Olfactory Responses of the Predatory Mites (N eoseiulus cucumeris) and Insects (O rius strigicollis ) to Two Different Plant Species Infested with Onion Thrips (T hrips tabaci)

  • Satoshi Tatemoto
  • Takeshi Shimoda


Responses of Neoseiulus cucumeris (a predatory mite) and the predatory insect Orius strigicollis to volatiles associated with two different plant species infested with onion thrips, Thrips tabaci, were examined in a Y-tube olfactometer. Both predators species showed a significant preference for volatiles from infested cucumber leaves without T. tabaci over clean air. However, they were not attracted to volatiles from uninfested cucumber leaves, artificially damaged cucumber leaves, or volatiles from T. tabaci plus their visible products collected from cucumber leaves. These results suggest that both predator species are capable of exploiting herbivore-induced volatiles from T. tabaci-infested cucumber leaves as a foraging cue. Neither predator was attracted to volatiles from uninfested spring onion leaves, infested spring onion leaves without T. tabaci, or volatiles from T. tabaci plus their visible products collected from spring onion leaves. Interestingly, they avoided volatiles from artificially damaged spring onion leaves. A possible explanation for the non-significant olfactory responses of the predator species to spring onion plants with infestation damage of T. tabaci is discussed.


Spring onion Cucumber Thrips tabaci Neoseiulus cucumeris Orius strigicollis Herbivore-induced volatiles Attraction Avoidance 



We thank Junji Takabayashi, Rika Ozawa, and Hiromichi Nitta for their constructive comments during the study. We also express gratitude to Kouichi Yamaguchi for providing us with the predatory mites. This study was supported by a Grant-in-Aid for Scientific Research (No. 19380188) of the Japan Society for the Promotion of Science.


  1. Aratchige, N. S., Lesna, I., and Sabelis, M. W. 2004. Below-ground plant parts emit herbivore-induced volatiles: olfactory responses of a predatory mite to tulip bulbs infested by rust mites. Exp. Appl. Acarol. 33:21–30.PubMedCrossRefGoogle Scholar
  2. Auger, J., Dugravot, S., and Thibout, E. 1989. Leek odor analysis by gas chromatography and identification of the most active substance for the leek moth, Acrolepiopsis assectella. J. Chem. Ecol. 15:1847–1854.CrossRefGoogle Scholar
  3. Bennison, J., Maulden, K., Dewhirst, S., Pow, E., Slatter, P., and Wadhams, L. 2002. Towards the development of a push–pull strategy for improving biological control of western flower thrips on chrysanthemum, pp. 199–206, in R. Marullo and L. Mound (eds.). Thrips and Tospoviruses. Proceedings of the 7th International Symposium on Thysanoptera, Reggio Calabria, Italy.Google Scholar
  4. Brødsgaard, H. F., and Hansen, L. S. 1992. Effect of Amblyseius cucumeris and Amblyseius barkeri as biological control agents of Thrips tabaci on glasshouse cucumbers. Biocontrol Sci. Technol. 2:215–223.CrossRefGoogle Scholar
  5. Childers, C. C. 1997. Feeding and oviposition injuries to plants, pp. 505–537, in T. Lewis (ed.). Thrips as Crop Pests. CAB International, New York.Google Scholar
  6. Choh, Y., Shimoda, T., Ozawa., R., Dicke, M., and Takabayashi, J. 2004. Exposure of lima bean leaves to volatiles from herbivore-infested conspecific plants results in emission of carnivore attractants: active of passive process. J. Chem. Ecol. 30:1305–1317.PubMedCrossRefGoogle Scholar
