Abstract
We conducted defoliation experiments with 7- to 8-year-old clones of Douglas fir [Pseudotsuga menziesii (Mirb.) Franco var. glauca] to assess the role of monoterpenes as a resistance mechanism to western spruce budworm (Choristoneura occidentalis Freeman) defoliation. The grafted clones were derived from mature trees that showed resistance or susceptibility to budworm defoliation in the forest. All clones were exposed to either budworm defoliation or nondefoliation treatments in 1998 and 1999 under greenhouse conditions. We found that the total concentration of monoterpenes in current-year foliage varied greatly between two consecutive years in clones in the greenhouse and in their corresponding mature trees in the forest. Fractional composition of different monoterpenes was similar between different years and between clones and mature trees, indicating genetic control of this trait. Two different defoliation experiments were conducted to assess the importance of budburst phenology as a factor determining host plant resistance. In the 1998 experiment, budworm feeding was matched to the budburst of each individual plant. Monoterpene concentration was high in 1998, and budworm potential fitness was greater on clones from the resistant mature trees that had lower concentrations of total monoterpenes. In the 1999 experiment, budworm feeding was matched to budburst of the whole population of plants in order to mimic conditions similar to insects feeding on trees in the field. The concentration of monoterpenes was low in 1999, and budworm fitness was not related to monoterpenes. Total monoterpene concentration was negatively related to foliar nitrogen concentration, suggesting that C/N balance may affect monoterpene synthesis in needles. However, tree growth was not related to total monoterpene concentration. We concluded that expression of differences in budworm resistance among Douglas fir genotypes might be caused by interactions among multiple resistance mechanisms such as needle monoterpenes and tree budburst phenology.
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REFERENCES
Annila, E., Hiltunen, R., and Loyttyniemi, R. 1984.Defoliation by Neodiprion sertifer (Hymenoptera,Diprionidae) in relation to the terpene composition of Pinus contorta.Ann. Entomol. Fenn. 50:33–36.
Bryant, J. P., Chapin, F. S., and Klein, D. R. 1983.Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory.Oikos 40:357–368.
Cates, R. G. and Redak, R. A.1988. Variation in the terpene chemistry of Douglas-fir and its relationship to western spruce budworm success, pp. 317–341, inK. C. Spencer (ed.).Chemical Mediation of Coevolution.Academic Press, San Diego, California.
Cates, R. G. and Zou, J. 1990.Douglas-fir (Pseudotsuga menziesii) terpene chemistry and its role in budworm (Choristoneura occidentalis) dynamics, pp. 69–182, inA. Watt, S. Leatyer, M. Honter, and N. Kidd (eds.). Population Dynamics of Forest Insects. Intercept Ltd., London.
Cates, R. G., Redak, R., and Henderson, C. 1983.Pattern in defensive natural product chemistry:Douglas-fir and western spruce budworm interaction.Am. Chem. Soc. Symp. Ser. 208:3–19.
Cates, R. G., Henderson, C., and Redak, R. 1987.Responses of western spruce budworm to varying levels of nitrogen and terpenes.Oecologia73:372–316.
Chen, Z., Kolb, T. E., and Clancy, K. M. 2001a.Mechanisms of Douglas-fir resistance to western spruce budworm defoliation: Budburst phenology, photosynthetic compensation, and growth rate. Tree Physiol.21:1159–1169.
Chen, Z., Kolb, T. E., Clancy, K. M., Hipkins, V. D., and Dewald, L. E. 2001b. Allozyme variation in interior Douglas-fir: Association with growth and resistance to western spruce budworm herbivory.Can. J. For. Res. 31:1691–1700.
Clancy, K. M. 1991a. Douglas-fir nutrients and terpenes as potential factors influencing western spruce budworm defoliation, pp. 124–134, in Y. N. Baranchikov, W. J. Mattson, F. Pain, and T. L. Payne (eds.).Forest Insect Guilds: Patterns of Interaction with Host Trees.USDA Forest Service General Technical Paper NE-153.
Clancy, K. M.1991b. Multiple-generation bioassay for investigating western spruce budworm (Lepidoptera: Tortricidae) nutritional ecology.Environ. Entomol.20:1363–1374.
Clancy, K. M.1992.Response of western spruce budworm (Lepidoptera: Tortricidae) to increased nitrogen in artificial diets.Environ. Entomol.21:331–344.
Clancy, K. M. 1993.Are terpenes defensive compounds for the western spruce budworm? Suppl. Bull. Ecol. Soc. Am.74:193.
