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Journal of Chemical Ecology

, 32:325 | Cite as

Impact of Botanical Pesticides Derived from Melia azedarach and Azadirachta indica Plants on the Emission of Volatiles that Attract Parasitoids of the Diamondback Moth to Cabbage Plants

  • Deidre S. Charleston
  • Rieta Gols
  • Kees A. Hordijk
  • Rami Kfir
  • Louise E. M. Vet
  • Marcel Dicke
Article

Abstract

Herbivorous and carnivorous arthropods use chemical information from plants during foraging. Aqueous leaf extracts from the syringa tree Melia azedarach and commercial formulations from the neem tree Azadirachta indica, Neemix 4.5®, were investigated for their impact on the flight response of two parasitoids, Cotesia plutellae and Diadromus collaris. Cotesia plutellae was attracted only to Plutella xylostella-infested cabbage plants in a wind tunnel after an oviposition experience. Female C. plutellae did not distinguish between P. xylostella-infested cabbage plants treated with neem and control P. xylostella-infested plants. However, females preferred infested cabbage plants that had been treated with syringa extract to control infested plants. Syringa extract on filter paper did not attract C. plutellae. This suggests that an interaction between the plant and the syringa extract enhances parasitoid attraction. Diadromus collaris was not attracted to cabbage plants in a wind tunnel and did not distinguish between caterpillar-damaged and undamaged cabbage plants. Headspace analysis revealed 49 compounds in both control cabbage plants and cabbage plants that had been treated with the syringa extract. Among these are alcohols, aldehydes, ketones, esters, terpenoids, sulfides, and an isothiocyanate. Cabbage plants that had been treated with the syringa extract emitted larger quantities of volatiles, and these increased quantities were not derived from the syringa extract. Therefore, the syringa extract seemed to induce the emission of cabbage volatiles. To our knowledge, this is the first example of a plant extract inducing the emission of plant volatiles in another plant. This interesting phenomenon likely explains the preference of C. plutellae parasitoids for cabbage plants that have been treated with syringa extracts.

Key Words

Botanical pesticides parasitoid behavior Plutella xylostella induced plant volatiles elicitor 

Notes

Acknowledgments

This research was carried out through a grant awarded under the IFS/KNAW Carolina MacGillavry Ph.D. Fellowship Program. The ARC-PPRI provided the working space and facilities. Staff of the ARC-PPRI insectary provided the insects used in the experiments. Elisa Garzo converted the wind tunnel sketch into digital format and Roland Mumm helped with the principal component analysis.

