Skip to main content
Log in

Primary and Secondary Metabolite Profiles of Lodgepole Pine Trees Change with Elevation, but Not with Latitude

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Climate change has a large influence on plant functional and phenotypic traits including plant primary and secondary metabolites. One well-established approach to investigating the variation in plant metabolites involves studying plant populations along elevation and latitude gradients. We considered how two space-for-time climate change gradients (elevation and latitude) influence carbohydrate reserves (soluble sugars, starches) and secondary metabolites (monoterpenes, diterpene resin acids) of lodgepole pine trees in western Canada. We were particularly interested in the relationship of terpenes and carbohydrates with a wide range of tree, site, and climatic factors. We found that only elevation had a strong influence on the expression of both terpenes and carbohydrates of trees. Specifically, as elevation increased, concentrations of monoterpenes and diterpenes generally increased and soluble sugars (glucose, sucrose, total sugars) decreased. In contrast, latitude had no impact on either of terpenes or carbohydrates. Furthermore, we found a positive relationship between concentrations of starch and total terpenes and diterpenes in the elevation study; whereas neither starches nor sugars were correlated to terpenes in the latitude study. Similarly, both terpenes and carbohydrates had a much greater number of significant correlations to site characteristics such as slope, basal area index, and sand basal area, in the elevational than in the latitude study. Overall, these results support the conclusion that both biotic and abiotic factors likely drive the patterns of primary and secondary metabolite profiles of lodgepole pine along geographical gradients. Also, presence of a positive relationship between terpenes and starches suggests an interaction between primary ad secondary metabolites of lodgepole pine trees.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

Data will be available upon acceptance of the manuscript.

References

  • Alberta Agriculture and Forestry (2017) Derived Ecosite Phase (DEP). Accessed from https://open.alberta.ca/opendata/derived-ecosite-phase on April 22, 2020

  • 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(3):605–615

    Google Scholar 

  • Blois JL, Williams JW, Fitzpatrick MC, Jackson ST, Ferrier S (2013) Space can substitute for time in predicting climate-change effects on biodiversity. Proc Natl Acad Sci 110:9374–9379

    CAS  PubMed  Google Scholar 

  • Bloom SA (1981) Similarity indices in community studies: potential pitfalls. Mar Ecol Prog Ser 5:125–128

    Google Scholar 

  • 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 41:1174–1188

    Google Scholar 

  • Buckley J, Widmer A, Mescher MC, De Moraes CM (2019) Variation in growth and defence traits among plant populations at different elevations: implications for adaptation to climate change. J Ecol 107:2478–2492

    CAS  Google Scholar 

  • Cabon A, Peters RL, Fonti P, Martínez-Vilalta J, Miquel DC (2020) Temperature and water potential co-limit stem cambial activity along steep elevational gradient. New Phytol 26:1325–1340

    Google Scholar 

  • Cale JA, Muskens M, Najar A, Ishangulyyeva G, Hussain A, Kanekar SS, Klutsch JG, Taft S, Erbilgin N (2017) Rapid monoterpene induction promotes the susceptibility of a novel host pine to mountain pine beetle colonization but not to beetle-vectored fungi. Tree Phys 37:1597–1610

    CAS  Google Scholar 

  • Cale JA, Klutsch JG, Dykstra CB, Peters B, Erbilgin N (2019) Pathophysiological responses of pine defensive metabolites largely lack differences between pine species but vary with eliciting ophiostomatoid fungal species. Tree Phys 39:1121–1135

    CAS  Google Scholar 

  • Celedon JM, Bohlmann J (2019) Oleoresin defenses in conifers: chemical diversity, terpene synthases and limitations of oleoresin defense under climate change. New Phytol 224:1444–1463

    CAS  PubMed  Google Scholar 

  • Chappell J (2002) The genetics and molecular genetics of terpene and sterol origami. Cur Opp Plant Biol 5:151–157

    CAS  Google Scholar 

  • Chiu CC, Keeling CI, Bohlmann J (2017) Toxicity of pine monoterpenes to mountain pine beetle. Sci Rep 7:8858

