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Differential Attractiveness of Induced Odors Emitted by Eight Maize Varieties for the Parasitoid Cotesia marginiventris: Is Quality or Quantity Important?

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Abstract

Herbivore-induced plant volatiles can function as indirect defense signals that attract natural enemies of herbivores. Several parasitoids are known to exploit these plant-provided cues to locate their hosts. One such parasitoid is the generalist Cotesia marginiventris, which is, among others, attracted to maize volatiles induced by caterpillar damage. Maize plants can be induced to produce the same blend of attractive volatiles by treating them with regurgitant of Spodoptera species. We collected and analyzed the regurgitant-induced emissions of two plant species (cowpea and maize) and of eight Mexican maize varieties and found significant differences among their volatile emissions, both in terms of total quantity and the quality of the blends. In a Y-tube olfactometer, the odors of the same artificially induced plant species and Mexican varieties were offered in dual choice experiments to naïve mated females of C. marginiventris. Wasps preferred cowpea over maize odor and, in 3 of 12 combinations with the maize varieties, they showed a preference for the odors of one of the varieties. A comparison of the odor collection with results from the behavioral assays indicates that not only the quantity of the volatile emissions, but also the quality composition of the volatile blends is important for attraction of C. marginiventris. The results are discussed in the context of the possibility of breeding crop varieties that are particularly attractive to parasitoids.

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REFERENCES

  • Agelopoulus, N. G. and Keller, M. A. 1994.Plant-natural enemy association in tritrophic system, Cotesia rubecula–Pieris rapae–Brassicaceae (Cruciferae). III: Collection and identification of plant and frass volatiles.J. Chem. Ecol. 20:1955–1967.

    Google Scholar 

  • Agelopoulus, N. G., Dicke, M., and Posthumus, M. A. 1995.Role of volatile infochemicals emitted by feces of larvae in host-searching behavior of parasitoid Cotesia rubecula (Hymenoptera: Braconidae): A behavioral and chemical study.J. Chem. Ecol.21:1789–1811.

    Google Scholar 

  • Agelopoulus, N. G., Chamberlain, K., and Pickett, J.A.2000.Factors affecting volatile emissions of intact potato plants, Solanum tuberosum: variability of quantities and stability of ratios.J. Chem. Ecol.26:497–510.

    Google Scholar 

  • Andrews, K. L.1988.Latin American research on Spodoptera frugiperda (Lepidoptera: Noctuidae). Fla. Entomol.71:630–653.

    Google Scholar 

  • Benrey, B., Denno, R. F., and Kaiser, L. 1997.The influence of plant species on attraction and host acceptance in Cotesia glomerata (Hymenoptera: Braconidae).J. Insect Behav. 10:619–630.

    Google Scholar 

  • Bernasconi, M. L., Turlings, T. C. J., Ambrosetti, L., Bassetti, P., and Dorn, S. 1998. Herbivoreinduced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis.Entomol. Exp. Appl.87:133–142.

    Google Scholar 

  • Bertschy, C., Turlings, T. C. J., Bellotti, A., and Dorn, S.1997.Chemically-mediated attraction of three parasitoid species to mealybug-infested cassava leaves.Fla. Entomol.80:383–395.

    Google Scholar 

  • Blaakmeer, A., Geervliet, J. B. F., Van Loon, J. J. A., Posthumus, M. A., Van Beek, T. A., and De Groot, A. 1994.Comparative headspace analysis of cabbage plants damaged by two species of Pieris caterpillars: Consequences for in-flight host location by Cotesia parasitoids.Entomol. Exp. Appl.73:175–182.

    Google Scholar 

  • Bolter, C. J., Dicke, M., Van Loon, J. J. A., Visser, J. H., and Posthumus, M. A. 1997. Attraction of Colorado potato beetle to herbivore-damaged plants during herbivory and after its termination. J. Chem. Ecol. 23:1003–1023.

    Google Scholar 

  • Bottrell, D. G. and Barbosa, P. 1998.Manipulating natural enemies by plant variety selection and modification: A realistic strategy? Annu. Rev. Entomol. 43:347–367.

    PubMed  Google Scholar 

  • 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 specificity.J. Chem. Ecol.23:1589–1606.

    Google Scholar 

  • DeMoraes, C. and Lewis, W. J. 1999.Analyses of two parasitoids with convergent foraging strategies.J. Insect Behav. 12:571–583.

    Google Scholar 

  • DeMoraes, C. M., Lewis, W. J., ParÉ, P.W., Alborn, H. T., and Tumlinson, J. H. 1998.Herbivoreinfested plants selectively attract parasitoids.Nature 393:570–573.

