Journal of Chemical Ecology

, Volume 25, Issue 8, pp 1961–1979 | Cite as

The Role of Plant Rapidly Induced Responses in Asymmetric Interspecific Interactions Among Insect Herbivores

  • Moshe Inbar
  • Hamed Doostdar
  • Gary L. Leibee
  • Richard T. Mayer


The role of induced responses of tomato, Lycopersicon esculentum, in interspecific interactions between two polyphagous herbivores, the silverleaf whitefly, Bemisia argentifolii (WF), and the vegetable leafminer, Liriomyza trifolii (LM), was characterized in laboratory and field experiments. Feeding by LMs and WFs induced local and systemic production of putative defensive proteins, i.e., chitinases, peroxidases, β-1,3-glucanases, and lysozymes. The magnitude of the induction for each defensive protein varied between species. Unlike WFs, LMs caused a 33% local reduction in total foliar protein content. In a whole-plant choice experiment, adult LM feeding, oviposition, and larval survival were reduced by 47.7%, 30.7%, and 26.5%, respectively, for the WF-infested host compared with the controls. Early WF infestations also had negative systemic (plant-mediated) effects on LMs. Adult LMs preferred leaves from control plants to leaves of plants that had been previously infested with WFs; no reciprocal effect of LMs on WFs were found. Feeding by Helicoverpa zea larvae, which has been shown previously to affect LM performance, had no effect on WF survival and development. LM natural population dynamics were monitored on WF-preinfested and control plants in a field experiment. WF-infested plants were less suitable for LM development with an overall 41% reduction in LM population density. These results demonstrate asymmetric direct and plant-mediated interspecific interactions between generalist herbivores feeding simultaneously on the same host. Possible mechanisms by which WFs overcome plant defenses are suggested. This ability may also contribute to WF success that makes them a major pest worldwide. The study supports the idea that over an evolutionary time scale, herbivores sharing the same host plant will automatically compete.

