Skip to main content
Log in

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

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

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.

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

Access this article

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

  • 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 88:469–494

    Article  Google Scholar 

  • 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):571–578

    Article  Google Scholar 

  • 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):e76548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 30:495–506

    Article  Google Scholar 

  • 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 89:749–759

    Article  Google Scholar 

  • 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 67:1375–1385

    Article  CAS  PubMed  Google Scholar 

  • 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 70:324–331

    Article  CAS  PubMed  Google Scholar 

  • 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):823–835

    Article  Google Scholar 

  • 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):2318–2327

    Article  CAS  PubMed  Google Scholar 

  • Diepenbrock LM, Burrack HJ (2016) Variation of within-crop microhabitat use by Drosophila suzukii (Diptera: Drosophilidae) in blackberry. J Appl Entomol 141:1–7

    Article  CAS  Google Scholar 

  • 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 27–43

    Chapter  Google Scholar 

  • 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):1083–1090

    Article  CAS  PubMed  Google Scholar 

  • Flinn PW, Hagstrum DW (1995) Simulation model of Cephalonomia waterstoni (Hymenoptera: Bethylidae) parasitizing the rusty grain beetle (Coleoptera: Cucujidae). Environ Entomol 24:1608–1615

    Article  Google Scholar 

  • Gabarra R, Riudavets J, Rodríguez GA, Pujade-Villar J, Arnó J (2015) Prospects for the biological control of Drosophila suzukii. BioControl 84:28–35

    Google Scholar 

  • 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 123:186–187

    Google Scholar 

  • 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 91:1241–1250

    Article  Google Scholar 

  • 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 109:197–204

    Google Scholar 

  • 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):166–174

    Article  PubMed  Google Scholar 

  • 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 89:643–651

    Article  Google Scholar 

  • Heimpel NJ, Mills GE (2017) Biological control: ecology and applications. Cambridge University Press, Cambridge, p 379

    Book  Google Scholar 

  • 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 107:1508–1518

    Article  PubMed  Google Scholar 

  • 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):e0183525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalajdzic P, Schetelig MF (2016) CRISPR/Cas-mediated gene editing using purified protein in Drosophila suzukii. Entomol Exp et Appl 164(3):350–362

    Article  CAS  Google Scholar 

  • Kaser JM, Heimpel GE (2015) Linking risk and efficacy in biological control host–parasitoid models. Biol Control 90:49–60

    Article  Google Scholar 

  • 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):735–748

    Article  Google Scholar 

  • 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):37–46

    Article  Google Scholar 

  • 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 7:40697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):e0180821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):2151–2158

    Article  CAS  PubMed  Google Scholar 

  • 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):219–226

    Article  Google Scholar 

  • 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):1348–1355

    Article  PubMed  Google Scholar 

  • 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 108:117–129

    Article  Google Scholar 

  • 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 89:837–850

    Article  Google Scholar 

  • Mazzi D, Bravin E, Meraner M, Finger R, Kuske S (2017) Economic impact of the introduction and establishment of Drosophila suzukii on sweet cherry production in Switzerland. Insects 8(1):18

    Article  PubMed Central  Google Scholar 

  • 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 68:255–263

    Google Scholar 

  • 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):489–503

    Article  Google Scholar 

  • 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 52:429–437

    Article  CAS  Google Scholar 

  • 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):725–733

    Article  Google Scholar 

  • 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. https://doi.org/10.1007/s12080-018-0382-3

    Article  Google Scholar 

  • 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):535–542

    Article  CAS  PubMed  Google Scholar 

  • 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):815–821

    Article  Google Scholar 

  • 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 84:28–35

    Article  Google Scholar 

  • 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 89:689–700

    Article  Google Scholar 

  • 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 112:20–27

    Article  Google Scholar 

  • 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 117:188–196

    Article  Google Scholar 

  • 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 54:126–133

    Article  CAS  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 61:387–397

    Article  CAS  Google Scholar 

  • 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):e106909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 89:653–665

    Article  Google Scholar 

  • Xu HY, Yang NW, Fan FH (2013) Competitive interactions between parasitoids provide new insight into host suppression. PLoS ONE 8(11):e82003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marco Valerio Rossi Stacconi.

Additional information

Handling Editor: Dirk Babendreier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rossi Stacconi, M.V., Grassi, A., Ioriatti, C. et al. Augmentative releases of Trichopria drosophilae for the suppression of early season Drosophila suzukii populations. BioControl 64, 9–19 (2019). https://doi.org/10.1007/s10526-018-09914-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-018-09914-0

Keywords

Navigation