Skip to main content
Log in

Identification and Field Evaluation of Fermentation Volatiles from Wine and Vinegar that Mediate Attraction of Spotted Wing Drosophila, Drosophila suzukii

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

Abstract

Previous studies suggest that olfactory cues from damaged and fermented fruits play important roles in resource recognition of polyphagous spotted wing Drosophila flies (SWD), Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). They are attracted to fermented sweet materials, such as decomposing fruits but also wines and vinegars, and to ubiquitous fermentation volatiles, such as acetic acid and ethanol. Gas chromatography coupled with electroantennographic detection (GC-EAD), gas chromatography-mass spectrometry (GC-MS), two-choice laboratory bioassays, and field trapping experiments were used to identify volatile compounds from wine and vinegar that are involved in SWD attraction. In addition to acetic acid and ethanol, consistent EAD responses were obtained for 13 volatile wine compounds and seven volatile vinegar compounds, with all of the vinegar EAD-active compounds also present in wine. In a field trapping experiment, the 9-component vinegar blend and 15-component wine blend were similarly attractive when compared to an acetic acid plus ethanol mixture, but were not as attractive as the wine plus vinegar mixture. In two-choice laboratory bioassays, 7 EAD-active compounds (ethyl acetate, ethyl butyrate, ethyl lactate, 1-hexanol, isoamyl acetate, 2-methylbutyl acetate, and ethyl sorbate), when added singly to the mixture at the same concentrations tested in the field, decreased the attraction of SWD to the mixture of acetic acid and ethanol. The blends composed of the remaining EAD-active chemicals, an 8-component wine blend [acetic acid + ethanol + acetoin + grape butyrate + methionol + isoamyl lactate + 2-phenylethanol + diethyl succinate] and a 5-component vinegar blend [acetic acid + ethanol + acetoin + grape butyrate + 2-phenylethanol] were more attractive than the acetic acid plus ethanol mixture, and as attractive as the wine plus vinegar mixture in both laboratory assays and the field trapping experiment. These results indicate that these volatiles in wine and vinegar are crucial for SWD attraction to fermented materials on which they feed as adults.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ai, M., Min, S., Grosjean, Y., Leblanc, C., Bell, R., Benton, R., and Suh, G. S. B. 2010. Acid sensing by the Drosophila olfactory system. Nature 468:691–U112.

    Article  PubMed  CAS  Google Scholar 

  • Alagarmalai, J., Nestel, D., Dragushich, D., Nemny-Lavy, E., Anshelevich, L., Zada, A., and Soroker, V. 2009. Identification of host attractants for the Ethiopian fruit fly, Dacus ciliatus Loew. J. Chem. Ecol. 35:542–551.

    Article  PubMed  CAS  Google Scholar 

  • Antonelli, A., Castellari, L., Zambonelli, C., and Carnacini, A. 1999. Yeast influence on volatile composition of wines. J. Agr. Food Chem. 47:1139–1144.

    Article  CAS  Google Scholar 

  • Barata, A., Malfeito-Ferreira, M., and Loureiro, V. 2012. The microbial ecology of wine grape berries. Int. J. Food Microbiol. 153:243–259.

    Article  PubMed  CAS  Google Scholar 

  • Barrows, W. M. 1907. The reactions of the pomace fly, Drosophila ampelophila Loew, to odorous substances. J. Exp. Zoology 4:515–537.

    Article  Google Scholar 

  • Becher, P. G., Bengtsson, M., Hansson, B. S., and Witzgall, P. 2010. Flying the fly: long-range flight behavior of Drosophila melanogaster to attractive odors. J. Chem. Ecol. 36:599–607.

    Article  PubMed  CAS  Google Scholar 

  • Becher, P. G., Flick, G., Rozpędowska, E., Schmidt, A., Hagman, A., Lebreton, S., Larsson, M. C., Hansson, B. S., Piškur, J., Witzgall, P., and Bengtsson, M. 2012. Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development. Funct. Ecol. 26:822–828.

