Advertisement

Journal of Chemical Ecology

, Volume 28, Issue 9, pp 1717–1732 | Cite as

Systemic Release of Herbivore-Induced Plant Volatiles by Turnips Infested by Concealed Root-Feeding Larvae Delia radicum L.

  • N. Neveu
  • J. Grandgirard
  • J. P. Nenon
  • A. M. Cortesero
Article

Abstract

When attacked by herbivorous insects, many plants emit volatile compounds that are used as cues by predators and parasitoids foraging for prey or hosts. While such interactions have been demonstrated in several host–plant complexes, in most studies, the herbivores involved are leaf-feeding arthropods. We studied the long-range plant volatiles involved in host location in a system based on a very different interaction since the herbivore is a fly whose larvae feed on the roots of cole plants in the cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae). The parasitoid studied is Trybliographa rapae Westwood (Hymenoptera: Figitidae), a specialist larval endoparasitoid of D. radicum. Using a four-arm olfactometer, the attraction of naive T. rapae females toward uninfested and infested turnip plants was investigated. T. rapae females were not attracted to volatiles emanating from uninfested plants, whether presented as whole plants, roots, or leaves. In contrast, they were highly attracted to volatiles emitted by roots infested with D. radicum larvae, by undamaged parts of infested roots, and by undamaged leaves of infested plants. The production of parasitoid-attracting volatiles appeared to be systemic in this particular tritrophic system. The possible factors triggering this volatile emission were also investigated. Volatiles from leaves of water-stressed plants and artificially damaged plants were not attractive to T. rapae females, while volatiles emitted by leaves of artificially damaged plants treated with crushed D. radicum larvae were highly attractive. However, T. rapae females were not attracted to volatiles emitted by artificially damaged plants treated only with crushed salivary glands from D. radicum larvae. These results demonstrate the systemic production of herbivore-induced volatiles in this host-plant complex. Although the emission of parasitoid attracting volatiles is induced by factors present in the herbivorous host, their exact origin remains unclear. The probable nature of the volatiles involved and the possible origin of the elicitor of volatiles release are discussed.

