs in or, less frequently, outside the fruit, for 3 to 15 days. healthy, unwounded fruit thanks to the serrated female Depending on the temperature, a minimum of 8 days is ovipositor and not only on damaged or overripe fruits required from oviposition to adult emergence. This very (Sasaki and Sato, 1995). Hence, ripening fruits are pre- short generation time implies that D. suzukii can com- ferred over overripe ones (Mitsui et al., 2006). plete several generations in a single cropping cycle and Most damage caused by D. suzukii is due to larvae up to 7 to 15 generations in a year, according to the spe- feeding on fruit flesh, however the insertion of the cific climatic conditions, thus allowing an explosive prominent ovipositor into the skin of the fruit can cause population growth (life-cycle details can be found in physical damage to the fruit, as it provides access to sec- Kanzawa, 1939; Mitsui et al., 2006; Walsh et al., 2011).

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Tolerance of a wide range of climatic conditions come a field host (with soft skinned varieties being The ability to survive and reproduce in a wide range more impacted) (Griffo et al., 2012). of climatic conditions is obviously a relevant factor for The host-choice flexibility of D. suzukii is also dem- . Limiting temperatures for D. suzukii reproduc- onstrated by the ability to develop also on tomato under tion are between 10 and 32 °C for oviposition and up to laboratory conditions (not recorded so far as a host in 30 °C for male fertility (Sakai et al., 2005). The peak of the field, even if D. suzukii adults have been trapped in activity and development is around 20 to 25 °C (Kan- tomato crops in France (EPPO website). zawa, 1939). D. suzukii can thus be considered a spe- The wide host range represents a pest management cies with high thermal tolerance, being both heat toler- constraint not only because D. suzukii can cause damage (viable D. suzukii populations resist to the hot to many species, but also because populations can sur- summers in Spain) and cold tolerant (D. suzukii is pre- vive almost everywhere, alternating hosts with different sent in cold areas, such as mountain regions in Japan ripening times through the year, both cultivated and and Alpine areas). wild. Indeed, crop plants, usually cultivated in high den- Adults are particularly tolerant to cold compared to sity monoculture, allow rapid and impressive population other drosophilids (Kimura, 1988) and mated females in growth, while wild hosts and ornamental plants may reproductive diapause are considered to be the overwin- serve as refuges from management treatments, and pro- tering stage of D. suzukii (Kanzawa, 1939; Mitsui et al., vide later re-infestation sources and overwintering habi- 2010; Walsh et al., 2011). Whether this tolerance is tats (Klick et al., 2012). physiological or mediated by behavioural adaptation is The wide host range and the ability to damage thick still unclear and several authors suggest that D. suzukii ripening fruits, gives to D. suzukii a wide but at the survival under harsh conditions might be increased by same time specialized ecological niche. However, over- altitudinal migration (Mitsui et al., 2010), acclimatiza- lapping niches and possible competition with other dro- tion (Walsh et al., 2011) and/or overwintering in man- sophilids needs to be investigated. made habitats or other sheltered sites (Kimura, 2004). High dispersal potential Wide host range D. suzukii has a high dispersal potential (Hauser, D. suzukii is able to develop on a very wide range of 2011; Calabria et al., 2012), which would seem to be both cultivated and wild soft-skinned fruits with many confirmed by its rapid spread in invaded countries and host plants in the native and in the invaded areas, with its presence on several continents, as well as remote is- berries being the preferred hosts. The following list of lands (i.e. ; Kaneshiro, 1983;). Passive diffusion D. suzukii host plants grouped based on botanical family due to global trade is likely the main cause of the spread should be still considered tentative, since some informa- of D. suzukii, as for many other invasive species (West- tion is not well documented: Rosaceae - Fragaria phal et al., 2008). The apparently intact and healthy ananassa (strawberry), Rubus idaeus (raspberry), Rubus status (before larval activity) of the fruits infested with fruticosus, , and D. suzukii is likely to compound the problem, as it in- other Rubus species and hybrids of the creases the risk that infestation will remain undetected group, Rubus ursinus (marionberry), Prunus avium and thus the risk of passive dissemination of D. suzukii (sweet cherry), Prunus armeniaca (apricot), Prunus (Calabria et al., 2012). persica (peach), Prunus domestica (plum), Eriobotrya japonica (loquat); Ericaceae - Vaccinium species and hybrids of the blueberry group; Grossulariaceae - Ribes A research agenda for integrated pest