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To compete or defend: linking functional trait variation with life-history tradeoffs in a foundation tree species

Abstract

Although chemical deterrents to herbivory often exact costs in terms of plant growth, the manner in which those costs arise, and their physiological relationship to other functional traits, remain unclear. In the absence of appreciable herbivory, we examined interrelationships among chemical defense levels and other foliar functional traits (e.g., light-saturated photosynthesis, specific leaf area, nitrogen concentration) as co-determinants of tree growth and, by extension, competitive ability in high-density populations comprising 16 genotypes of Populus tremuloides. Across genotypes, concentrations of chemical defenses were not significantly related to other leaf functional traits, but levels of the salicinoid phenolic glycosides (SPGs) salicin, salicortin and tremulacin were each negatively correlated with relative mass growth (RMG) of aboveground woody tissue (P ≤ 0.001). RMG, in turn, underpinned 77% of the genotypic variation in relative height growth (our index of competitive ability). RMG was also positively related to light-saturated photosynthesis (P ≤ 0.001), which, together with the three SPGs, explained 86% of genotypic RMG variation (P ≤ 0.001). Moreover, results of a carbon balance simulation indicated that costs of resource allocation to SPGs, reaching nearly a third of annual crown photosynthesis, were likely mediated by substantial metabolic turnover, particularly for salicin. The lack of discernible links between foliar defense allocation and other (measured) functional traits, and the illustrated potential of metabolic turnover to reconcile influences of SPG allocation on RMG, shed additional light on fundamental physiological mechanisms underlying evolutionary tradeoffs between chemical defense investment and competitive ability in a foundation tree species.

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References

  1. Aarssen LW (1995) Hypothesis for the evolution of apical dominance in plants: implications for the interpretation of overcompensation. Oikos 74:149–156

  2. Agrawal AA (2011) Current trends in the evolutionary ecology of plant defense. Funct Ecol 25:420–432

  3. AWON. UW-Madison Automated Weather Observing Network. University of Wisconsin Extension, https://agwx.soils.wisc.edu/uwex_agwx/awon. Accessed March 15, 2015

  4. Babst BA, Harding SA, Tsai C (2010) Biosynthesis of phenolic glycosides from phenylpropanoid and benzenoid presursors in Populus. J Chem Ecol 36:286–297

  5. Ballhorn DJ, Godschalx AL, Smart SM, Kautz S, Schadler M (2014) Chemical defense lowers plant competitiveness. Oecologia 176:811–824

  6. Boeckler GA, Gershenzon J, Unsicker SB (2011) Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochem 72:1497–1509

  7. Bond-Lamberty B, Wang C, Gower ST (2002) Aboveground and belowground biomass and sapwood area allometric equations for six boreal tree species of northern Manitoba. Can J For Res 32:1441–1450

  8. Campos ML, Yoshida Y, Major IT, Ferreira D, Weraduwage SM, Froehlich JE et al (2016) Rewiring of jasmonate and phytochrome B signaling uncouples plant growth-defense tradeoffs. Nat Commun 7:12570. https://doi.org/10.1038/ncomms12570

  9. Cipollini D, Lieurance DM (2012) Expression and costs of induced defense traits in Allaria petiolata, a widespread invasive plant. Basic Appl Ecol 13:432–440

  10. Cipollini D, Walters D, Voelckel C (2014) Costs of resistance in plants: from theory to evidence. Ann Plant Rev 47:263–308

  11. Cole CT (2005) Allelic and population variation of microsatellite loci in aspen (Populus tremuloides). New Phytol 167:155–164

  12. Cole CT, Stevens MT, Anderson JE, Lindroth RL (2016) Heterozygosity, gender, and the growth-defense trade-off in quaking aspen. Oecologia 181:381–390

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

  14. 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. https://doi.org/10.1111/1365-2435.13425

  15. Dillaway DN, Kruger EL (2011) Leaf respiratory acclimation to climate: comparisons among boreal and temperate tree species along a latitudinal transect. Tree Physiol 31:1114–1127

  16. Dillaway DN, Kruger EL (2014) Trends in seedling growth and carbon-use efficiency differ among tree species along a latitudinal transect. Glob Change Biol 20:908–922