Clancy, K. M.2001. Biochemical characteristics of Douglas-fir trees resistant to damage from the western spruce budworm: patterns from three populations, pp. 115–125, in R. I. Alfaro, K. Day, S. Salom, A. Liebhold, H. Evans, F. Lieutier, M. Wagner, K. Futai, K. Suzuki, and K. S. S. Nair (eds.). Protection of World Forests: Advances in Research.IUFRO World Series No.IUFRO Secretariat, Vienna, Austria.
Clancy, K. M., Wagner, M. R., and Tinus, R. W.1988a.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, New York.
Clancy, K. M., Wagner, M. R., and Tinus, R. W. 1988b. Variation in host foliage nutrient concentrations in relation to western spruce budworm herbivory.Can. J. For. Res.18:530–539.
Clancy, K. M., Foust, R. D., Huntsberger, T. G., Whitaker, J. G., and Whitaker, D. M.1992.Technique for using microencapsulated terpenes in lepidopteran artificial diets.J. Chem. Ecol. 18:543–560.
Clancy, K. M., Itami, J. K., and Huebner, D. P. 1993. Douglas-fir nutrients and terpenes: potential resistance factors to western spruce budworm defoliation.For. Sci. 39:78–94.
Clancy, K. M., Wagner, M. R., and Reich, P. B.1995.Ecophysiology and insect herbivory, pp. 125–180, in W. K. Smith and T. M. Hinckley (eds.). Ecophysiology of Coniferous Forests. Academic Press, San Diego, California.
Dodds, K. A., Clancy, K. M., Leyva, K. J., Greenberg, D., and Price, P. W. 1996.Effects of Douglas-fir foliage age class on western spruce budworm oviposition choice and larval performance. Great Basin Nat. 56:135–141.
Felipe, B. L., Hasegawa, M., and Cedeno, A.1994.Mono-and sequisterpene variation in Pinus caribaea needles and its relationship to Atta laevigata herbivory.Biochem. Syst. Ecol.22:437–445.
Gambliel, H. and Cates, R.1995. Terpene changes due to maturation and canopy level in Douglas-fir (Pseudotsuga menziesii) flush needle oil.Biochem. Syst. Ecol.23:469–476.
Gershenzon, J. 1994.The cost of plant chemical defense against herbivory: a biochemical perspective, pp.105–173, in E. A. Bernays (ed.). Insect–Plant Interactions, Vol.5.CRC Press, Boca Roton, Florida.
Gershenzon, J. and Croteau, R. 1991. Terpenoids, pp. 165–219, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores, Their Interactions with Secondary Metabolites, the Chemical Participants. Academic Press, New York.
Hanover, J. W.1992.Applications of terpene analysis in forest genetics.New For.6:159–178.
Hanula, J. L., Berisford, C. W., and Debarr, G. L. 1985.Monoterpene oviposition stimulants of Dioryctria amatella in volatiles from fusiform rust galls and second-year loblolly pine cones. J. Chem. Ecol.11:943–952.
Harborne, J. B. 1991.Recent advances in the ecological chemistry of plant terpenoids, pp.399–426, in J. B. Harborne and F. A. Tomes-Barberan (eds.). Ecological Chemistry and Biochemistry of Plant Terpenoids.Clarenden Press, Oxford. THE ROLE OF MONOTERPENES IN RESISTANCE OF DOUGLAS FIR 919
Hartmann, H. T. and Kester, D. E. (eds.). 1983.Plant Propagation: Principles and Practices. Prentice-Hall, Inc. Englewood, Cliffs, New Jersey.
Hedin, P. A., Maxwell, F. G., and Jekins, J. N.1974.Insect plant attractants, feeding stimulants,repellents, deterrents, and other related factors affecting insect behavior, pp. 497–557, in F. G. Maxwell and F. A. Harris (eds.).Proc. Summer Insect Biological Control of Plant Insects and Diseases. University of Mississippi Press, Jackson, Mississippi.
Johnson, R. H., Young, B. L., and Alstad, D. N.1997.Responses of ponderosa pine growth and volatile terpene concentrations to manipulation of soil water and sunlight availability.Can. J. For. Res.27:1794–1804.
Kogan, M.1975. Plant resistance in pest management. pp. 103–146, inR. L. Metcalf and W. H. Luckman (eds.). Introduction to Insect Pest Management.Wiley, New York.
Langenheim, J. H.1994.Higher plant terpenoids: A phytocentric overview of their ecological roles. J. Chem. Ecol. 20:223–1280.
Larsson, S., Oren, R., Waring, R. H., and Barrett, J. W. 1983.Attacks of mountain pine beetle as related to tree vigor of ponderosa pine.For. Sci.29:395–402.
