Skip to main content
SpringerLink
Log in

The Attraction of Spodoptera frugiperda Neonates to Cowpea Seedlings is Mediated by Volatiles Induced by Conspecific Herbivory and the Elicitor Inceptin

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Neonate fall armyworms [FAW; Spodoptera frugiperda (Smith)] often encounter conspecific herbivore damage as they disperse from an egg mass to an initial feeding site. We investigated the orientation responses of dispersing neonates to herbivore damage in cowpea seedlings, specifically examining whether neonate behaviors were affected by inceptin, the primary elicitor of FAW-induced defenses in cowpea leaves. We focused on responses to damage caused by conspecific first instars, as might occur during the dispersal of siblings from an egg mass. Inceptin contents of damaging first instar FAW were controlled through their diets, with leaf-fed FAW producing inceptins in their oral secretions, and root-fed or starved FAW lacking these elicitors. In a bioassay designed to evaluate neonate dispersal off a host plant, a higher percentage of neonates remained on herbivore-induced or inceptin-treated plants than on undamaged plants, mechanically damaged plants, freshly damaged plants, or on plants damaged by FAW lacking inceptins. Further investigations of neonate responses to plant odors with a four-arm olfactometer demonstrated that neonate attraction to odors from 4-h old FAW damage was strongly dependent on previous diet of the damaging larvae. Neonates were attracted to odors from 4-h old FAW damage over odors from undamaged plants or fresh FAW damage, provided that the damaging larvae had previously ingested leaf material. In a direct comparison of odors from induced plants, plants damaged by leaf-fed FAW were as attractive as plants treated with synthetic inceptin. GC-MS analysis confirmed that (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) was the major volatile induced by FAW herbivory. While both DMNT and undamaged plant odors were more attractive than air, neonates preferred DMNT-supplemented plant odors. These results suggest that neonate FAW exploit herbivore-induced plant volatiles as host plant location and recognition cues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Anderson, P., Hilker, M., and Löfqvist, J. 1995. Larval diet influence on oviposition behavior in Spodoptera littoralis. Entomol. Exp. Appl 74:71–82.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bernays, E. A., Singer, M. S., and odrigues, D. 2004. Foraging in nature: foraging efficiency and attentiveness in caterpillars with different diet breadths. Ecol. Entomol 29:389–397.

    Article  Google Scholar 

  • Bolter, C. J., Dicke, M., Vanloon, 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.

    Article  CAS  Google Scholar 

  • Carroll, M. J., Schmelz, E. A., Meagher, R. L., and Teal, P. E. A. 2006. Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. J. Chem. Ecol 32:1911–1924.

    Article  PubMed  CAS  Google Scholar 

  • Carlsson, M. A., Anderson, P., Hartlieb, E., and Hansson, B. S. 1999. Experience-dependent modification of orientational response to olfactory cues in larvae of Spodoptera littoralis. J. Chem. Ecol 25:2445–2454.

    Article  CAS  Google Scholar 

  • Chapman, J. W., Williams, T., Escribano, A., Caballero, P., Cave, R. D., and Goulson, D. 1999. Fitness consequences of cannibalism in the fall armyworm, Spodoptera frugiperda. Behav. Ecol 10:298–303.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • D’alessandro, M., Held, M., Triponec, Y., and Turlings, T. C. J. 2006. The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J. Chem. Ecol 32:2733–2748.

    Article  PubMed  CAS  Google Scholar 

  • D’alessandro, M., and Turlings, T. C. J. 2005. In situ modification of herbivore-induced plant odors: A novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. Chem. Senses 30:739–753.

    Article  PubMed  CAS  Google Scholar 

  • Davis, F. M., Williams, W. P., Chang, Y. M., Baker, G. T., and Hedin, P. A. 1999. Differential growth of fall armyworm larvae (Lepidoptera: Noctuidae) reared on three phenotypic regions of whorl leaves from a resistant and a susceptible maize hybrid. Fla. Entomol 82:248–254.

    Article  Google Scholar 

  • De Moraes, C. M., Mescher, M. C., and Tumlinson, J. H. 2001. Caterpillar-induced nocturnal plant volatiles repel nonspecific females. Nature 410:577–580.

