, Volume 64, Issue 1, pp 9–19 | Cite as

Augmentative releases of Trichopria drosophilae for the suppression of early season Drosophila suzukii populations

  • Marco Valerio Rossi StacconiEmail author
  • Alberto Grassi
  • Claudio Ioriatti
  • Gianfranco Anfora


Biological control agents may play an important role in regulating Drosophila suzukii Matsumura (Diptera: Drosophilidae), particularly after the winter population bottleneck. Here we test the ability of the cosmopolitan pupal parasitoid, Trichopria drosophilae (Perkins) (Hymenoptera: Diapriidae), to reduce early season D. suzukii populations. We performed augmentative releases of the parasitoid during late March–April and carried out extensive monitoring activity on both parasitoid and fly populations. Results clearly showed a mitigation of the D. suzukii population in the treated areas, associated with a higher T. drosophilae parasitism. A 34% reduction in fruit infestation was observed in the unmanaged vegetation surrounding orchards. Accordingly, pest eclosion was significantly lower in the treated area compared to the untreated one. Our results suggest that augmentative release of T. drosophilae can improve pest control of D. suzukii in the unmanaged areas surrounding the crops, thus lowering the severity of pest outbreaks in the orchards.


Biological control Spotted-wing drosophila Diapriidae Field trials Parasitism Cherry 



We thank Mrs. Linda Brewer and Mr. Daniel T. Dalton (Oregon State University, Horticulture) for improving the English of the manuscript, prof. Vaughn Walton (Oregon State University, Horticulture) for critical revision of the study, Dr. Valerio Mazzoni (Fondazione Edmund Mach, Italy) and Dr. Lan Xue (Oregon State University, Statistics) for statistical advice and Mr. Marco Mosti (Bioplanet s.c.a.) for providing the parasitoids used in this study. Funding for research was partially provided by the Fondazione Cassa di Risparmio Trento e Rovereto (CaRiTRo) (grant number: 1238/2015 giovani ricercatori).


