Skip to main content
Log in

Interactions Among Insect Herbivore Guilds: Influence of Thrips Bud Injury on Foliar Chemistry and Suitability to Gypsy Moths

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

Abstract

This study investigated the consequences of early season bud herbivory on host-plant phytochemistry and subsequent effects on a later mid-season leaf-feeding herbivore, to test the hypothesis that temporally segregated interguild interactions could affect herbivore success through plant-mediated responses. Our system consisted of American bass wood, Tilia americana, a bud-feeding thrips species, Thrips calcaratus, and the folivorous gypsy moth, Lymantria dispar. The impact of thrips bud-feeding on American basswood foliar chemistry and subsequent effects on gypsy moth larval preference and performance were measured. Foliar total nonstructural carbohydrates increased and phenolic levels decreased in response to bud injury, which affected larval feeding preference. In a two-choice test, gypsy moth larvae preferred leaf discs with high carbohydrate and low phenolic levels. The effects on larval performance depended on the extent of prior bud injury and were correlated with carbohydrate concentrations. In an early season assay, larval performance was lowest on moderately bud-damaged tissue, which also had the lowest total nonstructural carbohydrates. In a mid-season assay, larval performance and carbohydrate concentrations were highest in severely bud-damaged foliage. Foliar phenolics were highest in severely bud-damaged tissue in the early season assay, and in moderately damaged tissue in the mid-season assay. Gypsy moth performance was not correlated with foliar phenolic levels. Secondary (reflushed) foliage had higher carbohydrate levels than did primary (original) foliage, which correlated with increased larval performance. This study illustrates that bud-feeding herbivores can alter the phytochemistry and subsequent suitability of host-plant foliage for later folivores. The implications of these results to interactions between feeding guilds, community structure, and forest health are discussed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  • Abacus Concepts. 1989. SuperANOVA: Accessible General Linear Modeling. Abacus Concepts, Inc., Berkeley, California.

    Google Scholar 

  • Abeles, F. B., Morgan, P. W., and Saltveit, M. E., Jr. 1992. Ethylene in Plant Biology, 2nd ed. Academic Press, New York.

    Google Scholar 

  • Baldwin, I. T., and Schmelz, E. A. 1996. Immunological “memory” in the induced accumulation of nicotine in wild tobacco. Ecology 77:236–246.

    Google Scholar 

  • Barbosa, P., and Krischik, V. A. 1987. Influence of alkaloids on feeding preference of deciduous forest trees by the gypsy moth Lymantria dispar. Am. Nat. 130:53–69.

    Google Scholar 

  • Bauce, E., and Carisey, N. 1996. Larval feeding behaviour affects the impact of staminate flower production on the suitability of balsam fir trees for spruce budworm. Oecologia 105:126–131.

    Google Scholar 

  • Bergelson, J. M., Fowler, S., and Hartley, S. 1986. The effects of foliage damage on case-bearing moth larvae, Coleophora serratella, feeding on birch. Ecol. Entomol. 11:241–250.

    Google Scholar 

  • Berrie, A. M. M. 1984. Germination and dormancy, pp. 440–468, in M. B. Berrie (ed.). Advanced Plant Physiology. Pitman Press, London.

    Google Scholar 

  • Bosshard, W. 1986. Sanasilva: Couronnes d'arbres avec indication de la perte d'aiguilles ou de feuilles en pourcents. Institut federal de recherches forestières, Birmensdorf, Switzerland.

    Google Scholar 

  • Bourchier, R. S., and Nealis, V. G. 1993. Development and growth of early-and late-instar gypsy moth (Lepidoptera: Lymantriidae) feeding on tannin-supplemented diets. Environ. Entomol. 22:642–646.

    Google Scholar 

  • Bultman, T. L., and Ganey, D. T. 1995. Induced resistance to fall armyworm (Lepidoptera: Noctuidae) mediated by a fungal endophyte. Environ. Entomol. 24:1196–1200.

