Journal of Chemical Ecology

, Volume 37, Issue 8, pp 808–817 | Cite as

Responses of Bark Beetle-Associated Bacteria to Host Monoterpenes and Their Relationship to Insect Life Histories

  • Aaron S. Adams
  • Celia K. Boone
  • Jörg Bohlmann
  • Kenneth F. RaffaEmail author


Bark beetles that colonize living conifers and their microbial associates encounter constitutive and induced chemical defenses of their host. Monoterpene hydrocarbons comprise a major component of these allelochemicals, and many are antibiotic to insects, fungi, and bacteria. Some bark beetle species exhaust these defenses by killing their host through mass attacks mediated by aggregation pheromones. Others lack adult aggregation pheromones and do not engage in pheromone-mediated mass attacks, but rather have the ability to complete development within live hosts. In the former species, the larvae develop in tissue largely depleted of host terpenes, whereas in the latter exposure to these compounds persists throughout development. A substantial literature exists on how monoterpenes affect bark beetles and their associated fungi, but little is known of how they affect bacteria, which in turn can influence beetle performance in various manners. We tested several bacteria from two bark beetle species for their ability to grow in the presence of a diversity of host monoterpenes. Bacteria were isolated from the mountain pine beetle, Dendroctonus ponderosae Hopkins, which typically kills trees during colonization, and the red turpentine beetle, Dendroctonus valens LeConte, which often lives in their host without causing mortality. Bacteria from D. ponderosae were gram-positive Actinobacteria and Bacilli; one yeast also was tested. Bacteria from D. valens were Actinobacteria, Bacilli, and γ-Proteobacteria. Bacteria from D. valens were more tolerant of monoterpenes than were those from D. ponderosae. Bacteria from D. ponderosae did not grow in the presence of α-pinene and 3-carene, and grew in, but were inhibited by, β-pinene and β-phellandrene. Limonene and myrcene had little inhibitory effect on bacteria from either beetle species. Tolerance to these antibiotic compounds appears to have resulted from adaptation to living in a terpene-rich environment.

Key Words

Actinobacteria Bacillales Bacteria Dendroctonus ponderosae Dendroctonus valens Host defense Monoterpenes Polymerase chain reaction (PCR) γ-Proteobacteria 



We thank N. Erbilgin (University of Alberta, Edmonton, AB) and K. Bleiker (Canadian Forest Service, Victoria, BC, Canada) for assistance in collecting mountain pine beetles. C. Currie (University of Wisconsin, Madison, WI, USA) for use of the microplate reader and S. Adams (University of Wisconsin, Madison, WI, USA) for sequencing. This research was supported by funding from the USDA National Research Initiative (2003-3502-13528) and the Natural Sciences and Engineering Research Council of Canada, Genome Canada and Genome British Columbia. Helpful critiques by three anonymous reviewers improved the quality of our paper and are much appreciated.


  1. Adams, A. S., Adams, S. M., Currie, C. R., Gillette, N. E., and Raffa, K. F. 2010. Geographic variation in bacterial communities associated with the red turpentine beetle (Coleoptera: Curculionidae). Environ. Entomol. 39:406–414.PubMedCrossRefGoogle Scholar
  2. Adams, A. S., Currie, C. R., Cardoza, Y. J., Klepzig, K. D., and Raffa, K. F. 2009. Effects of symbiotic bacteria and tree chemistry on the growth and reproduction of bark beetle fungal symbionts. Can. J. For. Res. 39:1133–1147.CrossRefGoogle Scholar
  3. Adams, A. S., Six, D. L., Adams, S. M., and Holben, W. E. 2008. In vitro interactions between yeasts and bacteria and the fungal symbionts of the mountain pine beetle (Dendroctonus ponderosae). Microb. Ecol. 56:460–466.PubMedCrossRefGoogle Scholar
