Skip to main content

Constitutive and Induced Defenses in Long-lived Pines Do Not Trade Off but Are Influenced by Climate

Abstract

Plants resist herbivores and pathogens by using constitutive (baseline) and inducible (change in defense after an attack) defenses. Inducibility has long been predicted to trade off with constitutive defense, reflecting the economic use of resources. However, empirical evidence for such tradeoffs is variable, and we still lack understanding about when and where defense trade-offs occur. We tested for tradeoffs between constitutive and induced defenses in natural populations of three species of long-lived pines (Pinus balfouriana, P. flexilis, P. longaeva) that differ greatly in constitutive defense and resistance to mountain pine beetle (MPB, Dendroctonus ponderosae). We also assessed how climate influenced constitutive and inducible defenses. At seven high-elevation sites in the western U.S., we simulated MPB attack to induce defenses and measured concentrations of terpene-based phloem defenses on days 0, 15, and 30. Constitutive and induced defenses did not trade off among or within species. Simulated MPB attack induced large increases in defense concentrations in all species independent of constitutive levels. MPB and its symbiotic fungi typically kill trees and thus could be selective forces maintaining strong inducibility within and among species. The contrasting constitutive concentrations in these species could be driven by the adaptation for specializing in harsh, high-elevation environments (e.g., P. balfouriana and P. longaeva) or by competition (e.g., P. flexilis), though these hypotheses have not been empirically examined. Climate influenced defenses, with the greatest concentrations of constitutive and induced defenses occurring at the coldest and driest sites. The interactions between climate and defenses have implications for these species under climate change.

This is a preview of subscription content, access via your institution.

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

Data Availability

The data sets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Code Availability

The code for data analysis generated during the current study is available from the corresponding author on reasonable request.

References

  • Adams AS, Boone CK, Bohlmann J, Raffa KF (2011) Responses of bark beetle-associated bacteria to host monoterpenes and their relationship to insect life histories. J Chem Ecol 37:808–817

    CAS  PubMed  Article  Google Scholar 

  • Agrawal AA, Conner JK, Rasmann S (2010) Tradeoffs and negative correlations in evolutionary ecology. In: Bell M, Eanes W, Futuyma D, Levinton J (eds) Evolution since Darwin: the first 150 years. Sinauer Associates, Sunderland, MA, pp 243–268

    Google Scholar 

  • Agrawal AA, Hastings AP (2019) Trade-offs constrain the evolution of an inducible defense within but not between plant species. Ecology 100:e02857

    PubMed  Article  Google Scholar 

  • Beasley RS, Klemmedson JO (1980) Ecological relationships of bristlecone pine. Am Midl Nat 104:242–252

    Article  Google Scholar 

  • Bentz B, Vandygriff J, Jensen C, Coleman T, Maloney P, Smith S, Grady A, Schen-Langenheim G (2014) Mountain pine beetle voltinism and life history characteristics across latitudinal and elevational gradients in the western United States. For Sci 60:434–449

    Article  Google Scholar 

  • Bentz BJ, Boone C, Raffa KF (2015) Tree response and mountain pine beetle attack preference, reproduction and emergence timing in mixed whitebark and lodgepole pine stands. Agr For Entomol 17:421–432

    Article  Google Scholar 

  • Bentz BJ, Hood SM, Hansen EM et al (2017) Defense traits in the long-lived Great Basin bristlecone pine and resistance to the native herbivore mountain pine beetle. New Phytol 213:611–624

    CAS  PubMed  Article  Google Scholar 

  • Bentz BJ, Millar CI, Vandygriff JC, Hansen EM (2022) Great Basin bristlecone pine mortality: causal factors and management implications. For Ecol Manag 509:120099

    Article  Google Scholar 

  • Bingham RA, Agrawal AA (2010) Specificity and trade-offs in the induced plant defence of common milkweed Asclepias syriaca to two lepidopteran herbivores. J Ecol 98:1014–1022

    Article  Google Scholar 

  • Brody AK, Karban R (1992) Lack of a tradeoff between constitutive and induced defenses among varieties of cotton. Oikos 65:301–306

    Article  Google Scholar 

  • Brooks ME, Kristensen K, van Benthem KJ et al (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378. https://doi.org/10.32614/RJ-2017-066

    Article  Google Scholar 

  • Bruening JM, Tran TJ, Bunn AG, Weiss SB, Salzer MW (2017) Fine-scale modeling of bristlecone pine treeline position in the Great Basin, USA. Environ Res Lett 12:014008

    Article  Google Scholar 

  • Brutovska E, Samelova A, Dušička J, Mičieta K (2013) Ageing of trees: application of general ageing theories. Ageing Res Rev 12:855–866

    PubMed  Article  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  Article  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Cipollini D, Heil M (2010) Costs and benefits of induced resistance to herbivores and pathogens in plants. Plant Sci Rev 5:1–25

    Google Scholar 

  • Cleaver CM, Jacobi WR, Burns KS, Means RE (2015) Limber pine in the central and southern Rocky Mountains: stand conditions and interactions with blister rust, mistletoe, and bark beetles. For Ecol Manag 358:139–153

    Article  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    CAS  PubMed  Article  Google Scholar 

  • Craine JM, Dybzinski R (2013) Mechanisms of plant competition for nutrients, water and light. Funct Ecol 27:833–840

    Article  Google Scholar 

  • Dudney JC, Nesmith JC, Cahill MC et al (2020) Compounding effects of white pine blister rust, mountain pine beetle, and fire threaten four white pine species. Ecosphere 11:e03263

    Article  Google Scholar 

  • Eckert AJ, Tearse BR, Hall BD (2008) A phylogeographical analysis of the range disjunction for foxtail pine (Pinus balfouriana, Pinaceae): the role of Pleistocene glaciation. Mol Ecol 17:1983–1997

    CAS  PubMed  Article  Google Scholar 

  • Eidson EL, Mock KE, Bentz BJ (2018) Low offspring survival in mountain pine beetle infesting the resistant Great Basin bristlecone pine supports the preference-performance hypothesis. PLoS ONE 13:e0196732

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Endara M-J, Coley PD (2011) The resource availability hypothesis revisited: a meta-analysis. Funct Ecol 25:389–398

    Article  Google Scholar 

  • Erbilgin N, Ma C, Whitehouse C et al (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  Article  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

    Article  Google Scholar 

  • Fine PV, Miller ZJ, Mesones I, Irazuzta S, Appel HM, Stevens MHH et al (2006) The growth–defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87:S150–S162

    PubMed  Article  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  Article  Google Scholar 

  • Gray CA, Runyon JB, Jenkins MJ, Giunta AD (2015) Mountain pine beetles use volatile cues to locate host limber pine and avoid non-host Great Basin bristlecone pine. PLoS ONE 10:e0135752

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Gray CA, Runyon JB, Jenkins MJ (2019) Great Basin bristlecone pine volatiles as a climate change signal across environmental gradients. Front For Glob Chang 2:10

    Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  • Hahn PG, Agrawal AA, Sussman KI, Maron JL (2019) Population variation, environmental gradients, and the evolutionary ecology of plant defense against herbivory. Am Nat 193:20–34

    PubMed  Article  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    CAS  PubMed  Article  Google Scholar 

  • Howe M, Mason CJ, Gratton C et al (2020) Relationships between conifer constitutive and inducible defenses against bark beetles change across levels of biological and ecological scale. Oikos 129:1093–1107

    Article  Google Scholar 

  • Karban R (2011) The ecology and evolution of induced resistance against herbivores. Funct Ecol 25:339–347

    Article  Google Scholar 

  • Karban R (2020) The ecology and evolution of induced responses to herbivory and how plants perceive risk. Ecol Ent 45:1–9

    Article  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  Article  Google Scholar 

  • Keefover-Ring K, Trowbridge A, Mason C, Raffa KF (2016) Rapid induction of multiple terpenoid groups by ponderosa pine in response to bark beetle-associated fungi. J Chem Ecol 42:1–12

    CAS  PubMed  Article  Google Scholar 

  • Kempel A, Schädler M, Chrobock T, Fischer M, van Kleunen M (2011) Tradeoffs associated with constitutive and induced plant resistance against herbivory. Proc Natl Acad Sci USA 108:5685–5689

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kopaczyk JM, Warguła J, Jelonek T (2020) The variability of terpenes in conifers under developmental and environmental stimuli. Environ Exp Bot 25:104197

    Article  CAS  Google Scholar 

  • Koricheva J, Nykänen H, Gianoli E (2004) Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades, masters of all? Am Nat 163:SE64–SE75

    Article  Google Scholar 

  • LaMarche VC Jr (1969) Environment in relation to age of bristlecone pines. Ecology 50:53–59

    Article  Google Scholar 

  • Lenth R(2021) emmeans: Estimated Marginal Means, aka Least-Squares Means. Version 1.6.2-1URL https://CRAN.R-project.org/package=emmeans

  • Lewinsohn E, Gijzen M, Croteau R (1991) Defense mechanisms of conifers: differences in constitutive and wound-induced monoterpene biosynthesis among species. Plant Physiol 96:44–49

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Litvak ME, Monson RK (1998) Patterns of induced and constitutive monoterpene production in conifer needles in relation to insect herbivory. Oecologia 114:531–540

    PubMed  Article  Google Scholar 

  • Lloyd A (1998) Growth of foxtail pine seedlings at treeline in the southeastern Sierra Nevada, California, USA. Ecoscience 5:250–257

    Article  Google Scholar 

  • Lombardero MJ, Ayres MP, Lorio PL Jr, Ruel JJ (2000) Environmental effects on constitutive and inducible resin defences of Pinus taeda. Ecol Lett 3:329–339

    Article  Google Scholar 

  • López-Goldar X, Zas R, Sampedro L (2020) Resource availability drives microevolutionary patterns of plant defences. Funct Ecol 34:1640–1652

    Article  Google Scholar 

  • Lutz JA, Van Wagtendonk JW, Franklin JF (2010) Climatic water deficit, tree species ranges, and climate change in Yosemite National Park. J Biogeogr 37:936–950

    Article  Google Scholar 

  • Millar CI, Westfall RD, Delany DL (2007) Response of high-elevation limber pine (Pinus flexilis) to multiyear droughts and 20th-century warming, Sierra Nevada, California, USA. Can J Forest Res 37:2508–2520

    Article  Google Scholar 

  • Moreira X, Mooney KA, Rasmann S, Petrym KW, 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  Article  Google Scholar 

  • Moreira X, Petry WK, Mooney KA, Rasmann S, Abdala-Roberts L (2018) Elevational gradients in plant defences and insect herbivory: recent advances in the field and prospects for future research. Ecography 41:1485–1496

    Article  Google Scholar 

  • Morris WF, Traw MB, Bergelson J (2006) On testing for a tradeoff between constitutive and induced resistance. Oikos 112:102–110

    Article  Google Scholar 

  • Mullin M, Klutsch JG, Cale JA, Hussain A, Zhao S, Whitehouse C, Erbilgin N (2021) Primary and secondary metabolite profiles of lodgepole pine trees change with elevation, but not with latitude. J Chem Ecol 47:280–293

    CAS  PubMed  Article  Google Scholar 

  • Nesmith JC, Wright M, Jules ES, McKinney ST (2019) Whitebark and foxtail pine in Yosemite, Sequoia, and Kings Canyon National Parks: Initial assessment of stand structure and condition. Forests 10:35

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R et al (2020) vegan: Community Ecology Package. R

  • package version 2.5-7. Available at: http://CRAN.R-project.org/package=vegan

  • (accessed 28 March 2022)

  • Piovesan G, Biondi F (2021) On tree longevity. New Phytol 231:1318–1337

    PubMed  Article  Google Scholar 

  • Powell EN, Raffa KF (2011) Fire injury reduces inducible defenses of lodgepole pine against mountain pine beetle. J Chem Ecol 37:1184–1192

    CAS  PubMed  Article  Google Scholar 

  • R Core Team (2021) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • 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 115:723–734

    Article  Google Scholar 

  • Raffa KF, Aukema B, Erbilgin N, Klepzig K, Wallin K(2005) Interactions among conifer terpenoids and bark beetles across multiple levels of scale: an attempt to understand links between population patterns and physiological processes. In: Romeo JT (ed) Recent Advances in Phytochemistry. Elsevier, Toronto, Canada, pp 79–118

  • Raffa KF, Aukema BH, Bentz BJ et al (2008) Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. Bioscience 58:501–517

    Article  Google Scholar 

  • Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecol Lett 14:476–483

    PubMed  Article  Google Scholar 

  • Redmond MD(2019) CWD and AET function V1.0.2. Zenodo. https://doi.org/10.5281/zenodo.4490031

  • Reid M, Sekhon J, LaFramboise L (2017) Toxicity of monoterpene structure, diversity and concentration to mountain pine beetles, Dendroctonus ponderosae: beetle traits matter more. J Chem Ecol 43:351–361

    CAS  PubMed  Article  Google Scholar 

  • Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DF (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 3–54

    Google Scholar 

  • Rossi S, Anfodillo T, Menardi R (2006) Trephor: a new tool for sampling microcores from tree stems. Iawa J 27:89–97

    Article  Google Scholar 

  • Rundel PW, Parsons DJ, Gordon DT (1977) Montane and subalpine vegetation of the Sierra Nevada and Cascade Ranges. In: Barbour MG, Major J (eds) Terrestrial vegetation of California. Wiley, New York, pp 559–599

    Google Scholar 

  • Salazar D, Marquis RJ (2012) Herbivore pressure increases toward the equator. Proc Natl Acad Sci USA 109:12616–12620

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Salzer M, Baisan C(2013) Dendrochronology of the “Currey Tree.” In: Second American Dendrochronology Conference. pp 13–17

  • 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

    Article  Google Scholar 

  • Schoettle AW, Rochelle SG (2000) Morphological variation of Pinus flexilis (Pinaceae), a bird-dispersed pine, across a range of elevations. Am J Bot 87:1797–1806

    CAS  PubMed  Article  Google Scholar 

  • Soderberg DN, Bentz BJ, Runyon JB, Hood SM, Mock(2022) Chemical defense strategies, induction timing, growth, and tradeoffs among and within co-occurring Pinus aristata and Pinus flexilis. Ecosphere, in press

  • Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55

    PubMed  Article  Google Scholar 

  • Stephenson NL (1990) Climatic control of vegetation distribution: the role of the water balance. Am Nat 135:649–670

    Article  Google Scholar 

  • Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185

    CAS  PubMed  Article  Google Scholar 

  • Thaler JS, Karban R (1997) A phylogenetic reconstruction of constitutive and induced resistance in Gossypium. Am Nat 149:1139–1146

    CAS  PubMed  Article  Google Scholar 

  • Underwood N, Morris W, Gross K, Lockwood III JR (2000) Induced resistance to Mexican bean beetles in soybean: variation among genotypes and lack of correlation with constitutive resistance. Oecologia 122:83–89

    CAS  PubMed  Article  Google Scholar 

  • van der Meijden E, Wijn M, Verkaar HJ (1988) Defence and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:S355–S363

    Article  Google Scholar 

  • Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291

    CAS  PubMed  Article  Google Scholar 

  • Villari C, Faccoli M, Battisti A, Bonello P, Marini L (2014) Testing phenotypic trade-offs in the chemical defence strategy of Scots pine under growth-limiting field conditions. Tree Physiol 34:919–930

    CAS  PubMed  Article  Google Scholar 

  • Windmuller-Campione MA, Long JN (2016) Limber pine (Pinus flexilis James), a flexible generalist of forest communities in the intermountain west. PLoS ONE 11:e0160324

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Zangerl AR, Bazzaz FA (1992) Theory and pattern in plant defense allocation. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens. Ecology, evolution, and genetics. University of Chicago Press, Chicago, Illinois, pp 363–391

    Google Scholar 

  • Zaynab M, Fatima M, Abbas S, Sharif Y, Umair M, Zafar MH, Bahadar K (2018) Role of secondary metabolites in plant defense against pathogens. Microb Pathogenesis 124:198–202

    CAS  Article  Google Scholar 

  • Zhao T, Krokene P, Hu J, Christiansen E, Björklund N, Långström B, Solheim H, Borg-Karlson AK (2011) Induced terpene accumulation in Norway spruce inhibits bark beetle colonization in a dose-dependent manner. PLoS ONE 6:e26649

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references

Acknowledgements

We thank Sharon Hood, Matt Hansen, Jim Vandygriff, David Soderberg, Amanda Townsend, and Jared Trilling for technical assistance. In addition, we thank Scott Baggett (Rocky Mountain Research Station) for statistical advice and Bill Morris (Duke University) for sharing code to run the Monte Carlo procedure. The findings and conclusions in this publication are those of the authors and should not be construed to represent any official USDA or U.S. Government determination or policy.

Funding

This study was funded by the USDA Forest Service, Forest Health Monitoring (WC-EM-F-14-1, INT-EM-17-03) and the Rocky Mountain Research Station.

Author information

Authors and Affiliations

Authors

Contributions

JBR and BJB conceived and designed the experiments and performed the experiments. JBR, BJB, CAQ analyzed the data. JBR and BJB wrote the manuscript; CAQ provided editorial advice.

Corresponding author

Correspondence to Justin B. Runyon.

Ethics declarations

Conflicts of interest/Competing interests:

The authors declare that they have no conflict of interest.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Runyon and Bentz share co-first authorship and contributed equally to this manuscript.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Below is the link to the electronic supplementary material.

Supplementary Material 1

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Runyon, J.B., Bentz, B.J. & Qubain, C.A. Constitutive and Induced Defenses in Long-lived Pines Do Not Trade Off but Are Influenced by Climate. J Chem Ecol (2022). https://doi.org/10.1007/s10886-022-01377-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10886-022-01377-z

Keywords

  • Mountain pine beetle
  • Pinus longaeva
  • Pinus balfouriana
  • Pinus flexilis
  • Defenses