Abstract
Patterns of trait expression within some plant species have recently been shown to align with the leaf economics spectrum paradigm. Resistance to herbivores is also expected to covary with leaf economics traits. We selected 36 mature Populus tremuloides genotypes in a common garden to assess whether aspen leaf economics patterns follow those observed among species globally. We also evaluated leaf economics strategies in the context of insect resistance by conducting bioassays to determine the effects of plant traits on preference and performance of Lymantria dispar. We found that: (1) intraspecific trait patterns of P. tremuloides parallel those exhibited by the interspecific leaf economics spectrum, (2) herbivores preferred leaves from genotypes with resource-acquisitive strategies, and (3) herbivores also performed best on genotypes with resource-acquisitive strategies. We conclude that a leaf economics spectrum that incorporates defense traits is a useful tool for explaining intraspecific patterns of variation in plant strategies, including resistance to herbivores.
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Data availability
The datasets generated in this research are available from the corresponding author upon reasonable request and at the dryad link included in the supplemental information section.
Code availability
The code used to analyze these data is available from the corresponding author upon reasonable request.
References
Agrawal AA (2020) A scale-dependent framework for trade-offs, syndromes, and specialization in organismal biology. Ecology 101:1–24. https://doi.org/10.1002/ecy.2924
Anderegg LDL, Berner LT, Badgley G et al (2018) Within-species patterns challenge our understanding of the leaf economics spectrum. Ecol Lett 21:734–744. https://doi.org/10.1111/ele.12945
Armani M, Goodale UM, Charles-Dominique T et al (2020) Structural defence is coupled with the leaf economic spectrum across saplings of spiny species. Oikos. https://doi.org/10.1111/oik.06960
Bailey JK, Wooley SC, Lindroth RL, Whitham TG (2006) Importance of species interactions to community heritability: a genetic basis to trophic-level interactions. Ecol Lett 9:78–85. https://doi.org/10.1111/j.1461-0248.2005.00844.x
Bangert RK, Turek RJ, Rehill B et al (2006) A genetic similarity rule determines arthropod community structure. Mol Ecol 15:1379–1391. https://doi.org/10.1111/j.1365-294X.2005.02749.x
Barker HL, Holeski LM, Lindroth RL (2018) Genotypic variation in plant traits shapes herbivorous insect and ant communities on a foundation tree species. PLoS ONE 13:1–21. https://doi.org/10.1371/journal.pone.0200954
Barker HL, Holeski LM, Lindroth RL (2019a) Independent and interactive effects of plant genotype and environment on plant traits and insect herbivore performance: a meta-analysis with Salicaceae. Funct Ecol 33:939–941. https://doi.org/10.1111/1365-2435.13165
Barker HL, Riehl JF, Bernhardsson C et al (2019b) Linking plant genes to insect communities: identifying the genetic bases of plant traits and community composition. Mol Ecol 28:4404–4421. https://doi.org/10.1111/mec.15158
Boeckler GA, Gershenzon J, Unsicker SB (2011) Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochemistry 72:1497–1509. https://doi.org/10.1016/j.phytochem.2011.01.038
Capinera JL, Barbosa P (1976) Dispersal of first-instar gypsy moth larvae in relation to population quality. Oecologia 26:53–60. https://doi.org/10.1007/BF00345652
Cole CT (2005) Allelic and population variation of microsatellite loci in aspen (Populus tremuloides). New Phytol 167:155–164. https://doi.org/10.1111/j.1469-8137.2005.01423.x
Cole CT, Stevens MT, Anderson JE, Lindroth RL (2016) Heterozygosity, gender, and the growth–defense trade-off in quaking aspen. Oecologia 181:381–390. https://doi.org/10.1007/s00442-016-3577-6
Cole CT, Morrow CJ, Barker HL et al (2021) Growing up aspen: ontogeny and trade-offs shape growth, defence and reproduction in a foundation species. Ann Bot 127:505–517. https://doi.org/10.1093/aob/mcaa070
Coley PD (1987) Interspecific variation in plant anti-herbivore properties: the role of habitat quality and rate of disturbance. New Phytol 106:251–263. https://doi.org/10.1111/j.1469-8137.1987.tb04693.x
Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230(80):895–899. https://doi.org/10.1126/science.230.4728.895
Cook SP, Webb RE, Podgwaite JD, Reardon RC (2003) Increased mortality of gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae) exposed to gypsy moth nuclear polyhedrosis virus in combination with the phenolic glycoside salicin. J Econ Entomol 96:1662–1667. https://doi.org/10.1603/0022-0493-96.6.1662
