Skip to main content Accessibility help
×
Home

Differences in the constitutive terpene profile of lodgepole pine across a geographical range in British Columbia, and correlation with historical attack by mountain pine beetle

  • Erin L. Clark (a1), Allan L. Carroll (a2) and Dezene P.W. Huber (a1)

Abstract

The mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Curculionidae), is a destructive insect pest in western Nearctic conifer forests. Currently, British Columbia, Canada, is experiencing the largest recorded outbreak of this insect, including areas that historically have had low climatic suitability for it. We analyzed 26 constitutive resin terpenes in phloem samples from British Columbia lodgepole pine (Pinus contorta) populations to test for differential resistance to mountain pine beetle attack, based upon the likelihood of previous exposure to mountain pine beetle. We assessed sampled trees for number of mountain pine beetle attacks, number of pupal chambers, and tree survival the following spring. Significant differences were found when levels of certain terpenes in lodgepole pine populations that had likely experienced substantial mountain pine beetle infestations in the past were compared with those in populations that likely had not experienced large outbreaks of mountain pine beetle. Although we expected southern pine populations to contain more total terpenes than northern populations, owing to higher historical exposure to the beetle, the converse was found. Northern populations generally had higher levels of constitutive terpenes and beetle attack than southern populations. Because several terpenes are kairomones to the mountain pine beetle and also serve as precursors for the synthesis of pheromones, the lower levels of terpenes expressed by lodgepole pines from the historical range of the mountain pine beetle may render them less chemically perceptible to foraging beetles.

Le dendroctone du pin ponderosa, Dendroctonus ponderosae Hopkins (Coleoptera : Curculionidae), est un insecte ravageur des forêts de conifères de l'Ouest néarctique. À présent, la Colombie-Britannique connaît l'épidémie la plus importante signalée de cet insecte, même dans des régions dont le climat dans le passé a été peu propice à ce coléoptère. Nous avons analysé 26 terpènes constitutifs dans des échantillons de phloème de populations de pins vrillés (Pinus contorta) de la Colombie-Britannique pour tester leurs différences de résistance aux attaques du dendroctone du pin ponderosa basées sur la probabilité d'expositions antérieures au dendroctone du pin ponderosa. Nous avons déterminé chez les arbres échantillonnés le nombre d'attaques par le dendroctone du pin ponderosa, le nombre de chambres nymphales et la survie des arbres au printemps suivant. Il existe des différences significatives de concentrations de certains terpènes entre les populations qui ont vraisemblablement connu d'importantes infestations de dendroctones du pin ponderosa dans le passé et les populations qui n’ont pas subi de telles grandes infestations du dendroctone du pin ponderosa. Bien que nous nous attendions à ce que les populations du sud contiennent plus de terpènes totaux que les populations du nord à cause de leur plus forte exposition dans le passé aux coléoptères, c’est l'inverse qui prévaut. Les populations nordiques ont généralement de plus fortes concentrations de terpènes constitutifs et de plus forts taux d'attaques des coléoptères que les populations du sud. Parce que plusieurs des terpènes sont des kairomones du dendroctone du pin ponderosa et servent de précurseurs dans la synthèse des phéromones, les concentrations plus faibles de terpènes affichées par les pins vrillés dans l'aire de répartition historique du dendroctone du pin ponderosa peut les rendre chimiquement moins perceptibles aux coléoptères en recherche de nourriture.

[Traduit par la Rédaction]