    Google Scholar 

  • Burden, R. S., and Kemp, M. S. 1983. (−)-7–Hydroxycalamenene, a phytoalexin from Tilia europa. Phytochemistry 22:1039–1040.

    Google Scholar 

  • Campbell, R. W., and Sloan, R. J. 1977. Forest stand responses to defoliation by the gypsy moth. For. Sci. Monogr. 19:1–34.

    Google Scholar 

  • Clancy, K. M. 1991. Douglas-fir nutrients and terpenes as potential factors influencing western spruce budworm defoliation, pp. 123–133, in Y. N. Baranchikov, W. J. Mattson, F. P. Hain, and T. L. Payne (eds.). Forest Insect Guilds: Patterns of Interaction with Host Trees. USDA For. Serv. Gen. Tech. Rep. NE-153. Radnor, Pennsylvania.

    Google Scholar 

  • Clancy, K. M., Wagner, M. R., and Tinus, R. W. 1988. Variations in nutrient levels as a defense: Identifying key nutritional traits of host plants of the western spruce budworm, pp. 203–213 in W. J. Mattson, J. Levieux, and C. Bernard-Dagan (eds.). Mechanisms of Woody Plant Defenses Against Insects—Search for Pattern. Springer-Verlag, New York.

    Google Scholar 

  • Clausen, T. P., Reichardt, P. B., Bryant, J. P., and Werner, R. A. 1991. Long-term and short-term induction in quaking aspen: related phenomena? pp. 71–84, in D. W. Tallamy and M. J. Raupp (eds.). Phytochemical Induction by Herbivores. Wiley, New York.

    Google Scholar 

  • Danell, K., and Huss-Danell, K. 1985. Feeding by insects and hares on birches earlier affected by moose browsing. Oikos 44:75–81.

    Google Scholar 

  • Drooz, A. T. 1985. Insects of Eastern Forests. USDA For. Serv. Misc. Publ. No. 1426. Washington, D.C., 608 pp.

  • Dunbar, D. M., and Stephens, G. R. 1975. Association of twolined chestnut borer and shoestring fungus with mortality of defoliated oak in Connecticut. For. Sci. 21:169–174.

    Google Scholar 

  • Faeth, S. H. 1986. Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology 67:479–494.

    Google Scholar 

  • Faeth, S. H. 1991. Variable induced responses: Direct and indirect effects on oak folivores, pp. 293–324, in D. W. Tallamy and M. J. Raupp (eds.). Phytochemical Induction by Herbivores. Wiley, New York.

    Google Scholar 

  • Faeth, S. H. 1992a. Do defoliation and subsequent phytochemical responses reduce future herbivory on oak trees? J. Chem. Ecol. 18:915–925.

    Google Scholar 

  • Faeth, S. H. 1992b. Interspecific and intraspecific interactions via plant responses to folivory—an experimental field test. Ecology 77:1802–1813.

    Google Scholar 

  • Feeney, P., and Bostock, H. 1968. Seasonal changes in the tannin content of oak leaves. Phytochemistry 7:871–880.

    Google Scholar 

  • Fowler, S. V., and McGarvin, M. 1986. The effects of leaf damage on the performance of insect herbivores on birch, Betula pubescens. J. Anim. Ecol. 55:565–573.

    Google Scholar 

  • Hartley, S. E., and Lawton, J. H. 1987. Effects of different types of damage on the chemistry of birch foliage and the responses of birch feeding insects. Oecologia 74:432–437.

    Google Scholar 

  • Haukioja, E. 1991. Induction of defenses in trees. Annu. Rev. Entomol. 36:25–42.

    Google Scholar 

  • Haukioja, E., and Niemela, P. 1979. Birch leaves as a resource for herbivores: Seasonal occurrence of increased resistance in foliage after mechanical damage of adjacent leaves. Oecologia 39:151–159.