References

  1. Agelopoulos, N. G. and Keller, M. A. 1994. Plant-natural enemy association in the tritrophic system, Cotesia rubeculaPieris rapaeBrassiceae (Cruciferae) III: collection and identification of plant and frass volatiles. J. Chem. Ecol. 20:1955–1967.CrossRefGoogle Scholar
  2. Akol, A. M., Njagi, P. G. N., Sithanantham, S. and Mueke, J. M. 2003. Effects of two neem insecticide formulations on the attractiveness, acceptability and suitability of diamondback moth larvae to the parasitoid, Diadegma mollipla (Holmgren) (Hym., Ichneumonidae). J. Appl. Entomol. 127:325–331.CrossRefGoogle Scholar
  3. Alborn, T., Turlings, T. C. J., Jones, T. H., Steinhagen, G., Loughrin, J. H. and Tumlinson, J. H. 1997. An elicitor of plant volatiles form beet armyworm oral secretion. Science 276:945–949.CrossRefGoogle Scholar
  4. Arimura, G., Ozawa, R., Horiuchi, J., Nishioka, T., and Takabayashi, J. 2001. Plant–plant interactions mediated by volatiles emitted from plants infested by spider mites. Biochem. Syst. Ecol. 29:1049–1061.CrossRefGoogle Scholar
  5. Ascher, K. R. S., Schmutterer, H., Zebitz, C. P. W., and Naqvi, S. N. H. 1995. The Persian lilac or chinaberry tree: Melia azedarach L., pp. 605–642, in H. Schmutterer (ed.), The Neem Tree: Source of Unique Natural Products for Integrated Pest Management, Medicine, Industry and Other Purposes. VCH Verlagsgesellschaft, Weinheim.Google Scholar
  6. Boeke, S. J. 2002. Traditional African plant products to protect stored cowpeas against insect damage: the battle against the beetle. Ph.D. Thesis. Wageningen University, The Netherlands.Google Scholar
  7. Boeke, S. J., Sinzogan, A. A. C., de Almeida, R. P., de Boer, P. W. M., Jeong, G., Kossou, D. K., and van Loon, J. J. A. 2003. Side-effects of cowpea treatment with botanical insecticides on two parasitoids of Callosobruchus maculatus. Entomol. Exp. Appl. 108:43–51.CrossRefGoogle Scholar
  8. Charleston, D. 2004. Integrating biological control and botanical pesticides for management of Plutella xylostella. Ph.D. Thesis, Wageningen University, The Netherlands.Google Scholar
  9. Charleston, D., Kfir, R., Dicke, M., and Vet, L. E. M. 2005. Impact of botanical pesticides derived from Melia azedarach and Azadirachta indica on the biology of two parasitoid species of the diamondback moth. Biol. Contemp. 33:131–142.CrossRefGoogle Scholar
  10. Choh, Y., Shimoda, T., Ozawa, R., Dicke, M., and Takabayashi, J. 2004. Exposure of lima beans to volatiles from herbivore-induced conspecific plants results in emission of carnivore attractants: Active or passive process? J. Chem. Ecol. 30:1305–1317.PubMedCrossRefGoogle Scholar
  11. Dicke, M. 1994. Local and systemic production of volatile herbivore-induced terpenoids: their role in plant–carnivore mutualism. J. Plant Physiol. 143:465–472.Google Scholar
  12. Dicke, M. 1999a. Direct and indirect effects of plants on performance of beneficial organisms, pp. 105–153. in J. R. Ruberson (ed.). Handbook of Pest Management. Marcel Dekker, Inc. New York.Google Scholar
  13. Dicke, M. 1999b. Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomol. Exp. Appl. 91:131–142.CrossRefGoogle Scholar
  14. Dicke, M. and Vet, L. E. M. 1999. Plant–carnivore interactions: evolutionary and ecological consequences for plant, herbivore and carnivore, pp. 483–520, in H. Olff, V. K. Brown, and R. H. Drent (eds.). Herbivores: Between Plants and Predators. Blackwell Science Ltd., Oxford.Google Scholar
  15. Dicke, M. and Bruin, J. 2001. Chemical information transfer between plants: back to the future. Biochem. Syst. Ecol. 29:981–994.CrossRefGoogle Scholar
