A comparison of naïve and conditioned responses of three generalist endoparasitoids of lepidopteran larvae to host-induced plant odours

Animal Biology

Volumn 56, Issue 2, 2006, Pages 205-220

  Tamò, Cristina ^a   Ricard, Ingrid ^b   Held, Matthias ^a   Davison, Anthony C ^b   Turlings, Ted C J ^a  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^b EPFL   (Switzerland)

Author keywords

Associative learning; Herbivore induced plant odours; Host finding; Parasitoids

Indexed keywords

CONDITIONING; HERBIVORE; ODOR; PARASITOID;

BRACONIDAE; CAMPOLETIS SONORENSIS; COTESIA; COTESIA MARGINIVENTRIS; GOSSYPIUM HIRSUTUM; HYMENOPTERA; ICHNEUMONIDAE; LEPIDOPTERA; MICROPLITIS RUFIVENTRIS; VESPOIDEA; VIGNA UNGUICULATA; ZEA MAYS;

EID: 33747890241     PISSN: 15707555     EISSN: None     Source Type: Journal    
DOI: 10.1163/157075606777304177     Document Type: Article

References (57)

1. Abou Zeid, N.A., El-Dakroury, M.S.I., El-Heneidy, A.H. & Abbas, M.S.T. (1978) Biology of Microplitis rufiventris Kok. parasitizing Heliothis armigera Hb. in Egypt. Agric. Res. Rev. (Cairo), 56, 31-36.
2. Altahtawy, M.M., Hammad, S.M. & Hegazi, E.M. (1976a) Studies on the dependence of Microplitis rufiventris Kok (Hym, Braconidae) parasitizing Spodoptera littoralis (Boisd) on own food as well as on food of its host. Z. Angew. Entomol.-J. Appl. Entomol., 81, 3-13.
3. Altahtawy, M.M., Hegazi, E.M. & Hammad, S.M. (1976b) Convenience of ages and instars of Spodoptera littoralis (Boisd) larvae for Microplitis rufiventris Kok - Mass rearing and biological-control of Cotton Leafworm. Z. Angew. Entomol.-J. Appl. Entomol., 81, 270-285.
4. Baehrecke, E.H., Vinson, S.B. & Williams, H.J. (1990) Foraging behavior of Campoletis sonorensis in response to Heliothis virescens and cotton plants. Entomol. Exp. Appl., 55, 47-57.
5. Brown, E.S. & Dewhurst, C.F. (1975) The genus Spodoptera (Lepidoptera, Noctuidae), in Africa and the Near East. Bull. Entomol. Res., 65, 221-262.
6. D'Alessandro, M. & Turlings, T.C.J. (2005) In situ modification of herbivore-induced plant odours: A novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. Chem. Senses, 30, 1-15.
7. D'Alessandro, M. & Turlings, T.C.J. (2006) Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. The Analyst, 131, 24-32.
8. Degenhardt, J., Gershenzon, J., Baldwin, I.T. & Kessler, A. (2003) Attracting friends to feast on foes: Engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr. Opin. Biotechnol., 14, 169-176.
9. Dmoch, J., Lewis, W.J., Martin, P.B. & Nordlund, D.A. (1985). Role of host-produced stimuli and learning in host selection behavior of Cotesia (= Apanteles) marginiventris (Cresson) (Hymenoptera, Braconidae). J. Chem. Ecol., 11, 453-463.
10. Drost, Y.C., Lewis, W.J., Zanen, P.O. & Keller, M.A. (1986) Beneficial arthropod behavior mediated by airborne semiochemicals. 1. Flight behavior and influence of preflight handling of Microplitis croceipes (Cresson). J. Chem. Ecol., 12, 1247-1262.
11. El-Minshawy, A.M. (1963) Studies on the morphology and biology of Spodoptera exigua Hb. and Spodoptera latebrosa. Faculty of Agriculture, Dissertation, University of Alexandria.
12. Eller, F.J., Tumlinson, J.H. & Lewis, W.J. (1992) Effect of host diet and preflight experience on the flight responses of Microplitis croceipes (Cresson). Physiol. Entomol., 17, 235-240.
13. Elzen, G.W., Williams, H.J. & Vinson, S.B. (1986) Wind-tunnel flight responses by Hymenopterous parasitoid Campoletis sonorensis to cotton cultivars and lines. Entomol. Exp. Appl., 42, 285-289.
14. Geervliet, J.B.F., Vreugdenhil, A.I., Dicke, M. & 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.
15. Gerling, D. (1969) The parasites of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae) eggs and larvae in Israel. Isr. J. Entomol., 4, 73-81.
16. Hammad, S.M., El-Minshawy, A.M. & Salama, A. (1965) Studies on Microplitis rufiventris Kok. (Hym., Braconidea). Bull Soc. Entomol. Egypte, 49, 215-219.