    Google Scholar 

  • 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 

  • Dicke, M. 1999.Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomol. Exp. Appl. 91:131–142.

    Google Scholar 

  • Dicke, M. and Van Loon, J. J. A.2000.Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context.Entomol. Exp. Appl.97:237–249.

    Google Scholar 

  • Dicke, M., Van Beek, T. A., Posthumus, M. A., Ben Dom, N., Van Bokhoven, H., and De Groot, A.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.

    Google Scholar 

  • Dicke, M., Sabelis, M.W., Takabayashi, J., Bruin, J., and Posthumus, M.A.1990b. Plant strategies of manipulating predator-prey interactions through allelochemicals: Prospects for application in pest control.J. Chem. Ecol. 16:3091–3119.

    Google Scholar 

  • Dmoch, J., Lewis, W. J., Martin, P. B., and Nordlund, D.A.1985.Role of host-produced stimuli and learning in host selection behavior of Cotesia (=Apanteles) marginiventris (Cresson).J. Chem. Ecol. 11:453–464.

    Google Scholar 

  • Drost, Y. C., Lewis, W. J., and Tumlinson, J. H.1988.Beneficial arthropod behavior mediated by airborne semiochemicals. V. Influence of rearing method, host plant, and adult experience on host-searching behavior of Microplitis croceipes (Cresson), a larval parasitoid of Heliothis.J. Chem. Ecol. 14:1607–1616.

    Google Scholar 

  • 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 

  • Eller, F. J., Tumlinson, J. H., and Lewis, W. J. 1988.Beneficial arthropod behavior mediated by airborne semiochemicals. II. Olfactometric studies of host location by the parasitoid Microplitis croceipes (Cresson) (Hymenoptera: Braconidae).J. Chem. Ecol.14:425–433.

    Google Scholar 

  • Elzen, G. W., Williams, H. J., and Vinson, S. B.1984.Isolation and identification of cotton synomones mediating searching behavior by parasitoid Campoletis sonorensis.J. Chem. Ecol. 10:1251–1264.

    Google Scholar 

  • Elzen, G. W., Williams, H. J., and Vinson, S. B. 1986.Wind tunnel flight responses by hymenopterous parasitoid Campoletis sonorensis to cotton cultivars and lines.Entomol. Exp. Appl. 43:285–289.

    Google Scholar 

  • Finidori-Logli, V., BagnÈres, A.-G., and ClÉment, 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 

  • Flint, H. M., Salter, S. S., and Walters, S. 1979.Caryophyllene: an attractant for the green lacewing.Environ. Entomol.8:1123–1125.

    Google Scholar 

  • Fritzsche Hoballah, M. E., and Turlings, T. C. J. 2001. Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids.Evol. Ecol. Res.3:1–13.

    Google Scholar 

  • Geervliet, J. B. F., Vet, L. E. M., and Dicke, M.1996.Innate response of the parasitoids Cotesia glomerata and C. rubecola (Hymenoptera: Braconidae) to volatiles from different plant-herbivore complexes.J. Insect Behav.9:525–538.

    Google Scholar 

  • Geervliet, J. B. F., Posthumus, M. A., Vet, L. E. M., and Dicke, M.1997.Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species. J. Chem. Ecol. 23:2935–2954.

    Google Scholar 

  • 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.

    Google Scholar 

  • GouinguenÉ, S., Degen, T., and Turlings, T. C. J.2001.Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte).Chemoecology 11:9–16.

    Google Scholar 

  • Halitschke, R., Kessler, A., Kahl, J., Lorenz, A., and Baldwin, I. T.2000. Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata.Oecologia 124:408–417.

    Google Scholar 

  • Heath, R. R. and Manukian, A.1992.Development and evaluation of systems to collect volatile semiochemicals from insects and plants using a charcoal-infused medium for air purification. J. Chem. Ecol. 18:1209–1226.

    Google Scholar 

  • Jalali, S. K., Singh, S. P., and Ballal, C.R.1987.Studies on host age preference and biology of exotic parasite, Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae).Entomon 12:59–62.

    Google Scholar 

  • Lewis, W. J. and Martin, J. W. R.1990.Semiochemicals for use with parasitoids: status and future. J. Chem. Ecol. 16:3067–3089. MAIZE ODORS AND PARASITOID ATTRACTION 967

    Google Scholar 

  • Loke, W. H., Ashley, T. R., and Sailer, R. I.1983.Influence of fall armyworm, Spodoptera frugiperda,(Lepidoptera: Noctuidae) larvae and corn plant damage on host finding in Apanteles marginiventris (Hymenoptera: Braconidae).Environ. Entomol. 12:911–915.

