Journal of Chemical Ecology

, Volume 38, Issue 11, pp 1419–1431 | Cite as

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

  • Dong H. Cha
  • Todd Adams
  • Helmuth Rogg
  • Peter J. Landolt
Article

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.

Keywords

Drosophila suzukii Spotted wing Drosophila Feeding attractant Trap Lure GC-EAD 

References

  1. 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.PubMedCrossRefGoogle Scholar
  2. 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.PubMedCrossRefGoogle Scholar
  3. Antonelli, A., Castellari, L., Zambonelli, C., and Carnacini, A. 1999. Yeast influence on volatile composition of wines. J. Agr. Food Chem. 47:1139–1144.CrossRefGoogle Scholar
  4. Barata, A., Malfeito-Ferreira, M., and Loureiro, V. 2012. The microbial ecology of wine grape berries. Int. J. Food Microbiol. 153:243–259.PubMedCrossRefGoogle Scholar
  5. Barrows, W. M. 1907. The reactions of the pomace fly, Drosophila ampelophila Loew, to odorous substances. J. Exp. Zoology 4:515–537.CrossRefGoogle Scholar
  6. 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.PubMedCrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.PubMedCrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. Bruce, T. J. A., Wadhams, L. J., and Woodcock, C. M. 2005. Insect host location: a volatile situation. Trends Plant Sci. 10:269–274.PubMedCrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 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.PubMedCrossRefGoogle Scholar
  13. 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.PubMedCrossRefGoogle Scholar
  14. 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.PubMedCrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. 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
  18. 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
  19. 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.CrossRefGoogle Scholar
  20. 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.
  21. 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.Google Scholar
  22. Dethier, V. G. 1947. Chemical Insect Attractants and Repellents. Maple Press Co., York, OA.Google Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. Fuyama, Y. 1976. Behavior genetics of olfactory responses in Drosophila. I. Olfactometry and strain differences in Drosophila melanogaster. Behav. Genet. 6:407–420.PubMedCrossRefGoogle Scholar
  26. 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.PubMedCrossRefGoogle Scholar
  27. 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.PubMedCrossRefGoogle Scholar
  28. 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.PubMedCrossRefGoogle Scholar
  29. 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.Google Scholar
  30. 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
  31. 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.PubMedCrossRefGoogle Scholar
  32. Kaneshiro, K. Y. 1983. Drosophila (Sophophora) suzukii (Matsumura). Proc. Hawaiian Entomol. Soc. 24:179.Google Scholar
  33. Kanzawa, T. 1934. Research into the fruit fly Drosophila suzukii Matsura. Yamanashi Prefecture Agricultural Experiment Station Report, October 1934, 48 p.Google Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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.Google Scholar
  38. 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.CrossRefGoogle Scholar
  39. 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.PubMedCrossRefGoogle Scholar
  40. 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.PubMedCrossRefGoogle Scholar
  41. McDonald, J. H. 2009. Handbook of Biological Statistics, 2nd ed. Sparky House Publishing, Baltimore, MD, USA.Google Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.PubMedCrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. 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.PubMedCrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. 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.CrossRefGoogle Scholar
  49. Primante, C. and Dötterl, S. 2010. A syrphid fly uses olfactory cues to find a non-yellow flower. J. Chem. Ecol. 36:1207–1210.PubMedCrossRefGoogle Scholar
  50. 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.CrossRefGoogle Scholar
  51. Reed, M. R. 1938. The olfactory reactions of Drosophila melanogaster Meigen to the products of fermenting banana. Physiol. Zool. 11:317–325.Google Scholar
  52. 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.CrossRefGoogle Scholar
  53. Roelofs, W. L. and Cardé, R. T. 1974. Oriental fruit moth and lesser appleworm attractant mixtures refined. Environ. Entomol. 3:586–588.Google Scholar
  54. Roelofs, W. and Comeau, A. 1971. Sex pheromone perception: synergists and inhibitors for the redbanded leafroller attractant. J. Insect Physiol. 17:435–449.CrossRefGoogle Scholar
  55. Romano, P. and Suzzi, G. 1996. Origin and production of acetoin during wine yeast fermentation. Appl. Environ. Microbiol. 62:309–315.PubMedGoogle Scholar
  56. SAS Institute. 2009. The mixed model procedure, version 9.2. www.sas.com.
  57. Schoonhoven, L. M., Jermy, T., and van Loon, J. J. A. 1998. Insect-Plant Biology. Chapman & Hall, London, UK.Google Scholar
  58. 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.PubMedCrossRefGoogle Scholar
  59. 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.PubMedCrossRefGoogle Scholar
  60. 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.
  61. 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.PubMedCrossRefGoogle Scholar
  62. 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.PubMedCrossRefGoogle Scholar
  63. 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.Google Scholar
  64. 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
  65. 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.PubMedCrossRefGoogle Scholar
  66. 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.CrossRefGoogle Scholar
  67. 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.CrossRefGoogle Scholar
  68. Zar, J. H. 1984. Biostatistical Analysis. Prentice-Hall, New Jersey.Google Scholar
  69. 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.CrossRefGoogle Scholar
  70. 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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York (outside the USA) 2012

Authors and Affiliations

  • Dong H. Cha
    • 1
  • Todd Adams
    • 2
  • Helmuth Rogg
    • 2
  • Peter J. Landolt
    • 1
  1. 1.Yakima Agricultural Research LaboratoryUSDA, ARSWapatoUSA
  2. 2.Oregon Department of AgricultureSalemUSA

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