Cope OL, Kruger EL, Rubert-Nason KF, Lindroth RL (2019) Chemical defense over decadal scales: ontogenetic allocation trajectories and consequences for fitness in a foundation tree species. Funct Ecol 33:2105–2115. https://doi.org/10.1111/1365-2435.13425
Cope OL, Keefover-Ring K, Kruger EL, Lindroth RL (2021) Growth–defense trade-offs shape population genetic composition in an iconic forest tree species. Proc Natl Acad Sci 118:1–6. https://doi.org/10.1073/pnas.2103162118
Cornelissen T, Wilson Fernandes G, Vasconcellos-Neto J (2008) Size does matter: variation in herbivory between and within plants and the plant vigor hypothesis. Oikos 117:1121–1130. https://doi.org/10.1111/j.0030-1299.2008.16588.x
Des Roches S, Post DM, Turley NE et al (2018) The ecological importance of intraspecific variation. Nat Ecol Evol 2:57–64. https://doi.org/10.1038/s41559-017-0402-5
Doane CC, McManus ML (eds) (1981) The Gypsy Moth: research toward integrated pest management (Technical Bulletin No. 1584). U.S. Department of Agriculture, Washington
Donaldson JR, Lindroth RL (2007) Genetics, environment, and their interaction determines efficacy of chemical defense in trembling aspen. Ecology 88:729–739. https://doi.org/10.1890/06-0064
Donovan LA, Maherali H, Caruso CM et al (2011) The evolution of the worldwide leaf economics spectrum. Trends Ecol Evol 26:88–95. https://doi.org/10.1016/j.tree.2010.11.011
Endara MJ, Coley PD (2011) The resource availability hypothesis revisited: a meta-analysis. Funct Ecol 25:389–398. https://doi.org/10.1111/j.1365-2435.2010.01803.x
Falk MA, Lindroth RL, Keefover K et al (2018) Genetic variation in aspen phytochemical patterns structures windows of opportunity for gypsy moth larvae. Oecologia 187:471–482. https://doi.org/10.1007/s00442-018-4160-0
Fritz RS, Crabb BA, Hochwender CG (2000) Preference and performance of a gall-inducing sawfly: a test of the plant vigor hypothesis. Oikos 89:555–563. https://doi.org/10.1034/j.1600-0706.2000.890315.x
Gong B, Zhang G (2014) Interactions between plants and herbivores: a review of plant defense. Acta Ecol Sin 34:325–336. https://doi.org/10.1016/j.chnaes.2013.07.010
Grady KC, Laughlin DC, Ferrier SM et al (2013) Conservative leaf economic traits correlate with fast growth of genotypes of a foundation riparian species near the thermal maximum extent of its geographic range. Funct Ecol 27:428–438. https://doi.org/10.1111/1365-2435.12060
Gripenberg S, Mayhew PJ, Parnell M, Roslin T (2010) A meta-analysis of preference–performance relationships in phytophagous insects. Ecol Lett 13:383–393. https://doi.org/10.1111/j.1461-0248.2009.01433.x
Heckman RW, Halliday FW, Mitchell CE (2019) A growth–defense trade-off is general across native and exotic grasses. Oecologia 191:609–620. https://doi.org/10.1007/s00442-019-04507-9
Hemming JDC, Lindroth RL (2000) Effects of phenolic glycosides and protein on gypsy moth (Lepidoptera: Lymantriidae) and forest tent caterpillar (Lepidoptera: Lasiocampidae) performance and detoxication activities. Environ Entomol 29:1108–1115. https://doi.org/10.1603/0046-225x-29.6.1108
Herms WJ, Mattson DA (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335
Hu YK, Pan X, Liu GF et al (2015) Novel evidence for within-species leaf economics spectrum at multiple spatial scales. Front Plant Sci 6:1–9. https://doi.org/10.3389/fpls.2015.00901
Hunt R (1982) Plant growth curves: the functional approach to plant growth analysis. Edward Arnold Ltd., London
Koricheva J, Hayes D (2018) The relative importance of plant intraspecific diversity in structuring arthropod communities: a meta-analysis. Funct Ecol 32:1704–1717. https://doi.org/10.1111/1365-2435.13062
Lance D, Barbosa P (1981) Host tree influences on the dispersal of first instar gypsy moths, Lymantria dispar (L.). Ecol Entomol 6:411–416. https://doi.org/10.1111/j.1365-2311.1981.tb00632.x
Lavenseau L (1982) Determination of the sex of caterpillars without dissection. Int J Insect Morphol Embryol 11:359–362. https://doi.org/10.1016/0020-7322(82)90025-3
Levins R, MacArthur R (1969) An hypothesis to explain the incidence of monophagy. Ecology 50:910–911. https://doi.org/10.2307/1933709
Liebhold AM, Gottschalk KW, Mason DA, Bush RR (1997) Forest susceptibility to the gypsy moth. J for 95:20–24. https://doi.org/10.1093/jof/95.5.20
Lindroth RL, St. Clair SB (2013) Adaptations of quaking aspen (Populus tremuloides Michx.) for defense against herbivores. For Ecol Manag 299:14–21. https://doi.org/10.1016/j.foreco.2012.11.018