Trybliographa rapae Delia radicum tritrophic interactions host location herbivore-induced volatiles systemic release root-feeders olfactometer 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949.Google Scholar
  2. Birch, A. E. N., Griffiths, D. W., and MacFarlane Smith, W. H. 1990. Changes in forage and oilseed rape (Brassica napus) root glucosinolates in response to attack by turnip root fly (Delia floralis). J. Sci. Food Agric. 51:309–320.Google Scholar
  3. Birch, A. E. N., Griffiths, D. W., Hopkins, R. J., MacFarlane Smith, W. H., and McKinlay, R. G. 1992. Glucosinolates responses of swede, kale, forage and oilseed rape to root damage by turnip root fly (Delia floralis) larvae. J. Sci. Food Agric. 60:1–9.Google Scholar
  4. Bruin, J., Sabelis, M. W., and Dicke, M. 1995. Do plants tap SOS signals from their infested neighbors? TREE 10:167–170.Google Scholar
  5. Cortesero, A. M., De Moraes, C. M., Stapel, J. O., Tumlinson, J. H., and Lewis, W. J. 1997. Comparisons and contrasts in host-foraging strategies of two larval parasitoids with different degrees of host specificity. J. Chem. Ecol. 23:1589–1606.Google Scholar
  6. Couty, A., Kaiser, L., Huet, D., and Pham-Delegue, M. H. 1999. The attractiveness of different odour sources from the fruit-host complex on Leptopilina boulardi, a larval parasitoid of frugivorous Drosophila spp. Physiol. Entomol. 24:76–82.Google Scholar
  7. Dicke, M. 1999a. Evolution of induced indirect defense of plants, pp. 62–88, in R. Tollrian and C. D. Harvell (eds.). The Ecology and Evolution of Inducible Defenses. Princeton University Press, Chichester, United Kingdom.Google Scholar
  8. Dicke, M. 1999b. Specificity of herbivore-induced plant defences, pp. 43–59, in D. J. Chadwick and J. Goode (eds.). Insect-Plant Interactions and Induced Plant Defence. Novartis Foundation Symposium 223, Wiley, Chichester, United Kingdom.Google Scholar
  9. Dicke, M. and Sabelis, M.W. 1988. How plants obtain predatory mites as bodyguards. Neth. J. Zool. 38:148–165.Google Scholar
  10. Dicke, M. and VanLoon, J. J. A. 2000. Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol. Exp. Appl. 97:237–249.Google Scholar
  11. 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. Olf, V. K. Brown, and R. H. Drent (eds.). Herbivores: Between Plants and Predators. Oxford University Press, Oxford, United Kingdom.Google Scholar
  12. Dicke, M., Sabellis, M. W., Takabayashi, J., Bruin, J., and Posthumus, M. A. 1990. Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. J. Chem. Ecol. 16:3091–3118.Google Scholar
  13. Dicke, M., Van Baarlen, P., Wessels, R, and Dijkman, H. 1993. Herbivory induces systemic production of plant volatiles that attract predators of the herbivore: Extraction of endogenous elicitor. J. Chem. Ecol. 19:581–599.Google Scholar
  14. Doane, J. F. and Chapman, R. K 1964. Development of the cabbage maggot Hylemyia brassicae (Bouché) on aseptic and decaying rutabaga tissue. Entomol. Exp. Appl. 115:119.Google Scholar
  15. Doughty, K. J., Blight, M. M., Bock, C. H., Fieldsend, J. K., and Pickett, J. A. 1996. Release of alkenyl isothiocyanates and other volatiles from Brassica rapa seedlings during infection by Alternaria brassicae. Phytochemistry 43:371–374.Google Scholar
  16. Drukker, B., Scutareanu, P., and Sabelis, M. W. 1995. Do anthocorid predators respond to synomones from Psylla-infested pear trees under field conditions. Enomol. Exp. Appl. 77:193–203.Google Scholar
  17. Du, Y. J., Poppy, G. M., and Powell, W. 1996. Relative importance of semiochemials from first and second trophic levels in host foraging behavior of Aphidius ervi. J. Chem. Ecol. 22:1591–1605.Google Scholar
  18. Dutton, A., Mattiacci, L., and Dorn, S. 2000. Learning used as a strategy for host stage location in an endophytic host-parasitoid system. Entomol Exp. Appl. 94:123–132.Google Scholar
  19. Felton, G. W. and Eichenseer, H. 1999. Herbivore saliva and its effects on plant defense against herbivores and pathogens, pp. 19–36, in A. A. Agrawal, S. Tuzun, and E. Bent (eds.). Induced Plant Defenses Against Pathogens and Herbivores.Google Scholar
  20. Finidori-Logli, V., Bagneres, A. G., and Clement, J. L. 1996. Role of plant volatiles in the search for a host by parasitoid Diglyphus isaea (Hymenoptera: Eulophidae). J. Chem. Ecol. 22:541–558.Google Scholar
  21. Geervliet, J. B. F., Vet, L. E. M., and Dicke, M. 1994. Volatiles from damaged plants as major cues in long-range host-searching by the specialist parasitoid Cotesia rubecula. Entomol. Exp. Appl. 73:289–297.Google Scholar
  22. GrassÉ, P. P. 1951. Traité de Zoologie. Insectes supérieurs et Hémiptéröýdes. Tome 10. Fascicule 1. Masson et Cie. Paris, pp. 975.Google Scholar