Latta, R. G., Linhart, Y. B., Lundquist, L., and Snyder, M. A.2000.Patterns of monoterpene variation within individual trees in ponderosa pine.J. Chem. Ecol.26:1341–1357.
Lerdau, M., Matson, P., Fall, R., and Monson, R.1995. Ecological controls over monoterpene emissions from Douglas-fir (Pseudotsuga menziesii).Ecology76:2640–2647.
Leyva, K. J., Clancy, K. M., and Price, P. W. 1995.Performance of wild versus laboratory populations of western spruce budworm (Lepidoptera: Tortricidae) feeding on Douglas-fir foliage.Environ. Entomol.24:80–87.
Manninen, A. M., Vuorinen, M., and Holopainen, J.K.1998.Variation in growth, chemical defense, and herbivore resistance in Scots pine provenances.J. Chem. Ecol.24:1315–1331.
Mattson, W. J. and Haack, R. A. 1987.The role of drought stress in provoking outbreaks of phytophagus insects, pp. 365–407, inP. Barbosaand Schultz, J. C. (eds.). Insect Outbreaks. Academic Press, Toronto.
Mattson, W. J. and Scriber, J. M. 1987.Nutritional ecology of insect folivores of woody plants: water, nitrogen, fiber, and mineral considerations, pp.105–146, inF. Slansky,Jr., and J. Rodriguez (eds.). Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates.Wiley, NewYork.
McClure, M. S. and Hare, J. D. 1984.Foliar terpenoids in Tsuga species and the fecundity of scale insects.Oecologia63:185–193.
McKinnon, M. L., Quiring, D. T., and Bauce, E. 1998.Influence of resource availability on growth and foliar chemistry within and among young white spruce trees.EcoScience5:295–305.
Nault, J. R., Manville, J. F., and Sahota, T. S. 1999.Spruce terpenes: Expression and weevil resistance.Can. J. For. Res.29:761–767.
Redak, R. and Cates, R. G. 1984.Douglas-fir (Pseudotsuga menziesii)–spruce budworm (Choristoneuraoccidentalis) interactions: The effect of nutrition, chemical defenses, tissue phenology, and tree physical parameters on budworm success.Oecologia62:61–67.
SAS Institute. 1995.JMP Statistics and Graphics Guide,Version 3. SAS Institute, Cary, North Carolina.
Shepherd, R. F.1983.A technique to study phenological interactions between Douglas-fir buds and emerging second-instar western spruce budworm, pp. 17–20, inR. L. Talerico, and M. Montgomery (eds.) Forest Defoliator–Host Interactions: A Comparison between Gypsy Moth and Spruce Budworms.USDA Forest Service General Technical Report NE-85.
Tomlin, E. S., Borden, J. H., and Pierce, H. D., Jr. 1997.Relationship between volatile foliar terpenes and resistance of Sitka spruce to the white pine weevil.For. Sci.43:501–508.
vonRudloff, E. and Rehfeldt, G. E. 1980. Chemosystematics studies in the genus Pseudotsuga. IV. Inheritance and geographic variation in the leaf oil terpenes of Douglas-fir for the Pacific Northwest.Can. J. For. Res. 58:546–556.
Wagner, M. R. and Zhang, Z. 1993.Host plant traits associated with resistance of ponderosa pine to the sawfly, Neodiprion fulviceps.Can. J. For. Res.23:839–845.
Wagner, M. R., Clancy, K. M., and Kirkbride, D. M.1987. Predicting number of oocytes in adult western spruce budworm, Choristoneura occidentalis (Lepidoptera: Tortricidae). Environ. Entomol.16:551–555.
Wagner, M. R., Clancy, K. M., and Tinus, R.W.1989.Maturational variation in needle essential oils from Pseudotsuga menziesii, Abies concolor, and Picea engelmannii.Phytochemistry 28:765–770.
Wilkinson, R. C. 1985.Comparative white-pine weevil attack susceptibility and cortical monoterpene composition of western and eastern white pines.For. Sci.31:39–42.
Zobel, B. and Talbert, J. (eds.). 1984. Applied Forest Tree Improvement.Waveland Press, Prospect Heights, Illinois.
Zou. J. and Cates, R. G. 1995. Foliage constituents of Douglas-fir (Pseudotsuga menziesii): Their seasonal variation and potential role in Douglas-fir resistance and silviculture management.J. Chem. Ecol. 21:387–402.
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Chen, Z., Kolb, T.E. & Clancy, K.M. The Role of Monoterpenes in Resistance of Douglas Fir to Western Spruce Budworm Defoliation. J Chem Ecol 28, 897–920 (2002). https://doi.org/10.1023/A:1015297315104
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DOI: https://doi.org/10.1023/A:1015297315104