man- species including the cultivated currants; Moraceae - agement Ficus carica (fig), Morus spp. (mulberry); Rhamnaceae - Rhamnus alpina ssp. fallax, Rhamnus frangula (buck- Estimating the costs associated with D. suzukii impact is thorn); Cornaceae - Cornus spp. (dogwood); Actinidi- a complex task, with several factors (direct and indirect aceae - Actinidia arguta (hardy kiwi); Ebenaceae - costs) that must be taken into account, their interdepen- Diospyros kaki (persimmon); Myrtaceae - Eugenia dency and the dynamic nature of the system (Goodhue uniflora (Surinam cherry); Rutaceae - Murraya panicu- et al., 2011; Walsh et al., 2011). Preliminary studies in lata (orange jasmine); Myricaceae - Myrica rubra (Chi- the USA indicate an annual loss of more than 500 mil- nese bayberry); Caprifoliaceae - Lonicera spp. (honey- lion dollars in five affected crops (strawberries, blueber- suckle); Elaeagnaceae - Elaeagnus spp.; Adoxaceae - ries, raspberries, blackberries and cherries) in three Sambucus nigra (black elder); Vitaceae - Vitis vinifera, states (California, Oregon and Washington) (Bolda et Vitis labrusca (Kanzawa, 1939; Grassi et al., 2011; Lee al., 2010). Because of regional monoculture, economi- et al., 2011b; Seljak, 2011; Walsh et al., 2011). How- cal losses might be even larger in proportion at a local ever, current data suggest that host preference is heavily scale. A preliminary study estimated that Trento prov- dependent upon the local abundance of hosts. ince (Northern Italy), the area devoted to small fruit cul- The V. vinifera case is still matter of verification. De- tivation (about 400 hectares) faced a loss around spite laboratory experiments that showed a significantly 500,000 € in 2010 and 3 million € in 2011 (Ioriatti et lower oviposition susceptibility and developmental rate al., 2011). of D. suzukii on grapes than on berries and cherry (Lee While fast answers to D. suzukii could be provided by et al., 2011a), recent observations in vineyards in changes in the pesticide regulations and by sanitation Northern Italy would indicate that V. vinifera can be- procedures, these management techniques will only

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have short-term application and effects. Solutions that really highly performing and species-specific trap has are effective and sustainable over the long term are hard not been developed yet (Walsh et al., 2011). Further re- to find in the absence of detailed knowledge of the pest search on baits, trap design and trapping protocols is species life history, as well as of its biological attributes thus needed. and population dynamics. Research on fundamental as- In addition to optimizing bait (with single or multiple pects is thus a key step enabling future management so- components), trap shape, and colour, it is also important lutions. to study the effects of trap placement both in terms of Below we propose a research agenda, which identifies space and time. Traps are currently either placed on the the main relevant topics we consider to be fundamental. ground or hung on plants near fruits, and preliminary The research agenda is based on a paradigm we called evidence indicates that traps perform best when placed the “3M framework”, which stands for Monitoring, in cool and shaded areas (Walsh et al., 2011). Future Modelling and Managing. These steps should be tightly research should investigate the importance of spatial interconnected to each other in order to properly face a variables, both on the microscale (e.g. height, on plants pest invasion challenge; however, for clarity, we will or on the ground) and on the mesoscale (e.g. inside crop treat them separately in this review. areas or along the boarders), as well as the importance of the timing of trapping. Here, e.g., mass trapping Monitoring could be more effective at the onset of the season than A reliable monitoring of the pest presence is the first later on, when the population has already reached high step for a successful integrated pest management (IPM). densities. So far, the monitoring of D. suzukii has been based on trapping methods available for other pests and for Dro- Modelling sophilidae in general, i.e. fermentation baits and vine- Understanding ecological factors influencing feeding, gar, with the main baits being represented by one or a survival, and reproduction is crucial in order to under- mix of the following substances: ripe bananas, straw- stand and forecast the current and future distribution and berry puree, cherry juice, citronella oil, geranium oil, population dynamics of D. suzukii. Attention should be apple cider, vinegar, cherry wine, sugar and yeast mix- paid to both the spatial (distribution at large and small tures (Wu et al., 2007; Walsh et al., 2011). A recent scales) and temporal scale (seasonal variation in abun- study showed a high level of attraction to a combination dance). Coupling high resolution techniques (such as of vinegar and