  4. Aukema, B. H., Carroll, A. L., Zhu, J., Raffa, K .F., Sickley, T. A., and Taylor, S. W. 2006. Landscape level analysis of mountain pine beetle in British Columbia, Canada: spatiotemporal developments and spatial synchrony within the present outbreak. Ecography 29:427–441.CrossRefGoogle Scholar
  5. Aukema, B. H., Zhu, J., Møller, J., Rasmussen, J. G., and Raffa, K. F. 2010. Predisposition to bark beetle attack by root herbivores and associated pathogens: roles in forest decline, gap formation, and persistence of endemic bark beetle populations. For. Ecol. Manag. 259:374–382.CrossRefGoogle Scholar
  6. Bentz, B. J., Logan, J., Macmahon, J., Allen, C. D., Ayres, M., Berg, E., Carroll, A., Hansen, M., Hicke, J., Joyce, L., Macfarlane, W., Munson, S., Negrón, J., Paine, T., Powell, J., Raffa, K., Régnière, J., Reid, M., Romme, B., Seybold, S. J., Six, D., Tomback, D., Vandygriff, J., Veblen, T., White, M., Witcosky, J., and Wood, D. 2009. Bark Beetle Outbreaks in Western North America: Causes and Consequences. University of Utah Press, Chicago, IL.Google Scholar
  7. Bentz, B. J., Régnière, J., Fettig, C. J., Hansen, E. M., Hayes, J. L., Hicke, J. A., Kelsey, R. G., Negrón, J. F., and Seybold, S. J. 2010. Climate change and bark beetles of the western United States and Canada: direct and indirect effects. BioScience 60:602–613CrossRefGoogle Scholar
  8. Berryman, A. A. 1986. Forest Insects: Principles and Practice of Population Management. Plenum Press, New York.Google Scholar
  9. Boone, C. K., Aukema, B. H., Bohlmann, J., Carroll, A. L., and Raffa, K. F. 2011. Efficacy of tree defense physiology varies with bark beetle population density: a basis for positive feedback in eruptive species. Can. J. For. Res. 41:1174–1188.CrossRefGoogle Scholar
  10. Boone, C. K., Six, D. L., and Raffa, K. F. 2008a. The enemy of my enemy is still my enemy: competitors add to predator load of a tree-killing bark beetle. Agric. For. Entomol. 10:411–421.CrossRefGoogle Scholar
  11. Boone, C. K., Six, D. L., Zheng, Y., and Raffa, K. F. 2008b. Exploitation of microbial symbionts of bark beetles by parasitoids and dipteran predators. Environ. Entomol. 37:150–161.PubMedCrossRefGoogle Scholar
  12. Borden, J. H., Pureswaran, D. S., and Lafontaine, J. P. 2008. Synergistic blends of monoterpenes for aggregation pheromones of the mountain pine beetle (Coleoptera: Curculionidae). J. Econ. Entomol. 101:1266–1275.PubMedCrossRefGoogle Scholar
  13. Brand, J. M., Schultz, J., Barras, S. J., Edson, L. F., Payne, T. L., and Hedden, R. L. 1977. Bark beetle pheromones: enhancement of Dendroctonus frontalis (Coleoptera: Scolytidae) aggregation pheromone by yeast metabolites in laboratory assays. J. Chem. Ecol. 3:657–666.CrossRefGoogle Scholar
  14. Brignolas, F., Lacroix, B., Lieutier, F., Sauvard, D., Drouet, A., Claudot, A. C., Yart, A., Berryman, A. A., and Christiansen, E. 1995. Induced responses in phenolic metabolism in two Norway spruce clones after wounding and inoculations with Ophiostoma polonicum, a bark beetle-associated fungus. Plant Physiol. 109:821–827.PubMedGoogle Scholar
  15. Cardoza, Y. J., Klepzig, K. D., and Raffa, K. F. 2006. Bacteria in oral secretions of an endophytic insect inhibit antagonistic fungi. Ecol. Entomol. 31:636–645.CrossRefGoogle Scholar
  16. Cardoza, Y. J., Vasanthakumar, A., Suazo, A., and Raffa, K. F. 2009. Survey and phylogenetic analysis of culturable microbes in the oral secretions of three bark beetle species. Entomol. Exp. Appl. 131:138–147.CrossRefGoogle Scholar