    Article  PubMed  CAS  Google Scholar 

  • Del Campo, M. L., Miles, C. I., Schroeder, F. C., Mueller, C., Booker, R., and enwick, J. A. 2001. Host recognition by the tobacco hornworm is mediated by a host plant compound. Nature 411:186–189.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Dicke, M., and Sabelis, M. W. 1988. How plants obtain predatory mites as bodyguards. Neth. J. Zool 38:148–165.

    Google Scholar 

  • Dicke, M., Van Poecke, R. M. P., and De Boer, J. G. 2003. Inducible indirect defence of plants: from mechanisms to ecological functions. Bas. Appl. Ecol 4:27–42.

    Article  CAS  Google Scholar 

  • 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 PredatorsOxford, Blackwell Science Oxford.

    Google Scholar 

  • Doak, P. 2000. Population consequences of restricted dispersal for an insect herbivore in a subdivided habitat. Ecology 81:1828–1841.

    Article  Google Scholar 

  • Gouinguené, S., Alborn, H., and Turlings, T. C. J. 2003. Induction of volatile emissions in maize by different larval instars of Spodoptera littoralis. J. Chem. Ecol 29:145–162.

    Article  PubMed  Google Scholar 

  • Gouinguené, S., Pickett, J. A., Wadhams, L. J., Birkett, M. A., and Turlings, T. C. J. 2005. Antennal electrophysiological responses of three parasitic wasps to caterpillar-induced volatiles from maize (Zea mays mays), cotton (Gossypium herbaceum), and cowpea (Vigna unguiculata). J. Chem. Ecol 31:1023–1038.

    Article  PubMed  CAS  Google Scholar 

  • Harris, M. O., Sandanayake, M., and Foster, S. P. 1999. Chemical stimuli from apple influence the behavior of neonate caterpillars of the generalist herbivore, Epiphyas postvittana. J. Chem. Ecol 25:1717–1738.

    Article  CAS  Google Scholar 

  • Heath, R. R., and Manukian, A. 1994. An automated-system for use in collecting volatile chemicals released from plants. J. Chem. Ecol 20:593–608.

    Article  CAS  Google Scholar 

  • Heath, R. R., and Sonnet, P. E. 1980. Technique for in situ coating of Ag+ onto silica gel in HPLC columns for the separation of geometrical isomers. J. Liquid Chromatogr 3:1129–1135.

    Article  CAS  Google Scholar 

  • Hilker, M., and Klein, B. 1989. Investigation of oviposition deterrent in larval frass of Spodoptera littoralis (Boisd.). J. Chem. Ecol 15:929–938.

    Article  Google Scholar 

  • Hoballah, M. E., Kollner, T. G., Degenhardt, J., and Turlings, T. C. J. 2004. Costs of induced volatile production in maize. Oikos 105:168–180.

    Article  Google Scholar 

  • Hoballah, M. E., and 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.

    Article  PubMed  CAS  Google Scholar 

  • Hoballah, M. E. F., Tamo, C., and 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.

    Article  PubMed  CAS  Google Scholar 

  • Kessler, A., and Baldwin, I. T. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144.

    Article  PubMed  CAS  Google Scholar 

  • Kessler, A., and Baldwin, I. T. 2002. Plant responses to insect herbivory: The emerging molecular analysis. Annu. Rev. Plant Biol 53:299–328.

    Article  PubMed  CAS  Google Scholar 

  • Landolt, P. J. 1993. Effects of host plant leaf damage on cabbage moth attraction and oviposition. Entomol. Exp. Appl 67:79–85.

    Article  Google Scholar 

  • Landolt, P. J., Brumley, J. A., Smithhisler, C. L., Biddick, L. L., and Hofstetter, R. W. 2000. Apple fruit infested with codling moth are more attractive to neonate codling moth larvae and possess increased amounts of (E,E)-alpha-farnesene. J. Chem. Ecol 26:1685–1699.

    Article  CAS  Google Scholar 

  • Luginbill, P. 1928. The fall armyworm. U.S. Department of Agriculture Technical Bulletin 34:1–91.

