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First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents


The invasive spotted wing drosophila, Drosophila suzukii Matsumura (Dipt.: Drosophilidae), a native of East Asia, has widely established in North America and Europe, where it is a serious pest of small and stone fruit crops. The lack of effective indigenous parasitoids of D. suzukii in the recently colonized regions prompted the first foreign exploration for co-evolved parasitoids in South Korea during 2013 and 2014. We collected the larval parasitoids Asobara japonica Belokobylskij, A. leveri (Nixon) and A. brevicauda Guerrieri & van Achterberg (Hym.: Braconidae), Ganaspis brasiliensis (Ihering), Leptopilina japonica japonica Novković & Kimura and L. j. formosana Novković & Kimura (Hym.: Figitidae); and the pupal parasitoids Pachycrepoideus vindemiae (Rondani) (Hym.: Pteromalidae) and Trichopria drosophilae Perkins (Hym.: Diapriidae). From UC Berkeley quarantine records, percentage parasitism ranged from 0 to 17.1 % and varied by geography, season, and collection methods. Asobara japonica was the most common parasitoid species. Higher numbers of parasitoids were reared from field-picked fruit as opposed to traps baited with uninfested fruit. Quarantine bioassays confirmed that A. japonica, G. brasiliensis, L. j. japonica, P. vindemiae, and T. drosophilae developed from D. suzukii. Female individuals of the endoparasitoid, A. japonica, were larger when reared on the larger D. suzukii larvae compared with those reared on the smaller larvae of D. melanogaster Meigen. Larger parasitoid size was associated with longer developmental time. Several of the South Korean parasitoid species have the potential for use in classical biological control and may contribute to the suppression of D. suzukii in the newly invaded regions.

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  1. Adrion JR, Kousathanas A, Pascual M, Burrack HJ, Haddad NM, Bergland AO et al (2014) Drosophila suzukii: the genetic footprint of a recent, worldwide invasion. Mol Biol Evol 31:3148–3163

  2. Asplen M, Anfora G, Biondi A, Choi D-S, Chu D, Daane KM et al (2015) Invasion biology of spotted wing drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494

  3. 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. Proc R Soc Biol Sci Ser B 281:2013–2840

  4. Beers EH, Van Steenwyk RA, Shearer PW, Coates WW, Grant JA (2011) Developing Drosophila suzukii management programs for sweet cherry in the western United States. Pest Manag Sci 67:1386–1395

  5. Bolda MP, Goodhue RE, Zalom FG (2010) Spotted wing drosophila: potential economic impact of a newly established pest. Giannini Foundation of Agricultural Economics, University of California

  6. Bruck DJ, Bolda M, Tanigoshi L, Klick J, Kleiber J, DeFrancesco J et al (2011) Laboratory and field comparisons of insecticides to reduce infestation of Drosophila suzukii in berry crops. Pest Manag Sci 67:1375–1385

  7. Buffington ML, Forshage M (2016) Redescription of Ganaspis brasiliensis (Ihering, 1905), new combination (Hymenoptera: Figitidae), a natural enemy of the invasive Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae). Proc Entomol Soc Wash 118(1):1–13

  8. Burrack HJ, Fernandez GE, Spivey T, Kraus DA (2013) Variation in selection and utilization of host crops in the field and laboratory by Drosophila suzukii Matsumara (Diptera: Drosophilidae), an invasive frugivore. Pest Manag Sci 69:1173–1180

  9. Calabria G, Máca J, Bachli G, Serra L, Pascual M (2012) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136:139–147

  10. Carton Y, Boulétreau B, van Alphen JJM, van Lenteren JC (1986) The Drosophila parasitic wasps. In: Ashburner M, Carson HL, Thompson JN (eds) The genetics and biology of Drosophila. Academic Press, London, pp 347–394

  11. Chabert S, Allemand R, Poyet M, Eslin P, Gibert P (2012) Ability of European parasitoids (Hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii. Biol Control 63:40–47

  12. Chiu JC, Jiang X, Zhao L, Hamm CA, Cridland JM, Saelao P et al (2013) Genome of Drosophila suzukii, the spotted wing drosophila. G3 3:2257–2271

  13. Cini A, Anfora G, Escudero-Colomar LA, Grassi A, Santosuosso U, Seljak G et al (2014) Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe. J Pest Sci 87:559–566

  14. 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 Manag Sci 67:1368–1374

  15. Deprá M, Poppe JL, Schmitz HJ, De Toni DC, Valente VLS (2014) The first records of the invasive pest Drosophila suzukii in the South American continent. J Pest Sci 87:379–383

  16. Desneux N, Blahnik R, Delebecque CJ, Heimpel GE (2012) Host phylogeny and specialisation in parasitoids. Ecol Lett 15:453–460