  23. Guerrieri, E., Pennachio, F., and Tremblay, E. 1993. Flight behaviour of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae) in response to plant and host volatiles. Eur. J. Entomol. 90:415–421.Google Scholar
  24. 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
  25. Halitschke, R., Schittko, U., Pohnert, G., Boland, W., and Baldwin, I. T. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol. 125:711–717.Google Scholar
  26. Hopkins, R. J., Griffiths, D. W., Birch, A. E. N., McKinlay, R. G., and Hall, J. E. 1993. Relationships between turnip root fly (Delia floralis) larval development and the sugar content of swede (Brassica napus ssp. rapifera) roots. Ann. Appl. Biol. 122:405–415.Google Scholar
  27. Hopkins, R. J., Birch, A. E. N., Griffiths, D. W., Morrison, I. M., and McKinlay, R. G. 1995. Changes in the dry matter, sugar, plant fibre and lignin contents of swede, rape and kale roots in response to turnip fly (Delia floralis) larval damage. J. Sci. Food Agric. 69:321–328.Google Scholar
  28. Johnson, D. E. 1930. The relation of the cabbage maggot and other insects to the spread and development of soft rot of Cruciferae. Phytopathology 20:857–872.Google Scholar
  29. Jones, T. H. 1986. The biology of host and parasitoid. Patterns of parasitism by Trybliographa Rapae Westw., a cynipid parasitoid of the cabbage root fly. PhD dissertation. University of London, United Kingdom.Google Scholar
  30. 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 damaged and herbivore elicitor. J. Chem. Ecol. 20:2229–2247.Google Scholar
  31. Mattiacci, L., Dicke, M., and Posthumus, M. A. 1995. Ø-glucosidase: an elicitor of herbivoreinduced plant odor that attracts host-searching parasitic wasps. Proc. Natl. Acad. Sci. USA 92:2036–2040.Google Scholar
  32. McAuslane, H. J., Vinson, S. B., and Williams, H. J. 1991. Stimuli influencing host microhabitat location in the parasitoid Campoletis sonorensis. Entomol. Exp. Appl. 58:267–277.Google Scholar
  33. Mori, N., Alborn, H. T., Teal, P. E. A., and Tumlinson, J. H. 2001. Enzymatic decomposition of elicitors of plant volatiles in Heliothis virescens and Helicoverpa zea. J. Insect Physiol. 47:749–757.Google Scholar
  34. Neveu, N., Kacem, N. and Nenon, J. P. 1996. A method for rearing Trybliographa rapae W. on Delia radicum L. OILB/SROP Bull. 19:173–178.Google Scholar
  35. Petitt, F. L. Turlings, T. C. J., and Wolf, S. P. 1992. Adult experience modifies attraction of the leafminer parasitoid Opius dissitus (Hymenoptera: Braconidae) to volatile semiochemicals. J. Insect Behav. 5: 623–634.Google Scholar
  36. Pettersson, J. 1970. An aphid sex attractant. I. Biological studies. Entomol. Scand. 1:63–73.Google Scholar
  37. Pickett, J. A., Chamberlain, K., Poppy, G. M., and Woodcock, C. M. 1999. Exploiting insect responses in identifying plant signals, pp. 253–65, in D. J. Chadwick and J Goode (eds.). Insect-Plant Interactions and Induced Plant Defence.Novartis Foundation Symposium 223,Wiley, Chichester, United Kingdom.Google Scholar
  38. Pohnert, G., Koch, T., and Boland, W. 1999. Synthesis of volicitin: a novel three component Wittig approach to chiral 17-hydroxylinolenic acid. Chem. Commun. 12:1087–1088.Google Scholar
  39. Potting, R. P. J., Vet, L. E. M., and Dicke, M. 1995. Host microhabitat location by stem-borer parasitoid Cotesia flavipes: the role of herbivore volatiles and locally and systemically induced plant volatiles. J. Chem. Ecol. 21:525–539.Google Scholar
  40. Potting, R. P. J., Poppy, G. M., and Schuler, T. H. 1999. The role of volatiles from cruciferous plants and preflight experience in the foraging behaviour of the specialist parasitoid Cotesia plutellae. Entomol. Exp. Appl. 93:87–95.Google Scholar
  41. RÖse, U. S. R., Manukian, A., Heath, R. R., and Tumlinson, J. H. 1996. Volatile semiochemicals released from undamaged cotton leaves:Asystemic response of living plants to caterpillar damage. Plant Physiol. 111:487–495.Google Scholar
  42. Sabelis, M., Janssen, A., Pallini, A., Venzon, M., Bruin, J., Drukker, B., and Scutareanu, P. 1999. Behavioral responses of predatory and herbivorous arthropods to induced plant volatiles: from evolutionary ecology to agricultural applications, pp. 269–296, in A. A. Agrawal, S. Tuzun and E. Bent (eds.). Induced Plant Defenses Against Pathogens and Herbivores. APS Press, Saint Paul, Minnesota.Google Scholar
  43. Steidle, J. L. M. and SchÖller, M. 1997. Olfatory host location and learning in the granary weevil parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). J. Insect Behav. 10: 331–342.Google Scholar
