Journal of Chemical Ecology

, Volume 39, Issue 9, pp 1209–1220 | Cite as

The Lodgepole × Jack Pine Hybrid Zone in Alberta, Canada: A Stepping Stone for the Mountain Pine Beetle on its Journey East Across the Boreal Forest?

  • Inka LusebrinkEmail author
  • Nadir Erbilgin
  • Maya L. Evenden


Historical data show that outbreaks of the tree killing mountain pine beetle are often preceded by periods of drought. Global climate change impacts drought frequency and severity and is implicated in the range expansion of the mountain pine beetle into formerly unsuitable habitats. Its expanded range has recently reached the lodgepole × jack pine hybrid zone in central Alberta, Canada, which could act as a transition from its historical lodgepole pine host to a jack pine host present in the boreal forest. This field study tested the effects of water limitation on chemical defenses of mature trees against mountain pine beetle-associated microorganisms and on beetle brood success in lodgepole × jack pine hybrid trees. Tree chemical defenses as measured by monoterpene emission from tree boles and monoterpene concentration in needles were greater in trees that experienced water deficit compared to well-watered trees. Myrcene was identified as specific defensive compound, since it significantly increased upon inoculation with dead mountain pine beetles. Beetles reared in bolts from trees that experienced water deficit emerged with a higher fat content, demonstrating for the first time experimentally that drought conditions benefit mountain pine beetles. Further, our study demonstrated that volatile chemical emission from tree boles and phloem chemistry place the hybrid tree chemotype in-between lodgepole pine and jack pine, which might facilitate the host shift from lodgepole pine to jack pine.


Mountain pine beetle Range expansion Drought Tree defenses Beetle condition 



We acknowledge Adriana Arango, Jeremiah Bolstad, Janice Cooke, Christina Elliott, Matt Ferguson, Andrew Ho, Ed Hunt, Brad Jones, Jean Linsky, Boyd Mori, and William Sperling for their help before and during the field season; Miles Dyck for providing us with the TDR equipment; Celia Boone for sharing β-phellandrene. We particularly acknowledge Adrianne Rice for providing fungal culture and knowledge; Tim McCready from Millar Western Forest Products Ltd. for providing a suitable field site; Jörg Bohlmann for comments on the manuscript. Funding for this research was provided through grants from the Government of Alberta through Genome Alberta, the Government of British Columbia through Genome BC and Genome Canada in support of the Tria 1 and Tria 2 projects ( of which MLE and NE are co-investigators.


  1. Adams AS, Six DL (2007) Temporal variation and prevalence of fungi associated with developmental stages of Dendroctonus ponderosae (Coleoptera: Curculionidae). Environ Entomol 36:64–72PubMedCrossRefGoogle Scholar
  2. Adams AS, Six DL, Adams S, Holben W (2008) In vitro interactions between yeasts and bacteria and the fungal symbionts of the mountain pine beetle (Dendroctonus ponderosae). Microb Ecol 56:460–466PubMedCrossRefGoogle Scholar
  3. Adams AS, Aylward FO, Adams SM, Erbilgin N, Aukema BH, Currie CR, Suen G, Raffa KF (2013) Mountain pine beetles colonizing historical and naïve host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl Environ Microbiol 79:3468–3475PubMedCrossRefGoogle Scholar