    Article  Google Scholar 

  • Beers, E. H., van Steenwyk, R. A., Shearer, P. W., Coates, W. W., and Grant, J. A. 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 

  • Bruce, T. J. A. and Pickett, J. A. 2011. Perception of plant volatile blends by herbivorous insects — Finding the right mix. Phytochemistry 13:1605–1611.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Calabria, G., Maca, J., Bachli, G., Serra, L., and 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 

  • Cha, D. H., Linn Jr., C. E., Teal, P. E. A., Zhang, A., Roelofs, W. L., and Loeb, G. M. 2011a. Eavesdropping on plant volatiles by a specialist moth: significance of ratio and concentration. PLoS One 6:e17033.

    Article  PubMed  CAS  Google Scholar 

  • Cha, D. H., Powell, T. H. Q., Feder, J. L., and Linn Jr., C. E. 2011b. Identification of host fruit volatiles from three mayhaw species (Crataegus Series Aestivales) attractive to mayhaw-origin Rhagoletis pomonella flies in the Southern United States. J. Chem. Ecol. 37:961–973.

    Article  PubMed  CAS  Google Scholar 

  • Cha, D. H., Powell, T. H. Q., Feder, J. L., and Linn Jr., C. E. 2011c. Identification of fruit volatiles from green hawthorn (Crataegus viridis) and blueberry hawthorn (Crataegus brachyacantha) host plants attractive to different phenotypes of Rhagoletis pomonella flies in the Southern United States. J. Chem. Ecol. 37:974–983.

    Article  PubMed  CAS  Google Scholar 

  • Cha, D. H., Powell, T. H. Q., Feder, J. L., and Linn Jr., C. E. 2012a. Geographic variation in fruit volatiles emitted by the hawthorn Crataegus mollis and its consequences for host race formation in the apple maggot fly, Rhagoletis pomonella. Entomol. Exp. Appl. 143:254–268.

    Article  CAS  Google Scholar 

  • Cha, D. H., Yee, W. L., Goughnour, R. B., Sim, S. B., Powell, T. H. Q., Feder, J. L., and Linn Jr., C. E. 2012b. Identification of host fruit volatiles from domestic apple (Malus domestica), native black hawthorn (Crataegus douglasii) and introduced ornamental hawthorn (C. monogyna) attractive to Rhagoletis pomonella flies from the Western United States. J. Chem. Ecol. 38:319–329.

    Article  PubMed  CAS  Google Scholar 

  • Cini, A., Ioriatti, C., and Anfora, G. 2012. A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull. Insect. 65:149–160.

    Google Scholar 

  • Cossé, A. A. and Baker, T. C. 1996. House flies and pig manure volatiles: wind tunnel behavioral studies and electrophysiological evaluations. J. Agric. Entomol. 13:301–317.

    Google Scholar 

  • Cossé, A. A., Todd, J. L., Millar, J. G., Martínez, L. A., and Baker, T. C. 1995. Electroantennographic and coupled gas chromatographic-electroantennographic responses of the mediterranean fruit fly, Ceratitis capitata, to male-produced volatiles and mango odor. J. Chem. Ecol. 21:1823–1836.

    Article  Google Scholar 

  • Davis, T. S., Boundy-Mills, K., and Landolt, P. J. 2012. Volatile emissions from an epiphytic fungus are semiochemicals for eusocial wasps. Microb. Ecol. doi:10.1007/s00248-012-0074-2.

  • Delfinado, M. D. and Hardy, D. E. 1977. A Catalog of the Diptera of the Oriental Region. Volume III. Suborder Cyclorrapha. The University Press of Hawaii, Honolulu.

  • Dethier, V. G. 1947. Chemical Insect Attractants and Repellents. Maple Press Co., York, OA.

  • Dicke, M. and van Loon, J. J. A. 2000. Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol. Exp. Appl. 97:237–249.