wine, possibly due to a synergistic effect georeferencing) with basic biological knowledge (e.g. of acetic acid, ethanol and other vinegar/wine volatiles life cycle, life history traits) will allow the prediction of (Landolt et al., 2012). the fine scale distribution, pest pressure maps and de- While D. melanogaster and other drosophilids can gree day models, allowing reliable estimates of D. su- complete all life stages on the same fermenting materi- zukii impact and economic losses. This will improve the als, gravid D. suzukii females need to find undamaged choices in sanitation, management and socio- ripening fruits for oviposition. It is therefore likely that economical procedures, and, as a consequence, improve the odour produced by fermenting fruits represents a the effectiveness of pest management decisions. generic food cue to D. suzukii, whereas egg-laying fe- A landscape ecology approach would also be crucial males target volatiles from fresh fruits specifically. Un- to understand the movement of D. suzukii across the fortunately, the knowledge of the sensory and chemical landscape, highlighting possible refuge areas as well as ecology of D. suzukii in relation to feeding, mating and potential sources of re-infestation (Ohrn and Dreves, oviposition is still extremely poor. In particular, the 2012). Modelling should also tackle the timing of identification of the most behaviourally-active volatiles D. suzukii population growth, starting from the first sea- emitted by fruits host of D. suzukii might allow the de- sonal re-infestations to forecast the seasonal dynamics. velopment of more selective and powerful attractant This could help in understanding when to set the trap lures that could be released at controlled rates from dis- and deliver the chemical treatments. Degree-day models pensers. Knowledge of kairomones for D. suzukii will are currently being developed (Damus, 2009; Coop, also form the basis of environmentally friendly strate- 2010), but future research will result in more precise gies, such as mass trapping and attract and kill, which and specific models. showed promising results in initial studies (Kanzawa, The interactions between D. suzukii and the several 1934; Wu et al., 2007). host plants should be taken carefully into account. This The trapping performance is also highly influenced by step could be facilitated by the availability of the trap’s colour, shape and structure. Red and black phenological models for many host species. However it have been shown to be the most attractive colours, may also be hindered by the great number of D. suzukii hence coloured traps would be recommended (Mitsui et hosts. It is thus imperative to deepen our understanding al., 2006; Edwards et al., 2012). The most currently of D. suzukii-host plant interactions and dynamics. used traps are plastic bottles or cups with multiple small Therefore, research should investigate host preference lateral holes (diameter between 5-10 mm) containing and the factors affecting D. suzukii choice of oviposition the liquid bait. The addition of a small drop of surfac- and feeding sites, such as local abundance, population tant or the placement of sticky cards inside the trap in- history or prior experience. Interesting insights in this creases trapping efficiency by preventing the escape of regard could be gathered through the study of D. suzukii flies (Walsh et al., 2011). Even though some trapping biology in its native range, where such phytophagous- protocols already exist (e.g. Dreves et al., 2009), a plant interactions evolved. Initial laboratory experi-

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ments indicate that, while D. suzukii could show prefer- onstrated that covering plants with netting (0.98 mm ences toward certain host plants in nature, it could also mesh size) fully prevented the D. suzukii infestations show differences in the breeding success and thus in the (Kawase et al., 2007). level of impact on different hosts (Lee et al., 2011a). The mechanisms of host reactions and differences in Chemical control their susceptibility (among species, among varieties and Current control efforts for D. suzukii rely heavily on across landscape and times) will thus be worth of inves- the use of . Unfortunately, the insecticides tigating. The integration of crop phenology, pest life cy- which are currently available to growers for control of cle and host-pest interactions will allow the prediction D. suzukii are not very effective, since the use of highly of spread and impact. efficient broad spectrum chemicals is being progres- sively restricted. In particular, organic production is se- Managing riously threatened because only few natural insecticides Preventing new introduction and are admitted and their efficacy against D. suzukii is ei- re-infestation ther not known or lower than the conventional insecti- D. suzukii is spreading across Europe and eradication cides (Walsh et al., 2011). Furthermore, the