  4. Alfaro RI, Campbell E, Hawkes BC (2010) Historical frequency, intensity and extent of mountain pine beetle disturbance in British Columbia B.C. Natural Resources Canada, Canadian Forest Service, Pacific Forestry Centre, Victoria, BC. Mountain Pine Beetle Working Paper 2009–30Google Scholar
  5. Atkins MD (1966) Laboratory studies on the behaviour of the Douglas-fir beetle, Dendroctonus pseudotsugae Hopkins. Can Entomol 98:953–991CrossRefGoogle Scholar
  6. Atkins MD (1975) On factors affecting the size, fat content and behavior of a scolytid. Z Angew Entomol 78(1–4):209–218Google Scholar
  7. Ayres MP, Wilkens RT, Ruel JJ, Lombardero MJ, Vallery E (2000) Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi. Ecology 81:2198–2210CrossRefGoogle Scholar
  8. Becerra JX (1997) Insects on plants: macroevolutionary chemical trends in host use. Science 276:253–256PubMedCrossRefGoogle Scholar
  9. Blanch JS, Penuelas J, Llusia J (2007) Sensitivity of terpene emissions to drought and fertilization in terpene-storing Pinus halepensis and non-storing Quercus ilex. Physiol Plant 131:211–225PubMedGoogle Scholar
  10. Bleiker KP, Six DL (2007) Dietary benefits of fungal associates to an eruptive herbivore: potential implications of multiple associates on host population dynamics. Environ Entomol 36:1384–1396PubMedCrossRefGoogle Scholar
  11. Blomquist GJ, Figueroa-Teran R, Aw M, Song M, Gorzalski A, Abbott NL, Chang E, Tittiger C (2010) Pheromone production in bark beetles. Insect Biochem Mol 40:699–712CrossRefGoogle Scholar
  12. Bohlmann J (2012) Pine terpenoid defences in the mountain pine beetle epidemic and in other conifer pest interactions: specialized enemies are eating holes into a diverse, dynamic and durable defence system. Tree Physiol 32:943–945PubMedCrossRefGoogle Scholar
  13. Bonello P, Blodgett JT (2003) Pinus nigraSphaeropsis sapinea as a model pathosystem to investigate local and systemic effects of fungal infection of pines. Physiol Mol Plant Pathol 63:249–261CrossRefGoogle Scholar
  14. Boone CK, Aukema BH, Bohlmann J, Carroll AL, Raffa KF (2011) Efficacy of tree defense physiology varies with bark beetle population density: a basis for positive feedback in eruptive species. Can J For Res 41:1174–1188CrossRefGoogle Scholar
  15. Borden JH, Pureswaran DS, Lafontaine JP (2008) Synergistic blends of monoterpenes for aggregation pheromones of the mountain pine beetle (Coleoptera: Curculionidae). J Econ Entomol 101:1266–1275PubMedCrossRefGoogle Scholar
  16. Breshears DD, Myers OB, Meyer CW, Barnes FJ, Zou CB, Allen CD, Mcdowell NG, Pockman WT (2009) Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements. Front Ecol Environ 7:185–189CrossRefGoogle Scholar
  17. Byers JA (1989) Chemical ecology of bark beetles. Experientia 45:271–283CrossRefGoogle Scholar
  18. Byers JA, Lanne BS, Löfqvist J, Schlyter F, Bergström G (1985) Olfactory recognition of host-tree susceptibility by pine shoot beetles. Naturwissenschaften 72:324–326CrossRefGoogle Scholar
  19. Carroll AL, Taylor SW, Régnière J, Safranyik L (2004) Effects of climate and climate change on the mountain pine beetle, pp. 221–230. In: Shore TL, Brooks JE, Stone JE (eds) Challenges and solutions: Proceedings of the mountain pine beetle symposium, Kelowna, British Columbia. Information report BC-X-399, Pacific Forestry Centre, Canadian Forest Service, Natural Resources Canada, Victoria, British ColumbiaGoogle Scholar