    Google Scholar 

  • Loughrin, J. H., Manukian, A., Heath, R. R., and Tumlinson, J. H. 1995.Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae.J. Chem. Ecol.21:1217–1227.

    Google Scholar 

  • 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.

    Google Scholar 

  • McAuslane, H. J. and Alborn, H. T. 1998.Systemic induction of allelochemicals in glanded and glandless isogenic cotton by Spodoptera exigua feeding.J. Chem. Ecol.24:399–417.

    Google Scholar 

  • McCall, P. J., Turlings, T. C. J., Loughrin, J., Proveaux, A. T., and Tumlinson, J. H. 1994.Herbivore-induced volatile emissions from cotton (Gossypium hirsutum L:) seedlings.J. Chem. Ecol.20:3039–3050.

    Google Scholar 

  • Ngi-Song, A. J., Overholt, W. A., Njagi, P. G. N., Dicke, M., Ayertey, J. N., and Lwande, W.1996.Volatile infochemicals used in host and host habitat location by Cotesia flavipes Cameron and cotesia sesamiae (Cameron) (Hymenoptera: Braconidae), larval parasitoids of stemboresrs on graminae.J. Chem. Ecol.22:307–323.

    Google Scholar 

  • Ozawa, R., Shimoda, T., Kawaguchi, M., Arimura, G., Horiuchi, J., Nishioka, N., and Takabayashi, J.2000.Lotus japonicus infested with herbivorous mites emits volatile compounds that attract predatory mites.J. Plant Res.113:427–433.

    Google Scholar 

  • Papaj, D. R. and Vet, L. E.M.1990.Odor learning and foraging success in the parasitoid, Leptopilina heterotoma.J. Chem. Ecol. 16:3137–3150.

    Google Scholar 

  • Roland, J., Denford, K. E., and Jimenez, L.1995.Borneol as an attractant for Cyzenis albicans, a tachinid parasitoid of the winter moth, Operophtera brumata L. (Lepidoptera: Geometridae). Can. Entomol. 127:413–421.

    Google Scholar 

  • RÖse, U. S. R., Lewis, W. J., and Tumlinson, J. H. 1998.Specificity of systematically released cotton volatiles as attractants for specialist and generalist parasitic wasp.J. Chem. Ecol. 24:303–319.

    Google Scholar 

  • Sabelis, M. W., Van Baalen, M., Bakker, F. M., Bruin, J., Drukker, B., Egas, M., Janssen, A. R. M., Lesna, I. K., Pels, B., Van Rijn, P. C. J., and Scutareau, P.1999.The evolution of direct and indirect plant defence against herbivorous arthropods, pp. 109–166, in H. Olf, V. K. Brown and R. H. Drent (eds.).Herbivores: Between Plants and Predators.Blackwell, Oxford.

    Google Scholar 

  • Sabelis, M. W. and Van DeBaan, H. E.1983.Location of distant spider-mite colonies by phytoseiid predators: Demonstration of specific Kairomones emitted by Tetranychus urlicae and Panonychus ulna (Acari: Phytoseiidae, Tetranychidae).Entomol. Exp. Appl.33:303–314.

    Google Scholar 

  • Scutareanu, P., Drukker, B., Bruin, J., Posthumus, M. A., and Sabelis, M. W.1997. Volatiles from Psylla-infested pear trees and their possible involvement in attraction of anthocorid predators. J. Chem. Ecol. 23:2241–2261.

    Google Scholar 

  • Steinberg, S., Dicke, M., Vet, L. E. M., and Wanningen, R.1992.Response of the braconid parasitoid Cotesia (DApanteles) glomerata to volatile infochemicals: effects of bioassay setup, parasitoid age and experience and barometric flux.Entomologia. Entomol. Exp. Appl.63: 163–175.

    Google Scholar 

  • 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 

  • Takabayashi, J., Dicke, M., and Posthumus, M. A. 1991.Variation in composition of predatorattracting allelochemicals emitted by herbivore-infested plants: Relative influence of plant and herbivore.Chemoecology2:1–6.

    Google Scholar 

  • Takabayashi, J., Dicke, M., and Posthumus, M. A. 1994a. Volatile herbivore-induced terpenoids in plant–mite interactions: Variation caused by biotic and abiotic factors.J. Chem. Ecol. 20:1329–1354.

    Google Scholar 

  • Takabayashi, J., Dicke, M., Takahashi, S., Posthumus, M. A., and Van Beek, T. A. 1994b.Leaf age affects composition of herbivore-induced synomones and attraction of predatory mites. J. Chem. Ecol.20:373–386.

    Google Scholar 

  • Turlings, T. C. J. and Benrey, B. 1998.Effects of plant metabolites on the behavior and development of parasitic wasps.Ecoscience 5:321–333.

