Journal of Pest Science

, Volume 89, Issue 3, pp 689–700 | Cite as

Multiple lines of evidence for reproductive winter diapause in the invasive pest Drosophila suzukii: useful clues for control strategies

  • Marco Valerio Rossi-Stacconi
  • Rupinder Kaur
  • Valerio Mazzoni
  • Lino Ometto
  • Alberto Grassi
  • Angela Gottardello
  • Omar Rota-Stabelli
  • Gianfranco Anfora
Original Paper


Successful management of invasive pests, such as Drosophila suzukii, relies on a fine understanding of their biology. Genomic and physiological studies have suggested that the invasive success of D. suzukii is strongly associated with its ability to overwinter in a reproductive diapause state. Here, we coupled field surveys with comparative morphology and genetics to increase our understanding of D. suzukii overwintering behavior and provide useful indications for its management. The results of a 4-year-long field trapping in an Italian mountain region indicate that D. suzukii is continuously captured during winter months and that the number of captures is correlated with temperature. Capture patterns are also contrasting between sexes: while females are more abundantly caught during winter and summer, males are more abundant in spring and autumn. We found that overwintering could occur not only in natural environments, such as woods, but also in anthropic shelters. Comparative morphology and genetics further indicate that spermathecae may play an important adaptive role during winter. Our results unveil complex winter biology in D. suzukii and highlight how the number of overwintering females is an earlier predictor of summer population size. We hence propose that in a given year infestation may be better forecasted by taking into account the captures of the previous winter. We recommend that control methods be diapause-aware. For instance, they should take place in late winter/early spring and close to natural environments, and not only in fruit ripening season and close to orchards.


Spotted wing drosophila Diapause Overwintering Integrated pest management Cyp4d20 cytochrome 



This research was partially funded by the Autonomous Province of Trento (Italy) through Grandi Progetti, Project LExEM (Laboratory of Excellence for Epidemiology and Modeling, We are thankful to Karen Wells (Agricultural Research Service USDA, Parlier, California) for reviewing the English.