fast genera- and containment do not seem feasible (EPPO website). tion turnover requires many chemical interventions at However, in order to keep D. suzukii populations at a the ripening stage, which can increase the risk of resi- manageable level, it is critical to avoid recurrent intro- dues in fruits, promote insect resistance and negatively ductions and re-infestations. affect pollinators and other beneficial species. From this perspective, it is crucial to understand However, due to the lack of specific insecticides where the pest comes from, by which vectors it has been against D. suzukii larvae within fruits, research has been and is still being introduced, and determine the most focused on treatments based on chemicals targeting likely sources of re-introduction in a certain region and adults. Kanzawa (1939) found that camphor oil was the re-infestation of a specific crop area. International trade most effective of the treatments he employed, followed is considered a key factor increasing the likelihood of by nicotine sulphate, kerosene emulsion, and neoton but biological invasion (Westphal et al., 2008) and unde- no treatment totally prevented oviposition and most of tected infested fruits are believed to be the most likely these materials are no longer used or acceptable. Recent pathway of colonization for D. suzukii (EPPO website). laboratory and field studies both in the USA and in EU Through population genetics it would be possible to dis- revealed that among the registered insecticides organo- close D. suzukii colonization patterns and dynamics phosphates, timely applications of pyrethrins and spino- (e.g. Fernandez Iriarte et al., 2009 for a related species) syns can provide good contact activity and residual im- and to trace the routes of invasion, which could allow pact for up to 12-14 days (Beers et al., 2011; Bruck et prevention of recurrent introductions. Based on prelimi- al., 2011; Profaizer et al., 2012). In contrast, the effi- nary genetic results and on the similarities between the cacy of the neonicotinoids as adulticides was not satis- dates of introduction, Calabria et al. (2012) suggested factory (Bruck et al., 2011). that the D. suzukii invasions in North America and in Initial trials in the Trentino Province indicated that Europe could be related. only lambda-cyhalothrin provided an adequate level of Removing any possible source of D. suzukii either control. However, at high population densities repeated outside (wild hosts, sites in neighbouring grower fields applications by alternating pyrethrins and spinosad in and ornamental plants in backyard gardens) or inside the strawberry plantations only reduced the damage imme- orchard (fruit production waste) is crucial in order to diately after the treatment and had negligible impact at prevent re-infestations on local scale, and thus repre- the end of the harvest time (Grassi et al., 2012). There- sents a key step in IPM (Walsh et al., 2011). Any fruit fore, future research needs to address not only identifi- that remains in the crop can be a food source or a breed- cation of effective chemicals, but must also consider ing site for D. suzukii, thus acting as a potential re- how protocols for delivery of chemicals can be opti- infestation source. However, once removed, fruits must mized. In addition, growers should undertake a pesticide be destroyed. Several widely used techniques, e.g. com- rotation, in order to avoid or at least delay the evolution posting could in fact worsen the problem, since the of resistance, which can be easy in Droso- fruits and the larvae are not rapidly destroyed, but rather phila species (even associated with a single resistance are able to develop rapidly in the warm environment allele, see Ffrench-Constant and Roush, 1991) also produced by decomposition processes. Several options thanks to the numerous generations per year. for effective disposal of potentially contaminated fruit material have been proposed, e.g. solarization, insecti- Control strategies based on in- cide treatment, disposal in closed containers, crushing, terferences with communication cold treatment, bagging and burial (Walsh et al., 2011; Among the environmentally safe strategies those EPPO website). These sanitation procedures should be based on the interferences with the insect communica- widely applied in the affected areas, in order to avoid tion, both intra- and inter-specific, are often the most the persistence of neglected re-infestation sources. effective and enduring ones (i.e. mating disruption, at- Therefore, many local entities officially imposed sanita- tract and kill, mass trapping). These approaches act ei- tion measures to growers. Research is underway for the ther by reducing the population survival (attract and kill, evaluation of other management methods based on mass trapping) and/or by interfering with its reproduc- physical barriers. As an example, in Japan it was dem- tion (mating disruption).