  17. Donaldson JR, Lindroth RL (2007) Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen. Ecology 88:729–739

  18. Donaldson JR, Kruger EL, Lindroth RL (2006a) Competition- and resource-mediated tradeoffs between growth and defensive chemistry in trembling aspen (Populus tremuloides). New Phytol 169:561–570

  19. Donaldson JR, Stevens MT, Barnhill HR, Lindroth RL (2006b) Age-related shifts in leaf chemistry of clonal aspen (Populus tremuloides). J Chem Ecol 32:1415–1429

  20. Fagerstrom T (1989) Anti-herbivory chemical defense in plants: a note on the concept of cost. Am Nat 133:281–287

  21. Feng Y, Leia Y, Wanga R, Callaway RM, Valiente-Banuet A, Inderjit LY, Zheng Y (2009) Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. Proc Natl Acad Sci 106:1853–1856

  22. Gershenzon J (1994) Metabolic costs of terpenoid accumulation in higher-plants. J Chem Ecol 20:1281–1328

  23. Goodger JQD, Gleadow RM (2006) Growth cost and ontogenetic expression patterns of defense in cyanogenic Eucalyptus spp. Trees 20:757–765

  24. Haikio E, Makkonen M, Julkenen-Tiitto J, Sitte J, Freiwald T, Pandey V et al (2009) Performance and secondary chemistry of two hybrid aspen (Populus tremula L. × Populus tremuloides Michx.) clones in long-term elevated ozone exposure. J Chem Ecol 35:664–678

  25. Hanson P, McRoberts R, Isebrands JG, Dixon R (1987) An optimal sampling strategy for determining CO2 exchange rate as a function of photosynthetic photon flux density. Photosynthetica 21:98–101

  26. Harding SA, Jarvie MM, Lindroth RL, Tsai C (2009) A comparative analysis of phenylpropanoid metabolism, N utilization, and carbon partitioning in fast- and slow-growing Populus hybrid clones. J Exp Bot 60:3443–3452

  27. Hemming JD, Lindroth RL (1999) Effects of light and nutrient availability on aspen: growth, phytochemistry, and insect performance. J Chem Ecol 25:1687–1714

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

  29. Holeski LM, McKenzie SC, Kruger EL, Couture JJ, Rubert-Nason K, Lindroth RL (2016) Phytochemical traits underlie genotypic variation in susceptibility of quaking aspen (Populus tremuloides) to browsing by a keystone forest ungulate. J Ecol 104:850–863. https://doi.org/10.1111/1365-2745.12559

  30. Kaakinen S, Kostiainen K, Ek F et al (2004) Stem wood properties of Populus tremuloides, Betula papyrifera and Acer saccharum saplings after 3 years of treatments to elevated carbon dioxide and ozone. Glob Change Biol 10:1513–1525

  31. Kaelke CM, Kruger EL, Reich PB (2001) Trade-offs in seedling survival, growth, and physiology among hardwood species of contrasting successional status along a light-availability gradient. Can J For Res 31:1602–1616

  32. Keefover-Ring K, Rubert-Nason KF, Bennett AE, Lindroth RL (2015) Growth and chemical responses of trembling aspen to simulated browsing and ungulate saliva. J Plant Ecol 9:474–484

  33. Kempel A, Schadler M, Chrobock T, Fischer M, van Kleunen M (2011) Tradeoffs associated with constitutive and induced plant resistance against herbivory. Proc Nat Acad Sci 108(14):5685–5689

  34. Kleiner KW, Raffa KF, Dickson RE (1999) Partitioning of 14C-labeled photosynthate to allelochemicals and primary metabolites in source and sink leaves of aspen: evidence for secondary metabolite turnover. Oecologia 119:408–418

  35. Koricheva J (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83:176–190

  36. Kruger EL, Volin JC (2006) Reexamining the empirical relation between plant growth and leaf photosynthesis. Funct Plant Biol 33:421–429

  37. Lewis JD, Olszyk D, Tingey DT (1999) Seasonal patterns of photosynthetic light response in Douglas-fir seedlings subjected to elevated atmospheric CO2 and temperature. Tree Physiol 19:243–252