  1. 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. J Pest Sci 88:469–494CrossRefGoogle Scholar
  2. Benito NP, Lopes-da-Silva L, Silva Sivori, dos Santos R (2016) Potential spread and economic impact of invasive Drosophila suzukii in Brazil. Pesqui Agropecu Bras 51(5):571–578CrossRefGoogle Scholar
  3. Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8(9):e76548CrossRefGoogle Scholar
  4. Biondi A, Wang XG, Miller JC, Miller B, Shearer PW, Zappalà L, Siscaro G, Walton VW, Hoelmer KA, Daane KM (2017) Innate olfactory responses of Asobara japonica toward fruits infested by the invasive spotted wing drosophila. J Insect Behav 30:495–506CrossRefGoogle Scholar
  5. 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. J Pest Sci 89:749–759CrossRefGoogle Scholar
  6. Bruck DJ, Bolda M, Tanigoshi L, Klick J, Kleiber J, DeFrancesco J, Gerdeman B, Spitler H (2011) Laboratory and field comparisons of insecticides to reduce infestation of Drosophila suzukii in berry crops. Pest Manag Sci 67:1375–1385CrossRefGoogle Scholar
  7. Cha DH, Adams T, Werle CT, Sampson BJ, Adamczyk JJ, Rogg H, Landolt PJ (2014) A four-component synthetic attractant for Drosophila suzukii (Diptera: Drosophilidae) isolated from fermented bait headspace. Pest Manag Sci 70:324–331CrossRefGoogle Scholar
  8. Daane KM, Wang XG, Biondi A, Miller B, Miller JC, Riedl H, Shearer PW, Guerrieri E, Giorgini M, Buffington M, van Achterberg K, Song Y, Kang T, Yi H, Jung C, Lee DW, Chung BK, Hoelmer KA, Walton VM (2016) First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. J Pest Sci 89(3):823–835CrossRefGoogle Scholar
  9. 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 Manag Sci 73(11):2318–2327CrossRefGoogle Scholar
  10. Diepenbrock LM, Burrack HJ (2016) Variation of within-crop microhabitat use by Drosophila suzukii (Diptera: Drosophilidae) in blackberry. J Appl Entomol 141:1–7CrossRefGoogle Scholar
  11. Dutcher JD (2007) A review of resurgence and replacement causing pest outbreaks in IPM. In: Ciancio A, Mukerji KG (eds) General concepts in integrated pest and disease management. Integrated management of plants pests and diseases, vol 1. Springer, Dordrecht, pp 27–43CrossRefGoogle Scholar
  12. 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 Manag Sci 73(6):1083–1090CrossRefGoogle Scholar
  13. Flinn PW, Hagstrum DW (1995) Simulation model of Cephalonomia waterstoni (Hymenoptera: Bethylidae) parasitizing the rusty grain beetle (Coleoptera: Cucujidae). Environ Entomol 24:1608–1615CrossRefGoogle Scholar
  14. Gabarra R, Riudavets J, Rodríguez GA, Pujade-Villar J, Arnó J (2015) Prospects for the biological control of Drosophila suzukii. BioControl 84:28–35Google Scholar
  15. Girod P, Rossignaud L, Haye T, Kenis M (2017) First results of the testing of Asian parasitoids as potential biological control agents of the Spotted Wing Drosophila, Drosophila suzukii. IOBC/WPRS Bull 123:186–187Google Scholar
  16. Girod P, Lierhmann O, Urvois T, Turlings TCJ, Kenis M, Haye T (2018) Host specificity of Asian parasitoids for potential classical biological control of Drosophila suzukii. J Pest Sci 91:1241–1250CrossRefGoogle Scholar
  17. 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/WPRS Bull 109:197–204Google Scholar
  18. Grassi A, Gottardello A, Dalton DT, Tait G, Rendon D, Ioriatti C, Gibeaut D, Rossi Stacconi MV, Walton VM (2018) Seasonal reproductive biology of Drosophila suzukii (Diptera: Drosophilidae) in temperate climates. Environ Entomol 47(1):166–174CrossRefGoogle Scholar
  19. 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. J Pest Sci 89:643–651CrossRefGoogle Scholar
  20. Heimpel NJ, Mills GE (2017) Biological control: ecology and applications. Cambridge University Press, Cambridge, p 379CrossRefGoogle Scholar
  21. Iglesias LE, Nyoike TW, Liburd OE (2014) Effect of trap design, bait type, and age on captures of Drosophila suzukii (Diptera: Drosophilidae) in berry crops. J Econ Entomol 107:1508–1518CrossRefGoogle Scholar
  22. Kaçar G, Wang XG, Biondi A, Daane KM (2017) Linear functional response by two pupal Drosophila parasitoids foraging within single or multiple patch environments. PLoS ONE 12(8):e0183525CrossRefGoogle Scholar
  23. Kalajdzic P, Schetelig MF (2016) CRISPR/Cas-mediated gene editing using purified protein in Drosophila suzukii. Entomol Exp et Appl 164(3):350–362CrossRefGoogle Scholar
  24. Kaser JM, Heimpel GE (2015) Linking risk and efficacy in biological control host–parasitoid models. Biol Control 90:49–60CrossRefGoogle Scholar
  25. Kenis M, Tonina L, Eschen R, van der Sluis B, Sancassani M, Mori N, Haye T, Helsen H (2016) Non-crop plants used as hosts by Drosophila suzukii in Europe. J Pest Sci 89(3):735–748CrossRefGoogle Scholar
  26. Klick J, Yang WQ, Walton VM, Dalton DT, Hagler JR, Dreves AJ, Lee JC, Bruck DJ (2016) Distribution and activity of Drosophila suzukii in cultivated raspberry and surrounding vegetation. J Appl Entomol 140(1–2):37–46CrossRefGoogle Scholar
  27. Knoll V, Ellenbroek T, Romeis J, Collatz J (2017) Seasonal and regional presence of hymenopteran parasitoids of Drosophila in Switzerland and their ability to parasitize the invasive Drosophila suzukii. Sci Rep 7:40697CrossRefGoogle Scholar
  28. Lanouette G, Brodeur J, Fournier F, Martel V, Vreysen M, Cáceres C, Firlej A (2017) The sterile insect technique for the management of the spotted wing drosophila, Drosophila suzukii: establishing the optimum irradiation dose. PLoS ONE 12(9):e0180821CrossRefGoogle Scholar
  29. Leach H, van Timmeren S, Isaacs R (2016) Exclusion netting delays and reduces Drosophila suzukii (Diptera: Drosophilidae) infestation in raspberries. J Econ Entomol 109(5):2151–2158CrossRefGoogle Scholar