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Although more research is needed to decipher the sex- other hand, japonica Novkovic et Kimura ual communication of D. suzukii, advantage could be (Hymenoptera ) and japonica Be- taken from the vast knowledge on the model organism lokobylskij (Hymenoptera Braconidae) were able to at- D. melanogaster. Drosophila species use aggregation tack larvae and pupae only in fallen decaying fruits and pheromones which often act in synergism with food attacked a wide range of drosophilid hosts (Mitsui and odours (Bartelt et al., 1985). It might be speculated that Kimura, 2010; Kimura unpublished data). D. suzukii releases also cuticular hydrocarbons which However, it has been recently demonstrated that in- act as sex pheromones for a short range attraction (An- creased constitutive hemocyte levels involved in encap- tony and Jallon, 1982). sulation of parasitoid eggs enable D. suzukii larvae to In addition, both visual cues and air-borne sounds produce a more vigorous immune response and resis- emitted by wing vibrations have been demonstrated to tance than D. melanogaster to their generalist parasitic play a role in the short-range courtship of D. suzukii wasps (Kacsoh and Schlenke, 2012). (Ewing, 1978; Fuyama, 1979). Similarly to D. melano- Nevertheless, another approach for the biological con- gaster, sex peptides produced in the D. suzukii male ac- trol of D. suzukii would be to enhance the effect of bene- cessory glands and transferred into the female during ficial organisms already present in the newly invaded ar- copulation were shown to suppress the female receptiv- eas, generalist and widespread species having D. suzukii ity and to stimulate oviposition (Ohashi et al., 1991; in their host range or, otherwise, species able to adapt Schmidt et al., 1993). their selection strategies to the invader. Indeed, Pachy- Whether the D. suzukii mating and oviposition behav- crepoideus vindemmiae (Rondani) (Hymenoptera Ptero- iour is susceptible to be disrupted with affordable and malidae), a generalist pupal parasitoid considered for a effective methods based on synthetic pheromones, on long time as a major natural enemy of D. melanogaster mechanical signals (i.e. vibrational mating disruption; (Martelli, 1910), was recently found to be also associated Eriksson et al., 2012), or by combinations of them is with D. suzukii in USA (Brown et al., 2011). still matter of conjecture, but is a promising area for fu- Two promising candidates are also Asobara tabida ture research. Nees and its sibling species Asobara rufescens Foerster (Hymenoptera Braconidae), which are the most com- Biological control mon parasitoids of frugivorous drosophilids in Europe There are multiple biocontrol agents (fungi, bacteria, (Vet et al., 1984) and shown able to develop on D. su- viruses and other natural enemies of the pest, such as zukii in the field in Japan (Mitsui et al., 2007). Likewise predators and parasitoids) that could be employed in and in accordance with observations in Japan, generalist IPM for D. suzukii. species of the Trichopria (Hymenoptera Diaprii- dae) distributed in US and EU are likely to accept D. Biocontrol activity of microorganisms: suzukii as an additional host (Kimura, personal commu- Recently, DNA viruses have been isolated also in nication). Furthermore, the impact on D. suzukii popula- Drosophila species (Unkless, 2011) and were found to tion of generalist predators, such as several be related to other viruses used for pest control. These (Rhynchota Anthocoridae) species, is under evaluation findings open the way for the evaluation of control of in different laboratories. D. suzukii based on viral pathogens and research is ur- gently needed on this subject. Exploiting pest-endosymbionts associations: A promising, but sometimes neglected method of re- Parasitoids: ducing pest populations is the exploitation of the inti- Research on as biocontrol agents is also mate association of the pest species with