  7. De Boer, J. G., Posthumus, M. A., and Dicke, M. 2004. Identification of volatiles that are used in discrimination between plants infested with prey or non–prey herbivores by a predatory mite. J. Chem. Ecol. 30:2215–2230.PubMedCrossRefGoogle Scholar
  8. De Boer, J. G., Snoeren, T. A., and Dicke, M. 2005. Predatory mites learn to discriminate between plant volatiles induced by prey and nonprey herbivores. Anim. Behav. 69:869–879.CrossRefGoogle Scholar
  9. Dicke, M. 1999a. Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomol. Exp. Appl. 91:131–142.CrossRefGoogle Scholar
  10. Dicke, M. 1999b. Evolution of induced indirect defense of plants, pp. 63–88, in R. Tollrian, and C. D. Harvell (eds.). The Ecology and Evolution of Inducible Defense, Princeton University Press, Princeton.Google Scholar
  11. Dicke, M., Van Beek, T. A., Posthumus, M. A., Ben Don, N., Van Bokhoven, H., and De Groot, A. E. 1990a. Isolation and identification of volatile kairomone that affects acarine predator–prey interactions: Involvement of host plant in its production. J. Chem. Ecol. 16:381–396.CrossRefGoogle Scholar
  12. Dicke, M., Van Der Maas, K. J., Takabayashi, J., and Vet, L. E. M. 1990b. Learning affects response of volatile allelochemicals by predatory mites. Proc. Exp. Appl. Entomol. 1:31–36.Google Scholar
  13. Dicke, M., Takabayashi, J., Posthumus, M. A., Schütte, C., and Olga, E. K. 1998. Plant-phytoseiid interactions mediated by herbivore-induced plant volatiles: Variation in production of cues and in responses of predatory mites. Exp. Appl. Acarol. 22:311–333.CrossRefGoogle Scholar
  14. Dicke, M., Agrawal, A. A., and Bruin, J. 2003. Plant talk, but are they deaf. Trends Pl. Sci. 8:403–405.CrossRefGoogle Scholar
  15. Doederlein, T. A., and Sites, R. W. 1993. Host plant preferences of Frankliniella occidentalis and Thrips tabaci (Thysanoptera: Thripidae) for onions and associated weeds on the Souther High Plains. J. Econ. Entomol. 86:1706–1713.Google Scholar
  16. Doi, M., Zen, S., Okuda, M., Nakamura, H., Kato, K., and Hanada, K. 2003. Leaf necrosis disease of lisianthus (Eustoma ganadiflorum) caused by Iris yellow spots virus. Jpn. J. Phytopathol. 69:181–188. (in Japanese with English summary).Google Scholar
  17. Drukker, B., Scutareanu, P., and Sabelis, M. W. 1995. Do anthocorid predators respond to synomones from Psylla-infested pear trees under field conditions? Entomol. Exp. Appl. 77:193–203.CrossRefGoogle Scholar
  18. Drukker, B., Bruin, J., Jacobs, G., Kroon, A., and Sabelis, M. W. 2000a. How predatory mites learn to cope with variability in volatile plant signals in the environment of their herbivorous prey. Exp. Appl. Acarol. 24:881–895.PubMedCrossRefGoogle Scholar
  19. Drukker, B., Bruin, J., and Sabelis, M. W. 2000b. Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey. Physiol. Entomol. 25:260–265.CrossRefGoogle Scholar
  20. Dugravot, S., and Thibout, E. 2006. Consequences for a specialist insect and its parasitoid of the response of Allium porrum to conspecific herbivore attack. Physiol. Entomol. 31:73–79.CrossRefGoogle Scholar
  21. Dugravot, S., Thibout, E., Abo-Ghalia, A., and Huignard, J. 2004. How a specialist and a non-specialist insect cope with dimethyl disulfide produced by Allium porrum? Entomol. Exp. Appl. 113:173–179.CrossRefGoogle Scholar
  22. Dugravot, S., Mondy, N., Mandon, N., and Thibout, E. 2005. Increased sulfur precursors and volatiles production by the leek Allium porrum in response to specialist insect attack. J. Chem. Ecol. 31:1299–1314.PubMedCrossRefGoogle Scholar
