Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Department of Environmental Science, Policy and Management, University of California Berkeley, Berkeley, CA, USA

    Kent M. Daane, Xin-Geng Wang & Antonio Biondi

  2. Department of Agriculture, Food and Environment, University of Catania, Catania, Italy

    Antonio Biondi

  3. Department of Horticulture, Oregon State University, Corvallis, OR, USA

    Betsey Miller, Jeffrey C. Miller & Vaughn M. Walton

  4. Department of Horticulture, Mid-Columbia Extension and Experiment Station, Oregon State University, Hood River, OR, USA

    Helmut Riedl & Peter W. Shearer

  5. Institute for Sustainable Plant Protection, CNR, Portici, Italy

    Emilio Guerrieri & Massimo Giorgini

  6. Systematic Entomology Laboratory, USDA Agricultural Research Service, Washington, D.C., USA

    Matthew Buffington

  7. Department of Entomology, National Museum of Natural History, Leiden, The Netherlands

    Kees van Achterberg

  8. Gyeongsang University, Jinju, South Korea

    Yoohan Song & Taegun Kang

  9. Seoul Women’s University, Seoul, South Korea

    Hoonbok Yi

  10. Department of Plant Medicine, Andong National University, Andong, South Korea

    Chuleui Jung

  11. Department of Applied Biology, Kyungpook National University, Daegu, South Korea

    Dong Woon Lee

  12. Gyeongnam Agricultural Research and Extension Service, Jinju, South Korea

    Bu-Keun Chung

  13. Beneficial Insects Introduction Research Unit, USDA Agricultural Research Service, Newark, DE, USA

    Kim A. Hoelmer

Authors
  1. Kent M. Daane
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xin-Geng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antonio Biondi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Betsey Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jeffrey C. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Helmut Riedl
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Peter W. Shearer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Emilio Guerrieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Massimo Giorgini
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Matthew Buffington
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Kees van Achterberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yoohan Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Taegun Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Hoonbok Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Chuleui Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Dong Woon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Bu-Keun Chung
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Kim A. Hoelmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Vaughn M. Walton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kent M. Daane.

Additional information

Communicated by M. Traugott.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Daane, K.M., Wang, XG., 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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-016-0740-0

Keywords

Search

Navigation