    Google Scholar 

  • Turlings, T. C. J, Tumlinson, J. H., Lewis, W. J., and Vet, L. E. M.1989.Beneficial arthropod behavior mediated by airborne semiochemicals. VIII. 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.2:217–226.

    Google Scholar 

  • Turlings, T. C. J., Tumlinson, J. H., and Lewis, W. J.1990a.Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps.Science 250:1251–1253.

    Google Scholar 

  • Turlings, T. C. J., Scheepmaker, J.W. A., Vet, L. E. M., Tumlinson, J. H., and Lewis, W. J. 1990b.How contact foraging experiences affect preferences for host-related odors in the larval parasitoid Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae).J. Chem. Ecol.16:1577–1589.

    Google Scholar 

  • Turlings, T. C. J., Tumlinson, J. H., Heath, R. R., Proveaux, A. T., and Doolittle, R. E. 1991a.Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts.J. Chem. Ecol. 17:2235–2250.

    Google Scholar 

  • Turlings, T. C. J., Tumlinson, J. H., Eller, F. J., and Lewis, W. J.1991b.Larval-damaged plants:Source of volatile synomones that guide the parasitoid Cotesia marginiventris to the micro-habitat of its hosts.Entomol. Exp. Appl.58:75–82.

    Google Scholar 

  • Turlings, T.C. J., McCall, P. J., Alborn, H.T., and Tumlinson, J.H.1993a.Anelicitor in caterpillar oral secretions that induces corn seedlings to emit chemical signals attractive to parasitic wasps. J. Chem. Ecol. 19:411–425.

    Google Scholar 

  • Turlings, T. C. J., WÄckers, F. L., Vet, L. E. M., Lewis, W. J., Lewis, A. C., and Tumlinson, J. H. 1993b. Learning of host-finding cues by hymenopterous parasitoids, pp. 51–78, in D. R. Papaj et al. (eds.).Insect Learning. Ecological and Evolutionary Perspectives.Chapman & Hall, New York.

    Google Scholar 

  • Turlings, T. C. J., Lengwiler, U. B., Bernasconi, M. L., and Wechsler, D.1998.Timing of induced volatile emissions in maize seedlings.Planta 207:146–152.

    Google Scholar 

  • Vaughn, T. T., Antolin, M. F., and Bjostad, L. B.1996.Behavioral and physiological responses of Diaeretiella rapae to semiochemicals.Entomol. Exp. Appl.78:187–196.

    Google Scholar 

  • 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 

  • Vet, L. E. M. and Groenewold, A. W.1990.Semiochemicals and learning in parasitoids.J. Chem. Ecol. 16:3119–3135.

    Google Scholar 

  • Wardle, A. R. and Borden, J. H.1985.Age-dependent associative learning by Exeristes roborator (F.) (Hymenoptera: Ichneumonidae).Can. Entomol.117:605–616.

    Google Scholar 

  • Wardle, A. R. and Borden, J. H.1989.Learning of an olfactory stimulus associated with a host microhabitat by Exeristes roborator.Entomol. Exp. Appl.51:271–279.

    Google Scholar 

  • Weissbecker, B., Van Loon, J. J. A., and Dicke, M.1999.Electroantennogram responses of a predator, Perillus bioculatus, and its prey, Leptinotarsa decemlineata, to plant volatiles.J. Chem. Ecol.25:2313–2325.

    Google Scholar 

  • Weissbecker, B., Van Loon, J. J. A., Posthumus, M. A., Bouwmeester, H. J., and Dicke, M.2000.Identification of volatile potato sesquiterpenoids and their olfactory detection by the two-spotted stinkbug Perillus bioculatus.J. Chem. Ecol.26:1433–1445.

    Google Scholar 

  • Whitman, D. W. and Eller, F. J. 1990.Parasitic wasps orient to green leaf volatiles.Chemoecology 1:69–76.

    Google Scholar 

  • Wickremasinghe, M. G. V. and Van Emden, H. F.1992.Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile chemical cues from the host plants of their aphid prey.Physiol. Entomol.17:297–304.

    Google Scholar 

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  1. Institut de Zoologie, Laboratoire d'Ecologie Animale et Entomologie (LEAE), Université de Neuchâtel, Case Postale 2, 2007, Neuchâtel, Switzerland

    Maria Elena Fritzsche Hoballah, Cristina Tamò & Ted C. J. Turlings

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  1. Maria Elena Fritzsche Hoballah
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Hoballah, M.E.F., Tamò, C. & Turlings, T.C.J. 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 (2002). https://doi.org/10.1023/A:1015253600083

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