    Google Scholar 

  • Meagher, R. L., Nagoshi, R. N., Stuhl, C., M, and E. R. 2004. Larval development of fall armyworm (Lepidoptera: Noctuidae) on different cover crop plants. Fla. Entomol 87:454–460.

    Article  Google Scholar 

  • Meiners, T., and Hilker, M. 1997. Host location in Oomyzus gallerucae (Hymenoptera: Eulophidae), an egg parasitoid of the elm leaf beetle Xanthogaleruca luteola (Coleoptera, Chrysomelidae). Oecologia 112:87–93.

    Article  Google Scholar 

  • Meiners, T., and Hilker, M. 2000. Induction of plant synomones by oviposition of a phytophagous insect. J. Chem. Ecol 26:221–232.

    Article  CAS  Google Scholar 

  • Paré, P. W., Farag, M. A., Krishnamachari, V., Zhang, H. M., yu, C. M., and Kloepper, J. W. 2005. Elicitors and priming agents initiate plant defense responses. Photosynth. Res 85:149–159.

    Article  PubMed  CAS  Google Scholar 

  • Paré, P. W., and Tumlinson, J. H. 1997. Induced synthesis of plant volatiles. Nature 385:30–31.

    Article  Google Scholar 

  • Paré, P. W., and Tumlinson, J. H. 1999. Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331.

    Article  PubMed  Google Scholar 

  • Pickett, J. A., Bruce, T. J. A., Chamberlain, K., Hassannali, A., Khan, Z. R., Matthes, M. C., Napier, J. A., Smart, L. E., Wadhams, L. J., and Woodcock, C. M. 2006. Plant volatiles yielding new ways to exploit plant defence, pp. 161–173, in M. Dicke, and W. Takken (eds.). Chemical Ecology: from Gene to EcosystemSpringer, Wageningen, The Netherlands.

    Google Scholar 

  • Pitre, H. N., Mulrooney, J. E., and Hogg, D. B. 1983. Fall armyworm (Lepidoptera: Noctuidae) oviposition: crop preferences and egg distribution on plants. J. Econ. Entomol 76:463–466.

    Google Scholar 

  • Prokopy, R. J., and Roitberg, B. D. 2001. Joining and avoidance behavior in nonsocial insects. Annu. Rev. Entomol 46:631–665.

    Article  PubMed  CAS  Google Scholar 

  • Renwick, J. A. A. 2001. Variable diets and changing taste in plant-insect relationships. J. Chem. Ecol 27:1063–1076.

    Article  PubMed  CAS  Google Scholar 

  • Roitberg, B. D., and Mangel, M. 1993. Parent-offspring conflict and life history consequences in herbivorous insects. Am. Nat 1442:443–456.

    Article  Google Scholar 

  • Rott, A. S., Hackermann, J., Brand, N., Vallat, A., and Dorn, S. 2005. Parasitoid exploitation of the seasonal variation in host plant volatile emission for herbivore location. Entomol. Exp. Appl 115:199–205.

    Article  CAS  Google Scholar 

  • Schmelz, E. A., Alborn, H. T., and Tumlinson, J. H. 2001. The influence of intact-plant and excised-leaf bioassay designs on volicitin- and jasmonic acid-induced sesquiterpene volatile release in Zea mays. Planta 214:171–179.

    Article  PubMed  CAS  Google Scholar 

  • Schmelz, E. A., Carroll, M. J., Leclere, S., Phipps, S. M., Meredith, J., Chourey, P. S., Alborn, H. T., and Teal, P. E. A. 2006. Fragments of ATP synthase mediate plant perception of insect attack. Proc. Natl. Acad. Sci. U.S.A 103:8894–8899.

    Article  PubMed  CAS  Google Scholar 

  • Schoonhoven, L. M., and Van Loon, J. J. A. 2002. An inventory of taste in caterpillars: Each species its own key. Acta Zool. Acad. Sci. H 48:215–263.

    Google Scholar 

  • Shiojiri, K., Ozawa, R., and Takabayashi, J. 2006a. Plant volatiles, rather than light, determine the nocturnal behavior of a caterpillar. Plos Biology 4:1044–1047.