  20. Cerezke HF (1995) Egg gallery, brood production, and adult characteristics of mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae), in three pine hosts. Can Entomol 127:955–965CrossRefGoogle Scholar
  21. Coppedge BR, Stephen FM, Felton GW (1995) Variation in female southern pine beetle size and lipid-content in relation to fungal associates. Can Entomol 127:145–154CrossRefGoogle Scholar
  22. Cudmore TJ, Björklund N, Carroll AL, Lindgren BS (2010) Climate change and range expansion of an aggressive bark beetle: evidence of higher beetle reproduction in naïve host tree populations. J Appl Ecol 47:1036–1043CrossRefGoogle Scholar
  23. Cullingham CI, Cooke JEK, Dang S, Davis CS, Cooke BJ, Coltman DW (2011) Mountain pine beetle host-range expansion threatens the boreal forest. Mol Ecol 20:2157–2171PubMedCrossRefGoogle Scholar
  24. Cullingham CI, James PMA, Cooke JEK, Coltman DW (2012) Characterizing the physical and genetic structure of the lodgepole pine × jack pine hybrid zone: mosaic structure and differential introgression. Evol Appl 5:879–891PubMedCrossRefGoogle Scholar
  25. Diguistini S, Wang Y, Liao NY, Taylor G, Tanguay P, Feau N, Henrissat B, Chan SK, Hesse-Orce U, Alamouti SM, Tsui CKM, Docking RT, Levasseur A, Haridas S, Robertson G, Birol I, Holt RA, Marra MA, Hamelin RC, Hirst M, Jones SJM, Bohlmann J, 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 108:2504–2509PubMedCrossRefGoogle Scholar
  26. Erbilgin N, Mori SR, Sun JH, Stein JD, Owen DR, Merrill LD, Campos Bolaños R, Raffa KF, Méndez Montiel T, Wood DL, Gillette NE (2007) Response to host volatiles by native and introduced populations of Dendroctonus valens (Coleoptera: Curculionidae, Scolytinae) in North America and China. J Chem Ecol 33:131–146PubMedCrossRefGoogle Scholar
  27. Futuyma DJ, Keese MC, Funk DJ (1995) Genetic constraints on macroevolution: the evolution of host affiliation in the leaf beetle genus Ophraella. Evolution 49:797–809CrossRefGoogle Scholar
  28. Gollob L (1980) Monoterpene composition in bark beetle-resistant loblolly pine. Naturwissenschaften 67(8):409–410CrossRefGoogle Scholar
  29. Goodsman DW, Erbilgin N, Lieffers VJ (2012) The impact of phloem nutrients on overwintering mountain pine beetles and their fungal symbionts. Environ Entomol 41:478–486PubMedCrossRefGoogle Scholar
  30. Graf M, Reid ML, Aukema BH, Lindgren BS (2012) Association of tree diameter with body size and lipid content of mountain pine beetles. Can Entomol 144:467–477CrossRefGoogle Scholar
  31. Herms DA, Mattson WJ (1992) The dilemma of plants: To grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  32. Hillel D (1998) Environmental soil physics. Academic, San DiegoGoogle Scholar
  33. Johnson RH, Young BL, Alstad DN (1997) Responses of ponderosa pine growth and volatile terpene concentrations to manipulation of soil water and sunlight availability. Can J Forest Res 27:1794–1804CrossRefGoogle Scholar
  34. Jost RW, Rice AV, Langor DW, Boluk Y (2008) Monoterpene emissions from lodgepole and jack pine bark inoculated with mountain pine beetle-associated fungi. J Wood Chem Technol 28:37–46CrossRefGoogle Scholar
  35. Kainulainen P, Oksanen J, Palomäki V, Holopainen JK, Holopainen T (1992) Effect of drought and waterlogging stress on needle monoterpenes of Picea abies. Can J Bot 70:1613–1616CrossRefGoogle Scholar
