Abstract
The mechanical strengthening of leaves protects seedlings from herbivore damage, particularly in shade-tolerant evergreens. Interspecific studies have shown that leaf mass per area (LMA) and leaf toughness (force-to-punch) can play this role. Here we compared the influence of LMA and leaf toughness on herbivory and plant performance in a temperate rainforest. In seedlings of 14 evergreen species, we addressed the across-species relationship between LMA and force-to-punch, and compared the strength of their associations with herbivory and with species’ light requirements. Moreover, in four understory species we performed a multivariate analysis within-species, analogue to phenotypic selection analysis, evaluating the correlation between seedling performance, estimated as chlorophyll fluorescence (Fv/Fm), and force-to-punch, LMA, lamina density and lamina thickness. LMA and force-to-punch were positively associated across species. Herbivory was negatively correlated with both force-to-punch and LMA, but a stepwise multiple regression showed that force-to-punch was a better predictor of herbivory. Neither leaf lamina density nor thickness were associated with herbivore damage. Those species that were more shade-tolerant had leaves with higher force-to-punch and higher LMA, and less slender seedlings. In the within-species analyses in four shade-tolerant species, seedling performance was generally positively associated with force-to-punch, but not with LMA, lamina thickness, or lamina density. Both interspecific and within-species analyses showed that force-to-punch is more strongly related to herbivore damage and plant performance than LMA. This consistency between interspecific patterns of trait covariation and within-species trait-performance associations suggests that natural selection could have shaped the relationships between mechanical traits and ecological roles observed across species.
Similar content being viewed by others
Data availability
The data underlying this study are available from the author on request.
Code availability
Not applicable
References
Ackerly DD, Reich PB (1999) Convergence and correlations among leaf size and function in seed plants: a comparative test using independent contrasts. Am J Bot 86:1272–1281
Ackerly DD, Dudley SA, Sultan SE, Schmitt J, Coleman JS, Linder CR, Sandquist DR, Geber MA, Evans AS, Dawson TE, Lechowicz MJ (2000) The evolution of plant ecophysiological traits: recent advances and future directions. Bioscience 50:979–995
Alvarez-Clare S, Kitajima K (2007) Physical defence traits enhance seedling survival of neotropical tree species. Funct Ecol 21:1044–1054
Anderegg LDL, Berner LT, Badgley G, Sethi ML, Law BE, HilleRisLambers J (2018) Within-species patterns challenge our understanding of the leaf economics spectrum. Ecol Lett 21:734–744
Aragón CF, Escudero A, Valladares F (2008) Stress-induced dynamic adjustments of reproduction differentially affect fitness components of a semi‐arid plant. J Ecol 96:222–229
Aranwela N, Sanson G, Read J (1999) Methods of assessing leaf-fracture properties. New Phytol 144:369–383
Arntz AM, DeLucia EH, Jordan N (2000) From fluorescence to fitness: variation in photosynthetic rate affects fecundity and survivorship. Ecology 81:2567–2576
Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745
Clark DB, Clark DA (1989) The role of physical damage in the seedling mortality regime of a neotropical rain forest. Oikos 55:225–230
Clark DB, Clark DA (1991) The impact of physical damage on canopy tree regeneration in tropical rain forest. J Ecol 79:447–457
Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335
Díaz S, Kattge J, Cornelissen JHC, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Prentice IC, Garnier E, Bönisch G, Westoby M, Poorter H, Reich PB, Moles AT, Dickie J, Gillison AN, Zanne AE, Chave J, Wright SJ, 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
Domínguez CA, Dirzo R, Bullock SH (1989) On the function of floral nectar in Croton suberosus (Euphorbiaceae). Oikos 56:109–114
Dorsch K (2003) Hydrogeologische Untersuchungen der Geothermalfelder von Puyehue und Cordón Caulle, Chile. Dissertation, Ludwig-Maximilians Universität
Drake DR, Pratt LW (2001) Seedling mortality in Hawaiian rain forest: the role of small-scale physical disturbance. Biotropica 33:319–323
Futuyma DJ (2005) Evolutionary biology. In: Futuyma DJ (ed) Evolution. Sinauer Associates, Sunderland, pp 1–15
Gianoli E (2001) Lack of differential plasticity to shading of internodes and petioles with growth habit in Convolvulus arvensis (Convolvulaceae). Int J Plant Sci 162:1247–1252
Gianoli E, Saldaña A (2013) Phenotypic selection on leaf functional traits of two congeneric species in a temperate rainforest is consistent with their shade tolerance. Oecologia 173:13–21
Gianoli E, Salgado-Luarte C (2017) Tolerance to herbivory and the resource availability hypothesis. Biol Lett 13:20170120
Gianoli E, Saldaña A, Jiménez-Castillo M, Valladares F (2010) Distribution and abundance of vines along the light gradient in a southern temperate rainforest. J Veg Sci 21:66–73