    Google Scholar 

  • Haukioja, E., Niemela, P., Iso-Livari, L., Ojala, H., and Aro, E. 1978. Birch leaves as a resource of herbivores. I. Variation in the suitability of leaves. Kevo. Subarctic Res. Stn. Rep. 14, pp. 5–12.

  • Haukioja, E., RuohomÄki, K., Senn, J., Suomela, J., and Walls, M. 1990. Consequences of herbivory in the mountain birch (Betula pubescens ssp tortuosa): Importance of the functional organization of the tree. Oecologia 82:238–247.

    Google Scholar 

  • Hillis, W. E., and Swain, T. 1959. The phenolic constituents of Prunus domestica II. The analysis of tissues of the Victoria plum tree. J. Sci. Food Agric. 10:135–144.

    Google Scholar 

  • Hunter, M. D. 1987. Opposing effects of spring defoliation on late season oak caterpillars. Ecol. Entomol. 12:373–382.

    Google Scholar 

  • Hyodo, H., and Yang, S. F. 1971. Ethylene-enhanced synthesis of phenylalanine ammonialyase in pea seedlings. Plant Physiol. 47:765–770.

    Google Scholar 

  • Jones, C. G., and Coleman, J. S. 1988. Leaf disc size and insect feeding preference: implications for assays and studies on induction of plant defense. Entomol. Exp. Appl. 47:167–172.

    Google Scholar 

  • Karban, R., and Myers, J. H. 1989. Induced plant responses to herbivory. Annu. Rev. Ecol. Syst. 20:331–348.

    Google Scholar 

  • Karban, R., and Niiho, C. 1995. Induced resistance and susceptibility to herbivory: Plant memory and altered plant development. Ecology 76:1220–1225.

    Google Scholar 

  • Kelsey, R. G., and Harmon, M. E. 1989. Distribution and variation of extractable total phenols and tannins in the logs of four conifers after one year on the ground. Can. J. For. Res. 19:1030–1036.

    Google Scholar 

  • Klepzig, K. D., Raffa, K. F., and Smalley, E. B. 1991. Association of an insect-fungal complex with red pine decline in Wisconsin. For. Sci. 37:1119–1139.

    Google Scholar 

  • Klepzig, K. D., Raffa, K. F., and Smalley, E. B. 1996. Combined chemical defenses against an insect-fungal complex. J. Chem. Ecol. 22:1367–1388.

    Google Scholar 

  • 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.). Wiley Phytochemical Induction by Herbivores. New York.

  • Kolb, T. E., McCormick, L. H., Simons, E. E., and Jeffery, D. J. 1992. Impacts of pear thrips damage on root carbohydrate, sap, and crown characteristics of sugar maples in a Pennsylvania sugarbush. For. Sci. 38:381–392.

    Google Scholar 

  • Krause, S. C., and Raffa, K. F. 1992. Comparison of insect, fungal, and mechanically induced defoliation of larch: Effects on plant productivity and host suitability and availability. Oecologia 90:411–416.

    Google Scholar 

  • Krause, S. C., and Raffa, K. F. 1995. Defoliation intensity and larval age interact to affect sawfly performance on previously injured Pinus resinosa. Oecologia 104:24–30.

    Google Scholar 

  • Kuhlman, H. M. 1971. Effects of defoliation on growth and mortality of trees. Annu. Rev. Entomol. 16:289–324.

    Google Scholar 

  • Martin, M. A., Cappuccino, N., and Ducharme, D. 1994. Performance of Symydobius americanus (Homoptera: Aphididae) on paper birch grazed by caterpillars. Ecol. Entomol. 19:6–10.

    Google Scholar 

  • Mattson, W. J., and Koller, C. N. 1983. Spruce budworm performance in relation to matching selected chemical traits of its hosts, pp. 138–148, in A. S. Isaev (ed.). The Role of Insect Plant Relationships in the Population Dynamics of Forest Pests. International Union of Forestry Research Organizations, USSR Academy of Sciences.