Copyright

Corresponding author

1 Corresponding author (e-mail: eclark1@unbc.ca).

References

Hide All
Amman, G.D. 1972. Mountain pine beetle brood production in relation to thickness of lodgepole pine phloem. Journal of Economic Entomology, 65: 138140.
Amman, G.D., and Cole, W.E. 1983. Mountain pine beetle dynamics in lodgepole pine forests. Part II: Population dynamics. United States Forest Service General Technical Report INT-145.
Amman, G.D., and Pace, V.E. 1976. Optimum egg gallery densities for the mountain pine beetle in relation to lodgepole pine phloem thickness. United States Forest Service Research Note INT-209.
Atkins, M.D. 1966. Behavioral variation among scolytids in relation to their habitat. The Canadian Entomologist, 98: 285288. doi:10.4039/Ent98285-3.
Bell, W.J. 1990. Searching behaviour: the behavioural ecology of finding resources. Chapman and Hall, New York.
Berryman, A.A. 1976. Theoretical explanation of mountain pine beetle dynamics in lodgepole pine forests. Environmental Entomology, 5: 12251233.
Borden, J.H. 1985. Aggregation pheromones. In Comprehensive insect physiology, biochemistry, and pharmacology. Edited by Kerkut, G.A. and Gilbert, L.I.. Pergamon Press, Oxford, United Kingdom. pp. 257285.
Borden, J.H., Ryker, L.J., Chong, L.J., Pierce, F., Johnston, B.D., and Oehlschlager, A.C. 1987. Response of the mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae), to five semiochemicals in British Columbia lodgepole pine forests. Canadian Journal of Forest Research, 17: 118128. doi:10. 1139/x87-023.
Carroll, A.L., Taylor, S.W., Régnière, J., and Safranyik, L. 2004. Effects of climate change on range expansion by the mountain pine beetle in British Columbia. In Proceedings of the Mountain Pine Beetle Symposium: Challenges and Solutions, Kelowna, British Columbia, 30–31 October 2003. Edited by Shore, T.L.Brooks, J.E., and Stone, J.E.. Natural Resources Canada, Victoria, British Columbia. pp. 223232.
Christiansen, E., Waring, R.H., and Berryman, A.A. 1987. Resistance of conifers to bark beetle attack: searching for general relationships. Forest Ecology and Management, 22: 89106. doi:10.1016/0378-1127(87)90098-3.
Cole, W.E., and Amman, G.D. 1969. Mountain pine beetle infestations in relation to lodgepole pine diameters. United States Forest Service. INT-95.
Cole, W.E., Guymon, E.P., Jensen, C.E. 1981. Monoterpenes of lodgepole pine phloem as related to mountain pine beetles. United States Forest Service Research Paper INT-281.
Conn, J.E., Borden, J.H., Scott, B.E., Friskie, L.M., Pierce, H.D. Jr, and Oehlschlager, A.C. 1983. Semiochemicals for the mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Scolytidae) in British Columbia: field trapping studies. Canadian Journal of Forest Research, 13: 320324. doi:10.1139/x83-045.
Conn, J.E., Borden, J.H., Hunt, D.W.A., Holman, J., Whitney, H.S., Spanier, O.J., Pierce, H.D. Jr, and Oehlschlager, A.C. 1984. Pheromone production by axenically reared Dendroctonus ponderosae and Ips paraconfusus (Coleoptera: Scolytidae). Journal of Chemical Ecology, 10: 281290. doi:10.1007/BF00987856.
Coyne, J.F., and Lott, L.H. 1976. Toxicity of substances in pine oleoresin to southern pine beetles. The Journal of the Georgia Entomological Society, 11: 297301.
Craighead, F.C., Miller, J.M., Evenden, J.C., and Keen, F.P. 1931. Control work against bark beetles in western forests and an appraisal of its results. Journal of Forestry, 29: 10011018.
Dahlsten, D.L. 1982. Relationship between bark beetles and their natural enemies. In Bark beetles in North American conifers: a system for the study of evolutionary biology. Edited by Mitton, J.B. and Sturgeon, K.B.. University of Texas Press, Austin, Texas. pp. 140182.
Elkinton, J.S., and Wood, D.L. 1980. Feeding and boring behavior of the bark beetle Ips paraconfusus (Coleoptera: Scolytidae) on the bark of a host and its non-host tree species. The Canadian Entomologist, 112: 797809. doi:10.4039/Ent112797-8.