  16. Dicke, M., van Beek, T. A., Posthumus, M. A., Dom, N. B., van Bokhoven, H., and de Groot, A. E. 1990. 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
  17. Dicke, M., Gols, R., Ludeking, D., and Posthumus, M. A. 1999. Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. J. Chem. Ecol. 25:1907–1922.CrossRefGoogle Scholar
  18. Engelberth, J., Alborn, H. T., Schmelz, E. A., and Tumlinson, J. H. 2004. Airborne signals prime plants agaianst herbivore attack. Proc. Natl. Acad. Sci. U. S. A. 101:1781–1785.PubMedCrossRefGoogle Scholar
  19. Geervliet, J. B. F. 1997. Infochemical use by insect parasitoids in a tritrophic context: comparison of a generalist and a specialist. Ph.D. Thesis. Wageningen University, The Netherlands.Google Scholar
  20. Geervliet, JBF, Vet, L. E. M. and Dicke, M. 1996. Innate responses of the parasitoids Cotesia glomerata and C. rubecula (Hymenoptera: Braconidae) to volatiles from different plant–herbivore complexes. J. Insect Behav. 9:525–538.CrossRefGoogle Scholar
  21. Geervliet, J. B. F., Posthumus, M. A., Vet, L. E. M. and Dicke, M. 1997. Comparative analysis of headspace from different caterpillar-infested or uninfested food plants of Pieris species. J. Chem. Ecol. 23:2935–2954.CrossRefGoogle Scholar
  22. Geervliet, J. B. F., Vreugdenhil, A. I., Dicke, M., and Vet, L. E. M. 1998. Learning to discriminate between infochemicals from different plant–host complexes by the parasitoids Cotesia glomerata and C. rubecula. Entomol. Exp. Appl. 86:241–252.CrossRefGoogle Scholar
  23. Gohole, L. S., Overholt, W. A., Khan, Z. R., and Vet, L. E. M. 2003. Role of volatiles emitted by host and non-host plants in the foraging behaviour of Dentichasmias busseolae, a pupal parasitoid of the spotted stemborer Chilo partellus. Entomol. Exp. Appl. 107:1–10.CrossRefGoogle Scholar
  24. Gols, R., Posthumus, M. A., and Dicke, M. 1999. Jasmonic acid induces the production of gerbera volatiles that attract the biological control agent Phytoseiulus persimilis. Entomol. Exp. Appl. 93:77–86.CrossRefGoogle Scholar
  25. Gols, R., Roosjen, M., Dijkman H., and Dicke, M. 2003. Induction of direct and indirect plant responses by jasmonic acid, low spider mite densities, or a combination of jasmonic acid treatment and spider mite infestation. J. Chem. Ecol. 29:2651–2666.PubMedCrossRefGoogle Scholar
  26. Hatanaka, A. 1993. The biogeneration of green odour by green leaves. Phytochemistry 34:1201–1218.CrossRefGoogle Scholar
  27. Hilker, M. and Meiners, T. 2002. Induction of plant responses to oviposition and feeding by herbivorous arthropods: a comparison. Entomol. Exp. Appl. 104:181–192.CrossRefGoogle Scholar
  28. Horiuchi, J., Arimura, G., Ozawa, R., Shimoda, T., Takabayashi, J. and Nishioka, T. 2001. Exogenous ACC enhances volatile production mediated by jasmonic acid in lima bean leaves. FEBS Lett. 509:332–336PubMedCrossRefGoogle Scholar
  29. James, D. G. 2005. Further field evaluation of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. J. Chem. Ecol. 31:481–495PubMedCrossRefGoogle Scholar
  30. Kfir, R. 2003. Biological control of the diamondback moth Plutella xylostella in Africa, pp. 363–375, in P. Neuenschwander, C. Borgemeister, and J. Langewald (eds.). Biological Control in IPM systems in Africa. CABI Publishing, Wallingford, Oxon.Google Scholar
  31. Lecomte, C. and Pouzat, J. 1985. EAG responses of two ichneumonid parasitoids, Diadromus pulchellus and Diadromus collaris, to odours emitted by plants, the phytophagous-host Acrolepiopsis assectella and the sexual partner. Entomol. Exp. Appl. 39:295–306.Google Scholar