endosymbionts urgently needed, although a control approach based on (Zindel et al., 2011). Arthropods are frequently infected natural enemies would probably be very diffi- with one or more micro-organisms which can have cult for a high-reproduction species like D. suzukii. beneficial, neutral or detrimental effects on their hosts. Nevertheless, several valuable studies on this topic have These interactions may directly or indirectly influence been performed in Japan, in the native range of the spe- the population dynamics of many pest species and could cies. Potentially, results from these studies could help thus potentially be of great interest for agricultural pest identify novel management strategies based on introduc- management (Zindel et al., 2011). tion and permanent establishment of natural enemies of For example, the obligate intracellular bacteria of the D. suzukii from its native range for a long-term control. genus Wolbachia are estimated to infect more than half Early experiments tested the efficacy of Phaenopria of the living insect species, whose reproduction they are spp. (Hymenoptera Diapriidae) under laboratory condi- able to manipulate by provoking several phenotypic ef- tions, however, results were unsatisfactory (Kanzawa, fects (cytoplasmic incompatibility, induction of parthe- 1939). More recent studies have explored the occur- nogenesis, male killing and feminization) (Werren et al., rence and biology of several D. suzukii parasitoids in 2008; Zindel et al., 2011). Japan (Ideo et al., 2008; Mitsui et al., 2007; Kimura un- Cytoplasmic incompatibility (CI) is the most common published data). Species of the genus Ganaspis (Hy- reproductive effect induced by Wolbachia in their hosts. menoptera Figitidae) showed the highest rates of D. su- CI prevents infected males from successfully mating zukii parasitism (ranging from about 2 to 7%). These with females with different Wolbachia infection status species lay eggs in larvae that are feeding in fruits and (non-infected or infected with different and incompatible exhibits a high level of specificity for D. suzukii. On the strains) (Werren et al., 2008). Thus, CI could be used to

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suppress insect pest populations in a manner analogous D. suzukii as a vector of plants to the sterile insect technique (SIT) by releasing males pathogens carrying CI-inducing endosymbionts (see Zabalou et al., An important topic to address is whether D. suzukii 2004). Wolbachia inducing CI have been widely discov- could act as a vector of plant pathogens, thus provoking ered in several Drosophilidae (reviewed in Werren et al., additional damages to the attacked species. Indeed, Dro- 2008) and preliminary results suggest that also D. suzukii sophila flies have long been recognised as microorganism is infected with Wolbachia (Siozios unpublished data). disseminators and the role of fungal disease vectoring has However, Wolbachia has complex phenotypic effects on been demonstrated for D. melanogaster, which carries its hosts, depending on strain, host genotype and interac- (both on its cuticle and inside its digestive tract) the fun- tions between them. In addition to CI, Wolbachia infec- gus Botrytis cinerea (Louis et al., 1996). While D. mela- tion could have significant survival and fecundity effects nogaster only attacks overripe/rotten fruits, thus limiting in drosophilids (Fry et al., 2004). It has recently been the damage caused by B. cinerea, D. suzukii targets intact discovered that Wolbachia infection enhances fertility in fruits, making it possible for the fungus to penetrate in- Tsacas et David, with an average side. Research should thus investigate the potential of four-fold increase in the egg laying rate of infected flies, D. suzukii as a carrier of other microbial diseases. compared to uninfected individuals (Fast et al., 2011). Indeed, a possible link between the D. suzukii spread Future research should address the extremely high fe- and the