  17. Emiljanowicz LM, Ryan GD, Langille A, Newman J (2014) Development, reproductive output and population growth of the fruit fly pest Drosophila suzukii (Diptera: Drosophilidae) on artificial diet. J Econ Entomol 107:1392–1398

  18. Gabarra R, Riudavets J, Rodríguez GA, Pujade-Villar J, Arnó J (2015) Prospects for the biological control of Drosophila suzukii. Biocontrol 60:331–339

  19. 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 Manag Sci 67:1396–1402

  20. Guerrieri E, Giorgini M, Cascone P, Carpenito S, van Achterberg C (2016) Species diversity in the parasitoid genus Asobara (Hymenoptera: Braconidae) from the native area of the fruit fly pest Drosophila suzukii (Diptera: Drosophilidae). PLoS One 11:e0147382

  21. 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 Manag Sci 67:1352–1357

  22. Ideo S, Watada M, Mitsui H, Kimura MT (2008) Host range of Asobara japonica (Hym.: Braconidae), a larval parasitoid of drosophilid flies. Entomol Sci 11:1–6

  23. 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. J Econ Entomol 108:1148–1155

  24. Kacsoh BZ, Schlenke TA (2012) High hemocyte load is associated with increased resistance against parasitoids in Drosophila suzukii, a relative of D. melanogaster. PLoS One 7:e34721

  25. Kanzawa T (1939) Studies on Drosophila suzukii Mats (in Japanese): Yamanashi Agricultural Experimental Station. Kofu, Japan

  26. Kasuya N, Mitsui H, Ideo S, Watada M, Kimura MT (2013) Ecological, morphological and molecular studies on Ganaspis individuals (Hymenoptera: Figitidae) attacking Drosophila suzukii (Diptera: Drosophilidae). Appl Entomol Zool 48:87–92

  27. Kinjo H, Kunimi Y, Ban T, Nakai M (2013) Oviposition efficacy of Drosophila suzukii (Diptera: Drosophilidae) on different cultivars of blueberry. J Econ Entomol 106:1767–1771

  28. Klick J, Lee JC, Hagler JR, Bruck DJ, Yang WQ (2014) Evaluating Drosophila suzukii immunomarking for mark-capture research. Entomol Exp Appl 152:31–41

  29. Klick J, Yang W, Walton V, Dalton D, Hagler J, Dreves A, Lee JC, Bruck D (2015) Distribution and activity of Drosophila suzukii in cultivated raspberry and surrounding vegetation. J Appl Entomol. doi:10.1111/jen.12234

  30. Kraaijeveld AR (1999) Kleptoparasitism as an explanation for paradoxical oviposition decisions of the parasitoid Asobara tabida. J Evol Biol 12:129–133

  31. Lee JC, Bruck DJ, Curry H, Edwards D, Haviland DR, Van Steenwyk RA et al (2011) The susceptibility of small fruits and cherries to the spotted-wing drosophila, Drosophila suzukii. Pest Manag Sci 67:1358–1367

  32. Lee JC, Dreves AJ, Cave AM, Kawai S, Isaacs R, Miller JC et al (2015) Infestation of wild and ornamental noncrop fruits by Drosophila suzukii (Diptera: Drosophilidae). Ann Entomol Soc Am 108:117–129

  33. Miller B, Anfora G, Buffington M, Daane KM, Dalton DT et al (2015) Seasonal occurrence of resident parasitoids associated with Drosophila suzukii in two small fruit production regions of Italy and the USA. Bull Insectol 68:255–263

  34. Mitsui H, Kimura MT (2010) Distribution, abundance and host association of two parasitoid species attacking frugivorous drosophilid larvae in central Japan. Eur J Entomol 107:535–540

  35. Mitsui H, Takahashi KH, Kimura MT (2006) Spatial distributions and clutch sizes of Drosophila species ovipositing on cherry fruits of different stages. Popul Ecol 48:233–237

  36. Mitsui H, Van Achterberg K, Nordlander G, Kimura MT (2007) Geographical distributions and host associations of larval parasitoids of frugivorous Drosophilidae in Japan. J Nat Hist 41:1731–1738

  37. Murata Y, Ideo S, Watada M, Mitsui H, Kimura MT (2009) Genetic and physiological variation among sexual and parthenogenetic populations of Asobara japonica (Hymenoptera: Braconidae), a larval parasitoid of drosophilid flies. Eur J Entomol 106:171–178

  38. Nomano FY, Mitsui H, Kimura MT (2015) Capacity of Japanese Asobara species (Hymenoptera; Braconidae) to parasitize a fruit pest Drosophila suzukii (Diptera; Drosophilidae). J Appl Entomol 139:105–113

