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Combined chemical defenses against an insect-fungal complex

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This study considered how host plant allelochemicals may contribute to defense against insects and fungi that jointly colonize the subcortical tissues of trees, the relative roles of constitutive and inducible chemistry in these defenses, and how the actions of two different feeding guilds might be interrelated. Our model consisted of the coniferous treePinus resinosa, the root- and lower stem-colonizing beetlesHylastes porculus andDendroctonus valens, and their associated fungiLeptographium procerum andL. terebrantis, and the stem-colonizing bark beetleIps pini and its associated fungusOphiostoma ips. In a novel bioassay, extracts from reaction tissue elicted by wound inoculation withL. terebrantis were more repellent to beetles than were similar extracts from constitutive or mechanically wounded tissue. The effect on beetle behavior was more pronounced in nonpolar extracts, which contain mostly monoterpenes, than in polar extracts, which contain mostly phenolics. Synthetic monoterpenes at concentrations present in the various tissues exerted similar effects and were likewise repellent in dose-response experiments. Growth ofL. procerum andL. terebrantis was inhibited by polar extracts from constitutive and reaction tissue. Inhibition was higher in wounded than control tissue, but the inhibition response did not vary with the type of wounding. Synthetic monoterpenes strongly inhibited spore germination and mycelial growth of both fungi. Colonization of red pine roots byLeptographium spp. altered the subsequent effects of extracts of stem phloem tissue onI. pini. These effects varied with host condition. Beetles preferred extracts from constitutive stem phloem tissue of healthy trees to that of root-diseased trees. However, extracts from reaction tissues of healthy trees were more repellent toI. pini than were the reaction tissues of root-diseased trees. The implications of these results to plant defense against insect-fungal complexes and interactions among different feeding guilds are discussed.

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References

  • Abacus Concepts. 1989. SuperANOVA. Abacus Concepts, Inc., Berkeley, California.

    Google Scholar 

  • Barbosa, P., Krischik, V. A., andJones, C. G. (eds.). 1991. Microbial Mediation of Plant-Herbivore Interactions. Wiley, New York.

    Google Scholar 

  • Barras, S. J. 1970. Antagonism betweenDendroctonus frontalis and the fungusCeratocystis minor.Ann. Entomol. Soc. Am. 63:1187–1190.

    Google Scholar 

  • Berenbaum, M. R., Zangerl, A. R., andLee, K. 1989. Chemical barriers to adaptation by a specialist herbivore.Oecologia 80:501–506.

    Article  Google Scholar 

  • Berryman, A. A. 1972. Resistance of conifers to invasion by bark beetle-fungus associations.BioScience 22:598–602.

    Google Scholar 

  • Berryman, A. A. 1988. Towards a unified theory of plant defense, pp. 39–56,in W. J. Mattson, J. Levieux, and C. Bernard-Dagan (eds.). Mechanisms of Woody Plant Defenses Against Insects: Search for Pattern. Springer, New York.

    Google Scholar 

  • Berryman, A. A., Dennis, B., Raffa, K. F., andStenseth, N. C. 1985. Evolution of optimal group attack, with particular reference to bark beetles (Coleoptera: Scolytidae).Ecology 66:898–903.

    Google Scholar 

  • Bordasch, R. P., andBerryman, A. A. 1977. Host resistance to the fir engraver beetle,Scolytus ventralis (Coleoptera: Scolytidae) 2. Repellency ofAbies grandis resins and some monoterpenes.Can. Entomol. 109:95–100.

    CAS  Google Scholar 

  • Bridges, J. R. 1987. Effets of terpenoid compounds on growth of symbiotic fungi associated with the southern pine beetle.Phytopathology 77:83–85.

    CAS  Google Scholar 

  • Bridges, J. R., andPerry, T. J. 1985. Effects of mycangial fungi on gallery construction and distribution of bluestain in southern pine beetle-infested pine bolts.J. Entomol. Sci. 20:271–275.

    Google Scholar 

  • Cheniclet, C., Bernard-Dagan, C., andPauly, G. 1988. Terpene biosynthesis under pathological conditions, pp. 93–116.in W. J. Mattson, J. Levieux, and C. Bernard-Dagan (eds.). Mechanisms of Woody Plant Defenses Against Insects: Search for Pattern. Springer, New York.

    Google Scholar 

  • Cobb, F. W., Jr., Krstic, M., Zavarin, E., andBarber, H. W., Jr. 1968. Inhibitory effects of volatile oleoresin components onFomes annosus and fourCeratocystis species.Phytopathology 58:1327–1335.