  23. Edelson, J. V., Cartwright, B., and Royer, T. A. 1989. Economics of controlling onion thrips (Thysanoptera: Thripidae) on onions with insecticides in south Texas. J. Econ. Entomol. 82:561–564.Google Scholar
  24. Gillespie, D. R. 1989. Biological control of thrips [Thysanoptera: Thripidae] on greenhouse cucumbers by Amblyseius cucumeris. Entomophaga 34:185–192.CrossRefGoogle Scholar
  25. Hinomoto, N., Muraji, M., Noda, T., Shimizu, T., and Kawasaki, K. 2004. Identification of five Orius in Japan by multiplex polymerase chain reaction. Biol. Contol. 31:276–279.CrossRefGoogle Scholar
  26. Hori, M., and Harada, H. 1995. Screening plants resistant to green peach aphid, Myzus persicae (Sulzer) (Homoptera: Aphididae). Appl. Entomol. Zool. 30:246–249.Google Scholar
  27. Hoy., C. W., and Glenister., C. S. 1991. Releasing Amblyseius spp. (Acarina: Phytoseiidae) to control Thrips tabaci (Thysanoptera: Thripidae) on cabbage. Entomophaga 36:561–573.CrossRefGoogle Scholar
  28. James, D. G., and Price, T. S. 2004. Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J. Chem. Ecol. 30:1613–1628.PubMedCrossRefGoogle Scholar
  29. Janssen, A., Pallini, A., Venzon, M., and Sabelis, M. W. 1998. Behaviour and indirect interactions in food webs of plant-inhabiting arthropods. Exp. Appl. Acarol. 22:497–521.CrossRefGoogle Scholar
  30. Karban, R., and Baldwin, I. T. 1997. Induced Responses to Herbivory. Chicago University Press, Chicago, IL, USA.Google Scholar
  31. Kendall., D. M., and Bjostad, L. B. 1987. Susceptibility of onion growth stages to onion thrips (Thysanoptera: thripidae) damage and mechanical defoliation. Environ. Entomol. 16:859–863.Google Scholar
  32. Kritzman., A., Lampel, M., Raccah, B., and Gera, A. 2001. Distribution and transmission of Iris yellow spot virus. Plant Disease 85:838–842.CrossRefGoogle Scholar
  33. Maeda, T., Liu, Y., Ishiwari, H., and Shimoda, T. 2006. Conditioned olfactory responses of a predatory mite, Neoseiulus womersleyi, to volatiles from prey-infested plants. Entomol. Exp. Appl. 121:167–175.CrossRefGoogle Scholar
  34. Ozawa, R., Arimura, G., Takabayashi, J., Shimoda, T., and Nishioka, T. 2000. Involvement of jasmonic- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiol. 41:391–398.PubMedGoogle Scholar
  35. Scutareanu, P., Drukker, B., Bruin, J., Posthumus, M. A., and Sabelis, M. W. 1996. Leaf volatiles and polyphenols in pear trees infested by Psylla pyricola. Evidence of simultaneously induced responses. Chemoeology 7:34–38.CrossRefGoogle Scholar
  36. Shelton, A. M., Wilsey, W. T., and Schmaedick, M. A. 1998. Management of onion thrips (Thysanoptera: Thripidae) on cabbage by using plant resistance and insecticides. J. Econ. Entomol. 91:329–333.Google Scholar
  37. Shimoda, T., and Dicke, M. 1999. Volatile stimuli related to feeding activity of nonprey caterpillars, Spodoptera exigua, affect olfactory response of the predatory mite, Phytoseiulus persimilis. J. Chem. Ecol. 23:2033–2048.CrossRefGoogle Scholar
  38. Shimoda, T., Ozawa, R., Sano, K., Yano, E., and Takabayashi, J. 2005. The involvement of volatile infochemicals from spider mites and from food-plants in prey location of the generalist predatory mite, Neoseiulus californicus. J. Chem. Ecol. 31:2019–2032.PubMedCrossRefGoogle Scholar