expansion of two host plants diseases (Monilinia cundity found in D. suzukii, in order to assess whether it brown rots and Botrytis rots) in Slovenia has been sug- is linked in a similar way to Wolbachia infections. Fi- gested (Seljiak, personal communication). Interestingly, nally, due to the rapid spread of Wolbachia in insect also the occurrence of interactions between specific population, these bacteria have also been suggested as yeast species associated with D. suzukii and the yeast vectors for desirable genetic modification that could be profile of the host fruits has recently been proposed, used in control efforts (Sinkins and Gould, 2006). which paves the way for another intriguing field of re- The control potential of Wolbachia is also related to the search on this pest (Hamby et al., 2011). natural enemies of the pest species. Indeed, Wolbachia was shown to induce parthenogenesis in several hymen- Taking advantage from a close optera parasitoids (Werren et al., 2008), thus suggesting relative: the model system potential advantages in their rearing, releasing and effi- D. melanogaster cacy. In addition, a fertility-enhancing effect similar to This review highlighted that knowledge about D. su- that found in D. mauritiana, has been revealed in the zukii is still limited but great advantage could be taken D. suzukii parasitoid A. tabida (Dedeine et al., 2001). from the vast experience on the related excellent model On the other hand, Spiroplasma bacteria can rescue organism, D. melanogaster. Their close relationship of- the sterilization effect induced by a nematode on Dro- fers also fascinating opportunities for addressing some sophila neotestacea Grimaldi, James et Jaenike (Jae- longstanding questions in the field of insect biology nicke et al., 2010), while Wolbachia infections in with a practical outcome. D. melanogaster flies reduce the impact of the fungal For instance, comparative research in D. melanogaster pathogen Beauveria bassiana (Panteleev et al., 2007) will accelerate progress in improving the effectiveness and of viruses (Werren et al., 2008). These three exam- of insecticides. In addition, comparisons with D. mela- ples are of particular interests, since nematodes, fungal nogaster could shed light on the evolution of ecological pathogens and viruses are three widely used options for innovations (as shown in other drosophila flies, Dekker biocontrol of pest insects and candidate biocontrol et al., 2006) and help researchers in understanding what agents for D. suzukii. makes a species invasive. By harnessing the biology workhorse D. melanogaster, Other IPM strategies as well as the high priority pest D. suzukii, the Droso- Reducing pest population is also possible by inunda- phila genus will probably become a model also for agri- tive releases of sterile insects. The development of the cultural and crop protection studies. SIT represents a major breakthrough in pest manage- ment science (Vreysen et al., 2006). Indeed, SIT has several advantages compared to other control strategies, Conclusions e.g. being safe to non-target organisms and acting with an inverse density-dependent mechanism; in addition, The rapid spread of the invasive fruit pest D. suzukii SIT could be integrated with other control strategies poses a challenge to fruit production in Western coun- (Vreysen et al., 2006). Therefore, the feasibility, proce- tries. The biology of D. suzukii suggests that an effec- dures and possible drawbacks of SIT applied to D. su- tive control effort requires an area wide IPM program. zukii management, with male sterility either induced by In order to accomplish this, research needs to address irradiation or based on transgenic insect strains, should D. suzukii basic biology, the development of manage- be investigated, to promote successful use of SIT in the ment tools, the transfer of knowledge and technology to management of several pest species (Dyck et al., 2005). users and, finally, the implementation of the IPM pro- This would include a requirement for mass rearing of gram also at a cultural and societal level (Lee et al., high quality and competitive insects. The short genera- 2011b; Dreves, 2011). While short term solutions to tion time and large field populations would present a limit the current dramatic damage are strongly needed, challenge for control by SIT. only long-term and environmentally friendly manage-

