Advertisement

Journal of Chemical Ecology

, Volume 30, Issue 5, pp 945–964 | Cite as

Identification of Volatile Synomones, Induced by Nezara viridula Feeding and Oviposition on Bean spp., That Attract the Egg Parasitoid Trissolcus basalis

  • Stefano Colazza
  • J. Steven McElfresh
  • Jocelyn G. Millar
Article

Abstract

Bean plants (Vicia faba L. and Phaseolus vulgaris L.) damaged by feeding activity of Nezara viridula (L.) (Heteroptera: Pentatomidae), and onto which an egg mass had been laid, produced volatiles that attracted the egg parasitoid Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae). Extracts of volatiles of broad bean and French bean plants induced by adults of N. viridula as a result of their feeding activity, oviposition activity, and feeding and oviposition activity combined were analyzed by gas chromatography–mass spectrometry (GC–MS), and tested in Y-tube olfactometer bioassays as attractants for T. basalis females. In extracts from undamaged leguminous plants, green-leaf volatiles were absent or scarcely detected, and monoterpenes and sesquiterpenes were present at trace levels. No significant differences were detected in the profiles of volatiles of undamaged plants, and undamaged plants on which bugs were allowed only to lay eggs. In contrast, feeding and oviposition by adults of N. viridula induced in both leguminous plants a significant increase in terpenoids such as linalool, (E)-β-caryophyllene, (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene, and (3E)-4,8-dimethyl-1,3,7-nonatriene, which was induced only in French bean plants. Quantitative comparisons revealed increased levels of (E)-β-caryophyllene in extracts from feeding-damaged plants with N. viridula egg masses compared to feeding-damaged plants without egg masses. In Y-tube olfactometer bioassays, T. basalis females were attracted by extracts of both leguminous plants only when N. viridula adults were allowed to feed and oviposit upon them. Fractionation of extracts of volatiles from broad bean plants with N. viridula feeding damage and egg masses yielded two fractions, but only the fraction containing (E)-β-caryophyllene was attractive to the egg parasitoid. These findings indicate that N. viridula feeding and oviposition induce leguminous plants to produce blends of volatiles that are characterized by increased amounts of (E)-β-caryophyllene, and these blends attract female T. basalis. The role of (E)-β-caryophyllene as a potential synomone for T. basalis is discussed.