17. Gouinguené, S., Pickett, J.A., Wadhams, L.J., Birkett, M.A. & Turlings, T.C.J. (2005) Antennal electrophysiological responses of three parasitic wasps to the caterpillar-induced volatiles from maize, cowpea and cotton. J. Chem. Ecol., 31, 1023-1038.
18. Hegazi, E.M., Elminshawy, A.M. & Hammad, S.M. (1977) Suitability of Spodoptera littoralis larvae for development of Microplitis rufiventris. J. Agric. Sci., 89, 659-662.
19. Hegazi, E.M., Hammad, S.M., Altahtawy, M.M. & El-Sawaf, S.K. (1973) Parasites of the larval stage of the cotton leaf-worm Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae) in Alexandria region. Z. Angew. Entomol.-J. Appl. Entomol., 74, 332-336.
20. Hegazi, E.M. & Shabaan, M.A. (1984) Competition and the superparasitism of Spodoptera littoralis (Boisd.) larvae by Microplitis rufiventris Kok. J. Agric. Sci., 103, 181-187.
21. Hérard, F., Keller, M.A., Lewis, W.J. & Tumlinson, J.H. (1988) Beneficial arthropod behavior mediated by airborne semiochemicals. 4. Influence of host diet on host-oriented flight chamber responses of Microplitis demolitor Wilkinson (Hymenoptera, Braconidae). J. Chem. Ecol., 14, 1597-1606.
22. Hoballah, M.E., Degen, T., Bergvinson, D., Savidan, A., Tamò, C. & Turlings, T.C.J. (2004) Occurrence and direct control potential of parasitoids and predators of the fall armyworm (Lepidoptera: Noctuidae) on maize in the subtropical lowlands of Mexico. Agric. For. Entomol., 6, 83-88.
23. Hoballah, M.E. & Turlings, T.C.J. (2005) The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J. Chem. Ecol., 31, 2003-2018.
24. Hoballah, M.E.F., Tamo, C. & Turlings, T.C.J. (2002) Differential attractiveness of induced odors emitted by eight maize varieties for the parasitoid Cotesia marginiventris: Is quality or quantity important? J. Chem. Ecol., 28, 951-968.
25. Hodges, R.W., Dominick, T., Davis, D.R., Ferguson, D.C., Franclemont, J.G., Munroe, E.G. & Powell, J.A. (1983) Checklist of the Lepidoptera of America And North of Mexico. Washington, D.C., The Wedge Entomological Research Foundation, 284 pp.
26. Ibrahim, M. & Tawfik, K. (1975) A report on the survey of natural enemies attacking the American bollworm. Cairo, Agricultural Research Center, Plant Protection Research Institute.
27. Isenhour, D.J. (1985) Campoletis sonorensis Hym, Ichneumonidae as a parasitoid of Spodoptera frugiperda Lep, Noctuidae - Host stage preference and functional response. Entomophaga, 30, 31-36.
28. Jalali, S.K., Singh, S.P. & Ballal, C.R. (1987) Studies on host age preference and biology of exotic parasite, Cotesia marginiventris (Cresson) (Hymenoptera, Braconidae). Entomon, 12, 59-62.
29. Lewis, W.J., Tumlinson, J.H. & Krasnoff, S. (1991) Chemically mediated associative learning - an important function in the foraging behavior of Microplitis croceipes (Cresson). J. Chem. Ecol., 17, 1309-1325.
30. Lingren, P.D., Guerra, R.J., Nickelse, J.W. & White, C. (1970) Hosts and host-age preference of Campoletis perdistinctus (Hymenoptera, Ichneumonidae). J. Econ. Entomol., 63, 518-522.
31. Loughrin, J.H., Manukian, A., Heath, R.R. & Tumlinson, J.H. (1995) Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. J. Chem. Ecol., 21, 1217-1227.
32. McAuslane, H.J., Vinson, S.B. & Williams, H.J. (1991) Influence of adult experience on host microhabitat location by the generalist parasitoid, Campoletis sonorensis (Hymenoptera, Ichneumonidae). J. Insect Behav., 4, 101-113.
33. McCall, P.J., Turlings, T.C.J., Loughrin, J., Proveaux, A.T. & Tumlinson, J.H. (1994) Herbivore-induced volatile emissions from cotton (Gossypium hirsutum L) seedlings. J. Chem. Ecol., 20, 3039-3050.
34. Meier, N.F. (1929) Schlupfwespen die in Russland in den Jahren 1881-1926 aus Schaedlingen gezogen sind (Fortsetzung). Izv. Otd. Prokl. Entomol., 4, 231-248.
35. Murray, D.A.H. & Rynne, K.P. (1994) Effect of host-plant on parasitism of Helicoverpa armigera (Lep, Noctuidae) by Microplitis demolitor (Hymenoptera, Braconidae). Entomophaga 39, 251-255.