  17. Carroll, A., Taylor, S. W., Régnière, J., and Safranyik, L. 2003. Effects of climate change on range expansion by the mountain pine beetle in British Columbia, pp. 223–232, in T. L. Shore, J. E. Brooks, and J. E. Stone (eds.). Mountain Pine Beetle Symposium: Challenges and Solutions, Nat. Res. Ca., Can. For. Serv., Victoria, Report No. BC-X-399.Google Scholar
  18. Chang, H. C. and Oriel, P. 1994. Bioproduction of perillyl alcohol and related monoterpenes by isolates of Bacillus stearothermophilus. J. Food Sci. 59:660–662.CrossRefGoogle Scholar
  19. Coulson, R. N. and Witter, J. A. 1984. Forest Entomology: Ecology and Management. Wiley & Sons, New York.Google Scholar
  20. Critchfield, W. B. 1985. The late Quaternary history of lodgepole and jack pines. Can. J. For. Res. 15:749–772.CrossRefGoogle Scholar
  21. Cullingham, C. I., Cooke, J. E. K., Dand, S., Davis, C. S., Cooke, B. J., and Coltman, D. W. 2011. Mountain pine beetle host-range expansion threatens the boreal forest. Mol. Ecol. 20:2157–2171.PubMedCrossRefGoogle Scholar
  22. Davis, T. S., Hofstetter, R. W., Foster, J. T., Foote, N. E., and Keim, P. 2011. Interactions between the yeast Ogataea pini and filamentous fungi associated with the western pine beetle. Microb. Ecol. 61:626–634.PubMedCrossRefGoogle Scholar
  23. Delalibera, I. JR., Vasanthakumar, A., Burwitz, B. J., Schloss, P. D., Klepzig, K. D., Handelsman, J., and Raffa, K. F. 2007. Composition of the bacterial community in the gut of the pine engraver, Ips pini (Say) (Coleoptera) colonizing red pine. Symbiosis 43:93–104.Google Scholar
  24. Diguistini, S., Want, Y., Liao, N. Y., Taylor, G., Tanguay, P., Feau, N., Henrissat, B., Chan, S. K., Hesse-Orce, U., Massoumi Alamouti, S., Tsui, C. K. M., Docking, R. T., Levasseur, A., Haridas, S., Robertson, G., Birol, I., Holt, R. A., Marra, M. A., Hamelin, R. C., Hirst, M., Jones, S. J. M., Bohlmann, J., and Breuil, C. 2011. Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen. Proc. Natl. Acad. Sci. U.S.A. 108:2504–2509.PubMedCrossRefGoogle Scholar
  25. Erbilgin, N., Mori, S. R., Sun, J. H., Stein, J. D., Owen, D. R., Merrill, L. D., Campos Bolaños, R., Raffa, K. F., Méndez Montiel, R., Wood, D. L. and Gillette, N. E. 2007. Response to host volatiles by native and introduced populations of Dendroctonus valens (Coleoptera: Curculionidae, Scolytinae) in North America and China. J. Chem. Ecol. 33:131–146.PubMedCrossRefGoogle Scholar
  26. Furniss, M. M. and Schenk, J. A. 1969. Sustained natural infestation by the mountain pine beetle in seven new Pinus and Picea hosts. J. Econ. Entomol. 62:518–519.Google Scholar
  27. Furniss, R. L. and Carolin, V. M. 1977. Western Forest Insects. USDA For. Serv. Misc. Publ. No. 1339. Washington, D.C. 654 pp.Google Scholar
  28. Geib, S. M., Filley, T. R., Hatcher, P. G., Hoover, K., Carlson, J. E., Del Mar Jimenez-Gasco, M., Nakagawa-Izumi, A., Sleighter, R. L., and Tien, M. 2008. Lignin degradation in wood-feeding insects. Proc. Nat. Acad. Sci. U.S.A. 105:12932–12937.CrossRefGoogle Scholar
  29. Hobson, K. R., Wood, D. L., Cool, L. G., White, P. R., Ohtsuka, T., Kubo, I., and Zavarin, E. 1993. Chiral specificity in response by the bark beetle Dendroctonus valens to host kairomones. J. Chem. Ecol. 19:1837–1846.CrossRefGoogle Scholar
  30. Hofstetter, R. W., Mahfouz, J. B., Klepzig, K. D., and Ayres, M. P. 2005. Effects of tree phytochemistry on the interactions among endophloedic fungi associated with the southern pine beetle. J. Chem. Ecol. 31:539–560.PubMedCrossRefGoogle Scholar
  31. Holben, W. E., Williams, P., Saarinen, M., Särkilahti, L. K., and Apajalahti, J. H. A. 2002. Phylogenetic analysis of intestinal microflora indicates a novel mycoplasma phylotype in farmed and wild salmon. Microb. Ecol. 44:175–185.PubMedCrossRefGoogle Scholar