    Article  CAS  Google Scholar 

  • Fishman, A., Eroshov, M., Dee-Noor, S. S., van Mil, J., Cogan, U., and Effenberger, R. 2001. A two-step enzymatic resolution process for large-scale production of (S)- and (R)-ethyl-3-hydroxybutyrate. Biotech. Bioeng. 74:256–263.

    Article  CAS  Google Scholar 

  • Fuyama, Y. 1976. Behavior genetics of olfactory responses in Drosophila. I. Olfactometry and strain differences in Drosophila melanogaster. Behav. Genet. 6:407–420.

    Article  PubMed  CAS  Google Scholar 

  • Goodhue, R. E., Bolda, M., Farnsworth, D., Williams, J. C., and Zalom, F. G. 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 

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

    Article  PubMed  CAS  Google Scholar 

  • Hauser, M. 2011. A historic account of the invastion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Manag. Sci. 67:1352–1357.

    Article  PubMed  CAS  Google Scholar 

  • Hayashibe, M., Katoda, S., Owada, H., Yoshida, H., Katayose, A., and Terashim, T. 1970. Methionine metabolism in yeast.1. methionol formation. J. Ferm. Tech. 48:22–28.

    CAS  Google Scholar 

  • Hilker, M. and McNeil, J. 2007. Chemical and behavioral ecology in insect parasitoids: how to behave optimally in a complex odourous environment, pp. 92–112, in E. Wajnberg, C. Bernstein, and J. van Alphen (eds.), Behavioral Ecology of Insect Parasitoids. Blackwell Publishing, Malden, MA.

    Google Scholar 

  • Joseph, R. M., Devineni, A. V., King, I. F. G., and Heberlein, U. 2009. Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila. Proc. Natl. Acad. Sci. USA 106:11352–11357.

    Article  PubMed  CAS  Google Scholar 

  • Kaneshiro, K. Y. 1983. Drosophila (Sophophora) suzukii (Matsumura). Proc. Hawaiian Entomol. Soc. 24:179.

    Google Scholar 

  • Kanzawa, T. 1934. Research into the fruit fly Drosophila suzukii Matsura. Yamanashi Prefecture Agricultural Experiment Station Report, October 1934, 48 p.

  • Kendra, P. E., Montgomery, W. S., Epsky, N. D., and Heath, R. R. 2009. Electroantennogram and behavioral responses of Anastrepha suspense (Diptera: Tephritidae) to putrescine and ammonium bicarbonate lures. Environ. Entomol. 38:1259–1266.

    Article  PubMed  CAS  Google Scholar 

  • Landolt, P. J. and Alfaro, J. F. 2001. Trapping Lacanobia subjuncta, Xestia c-nigrum, and Mamestra configurata (Lepidoptera: Noctuidae) with acetic acid and 3-methyl-1-butanol in controlled release dispensers. Environ. Entomol. 30:656–662.

    Article  CAS  Google Scholar 

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

  • Lee, J.-E., Hong, Y.-S., and Lee, C.-H. 2009. Characterization of fermentative behaviors of lactic acid bacteria in grape wines through H-1 NMR- and GC-based metabolic profiling. J. Agr. Food Chem. 57:4810–4817.

    Article  CAS  Google Scholar 

  • Lee, J. C., Bruck, D. J., Curry, H., Edwards, D., Haviland, D. R., Vansteenwyck, R. A., and Youngey, B. M. 2011a. The susceptibility of small fruit and cherries to the spotted wing Drosophila, Drosophila suzukii. Pest Manag. Sci. 67:1358–1367.

    Article  PubMed  CAS  Google Scholar 

  • Lee, J. C., Bruck, D. J., Dreves, A. J., Ioratti, C., Vost, H., and Baufield, P. 2011b. In focus: spotted wing Drosophila, Drosophila suzukii, across perspectives. Pest Manag. Sci. 67:1349–1351.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, J. H. 2009. Handbook of Biological Statistics, 2nd ed. Sparky House Publishing, Baltimore, MD, USA.

