Abstract
Leaf defenses have long been studied in the context of plant growth rate, resource availability, and optimal investment theory. Likewise, one of the central modern paradigms of plant ecophysiology, the leaf economics spectrum (LES), has been extensively studied in the context of these factors across ecological scales ranging from global species data sets to temporal shifts within individuals. Despite strong physiological links between LES strategy and leaf defenses in structure, function, and resource investment, the relationship between these trait classes has not been well explored. This study investigates the relationship between leaf defenses and LES strategy across whole-plant ontogeny in three diverse Helianthus species known to exhibit dramatic ontogenetic shifts in LES strategy, focusing primarily on physical and quantitative chemical defenses. Plants were grown under controlled environmental conditions and sampled for LES and defense traits at four ontogenetic stages. Defenses were found to shift strongly with ontogeny, and to correlate strongly with LES strategy. More advanced ontogenetic stages with more conservative LES strategy leaves had higher tannin activity and toughness in all species, and higher leaf dry matter content in two of three species. Modeling results in two species support the conclusion that changes in defenses drive changes in LES strategy through ontogeny, and in one species that changes in defenses and LES strategy are likely independently driven by ontogeny. Results of this study support the hypothesis that leaf-level allocation to defenses might be an important determinant of leaf economic traits, where high investment in defenses drives a conservative LES strategy.
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References
Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432. doi:10.1111/j.1365-2435.2010.01796.x
Agrawal AA, Conner JK, Stinchcombe JR (2004) Evolution of plant resistance and tolerance to frost damage. Ecol Lett 7:1199–1208. doi:10.1111/j.1461-0248.2004.00680.x
Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175:481–493. doi:10.1086/650722
Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67
Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst 16:363–392. doi:10.2307/2097053
Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448
Brouillette LC, Mason CM, Shirk RY, Donovan LA (2014) Adaptive differentiation of traits related to resource use in a desert annual along a resource gradient. New Phytol 201:1316–1327. doi:10.1111/nph.12628
Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899. doi:10.1126/science.230.4728.895
Cooke J, Leishman MR (2011) Silicon concentration and leaf longevity: is silicon a player in the leaf dry mass spectrum? Funct Ecol 25:1181–1188. doi:10.1111/j.1365-2435.2011.01880.x
Donovan LA, Maherali H, Caruso CM, Huber H, de Kroon H (2011) The evolution of the worldwide leaf economics spectrum. Trends Ecol Evol 26:88–95. doi:10.1016/j.tree.2010.11.011
Donovan LA, Mason CM, Bowsher AW, Goolsby EW, Ishibashi CDA (2014) Ecological and evolutionary lability of plant traits affecting carbon and nutrient cycling. J Ecol 102:302–314. doi:10.1111/1365-2745.12193
Dunbar-Co S, Sporck Margaret J, Sack L (2009) Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago radiation. Int J Plant Sci 170:61–75. doi:10.1086/593111
Ehleringer J (1984) Ecology and ecophysiology of leaf pubescence in North American desert plants. Biol Chem Plant Trichomes 113–132
Elger A, Willby NJ (2003) Leaf dry matter content as an integrative expression of plant palatability: the case of freshwater macrophytes. Funct Ecol 17:58–65. doi:10.1046/j.1365-2435.2003.00700.x
Endara M-J, Coley PD (2011) The resource availability hypothesis revisited: a meta-analysis. Funct Ecol 25:389–398. doi:10.1111/j.1365-2435.2010.01803.x
Freschet GT, Cornelissen JHC, van Logtestijn RSP, Aerts R (2010) Evidence of the ‘plant economics spectrum’ in a subarctic flora. J Ecol 98:362–373. doi:10.1111/j.1365-2745.2009.01615.x
Futuyma DJ, Agrawal AA (2009) Macroevolution and the biological diversity of plants and herbivores. Proc Natl Acad Sci USA 106:18054–18061. doi:10.1073/pnas.0904106106
Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge, UK
Grady KC 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. doi:10.1111/1365-2435.12060
Hagerman AE (1987) Radial diffusion method for determining tannin in plant extracts. J Chem Ecol 13:437–449. doi:10.1007/bf01880091
Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspect Plant Ecol Evol Syst 8:157–178. doi:10.1016/j.ppees.2007.01.001
Heberling JM, Fridley JD (2012) Biogeographic constraints on the world-wide leaf economics spectrum. Global Ecol Biogeogr 21:1137–1146. doi:10.1111/j.1466-8238.2012.00761.x
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335. doi:10.2307/2830650
Ishida A, Yazaki K, Hoe AL (2005) Ontogenetic transition of leaf physiology and anatomy from seedlings to mature trees of a rain forest pioneer tree, Macaranga gigantea. Tree Physiol 25:513–522
Jullien A, Allirand J-M, Mathieu A, Andrieu B, Ney B (2009) Variations in leaf mass per area according to N nutrition, plant age, and leaf position reflect ontogenetic plasticity in winter oilseed rape (Brassica napus L.). Field Crop Res 114:188–197. doi:10.1016/j.fcr.2009.07.015
Kikuzawa K, Onoda Y, Wright IJ, Reich PB (2013) Mechanisms underlying global temperature-related patterns in leaf longevity. Global Ecol Biogeogr 22:982–993. doi:10.1111/geb.12042
Kitajima K, Poorter L (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. doi:10.1111/j.1469-8137.2010.03212.x
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. doi:10.1111/j.1469-8137.2012.04203.x
Korth KL, et al. (2006) Medicago truncatula mutants demonstrate the role of plant calcium oxalate crystals as an effective defense against chewing insects. Plant Physiol 141:188–195. doi:10.1104/pp.106.076737
Levin DA (1973) The role of trichomes in plant defense. Q Rev Biol 48:3–15. doi:10.2307/2822621
Liakoura V, Stefanou M, Manetas Y, Cholevas C, Karabourniotis G (1997) Trichome density and its UV-B protective potential are affected by shading and leaf position on the canopy. Environ Exp Bot 38:223–229. doi:10.1016/S0098-8472(97)00005-1
Lieurance D, Cipollini D (2013) Environmental influences on growth and defence responses of the invasive shrub, Lonicera maackii, to simulated and real herbivory in the juvenile stage. Ann Bot 112:741–749. doi:10.1093/aob/mct070
Lincoln D (1985) Host-plant protein and phenolic resin effects on larval growth and survival of a butterfly. J Chem Ecol 11:1459–1467. doi:10.1007/bf01012192
Lloyd J, Bloomfield K, Domingues TF, Farquhar GD (2013) Photosynthetically relevant foliar traits correlating better on a mass vs an area basis: of ecophysiological relevance or just a case of mathematical imperatives and statistical quicksand? New Phytol 199:311–321. doi:10.1111/nph.12281
Markó G, Gyuricza V, Bernáth J, Altbacker V (2008) Essential oil yield and composition reflect browsing damage of junipers. J Chem Ecol 34:1545–1552. doi:10.1007/s10886-008-9557-5
Mason CM, McGaughey SE, Donovan LA (2013) Ontogeny strongly and differentially alters leaf economic and other key traits in three diverse Helianthus species. J Exp Bot 64:4089–4099. doi:10.1093/jxb/ert249
Massey FP, Ennos AR, Hartley SE (2006) Silica in grasses as a defence against insect herbivores: contrasting effects on folivores and a phloem feeder. J Anim Ecol 75:595–603. doi:10.1111/j.1365-2656.2006.01082.x
Mediavilla S, Escudero A (2009) Ontogenetic changes in leaf phenology of two co-occurring Mediterranean oaks differing in leaf life span. Ecol Res 24:1083–1090. doi:10.1007/s11284-009-0587-4
Moles AT et al (2011) Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes. New Phytol 191:777–788. doi:10.1111/j.1469-8137.2011.03732.x
Moles AT et al (2013) Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat? New Phytol 198:252–263. doi:10.1111/nph.12116
Mooney HA (1972) The carbon balance of plants. Annu Rev Ecol Syst 3:315–346. doi:10.2307/2096851
Niinemets Ü (2004) Adaptive adjustments to light in foliage and whole-plant characteristics depend on relative age in the perennial herb Leontodon hispidus. New Phytol 162:683–696. doi:10.1111/j.1469-8137.2004.01071.x
Ordonez JC, van Bodegom PM, Witte JPM, Wright IJ, Reich PB, Aerts R (2009) A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Glob Ecol Biogeogr 18:137–149. doi:10.1111/j.1466-8238.2008.00441.x
Osnas JLD, Lichstein JW, Reich PB, Pacala SW (2013) Global leaf trait relationships: mass, area, and the leaf economics spectrum. Science 340:741–744. doi:10.1126/science.1231574
Palow DT, Nolting K, Kitajima K, Sack L (2012) Functional trait divergence of juveniles and adults of nine Inga species with contrasting soil preference in a tropical rain forest. Funct Ecol 26:1144–1152. doi:10.1111/j.1365-2435.2012.02019.x
Pérez-Ramos IM et al (2012) Evidence for a ‘plant community economics spectrum’ driven by nutrient and water limitations in a Mediterranean rangeland of southern France. J Ecol 100:1315–1327. doi:10.1111/1365-2745.12000