  44. 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. 19:47–58.Google Scholar
  45. Takabayashi, J. and Dicke, M. 1996. Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci. 1:109–113.Google Scholar
  46. 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.Google Scholar
  47. Tamer, A. 1994. Laboratory investigations of the relationships between the cabbage root fly Delia radicum and its parasitoid, Trybliographa rapae. OILB/SROP Bull. 17:148–152.Google Scholar
  48. Tumlinson, J. H., Turlings, T. C. J., and Lewis, W. J. 1992. The semiochemicals complexes that mediate insect parasitoid foraging. Agric. Zool. Rev. 5:221–252.Google Scholar
  49. Tumlinson, J. H., Pare, P.W., and Lewis, W. J. 1999. Plant production of volatile semiochemicals in response to insect-derived elicitors, pp. 95–109, in D. J. Chadwick and J. Goode (eds.). Insect-Plant Interactions and Induced Plant Defence. Novartis Foundation Symposium 223,Wiley, Chichester, United Kingdom.Google Scholar
  50. 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
  51. Turlings, T. C. J. and Tumlinson, J. H. 1992. Systemic release of chemical signals by herbivoreinjured corn. Proc. Natl. Acad. Sci. USA 89:8399–8402.Google Scholar
  52. Turlings, T. C. J., Tumlinson, J. H., and Lewis, W. J. 1990. Exploitation of herbivore-induced plant volatiles by host-seeking parasitic wasps. Science 250:1251–1253.Google Scholar
  53. Turlings, T. C. J., McCall, P. J., Alborn, H. T., and Tumlinson, J.H. 1993. An elicitor in caterpillar oral secretions that induces corn seedlings to emit chemicals attractive to parasitic wasps. J. Chem. Ecol. 19:411–425.Google Scholar
  54. 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. USA 92:4169–4174.Google Scholar
  55. Turlings, T. C. J., Alborn, H. T., Loughrin, J. H., and Tumlinson, J. H. 2000. Volicitin, an elicitor of maize volatiles in oral secretion of Spodoptera exigua: isolation and bioactivity. J. Chem. Ecol. 26:189–202.Google Scholar
  56. Van Alphen, J. J. M. and Jervis, M. A., 1996. Foraging behavior. pp. 1–62, in M. Jervis and N. Kidd (eds.). Insect Natural Enemies. Practical Approaches to Their Study and Evaluation. Chapman and Hall, London.Google Scholar
  57. Van Der Meijden, E. and Klinkhamer, P. G. L. 2000. Conflicting interests of plants and the natural enemies of herbivores. Oikos 89:202–208.Google Scholar
  58. Van Loon, J. J. A., DeBoer, J. G., and Dicke, M. 2000. Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction. Entomol. Exp. Appl. 97:219–227.Google Scholar
  59. Vet, L. E. M. 1985. Olfactory microhabitat location in some Eucoilid and Alysiine species (Hymenoptera), larval parasitoids of Diptera. Neth. J. Zool. 35:720–730.Google Scholar
  60. 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.Google Scholar
  61. Vet, L. E. M. and Van Alphen, J. J. M. 1985. A comparative functional approach to the host detection behaviour of parasitic wasps.1. A qualitative study on Eucoilidae and Alysiinae. Oikos 44:478–486.Google Scholar
  62. Vet, L. E. M., Van Lenteren, J. C., Heymans, M., and Meelis, E. 1983. An airflow olfactometer to measuring olfactory responses of hymenopterous parasitoids and other small insects. Physiol. Entomol. 8:97–106.Google Scholar
  63. Vet, L. E. M., WÄckers, F. L., and Dicke, M. 1991. How to hunt for hiding hosts: the reliabilitydetectability problem in foraging parasitoids. Neth. J. Zool. 41:202–213.Google Scholar
  64. Vinson, S. B. 1991. Chemical signals used by parasitoids, pp. 15–42, in F. Bin (ed.). Insect Parasitoids, 4th European Workshop-Perugia, 3-5 April, 1991 REDIA Vol 74 “Appendice.”Google Scholar
  65. Whitman, D. W. and Eller, F. J. 1990. Parasitic wasps orient to green leaf volatiles. Chemoecology 1:69–75.Google Scholar
  66. Wishart, G. 1957. Surveys of parasites of Hylemya spp. (Diptera: Anthomyiidae) that attack cruciferous crops in Canada. Can. Entomol. 89:450–455.Google Scholar
  67. Wishart, G. and Monteith, E. 1954. Trybliographa rapae (Westw.) (Hymenoptera: Cynipidae), a parasite of Hylemya spp. (Diptera: Anthomyiidae). Can. Entomol. 4:145–155.Google Scholar
  68. Wishart, G., Colhoun, E. H., and Monteith, A. E. 1957. Parasites of Hylemya spp. (Diptera: Anthomyiidae) that attack cruciferous crops in Europe. Can. Entomol. 89: 510–517.Google Scholar

Copyright information

© Plenum Publishing Corporation 2002

Authors and Affiliations

  • N. Neveu
    • 1
  • J. Grandgirard
    • 1
  • J. P. Nenon
    • 1
  • A. M. Cortesero
    • 1
  1. 1.Laboratoire d'Ecobiologie des Insectes ParasitoïdesUniversité de Rennes 1Rennes cedexFrance

Personalised recommendations