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ment approaches will allow a sustainable control of this CALABRIA G., MACA J., BACHLI G., SERRA L., PASCUAL M., pest. To this aim, research should be carried out to shed 2012.- First records of the potential pest species Drosophila light on many knowledge gaps that are still present. The suzukii (Diptera: Drosophilidae) in Europe.- Journal of Ap- future will surely see a great increase in the knowledge plied Entomology, 136: 139-147. CHUNG Y. J., 1955.- Collection of wild Drosophila on of D. suzukii biology, impact and management. Quelpart Island, Korea.- Drosophila Information Service, 29: 111. COOP L., 2010.- Online phenology and degree-day model for Acknowledgements agricultural and decision-making in the US.- Integrated Plant Protection Center, Botany & Plant Pathology Dep. The authors warmly thank all the speakers and partici- Oregon State University, Corvallis, Oregon, USA. [online] pants of the D. suzukii meeting in Trento and the col- URL: http://uspest.org/risk/models?spp_swd leagues of “Fondazione Edmund Mach” for the enlight- DA MATA R. A., TIDON R., CORTES L. G., DE MARCO P., DINIZ- FILHO J. A. F., 2010.- Invasive and flexible: niche shift in ening discussions. We are grateful to R. Cervo for the the drosophilid Zaprionus indianus (Insecta, Diptera).- Bio- critical reading of an early version of the manuscript. logical Invasions, 12: 1231-1241. Thanks also to I. Pertot, O. Rota Stabelli, V. Mazzoni, DAMUS M., 2009.- Some preliminary results from Climex S. Siozios, J. Bengtsson and B. Mazza for the useful and Maxent distribution modeling of Drosophila comments and to Carlotta Cini and Flavia Evangelista suzukii. Version 2.- CFIA Plant Health Risk for the language revision. We thank Sabrina Pintus of Assessment, Ottawa, Canada. [online] URL: the “Ministero delle Politiche Agricole Alimentari e Fo- http://entomology.oregonstate.edu/sites/default/files/Drosop restali” (Italy) for her suggestions. The preparation of hilaSuzukiiInfestationModel.pdf the review was funded by Autonomous Province of DEDEINE F., VAVRE F., FLEURY F., LOPPIN B., HOCHBERG M. E., BOULETREAU M., 2001.- Removing symbiotic Wolbachia Trento, Call for Proposal Major Projects 2006, Project bacteria specifically inhibits oogenesis in a parasitic wasp.- ENVIROCHANGE. Proceedings of the National Academy of Science USA, 98: 6247-6252. DEKKER T., IBBA I., SIJU K. P., STENSMYR M. C., HANSSON B. References S., 2006.- Olfactory shifts parallel superspecialism for toxic fruit in Drosophila melanogaster sibling, D. sechellia.- Cur- rent Biology, 16: 101-109. AMIN UD DIN M., MAZHAR K., HAQUE S., AHMED M., 2005.- A DREVES A. 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ZABALOU S., RIEGLER M., THEODORAKOPOULOU M, STAUFFER Authors’ addresses: Gianfranco ANFORA (corresponding C., SAVAKIS C., BOURTZIS K., 2004.- Wolbachia-induced cy- author, [email protected]), Claudio IORIATTI, Re- toplasmic incompatibility as a means for insect pest popula- search and Innovation Centre, Fondazione Edmund Mach, via tion control.- Proceedings of the National Academy of Sci- Edmund Mach 1, 38010 San Michele all’Adige (TN), Italy; ence USA, 101: 15042-15045. Alessandro CINI, Laboratoire Ecologie & Evolution UMR ZINDEL R., GOTTLIEB Y., AEBI A., 2011.- Arthropod symbio- 7625, Université Pierre et Marie Curie, 7 quai St Bernard, ses: a neglected parameter in pest- and disease-control pro- 75252 Paris, France. grammes.- Journal of Applied Ecology, 48: 864-872. Received March 30, 2012. Accepted May 2, 2012.

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