    CAS  Google Scholar 

  • Cook, S. P., andHain, F. P. 1986. Defensive mechanisms of loblolly and shortleaf pine against attack by southern pine beetle,Dendroctonus frontalis Zimmerman, and its fungal associate,Ceratocystis minor (Hedgecock) Hunt.J. Chem. Ecol. 12:1397–1406.

    Article  Google Scholar 

  • Coyne, J. F., andLott, L. H. 1976. Toxicity of substances in pine oleoresin to southern pine beetles.J. Ga. Entomol. Soc. 11:301–305.

    CAS  Google Scholar 

  • De Groot, R. C. 1972. Growth of wood-inhabiting fungi in saturated atmospheres of monoterpenoids.Mycologia 64:863–870.

    PubMed  Google Scholar 

  • Delorme, L., andLieutier, F. 1990. Monoterpene composition of the preformed and induced resins of Scots pine, and their effect on bark beetles and associated fungi.Eur. J. For. Pathol. 20:304–316.

    Google Scholar 

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

    Google Scholar 

  • Fox, J. W., Wood, D. L., Akers, R. P., andParmeter, J. R., Jr. 1993. Survival and development ofIps paraconfusus Lanier (Coleoptera: Scolytidae) reared axenically and with tree-pathogenic fungi vectored by cohabitingDendroctonus species.Can. Entomol. 125:1157–1167.

    Google Scholar 

  • Hain, F. P., Mawby, W. D., Cook, S. P., andArthur, F. H. 1983. Host conifer reaction to stem invasion.Z. Angew. Entomol. 96:247–256.

    Google Scholar 

  • Hammerschmidt, R. 1993. The nature and generation of systemic signals induced by pathogens, arthropod herbivores, and wounds.Adv. Plant Pathol. 10:307–337.

    Google Scholar 

  • Harrington, T. C. 1993. Diseases of conifers caused by species ofOphiostoma andLeptographium, pp. 161–172,in M. J. Wingfield, K. A. Seifert, and J. F. Webber (eds.),Ceratocystis andOphiostoma: Taxonomy, Ecology and Pathogenicity. American Phytopathological Society Press, St. Paul, Minnesota.

    Google Scholar 

  • Hemingway, R. W., McGraw, G. W., andBarras, S. J. 1977. Polyphenols inCeratocysis minor infectedPinus taeda: fungal metabolites of phloem and xylem phenols.J. Agric. Food Chem. 25:717–722.

    Article  CAS  Google Scholar 

  • Herms, D. A., andMattson, W. J. 1992. The dilemma of plants: to grow or defend.Q. Rev. Biol. 67:283–335.

    Article  Google Scholar 

  • Jorgensen, E. 1961. The formation of pinosylvin and its monomethyl ether in the sapwood ofPinus resinosa Ait.Can. J. Bot. 39:1765–1772.

    CAS  Google Scholar 

  • Klepzig, K. D. 1994. Interactions of stress, plant chemical defenses and subcortical insect-fungal complexes in red pine decline. PhD dissertation, University of Wisconsin, Madison, Wisconsin.

    Google Scholar 

  • Klepzig, K. D., Raffa, K. F., andSmalley, 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., Smalley, E. B., andRaffa, K. F. 1995a.Dendroctonus valens (Coleoptera: Scolytidae): Vectors of pathogenic fungi (Ophiostomatales) associated with red pine decline disease.Great Lakes Entomol. 28:81–87.

    Google Scholar 

  • Klepzig, K. D., Kruger, E. L., Smalley, E. B., andRaffa, K. F. 1995b. Effects of biotic and abiotic stress on induced accumulation of terpenes and phenolics in red pines inoculated with bark beetle vectored fungus.J. Chem. Ecol. 21:601–626.

    CAS  Google Scholar 

  • Krischik, V. A., Goth, R. W., andBarbosa, P. 1991. Generalized plant defense: Effects on multiple species.Oecologia 85:562–571.

    Article  Google Scholar 

  • Lewinsohn, E., Gijzen, M., Savage, T. J., andCroteau, R. 1991. Defense mechanisms of conifers.Physiol. Plant Pathol. 96:38–43.

    CAS  Google Scholar 

  • Lorio, P. L., Jr. 1986. Growth-differentiation balance: a basis for understanding southern pine beetle-tree interactions.For. Ecol. Manage. 14:259–273.

    Google Scholar 

  • Manion, P. D. 1991. Tree Disease Concepts, 2nd ed. Prentice-Hall, Englewood Cliffs, New Jersey, 402 pp.

    Google Scholar 

  • Miller, R. H., Berryman, A. A., andRyan, C. A. 1986. Biotic elicitors of defense reactions in lodgepole pine.Phytochemistry 25:611–612.