Gianoli E, Salgado-Luarte C, Escobedo VM (2023) Shade tolerance and the relationship between herbivory and light availability. Int J Plant Sci 184:519–524
Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114
Gommers CMM, Visser EJW, St Onge KR, Voesenek LACJ, Pierik R (2013) Shade tolerance: when growing tall is not an option. Trends Plant Sci 18:65–71
Gray GR, Chauvin LP, Sarhan F, Huner NP (1997) Cold acclimation and freezing tolerance (a complex interaction of light and temperature). Plant Physiol 114:467–474
Hüner NP, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230
Hunter JP (1998) Key innovations and the ecology of macroevolution. Trends Ecol Evol 13:31–36
Jin Y, Qian H (2023) U. PhyloMaker: an R package that can generate large phylogenetic trees for plants and animals. Plant Divers 45:347–352
Kitajima K, Poorter H (2010) Tissue-level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. New Phytol 186:708–721
Kitajima K, Llorens A-M, Stefanescu C, Timchenko MV, Lucas PW, Wright SJ (2012) How cellulose-based leaf toughness and lamina density contribute to long leaf lifespans of shade‐tolerant species. New Phytol 195:640–652
Kuusk V, Niinemets Ü, Valladares F (2018) A major trade-off between structural and photosynthetic investments operative across plant and needle ages in three Mediterranean pines. Tree Physiol 38:543–557
Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226
Linder CR (2000) Adaptive evolution of seed oil composition. Am Nat 156:442–458
Lusk CH (2002) Leaf area accumulation helps juvenile evergreen trees tolerate shade in a temperate rainforest. Oecologia 132:188–196
Lusk CH, Corcuera LJ (2011) Effects of light availability and growth rate on leaf lifespan of four temperate rainforest Proteaceae. Rev Chil Hist Nat 84:269–277
Lusk CH, Warton DI (2007) Global meta-analysis shows that relationships of leaf mass per area with species shade tolerance depend on leaf habit and ontogeny. New Phytol 176:764–774
Lusk CH, Chazdon RL, Hofmann G (2006) A bounded null model explains juvenile tree community structure along light availability gradients in a temperate rain forest. Oikos 112:131–137
Lusk CH, Reich PB, Montgomery RA, Ackerly DA, Cavender-Bares J (2008a) Why are evergreen leaves so contrary about shade? Trends Ecol Evol 23:299–303
Lusk CH, Falster DS, Jara-Vergara CK, Jiménez‐Castillo M, Saldaña‐Mendoza A (2008b) Ontogenetic variation in light requirements of juvenile rainforest evergreens. Funct Ecol 22:454–459
Lusk CH, Onoda Y, Kooyman R, Gutiérrez-Girón A (2010) Reconciling species‐level vs plastic responses of evergreen leaf structure to light gradients: shade leaves punch above their weight. New Phytol 186:429–438
Lusk CH, Pérez-Millaqueo MM, Piper FI, Saldaña A (2011) Ontogeny, understorey light interception and simulated carbon gain of juvenile rainforest evergreens differing in shade tolerance. Ann Bot 108:419–428
Madriaza K, Saldaña A, Salgado-Luarte C, Escobedo VM, Gianoli E (2019) Chlorophyll fluorescence may predict tolerance to herbivory. Int J Plant Sci 180:81–85
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence: a practical guide. J Exp Bot 51:659–668
Molina-Montenegro MA, Torres-Díaz C, Gallardo-Cerda J, Leppe M, Gianoli E (2013) Seabirds modify El Niño effects on tree growth in a southern Pacific island. Ecology 94:2415–2425
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998
Nabity PD, Zavala JA, DeLucia EH (2009) Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Ann Bot 103:655–663
Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Funct Ecol 18:419–425
Onoda Y, Westoby M, Adler PB, Choong AM, Clissold FJ, Cornelissen JH, Díaz S, Dominy NJ, Elgart A, Enrico L, Fine PVA, Howard JJ, Jalili A, Kitajima K, Kurokawa H, McArthur C, Lucas PW, Markesteijn L, Pérez-Harguindeguy N, Poorter L, Richards L, Santiago LS, Sosinski EE, Van Bael SA, Warton DI, Wright IJ, Wright SJ, Yamashita N (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312
Onoda Y, Wright IJ, Evans JR, Hikosaka K, Kitajima K, Niinemets Ü, Poorter H, Tosens T, Westoby M (2017) Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytol 214:1447–1463
Osnas JLD, Katabuchi M, Kitajima K, Wright SJ, Reich PB, Van Bael SA, Kraft NJB, Samaniego MJ, Pacala SW, Lichstein JW (2018) Divergent drivers of leaf trait variation within species, among species, and among functional groups. Proc Natl Acad Sci USA 115:5480–5485
Pérez-Harguindeguy N, Díaz S, Vendramini F, Cornelissen JH, Gurvich DE, Cabido M (2003) Leaf traits and herbivore selection in the field and in cafeteria experiments. Austral Ecol 28:642–650
Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588
Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) (1991) Plant-animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York
Qian H, Jin Y (2016) An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. J Plant Ecol 9:233–239
R Core Team (2016) R: a language and environment for statistical computing. Vienna, Austria
Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: traits, spectra, and strategies. Int J Plant Sci 64:S143–S164
Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223
Saldaña A, Lusk CH (2003) Influencia De las especies del dosel en la disponibilidad de recursos y regeneración avanzada en un bosque templado lluvioso del sur de Chile. Rev Chil Hist Nat 76:639–650
Saldaña A, Gianoli E, Lusk CH (2005) Ecophysiological responses to light availability in three Blechnum species (Pteridophyta, Blechnaceae) of different ecological breadth. Oecologia 145:252–257
Saldaña A, Lusk CH, Gonzáles WL, Gianoli E (2007) Natural selection on ecophysiological traits of a fern species in a temperate rainforest. Evol Ecol 21:651–662
Salgado-Luarte C, Gianoli E (2010) Herbivory on temperate rainforest seedlings in sun and shade: resistance, tolerance and habitat distribution. PLoS ONE 5:e11460
Salgado-Luarte C, Gianoli E (2012) Herbivores modify selection on plant functional traits in a temperate rainforest understory. Am Nat 180:E42–E53
Salgado-Luarte C, Gianoli E (2017) Shade tolerance and herbivory are associated with RGR of tree species via different functional traits. Plant Biol 19:413–419
Salgado-Luarte C, González-Teuber M, Madriaza K, Gianoli E (2023) Trade-off between plant resistance and tolerance to herbivory: mechanical defenses outweigh chemical defenses. Ecology 104:e3860
Schluter D (1996) Ecological causes of adaptive radiation. Am Nat 148:S40–S64
Shabala S (2003) Screening plants for environmental fitness: chlorophyll fluorescence as a Holy Grail for plant breeders. In: Hemantaranjan A (ed) Advances in Plant Physiology, vol 5. Scientific, Jodhpur, pp 287–340
Shah DU, Reynolds TP, Ramage MH (2017) The strength of plants: theory and experimental methods to measure the mechanical properties of stems. J Exp Bot 68:4497–4516
Symonds MRE, Blomberg SP (2014) A primer on phylogenetic generalised least squares. In: Garamszegi LZ (ed) Modern phylogenetic comparative methods and their application in evolutionary biology: concepts and practice. Springer, Berlin, pp 105–130
Thomson VP, Cunningham SA, Ball MC, Nicotra AB (2003) Compensation for herbivory by Cucumis sativus through increased photosynthetic capacity and efficiency. Oecologia 134:167–175
Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 39:237–257
Valladares F, Saldaña A, Gianoli E (2012) Costs versus risks: architectural changes with changing light quantity and quality in saplings of temperate rainforest trees of different shade tolerance. Austral Ecol 37:35–43
Van Gelder HA, Poorter L, Sterck F (2006) Wood mechanics, allometry, and life-history variation in a tropical rain forest tree community. New Phytol 171:367–378
Walters MB, Reich PB (1999) Low-light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad-leaved evergreen species differ? New Phytol 143:143–154
Westbrook JW, Kitajima K, Burleigh JG, Kress WJ, Erickson DL, Wright SJ (2011) What makes a leaf tough? Patterns of correlated evolution between leaf toughness traits and demographic rates among 197 shade-tolerant woody species in a neotropical forest. Am Nat 177:800–811
Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Evol Syst 33:125–159
Wilson KE, Ivanov AG, Öquist G, Grodzinski B, Sarhan F, Hüner NP (2006) Energy balance, organellar redox status, and acclimation to environmental stress. Botany 84:1355–1370
Witkowski ETF, Lamont BB (1991) Leaf specific mass confounds leaf density and thickness. Oecologia 88:486–493
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JH, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Pieter P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG, McGlinn DJ, O’Meara BC, Moles AT, Reich PB, Royer DL, Soltis DE, Stevens PF, Westoby M, Wright IJ, Aarssen L, Bertin RI, Calaminus A, Govaerts R, Hemmings F, Leishman MR, Oleksyn J, Soltis PS, Swenson NG, Warman L, Beaulieu JM (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506:89–92
Acknowledgements
We thank CONAF (National Forestry Corporation) for granting permits to work in Puyehue National Park. We are grateful to Y. Alcayaga, A. Vigil and K. Madriaza for help with fieldwork. VME was supported by FONDECYT 3200434.
Funding
This study was funded by FONDECYT (Fondo Nacional de Desarrollo Científico y Tecnológico) grants 1140070 and 1180334 awarded to EG.
Author information
Authors and Affiliations
Contributions
Conceptualization, EG; methodology, EG, CSL, VME, GCS; formal analysis, EG, VME; data curation, EG, VME; writing—original draft preparation, EG; writing—review and editing, EG, CSL, VME, GCS; funding acquisition, EG.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
All authors agreed with the content of the manuscript and all gave explicit consent to submit.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gianoli, E., Salgado-Luarte, C., Escobedo, V.M. et al. Leaf toughness is a better predictor of herbivory and plant performance than leaf mass per area (LMA) in temperate evergreens. Evol Ecol (2024). https://doi.org/10.1007/s10682-024-10298-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10682-024-10298-0