    PubMed  PubMed Central  Google Scholar 

  • Cudmore TJ, Bjorklund 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 47:1036–1043

    Google Scholar 

  • Cullingham CI, James PMA, Cooke JE, Coltman DW (2012) Characterizing the physical and genetic structure of the lodgepole pine x jack pine hybrid zone: mosaic structure and differential introgression. Evol Appl 5:879–891

    PubMed  PubMed Central  Google Scholar 

  • Defossez E, Pellissier L, Rasmann S (2018) The unfolding of plant growth form-defence syndromes along elevation gradients. Ecol Lett 21:609–618

    PubMed  Google Scholar 

  • Díaz S, Kattge J, Cornelissen JHC, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Colin Prentice I, Garnier E, Bönisch G, Westoby M, Poorter H, Reich PB, Moles AT, Dickie J, Gillison AN, Zanne AE, Chave J, Joseph Wright S, Sheremet’ev SN, Jactel H, Baraloto C, Cerabolini B, Pierce S, Shipley B, Kirkup D, Casanoves F, Joswig JS, Günther A, Falczuk V, Rüger N, Mahecha MD, Gorné LD (2016) The global spectrum of plant form and function. Nature 529:167–171

    PubMed  Google Scholar 

  • Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Ann Rev Plant Biol 65:667–687

    CAS  Google Scholar 

  • Duan Q, Bonn B, Kreuzwieser J (2020) Terpenoids are transported in the xylem sap of Norway spruce. Plant Cell Environ 43:1766–1778

    CAS  PubMed  Google Scholar 

  • Elmendorf SC, GHR H, Hollister RD, Fosaae AM, Gouldf WA, Hermanutzg L, Hofgaardh A, Jónsdóttiri IS, Jorgensonk JC, Lévesquel E et al (2015) Experiment, monitoring, and gradient methods used to infer climate change effects on plant communities yield consistent patterns. Proc Natl Acad Sci 112:448–452

    CAS  PubMed  Google Scholar 

  • Erbilgin N (2019) Phytochemicals as mediators for host range expansion of a native invasive forest insect herbivore. New Phytol 221:1268–1278

    PubMed  Google Scholar 

  • Erbilgin N, Colgan LJ (2012) Different effects of plant ontogeny and damage type on phloem and foliage monoterpenes in jack pine (Pinus banksiana). Tree Phys 32:946–957

    CAS  Google Scholar 

  • 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 naïve host ecosystem. New Phytol 201:940–950

    PubMed  Google Scholar 

  • Erbilgin N, Cale JA, Hussain A, Ishangulyyeva G, Klutsch JG, Najar A, Zhao S (2017) Weathering the storm: how lodgepole pine trees survive mountain pine beetle outbreaks. Oecologia 184:469–478

    PubMed  Google Scholar 

  • Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:353–376

    CAS  PubMed  Google Scholar 

  • Ferrenberg S, Langenhan JM, Loskot SA, Rozal LM, Mitton JB (2017) Resin monoterpene defenses decline within three widespread species of pine (Pinus) along a 1530-m elevational gradient. Ecosphere 8:e01975. https://doi.org/10.1002/ecs2.1975

    Article  Google Scholar 

  • Forrest GI (1981) Geographical variation in oleoresin monoterpene composition of Pinus contorta from natural stands and planted seed collections. Biochem Syst Ecol 9:97–103

    CAS  Google Scholar 

  • Forrest GI (1987) A range wide comparison of outlying and central lodgepole pine populations based on oleoresin monoterpene analysis. Biochem Syst Ecol 15:15–30

    Google Scholar 

  • Galmán A, Abdala-Roberts L, Zhang S, Berny-Mier y Terán JC, Rasmann S, Moreira X (2018) A global analysis of elevational gradients in leaf herbivory and its underlying drivers: effects of plant growth form, leaf habit, and climatic correlates. J Ecol 106:413–421