  36. Keeling CI, Bohlmann J (2006) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:657–675PubMedCrossRefGoogle Scholar
  37. Kelley ST, Farrell BD (1998) Is specialization a dead end? The phylogeny of host use in Dendroctonus bark beetles (Scolytidae). Evolution 52:1731–1743CrossRefGoogle Scholar
  38. Kenkel NC, Hendrie ML, Bella IE (1997) A long-term study of Pinus banksiana population dynamics. J Veg Sci 8:241–254CrossRefGoogle Scholar
  39. Khadempour L, Lemay V, Jack D, Bohlmann J, Breuil C (2012) The relative abundance of mountain pine beetle fungal associates changes through the beetle life cycle in pine trees. Microb Ecol 64:909–917PubMedCrossRefGoogle Scholar
  40. Krokene P, Solheim H (1998) Pathogenicity of four blue-stain fungi associated with aggressive and nonaggressive bark beetles. Phytopathology 88:39–44PubMedCrossRefGoogle Scholar
  41. Krokene P, Nagy NE, Solheim H (2008) Methyl jasmonate and oxalic acid treatment of Norway spruce: anatomically based defense responses and increased resistance against fungal infection. Tree Physiol 28:29–35PubMedCrossRefGoogle Scholar
  42. Langenheim JH (1994) Higher plant terpenoids: a phytocentric overview of their ecological roles. J Chem Ecol 20:1223–1280CrossRefGoogle Scholar
  43. Lee S, Kim JJ, Breuil C (2005) Leptographium longiclavatum sp nov., a new species associated with the mountain pine beetle, Dendroctonus ponderosae. Mycol Res 109:1162–1170PubMedCrossRefGoogle Scholar
  44. Legendre P, Durand S (2010) rdaTest: Canonical redundancy analysis (R package version 1.7). URL
  45. Lieutier F, Yart A, Ye H, Sauvard D, Gallois V (2004) Variations in growth and virulence of Leptographium wingfieldii Morelet, a fungus associated with the bark beetle Tomicus piniperda L. Ann For Sci 61:45–53CrossRefGoogle Scholar
  46. Lieutier F, Yart A, Salle A (2009) Stimulation of tree defenses by Ophiostomatoid fungi can explain attack success of bark beetles on conifers. Ann For Sci 66:801–801CrossRefGoogle Scholar
  47. Llusià J, Peñuelas J (1998) Changes in terpene content and emission in potted Mediterranean woody plants under severe drought. Can J Bot 76:1366–1373Google Scholar
  48. Lombardero MJ, Ayres MP, Lorio PL Jr, Ruel JJ (2000) Environmental effects on constitutive and inducible resin defences of Pinus taeda. Ecol Lett 3:329–339CrossRefGoogle Scholar
  49. Lusebrink I, Evenden ML, Blanchet FG, Cooke JEK, Erbilgin N (2011) Effect of water stress and fungal inoculation on monoterpene emission from an historical and a new pine host of the mountain pine beetle. J Chem Ecol 37:1013–1026PubMedCrossRefGoogle Scholar
  50. Masuya H, Kaneko S, Yamaoka Y (2003) Comparative virulence of blue-stain fungi isolated from Japanese red pine. J For Res 8:0083–0088CrossRefGoogle Scholar
  51. Mattson WJ, Haack RA (1987) The role of drought in outbreaks of plant-eating insects. BioScience 37:110–118CrossRefGoogle Scholar
  52. Mirov NT (1956) Composition of turpentine of lodgepole × jack pine hybrids. Can J Bot 34:443–457CrossRefGoogle Scholar
  53. Monson RK, Lerdau MT, Sharkey TD, Schimel DS, Fall R (1995) Biological aspects of constructing volatile organic compound emission inventories. Atmos Environ 29:2989–3002CrossRefGoogle Scholar
  54. Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Sólymos P, Stevens MHH, Wagner H (2010) Vegan: Community ecology package. R package version 1.17-4.