  32. Hopkins, A. D. 1909. Contributions toward a monograph of the scolytid beetles. I. The genus Dendroctonus. USDA Bur. Entomol. Technol. Ser. 17, Part I.Google Scholar
  33. Huber, D. P. W., Aukema, B. H., Hodgkinson, R. S., and Lindgren, B. S. 2009. Successful reproduction and brood production in live, standing interior hybrid spruce, Picea engelmannii x glauca, by mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae). Agric. For. Entomol. 11:83–89.CrossRefGoogle Scholar
  34. Hulcr, J., Adams, A. S., Raffa, K., Hofstetter, R. W., Klepzig, K. D., and Currie, C. R. 2011. Presence and diversity of Streptomyces in Dendroctonus and sympatric bark beetle galleries across North America. Microb. Ecol. 61:759–768.PubMedCrossRefGoogle Scholar
  35. Jiménez, J. I., Nogales, J., García, J. L., and Díaz, E. 2010. A genomic view of the catabolism of aromatic compounds in Pseudomonas, pp. 1297–1325, in K. N. Timmis (ed.). Handbook of Hydrocarbon and Lipid Microbiology. Springer-Verlag, Heidelberg, Germany.CrossRefGoogle Scholar
  36. Keeling, C. I. and Bohlmann, J. 2006. Diterpene resin acids in conifers. Phytochemistry 67:2415–2423.PubMedCrossRefGoogle Scholar
  37. Kelley, S. T. and Farrell, B. D. 1998. Is specialization a dead end? The phylogeny of host use in Dendroctonus bark beetles (Scolytidae). Evolution 52:1731–1743.CrossRefGoogle Scholar
  38. 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
  39. Klepzig, K. D., Smalley, E. B., and Raffa, K.F. 1996. Combined chemical defenses against an insect-fungal complex. J. Chem. Ecol. 22:1367–1388.CrossRefGoogle Scholar
  40. Leufvén, A., Bergström, G., and Falsen, E. 1988. Oxygenated monoterpenes produced by yeasts, isolated from Ips typographus (Coleoptera, Scolytidae) and grown in phloem medium. J. Chem. Ecol. 14:353–362.CrossRefGoogle Scholar
  41. Lewinsohn, E., Gijzen, M., Savage, T. J., and Croteau, R. 1991. Defense mechanisms of conifers. Plant Physiol. 96:38–43.Google Scholar
  42. Logan, J. A., Régnière, J., and Powell, J. A. 2003. Assessing the impacts of global warming on forest pest dynamics. Front. Ecol. Environ. 1:130–137.CrossRefGoogle Scholar
  43. Logan, J. A., Macfarlane, W. W., and Willcox, L. 2010. Whitebark pine vulnerability to climate change induced mountain pine beetle disturbance in the Greater Yellowstone Ecosystem. Ecol. Appl. 20:895–902.PubMedCrossRefGoogle Scholar
  44. Lu, M., Wingfield, M. J., Gillette, N. E., Mori, S. R., and Sun, J. -H. 2010. Complex interactions among host pines and fungi vectored by an invasive bark beetle. New Phytol. 187:859–866.PubMedCrossRefGoogle Scholar
  45. Middelbeek, E. J., Jenkins, R. O., and Drijver-De Hass, S. J. 1992. Growth in batch culture, pp. 79–106, in T. G. Cartledge (ed.). In vitro Cultivation of Micro-organisms. Butterworth-Heinemann Ltd., Oxford, U.K.Google Scholar
  46. Miller, D. R. and Lindgren, B. S. 2000. Comparison of α-pinene and myrcene on attraction of mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Scolytidae) to pheromones in stands of western white pine. J. Entomol. Soc. Brit. Col. 97:41–46.Google Scholar
  47. Morales-Jiménez, J., Zúñiga, G., Villa-Tanaca, L., and Hernández-Rodríguez, C. 2009. Bacterial community and nitrogen fixation in the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae: Scolytinae). Microb. Ecol. 58:897–891.CrossRefGoogle Scholar
  48. Nealis, V. and Peter, B. 2008. Risk assessment of the threat of mountain pine beetle to Canada’s boreal and eastern pine forests. Natural Resources Canada, Canadian Forest Service, Information Report BC-X-417, 31 pp.Google Scholar
  49. Ott, D. S. 2009. Genetic variation of lodgepole pine Pinus contorta chemical and physical defenses that affect mountain pine beetle Dendroctonus ponderosae attack and tree mortality. Thesis, M.S., Univ. Northern British Columbia, Prince George, B.C., Canada.Google Scholar