    Google Scholar 

  • Godfrey JM, Riggio J, Orozco J, Guzmán-Delgado P, Chin ARO, Zwieniecki MA (2020) Ray fractions and carbohydrate dynamics of tree species along a 2750 m elevation gradient indicate climate response, not spatial storage limitation. New Phytol 225:2314–2330

    CAS  PubMed  Google Scholar 

  • Goodsman DW, Lusebrink I, Landhausser 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 197:586–594

    CAS  PubMed  Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Software 22:1–19

    Google Scholar 

  • Hahn PG, Maron JL (2016) A framework for predicting intraspecific variation in plant defense. Trend Ecol Evol 31:646–656

    Google Scholar 

  • Hall DE, Zerbe P, Jancsik S, Quesada AL, Dullat H, Madilano LL, Yuen M, Bohlmann J (2013) Evolution of conifer diterpene synthase: diterpene resin acid biosynthesis in lodgepole pine and jack pine involves monofunctional and bifunctional diterpene synthases. Plant Physiol 161:600–616

    CAS  PubMed  Google Scholar 

  • Hargreaves AL, Germain RM, Bontrager M, Persi J, Angert AL (2020) Local adaptation to biotic interactions: a meta-analysis across latitudes. Am Nat 195:395–411

    PubMed  Google Scholar 

  • Hartmann H, Trumbore S (2016) Understanding the roles of nonstructural carbohydrates in forest trees – from what we can measure to what we want to know. New Phytol 211:386–403

    CAS  PubMed  Google Scholar 

  • Hew C-S, Krotkov G, Canvin DT (1969) Effects of temperature on photosynthesis and CO2 evolution in light and darkness by green leaves. Plant Phys 44:671–677

    CAS  Google Scholar 

  • Hoch G, Körner C (2012) Global patterns of mobile carbon stores in trees at the high-elevation tree line. Glob Ecol Biogeogr 21:861–871

    Google Scholar 

  • Huang J, Kautz M, Trowbridge AM, Hammerbacher A, Raffa KF, Adams HD, Goodsman DW, Xu C, Meddens AJH, Kandasamy D, Gershenzon J, Seidl R, Hartmann H (2020) Tree defense and bark beetles in drying world: carbon partitioning, functioning and modelling. New Phytol 225:26–36

    PubMed  Google Scholar 

  • Hussain A, Classens G, Guevara-Rozo S, Cale JA, Rajabzadeh R, Peters BR, Erbilgin N (2020) Spatial variation in soil available water holding capacity alters carbon mobilization and allocation to chemical defenses along jack pine stems. Environ Exp Bot 171:103902

    CAS  Google Scholar 

  • 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 170:657–675

    CAS  PubMed  Google Scholar 

  • Kersten PJ, Kooper BJ, Raffa KF, Illman BL (2006) Rapid analysis of abietanes in conifers. J Chem Ecol 32:2679–2685

    CAS  PubMed  Google Scholar 

  • Klutsch JG, Cale JA, Whitehouse C, Kanekar SS, Erbilgin N (2017) Trap trees: an effective method of monitoring mountain pine beetle activities in novel habitats. Can J For Res 47:1432–1437

    CAS  Google Scholar 

  • Kopper BJ, Illman BL, Kersten PJ, Klepzig KD, Raffa KF (2005) Effects of diterpene acids on components of a conifer bark beetle–fungal interaction: tolerance by Ips pini and sensitivity by its associate Ophiostoma ips. Environ Entomol 34:486–493

    CAS  Google Scholar 

  • Lahr EC, Krokene P (2013) Conifer stored resources and resistance to a fungus associated with the spruce bark beetle Ips typographus. PLoS One 8:e72405

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lahr EC, Sala A (2014) Species, elevation, and diameter affect whitebark pine and lodgepole pine stored resources in the sapwood and phloem: implications for bark beetle outbreaks. Can J For Res 44:1312–1319

    CAS  Google Scholar 

  • Linkosalo T, Heikkinen J, Pulkkinen P, Mäkipää R (2014) Fluorescence measurements show stronger cold inhibition of photosynthetic light reactions in Scots pine compared to Norway spruce as well as during spring compared to autumn. Fron Plant Sci 5:264. https://doi.org/10.3389/fpls.2014.00264