  55. Ott DS, Yanchuk AD, Huber DPW, Wallin KF (2011) Genetic variation of lodgepole pine, Pinus contorta var. latifolia, chemical and physical defenses that affect mountain pine beetle, Dendroctonus ponderosae, attack and tree mortality. J Chem Ecol 37:1002–1012PubMedCrossRefGoogle Scholar
  56. Paine TD, Raffa KF, Harrington TC (1997) Interactions among Scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev Entomol 42:179–206PubMedCrossRefGoogle Scholar
  57. Parmesan C (1996) Climate and species’ range. Nature 382:765–766CrossRefGoogle Scholar
  58. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669CrossRefGoogle Scholar
  59. Pitman GB, Vite JP, Kinzer GW, Fentiman AF (1968) Bark beetle attractants: trans-verbenol isolated from Dendroctonus. Nature 218:168–169CrossRefGoogle Scholar
  60. Pureswaran DS, Gries R, Borden JH (2004) Quantitative variation in monoterpenes in four species of conifers. Biochem Syst Ecol 32:1109–1136CrossRefGoogle Scholar
  61. R Development Core Team (2012) R: a language and environment for statistical computing (version 2.12.0). R Foundation for Statistical Computing, Vienna, Austria. URL
  62. Raffa KF, Berryman AA (1983) Physiological-aspects of lodgepole pine wound responses to a fungal symbiont of the mountain pine beetle, Dendroctonus ponderosae (Coleoptera, Scolytidae). Can Entomol 115:723–734CrossRefGoogle Scholar
  63. Raffa KF, Smalley EB (1995) Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle-fungal complexes. Oecologia 102:285–295CrossRefGoogle Scholar
  64. Reid RW, Whitney HS, Watson JA (1967) Reactions of lodgepole pine to attack by Dendroctonus ponderosae and blue stain fungi. Can J Bot 45:1115–1126CrossRefGoogle Scholar
  65. Rhoades DF (1990) Analysis of monoterpenes emitted and absorbed by undamaged boles of lodgepole pine. Phytochemistry 29:1463–1465CrossRefGoogle Scholar
  66. Rice AV, Langor DW (2008) A comparison of heat pulse velocity and lesion lengths for assessing the relative virulence of mountain pine beetle-associated fungi on jack pine. Forest Pathol 38:257–262CrossRefGoogle Scholar
  67. Rice AV, Thormann MN, Langor DW (2007a) Mountain pine beetle associated blue-stain fungi cause lesions on jack pine, lodgepole pine, and lodgepole × jack pine hybrids in Alberta. Can J Bot 85:307–315CrossRefGoogle Scholar
  68. Rice AV, Thormann MN, Langor DW (2007b) Virulence of, and interactions among, mountain pine beetle associated blue-stain fungi on two pine species and their hybrids in Alberta. Can J Bot 85:316–323CrossRefGoogle Scholar
  69. Rice AV, Thormann MN, Langor DW (2008) Mountain pine beetle-associated blue-stain fungi are differentially adapted to boreal temperatures. Forest Pathol 38:113–123CrossRefGoogle Scholar
  70. Robinson DA, Jones SB, Wraith JM, Or D, Friedman SP (2003) A review of advances in dielectric and electrical conductivity measurement in soils using time domain reflectometry. Vadose Zone J 2:444–475Google Scholar
  71. Rudinsky JA, Morgan ME, Libbey LM, Putnam TB (1974) Antiaggregative-rivalry pheromone of mountain pine beetle Coleoptera-Scolytidae, and a new arrestant of southern pine beetle Coleoptera-Scolytidae. Environ Entomol 3:90–98Google Scholar
  72. Ryker LC, Libbey LM (1982) Frontalin in the male mountain pine beetle. J Chem Ecol 8:1399–1409CrossRefGoogle Scholar
  73. Safranyik L, Carroll AL (2006) The biology and epidemiology of the mountain pine beetle in lodgepole pine forests, pp 3–66. In: Safranyik L, Wilson B (eds) The mountain pine beetle: a synthesis of its biology, management and impacts on lodgepole pine. Pacific Forestry Centre, Canadian Forest Service, Natural Resources Canada, Victoria, British ColumbiaGoogle Scholar