  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. Ayrinhac A, Debat V, Gibert P, Kister AG, Legout H, Moreteau B, Vergilino R, David JR (2004) Cold adaptation in geographical populations of Drosophila melanogaster: phenotypic plasticity is more important than genetic variability. Funct Ecol 18:700–706CrossRefGoogle Scholar
  3. 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. doi: 10.1007/s10340-016-0739-6 Google Scholar
  4. Cattel J, Kaur R, Gibert P, Martinez J, Fraimout A, Jiggins F et al (2016) Wolbachia in European populations of the invasive pest Drosophila suzukii: regional variation in infection frequencies. PLoS One 11(1):e0147766. doi: 10.1371/journal.pone.0147766 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cha D, Adams T, Rogg H, Landolt PJ (2012) Identification and field evaluation of fermentation volatiles from wine and vinegar that mediate attraction of spotted wing Drosophila, Drosophila suzukii. J Chem Ecol 38:1419–1431CrossRefPubMedGoogle Scholar
  6. Cha DH, Hesler SP, Cowles RS, Vogt H, Loeb GM, Landolt PJ (2013) Comparison of a synthetic chemical lure and standard fermented baits for trapping Drosophila suzukii (Diptera: Drosophilidae). Environ Entomol 42:1052–1060CrossRefPubMedGoogle Scholar
  7. Cha DH, Adams T, Werle CT, Sampson BJ, Adamczyk JJ Jr, Rogg H, Landolt PJ (2014) A four-component synthetic attractant for Drosophila suzukii (Diptera: Drosophilidae) isolated from fermented bait headspace. Pest Manag Sci 70:324–331CrossRefPubMedGoogle Scholar
  8. Chapman RF (1998) The insects; structure and function, 4th edn. Cambridge University Press, Cambridge, p 403. ISBN 0-521-57048-4Google Scholar
  9. Cini A, Ioriatti C, Anfora G (2012) A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull Insectol 65(1):149–160Google Scholar
  10. Cini A, Anfora G, Escudero-Colomar LA, Grassi A, Santosuosso U, Seljak G, Papini A (2014) Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe. J Pest Sci 87:559–566CrossRefGoogle Scholar
  11. 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(11):1368–1374CrossRefPubMedGoogle Scholar
  12. De Ros G, Conci S, Pantezzi T, Savini G (2015) The economic impact of invasive pest Drosophila suzukii on berry production in the Province of Trento, Italy. J Berry Res 5(2):89–96CrossRefGoogle Scholar
  13. Dekker T, Mansourian S, Revadi S, Lebreton S, Becher P, Angeli S, Rota-Stabelli O, Anfora G (2015) From pheromone to antagonist: cis-vaccenyl acetate loss in Drosophila suzukii reverses its role in sexual communication. Proc R Soc B 282:20143018CrossRefPubMedPubMedCentralGoogle Scholar
  14. Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122CrossRefPubMedGoogle Scholar
  15. Denlinger DL (2008) Why study diapause? Entomol Res 38:1–9CrossRefGoogle Scholar
  16. Deprà 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 87:379–383CrossRefGoogle Scholar
  17. Gibert JM, Peronnet F, Schlotterer C (2007) Phenotypic plasticity in Drosophila pigmentation caused by temperature sensitivity of a chromatin regulator network. PLoS Genet 3:266–280CrossRefGoogle Scholar
  18. 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 Bull 109:197–204Google Scholar
  19. Hamby KA, Kwok RS, Zalom FG, Chiu JC (2013) Integrating circadian activity and gene expression profiles to predict chronotoxicity of Drosophila suzukii response to insecticides. PLoS One 8(7):e68472CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hamby KA, Bolda MP, Sheehan ME, Zalom FG (2014) Seasonal monitoring for Drosophila suzukii (Diptera: Drosophilidae) in California commercial raspberries. Environ Entomol 43(4):1008–1018CrossRefPubMedGoogle Scholar
  21. Harris DW, Hamby KA, Wilson HE, Zalom FG (2014) Seasonal monitoring od Drosophila suzukii (Diptera: Drosophilidae) in a mixed fruit production system. J Asia Pac Entomol 17:857–864CrossRefGoogle Scholar
  22. Hodek I, Iperti G (1983) Sensitivity to photoperiod in relation to diapause in Semiadalia undecimnotata females. Entomol Exp Appl 34(1):9–12CrossRefGoogle Scholar
  23. Jakobs R, Gariepy TD, Sinclair BJ (2015) Adult plasticity of cold tolerance in a continental-temperate population of Drosophila suzukii. J Insect Physiol 79:1–9CrossRefPubMedGoogle Scholar
  24. Kanzawa T (1939) Studies on Drosophila suzukii Mats. Yamanashi Agricultural Experimental Station, Kofu, pp 1–49Google Scholar
  25. Kimura MT (1988) Adaptation to temperate climates and evolution of over-wintering strategies in the Drosophila melanogaster species group. Evolution 42:1288–1297CrossRefGoogle Scholar
  26. Kimura MT (2004) Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions. Oecologia 140:442–449CrossRefPubMedGoogle Scholar
  27. Kleiber JR, Unelius CR, Lee JC, Suckling DM, Qian MC, Bruck DJ (2014) Attractiveness of fermentation and related products to spotted wing drosophila (Diptera: Drosophilidae). Environ Entomol 43(2):439–447CrossRefPubMedGoogle Scholar
  28. Knipling EF (1959) Sterile-male method of population control. Science 130:902–904CrossRefPubMedGoogle Scholar
  29. Kvam E, Dahle J (2003) Pigmented melanocytes are protected against ultraviolet-A-induced membrane damage. J Investig Dermatol 121:564–569CrossRefPubMedGoogle Scholar
  30. Landolt PJ, Adams T, Rogg H (2012) Trapping spotted wing drosophila, Drosophila suzukii (Matsumura), with combinations of vinegar and wine, and acetic acid and ethanol. J Appl Entomol 136:148–154CrossRefGoogle Scholar
  31. Laven H (1967) Eradication of Culex pipiens fatigans through cytoplasmic incompatibility. Nature 216:383–384CrossRefPubMedGoogle Scholar