  39. Shiojiri, K., Maeda, T., Arimura, G., Ozawa, R., Shimoda, T., and Takabayashi, J. 2002. Functions of plant infochemicals in tritrophic interactions between plants, herbivores and carnivorous natural enemies. Jpn. J. Appl. Entomol. Zool. 46:117–133 (in Japanese with English summary).CrossRefGoogle Scholar
  40. Shipp, J. L., and Wang, K. 2003. Evaluation of Amblyseius cucumeris (Acari: Phytoseiidae) and Orius insidiosus (Hemiptera: Anthocoridae) for control of Frankliniella occidentalis (Thysanoptera: Thripidae) on greenhouse tomatoes. Biol. Contol. 28:271–281.CrossRefGoogle Scholar
  41. Sokal, R. R., and Rohlf, F. J. 1995. Biometry. Freeman, New York. p. 887.Google Scholar
  42. Takabayashi, J., and Dicke, M. 1992. Response of predatory mites with different rearing histories to volatiles of uninfested plants. Entomol. Exp. Appl. 64:187–193.Google Scholar
  43. Takabayashi, J., and Dicke, M. 1996. Plant–carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci. 1:109–113.CrossRefGoogle Scholar
  44. Takabayashi, J., Shimoda, T., Dicke, M., Ashihara, W., and Takafuji, A. 2000. Induced response of tomato plants to injury by green and red strains of Tetranychus urticae. Exp. Appl. Acarol. 24:377–383.PubMedCrossRefGoogle Scholar
  45. Tsuchiya, M. 2001. Occurrence of blemished fruits caused by Thrips tabaci on Satsuma mandarin cultivated in the greenhouses in Shizuoka Prefecture. Ann. Rept. Kanto Pl. Plot. Soc. 48:153–155 (in Japanese with English summary).Google Scholar
  46. Tsuchiya, M. 2002. Infestation and oviposition of Thrips tabaci (Lindeman) on Satsuma mandarin (Citrus unshiu Marc.) Jpn.. J. Appl. Entomol. Zool. 46:217–224 (in Japanese with English summary).CrossRefGoogle Scholar
  47. Turlings, T. C. J., Wäckers, F. L., Vet, L. E. M., Lewis, W. J., and Tumlinson, J. H. 1993. Learning of host-finding cues by Hymenopterous parasitoids, pp. 51–78, in D. R. Papaj, and A. C. Lewis (eds.). Insect Learning. Chapman and Hall, New York.Google Scholar
  48. Venugopal, M. S., and Narayanan, V. 1981. Effects of allition on the green peach ahid (Myzus persicae Sulzer). Int. Pest. Cont. 93:130–131.Google Scholar
  49. Venzon, M., Janssen, A., and Sabelis, M. W. 1999. Attraction of a generalist predator towards herbivore-infested plants. Entomol. Exp. Appl. 93:305–314.CrossRefGoogle Scholar
  50. Vet, L. E. M., Lewis, W. J., and Carde, R. T. 1993. Parasitoid foraging and learning, pp. 65–101, in R. T. Carde, and W. J. Bell (eds.). Chemical Ecology of Insects 2. Chapman and Hall, New York.Google Scholar
  51. Wang, C. L., Lee, P. C., and Wu, Y. J. 2001. Field augmentation of Orius strigicollis for the control of thrips in Taiwan. International Seminar on Biological Control of IPEC 141–152.Google Scholar
  52. Williams, M. D. 2001. Biological control of thrips on ornamental crops: interactions between the predatory mite Neoseiulus cucumeris (Acari: Phytoseiidae) and western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), on cyclamen. Biocontrol Sci. Technol. 11:41–55.CrossRefGoogle Scholar
  53. Yasunaga, T. 1997. The flower bug genus Orius Wolff (Heteroptera: Anthocoridae) from Japan and Taiwan, Part II. Appl. Entomol. Zool. 32:379–386.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Hiroshima Prefecture Agriculture Research CenterHiroshimaJapan
  2. 2.Insect Pest Management Research TeamNational Agricultural Research CenterTsukubaJapan
  3. 3.Fruit Tree Research Division, Agricultural Technology Research CenterHiroshima Prefectural Technology Research InstituteHiroshimaJapan

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