    Article  Google Scholar 

  • Lintunen A, Paljakka T, Jyske T, Peltoniemi M, Sterck F, von Arx G, Cochard H, Copini P, Caldeira MC, Delzon S, Gebauer R, Grönlund L, Kiorapostolou N, Lechthaler S, Lobo-do-Vale R, Peters RL, Petit G, Prendin AL, Salmon Y, Steppe K, Urban J, Roig Juan S, Robert EMR, Hölttä T (2016) Osmolality and non-structural carbohydrate composition in the secondary phloem of trees across a latitudinal gradient in Europe. Front Plant Sci 7:726. https://doi.org/10.3389/fpls.2016.00726

    Article  PubMed  PubMed Central  Google Scholar 

  • Little EL Jr (1979) Checklist of United States trees (native and naturalized). USDA Forest Service, agriculture handbook no. 541; Washington, DC: USA

  • Lotan JE, Critchfield WB (1990) Pinus contorta Dougl. ex loud. In: Burns RM, Honkala BH, technical coordinators. Silvics of North America, Vol. 1. Washington, DC, USA: USDA Agriculture Handbook 654:302–315

  • Moreira X, Mooney KA, Rasmann S, Petry WK, Carrillo-Gavilán A, Zas R, Sampedro L (2014) Trade-offs between constitutive and induced defences drive geographical and climatic clines in pine chemical defences. Ecol Lett 17:537–546

    PubMed  Google Scholar 

  • Moreira X, Sampedro L, Zas R, Pearse IS (2016) Defensive traits in young pine trees cluster into two divergent syndromes related to early growth rate. PLoS One 11:e0152537

    PubMed  PubMed Central  Google Scholar 

  • Oksanen JF, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P et al (2018) Vegan: community ecology package. R package version 2.4–6. https://CRAN.R-project.org/package=vegan

  • Ott DS, Yanchuck AD, Huber DPW (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 37:1002–1012

    CAS  PubMed  Google Scholar 

  • Pallardy SG (2008) Carbohydrates. In: Pallardy SG (eds) Physiology of woody plants. 3rd edition. Elsevier, San Diego, CA, USA: Academic Press, pp 199–216

  • Pearse IS, Hipp AL (2012) Global patterns of leaf defenses in oak species. Evolution 66:2272–2286

    PubMed  Google Scholar 

  • Pureswaran DS, Borden JH (2005) Primary attraction and kairomonal host discrimination in three species of Dendroctonus (Coleoptera: Scolytidae). Agric For Entomol 7:219–230

    Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • 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. Rec Adv Phytochem 39:80–118

    Google Scholar 

  • Raffa KF, Powell EN, Townsend PA (2013) Temperature-driven range expansion of an irruptive insect heightened by weakly coevolved plant defenses. Proc Natl Acad Sci 110:2193–2198

    CAS  PubMed  Google Scholar 

  • Raffa KF, Mason CJ, Bonello P, Cook S, Erbilgin N, Keefover-Ring KJG, Villari C, Townsend PA (2017) Defence syndromes in lodgepole – whitebark pine ecosystems relate to degree of historical exposure to mountain pine beetles. Plant Cell Environ 40:1791–1806

    CAS  PubMed  Google Scholar 

  • Rasmann S, Pellissier L, Defossez E, Jactel H, Kunstler G (2014) Climate-driven change in plant–insect interactions along elevation gradients. Fun Ecol 28:46–54

    Google Scholar 

  • Roth M, Hussain A, Cale JA, Erbilgin N (2018) Successful colonization of lodgepole pine trees by mountain pine beetle increased monoterpene production and exhausted carbohydrate reserves. J Chem Ecol 44:209–214

    CAS  PubMed  Google Scholar 

  • Sampedro L, Moreira X, Zas R (2011) Costs of constitutive and herbivore induced chemical defences in pine trees emerge only under low nutrient availability. J Ecol 99:818–827