  32. Mattiacci, L., Dicke, M., and Posthumus, M. A. 1994. Induction of parasitoid attracting synomone in Brussels sprouts plants by feeding of Pieris brassicae larvae: role of mechanical damage and herbivore elicitor. J. Chem. Ecol. 20:2229–2247.CrossRefGoogle Scholar
  33. Mattiacci, L., Dicke, M., and Posthumus, M. A. 1995. beta-Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc. Natl. Acad. Sci. U. S. A. 92:2036–2040.PubMedCrossRefGoogle Scholar
  34. Mumm, R., Tiemann, T., Schulz, S., and Hilker, M. 2004. Analysis of volatiles from black pine (Pinus nigra): significance of wounding and egg deposition by a herbivorous sawfly. Phytochemistry 65:3221–3230.PubMedCrossRefGoogle Scholar
  35. Ozawa, R., Arimura, G., Takabayashi, J., Shimoda, T., and Nishioka, T. 2000. Involvement of jasmonate- and salicylate-related signaling pathways for production of specific herbivore-induced volatiles in plants. Plant Cell Physiol. 41:391–398.PubMedGoogle Scholar
  36. Ozawa, R., Shiojiri, K., Sabelis, M. W., Arimura, G. I., Nishioka, T., and Takabayashi, J. 2004. Corn plants treated with jasmonic acid attract more specialist parasitoids, thereby increasing parasitization of the common armyworm. J. Chem. Ecol. 30:1797–1808.PubMedCrossRefGoogle Scholar
  37. Pichersky, E. and Gershenzon, J. 2002. The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr. Opin. Plant Biol. 5:237–243.PubMedCrossRefGoogle Scholar
  38. Potting, R. P. J., Poppy, G. M., and Schuler, T. H. 1999. The role of volatiles from cruciferous plants and pre-flight experience in the foraging behaviour of the specialist parasitoid Cotesia plutellae. Entomol. Exp. Appl. 93:87–95.CrossRefGoogle Scholar
  39. Schmutterer, H. 1995. The Neem Tree: Source of Unique Natural Products for Integrated Pest Management, Medicine, Industry and Other Purposes. VCH Verlagsgesellschaft, Weinheim.Google Scholar
  40. Schmutterer, H. 1997. Side-effects of neem (Azadirachta indica) products on insect pathogens and natural enemies of spider mites and insects. J. Appl. Entomol. 121:121–128.CrossRefGoogle Scholar
  41. Schuler, T. H., Potting, R. P. J., Denholm, I., and Poppy, G. M. 1999. Parasitoid behaviour and Bt plants. Nature 400:825–826.PubMedCrossRefGoogle Scholar
  42. Schuler, T. H., Potting, R. P. J., Denholm, I., Clark, S. J., Clark, A. J., Stewart, C. N., and Poppy, G. M. 2003. Tritrophic choice experiments with Bt plants, the diamondback moth (Plutella xylostella) and the parasitoid Cotesia plutellae. Transgenic Res. 12:351–361.PubMedCrossRefGoogle Scholar
  43. Shiojiri, K., Takabayashi, J., Yano, S., and Takafuji, A. 2000a. Herbivore–species-specific interactions between crucifer plants and parasitic wasps (Hymenoptera: Braconidae) that are mediated by infochemicals present in areas damaged by herbivores. Appl. Entomol. Zool. 35:519–524.CrossRefGoogle Scholar
  44. Shiojiri, K., Takabayashi, J., Yano, S., and Takafuji, A. 2000b. Flight response of parasitoids toward plant–herbivore complexes: a comparative study of two parasitoid–herbivore systems on cabbage plants. Appl. Entomol. Zool. 35:87–92.CrossRefGoogle Scholar
  45. Shiojiri, K., Takabayashi, J., Yano, S., and Takafuji, A. 2001. Infochemically mediated tritrophic interaction webs on cabbage plants. Popul. Ecol. 43:23–29.CrossRefGoogle Scholar
  46. Smid, H. M., van Loon, J. J. A., Posthumus, M. A., and Vet, L. E. M. 2002. GC-EAG-analysis of volatiles from Brussels sprouts plants damaged by two species of Pieris caterpillars: olfactory receptive range of a specialist and a generalist parasitoid wasp species. Chemoecology 12:169–176.CrossRefGoogle Scholar
  47. Sokal, R. R and Rohlf, F. J. 1995. Biometry: The Principles and Practice of Statistics in Biological Research (3rd edition). W.H. Freeman and Company, New York.Google Scholar