  39. Ometto L, Cestaro A, Ramasamy S, Grassi A, Revadi S, Siozios S et al (2013) Linking genomics and ecology to investigate the complex evolution of an invasive Drosophila pest. Genome Biol Evol 5:745–757

  40. Poyet M, Havard S, Prévost G, Chabrerie O, Doury G, Gibert P et al (2013) Resistance of Drosophila suzukii to the larval parasitoids Leptopilina heterotoma and Asobara japonica is related to haemocyte load. Physiol Entomol 38:45–53

  41. Poyet M, Eslin P, Heraude M, Le Roux V, Prévost G, Gibert P et al (2014) Invasive host for invasive pest: when the Asiatic cherry fly (Drosophila suzukii) meets the American black cherry (Prunus serotina) in Europe. Agri For Entomol 16:251–259

  42. Rossi Stacconi MV, Grassi A, Dalton DT, Miller B, Ouantar M, Loni A et al (2013) First field records of Pachycrepoideus vindemiae as a parasitoid of Drosophila suzukii in European and Oregon small fruit production areas. Entomologia 1:1–15

  43. Rossi Stacconi MV, Buffington M, Daane KM, Dalton DT, Grassi A, Kaçar G et al (2015) Host stage preference, efficacy and fecundity of parasitoids attacking Drosophila suzukii in newly invaded areas. Biol Control 84:28–35

  44. Steffan SA, Lee JC, Singleton ME, Vilaire A, Walsh DB, Lavine LS et al (2013) Susceptibility of cranberries to Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 106:2424–2427

  45. Stewart TJ, Wang X-G, Molinar A, Daane KM (2014) Factors limiting peach as a potential host for Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 107:1771–1779

  46. Tochen S, Dalton DT, Wiman N, Hamm C, Shearer PW, Walton VM (2014) Temperature-related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry. Environ Entomol 43:501–510

  47. Van Alphen JJM, Janssen ARM (1982) Host selection by Asobara tabida (Braconidae: Alysinae) a larval parasitoids of fruit inhabiting Drosophila species 2: host species selection. Neth J Zool 32:194–214

  48. Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee J, Bruck DJ, Walton VM, O’Neal SD, Zalom FG (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag 2:G1–G7

  49. Wang XG, Kaçar G, Biondi A, Daane KM (2016) Life-history and host preference of Trichopria drosophilae, a pupal parasitoid of spotted wing drosophila. BioControl. doi:10.1007/s10526-016-9720-9

  50. Wiman NG, Walton VM, Dalton DT, Anfora G, Burrack HJ, Chiu JC et al (2014) Integrating temperature-dependent life table data into a matrix projection model for Drosophila suzukii population estimation. PLoS One 9:e106909

  51. Yu D, Zalom FG, Hamby KA (2013) Host status and fruit odor response of Drosophila suzukii (Diptera: Drosophilidae) to figs and mulberries. J Econ Entomol 106:1932–1937

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We thank Riki York and Kyoo Park (Oregon State University), Hyun Jung Kim and Jongwoo Nam (Seoul Women’s University), Uk-Jin Park and Rameswor Maharjan (Andong National University), Oh-Gyeong Kwon (Kyungpook National University), Deuk So Choi (Department of Plant Quarantine, Anyang-si), and Iksoo Kim (Chonnam National University, Gwangju) for assistance with collections in South Korea and Hongyin Chen and Chenxi Liu (Chinese Academy of Agricultural Science), Zon Qi Chen and Yang Wang (Yunnan Academy of Agricultural Science) for collections in China; John Hutchins and Brandy Chavez (University of California, Berkeley) for assistance with insect rearing in the quarantine; and Ken Bloem (Biological Control Coordinator, USDA, APHIS, PPQ) for program design. Antonio Biondi was supported through the People Programme of the European Union’s Seventh Framework Programme FP7/2007–2013 Project ASCII-PIRSES 318246 and from the Italian Ministry of Education, University and Research (PRIN project GEISCA, 2010CXXHJE_004). Funding for research was supported in the US by the USDA-NIFA award # 2010-51181-21167, the USDA APHIS (Farm bill, fund 14-8130-0463), and the California Cherry Board, and in Italy by the UE FP7/2007–2013 project ASCII under Grant agreement PIRSES-GA-2012-318246. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. USDA is an equal opportunity provider and employer.

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Correspondence to Kent M. Daane.

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Communicated by M. Traugott.

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Daane, K.M., Wang, X., Biondi, A. et al. First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. J Pest Sci 89, 823–835 (2016). https://doi.org/10.1007/s10340-016-0740-0

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  • Biological control
  • Invasive species
  • Parasitoid
  • Spotted wing drosophila