    Article  CAS  Google Scholar 

  • Shiojiri, K., Kishimoto, K., Ozawa, R., Kugimiya, S., Urashimo, S., Arimura, G., Horiuchi, J., Nishioka, T., Matsui, K., and Takabayashi, J. 2006b. Changing green leaf volatile biosynthesis in plants: An approach for improving plant resistance against both herbivores and pathogens. Proc. Natl. Acad. Sci. U.S.A 103:16672–16676.

    Article  PubMed  CAS  Google Scholar 

  • Sparks, A. N. 1979. A review of the biology of the fall armyworm. Fla. Entomol 62:82–86.

    Article  Google Scholar 

  • Stamps, J., and Krishnan, V. V. 2005. Nonintuitive cue use in habitat selection. Ecology 86:2860–2867.

    Article  Google Scholar 

  • Suazo, A., Torto, B., Teal, P. E. A., and Tumlinson, J. H. 2003. Response of the small hive beetle (Aethina tumida) to honey bee (Apis mellifera) and beehive-produced volatiles. Apidologie 34:525–533.

    Article  Google Scholar 

  • Thompson, J. N. 1988. Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol. Exp. Appl 47:3–14.

    Article  Google Scholar 

  • 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.

    Article  CAS  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.

    Article  CAS  Google Scholar 

  • Turlings, T. C. J., Loughrin, J. H., Mccall, P. J., ose, U. S., 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.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ward, S. A. 1987. Optimal habitat selection in time-limited dispersers. Am. Nat 129:568–579.

    Article  Google Scholar 

  • Weatherston, I., Miller, D., and Dohse, L. 1985. Capillaries as controlled-release devices for insect pheromones and other volatile substances - a reevaluation. Part I. Kinetics and development of predictive model for glass capillaries. J. Chem. Ecol 11:953–965.

    Article  Google Scholar 

  • Yang, G., Wiseman, B. R., and Espelie, K. E. 1993. Movement of neonate fall armyworm (Lepidoptera: Noctuidae) larvae on resistant and susceptible genotypes of corn. Environ. Entomol 22:547–553.

    Google Scholar 

  • Zalucki, M. P., Clarke, A. R., and Malcolm, S. B. 2002. Ecology and behavior of first instar larval Lepidoptera. Annu. Rev. Entomol 47:361–393.

    Article  PubMed  CAS  Google Scholar 

  • Zangerl, A. R. 2003. Evolution of induced plant responses to herbivores. Bas. Appl. Ecol 4:91–103.

    Article  Google Scholar 

  • Zangerl, A. R., and Berenbaum, M. R. 1992. Oviposition patterns and hostplant suitability - parsnip webworms and wild parsnip. Am. Midl. Nat 128:292–298.

    Article  Google Scholar 

Download references

Acknowledgment

We thank Sean Collins and Art Zangerl for comments that improved the manuscript. We especially thank Rob Meagher, Charlie Dillard, and Nancy Lowman for providing the insects used in these experiments. We also thank Julia Meredith and Mary Searle for assistance in the maintenance of plants used in this experiment.

Author information

Authors and Affiliations

  1. Center for Medical, Agricultural, and Veterinary Entomology, U.S. Department of Agriculture, Agricultural Research Service, Chemistry Research Unit, 1700 SW 23rd Dr., Gainesville, FL, 32608, USA

    Mark J. Carroll, Eric A. Schmelz & Peter E. A. Teal

Authors
  1. Mark J. Carroll
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eric A. Schmelz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter E. A. Teal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark J. Carroll.

Additional information

The use of trade, firm, or corporation names in this publication (or page) is for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the United States Department of Agriculture or the Agricultural Research Service of any product or service to the exclusion of others that may be suitable.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carroll, M.J., Schmelz, E.A. & Teal, P.E.A. The Attraction of Spodoptera frugiperda Neonates to Cowpea Seedlings is Mediated by Volatiles Induced by Conspecific Herbivory and the Elicitor Inceptin. J Chem Ecol 34, 291–300 (2008). https://doi.org/10.1007/s10886-007-9414-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-007-9414-y

Keywords

Search

Navigation