    Google Scholar 

  • Schemske DW, Mittelbach GG, Cornell HV, Sobel MJ, Roy K (2009) Is there a latitudinal gradient in the importance of biotic interactions? Ann Rev Ecol Evol Syst 40:245–269

    Google Scholar 

  • Shi H, Zhou Q, Liu X, Xie F, Li F, Zhang Q, Dang H (2019) Variations in carbon source-sink relationships in subalpine fir across elevational gradients. Plant Biol 21:64–70

    CAS  PubMed  Google Scholar 

  • Taft S, Najar A, Godbout J, Bousquet J, Erbilgin N (2015) Variations in foliar monoterpenes across the range of jack pine reveal three widespread chemotypes: implications to host expansion of invasive mountain pine beetle. Front Plant Sci 6:1–12

    Google Scholar 

  • Trouvelot S, Héloir M-C, Poinssot B, Gauthier A, Paris F, Guillier C, Combier M, Trdá L, Daire X, Adrian M (2014) Carbohydrates in plant immunity and plant protection: roles and potential applications as foliar sprays. Front Plant Sci 5:592. https://doi.org/10.3389/fpls.2014.00592

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang T, Hamann A, Mbogga M (2008) ClimateAB v3.21: a program to generate projected, normal, decadal, annual, seasonal and monthly interpolated climate data for Alberta. ISBN No. 978-0-7785-9184-9

  • Wiley R, Rogers BJ, Hodgkinson R, Landhäusser SM (2016) Non-structural carbohydrate dynamics of lodgepole pine dying from mountain pine beetle attack. New Phytol 209:550–562

    CAS  PubMed  Google Scholar 

  • Woods EC, Hastings AP, Turley NE, Heard SB, Agrawal AA (2012) Adaptive geographical clines in the growth and defense of a native plant. Ecol Monogr 82:149–168

    Google Scholar 

  • Zhao S, Erbilgin N (2019) Larger resin ducts are linked to the survival of lodgepole pine trees during mountain pine beetle outbreak. Front Plant Sci 10:1459. https://doi.org/10.3389/fpls.2019.01459

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Alberta Agriculture and Forestry and Parks Canada for their help for site selection. Field work was conducted by Gail Classens. We acknowledge the Associate Editor of the Journal of Chemical Ecology, Dr. Ann E Hagerman’s and two anonymous reviewers’ contributions to improve the quality of this manuscript during review process. We acknowledge that all research presented in the manuscript was conducted in accordance with all applicable laws and rules set forth by the provincial (Alberta) and federal governments and the University of Alberta, and that all necessary permits were in hand when the research was conducted.

Funding

Funding for this project was provided by NSERC-Discovery Award to NE, the Alberta Conservation Association ‘ACA Grants in Biodiversity Program’, and Government of Alberta ‘Master’s level Queen Elizabeth II-Graduate Scholarship’.

Author information

Authors and Affiliations

Authors

Contributions

NE and MM conceived the research project. MM designed and performed the studies and ran chemical and statistical analyses. AH and CW assisted in site selection, and data analyses. JK and JAC assisted in experimental design and running chemical analyses. JGK and SZ provided statistical advice. MM and NE wrote the manuscript; all authors provided editorial advice.

Corresponding author

Correspondence to Nadir Erbilgin.

Ethics declarations

Conflicts of Interest/Competing Interests

(include appropriate disclosures): None.

Ethics Approval

(include appropriate approvals or waivers): Not applicable.

Consent to Participate

(include appropriate statements): Not applicable.

Consent for Publication

(include appropriate statements): Not applicable.

Code Availability

(software application or custom code): Not applicable.

Supplementary Information

ESM 1

(DOCX 431 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mullin, M., Klutsch, J.G., Cale, J.A. et al. Primary and Secondary Metabolite Profiles of Lodgepole Pine Trees Change with Elevation, but Not with Latitude. J Chem Ecol 47, 280–293 (2021). https://doi.org/10.1007/s10886-021-01249-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-021-01249-y

Keywords

Navigation