  38. Lindroth RL, St. Clair SB (2013) Adaptations of quaking aspen (Populus tremuloides Michx.) for defense against herbivores. For Ecol Manag 299:14–21

  39. Madritch MD, Greene SG, Lindroth RL (2009) Genetic mosaics of ecosystem functioning across aspen-dominated landscapes. Oecologia 160:119–127

  40. Massad TJ, Dyer LA, Vega GC (2012) Costs of defense and a test of the carbon-nutrient balance and growth-differentiation balance hypotheses for two co-occurring classes of plant defense. PLoS ONE 7:e47554. https://doi.org/10.1371/journal.pone.0047554

  41. Massad TJ, Trumbore SE, Ganbat G, Reichelt M, Unsicker S, Boeckler A et al (2014) An optimal defense strategy for phenolic glycoside production in Populus trichocarpa—isotope labeling demonstrates secondary metabolite production in growing leaves. New Phytol 203:607–619

  42. Matsuki S, Koike T (2006) Comparison of leaf life span, photosynthesis and defensive traits across seven species of deciduous broad-leaf tree seedlings. Ann Bot 97:813–817

  43. Medhurst JL, Beadle CL (2005) Photosynthetic capacity and foliar nitrogen distribution in Eucalyptus nitens is altered by high-intensity thinning. Tree Physiol 25:981–991

  44. Mooney HA, Gulmon SL (1982) Constraints on leaf structure and function in reference to herbivory. Bioscience 32:198–206

  45. Moreira X, Zas R, Solla A, Sampedro L (2015) Differentiation of persistent anatomical defensive structures is costly and determined by nutrient availability and genetic growth-defense constraints. Tree Physiol 35:112–123

  46. Neilson EH, Goodger JQD, Woodrow IE, Moller BL (2013) Plant chemical defense: at what cost? Trends Plant Sci 18:250–258

  47. Noitsakis B, Jacquard P (1992) Competition between cyanogenic and acyanogenic morphs of Trifolium repens. Theor Appl Gen 83:443–450

  48. Osier TL, Lindroth RL (2006) Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia 148:293–303

  49. Osier TL, Hwang SY, Lindroth RL (2000) Within- and between-year variation in early season phytochemistry of quaking aspen (Populus tremuloides Michx.) clones. Biochem System Ecol 28:197–208

  50. Palo TR (1984) Distribution of birch (Betula spp.), willow (Salix spp.) and poplar (Populus spp.) secondary metabolites and their potential role as chemical defense against herbivores. J Chem Ecol 10:499–519

  51. Poorter H (1994) Construction costs and payback time of biomass: A whole plant perspective. In: Roy J, Garnier E (eds) A whole plant perspective of carbon–nitrogen interactions. SPB Academic Publishing, The Hague, pp 111–127

  52. Porter LJ, Hrstich LN, Chan BG (1985) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230

  53. Price PW, Waring GL, Julkunen-Tiitto R, Tahvanainen J, Mooney HA, Craig TP (1989) Carbon-nutrient balance hypothesis in within-species phytochemical variation of Salix lasiolepsis. J Chem Ecol 15:1117–1131

  54. Reichardt PB, Chapin FS, Bryant JP (1991) Carbon/nutrient balance as a predictor of plant defense in Alaskan balsam poplar: potential importance of metabolite turnover. Oecologia 88:401–406

  55. Ridenour WM, Vivanco JM, Feng YL, Horiuchi J, Callaway RM (2008) No evidence for trade-offs: centaurea plants from America are better competitors and defenders. Ecol Monogr 78:369–386

  56. Romme WH, Turner MG, Wallace LL (1995) Aspen, elk, and fire in northern Yellowstone National Park. Ecology 76:2097–2106

  57. Rubert-Nason KF, Couture JJ, Major IT, Constabel CP, Lindroth RL (2015) Influence of genotype, environment, and gypsy moth herbivory on local and systemic chemical defenses in trembling aspen (Populus tremuloides). J Chem Ecol 41:651–661

  58. Rubert-Nason KF, Keefover-Ring K, Lindroth RL (2018) Purification and analysis of salicinoids. Curr Anal Chem 14:424–429. https://doi.org/10.2174/1573411014666171221131933