  • Mattson, W. J., and Palmer, S. R. 1988. Changes in levels of foliar minerals and phenolics in trembling aspen, Populus tremuloides, in response to artificial defoliation, pp. 157–169, in W. J. Mattson, J. Levieux, and C. Bernard-Dagan (eds.). Mechanisms of Woody Plant Defenses Against Insects—Search for Pattern. Springer-Verlag, New York.

    Google Scholar 

  • Montgomery, M. E., and Wallner, W. E. 1988. The gypsy moth: a westward migrant, pp. 354–375, in A. A. Berryman (ed.). Dynamics of Forest Insect Populations. Plenum Press, New York.

    Google Scholar 

  • Neuvonen, S., and Haukioja, E. 1985. How to study induced plant resistance? Oecologia 66:456–457.

    Google Scholar 

  • Neuvonen, S., Hanhimaki, S., Suomela, J., and Haukioja, E. 1988. Early season damage to birch foliage affects the performance of a late season herbivore. J. Appl. Entomol. 105:182–189.

    Google Scholar 

  • Quarmby, C., and Allen, S. E. 1989. Organic constituents, pp. 160–201, in S. E. Allen (ed.). Chemical Analysis of Ecological Materials, 2nd ed. Wiley, New York.

    Google Scholar 

  • Raffa, K. F. 1991. Induced defensive reactions in conifer-bark beetle systems, pp. 245–276, in D. W. Tallamy and M. J. Raupp (eds.). Phytochemical Induction by Herbivores. Wiley, New York.

    Google Scholar 

  • Raffa, K. F., Hall, D. J., Kearby, W., and Katovich, S. 1992. Seasonal life history of introduced basswood thrips (Thysanoptera: Thripidae) in Wisconsin, with observations on associated thrips species. Environ. Entomol. 21:771–779.

    Google Scholar 

  • Redak, R. A., and Cates, R. G. 1984. Douglas-fir (Pseudotsuqa menziesii)-spruce budworm (Choristoneura occidentalis) interactions: The effect of nutrition, chemical defenses, tissue phenology, and tree physical parameters on budworm success. Oecologia 62:61–67.

    Google Scholar 

  • Rhoades, D. F. 1985. Offensive-defensive interactions between herbivores and plants: Their relevance in herbivore population dynamics and ecological theory. Am. Nat. 125:205–238.

    Google Scholar 

  • Rieske, L. K. 1995. Bionomics and induced phytochemical impacts of the introduced basswood thrips, Thrips calcaratus. PhD dissertation. University of Wisconsin, Madison, 166 pp.

    Google Scholar 

  • Rieske, L. K., and Raffa, K. F. 1995. Ethylene emission by a deciduous tree, Tilia americana, in response to feeding by the introduced basswood thrips, Thrips calcaratus. J. Chem. Ecol. 21:187–197.

    Google Scholar 

  • Rieske, L. K., Katovich, S. A., and Raffa, K. F. 1992. How to identify introduced basswood thrips. USDA Forest Service leaflet NA-FR-01–92. St. Paul, Minnesota.

    Google Scholar 

  • Robison, D. J., and Raffa, K. F. 1994. Characterization of hybrid poplar clones for resistance to the forest tent caterpillar. For. Sci. 40:1–29.

    Google Scholar 

  • Rossiter, M. C., Schultz, J. C., and Baldwin, I. T. 1988. Relationships among defoliation, red oak phenolics, and gypsy moth growth and reproduction. Ecology 69:267–277.

    Google Scholar 

  • Roth, S. K., Lindroth, R. L., and Montgomery, M. E. 1994. Effect of foliar phenolics and ascorbic acid on performance of the gypsy moth (Lymantria dispar). Biochem. System. Ecol. 22:341–451.