Legume Insecta Heteroptera Pentatomidae Scelionidae egg parasitoid oviposition-induced synomone terpenoid (E)-β-caryophyllene 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. Agelopoulos, N. G., Hooper, A. M., Maniar, S. P., Pickett, J. A., and Wadhams, L. J. 1999. A novel approach for isolation of volatile chemicals released by individual leaves of a plant in situ. J. Chem. Ecol. 25:1411–1425.Google Scholar
  2. Baldwin, I. T. and Preston, C. A. 1999. The eco-physiological complexity of plant responses to insect herbivores. Planta 208:137–145.Google Scholar
  3. Bernasconi, M. L., Turlings, T. C. J., Ambrosetti, L., Bassetti, P., and Dorn, S. 1998. Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis. Entomol. Exp. Appl. 87:133–142.Google Scholar
  4. Bichao, H., Borg-Karlson, A. K., Araujo, J., and Mustaparta, H. 2003. Identification of plant odours activating receptor neurones in the weevil Pissodes notatus F. (Coleoptera, Curculionidae). J. Comp. Physiol. 189:203–212.Google Scholar
  5. Boland, W., Koch, T., Krumm, T., Piel, J., and Jux, A. 1999. Induced biosynthesis of insect semiochemicals in plants, pp. 110–126, in D. J.Chadwick and J. A.Goode (eds.). Insect-Plant Interactions and Induced Plant Defence. Novartis Foundation Symposium 223. Wiley, Chicester, England.Google Scholar
  6. Colazza, S. and Bin, F. 1995. Efficiency of Trissolcus basalis (Hymenoptera: Scelionidae) as an egg parasitoid of Nezara viridula (Heteroptera: Pentatomidae) in central Italy. Environ. Entomol. 24:1703–1707.Google Scholar
  7. Colazza, S., Fucarino, A., Peri, E., Salerno, G., Conti, E., and Bin, F. 2004. Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. J. Exp. Biol. 207:47–53.Google Scholar
  8. Colazza, S., Cxeri, D., Peri, E., Lo Pinto, M., and Liotta, G. 1999a. A video tracking and motion analysis system for LINUX, in XII Int. Entomoph. Insect Workshop, Asilomar, CA, Sept. 26–30, 1999.Google Scholar
  9. Colazza, S. and Pompanon, F. 1994. Ritmo giornaliero dell'attività locomotoria degli adulti di Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae), pp. 647–650, in Atti XVII Congr. Naz. It. di Entomol., Udine 13-18 giugno 1994.Google Scholar
  10. Colazza, S., Rosi, M. C., and Clemente, A. 1997. Response of the egg parasitoid Telenomus busseolae to sex pheromone of Sesamia nonagrioides. J. Chem. Ecol. 23:2437–2444.Google Scholar
  11. Colazza, S., Salerno, G., and Wajnberg, E. 1999b. Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biol. Control 16:310–317.Google Scholar
  12. Cortesero, A. M., Stapel, J. O., and Lewis, W. J. 2000. Understanding and manipulating plant attributes to enhance biological control. Biol. Control 17:35–49.Google Scholar
  13. Degenhardt, J., Gershenzon, J., Baldwin, I. T., and Kessler, A. 2003. Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Cur. Opin. Biotechnol. 14:169–176.Google Scholar
  14. De Moraes, C. M., Lewis, W. J., Paré, P. W., Alborn, H. T., and Tumlinson, J. H. 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573.Google Scholar
  15. Dicke, M. 1999. Evolution of induced indirect defense of plant, pp. 62–88, in R. Tollrian and C. D. Harvell (eds.). The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton, NJ.Google Scholar
  16. Dicke, M. 2000. Chemical ecology of host-plant selection by herbivorous arthropods: A multitrophic perspective. Biochem. System. Ecol. 28:601–617.Google Scholar
  17. Dicke, M. andvan Loon, J. J. A. 2000. Multi-trophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol. Exp. Appl. 97:327–249.Google Scholar
  18. Donath, J. and Boland, W. 1995. Biosynthesis of acyclic homoterpenes: Enzyme selectivity and absolute configuration of the nerolidol precursor. Phytochemistry 39:785–790.Google Scholar
  19. Du, Y., Poppy, G. M., Powell, W., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1998. Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J. Chem. Ecol. 24:1355–1368.Google Scholar
  20. Elzen, G. W., Williams, H. J., and Vinson, S. B. 1984. Isolation and identification of cotton synomones mediating searching behavior by parasitoid Campolitis sonorensis. J. Chem. Ecol. 10:1251–11263.Google Scholar
  21. Flint, H. M., Salter, S. S., and Walters, S. 1979. Caryophyllene: An attractant for the green lacewing. Environ. Entomol. 8:1123–1125.Google Scholar
  22. Gäbler, A., Boland, W., Preiss, H., and Simon, H. 1991. Stereochemical studies on homoterpene biosynthesis in higher plants: mechanistic, phylogenetic, and ecological aspects. Helv. Chim. Acta 74:1773–1789.Google Scholar
  23. Gatehouse, J. A. 2002. Plant resistance towards insect herbivores: A dynamic interaction. New Phytol. (Tansley review no. 140) 156:145–169.Google Scholar
  24. Gouinguene, S. P. and Turlings, T. C. J. 2002. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol. 129:1296–1307.Google Scholar
  25. Guerrieri, E., Poppy, G. M., Powell, W., Tremblay, E., and Pennachio, F. 1999. Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi. J. Chem. Ecol. 25:1247–1261.Google Scholar
