Advertisement

Journal of Chemical Ecology

, Volume 44, Issue 2, pp 209–214 | Cite as

Successful Colonization of Lodgepole Pine Trees by Mountain Pine Beetle Increased Monoterpene Production and Exhausted Carbohydrate Reserves

  • Marla Roth
  • Altaf Hussain
  • Jonathan A. Cale
  • Nadir Erbilgin
Article

Abstract

Lodgepole pine (Pinus contorta) forests have experienced severe mortality from mountain pine beetle (MPB) (Dendroctonus ponderosae Hopkins) in western North America for the last several years. Although the mechanisms by which beetles kill host trees are unclear, they are likely linked to pine defense monoterpenes that are synthesized from carbohydrate reserves. However, how carbohydrates and monoterpenes interact in response to MPB colonization is unknown. Understanding this relationship could help to elucidate how pines succumb to bark beetle attack. We compared concentrations of individual and total monoterpenes and carbohydrates in the phloem of healthy pine trees with those naturally colonized by MPB. Trees attacked by MPB had nearly 300% more monoterpenes and 40% less carbohydrates. Total monoterpene concentrations were most strongly associated with the concentration of sugars in the phloem. These results suggest that bark beetle colonization likely depletes carbohydrate reserves by increasing the production of carbon-rich monoterpenes, and other carbon-based secondary compounds. Bark beetle attacks also reduce water transport causing the disruption of carbon transport between tree foliage and roots, which restricts carbon assimilation. Reduction in carbohydrate reserves likely contributes to tree mortality.

Keywords

Carbon balance Conifers Insect outbreaks Resource allocation Terpenes Tree chemical defenses Tree death 

Notes

Acknowledgements

The project received funding from the NSERC-Discovery to NE, The University of Alberta – Undergraduate Research Initiative for MR. Carbohydrate analysis was conducted by Maksat Igdyrov in Dr. Simon Landhäusser’s lab (Univ. Alberta). We also acknowledge that all research presented in the manuscript was conducted in accordance with all applicable laws and rules set forth by provincial (Alberta) and federal governments and the University of Alberta and all necessary permits were in hand when the research was conducted.