  50. Owen, D. R., Smith, S. L., and Seybold, S. J. 2010. The red turpentine beetle. USDA Forest Service, Forest Insect & Disease Leaflet No. 58, June 2010, 9 pp.Google Scholar
  51. Paine, T. D. and Hanlon, C. C. 1994. Influence of oleoresin constituents from Pinus ponderosa and Pinus jeffreyi on growth of mycangial fungi from Dendroctonus ponderosae and Dendroctonus jeffreyi. J. Chem. Ecol. 20:2551–2563.CrossRefGoogle Scholar
  52. Paine, T. D., Raffa, K. F., and Harrington, T. C. 1997. Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu. Rev. Entomol. 42:179–206.PubMedCrossRefGoogle Scholar
  53. Phillips, T. W., Nation, J. L., Wilkinson, R. C., Foltz, J. L., Pierce, H. D., and Oehlschlager, A. C. 1990. Response specificity of Dendroctonus terebrans (Coleoptera: Scolytidae) to enantiomers of its sex pheromones. Annu. Entomol. Soc. Am. 83:251–257.Google Scholar
  54. Pureswaran, D. S., Gries, R., and Borden, J. H. 2004. Quantitative variation in monoterpenes in four species of conifers. Biochem. System. Ecol. 32:1109–1136.CrossRefGoogle Scholar
  55. Raffa, K. F. and Berryman, A. A. 1982a. Physiological differences between lodgepole pines resistant and susceptible to the mountain pine beetle and associated microorganisms. Environ. Entomol. 11:486–492.Google Scholar
  56. Raffa, K. F. and Berryman, A. A. 1982b. Accumulation of monoterpenes and associated volatiles following fungal inoculation of grand fir with a fungus transmitted by the fir engraver, Scolytus ventralis (Coleoptera: Scolytidae). Can. Entomol. l14:797–810.Google Scholar
  57. Raffa, K. F. and Berryman, A. A. 1983. 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.CrossRefGoogle Scholar
  58. Raffa, K. F., Berryman, A. A., Simasko, J., Teal, W., and Wong, 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.Google Scholar
  59. Raffa, K. F., Phillips, T. W., and Salom, S. M. 1993. Strategies and mechanisms of host colonization by bark beetles, pp. 103–128, in T. O. Schowalter and G. Filip (eds.). Beetle-pathogen Interactions in Conifer Forests. Academic Press Ltd., London, UK.Google Scholar
  60. Raffa, K. F. and Smalley, E. B. 1995. Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle-fungal complexes. Oecologia 102:285–295.CrossRefGoogle Scholar
  61. Randall, C. B. 2006. Red Turpentine Beetle: Ecology and Management. Forest Health Protection and State Forestry Organizations. 7 pp.Google Scholar
  62. Rasmussen, L. A. 1974. Flight and attack behavior of mountain pine beetles in lodgepole pine of northern Utah and southern Idaho. USDA For. Serv., Intermountain Forest and Range Exp. St., Ogden, UT, Research Note INT-180. 7 pp.Google Scholar
  63. Reddemann, J. and Reinhard, S. 1996. The importance of monoterpenes in the aggregation of the spruce bark beetle (Coleoptera: Scolytidae: Ipini). Entomol. Gen. 21:69–80.Google Scholar
  64. Robert, J. A., Madilao, L. L., White, R., Yanchuk, A., King, J., and Bohlmann, J. 2010. Terpenoid metabolite profiling in Sitka spruce identifies association of dehydroabietic acid, (+)-3-carene, and terpinolene with resistance against white pine weevil. Botany 88:810–820.CrossRefGoogle Scholar
  65. Safranyik, L., Carroll, A. L., Riel, W. G., Shore, T. L., Peter, B., Nealis, V. G., and Taylor, S. W. 2010. Potential for range expansion of mountain pine beetle into the boreal forest of North America. Can. Entomol. 142:415–442.CrossRefGoogle Scholar
  66. Savithiry, N., Gage, D., Fu, W., and Oriel, P. 1998. Degradation of pinene by Bacillus pallidus BR425. Biodegr. 9:337–341.CrossRefGoogle Scholar
  67. Schmid, J. M. and Mata, S. A. 1991. Red turpentine beetles in partially cut stands of ponderosa pine. USDA Forest Service Rocky Mountain Research Station, Research Note RM-505, Fort Collins, CO, 3 pp.Google Scholar