Forrest, G.I. 1980. Geographical variation in the monoterpenes of Pinus contorta oleoresin. Biochemical Systematics and Ecology, 8: 343359. doi:10.1016/0305-1978(80)90037-X.
Franceschi, V.R., Krokene, P., Christiansen, E., and Krekling, T. 2005. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytologist, 167: 353376. PMID: 15998390 doi:10.1111/j.1469-8137.2005.01436.x.
Franklin, E.C., and Snyder, E.B. 1971. Variation and inheritance of monoterpene composition in longleaf pine. Forest Science, 17: 178179.
Gershenzon, J., and Croteau, R.B. 1991. Terpenoids. In Herbivores: their interactions with secondary plant metabolites. Edited by Rosenthal, G.A. and Berembaum, M.R.. Academic Press, San Diego, California. pp. 165219.
Gilmore, A.R. 1977. Effects of soil moisture stress on monoterpenes in loblolly pine. Journal of Chemical Ecology, 3: 667676. doi:10.1007/BF00988066.
Hanover, J.W. 1966. Genetics of terpenes: I. Gene control of monoterpene levels in Pinus monticola Dougl. Heredity, 21: 7384. doi:10.1038/hdy.1966.5.
Hanover, J.W., and Furniss, M.M. 1966. Monoterpene concentration in Douglas-fir in relation to geographic location and resistance to attack by the Douglas-fir beetle. In Joint Proceedings of the Second Genetics Workshop of the Society of American Foresters and the Seventh Lake States Forest Tree Improvement Conference. United States Forest Service Research Paper NC-6. pp. 2328.
Herms, D.A., and Mattson, W.J. 1992. The dilemma of plants: to grow or defend. The Quarterly Review of Biology, 67: 283335. doi:10.1086/417659.
Huber, D.P.W., Gries, R., Borden, J.H., and Pierce, H.D. Jr 2003. A survey of antennal responses by five species of coniferophagous bark beetles (Coleoptera: Scolytidae) to bark volatiles of six species of angiosperm trees. Chemoecology, 10: 103113. doi:10.1007/PL00001811.
Huber, D.P.W., Ralph, S., and Bohlmann, J. 2004. Genomic hardwiring and phenotypic plasticity of terpenoid-based defenses in conifers. Journal of Chemical Ecology, 30: 23992418. PMID:15724963 doi:10.1007/s10886-004-7942-2.
Hughes, P.R. 1973. Effect of α-pinene exposure on trans-verbenol synthesis in Dendroctonus ponderosae Hopk. Naturwissenschaften, 60: 261262. doi:10.1007/BF00625726.
Hunt, D.W.A., Borden, J.H., Lindgren, B.S., and Gries, G. 1989. The role of autoxidation of α-pinene in the production of pheromones of Dendroctonus ponderosae (Coleoptera: Scolytidae). Canadian Journal of Forest Research, 19: 12751282.
Hynum, B.G., and Berryman, A.A. 1980. Dendroctonus ponderosae (Coleoptera: Scolytidae): Preaggregation landing and gallery initiation on lodgepole pine. The Canadian Entomologist, 112: 185191. doi:10.4039/Ent112185-2.
Keeling, C.I., and Bohlmann, J. 2006. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defense of conifers against insects and pathogens. New Phytologist, 170: 657675. PMID:16684230 doi:10.1111/j.1469-8137.2006.01716.x.
Klepzig, K.D., Kruger, E.L., Smalley, E.B., and Raffa, K.F. 1995. Effects of biotic and abiotic stress on induced accumulation of terpenes and phenolics in red pines inoculated with bark beetle-vectored fungus. Journal of Chemical Ecology, 21: 601626. doi:10.1007/BF02033704.
Klepzig, K.D., Smalley, E.B., and Raffa, K.F. 1996. Combined chemical defenses against an insect–fungal complex. Journal of Chemical Ecology, 22: 13671388. doi:10.1007/BF02027719.
Lee, S., Kim, J.-J., and Breuil, C. 2006. Pathogenicity of Leptographium longiclavatum associated with Dendroctonus ponderosae to Pinus contorta. Canadian Journal of Forest Research, 36: 28672872. doi:10.1139/X06-194.
Lewinsohn, E., Gijzen, M., Muzika, R.M., Barton, K., and Croteau, R. 1993. Oleoresinosis in grand fir (Abies grandis) saplings and mature trees. Plant Physiology, 101: 10211028. PMID:12231755.