    Google Scholar 

  • McKenzie, J. A. and Parsons, P. A. 1972. Alcohol tolerance: an ecological parameter in the relative success of Drosophila melanogaster and Drosophila simulans. Oecologica 10:373–388.

    Article  Google Scholar 

  • Minks, A. K., Roelofs, W. L., Ritter, F. J., and Persoons, C. J. 1973. Reproductive isolation of two tortricid moth species by different ratios of a two-component sex attractant. Science 180:1073–1074.

    Article  PubMed  CAS  Google Scholar 

  • Mitsui, H., Takahashi, K., and Kimura, M. 2006. Spatial distributions and clutch sizes of Drosophila species ovipositing on cherry fruits of different stages. Popul. Ecol. 48:233–237.

    Article  Google Scholar 

  • Mowat, J., Gries, R., Khaskin, G., Gries, G., and Britton, R. 2009. (S)-2-pentyl (R)-3-hydroxyhexanoate, a banana volatile and its olfactory recognition by the common fruit fly, Drosophila melanogaster. J. Nat. Prod. 72:772–776.

    Article  PubMed  CAS  Google Scholar 

  • Nojima, S., Linn, C., Morris, B., Zhang, A. J., and Roelofs, W. 2003. Identification of host fruit volatiles from hawthorn (Crataegus spp.) attractive to hawthorn-origin Rhagoletis pomonella flies. J. Chem. Ecol. 29:321–336.

    Article  PubMed  CAS  Google Scholar 

  • Nout, M. J. R. and Bartelt, R. J. 1998. Attraction of a flying nitidulid (Carpophilus humeralis) to volatiles produced by yeasts grown on sweet corn and a corn-based medium. J. Chem. Ecol. 24:1217–1239.

    Article  CAS  Google Scholar 

  • Pivnick, K. A., Lamb, R. L., and Reed, D. 1992. Response of flea beetles, Phyllotreta spp., to mustard oils and nitriles in field trapping experiments. J. Chem. Ecol. 18:863–873.

    Article  CAS  Google Scholar 

  • Primante, C. and Dötterl, S. 2010. A syrphid fly uses olfactory cues to find a non-yellow flower. J. Chem. Ecol. 36:1207–1210.

    Article  PubMed  CAS  Google Scholar 

  • Raguso, R. A. 2008. Wake up and smell the roses: the ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39:549–569.

    Article  Google Scholar 

  • Reed, M. R. 1938. The olfactory reactions of Drosophila melanogaster Meigen to the products of fermenting banana. Physiol. Zool. 11:317–325.

    Google Scholar 

  • Rodan, A. R. and Rothenfluh, A. 2010. The genetics of behavioral alcohol responses in Drosophila, pp. 25–51, in M. T. Reilly and D. M. Lovinger (eds.), Functional Plasticity and Genetic Variation: Insights into the Neurobiology and Alcoholism. Elsevier Academic Press, San Diego, CA.

    Chapter  Google Scholar 

  • Roelofs, W. L. and Cardé, R. T. 1974. Oriental fruit moth and lesser appleworm attractant mixtures refined. Environ. Entomol. 3:586–588.

    Google Scholar 

  • Roelofs, W. and Comeau, A. 1971. Sex pheromone perception: synergists and inhibitors for the redbanded leafroller attractant. J. Insect Physiol. 17:435–449.

    Article  CAS  Google Scholar 

  • Romano, P. and Suzzi, G. 1996. Origin and production of acetoin during wine yeast fermentation. Appl. Environ. Microbiol. 62:309–315.

    PubMed  CAS  Google Scholar 

  • SAS Institute. 2009. The mixed model procedure, version 9.2. www.sas.com.

  • Schoonhoven, L. M., Jermy, T., and van Loon, J. J. A. 1998. Insect-Plant Biology. Chapman & Hall, London, UK.

    Google Scholar 

  • Siderhurst, M. S. and Jang, E. B. 2006. Female-biased attraction of oriental fruit fly, Bactrocera dorsalis (Hendel), to a blend of host fruit volatiles from Terminalia catappa L. J. Chem. Ecol. 32:2513–2524.

