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Weathering the storm: how lodgepole pine trees survive mountain pine beetle outbreaks

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Abstract

Recent mountain pine beetle outbreaks in western North America killed millions of lodgepole pine trees, leaving few survivors. However, the mechanism underlying the ability of trees to survive bark beetle outbreaks is unknown, but likely involve phytochemicals such as monoterpenes and fatty acids that can drive beetle aggregation and colonization on their hosts. Thus, we conducted a field survey of beetle-resistant lodgepole pine (Pinus contorta) trees to retrospectively deduce whether these phytochemicals underlie their survival by comparing their chemistry to that of non-attacked trees in the same stands. We also compared beetle attack characteristics between resistant and beetle-killed trees. Beetle-killed trees had more beetle attacks and longer ovipositional galleries than resistant trees, which also lacked the larval establishment found in beetle-killed trees. Resistant trees contained high amounts of toxic and attraction-inhibitive compounds and low amounts of pheromone-precursor and synergist compounds. During beetle host aggregation and colonization, these compounds likely served three critical roles in tree survival. First, low amounts of pheromone-precursor (α-pinene) and synergist (mycrene, terpinolene) compounds reduced or prevented beetles from attracting conspecifics to residual trees. Second, high amounts of 4-allyanisole further inhibited beetle attraction to its pheromone. Finally, high amounts of toxic limonene, 3-carene, 4-allyanisole, α-linolenic acid, and linoleic acid inhibited beetle gallery establishment and oviposition. We conclude that the variation of chemotypic expression of local plant populations can have profound ecological consequences including survival during insect outbreaks.

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Acknowledgements

Funding for this research was provided by NSERC–Discovery Award to NE. Devin Letourneau from Alberta Agriculture and Forestry provided great help for site selection. Drs. Justine Karst (University of Alberta) provided valuable inputs in the earlier phases of this work. 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.

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Authors and Affiliations

  1. Department of Renewable Resources, University of Alberta, 442 Earth Sciences Building, Edmonton, AB, T6G 2E3, Canada

    Nadir Erbilgin, Jonathan A. Cale, Altaf Hussain, Guncha Ishangulyyeva, Jennifer G. Klutsch, Ahmed Najar & Shiyang Zhao

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  1. Nadir Erbilgin
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  2. Jonathan A. Cale
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  3. Altaf Hussain
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  4. Guncha Ishangulyyeva
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  5. Jennifer G. Klutsch
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  6. Ahmed Najar
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  7. Shiyang Zhao
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Contributions

NE, JAC, and JGK conceived and designed the experiments. NE, JAC, JGK, GI, and SZ performed the experiments. AN and AH ran chemical analysis. JAC performed statistical analysis. NE wrote the manuscript; other authors provided editorial advice.

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Correspondence to Nadir Erbilgin.

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Communicated by Ian Kaplan.

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Supplementary material 1 (DOCX 13 kb)

442_2017_3865_MOESM2_ESM.docx

Supp. Image 1. Increment cores taken from resistant lodgepole pine (Pinus contorta) trees in western Alberta (Canada) in July 2016. This particular tree is about 56–57 years old. It was attacked by the mountain pine beetle (Dendroctonus ponderosae) once in 2006/2007 period and since then tree has recovered. Since the sample was taken in July 2016, the annual growth was not complete. Supp. Image 2. Increment cores taken from residual lodgepole pine (Pinus contorta) trees in western Alberta (Canada) in July 2016. This particular tree is about 52–53 years old. It was attacked by the mountain pine beetle (Dendroctonus ponderosae) multiple times from 2006 to 2009 and since then tree has recovered. Note the annual growth rate from 2012–2015. Since the sample was taken in July 2016, the annual growth was not complete. Supp. Image 3A. Mountain pine beetle (Dendroctonus ponderosae) activities on beetle-killed lodgepole pine (Pinus contorta) trees in western Alberta (Canada). Note the extensive oviposition (vertical) and larval (perpendicular to maternal) galleries as well as staining as a result of infection by fungal associates of beetle. Supp. Image 3B. Unsuccessful gallery establishment by mountain pine beetle (Dendroctonus ponderosae) on resistant lodgepole pine (Pinus contorta) trees in western Alberta (Canada). Note the failed oviposition gallery and absence of larval galleries and fungal staining. Short oviposition galleries and dead beetle inside the gallery signify failed reproduction due to toxic terpenes. (DOCX 1141 kb)

442_2017_3865_MOESM3_ESM.docx

Supp. Map 1. Aerial overview of mountain pine beetle (Dendroctonus ponderosae) outbreak in western Alberta in 2007. Red spots show where the outbreak occurred in lodgepole pine (Pinus contorta) forests. Supp. Map 2. Location of 14 lodgepole pine (Pinus contorta) forest stands sampled in western Alberta. Supp. Map 3. Aerial overview of mountain pine beetle (Dendroctonus ponderosae) outbreak in western Alberta in 2010. Red spots show where the outbreak occurred in lodgepole pine (Pinus contorta) forests. Note that beetle outbreak moved away from our study sites after 2010. (DOCX 1304 kb)

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Erbilgin, N., Cale, J.A., Hussain, A. et al. Weathering the storm: how lodgepole pine trees survive mountain pine beetle outbreaks. Oecologia 184, 469–478 (2017). https://doi.org/10.1007/s00442-017-3865-9

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