36. Paré, P.W. & Tumlinson, J.H. (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol., 114, 1161-1167.
37. Potting, R.P.J., Otten, H. & Vet, L.E.M. (1997) Absence of odour learning in the stemborer parasitoid Cotesia flavipes. Anim. Behav., 53, 1211-1223.
38. Röse, U.S.R., Manukian, A., Heath, R.R. & Tumlinson, J.H. (1996) Volatile semicohemicals released from undamaged cotton leaves - A systemic response of living plants to caterpillar damage. Plant Physiol., 111, 487-495.
39. Steidle, J.L.M. & van Loon, J.J.A. (2003) Dietary specialization and infochemical use in carnivorous arthropods: Testing a concept. Entomol. Exp. Appl., 108, 133-148.
40. Tamò, C. (2006) A comparative study on the plant odour preferences and learning ability of three solitary endoparasitoids of Spodoptera species. Dissertation, University of Neuchâtel.
41. Tawfik, M.F.S., Hafez, M. & Ibrahim, A.A. (1980) Immature stages of Microplitis rufiventris Kok (Hym, Braconidae). Dtsch. Entomol. Z., 27, 39-50.
42. Thompson, W.R. (1946) A catalogue of the parasites and predators of insect pests. Section 1: Host-parasite catalogue. Part 7: Parasites of the Lepidoptera. Commonwealth Institute of Biological Control, Ontario, Canada.
43. Turlings, T.C.J. (1990) Semiochemically mediated, host-searching behavior of the endoparasitic wasp Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae). Dissertation, University of Florida.
44. Turlings, T.C.J. & Benrey, B. (1998) Effects of plant metabolites on the behavior and development of parasitic wasps. Ecoscience, 5, 321-333.
45. Turlings, T.C.J. & Wäckers, F.L. (2004) Recruitment of predators and parasitoids by herbivore-damaged plants. In: R.T. Card́ & J. Millar (Eds.), Advances in Insect Chemical Ecology, pp. 21-75. Cambridge, Cambridge University Press.
46. Turlings, T.C.J., Davison, A.C. & Tamò, C. (2004) A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiol. Entomol., 29, 45-55.
47. Turlings, T.C.J., Lengwiler, U.B., Bernasconi, M.L. & Wechsler, D. (1998) Timing of induced volatile emissions in maize seedlings. Planta, 207, 146-152.
48. Turlings, T.C.J., Tumlinson, J.H., Eller, F.J. & Lewis, W.J. (1991) Larval-damaged plants - Source of volatile synomones that guide the parasitoid Cotesia marginiventris to the microhabitat of its hosts. Entomol. Exp. Appl., 58, 75-82.
49. Turlings, T.C.J., Tumlinson, J.H. & Lewis, W.J. (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science, 250, 1251-1253.
50. Turlings, T.C.J., Tumlinson, J.H., Lewis, W.J. & Vet, L.E.M. (1989) Beneficial arthropod behavior mediated by airborne semiochemicals. 8. Learning of host-related odors induced by a brief contact experience with host by-products in Cotesia marginiventris (Cresson), a generalist larval parasitoid. J. Insect Behav., 2, 217-225.
51. Turlings, T.C.J., Wäckers, F., Vet, L.M., Lewis, W.J. & Tumlinson, J.H. (1993) Learning of host-finding cues by hymenopterous parasitoids. In: D.R. Papaj & A. Lewis (Eds.), Insect Learning: Ecological and Evolutionary Perspectives, pp. 51-78. New York, Chapman & Hall.
52. Vet, L.E.M. (1999) From chemical to population ecology: Infochemical use in an evolutionary context. J. Chem. Ecol., 25, 31-49.
53. Vet, L.E.M. & Dicke, M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol., 37, 141-172.
54. Vet, L.E.M. & Groenewold, A.W. (1990) Semiochemicals and learning in parasitoids. J. Chem. Ecol., 16, 3119-3135.
55. Vet, L.E.M., Lewis, W.J. & Cardé, R.T. (1995) Parasitoid foraging and learning. In: R.T. Cardé & W.J. Bell (Eds.), Chemical Ecology of Insects 2, pp. 65-101. New York, Chapman & Hall.
56. Vet, L.E.M., Lewis, W.J., Papaj, D.R. & van Lenteren (1990) A variable-response model for parasitoid foraging behavior. J. Insect Behav., 3, 471-490.
57. Zanen, P.O. & Cardé, R.T. (1991) Learning and the role of host-specific volatiles during in-flight host-finding in the specialist parasitoid Microplitis croceipes. Physiol. Entomol., 16, 381-389.