    Article  PubMed  CAS  Google Scholar 

  • Siderhurst, M. S. and Jang, E. B. 2010. Cucumber volatile blend attractive to female melon fly, Bactrocera cucurbitae (Coquillett). J. Chem. Ecol. 36:699–708.

    Article  PubMed  CAS  Google Scholar 

  • Steck, G. J., Dixon, W. and Dean, D. 2009. Spotted wing Drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), a fruit pest new to North America. Pest Alerts. www.fl.dpi.com/enpp/ento/drosophila_suzukii.html.

  • Stökl, J., Strutz, A., Dafni, A., Svatos, A., Doubsky, J., Knaden, M., Sachse, S., Hansson, B. S., and Stensmyr, M. C. 2010. Deceptive pollination system targeting Drosophilids through olfactory mimicry of yeast. Curr. Biol. 20:1846–1852.

    Article  PubMed  Google Scholar 

  • Tasin, M., Betta, E., Carlin, S., Gasperi, F., Mattivi, F., and Pertot, I. 2011. Volatiles that encode host-plant quality in the grapevine moth. Phytochemistry 72:1999–2005.

    Article  PubMed  CAS  Google Scholar 

  • Wagner, K. and Rapp, A. 1999. Influence of yeasts on the formation of 2-phenylethanol during the alcoholic fermentation. Dtsch Lebensm Rundsch 95:304–309.

    CAS  Google Scholar 

  • Walsh, D. B., Bolda, M. P., Goodhow, R. E., Dreves, A. J., Lee, J., Bruck, D. V., Walton, M., O’NEAL, S. D., and Zalom, F. G. 2011. Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J. Integ. Pest Manag. 106:289–295.

    Google Scholar 

  • Witzgall, P., Proffit, M., Rozpedowska, E., Becher, P. G., Andreadis, S., Coracini, M., Lindblom, T. U., Ream, L. J., Hagman, A., Bengtsson, M., Kurtzman, C. P., Piskur, J., and Knight, A. 2012. “This is not an apple”-yeast mutualism in codling moth. J. Chem. Ecol. 38:949–957.

    Article  PubMed  Google Scholar 

  • Wright, G. A., Lutmerding, A., Dudareva, N., and Smith, B. H. 2005. Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honeybees (Apis mellifera). J. Comp. Physiol. A 191:105–114.

    Article  CAS  Google Scholar 

  • Yano, T., Aimi, T., Nakano, Y., and Tamai, M. 1997. Prediction of the concentrations of ethanol and acetic acid in the culture broth of a rice vinegar fermentation using near-infrared spectroscopy. J. Ferment. Bioeng. 84:461–465.

    Article  CAS  Google Scholar 

  • Zar, J. H. 1984. Biostatistical Analysis. Prentice-Hall, New Jersey.

    Google Scholar 

  • Zhang, A. J., Linn, C., Wright, S., Prokopy, R., Reissig, W., and Roelofs, W. 1999. Identification of a new blend of apple volatiles attractive to the apple maggot, Rhagoletis pomonella. J. Chem. Ecol. 25:1221–1232.

    Article  CAS  Google Scholar 

  • Zhu, J., Park, K.-C., and Baker, T. C. 2003. Identification of odors from overripe mango that attract vinegar flies, Drosophila melanogaster. J. Chem. Ecol. 29:899–909.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Jewel Brumley, Daryl Green, and Heather Headrick for technical supports and Alan Knight, Lee Reams, and Esteban Basoalto for supplying SWD. David Horton, Gregory Loeb, and two anonymous reviewers provided insightful suggestions for improvement to the manuscript. This research was supported in part by funding from the Washington Tree Fruit Research Commission.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dong H. Cha.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cha, D.H., Adams, T., Rogg, H. et al. 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 (2012). https://doi.org/10.1007/s10886-012-0196-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-012-0196-5

Keywords

Navigation