Herbivory induced response interspecific interactions leafminers pathogenesis related proteins plant defense tomato whiteflies 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Agrawal, A. A. 1998. Induced response to herbivory and increased plant performance. Science 279:1201-1202.Google Scholar
  2. 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
  3. Baldwin, I. T. 1994. Chemical changes rapidly induced by folivory, pp. 2-16, in E. A. Bernays, (ed.). Insect Plant Interactions, Vol. 5. CRC Press, Boca Raton, Florida.Google Scholar
  4. Berenbaum, M. R. 1991. Coumarins, pp. 221-249, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites, 2nd ed. Academic Press, San Diego.Google Scholar
  5. Bowles, D. J. 1990. Defense-related proteins in higher plants. Annu. Rev. Biochem. 59:873-907.Google Scholar
  6. Byrne, D. N., and Bellows, T. S., Jr. 1991. Whitefly biology. Annu. Rev. Entomol. 36:431-457.Google Scholar
  7. Carozzi, N., and Koziel, M. 1997. Advances in Insect Control: The Role of Transgenic Plants. Taylor & Francis, London.Google Scholar
  8. Cohen, A. C., Henneberry, T. J., and Chu, C. C. 1996. Geometric relationships between whitefly feeding behavior and vascular bundle arrangements. Entomol. Exp. Appl. 78:135-142.Google Scholar
  9. Danell, K., Huss-Danell, K., and Bergstrom, R. 1985. Interactions between browsing moose and two species of birch in Sweden. Ecology 66:1687-1878.Google Scholar
  10. Denno, R. F., McClure, M. S., and Ott, J. R. 1995. Interspecific interactions in phytophagous insects: Competition reexamined and resurrected. Annu. Rev. Entomol. 40:297-331.Google Scholar
  11. Duffey, S. S., and Felton, G. W. 1991. Enzymatic antinutritive defenses of the tomato plant against insects, pp. 166-197, in P. A. Hedin (ed.). Naturally Occurring Pest Bioregulators. ACS Symposium Series 449, Dallas, Fall 1989. American Chemical Society, Washington, D.C.Google Scholar
  12. Duffey, S. S., and Stout, M. J. 1996. Antinutritive and toxic components of plant defense against insects. Arch. Insect Biochem. Physiol. 32:3-37.Google Scholar
  13. Edwards, P. J., Wratten, S. D., and Cox, H. 1985. Wound induced changes in the acceptability of tomato to larvae of Spodoptera littoralis: A laboratory bioassay. Econ. Entomol. 10:155-158.Google Scholar
  14. Faeth, S. H. 1986. Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology 67:479-494.Google Scholar
  15. Felton, G. W., Summers, C. B., and Mueller, A. J. 1994. Oxidative responses in soybean foliage to herbivory by bean leaf beetle and three-cornered alfalfa hopper. J. Chem. Ecol. 20:639-649.Google Scholar
  16. Fowler, S. V., and Lawton, J. H. 1985. Rapidly induced defenses and talking trees: The devil's advocate position. Am. Nat. 126:181-195.Google Scholar
  17. Gerling, D., and Mayer, R. T. 1996. Bemisia 1995: Taxonomy, Biology, Damage Control and Management. Intercept Ltd., Andover, Hants., UK.Google Scholar
  18. Harrison, S., and Karban, R. 1986. Effects of an early-season folivorous moth on the success of a later-season species, mediated by a change in the quality of the shared host, Lupinus arboreus Sims. Oecologia 69:354-359.Google Scholar
  19. Hartley, S. E., and Lawton, J. H. 1991. Biochemical aspects and significance of the rapidly induced accumulation of phenolics in birch foliage, pp. 105-132, in D. W. Tallamy and M. J. Raupp (eds.). Phytochemical Induction by Herbivores, John Wiley & Sons, New York.Google Scholar
  20. Haukioja, E. 1990. Induction of defenses in trees. Annu. Rev. Entomol. 36:25-42.Google Scholar
  21. Hougen-Eitzman, D., and Karban, R. 1995. Mechanisms of interspecific competition that result in successful control of Pacific mites following inoculations of Willamette mites on grapevines. Oecologia 103:159-161.Google Scholar
  22. Hunter, M. D. 1992. Interactions within herbivores communities mediated by the host plant: the keystone herbivore concept, pp. 287-325, in M. D. Hunter, P. W. Price, and T. Ohgushi (eds.). Effects of Resource Distribution on Animal-Plant Interactions. Academic Press, San Diego.Google Scholar
  23. Inbar, M., Eshel, A., and Wool, D. 1995. Interspecific competition among phloem-feeding insects mediated by induced host-plant sinks. Ecology 76:1506-1515.Google Scholar
  24. Inbar, M., Doostdar, H. R., Sonoda, M., Leibee, G. L., and Mayer, R. T. 1998. Elicitors of plant defensive systems reduce insect densities and disease incidence. J. Chem. Ecol. 24:135-149.Google Scholar
  25. Inbar, M., Doostdar, H., and Mayer, R. T. 1999. The effects of sessile insects (whitefly nymphs) on leaf-chewing caterpillars. Environ. Entomol. 28(3):353-357.Google Scholar
  26. Janzen, D. H. 1973. Host plants as islands. II. Competition in evolutionary and contemporary time. Am. Nat. 107:786-790.Google Scholar
  27. Jones, C. G., Hopper, R. F., Coleman, J. S., and Krischik, V. A. 1993. Control of systemically induced herbivore resistance by plant vascular architecture. Oecologia 93:452-456.Google Scholar
  28. Karban, R., and Baldwin, I. T. 1997. Induced Response to Herbivory. University of Chicago Press, Chicago.Google Scholar
  29. Karban, R., and Myers, J. H. 1989. Induced plant responses to herbivory. Annu. Rev. Ecol. Syst. 20:331-348.Google Scholar
  30. Karban, R., Adamchak, R., and Schnathorst, W. C. 1987. Induced resistance and interspecific competition between spider mites and a vascular wilt fungus. Science 235:678-680.Google Scholar