Logan, J.A., and Powell, J.A. 2001. Ghost forests, global warming, and the mountain pine beetle (Coleoptera: Scolytidae). American Entomologist, 47: 160172.
Mickey, R.M., Dunn, O.J., and Clark, V.A. 2004. Applied statistics analysis of variance and regression. JohnWiley&Sons, Inc., Hoboken, NewJersey.
Mitton, J.B., and Sturgeon, K.B. 1982. Biotic interactions and evolutionary change. In Bark beetles in North American conifers: a system for the study of evolutionary biology. Edited by Mitton, J.B. and Sturgeon, K.B.. University of Texas Press, Austin, Texas. pp. 320.
Moeck, H.A., and Simmons, C.S. 1991. Primary attraction of mountain pine beetle, Dendroctonus ponderosae Hopk. (Coleoptera: Scolytidae), to bolts of lodgepole pine. The Canadian Entomologist, 123: 299304. doi:10.4039/Ent123299-2.
Pitman, G.B. 1971. Trans-verbenol and alphapinene: their utility in manipulation of the mountain pine beetle. Journal of Economic Entomology, 64: 426430.
Pureswaran, D.S., and Borden, J.H. 2003. Test of semiochemical mediated host specificity in four species of tree killing bark beetles (Coleoptera: Scolytidae). Environmental Entomology, 32: 963969. doi:10.1603/0046-225X-32.5.963.
Pureswaran, D.S., Gries, R., and Borden, J.H. 2004. Quantitative variation in monoterpenes in four species of conifers. Biochemical Systematics and Ecology, 32: 11091136. doi:10.1016/j.bse.2004.04.006.
Pureswaran, D.S., Sullivan, B.T., and Ayres, M.P. 2006. Fitness consequences of pheromone production and host selection strategies in a treekilling bark beetle (Coleoptera: Curculionidae: Scolytinae). Oecologia, 148: 720728. doi:10.1007/s00442-006-0400-9.
R Development Core Team. 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available from http://www.R-project.org [accessed September 2008].
Raffa, K.F., and Berryman, A.A. 1982. Physiological differences between lodgepole pines resistant and susceptible to the mountain pine beetle and associated microorganisms. Environmental Entomologist, 11: 486492.
Raffa, K.F., and Berryman, A.A. 1983 a. Physiological aspects of lodgepole pine wound responses to a fungal symbiont of the mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Scolytidae). The Canadian Entomologist, 115: 723734. doi:10.4039/Ent115723-7.
Raffa, K.F., and Berryman, A.A. 1983 b. The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleoptera: Scolytidae). Ecological Monographs, 53: 2749. doi:10.2307/1942586.
Raffa, K.F., and Berryman, A.A. 1987. Interacting selective pressures in conifer 2 bark beetle systems: a basis for reciprocal adaptations? The American Naturalist, 129: 234262. doi:10.1086/284633.
Raffa, K.F., Aukema, B.H., Bentz, B.J., Carroll, A.L., Hicke, J.A., Turnder, M.G., and Romme, W.H. 2008. Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. BioScience, 58: 501517. doi:10.1641/B580607.
Reid, R.W., Whitney, H.S., and Watson, J.A. 1967. Reactions of lodgepole pine to attack by Dendroctonus ponderosae Hopkins and blue stain fungi. Canadian Journal of Botany, 45: 11151126. doi:10.1139/b67-116.
Rockwood, D.L. 1973. Variation in the monoterpene composition of two oleoresin systems of loblolly pine. Forest Science, 19: 147153.
Rudinsky, J.A. 1962. Ecology of Scolytidae. In Annual review of entomology. Edited by Steinhaus, E.A. and Smith, R.F.. Annual Reviews, Inc., Palo Alto, California. pp. 327348.
Safranyik, L., and Carroll, A.L. 2006. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests. In The mountain pine beetle: a synthesis of biology, management, and impacts on lodgepole pine. Edited by Safranyik, L. and Wilson, W.R.. Pacific Forestry Centre, Canadian Forest Service, Natural Resources Canada, Victoria, British Columbia. pp. 366.