    Google Scholar 

  • Savopoulou-Soultani, M., Stavridis, D. G., Vassiliou, A., Stafilidis, J. E., and Iraklidis, I. 1994. Response of Lobesia botrana (Lepidoptera: Tortricidae) to levels of sugar and protein in artificial diets. J. Econ. Entomol. 87:84–90.

    Google Scholar 

  • Schoonhoven, L. M. 1968. Chemosensory bases of host plant selection. Annu. Rev. Entomol. 13:115–136.

    Google Scholar 

  • Schowalter, T. D. 1986. Herbivory in forested ecosystems. Annu. Rev. Entomol. 31:177–196.

    Google Scholar 

  • Schultz, J. C. 1988. Many factors influence the evolution of herbivore diets, but plant chemistry is central. Ecology 69:896–897.

    Google Scholar 

  • Scriber, J. M., and Slansky, F., Jr. 1981. The nutritional ecology of immature insects. Annu. Rev. Entomol. 26:183–211.

    Google Scholar 

  • Tallamy, D. W., and McCloud, E. S. 1991. Squash beetles, cucumber beetles, and inducible cucurbit responses, in D. W. Tallamy and M. J. Raupp (eds.). Phytochemical Induction by Herbivores. Wiley. New York.

    Google Scholar 

  • Tallamy, D. W., and Raupp, M. J. 1991. Phytochemical Induction by Herbivores. Wiley, New York.

    Google Scholar 

  • Wagner, M. R. 1988. Induced defenses in ponderosa pine against defoliating insects, pp. 141–156, in W. J. Mattson, J. Levieux, and C. Bernard-Dagan (eds.). Mechanisms of Woody Plant Defenses Against Insects—Search for Pattern. Springer-Verlag, New York.

    Google Scholar 

  • Wagner, M. R., and Blake, E. A. 1983. Western spruce budworm consumption—effects of host species and foliage chemistry, pp. 49–54, in Proceedings, Forest Defoliator-Host Interactions: A Comparison Between Gypsy Moth and Spruce Budworms. USDA For. Serv. Gen. Tech. Rep. NE-85.

  • Wagner, M. R., and Evans, P. D. 1985. Defoliation increases nutritional quality and allelochemics of pine seedlings. Oecologia 67:235–237.

    Google Scholar 

  • Wainhouse, D., Gate, I. M., and Lonsdale, D. 1988. Beech resistance to the beech scale: A variety of defenses, pp. 277–294, in W. J. Mattson, J. Levieux, and C. Bernard-Dagan (eds.). Mechanisms of Woody Plant Defenses Against Insects—Search for Pattern. Springer-Verlag, New York.

    Google Scholar 

  • Whitham, T. G., and Mopper, S. 1985. Chronic herbivory: Impacts on architecture and sex expression of pinyon pine. Science 228:1089–1091.

    Google Scholar 

  • Wright, L. C., Berryman, A. A., and Gurusiddaiah, S. 1979. Host resistance to the fir engraver beetle, Scolytus ventralis (Coleoptera: Scolytidae). 4. Effect of defoliation on wound monoterpene and inner bark carbohydrate concentrations. Can. Entomol. 111:1255–1262.

    Google Scholar 

  • Yang, S. F., and Pratt, H. K. 1978. The physiology of ethylene in wounded plant tissues, pp. 595–622, in G. Kahl (ed.). Biochemistry of Wounded Plant Tissues. Walter de Gruyter and Co, New York.

    Google Scholar 

  • Zou, J., and Cates, R. G. 1994. Role of Douglas fir (Pseudotsuqa menziesii) carbohydrates in resistance to budworm (Choristoneura occidentalis). J. Chem. Ecol. 20:395–405.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rieske, L.K., Raffa, K.F. Interactions Among Insect Herbivore Guilds: Influence of Thrips Bud Injury on Foliar Chemistry and Suitability to Gypsy Moths. J Chem Ecol 24, 501–523 (1998). https://doi.org/10.1023/A:1022364819779

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022364819779

Navigation