Lindroth RL, Scriber JM, Hsia MTS (1988) Chemical ecology of the tiger swallowtail: mediation of host use by phenolic glycosides. Ecology 69:814–822. https://doi.org/10.2307/1941031
Martin AR, Rapidel B, Roupsard O et al (2017) Intraspecific trait variation across multiple scales: the leaf economics spectrum in coffee. Funct Ecol 31:604–612. https://doi.org/10.1111/1365-2435.12790
Mason CM, Donovan LA (2015) Does investment in leaf defenses drive changes in leaf economic strategy? A focus on whole-plant ontogeny. Oecologia 177:1053–1066. https://doi.org/10.1007/s00442-014-3177-2
Mayhew PJ (1997) Adaptive patterns of host-plant selection by phytophagous insects. Nord Soc Oikos 79:417–428. https://doi.org/10.2307/3546884
McManus M, Csóka G (2007) History and impact of gypsy moth in North America and comparison to recent outbreaks in Europe. Acta Silv Lignaria Hungarica 3:47–64
Messier J, McGill BJ, Enquist BJ, Lechowicz MJ (2017) Trait variation and integration across scales: is the leaf economic spectrum present at local scales? Ecography (cop) 40:685–697. https://doi.org/10.1111/ecog.02006
Mitton JB, Grant MC (1996) Genetic variation and the natural history of quaking aspen. Bioscience 46:25–31. https://doi.org/10.2307/1312652
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens HH, Szoecs E, Wagner H (2020) vegan: Community Ecology Package. R package version 2.5-7. https://CRAN.R-project.org/package=vegan
Osier TL, Hwang S-Y, Lindroth RL (2000) Within- and between-year variation in early season phytochemistry of quaking aspen (Populus tremuloides Michx.) clones. Biochem Syst Ecol 28:197–208
Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251. https://doi.org/10.2307/3545270
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Reich PB (2014) The world-wide “fast-slow” plant economics spectrum: a traits manifesto. J Ecol 102:275–301. https://doi.org/10.1111/1365-2745.12211
Rubert-Nason K, Keefover-Ring K, Lindroth RL (2018) Purification and analysis of salicinoids. Curr Anal Chem 14:423–429. https://doi.org/10.2174/1573411014666171221131933
Simpson SJ, Raubenheimer D (2001) The geometric analysis of nutrient—allelochemical interactions: a case study using locusts. Ecology 82:422–439. https://doi.org/10.1890/0012-9658(2001)082[0422:TGAONA]2.0.CO;2
Solari P, Cerboneschi A, Masala C et al (2002) Chemoreception in larvae of the moth Lymantria dispar. Ital J Zool 69:305–312. https://doi.org/10.1080/11250000209356474
Underwood DLA (1994) Intraspecific variability in host plant quality and ovipositional preferences in Eucheira socialis (Lepidoptera: Pieridae). Ecol Entomol 19:245–256. https://doi.org/10.1111/j.1365-2311.1994.tb00416.x
Valladares G, Lawton JH (1991) Host-plant selection in the holly leaf-miner: does mother know best? J Anim Ecol 60:227. https://doi.org/10.2307/5456
Westerband AC, Funk JL, Barton KE (2021) Intraspecific trait variation in plants: a renewed focus on its role in ecological processes. Ann Bot 127:397–410. https://doi.org/10.1093/aob/mcab011
Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Züst T, Agrawal AA (2017) Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annu Rev Plant Biol 68:513–534. https://doi.org/10.1146/annurev-arplant-042916-040856
Züst T, Rasmann S, Agrawal AA (2015) Growth–defense tradeoffs for two major anti-herbivore traits of the common milkweed Asclepias syriaca. Oikos 124:1404–1415. https://doi.org/10.1111/oik.02075
Acknowledgements
We thank Chris Cole and Mark Zierden for assistance with chemical analyses and Chris Cole and Jenn Riehl for genotype verification. S. Jaeger’s work was supported by a UW Holstrom Environmental Research Fellowship. Comments from Colin Orians, Carlos Ballaré, and two anonymous reviewers improved the manuscript.
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This research was funded by USDA National Institute of Food and Agriculture grants 2016-67013-25088 and WIS01651.
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CJM, SJJ, and RLL conceived and designed the experiments. RLL secured funding. CJM and SJJ conducted fieldwork, laboratory work, and analyzed the data. CJM and RLL wrote the manuscript.
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Communicated by Colin Mark Orians.
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Morrow, C.J., Jaeger, S.J. & Lindroth, R.L. Intraspecific variation in plant economic traits predicts trembling aspen resistance to a generalist insect herbivore. Oecologia 199, 119–128 (2022). https://doi.org/10.1007/s00442-022-05158-z
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DOI: https://doi.org/10.1007/s00442-022-05158-z