  30. Leach H, Moses J, Hanson E, Fanning P, Isaacs R (2018) Rapid harvest schedules and fruit removal as non-chemical approaches for managing spotted wing Drosophila. J Pest Sci 91(1):219–226CrossRefGoogle Scholar
  31. 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 F, Bruck DJ (2013) Trap designs for monitoring Drosophila suzukii (Diptera: Drosophilidae). Environ Entomol 42(6):1348–1355CrossRefGoogle Scholar
  32. Lee JC, Dreves AJ, Cave AM, Kawai S, Isaacs R, Miller JC, van Timmeren S, Bruck DJ (2015) Infestation of wild and ornamental noncrop fruits by Drosophila suzukii (Diptera: Drosophilidae). Ann Entomol Soc Am 108:117–129CrossRefGoogle Scholar
  33. Mazzetto F, Marchetti E, Amiresmaeili N, Sacco D, Francati S, Jucker C, Dindo ML, Lupi D, Tavella L (2016) Drosophila parasitoids in northern Italy and their potential to attack the exotic pest Drosophila suzukii. J Pest Sci 89:837–850CrossRefGoogle Scholar
  34. 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):18CrossRefGoogle Scholar
  35. Miller B, Anfora G, Buffington M, Daane KM, Dalton DT, Hoelmer KM, Rossi Stacconi MV, Grassi A, Ioriatti C, Loni A, Miller JC, Ouantar M, Wang XG, Wiman NG, Walton VM (2015) Seasonal occurrence of resident parasitoids associated with Drosophila suzukii in two small fruit production regions of Italy and the USA. Bull Insectol 68:255–263Google Scholar
  36. Nikolouli K, Colinet H, Renault D, Enriquez T, Mouton L, Gibert P, Sassu F, Cáceres C, Stauffer C, Pereira R, Bourtzis K (2017) Sterile insect technique and Wolbachia symbiosis as potential tools for the control of the invasive species Drosophila suzukii. J Pest Sci 91(2):489–503CrossRefGoogle Scholar
  37. Nomano FY, Kasuya N, Matsumura A, Suwito A, Mitsui H, Buffington ML, Kimura MT (2017) Genetic differentiation of Ganaspis brasiliensis (Hymenoptera: Figitidae) from East and Southeast Asia. Appl Entomol Zool 52:429–437CrossRefGoogle Scholar
  38. Pelton E, Gratton C, Isaacs R, van Timmeren S, Blanton A, Guédot C (2016) Earlier activity of Drosophila suzukii in high woodland landscapes but relative abundance is unaffected. J Pest Sci 89(3):725–733CrossRefGoogle Scholar
  39. Pfab F, Rossi Stacconi MV, Anfora G, Grassi A, Walton V, Pugliese A (2018) Optimized timing of parasitoid release: a mathematical model for biological control of Drosophila suzukii. Theor Ecol. Google Scholar
  40. Rice KB, Short BD, Leskey TC (2017) Development of an attract-and-kill strategy for Drosophila suzukii (Diptera: Drosophilidae): Evaluation of attracticidal spheres under laboratory and field conditions. J Econ Entomol 110(2):535–542CrossRefGoogle Scholar
  41. Rogers MA, Burkness EC, Hutchison WD (2016) Evaluation of high tunnels for management of Drosophila suzukii in fall-bearing red raspberries: potential for reducing insecticide use. J Pest Sci 89(3):815–821CrossRefGoogle Scholar
  42. Rossi Stacconi MV, Buffington M, Daane KM, Dalton DT, Grassi A, Kaçar G, Miller B, Miller JC, Baser N, Ioriatti C, Walton VM, Wiman NG, Wang XG, Anfora G (2015) Host stage preference, efficacy and fecundity of parasitoids attacking Drosophila suzukii in newly invaded areas. Biol Control 84:28–35CrossRefGoogle Scholar
  43. 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. J Pest Sci 89:689–700CrossRefGoogle Scholar
  44. Rossi-Stacconi MV, Panel A, Baser N, Ioriatti C, Pantezzi T, Anfora G (2017) Comparative life history traits of indigenous Italian parasitoids of Drosophila suzukii and their effectiveness at different temperatures. Biol Control 112:20–27CrossRefGoogle Scholar
  45. Rossi-Stacconi MV, Amiresmaeili N, Biondi A, Carli C, Caruso S, Dindo ML, Francati S, Gottardello A, Grassi A, Lupi D, Marchetti E, Mazzetto F, Mori N, Pantezzi T, Tavella L, Tropea Garzia G, Tonina L, Vaccari G, Anfora G, Ioriatti C (2018) Host location and dispersal ability of the cosmopolitan parasitoid Trichopria drosophilae released to control the invasive spotted wing Drosophila. Biol Control 117:188–196CrossRefGoogle Scholar
  46. 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 Prot 54:126–133CrossRefGoogle Scholar
  47. 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 61:387–397CrossRefGoogle Scholar
  48. Wiman N, Walton VM, Dalton DT, Anfora G, Burrack HJ, Chiu JC, Daane KM, Grassi A, Miller B, Tochen S, Wang XG, Ioriatti C (2014) Integrating temperature-dependent life table data into a matrix projection model for Drosophila suzukii population estimation. PLoS ONE 9(9):e106909CrossRefGoogle Scholar
  49. Wiman NG, Dalton DT, Anfora G, Biondi A, Chiu JC, Daane KM, Gerdeman B, Gottardello A, Hamby KA, Isaacs R, Grassi A, Ioriatti C, Lee JC, Miller B, Rossi Stacconi MV, Shearer PW, Tanigoshi L, Wang X, Walton VM (2016) Drosophila suzukii population response to environment and management strategies. J Pest Sci 89:653–665CrossRefGoogle Scholar
  50. Xu HY, Yang NW, Fan FH (2013) Competitive interactions between parasitoids provide new insight into host suppression. PLoS ONE 8(11):e82003CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2018

Authors and Affiliations

  • Marco Valerio Rossi Stacconi
    • 1
    • 2
    Email author
  • Alberto Grassi
    • 2
  • Claudio Ioriatti
    • 2
  • Gianfranco Anfora
    • 3
    • 4
  1. 1.Department of HorticultureOregon State UniversityCorvallisUSA
  2. 2.Technology Transfer CentreFondazione Edmund Mach (FEM)San Michele All’adigeItaly
  3. 3.Research and Innovation CentreFondazione Edmund Mach (FEM)San Michele All’adigeItaly
  4. 4.Center Agriculture Food Environment (C3A)University of TrentoSan Michele All’adigeItaly

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