  26. Hilker, M., Kobs, C., Varama, M., and Schrank, K. 2002b. Insect egg deposition induces Pinus to attract egg parasitoids. J. Exp. Biol. 205:455–461.Google 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.Google Scholar
  28. Hilker, M., Rohfritsch, O., and Meiners, T. 2002a. The plant's response towards insect egg deposition, pp. 205–233, in M.Hilker and T.Meiners (eds.). Chemoecology of Insect Eggs and Egg Deposition. Blackwell, Berlin.Google Scholar
  29. Jones, W. A. 1988. World review of the parasitoids of the southern green stink bug, Nezara viridula (L.). Ann. Entomol. Soc. Am. 81:262–273.Google Scholar
  30. Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. The University Press of Chicago, Chicago.Google Scholar
  31. Mattiacci, L., Vinson, S. B., Williams, H. J., Aldrich, J. R., and Bin, F. 1993. A long-range attractant kairomone for the egg parasitoid Trissolcus basalis, isolated from defensive secretion of its host, Nezara viridula. J. Chem. Ecol. 19:1167–1181.Google Scholar
  32. Meiners, T. and Hilker, M. 2000. Induction of plant synomones by oviposition of a phytophagous insect. J. Chem. Ecol. 26:221–232.Google Scholar
  33. Mumm, R., Schrank, K., Wegener, R., Schulz, S., and Hilker, M. 2003. Chemical analysis of volatiles emitted by Pinus sylvestris after induction by insect oviposition. J. Chem. Ecol. 29:1235–1252.Google Scholar
  34. Paré, P. W. and Tumlinson, J. H. 1997. De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol. 114:1161–1167.Google Scholar
  35. Paré, P. W. and Tumlinson, J. H. 1999. Plant volatiles as a defense against insect herbivores. Plant Physiol. 121:325–332.Google Scholar
  36. Potting, R. P. J., Vet, L. E. M., and Dicke, M. 1995. Host microhabitat location by the stemborer parasitoid Cotesia flavipes: The role of locally and systemically induced plant volatiles. J. Chem. Ecol. 21:525–539.Google Scholar
  37. Rodriguez-Saona, C., Crafts-Brandner, S., Williams, L.,III, and Paré, P. W. 2002. Lygus hesperus feeding and salivary gland extracts induce volatile emission in plants. J. Chem. Ecol. 28:1733–1747.Google Scholar
  38. SPSS Inc. 2001. SPSS for Windows, Standard Version. SPSS Inc. Wacker Drive, Chicago.Google Scholar
  39. Steinberg, S., Dicke, M., and Vet, L. E. M. 1993. Relative importance of infochemicals from first and second trophic level in long-range host location by the larval parasitoid Cotesia glomerata. J. Chem. Ecol. 19:47–59.Google Scholar
  40. Takabayashi, J. and Dicke, M. 1996. Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci. 1:109–113.Google Scholar
  41. Todd, J. W. 1989. Ecology and behavior of Nezara viridula. Annu. Rev. Entomol. 34:273–292.Google Scholar
  42. Tumlinson, J. H., Lewis, W. J., and Vet, L. E. M. 1993a. How parasitic wasps find their hosts. Sci. Am. 268:100–106.Google Scholar
  43. Tumlinson, J. H., Turlings, T. C. J., and Lewis, W. J. 1993b. Semiochemically mediated foraging behavior in beneficial parasitic insects. Arch. Insect. Biochem. Physiol. 22:385–391.Google Scholar
  44. Turlings, T. C. J. and Benrey, B. 1998. Effects of plant metabolites on the behavior and development of parasitic wasps. Ecoscience 5:3241–3333.Google Scholar
  45. Turlings, T. C. J., Bernasconi, M., Bertossa, R., Bigler, F., Caloz, G., and Dorn, S. 1998. The induction of volatile emissions in maize by three herbivore species with different feeding habits—possible consequences for their natural enemies. Biol. Control 11:122–129.Google Scholar
  46. Turlings, T. C. J., Loughrin, J. H., McCall, P. J., Röse, U. S. R., 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.Google Scholar
  47. Turlings, T. C. J. and Tumlinson, J. H. 1992. Systemic release of chemical signals by herbivore injured maize. Proc. Natl. Acad. Sci. U.S.A. 89:8399–8402.Google Scholar
  48. Turlings, T. C. J., Tumlinson, J. H., and Lewis, W. J. 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253.Google Scholar
  49. Vinson, S. B. 1985. The behavior of parasitoids, pp. 417-469, in G. A. Kerkut and L. I. Gilbert (eds.). Comprehensive Insect Physiology, Biochemistry, and Pharmacology, vol. 9. Pergamon Press, Elmsford, New York.Google Scholar
  50. Vinson, S. B. 1998. The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol. Control 11:79–96.Google Scholar
  51. Wegener, R. and Schulz, S. 2002. Identification and synthesis of homoterpenoids emitted from elm leaves after elicitation by beetle eggs. Tetrahedron 58:315–319.Google Scholar
  52. Wegener, R., Schulz, S., Meiners, T., Hadwich, K., and Hilker, M. 2001. Analysis of volatiles induced by oviposition of elm leaf beetle Xanthogaleruca luteola on Ulmus minor. J. Chem. Ecol. 27:499–515.Google Scholar

Copyright information

© Plenum Publishing Corporation 2004

Authors and Affiliations

  • Stefano Colazza
    • 1
  • J. Steven McElfresh
    • 1
  • Jocelyn G. Millar
    • 2
  1. 1.S.En.Fi.MI.Zo. Department, Entomology, Zoology, and AcarologyUniversità di PalermoPalermoItaly
  2. 2.Department of EntomologyUniversity of CaliforniaRiversideUSA

Personalised recommendations