Poorter H, Lambers H, Evans JR (2014) Trait correlation networks: a whole-plant perspective on the recently criticized leaf economic spectrum. New Phytol 201:378–382. doi:10.1111/nph.12547
Quintero C, Bowers MD (2012) Changes in plant chemical defenses and nutritional quality as a function of ontogeny in Plantago lanceolata (Plantaginaceae). Oecologia 168:471–481. doi:10.1007/s00442-011-2114-x
Renteria LY, Jaramillo VJ (2011) Rainfall drives leaf traits and leaf nutrient resorption in a tropical dry forest in Mexico. Oecologia 165:201–211. doi:10.1007/s00442-010-1704-3
Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 3–54
Rhoades D, Cates R (1976) Toward a general theory of plant antiherbivore chemistry. In: Wallace J, Mansell R (eds) Biochemical interaction between plants and insects, vol 10. Springer, US, pp 168–213
Roslin T, Salminen JP (2008) Specialization pays off: contrasting effects of two types of tannins on oak specialist and generalist moth species. Oikos 117:1560–1568. doi:10.1111/j.0030-1299.2008.16725.x
Salminen JP, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338. doi:10.1111/j.1365-2435.2010.01826.x
Santiago LS, Kim SC (2009) Correlated evolution of leaf shape and physiology in the woody Sonchus alliance (Asteraceae: Sonchinae) in Macaronesia. Int J Plant Sci 170:83–92. doi:10.1086/593044
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Scriber JM (1977) Limiting effects of low leaf-water content on the nitrogen utilization, energy budget, and larval growth of Hyalophora cecropia (Lepidoptera: Saturniidae). Oecologia 28:269–287
Shimada T (2006) Salivary proteins as a defense against dietary tannins. J Chem Ecol 32:1149–1163. doi:10.1007/s10886-006-9077-0
Shipley B, Lechowicz MJ, Wright I, Reich PB (2006) Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology 87:535–541
Spalinger DE, Collins WB, Hanley TA, Cassara NE, Carnahan AM (2010) The impact of tannins on protein, dry matter, and energy digestion in moose (Alces alces). Can J Zool 88:977–987. doi:10.1139/z10-064
Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55
Timme RE, Simpson BB, Linder CR (2007) High-resolution phylogeny for Helianthus (Asteraceae) using the 18s-26s ribosomal DNA external transcribed spacer. Am J Bot 94:1837–1852
Tuomi J, Niemelä P, Stuart Chapin F III, Bryant J, Sirén S (1988) Defensive responses of trees in relation to their carbon/nutrient balance. In: Mattson W, Levieux J, Bernard-Dagan C (eds) Mechanisms of woody plant defenses against insects. Springer, New York, pp 57–72
Vasseur F, Violle C, Enquist BJ, Granier C, Vile D (2012) A common genetic basis to the origin of the leaf economics spectrum and metabolic scaling allometry. Ecol Lett 15:1149–1157. doi:10.1111/j.1461-0248.2012.01839.x
Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159. doi:10.1146/annurev.ecolsys.33.010802.150452
Westoby M, Reich PB, Wright IJ (2013) Understanding ecological variation across species: area-based vs mass-based expression of leaf traits. New Phytol 199:322–323. doi:10.1111/nph.12345
Wright IJ, Cannon K (2001) Relationships between leaf lifespan and structural defences in a low-nutrient, sclerophyll flora. Funct Ecol 15:351–359. doi:10.1046/j.1365-2435.2001.00522.x
Wright IJ et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827. doi:10.1038/nature02403
Wright IJ et al (2005) Modulation of leaf economic traits and trait relationships by climate. Global Ecol Biogeogr 14:411–421. doi:10.1111/j.1466-822x.2005.00172.x
Xiang S, Reich PB, Sun S, Atkin OK, Turnbull M (2013) Contrasting leaf trait scaling relationships in tropical and temperate wet forest species. Funct Ecol 27:522–534. doi:10.1111/1365-2435.12047
Acknowledgments
This work was supported by the National Science Foundation (grant no. 1122842 to L. A. D.). The authors thank Sarah McGaughey, Breanna Crowell, Karolina Heyduk, and Christina Graves for assistance with trait measurements and the Donovan Lab group for helpful comments on earlier versions of this manuscript.
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Communicated by Russell Monson.
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Mason, C.M., Donovan, L.A. Does investment in leaf defenses drive changes in leaf economic strategy? A focus on whole-plant ontogeny. Oecologia 177, 1053–1066 (2015). https://doi.org/10.1007/s00442-014-3177-2
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DOI: https://doi.org/10.1007/s00442-014-3177-2