    Article  CAS  Google Scholar 

  • Paine, T. D., andHanlon, C. C. 1994. Influence of oleoresin constituents fromPinus ponderosa andPinus jeffreyi on growth of mycangial fungi fromDendroctonus ponderosae andDendroctonus jeffreyi.J. Chem. Ecol. 20:2551–2563.

    CAS  Google Scholar 

  • Paine, T. D., Blanche, C. A., Nebeker, T. E., andStephen, F. M. 1987. Composition of loblolly pine resin defenses: Comparison of monoterpenes from induced lesion and sapwood resin.Can. J. For. Res. 17:1202–1206.

    CAS  Google Scholar 

  • Raffa, K. F., andBerryman, A. A. 1982. Accumulation of monoterpenes and associated volatiles following fungal inoculation of grand fir with a fungus vectored by the fir engraverScolytus ventralis (Coleoptera: Scolytidae).Can. Entomol. 114:797–810.

    CAS  Google Scholar 

  • Raffa, K. F., andBerryman, A. A. 1983a. The role of host plant resistance in the colonization behavior and ecology of bark beetles.Ecol. Monogr. 53:27–49.

    Google Scholar 

  • Raffa, K. F., andBerryman, A. A. 1983b. Physiological aspects of lodgepole pine wound responses to a fungal symbiont of the mountain pine beetle,Dendroctonus ponderosae (Coleoptera: Scolytidae).Can. Entomol. 115:723–734.

    Article  Google Scholar 

  • Raffa, K. F., andKlepzig, K. D. 1996. Effects of root inhabiting insect-fungal complexes on aspects of host resistance to bark beetles,in W. Mattson and P. Niemela (eds.). Dynamics of Herbivory: Quest for Pattern and Principle. USDA Forest Service, General Technical Report 183. North Central Forest Experiment Station, St. Paul, Minnesota. In press.

    Google Scholar 

  • Raffa, K. F., andSmalley, E. B. 1988. Response of red and jack pines to inoculation with microbial associated of the pine engraver,Ips pini (Coleoptera: Scolytidae).Can. J. For. Res. 18:581–586.

    Google Scholar 

  • Raffa, K. F., andSmalley, E. B. 1995. Interaction of pre-attack and induced monoterpene concentrations in conifer defense against bark beetle-microbial complexes.Oecologia 102:285–295.

    Article  Google Scholar 

  • Raffa, K. F., Berryman, A. A., Simasko, J., Teal, W., andWong, B. L. 1985. Effects of grand fir monoterpenes on the fir engraver,Scolytus ventralis (Coleoptera: Scolytidae), and its symbiotic fungus.Environ. Entomol. 14:552–556.

    CAS  Google Scholar 

  • Russell, C. E., andBerryman, A. A. 1976. Host resistance to the fir engraver beetle. I. Monoterpene composition ofAbies grandis pitch blisters and fungus-infected wounds.Can. J. Bot. 54:14–18.

    Article  Google Scholar 

  • SAS Insitute. 1982. SAS user's guide: Statistics. Cary, North Carolina.

    Google Scholar 

  • Schowalter, T. D., andFilip, G. M. (eds.). 1993. Beetle-Pathogen Interactions in Conifer Forests. Academic Press, San Diego, California.

    Google Scholar 

  • Schultz, J. C. 1983. Impact of variable plant chemical defenses on insect susceptibility to parasites, predators, and diseases.Symp. Am. Chem. Soc. 208:37–55.

    Google Scholar 

  • Shain, L. 1967. Resistance of sapwood in stems of loblolly pine to infection byFomes annosus.Phytopathology 57:1034–1045.

    Google Scholar 

  • Shrimpton, D. M., andWhitney, H. S. 1968. Inhibition of growth of blue stain fungi by wood extractives.Cam. J. Bot. 46:757–761.

    Article  CAS  Google Scholar 

  • Smith, R. H. 1963. Toxicity of pine resin vapors to three species ofDendroctonus bark beetles.J. Econ. Entomol. 56:827–831.

    CAS  Google Scholar 

  • Whitney, J. H. 1982. Relationships between bark beetles and symbiotic organisms. pp. 183–211,in J. B. Mitton and K. B. Sturgeon (eds.). Bark Beetles in North American Forests: A System for the Study of Evolutionary Biology. University of Texas Press, Austin, Texas.

    Google Scholar 

  • Wright, E. 1933. A cork-borer method for inoculating trees.Phyytopathology 23:487–488.

    Google Scholar 

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Klepzig, K.D., Smalley, E.B. & Raffa, K.F. Combined chemical defenses against an insect-fungal complex. J Chem Ecol 22, 1367–1388 (1996). https://doi.org/10.1007/BF02027719

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