  32. Li J, Zhao M, He P, Hidalgo M, Baker SD (2007) Differential metabolism of gefitinib and erlotinib by human cytochrome P450 enzymes. Clin Cancer Res 13:3731–3737CrossRefPubMedGoogle Scholar
  33. Malta J, Martins GF, Marques AE, Games PD, Zanuncio JC, Baracat-Pereira MC, Fernandes Salomão TM et al (2014) Insights into the proteome of the Spermatheca of the leaf-cutting ant Atta sexdens rubropilosa (Hymenoptera: Formicidae). Fla Entomol 97(4):1856–1861CrossRefGoogle Scholar
  34. Mitsui H, Beppu K, Kimura MT (2010) Seasonal life cycles and resource uses of flower and fruit-feeding drosophilid flies (Diptera: Drosophilidae) in central Japan. Entomol Sci 13:60–67CrossRefGoogle Scholar
  35. Neubaum DM, Wolfner MF (1999) Wise, winsome or weird: mechanisms of sperm storage in female animals. Curr Top Dev Biol 41:67–97CrossRefPubMedGoogle Scholar
  36. Nyamukondiwa C, Terblanche JS, Marshall KE, Sinclair BJ (2011) Basal cold but not heat tolerance constrains plasticity among Drosophila species (Diptera: Drosophilidae). J Evol Biol 24:1927–1938CrossRefPubMedGoogle Scholar
  37. Ometto L, Cestaro A, Ramasamy S, Grassi A, Revadi S, Siozios S, Moretto M, Fontana P, Varotto C, Pisani D, Dekker T, Wrobel N, Viola R, Pertot I, Cavalieri D, Blaxter M, Anfora G, Rota-Stabelli O (2013) Linking genomics and ecology to investigate the complex evolution of an invasive Drosophila pest. Genome Biol Evol 5(4):745–757CrossRefPubMedPubMedCentralGoogle 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. doi: 10.1007/s10340-016-0733-z Google Scholar
  39. Pettitt AN (1979) A non-parametric approach to the change-point problem. Appl Stat 28:126–135CrossRefGoogle Scholar
  40. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45CrossRefPubMedPubMedCentralGoogle Scholar
  41. Pitnick S, Markow T, Spicer GS (1999) Evolution of multiple kinds of female sperm-storage organs in Drosophila. Evolution 53(6):1804–1822CrossRefGoogle Scholar
  42. Revadi S, Lebreton S, Witzgall P, Anfora G, Dekker T, Becher P (2015) Sexual behavior of Drosophila suzukii. Insects 6(1):183–196CrossRefPubMedPubMedCentralGoogle Scholar
  43. Rota-Stabelli O, Blaxter M, Anfora G (2013) Quick guide: Drosophila suzukii. Curr Biol 23:R1–R3CrossRefGoogle Scholar
  44. Salminen TS, Hoikkala A (2013) Effect of temperature on the duration of sensitive period and on the number of photoperiodic cycles required for the induction of reproductive diapause in Drosophila montana. J Insect Physiol 59(4):450–457CrossRefPubMedGoogle Scholar
  45. Sasaki M, Sato R (1995) Bionomics of the cherry drosophila, Drosophila suzukii Matsumura (Diptera: Drosophilidae) in Futeushima Prefecture (Japan). Annu Rep Soc Plant Prot North Jpn 46:164–172Google Scholar
  46. Scott JG, Wen Z (2001) Cytochromes P450 of insects: the tip of the iceberg. Pest Manag Sci 57:958–967CrossRefPubMedGoogle Scholar
  47. Shaw WR, Teodori E, Mitchell SN, Baldini F, Gabrieli P, Rogers DW, Catteruccia F (2014) Mating activates the heme peroxidase HPX15 in the sperm storage organ to ensure fertility in Anopheles gambiae. Proc Natl Acad Sci USA 111(16):5854–5859CrossRefPubMedPubMedCentralGoogle Scholar
  48. Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences, 2nd edn. McGraw-Hill, Singapore, p 399Google Scholar
  49. Stephens AR, Asplen MK, Hutchison WD, Venette RC (2015) Cold hardiness of winter-acclimated Drosophila suzukii (Diptera: Drosophilidae) adults. Environ Entomol. doi: 10.1093/ee/nvv134 PubMedGoogle Scholar
  50. Sugumaran M (2002) Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Res 15:2–9CrossRefPubMedGoogle Scholar
  51. Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, New YorkGoogle Scholar
  52. True JR (2003) Insect melanism: the molecules matter. Trends Ecol Evol 18(12):640–647CrossRefGoogle Scholar
  53. Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee JC (2010) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag 2:G1–G7CrossRefGoogle Scholar
  54. Wilson TG (2001) Resistance of Drosophila to toxins. Annu Rev Entomol 46:545–571CrossRefPubMedGoogle Scholar
  55. Wiman NG, Walton VM, Dalton DT, Anfora G, Burrack HJ, Chiu JC, Daane KM, Grassi A, Miller B, Tochen S, Wang X, Ioriatti C (2014) Integrating temperature-dependent life table data into a matrix projection model for Drosophila suzukii population estimation. PLoS One 9(9):e106909CrossRefPubMedPubMedCentralGoogle Scholar
  56. Wu SR, Tai HK, Li ZY, Wang X, Yang SS, Sun W, Xiao C (2007) Field evaluation of different trapping methods of cherry fruit fly, Drosophila suzukii. J Yunnan Agric Univ 22(5):776–778Google Scholar
  57. Zabalou S, Riegler M, Theodorakopoulou M, Stauffer C, Savakis C, Bourtzis K (2004) Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc Natl Acad Sci USA 101:15042–15045CrossRefPubMedPubMedCentralGoogle Scholar
  58. Zachariassen KE (1985) Physiological reviews: physiology of cold tolerance in insects. Physiol Rev 65:799–832PubMedGoogle Scholar
  59. Zerulla FN, Schmidt S, Streitberger M, Zebitz CPW, Zelger R (2015) On the overwintering ability of Drosophila suzukii in South Tyrol. J Berry Res 5:41–48Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Marco Valerio Rossi-Stacconi
    • 1
  • Rupinder Kaur
    • 1
  • Valerio Mazzoni
    • 1
  • Lino Ometto
    • 1
  • Alberto Grassi
    • 2
  • Angela Gottardello
    • 2
  • Omar Rota-Stabelli
    • 1
  • Gianfranco Anfora
    • 1
  1. 1.Research and Innovation CentreFondazione Edmund Mach (FEM)San Michele all’AdigeItaly
  2. 2.Technological Transfer CentreFondazione Edmund Mach (FEM)San Michele all’AdigeItaly

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