Skip to main content

Advertisement

Springer Nature Link
Log in

Advances in the Chemical Ecology of the Spotted Wing Drosophila (Drosophila suzukii) and its Applications

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Significant progress has been made in understanding the cues involved in the host and mate seeking behaviors of spotted wing drosophila, Drosophila suzukii (Matsumura). This insect pest has been discovered in many fruit growing regions around the world since 2008. Unlike closely related Drosophila species, D. suzukii attacks fresh fruit and has become a severe pest of soft fruits including strawberry, cherry, blackberry, blueberry, raspberry, and may pose a threat to grapes. Prior to 2008, little was known about the courtship and host-seeking behaviors or chemical ecology of this pest. Since then, researchers have gained a better understanding of D. suzukii attraction to specific odors from fermentation, yeast, fruit, and leaf sources, and the visual cues that elicit long-range attraction. Several compounds have also been identified that elicit aversive behaviors in adult D. suzukii flies. Progress has been made in identifying the constituent compounds from these odor sources that elicit D. suzukii antennal responses in electrophysiological assays. Commercial lures based on food volatiles have been developed to attract D. suzukii using these components and efforts have been made to improve trap designs for monitoring this pest under field conditions. However, current food-based lures and trap technologies are not expected to be specific to D. suzukii and thus capture large numbers of non-target drosophilids. Attractive and aversive compounds are being evaluated for monitoring, mass trapping, and for the development of attract-and-kill and push-pull techniques to manage D. suzukii populations. This review outlines presently available research on the chemical ecology of D. suzukii and discusses areas for future research.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Abraham J, Zhang A, Angeli S, Abubeker S, Michel C, Feng Y, Rodriguez-Saona C (2015) Behavioral and antennal responses of Drosophila suzukii (Diptera: Drosophilidae) to volatiles from fruit extracts. Environ Entomol 44:356–367

    Article  PubMed  Google Scholar 

  • Abdel-Sattar E, Zaitoun A, Farag M, Gayed S, Harraz F (2010) Chemical composition, insecticidal and insect repellent activity of Schinus molle L. leaf and fruit essential oils against Trogoderma granarium and Tribolium castaneum. Nat Prod Res 24:226–235

    Article  PubMed  CAS  Google Scholar 

  • Adams C, Schenker J, McGhee P, Gut L, Brunner J, Miller J (2017) Maximizing information yield from pheromone-baited monitoring traps: estimating plume reach, trapping radius, and absolute density of Cydia pomonella (Lepidoptera: Tortricidae) in Michigan apple. J Econ Entomol 110:305–318

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Akasaka N, Higashikubo H, Ishii Y, Sakoda H, Fujiwara S (2017) Polyamines in brown rice vinegar function as potent attractants for the spotted wing drosophila. J Biosci Bioeng 123:78–83

    Article  PubMed  CAS  Google Scholar 

  • Alnajjar G, Judith C, Drummond F (2017) Behavioral and preventative management of Drosophila suzukii Matsumura (Diptera: Drosophilidae) in Maine wild blueberry (Vaccinium angustifolium Aiton) through attract and kill trapping and insect exclusion-netting. Int J Entomol Nematol 3:051–006

    Google Scholar 

  • Antony C, Davis T, Carlson D, Pechin J, Jallon J (1985) Compared behavioral responses of male Drosophila melanogaster (Canton-S) to natural and synthetic aphrodisiacs. J Chem Ecol 11:1617–1629

    Article  PubMed  CAS  Google Scholar 

  • Asplen M, Anfora G, Biondi A, Choi D, Chu D, Daane K, Gibert P, Gutierrez A, Hoelmer K, Hutchison W, Isaacs R, Jiang Z, Kárpáti Z, Kimura M, Pascual M, Philips C, Plantamp C, Ponti L, Vétek G, Vogt H (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 B 281:20132840

    Article  PubMed  Google Scholar 

  • Ballman E, Drummond F (2017) Infestation of wild fruit by Drosophila suzukii surrounding Maine wild blueberry fields. J Agric Urban Entomol 33:61–70

    Article  Google Scholar 

  • Basoalto E, Hilton R, Knight A (2013) Factors affecting the efficacy of a vinegar trap for Drosophila suzikii (Diptera: Drosophilidae). J of Appl Entomol 137:561–570