Safranyik, L., Shrimpton, D.M., and Whitney, H.S. 1974. Management of lodgepole pine to reduce losses from the mountain pine beetle. Victoria, BC. Technical Report No. 1, Pacific Forestry Centre, Canadian Forest Service, Natural Resources Canada, Victoria, British Columbia.
Seybold, S.J., Huber, D.P.W., Lee, J.C., Graves, A.D., and Bohlmann, J. 2006. Pine monoterpenes and pine bark beetles: a marriage of convenience for defense and chemical communication. Phytochemistry Reviews, 5: 143178. doi:10.1007/s11101-006-9002-8.
Shepherd, R.F. 1966. Factors influencing the orientation and rates of activity of Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae). The Canadian Entomologist, 98: 507518. doi: 10.4039/Ent98507-5.
Smith, R.H. 1963. Toxicity of pine resin vapors to three species of Dendroctonus bark beetles. Journal of Economic Entomology, 56: 827831.
Smith, R.H. 1965. Effect of monoterpene vapors on the western pine beetle. Journal of Economic Entomology, 58: 509510.
Smith, R.H. 1975. Formula for describing effect of insect and host tree factors on resistance to western pine beetle attack. Journal of Economic Entomology, 68: 841844.
Smith, R.H. 1983. Monoterpenes of lodgepole pine xylem resin: a regional study in western United States. Forest Science, 29: 333340.
Squillace, A.E. 1971. Inheritance of monoterpene composition in cortical oleoresin of slash pine. Forest Science, 17: 381387.
Sturgeon, K.B. 1979. Monoterpene variation in ponderosa pine xylem resin related to western pine beetle predation. Evolution, 33: 803814. doi:10.2307/2407647.
Tabachnick, B.G., and Fidell, L.S. 2001. Using multivariate statistics. 4th ed. Allyn and Bacon, Boston, Massachusetts.
Taylor, S.W., and Carroll, A.L. 2004. Disturbance, forest age, and mountain pine beetle outbreak dynamics in BC: a historical perspective. In Mountain Pine Beetle Symposium: Challenges and Solutions, Kelowna, British Columbia, 30–31 October 2003. Edited by Shore, T.L., Brooks, J.E., and Stone, J.E.. Pacific Forestry Centre, Canadian Forest Service, Natural Resources Canada, Victoria, British Columbia. pp. 4151.
Thompson, J.N. 1997. Evaluating the dynamics of coevolution among geographically structured populations. Ecology, 78: 16191623. doi:10.1890/0012-9658(1997)078[1619:ETDOCA]2.0.CO;2.
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. Forest Science, 43: 501508.
Wallin, K.F., and Raffa, K.F. 1999. Altered constitutive and inducible phloem monoterpenes following natural defoliation of jack pine: implications to host mediated interguild interactions and plant defense theories. Journal of Chemical Ecology, 25: 861880. doi:10.1023/A:1020853019309.
Wallin, K.F., and Raffa, K.F. 2000. Influences of host chemicals and internal physiology on the multiple steps of postlanding host acceptance behavior of Ips pini (Coleoptera: Scolytidae). Environmental Entomology, 29: 442453. doi:10.1603/0046-225X-29.3.442.
Wallin, K.F., and Raffa, K.F. 2004. Feedback between individual host selection behavior and population dynamics in an eruptive herbivore. Ecological Monographs, 74: 101116. doi:10.1890/02-4004.
Waring, R.H., and Pitman, G.B. 1985. Modifying lodgepole pine stands to change susceptibility to mountain pine beetle attack. Ecology, 66: 889897. doi:10.2307/1940551.
Westfall, J., and Ebata, T. 2008. Summary of forest health conditions in British Columbia. Pest Management Report No. 15, British Columbia Ministry of Forests and Range, Victoria, British Columbia.
Wood, S.L. 1982. The bark and ambrosia beetles of North and Central America (Coleoptera: Scolytidae): a taxonomic monograph. Great Basin Naturalist Memoirs No. 6, Brigham Young University, Provo, Utah.

Differences in the constitutive terpene profile of lodgepole pine across a geographical range in British Columbia, and correlation with historical attack by mountain pine beetle

  • Erin L. Clark (a1), Allan L. Carroll (a2) and Dezene P.W. Huber (a1)

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed