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

Justin B. Runyon1, Barbara J. Bentz2, Claire A. Qubain1
1USDA Forest Service – Rocky Mountain Research Station, Bozeman, USA
2USDA Forest Service, Rocky Mountain Research Station, Logan, USA

Tóm tắt

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.

Từ khóa


Tài liệu tham khảo

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 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 Agrawal AA, Hastings AP (2019) Trade-offs constrain the evolution of an inducible defense within but not between plant species. Ecology 100:e02857 Beasley RS, Klemmedson JO (1980) Ecological relationships of bristlecone pine. Am Midl Nat 104:242–252 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 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 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 Bentz BJ, Millar CI, Vandygriff JC, Hansen EM (2022) Great Basin bristlecone pine mortality: causal factors and management implications. For Ecol Manag 509:120099 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 Brody AK, Karban R (1992) Lack of a tradeoff between constitutive and induced defenses among varieties of cotton. Oikos 65:301–306 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 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 Brutovska E, Samelova A, Dušička J, Mičieta K (2013) Ageing of trees: application of general ageing theories. Ageing Res Rev 12:855–866 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 Chiu CC, Keeling CI, Bohlmann J (2017) Toxicity of pine monoterpenes to mountain pine beetle. Sci Rep 7:8858 Cipollini D, Heil M (2010) Costs and benefits of induced resistance to herbivores and pathogens in plants. Plant Sci Rev 5:1–25 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 Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899 Craine JM, Dybzinski R (2013) Mechanisms of plant competition for nutrients, water and light. Funct Ecol 27:833–840 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 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 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 Endara M-J, Coley PD (2011) The resource availability hypothesis revisited: a meta-analysis. Funct Ecol 25:389–398 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 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 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 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 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 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 Hahn PG, Maron JL (2016) A framework for predicting intraspecific variation in plant defense. Trends Ecol Evol 31:646–656 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 Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335 Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66 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 Karban R (2011) The ecology and evolution of induced resistance against herbivores. Funct Ecol 25:339–347 Karban R (2020) The ecology and evolution of induced responses to herbivory and how plants perceive risk. Ecol Ent 45:1–9 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 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 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 Kopaczyk JM, Warguła J, Jelonek T (2020) The variability of terpenes in conifers under developmental and environmental stimuli. Environ Exp Bot 25:104197 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 LaMarche VC Jr (1969) Environment in relation to age of bristlecone pines. Ecology 50:53–59 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 Litvak ME, Monson RK (1998) Patterns of induced and constitutive monoterpene production in conifer needles in relation to insect herbivory. Oecologia 114:531–540 Lloyd A (1998) Growth of foxtail pine seedlings at treeline in the southeastern Sierra Nevada, California, USA. Ecoscience 5:250–257 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 López-Goldar X, Zas R, Sampedro L (2020) Resource availability drives microevolutionary patterns of plant defences. Funct Ecol 34:1640–1652 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 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 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 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 Morris WF, Traw MB, Bergelson J (2006) On testing for a tradeoff between constitutive and induced resistance. Oikos 112:102–110 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 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 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 Powell EN, Raffa KF (2011) Fire injury reduces inducible defenses of lodgepole pine against mountain pine beetle. J Chem Ecol 37:1184–1192 R Core Team (2021) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria 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 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 Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecol Lett 14:476–483 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 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 Rossi S, Anfodillo T, Menardi R (2006) Trephor: a new tool for sampling microcores from tree stems. Iawa J 27:89–97 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 Salazar D, Marquis RJ (2012) Herbivore pressure increases toward the equator. Proc Natl Acad Sci USA 109:12616–12620 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 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 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 Stephenson NL (1990) Climatic control of vegetation distribution: the role of the water balance. Am Nat 135:649–670 Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185 Thaler JS, Karban R (1997) A phylogenetic reconstruction of constitutive and induced resistance in Gossypium. Am Nat 149:1139–1146 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 van der Meijden E, Wijn M, Verkaar HJ (1988) Defence and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:S355–S363 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 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 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 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 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 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