  48. Steinberg, S., Dicke, M., Vet, L. E. M., and Wanningen, R. 1992. Response of the braconid parasitoid Cotesia (=Apanteles) glomerata (L.) to volatile infochemicals: effects of bioassay set-up, parasitoid age and experience and barometric flux. Entomol. Exp. Appl. 63:163–175.CrossRefGoogle Scholar
  49. Steinberg, S., Dicke, M., and Vet, L. E. M. 1993. Relative importance of infochemicals form first and second trophic level in long range host location by the larval parasitoid Cotesia glomerata. J. Chem. Ecol. 19:47–59.CrossRefGoogle Scholar
  50. Takabayashi, J., Dicke, M., and Posthumus, M. A. 1994. Volatile herbivore-induced terpenoids in plant–mite interactions: variation caused by biotic and abiotic factors. J. Chem. Ecol. 20:1329–1354.CrossRefGoogle Scholar
  51. Talekar, N. S. and Shelton, A. M. 1993. Biology, ecology, and management of the diamondback moth. Annu. Rev. Entomol. 38:275–301.CrossRefGoogle Scholar
  52. Thaler, J. S. 1999. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–688.CrossRefGoogle Scholar
  53. Turlings, T. C. J., Tumlinson, J. H., and Lewis, W. J. 1990. Exploitation of herbivore-induced plant odours by host-seeking parasitic wasps. Science 250:1251–1253.PubMedCrossRefGoogle Scholar
  54. 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: Ecological and Evolutionary Perspectives. Chapman & Hall, New York.Google Scholar
  55. Turlings, T. C. J., Loughrin, J. H., McCall, P. J., Röse, U., Lewis, W. J., and Tumlinson, J. H. 1995. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc. Natl. Acad. Sci. U. S. A. 92:4169–4174.PubMedCrossRefGoogle Scholar
  56. Vet, L. E. M. 1999. Evolutionary aspects of plant–carnivore interactions, pp. 3–13. in Insect–Plant Interactions and Induced Plant Defence. Novartis Foundation Symposium 223. John Wiley & Sons Ltd., Chichester.CrossRefGoogle Scholar
  57. Vet, L. E. M. and Dicke, M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37:141–172.CrossRefGoogle Scholar
  58. Vet, L. E. M., Wäckers, F. L., and Dicke, M. 1991. How to hunt for hiding hosts: the reliability–detectability probL. E. M. in foraging parasitoids. Neth. J. Zool. 41:202–213.CrossRefGoogle Scholar
  59. Vet, L. E. M., Lewis, W. J., and Cardé, R. T. 1995. Parasitoid foraging and learning, pp. 65–101, in W. Bell and R. T. Cardé (eds.). Chemical Ecology of Insects (2nd edn). Chapman & Hall, London.Google Scholar
  60. Vet, L. E. M., de Jong, A. G., Franchi, E., and Papaj, D. R. 1998. The effect of complete versus incomplete information on odour discrimination in a parasitic wasp. Anim. Behav. 55:1271–1279.PubMedCrossRefGoogle Scholar
  61. Visser, J. H. and Ave, D. A. 1978. General green leaf volatiles in the olfactory orientation of the Colarado beetle, Leptinotarsa decimlineata. Entomol. Exp. Appl. 24:738–749.CrossRefGoogle Scholar
  62. Vuorinen, T., Nerg, A. M., Ibrahim, M. A., Reddy, G. V. P., and Holopainen, J. K. 2004. Emission of Plutella xylostella-induced compounds from cabbages grown at elevated CO2 and orientation behavior of the natural enemies. Plant Physiol. 135:1984–1992.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2006

Authors and Affiliations

  • Deidre S. Charleston
    • 1
  • Rieta Gols
    • 2
  • Kees A. Hordijk
    • 3
  • Rami Kfir
    • 1
  • Louise E. M. Vet
    • 2
    • 3
  • Marcel Dicke
    • 2
  1. 1.Insect Ecology, Agricultural Research CouncilPlant Protection Research InstituteQueenswoodSouth Africa
  2. 2.Laboratory of Entomology, Department of Plant SciencesWageningen UniversityWageningenThe Netherlands
  3. 3.Netherlands Institute of Ecology, NIOO-CLMaarssenThe Netherlands

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