  59. Ruuhola TM, Julkunen-Tiitto MRK (2000) Salicylates of intact Salix myrsinifolia plantlets do not undergo rapid metabolic turnover. Plant Physiol 122:895–905

  60. Sampedro L, Moreira X, Zas R (2011) Costs of constitutive and herbivore-induced chemical defenses in pine trees emerge only under low nutrient availability. J Ecol 99:818–827

  61. Scheurwater I, Dunnebacke M, Eising R, Lambers H (2000) Respiratory costs and rate of protein turnover in the roots of a fast-growing (Dactylis glomerata L.) and a slow-growing (Festuca ovina L.) grass species. J Exp Bot 51:1089–1097

  62. Schippers P, Vlam M, Zuidema PA, Sterck F (2015) Sapwood allocation in tropical trees: a test of hypotheses. Funct Plant Biol 42:697–709

  63. Simms EL, Rausher MD (1989) The evolution of resistance to herbivory in Ipomoea purpurea. II. Natural selection by insects and costs of resistance. Evolution 43:573–585

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

  65. Stevens MT, Kruger EL, Lindroth RL (2008) Variation in tolerance to herbivory is mediated by differences in biomass allocation in aspen. Funct Ecol 22:40–47

  66. Sumbele S, Fotelli MN, Nikolopuous D, Tooulakou G, Liakoura V, Liakopoulos G et al (2012) Photosynthetic capacity is negatively correlated with the concentration of leaf phenolic compounds across a range of different species. AoB Plants. https://doi.org/10.1093/aobpla/pls025

  67. Tullus A, Tullus H, Soo T, Parn L (2009) Above-ground biomass characteristics of young hybrid aspen (Populus tremula L. × P. tremuloides Michx.) plantations on former agricultural land in Estonia. Biomass Bioenergy 33:1617–1625

  68. Viola DV, Mordecai EA, Jaramillo AG, Sistla SA, Albertson LK, Gosnell JS et al (2010) Competition–defense tradeoffs and the maintenance of plant diversity. Proc Natl Acad Sci 107:17217–17222

  69. Volin JC, Kruger EL, Lindroth RL (2002) Responses of deciduous broadleaf trees to defoliation in a CO2 enriched atmosphere. Tree Physiol 22:435–448

  70. Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

  71. Zangerl AR, Arntz MA, Berenbaum MR (1997) Physiological price of an induced chemical defense: photosynthesis, respiration, biosynthesis, and growth. Oecologia 109:433–441

  72. Zavala JA, Patankar AG, Gase K, Baldwin IT (2004) Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. Proc Nat Acad Sci 101(6):1607–1612

  73. Zufferey V, Murisier F, Schultz HR (2000) A model analysis of the photosynthetic response of Vitis vinifera L. cvs Riesling and Chasselas leaves in the field: I. Interaction of age, light and temperature. Vitis 39:19–26

  74. Züst T, Agrawal AA (2017) Trade-offs between plant growth and defense against insect herbivory. Ann Rev Plant Biol 68:513–534

  75. 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

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Acknowledgements

Financial support for this study was provided by the National Science Foundation (grants DEB-0841609 and DEB-1456592) and the USDA McIntire-Stennis Program (grant WIS01842). We are grateful for the invaluable technical assistance provided by Andrew Helm, Kennedy Rubert-Nason, and Daniel Reeves.

Author information

RLL and ELK secured funding, and, with KKR, designed the study. LMH and KKR initiated and maintained the study. ELK, LMH and KKR collected and processed data. ELK conducted data analyses and simulations. ELK generated the first manuscript draft, and all authors contributed substantially to revisions.

Correspondence to Eric L. Kruger.

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The authors declare that they have no conflict of interest.

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Communicated by Fernando Valladares.

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Kruger, E.L., Keefover-Ring, K., Holeski, L.M. et al. To compete or defend: linking functional trait variation with life-history tradeoffs in a foundation tree species. Oecologia (2020). https://doi.org/10.1007/s00442-020-04622-y

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Keywords

  • Competition
  • Functional traits
  • Growth
  • Salicinoid phenolic glycosides
  • Photosynthesis