  31. Kogan, M., and Fischer, D. C. 1991. Inducible defenses in soybean against herbivorous insects, pp. 347-378, in D. W. Tallamy and M. J. Raupp (eds.). Phytochemical Induction by Herbivores. John Wiley & Sons, New York.Google Scholar
  32. Little, T. M., and Hills, J. F. 1978. Agricultural Experimentation: Design and Analysis. John Wiley & Sons, New York.Google Scholar
  33. Liu, T.-X., and Stansly, P. A. 1995. Oviposition by Bemisia argentifolii (Homoptera: Aleyrodidae) on tomato: Effects of leaf factors and insecticide residue. J. Econ. Entomol. 88:992-997.Google Scholar
  34. Martinsen, G. D., Driebe, E. M., and Whitham, T. G. 1998. Indirect interactions mediated by changing plant chemistry: Beaver browsing benefits beetles. Ecology 79:192-200.Google Scholar
  35. Masters, G. J., Brown, V. K., and Gange, A. C. 1993. Plant mediated interactions between above-and below-ground insect herbivores. Oikos 66:148-151.Google Scholar
  36. Mayer, R. T., McCollum, T. G., McDonald, R. E., Polston, J. E., and Doostdar, H. 1996. Bemisia feeding induces pathogenesis-related proteins in tomato, pp. 179-188, in D. Gerling and R. T. Mayer (eds.). Bemisia 1995: Taxonomy, Biology, Damage Control and Management. Intercept Ltd., Andover, Hants., UK.Google Scholar
  37. McKey, D. 1979. The distribution of secondary compounds within plants, pp. 55-133, in G. A. Rosenthal and D. H. Janzen (eds.). Herbivores, Their Interaction with Secondary Plant Metabolites. Academic Press, New York.Google Scholar
  38. Minkenberg, O. P. J. M., and Ottenheim, J. J. G. W. 1990. Effect of leaf nitrogen content of tomato plants on preference and performance of a leafmining fly. Oecologia 83:291-298.Google Scholar
  39. Mullin, C. A. 1986. Adaptive divergence of chewing and sucking arthropods to plant allelochemicals, pp. 175-209, in L. B. Brattsten and S. Ahmad (eds.). Molecular Aspects of Insect-plant Associations. Plenum Press, New York.Google Scholar
  40. Parrella, M. P. 1987. Biology of Liriomyza. Annu. Rev. Entomol. 32:201-224.Google Scholar
  41. Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N., and Weis, A. E. 1980. Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11:41-65.Google Scholar
  42. Rosenheim, J. A., Johnson, M. W., Mau, R. F. L., Welter, S. C., and Tabashnik, B. E. 1996. Biochemical preadaptations, founder events, and the evolution of resistance in arthropods. J. Econ. Entomol. 89:263-273.Google Scholar
  43. SAS Institute. 1988. SAS/STAT User's Guide. Release 6.11. SAS Institute, Cary, North Carolina.Google Scholar
  44. Schuster, D. J. 1998. Intraplant distribution of immature lifestages of Bemisia argentifolii (Homoptera: Aleyrodidae) on tomato. Environ. Entomol. 27:1-9.Google Scholar
  45. Schuster, D. J., and Beck, H. W. 1992. Presence-absence sampling for assessing densities of larval leafminers in field-grown tomatoes. Trop. Pest Manage. 38:254-256.Google Scholar
  46. Stout, M. J., and Duffey, S. S. 1996. Characterization of induced resistance in tomato plants. Entomol. Exp. Appl. 79:273-283.Google Scholar
  47. Stout, M. J., Workman, K. V., and Duffey, S. S. 1994. Differential induction of tomato foliar proteins by arthropod herbivores. J. Chem. Ecol. 20:2575-2594.Google Scholar
  48. Stout, M. J., Workman, K. V., and Duffey, S. S. 1996. Identity, spatial distribution, and variability of induced chemical responses in tomato plants. Entomol. Exp. Appl. 79:255-271.Google Scholar
  49. Strauss, S. Y. 1991. Indirect effects in community ecology: Their definition, study, and importance. Trends Ecol. Evol. 6:206-210.Google Scholar
  50. Strong, D. R., Lawton, J. H., and Southwood, R. 1984. Insect on plants: Community patterns and mechanisms. Harvard University Press, Cambridge, Massachusetts.Google Scholar
  51. Tallamy, D. W., and Raupp, M. J. 1991. Phytochemical Induction by Herbivores. John Wiley & Sons, New York.Google Scholar
  52. van Loon, L. C., Piepoint, W. C., Boller, T., and Conejero, V. 1994. Recommendations for naming plant pathogenesis-related proteins. Plant. Mol. Biol. Rep. 12:245-264.Google Scholar
  53. Walker-Simmons, M., and Ryan, C. A. 1977. Immunological identification of proteinase inhibitors I and II in isolated tomato leaf vacuoles. Plant Physiol. 60:61-63.Google Scholar
  54. Wang, X., Ding, X., Gopalakrishnan, B., Morgan, T. D., Johnson, L., White, F. F., Muthukrishnan, S., and Kramer, K. J. 1996. Characterization of a 46 kDa insect chitinase from transgenic tobacco. Insect Biochem. Mol. Biol. 26:1055-1064.Google Scholar
  55. Wilkens, R. T., Spoerke, J. M., and Stamp, N. E. 1996. Differential responses of growth and two soluble phenolics of tomato to resource availability. Ecology 77:247-258.Google Scholar
  56. Wootton, T. J. 1994. The nature and consequences of indirect effects in ecological communities. Annu. Rev. Ecol. Syst. 25:443-466.Google Scholar
  57. Zangerl, A. R. 1990. Furanocoumarin induction in wild parsnip: Evidence for an induced defense against herbivores. Ecology 71:1926-1932.Google Scholar

Copyright information

© Plenum Publishing Corporation 1999

Authors and Affiliations

  • Moshe Inbar
    • 1
    • 1
  • Hamed Doostdar
    • 2
  • Gary L. Leibee
    • 2
  • Richard T. Mayer
    • 1
  1. 1.US Horticultural Research LaboratoryUSDA, Agricultural Research ServiceOrlandoFlorida
  2. 2.University of Florida. IFAS, CFRECSanfordFlorida

Personalised recommendations