  68. Scott, J. J., Oh, D. -C., Yuceer, M. C., Klepzig, K. D., Clardy, J., and Currie, C. R. 2008. Bacterial protection of beetle-fungus mutualism. Science 322:63.PubMedCrossRefGoogle Scholar
  69. Seybold, S. J., Bohlmann, J., and Raffa, K. F. 2000. Biosynthesis of coniferophagous bark beetle pheromones and conifer isoprenoids: Evolutionary perspective and synthesis. Can. Entomol. 132:697–753.CrossRefGoogle Scholar
  70. 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. Phytochem. Rev. 5:143–178.CrossRefGoogle Scholar
  71. Shifrine, M. and Phaff, H. J. 1956. The association of yeasts with certain bark beetles. Mycologia 48:41–55.CrossRefGoogle Scholar
  72. Skrodenyte-Arbaciauskiene, V., Buda, V., Radziute, S., and Stunzenas, V. 2006. Myrcene-resistant bacteria isolated from the gut of phytophagous insect Ips typographus. Ekologija 4:1–6.Google Scholar
  73. Smith, R. H. 1961. Red turpentine beetle. USDA For. Serv., Forest Pest Leaflet 55. 8 pp.Google Scholar
  74. Smith, R. H. 1963. Toxicity of pine resin vapors to three species of Dendroctonus bark beetles. J. Econ. Entomol. 56:827–831.Google Scholar
  75. Smith, R. H. 2000. Xylem monoterpenes of pines: distribution, variation, genetics, function. USDA For. Serv., Gen. Tech. Rep. PSW-GTR-177.Google Scholar
  76. Sturgeon, K. B. 1979. Monoterpene variation in ponderosa pine xylem resin related to western pine beetle predation. Evolution 33:803–814.CrossRefGoogle Scholar
  77. Sun, J., Miao, Z., Zhang, Z., Zhang, Z., and Gillette, N. E. 2004. Red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Scolytidae), response to host semiochemicals in China. Environ. Entomol. 33:206–212.CrossRefGoogle Scholar
  78. 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. J. Chem. Ecol. 25:861–880.CrossRefGoogle Scholar
  79. 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). Environ. Entomol. 29:442–453.CrossRefGoogle Scholar
  80. Warnecke, F., Luginbuhl, P., Ivanova, N., Ghassemian, M., Richardson, T., Stege, J., Cayouette, M., Mchardy, A., Djordjevic, G., Aboushadi, N., et al. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565.PubMedCrossRefGoogle Scholar
  81. Whitney, H. S. 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 Conifers. University of Texas Press, Austin, TX.Google Scholar
  82. Wood, S. L. 1982. The bark and ambrosia beetles of North and Central America (Coleoptera: Scolytidae), a taxonomic monograph. Great Basin Nat. Mem. 6. Brigham Young University, Provo, UT.Google Scholar
  83. Wright, S. J., Caunt, P., Carter, D., and Baker, P. B. 1986. Microbial oxidation of alpha-pinene by Serratia marcescens. Appl. Microbiol. Biotech. 23:224–227.CrossRefGoogle Scholar
  84. Yan, Z., Sun, J., Owen, D., and Zhang, Z. 2005. The red turpentine beetle, Dendroctonus valens LeConte (Scolytidae): an exotic invasive pest of pine in China. Biodivers. Conserv. 14:1735–1760.CrossRefGoogle Scholar
  85. Zavarin, E., Critchfield, W. B., and Snajberk, K. 1969. Turpentine composition of Pinus contorta x Pinus banksiana hybrids and hybrid derivatives. Can. J. Bot. 47:1443–1453.CrossRefGoogle Scholar
  86. Zilber-Rosenberg, I. and Rosenberg, E. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32:723–735.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Aaron S. Adams
    • 1
  • Celia K. Boone
    • 1
    • 2
    • 3
  • Jörg Bohlmann
    • 2
  • Kenneth F. Raffa
    • 1
    Email author
  1. 1.Department of EntomologyUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Michael Smith LaboratoriesUniversity of British ColumbiaVancouverCanada
  3. 3.College of Ecosystem Science and ManagementUniversity of Northern British ColumbiaPrince GeorgeCanada

Personalised recommendations