    Article  Google Scholar 

  • Becher P, Jensen R, Natsopoulou M, Verschut V, De Fine LH (2017) Infection of Drosophila suzukii with the obligate insect-pathogenic fungus Entomophthora muscae. J Pest Sci 91:781–787

    Article  Google Scholar 

  • Bellamy D, Sisterson M, Walse S (2013) Quantifying host potentials: indexing postharvest fresh fruits for spotted wing drosophila, Drosophila suzukii. PLoS One 8:e61227

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bellutti N, Gallmetzer A, Innerebner G, Schmidt S, Zelger R, Koschier EH (2017) Dietary yeast affects preference and performance in Drosophila suzukii. J of Pest Sci 91:651–660

    Article  Google Scholar 

  • Benito N, Lopes-da-Silva M, Sivori Silva dos Santos R (2016) Potential spread and economic impact of invasive Drosophila suzukii in Brazil. Pesq Agropec Bras 51:571–578

    Article  Google Scholar 

  • Beers H, Van Steenwyk R, Shearer P, Coates W, Grant J (2011) Developing Drosophila suzukii management programs for sweet cherry in the western United States. Pest Manag Sci 67:1386–1395

    Article  PubMed  CAS  Google Scholar 

  • Bolda MP, Goodue RE, Zalom FG (2010) Spotted wing drosophila: potential economic impact of a newly established pest. Agric Resour Econ Update, University of California Giannini Foundation of Agricultural Economics 13:5–8

    Google Scholar 

  • Bruce T, Wadhams L, Woodcock C (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274

    Article  PubMed  CAS  Google Scholar 

  • Burger H, Dötterl S, Ayasse M (2010) Host-plant finding and recognition by visual and olfactory floral cues in an oligolectic bee. Funct Ecol 24:1234–1240

    Article  Google Scholar 

  • Burrack H, Fernandez G, Spivey T, Kraus D (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  PubMed  CAS  Google Scholar 

  • Burrack H, Asplen M, Bahder L, Collins J, Drummond F, Guédot C, Isaacs R, Johnson D, Blanton A, Lee J, Loeb G, Rodriguez-Saona C, Timmeren S, Walsh D, McPhie D (2015) Multistate comparison of attractants for monitoring Drosophila suzukii (Diptera: Drosophilidae) in blueberries and caneberries. Environ Entomol 44:704–712

    Article  PubMed  Google Scholar 

  • Campbell A, Borden J (2006) Integration of visual and olfactory cues of hosts and non-hosts by three bark beetles (Coleoptera: Scolytidae). Ecol Entomol 31:437–449

    Article  Google Scholar 

  • Cha DH, Adams TB, 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 38:1419–1431

    Article  PubMed  CAS  Google Scholar 

  • Cha DH, Hesler S, Cowles R, 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 42:1052–1060

    Article  PubMed  Google Scholar 

  • Cha DH, Adams TB, Werle C, Sampson B, Adamczyk J, 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  PubMed  CAS  Google Scholar 

  • Cha DH, Hesler SP, Park S, Adams TB, Zack RS, Rogg H, Loeb GM, Landolt PJ. (2015) Simpler is better: fewer non-target insects trapped with a four-component chemical lure vs. a chemically more complex food-type bait for . Entomol Exp App 154251-260

  • Cha DH, Landolt PJ, Adams TB (2017) Effect of chemical ratios of a microbial-based attractant on trap catch of Drosophila suzukii (Diptera: Drosophilidae). Environ Entomol 46:907–915

    Article  PubMed  Google Scholar 

  • Cha DH, Loeb G, Linn C, Hesler S, Landolt PJ (2018b) A multiple-choice bioassay approach for rapid screening of key attractant volatiles. Environ Entomol

  • Cha DH, Hesler S, Wallingford A, Zaman F, Jentsch P, Nyrop J, Loeb G (2018a) Comparison of commercial lures and food baits for early detection of fruit infestation risk by Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 111:645–652

    Article  PubMed  Google Scholar 

  • Choi M, Tang S, Ahn S, Amarasekare K, Shearer P, Lee J (2017) Effect of non-nutritive sugars to decrease the survivorship of spotted wing drosophila, Drosophila suzukii. J Insect Physiol 99:86–94

    Article  PubMed  CAS  Google Scholar 

  • Cook S, Khan Z, Picket J (2007) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375–400

    Article  PubMed  CAS  Google Scholar 

  • Couto A, Alenius M, Kickson B (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535–1547

    Article  PubMed  CAS  Google Scholar 

  • Cowles R, Rodriguez-Saona C, Holdcraft R, Loeb G, Elsensohn J, Hesler S (2015) Sucrose improves insecticide activity against Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 108:640–653

    Article  PubMed  Google Scholar 

  • Daane K, Wang X, Biondi A, Miller B, Miller J, Riedl H, Shearer P, Guerrieri E, Giorgini M, Buffington M, van Achterberg K, Song Y, Kang T, Yi H, Jung C, Lee D, Chung B, Hoelmer K, Walton V (2016) First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. J Pest Sci 89:823–835

    Article  Google Scholar 

  • Dalton D, Walton V, Shearer P, Walsh D, 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  PubMed  CAS  Google Scholar 

  • Das S, Trona F, Khallaf M, Schuh E, Knaden M, Hansson B, Sachse S (2017) Electrical synapses mediate synergism between pheromone and food odors in Drosophila melanogaster. Proc Natl Acad Sci 114:E9962–E9971

    Article  PubMed  CAS  Google Scholar 

  • Dekker T, Revadi S, Mansourian S, Ramasamy S, Lebreton S, Becher P, Angeli S, Rota-Stabelli O, Anfora G (2015) Loss of Drosophila pheromone reverses its role in sexual communication in Drosophila suzukii. Proc R Soc B 282:20143018

    Article  PubMed  CAS  Google Scholar 

  • Diepenbrock L, Swoboda-Bhattarai K, Burrack H (2016) Oviposition preference, fidelity, and fitness of Drosophila suzukii in a co-occurring crop and non-crop host system. J Pest Sci 89:761–769

    Article  Google Scholar 

  • Ebrahim S, Dweck H, Stokl J, Hofferberth J, Trona F, Weniger K, Rybak J, Seki Y, Stensmyr M, Sachse S, Hansson B, Knaden M (2015) Drosophila avoids parasitoids by sensing their semiochemicals via a dedicated olfactory circuit. PLoS Biol 13:e1002318

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ehlenfeldt MK, Martin RB Jr (2002) A survey of fruit firmness in Highbush blueberry and species-introgressed blueberry cultivars. HortScience 37(2):386–389

    Google Scholar 

  • Ejima A, Smith B, Lucas C, van der Goes van Naters W, Miller C, Carlson J, Levine J, Griffith L (2007) Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr Biol 17:599–605

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • El-Sayed A, Suckling D, Byers J, Jang E, Wearing C (2009) Potential of “lure and kill” in long-term pest management and eradication of invasive species. J Econ Entomol 102:815–835

    Article  PubMed  CAS  Google Scholar 

  • Elsensohn J, Loeb G (2018) Non-crop host sampling yields insights into small-scale population dynamics of Drosophila suzukii (Matsumura). Insects 9:5

    Article  PubMed Central  Google Scholar 

  • Evans R, Toews M, Sial A (2017) Diel periodicity of Drosophila suzukii (Diptera: Drosophilidae) under field conditions. PLoS One 12:e0171718

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Everaerts C, Farine J, Cobb M, Ferveur J (2010) Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PLoS One 5:e9607

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Faccoli M, Stergulc F (2008) Damage reduction and performance of mass trapping devices for forest protection against the spruce bark beetle, Ips typographus (Coleoptera Curculionidae Scolytinae). Annals Forest Sci 65:1–9

    Article  Google Scholar 

  • Farnsworth D, Hamby K, Bolda M, Goodhue R, Williams J, Zalom F (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 73:1083–1090

    Article  PubMed  CAS  Google Scholar 

  • Frewin A, Renkema J, Fraser H, Hallett R (2017) Evaluation of attractants for monitoring Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 110:1156–1163

    Article  PubMed  Google Scholar 

  • Gao H, Xu N, Chen H, Liu Q, Pu Q, Qin D, Zhai Y, Yu Y (2017) Impact of selected fungi from an artificial diet on the growth and development of Drosophila suzukii (Diptera: Drosophilidae). J Asia-Pacific Entomol 20:141–149

    Article  Google Scholar 

  • Gregg P, Del Socorro A, Landolt P (2018) Advances in attract-and-kill for agricultural pests: beyond pheromones. Annu Rev Entomol 63:453–470

    Article  PubMed  CAS  Google Scholar 

  • Goodhue R, Bolda M, Farnsworth D, Williams J, Zalom F (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  PubMed  CAS  Google Scholar 

  • Grabe V, Baschwitz A, Dweck H, Lavista-Llanos S, Hansson B, Sachse S (2016) Elucidating the neuronal architecture of olfactory glomeruli in the drosophila antennal lobe. Cell Rep 16:3401–3413

    Article  PubMed  CAS  Google Scholar 

  • Goold H, Kroukamp H, Williams T, Paulsen I, Varela C, Pretorius I (2017) Yeast’s balancing act between ethanol and glycerol production in low-alcohol wines. Microb Biotechnol 10:264–278

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guo A, Li L, Shou-Zhen X, Chun-hua F, Wolf R, Heisenberg M (1996) Conditioned visual flight orientation in Drosophila: dependence on age, practice, and diet. Learning Memory 3:49–59

    Article  PubMed  CAS  Google Scholar 

  • Hallem E, Carlson J (2006) Coding of odors by a receptor repertoire. Cell 125:143–160

    Article  PubMed  CAS  Google Scholar 

  • Hamby K, Hernández A, Boundy-Mills K, Zalom F (2012) Associations of yeasts with spotted-wing drosophila, Drosophila suzukii (Diptera: Drosophilidae) in cherries and raspberries. Appl Environ Microbiol 78:4869–4873

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hamby K, Becher P (2016) Current knowledge of interactions between Drosophila suzukii and microbes, and their potential utility for pest management. J Pest Sci 89:621–630

    Article  Google Scholar 

  • Harris D, Hamby K, Wilson H, Zalom F (2014) Seasonal monitoring of Drosophila suzukii (Diptera: Drosophilidae) in a mixed fruit production system. J Asia-Pacific Entomol 17:857–864

    Article  Google Scholar 

  • Hampton E, Koski C, Barsoian O, Faubert H, Cowles R, Alm S (2014) Use of early ripening cultivars to avoid infestation and mass trapping to manage Drosophila suzukii (Diptera: Drosophilidae) in Vaccinium corymbosum (Ericales: Ericaceae). J Econ Entomol 107:1849–1857

    Article  PubMed  Google Scholar 

  • Hickner P, Rivaldi C, Johnson C, Siddappaji M, Raster G, Syed Z (2016) The making of a pest: insights from the evolution of chemosensory receptor families in a pestiferous and invasive fly, Drosophila suzukii. BMC Genomics 17:648

    Article  PubMed  PubMed Central  Google Scholar 

  • Iglesias L, Nyoike T, Liburd O (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 

  • Karageorgi M, Bräcker L, Lebreton S, Minervino C, Cavey M, Siju K, Kadow I, Gompel N, Prud’homme B (2017) Evolution of multiple sensory systems drives novel egg-laying behavior in the fruit pest Drosophila suzukii. Curr Biol 27:847–853

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Keesey IW, Knaden M, Hansson BS (2015) Olfactory specialization in Drosophila suzukii supports an ecological shift in host preference from rotten to fresh fruit. J Chem Ecol 41:121–128

    Article  PubMed  PubMed Central  CAS  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 

  • Kirkpatrick DM, Leach HL, Xu P, Dong K, Isaacs R, Gut LJ (2018b) Comparative antennal and behavioral responses of summer and winter morph Dorophila suzukii (Diptera: Drosophildae) to ecologically relevant volatiles. Environ Entomol 47:700–706

  • Kirkpatrick DM, McGhee PS, Hermann SL, Gut LJ, Miller JR (2016) Alightment of spotted wing drosophila (Diptera: Drosophilidae) on odorless disks varying in color. Environ Entomol 45:185–191

    Article  PubMed  CAS  Google Scholar 

  • Kirkpatrick DM, McGhee PS, Gut LJ, Miller JR (2017) Improving monitoring tools for spotted wing drosophila, Drosophila suzukii. Entomol Exp Appl 164:87–93

    Article  CAS  Google Scholar 

  • Kirkpatrick DM, Gut LJ, Miller JR (2018a) Estimating monitoring trap plume reach and trapping area for Drosophila suzukii (Diptera: Drosophilidae) in Michigan tart cherry. J Econ Entomol 111:1285–1298

  • Kleiber J, Unelius C, Suckling D, Qian M, Bruck D (2014) Attractiveness of fermentation and related products to spotted wing drosophila (Diptera: Drosophilidae). Environ Entomol 43:439–447

    Article  PubMed  CAS  Google Scholar 

  • Klick J, Yang W, Walton V, Dalton D, Hagler J, Dreves A, Lee J, Bruck D (2016) Distribution and activity of Drosophila suzukii in cultivated raspberry and surrounding vegetation. J Appl Entomol 140:37–46

    Article  Google Scholar 

  • Knight A, Witzgall P (2013) Combining mutualistic yeast and pathogenic virus – a novel method for codling moth control. J Chem Ecol 39:1019–1026

    Article  PubMed  CAS  Google Scholar 

  • Krause Pham C, Ray A (2015) Conservation of olfactory avoidance in drosophila species and identification of repellents for Drosophila suzukii. Sci Rep 5:11527

    Article  PubMed  PubMed Central  Google Scholar 

  • Kurtovic A, Widmer A, Dickson B (2007) A single class of olfactory neurons mediates behavioral responses to a Drosophila sex pheromone. Nature 446:542–546

    Article  PubMed  CAS  Google Scholar 

  • Landolt P, Adams T, Rogg H (2012a) Trapping spotted wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), with combinations of vinegar and wine, and acetic acid and ethanol. J Appl Entomol 136:148–154

    Article  CAS  Google Scholar 

  • Landolt P, Adams T, Davis T, Rogg H (2012b) Spotted wing drosophila, Drosophila suzukii (Diptera: Drosophilidae), trapped with combinations of wines and vinegars. Florida Entomol 95:326–332

    Article  Google Scholar 

  • Lasa R, Tadeo E, Dinorín L, Lima I, Williams T (2017) Fruit firmness, superficial damage, and location modulate infestation by Drosophila suzukii and Zaprionus indianus: the case of guava in Veracruz, Mexico. Entomol Exp App 162:4–12

    Article  CAS  Google Scholar 

  • Le Bars D, Yvon M (2008) Formation of diacetyl and acetoin by Lactococcus lactis via aspartate catabolism. J Appl Microbiol 104:171–177

    PubMed  Google Scholar 

  • Lee J, Bruck D, Curry H, Edwards D, Haviland D, Van Steenwykd R, Yorgey B (2011a) The susceptibility of small fruits and cherries to the spotted-wing drosophila, Drosophila suzukii. Pest Manag Sci 67:1358–1367

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Bruck D, Dreves A, Ioriatti C, Vogt H, Baufeld P (2011b) In focus: spotted wing drosophila, Drosophila suzukii, across perspectives. Pest Manag Sci 67:1349–1351

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Burrack H, Barrantes L, Beers E, Dreves A, Hamby K, Haviland D, Isaacs R, Richardson T, Shearer P (2012) Evaluation of monitoring traps for Drosophila suzukii (Diptera: Drosophilidae) in North America. J Econ Entomol 105:1350–1357

    Article  PubMed  Google Scholar 

  • Lee J, Shearer P, Barrantes L, Beers E, Burrack H, Dalton D, Dreves A, Gut L, Hamby K, Haviland D, Isaacs R, Nielsen A, Richardson T, Rodriguez-Saona C, Stanley C, Walsh D, Walton V, Yee W, Zalom F, Bruck D (2013) Trap designs for monitoring Drosophila suzukii (Diptera: Drosophilidae). Environ Entomol 42:1348–1355

    Article  PubMed  Google Scholar 

  • Lee J, Dreves A, Cave A, Kawai S, Isaacs R, Miller J, Van Timmeren S, Bruck D (2015) Infestation of wild and ornamental non-crop fruits by Drosophila suzukii (Diptera: Drosophilidae). Ann Entomol Soc Am 108:117–129

    Article  Google Scholar 

  • Lee J, Dalton D, Swoboda-Bhattarai K, Bruck D, Burrack H, Strik B, Woltz J, Walton V (2016) Characterization and manipulation of fruit susceptibility to Drosophila suzukii. J Pest Sci 89:771–780

    Article  Google Scholar 

  • Little C, Chaptman T, Moreau D, Hillier N (2017) Susceptibility of selected boreal fruits and berries to the invasive pest Drosophila suzukii (Diptera: Drosophilidae). Pest Manag Sci 73:160–166

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Maia M, Moore S (2011) Plant-based insect repellents: a review of their efficacy, development and testing. Malar J 10:S11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mas A, Torija M, Garcia-Parrilla M, Troncoso A (2014) acetic acid bacteria and the production and quality of wine vinegar. The Scientific World Journal: 2014

  • Mazzetto F, Gonella E, Crotti E, Vacchini V, Syrpas M, Pontini M, Mangelinckx S, Daffonchio D, Alma A (2016) Olfactory attraction of Drosophila suzukii by symbiotic acetic acid bacteria. J Pest Sci 89:783–792

    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 8:18

    Article  PubMed Central  Google Scholar 

  • Mori B, Whitener A, Leinweber Y, Revadi S, Beers E, Witzgall P, Becher P (2017) Enhanced yeast feeding following mating facilitates control of the invasive fruit pest Drosophila suzukii. J Appl Ecol 54:170–177

    Article  Google Scholar 

  • Münch D and Galizia G (2015) DoOR 2.0 – comprehensive mapping of Drosophila melanogaster odorant responses. Sci reports 6: 21841

  • Murphy K, Tabuloc C, Cervantes K, Chiu J (2016) Ingestion of genetically modified yeast symbiont reduces fitness of an insect pest via RNA interference. Sci Rep 6

  • Parker J, Crowder D, Eigenbrode S, Snyder W (2016) Trap crop diversity enhances crop yield. Agric Ecosys Environ 232:254–262

    Article  Google Scholar 

  • Ramasamy S, Ometto L, Crava C, Revadi S, Kaur R, Horner D, Pisani D, Dekker T, Anfora G, Rota-Stabelli O (2016) The evolution of olfactory gene families in Drosophila and the genomic basis of chemical-ecological adaptation in Drosophila suzukii. Genome Biol Evol 8:2297–2311

    Article  PubMed  PubMed Central  Google Scholar 

  • Renkema J, Wright D, Buitenhuis R, Hallett R (2016) Plant essential oils and potassium metabisulfite as repellents for Drosophila suzukii (Diptera: Drosophilidae). Sci Rep 6:21432

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Renkema J, Buitenhuis R, Hallett R (2017) Reduced Drosophila suzukii infestation in berries using deterrent compounds and laminate polymer flakes. Insects 8:117

    Article  PubMed Central  Google Scholar 

  • Revadi S, Vitagliano S, Rossi-Stacconi M, Ramasamy S, Mansourian S, Carlin S, Vrhovsek U, Becher P, Mazzoni V, Rota-Stabelli O (2015) Olfactory responses of Drosophila suzukii females to host plant volatiles. Physiological Entomol 40:54–64

    Article  CAS  Google Scholar 

  • Rice K, Short B, Jones S, Leskey T (2016) Behavioral responses of Drosophila suzukii (Diptera: Drosophilidae) to visual stimuli under laboratory, semifield, and field conditions. Environ Entomol 45:1480–1488

    Article  PubMed  Google Scholar 

  • Rice K, Short B, Leskey T (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 110:535–542

    Article  PubMed  Google Scholar 

  • Romano P, Suzzi G (1996) Origin and production of acetoin during wine yeast fermentation. App Environ Microbiol 62:309

    CAS  Google Scholar 

  • Rombaut A, Guilhot R, Xuéreb A, Benoit L, Chapuis M, Pierre-Gibert P, Fellous S (2017) Invasive Drosophila suzukii facilitates Drosophila melanogaster infestation and sour rot outbreaks in vineyards. Royal Soc Open Sci 4:170117

    Article  CAS  Google Scholar 

  • Sampson B, Werle C, Stringer S, Adamczyk J (2017) Ingestible insecticides for spotted wing drosophila control: a polyol, Erythritol, and an insect growth regulator, Lufenuron. J Appl Entomol 141:8–18

    Article  CAS  Google Scholar 

  • Scheidler N, Liu C, Hamby K, Zalom F, Syed Z (2015) Volatile codes: correlation of olfactory signals and reception in Drosophila-yeast chemical communication. Sci Rep 5

  • Scott D (1986) Sexual mimicry regulates the attractiveness of mated Drosophila melanogaster females. Proc Natl Acad Sci 83:8429–8433

    Article  PubMed  CAS  Google Scholar 

  • Seow Y, Ong P, Liu S (2010) Production of flavor-active methionol from methionine metabolism by yeasts in coconut cream. International J Food Microbiol 143:235–240

    Article  CAS  Google Scholar 

  • Simmons F, Bradley T (1997) An analysis of resource allocation in response to dietary yeast in Drosophila melanogaster. J Insect Physiol 43:779–788

    Article  PubMed  CAS  Google Scholar 

  • Shawer R, Tonina L, Tirello P, Duso C, Mori N (2018) Laboratory and field trials to identify effective chemical control strategies for integrated management of Drosophila suzukii in European cherry orchards. Crop Prot 103:73–80

    Article  CAS  Google Scholar 

  • Skorupa D, Dervisefendic A, Zwiener J, Pletcher S (2008) Dietary composition specifies consumption, obesity, and lifespan in Drosophila melanogaster. Aging Cell 7:478–490

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Starmer W (1981) A comparison of Drosophila habitats according to the physiological attributes of the associated yeast communities. Evolution 35:35–53

    Article  Google Scholar 

  • Starmer W and Aberdeen V (1990) The nutritional importance of pure and mixed cultures of yeasts in the development of Drosophila mulleri larvae in Opuntia tissues and its relationship to host plant shifts. Ecol Evol genetics of Drosophila 145–160

  • Steffan S, Lee J, Singleton M, Vilaire A, Walsh D, Lavine L, Patten K (2013) Susceptibility of cranberries to Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 106:2424–2427

    Article  PubMed  Google Scholar 

  • Swoboda-Bhattarai K, McPhie D, Burrack H (2017) Reproductive status of Drosophila suzukii (Diptera: Drosophilidae) females influences attraction to fermentation-based baits and ripe fruits. J Econ Entomol 110:1648–1652

    Article  PubMed  Google Scholar 

  • Tasin M, Lucchi A, Ioriatti C, Mraihi M, De Cristofaro A, Boger Z, Anfora G (2011) Oviposition response of the moth Lobesia botrana to sensory cues from a host plant. Chem Senses 36:633–639

    Article  PubMed  Google Scholar 

  • Tochen S, Walton V, Lee J (2016) Impact of floral feeding on adult Drosophila suzukii survival and nutrient status. J Pest Sci 89:793–802

  • Tonina L, Grassi A, Caruso S, Mori N, Gottardello A, Anfora G, Giomi F, Vaccari G, Ioriatti C, (2018) Comparison of attractants for monitoring in sweet cherry orchards in Italy. J Appl Entomol 142 (1-2):18-25

  • Yu D, Zalom F, Hamby K (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 

  • Wallingford A, Hesler S, Cha D, Leob G (2016a) Behavioral response of spotted-wing drosophila, Drosophila suzukii Matsumura, to aversive odors and a potential oviposition deterrent in the field. Pest Manag Sci 72:701–706

    Article  PubMed  CAS  Google Scholar 

  • Wallingford A, Connelly H, Dore Brind’Amour G, Boucher M, Mafra-Neto A, Loeb G (2016b) Field evaluation of an oviposition deterrent for management of spotted-wing drosophila, Drosophila suzukii, and potential nontarget effects. J Econ Entomol 109:1779–1784

    Article  PubMed  Google Scholar 

  • Wallingford A, Cha D, Linn J, Wolfin M, Loeb G (2017) Robust manipulations of pest insect behaviour using repellents and practical application for integrated pest management. Environ Entomol 46:1041–1050