  74. Safranyik L, Shrimpton DM, Whitney HS (1975) An interpretation of the interaction between lodgepole pine, the mountain pine beetle and its associated blue stain fungi in western Canada. In: Baumgartner DM (ed) Management of lodgepole pine ecosystems. Washington State University Cooperative Extension Service, Pullman, Washington, pp 406–428Google Scholar
  75. Safranyik L, Carroll AL, Régnière J, Langor DW, Riel WG, Shore TL, Peter B, Cooke BJ, Nealis VG, Taylor SW (2010) Potential for range expansion of mountain pine beetle into the boreal forest of North America. Can Entomol 142:415–442CrossRefGoogle Scholar
  76. Schiebe C, Hammerbacher A, Birgersson G, Witzell J, Brodelius P, Gershenzon J, Hansson B, Krokene P, Schlyter F (2011) Inducibility of chemical defenses in Norway spruce bark is correlated with unsuccessful mass attacks by the spruce bark beetle. Oecologia 170:183–198CrossRefGoogle Scholar
  77. Seybold SJ, Huber DPW, Lee JC, Graves AD, Bohlmann J (2006) Pine monoterpenes and pine bark beetles: a marriage of convenience for defense and chemical communication. Phytochem Rev 5:143–178CrossRefGoogle Scholar
  78. Six DL, Klepzig KD (2004) Dendroctonus bark beetles as model systems for studies in symbiosis. Symbiosis 37:207–232Google Scholar
  79. Stange EE, Ayres MP (2001) Climate change impacts: insects. eLS. John Wiley & Sons, LtdGoogle Scholar
  80. Sturgeon KB (1979) Monoterpene variation in Ponderosa pine xylem resin related to western pine beetle predation. Evolution 33:803–814CrossRefGoogle Scholar
  81. Thomson AJ, Shrimpton DM (1984) Weather associated with the start of mountain pine beetle outbreaks. Can J For Res 14:255–258CrossRefGoogle Scholar
  82. Turtola S, Manninen A-M, Rikala R, Kainulainen P (2003) Drought stress alters the concentration of wood terpenoids in scots pine and Norway spruce seedlings J. Cheml Ecol 29:1981–1995CrossRefGoogle Scholar
  83. Vaněk T, Halík J, Vaňková R, Valterová I (2005) Formation of trans-verbenol and verbenone from α-pinene catalysed by immobilised Picea abies cells. Biosci Biotechnol Biochem 69:321–325PubMedCrossRefGoogle Scholar
  84. Vidacović M (1991) Conifers: morphology and variation. Graficki Zavod Hrvatske, Zagreb, CroatiaGoogle Scholar
  85. Wang Y, Lim L, Diguistini S, Robertson G, Bohlmann J, Breuil C (2013) A specialized ABC efflux transporter GcABC-G1 confers monoterpene resistance to Grosmannia clavigera, a bark beetle-associated fungal pathogen of pine trees. New Phytol 197:886–898PubMedCrossRefGoogle Scholar
  86. Whitehead AT, Del Scott T, Schmitz RF, Mori K (1989) Electroantennograms by mountain pine beetles, Dendroctonus ponderosae Hopkins, exposed to selected chiral semiochemicals. J Chem Ecol 15:2089–2099CrossRefGoogle Scholar
  87. Whitney HS (1971) Association of Dendroctonus ponderosae (Coleoptera: Scolytidae) with blue stain fungi and yeasts during brood development in lodgepole pine. Can Entomol 103:1495–1503CrossRefGoogle Scholar
  88. Yamaoka Y, Swanson RH, Hiratsuka Y (1990) Inoculation of lodgepole pine with four blue-stain fungi associated with mountain pine beetle, monitored by a heat pulse velocity (HPV) instrument. Can J Forest Res 20:31–36CrossRefGoogle Scholar
  89. Zhao T, Krokene P, Hu J, Christiansen E, Björklund N, Långström B, Solheim H, Borg-Karlson A-K (2011) Induced terpene accumulation in Norway spruce inhibits bark beetle colonization in a dose-dependent manner. PLoS One 6:e26649PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Inka Lusebrink
    • 1
    • 3
    Email author
  • Nadir Erbilgin
    • 2
  • Maya L. Evenden
    • 1
  1. 1.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  2. 2.Department of Renewable ResourcesUniversity of AlbertaEdmontonCanada
  3. 3.Centre for Biological SciencesUniversity of SouthamptonSouthamptonUK

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