References

  1. Arango-Velez A, El Kayal W, Copeland CCJ, Zaharia LI, Lusebrink I, Cooke JEK (2016) Differences in defense responses of Pinus contorta and Pinus banksiana to the mountain pine beetle fungal associate, Grosmannia clavigera are affected by water deficit. Plant Cell Environ 39:726–744CrossRefPubMedGoogle Scholar
  2. Barbaroux C, Bréda N, Dufrêne E (2003) Distribution of above-ground and below-ground carbohydrate reserves in adult trees of two contrasting broad-leaved species (Quercus petraea and Fagus sylvatica). New Phytol 157:605–615CrossRefGoogle Scholar
  3. 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
  4. Cale JA, Muskens M, Najar A, Ishangulyyeva G, Hussain A, Kanekar SS, Klutsch JG, Taft S, Erbilgin N (2017) Infection by a mycangial fungus causes differential feedbacks in the susceptibility of historical and novel host pines to mountain pine beetle. Tree Physiol 37:1597–1610CrossRefPubMedGoogle Scholar
  5. Chow PS, Landhäusser SM (2004) A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol 24:1129–1136CrossRefPubMedGoogle Scholar
  6. de la Mata R, Hood S, Sala A (2017) Insect outbreak shifts the direction of selection from past to slow growth rates in the long-lived conifer Pinus ponderosa. Proc Natl Acad Sci U S A 114:7391–7396CrossRefPubMedPubMedCentralGoogle Scholar
  7. Erbilgin N, Ma C, Whitehouse C, Shan B, Najar A, Evenden M (2014) Chemical similarity between historical and novel host plants promotes range and host expansion of the mountain pine beetle in a naive host ecosystem. New Phytol 201:940–950CrossRefPubMedGoogle Scholar
  8. Erbilgin N, Cale JA, Hussain A, Ishangulyyeva G, Klutsch JG, Najar A, Zhao S (2017a) Weathering the storm: how lodgepole pine trees survive mountain pine beetle outbreaks. Oecologia 184:469–478CrossRefPubMedGoogle Scholar
  9. Erbilgin N, Cale JA, Lusebrink I, Najar A, Klutsh JG, Sherwood P, Bonello E, Evenden ML (2017b) Water-deficit and fungal infection can differentially affect the production of different classes of defense compounds in two host pines of mountain pine beetle. Tree Physiol 37:338–350CrossRefPubMedGoogle Scholar
  10. Frank JM, Massman WJ, Ewers BE, Huckaby LS, Negrón JF (2014) Ecosystem CO2/H2O fluxes are explained by hydraulically limited gas exchange during tree mortality from spruce bark beetles. J Geophys Res Biogeosci 119:1195–1215CrossRefGoogle Scholar
  11. Goodsman DW, Lusebrink I, Landhäusser SM, Erbilgin N, Lieffers VJ (2013) Variation in carbon availability, defense chemistry and susceptibility to fungal invasion along the stems of mature trees. New Phytol 197:586–594CrossRefPubMedGoogle Scholar
  12. Keeling CI, Bohlmann J (2006) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence on conifers against insects and pathogens. New Phytol 170:657–675CrossRefPubMedGoogle Scholar
  13. Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL, Abata T, Safranyik L (2008) Mountain pine beetle and forest carbon feedback to climate change. Nature 452:987–990CrossRefPubMedGoogle Scholar
  14. Lahr EC, Krokene P (2013) Conifer stored resources and resistance to a fungus associated with the spruce bark beetle Ips typographus. PLoS One 8(8):e72405.  https://doi.org/10.1371/journal.pone.0072405 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Leuzinger S, Bigler C, Wolf A, Körner C (2009) Poor methodology for predicting large-scale tree die-off. Proc Natl Acad Sci U S A 106:E106CrossRefPubMedPubMedCentralGoogle Scholar
  16. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought. New Phytol 178:719–739CrossRefPubMedGoogle Scholar
  17. Miller RH, Berryman AA (1986) Carbohydrate allocation and mountain pine beetle attack in girdled lodgepole pines. Can J For Res 16:1036–1040CrossRefGoogle Scholar
  18. Oksanen J, Guillaume Blanchet F, Friendly M, Kindt P, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P et al (2017) Vegan: community ecology package. R package version 2.4–3. https://CRAN.R-project.org/package=vegan
  19. Page WG, Jenkins MJ, Runyon JB (2012) Mountain pine beetle attack alters the chemistry and flammability of lodgepole pine foliage. Can J For Res 42:1631–1647CrossRefGoogle Scholar
  20. Paine TD, Raffa KF, Harrington TC (1997) Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev Entomol 42:179–206CrossRefPubMedGoogle Scholar
  21. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL https://www.R-project.org/
  22. Raffa KF, Berryman AA (1983a) The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleoptera: Scolytidae). Ecol Monogr 53:27–49CrossRefGoogle Scholar
  23. Raffa KF, Berryman AA (1983b) Physiological aspects of lodgepole pine wound responses to a fungal symbiont of the mountain pine beetle. Can Entomol 115:723–734CrossRefGoogle Scholar
  24. Raffa KF, Aukema BH, Erbilgin N, Klepzig KD, Wallin KF (2005) Interactions among conifer terpenoids and bark beetles across multiple levels of scale: an attempt to understand links between population patterns and physiological processes. Recent Adv Phytochem 39:79–118CrossRefGoogle Scholar
  25. Raffa KF, Aukema BH, Bentz BJ, Carroll AL, Hicke JA, Turner MG, Romme WH (2008) Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. Bioscience 58:501–517CrossRefGoogle Scholar
  26. Raffa KF, Mason CJ, Bonello P, Cook S, Erbilgin N, Keefover-Ring K, Klutsch JG, Villari C, Townsend PA (2017) Defense sydromes in lodgepole-whitebark pine ecosystems related to degree of historical exposure to mountain pine beetles. Plant Cell Environ 40:1791–1806CrossRefPubMedGoogle Scholar
  27. Regier N, Streb S, Zeeman SC, Frey B (2010) Seasonal changes in starch and sugar content of poplar (Populus deltoides x nigra cv. Dorskamp) and the impact of stem girdling on carbohydrate allocation to roots. Tree Physiol 30:979–987CrossRefPubMedGoogle Scholar
  28. Saab VA, Latif QS, Rowland MM, Johnson TN, Chalfoun AD, Buskirk SW, Heyward JE, Dresser MA (2014) Ecological consequences of mountain pine beetle outbreaks for wildfire in western north American forests. For Sci 60:539–559Google Scholar
  29. Safranyik LL, 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
  30. Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol 186:274–281CrossRefPubMedGoogle Scholar
  31. Seybold SJ, Huber DP, 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
  32. van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF, Fulé PZ, Harmon ME, Larson AJ, Smith JM, Taylor AH et al (2009) Widespread increase of tree mortality rates in the western United States. Science 323:521–524CrossRefPubMedGoogle Scholar
  33. Vose JM, Ryan MG (2002) Seasonal respiration of foliage, fine roots, and woody tissues in relation to growth, tissue N, and photosynthesis. Glob Chang Biol 8:182–193CrossRefGoogle Scholar
  34. Wiley R, Rogers BJ, Hodgkinson R, Landhäusser SM (2016) Nonstructural carbohydrate dynamics of lodgepole pine dying from mountain pine beetle attack. New Phytol 209:550–562CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Marla Roth
    • 1
  • Altaf Hussain
    • 1
  • Jonathan A. Cale
    • 1
  • Nadir Erbilgin
    • 1
  1. 1.4-42 Earth Science Building, Department of Renewable ResourcesUniversity of AlbertaEdmontonCanada

Personalised recommendations