    Article  PubMed  Google Scholar 

  • Wallingford A, Cha D, Loeb G (2018) Evaluating a push–pull strategy for management of Drosophila suzukii Matsumura in red raspberry. Pest Manag Sci 74:120–125

    Article  PubMed  CAS  Google Scholar 

  • Walsh D, Bolda M, Goodhue R, Dreves D, Lee J, Bruck D, Walton V, O’Neal S, Zalom F (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integrated Pest Manag 2:G1–G7

    Article  Google Scholar 

  • Weng R, Chin J, Yew J, Bushati N, Cohen S (2013) miR-124 controls male reproductive success in Drosophila. eLife 2:1–16

    Article  Google Scholar 

  • Wenninger E, Stelinski L, Hall D (2009) Roles of olfactory cues, visual cues, and mating status in orientation of Diaphorina citri kuwayama (Hemiptera: Psyllidae) to four different host plants. Environ Entomol 38:225–234

    Article  PubMed  Google Scholar 

  • Witzgall P, Kirsch P, Cork A (2010) Sex pheromones and their impact on pest management. J Chem Ecol 36:80-100

  • Wong J, Wallingford A, Loeb G, Lee J (2018) Physiological status of Drosophila suzukii (Diptera: Drosophilidae) affects their response to attractive odors. J of Appl Entomol 00:1–10

    Google Scholar 

  • Young Y, Buckiewicz N, Long T (2018) Nutritional geometry and fitness consequences in Drosophila suzukii, the spotted-wing drosophila. Ecol Evolution 8:2842–2851

    Article  Google Scholar 

  • Zawistowski S, Richmond R (1986) Inhibition of courtship and mating of Drosophila melanogaster by the male-produced lipid, cis-vaccenyl acetate. J Insect Physiol 32:189–192

    Article  CAS  Google Scholar 

  • Ziegler A, Berthelot-Grosjean M, Grosjean Y (2013) The smell of love in Drosophila. Frontiers Physiol 4:1–5

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank members of the Syed lab, Paul Hickner and Nicole Scheidler. We would also like to thank Dong Cha and two anonymous reviewers for the insightful suggestions they provided to improve this manuscript. Pictures were contributed by Robert Holdcraft and permission was granted from Andermatt Biocontrol for use of their Drosa Pro image and Biobest for use of their Droso-Trap image. This research was supported in part by funding from the USDA NIFA Specialty Crops Research Initiative (SCRI) program (award no. 2015-51181-24252) and the USDA NIFA Crop Protection and Pest Management (CPPM) program (award no. 2015-70006-24152).

Author information

Author notes

  1. Kevin R. Cloonan and John Abraham contributed equally to this work.

Authors and Affiliations

  1. Department of Entomology, Rutgers University P.E. Marucci Center, 125A Lake Oswego Rd, Chatsworth, NJ, USA

    Kevin R. Cloonan & Cesar Rodriguez-Saona

  2. Department of Conservation Biology and Entomology, School of Biological Sciences, College of Agriculture and Natural Sciences, University of Cape Coast, Cape Coast, Ghana

    John Abraham

  3. Faculty of Science and Technology, Free University of Bozen-Bolzano, Piazza Università 5, 39100, Bozen-Bolzano, Italy

    Sergio Angeli

  4. Department of Entomology, University of Kentucky, Lexington, KY, 40546, USA

    Zainulabeuddin Syed

Authors
  1. Kevin R. Cloonan
    View author publications

    Search author on:PubMed Google Scholar

  2. John Abraham
    View author publications

    Search author on:PubMed Google Scholar

  3. Sergio Angeli
    View author publications

    Search author on:PubMed Google Scholar

  4. Zainulabeuddin Syed
    View author publications

    Search author on:PubMed Google Scholar

  5. Cesar Rodriguez-Saona
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Kevin R. Cloonan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cloonan, K.R., Abraham, J., Angeli, S. et al. Advances in the Chemical Ecology of the Spotted Wing Drosophila (Drosophila suzukii) and its Applications. J Chem Ecol 44, 922–939 (2018). https://doi.org/10.1007/s10886-018-1000-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-018-1000-y

Keywords

Profiles

  1. Kevin R. Cloonan View author profile