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Protein storage and root:shoot reallocation provide tolerance to damage in a hybrid willow system

  • Physiological ecology - Original Paper
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Abstract

To determine the mechanistic basis of tolerance, we evaluated six candidate traits for tolerance to damage using F2 interspecific hybrids in a willow hybrid system. A distinction was made between reproductive tolerance and biomass tolerance; reproductive tolerance was designated as a plant’s proportional change in catkin production following damage, while biomass tolerance referred to a plant’s proportional change in biomass (i.e., regrowth) following damage. F2 hybrids were generated to increase variation and independence among candidate traits. Using three clonally identical individuals, pre-damage candidate traits for tolerance to damage (root:shoot ratio, total nonstructural carbohydrate, and total available protein) and post-damage candidate traits (relative root:shoot ratio, phenolic ratio, and specific leaf area ratio) were measured. The range of variation for these six candidate traits was broad. Biomass was significantly increased two years after 50% shoot length removal, and catkin production was not significantly reduced when damaged, suggesting that F2 hybrids had great biomass tolerance and reproductive tolerance. Based on multiple regression methods, increased reproductive tolerance was associated with increased protein storage and decreased relative root:shoot ratio (reduced root allocation after damage). In addition, a positive relationship between biomass tolerance and condensed tannins was detected, and both traits were associated with increased reproductive tolerance. These four factors explained 57% of the variance in the reproductive tolerance of F2 hybrids, but biomass tolerance explained the majority of the variance in reproductive tolerance. Changes in plant architecture in response to plant damage may be the underlying mechanism that explains biomass tolerance.

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References

  • Agrawal AA, Strauss SY, Stout MJ (1999) Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53:1093–1104

    Article  Google Scholar 

  • Appel HM, Govenor HL, D’Ascenzo M, Siska E, Schultz JC (2001) Limitations of Folin assays of foliar phenolics in ecological studies. J Chem Ecol 27:761–778

    Article  PubMed  CAS  Google Scholar 

  • Argus GW (1986) The genus Salix (Salicaceae) in the southeastern United States. Syst Bot Monogr 9:1–170

    Article  Google Scholar 

  • Babst BA, Ferrieri RA, Thorpe MR, Orians CM (2005) Lymantria dispar herbivory induces rapid changes in carbon transport and partitioning in Populus nigra. Entomol Exp Appl 128:117–125

    Article  Google Scholar 

  • Belsky AJ, Carson WP, Jensen CL, Fox GA (1993) Overcompensation by plants: herbivore optimiation or red herring? Evol Ecol 7:109–121

    Article  Google Scholar 

  • Biere A (1996) Intra-specific variation in relative growth rate: impact on competitive ability and performance of Lychnis flos-cuculi in habitats differing in soil fertility. Plant and Soil 182:313–327

    Google Scholar 

  • Boege K, Dirzo R, Siemens D, Brown P (2007) Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? Ecol Lett 10:177–187

    Article  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive for the quantitation of microgram quantitites of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Broberg CL, Borden JH, Humble LM (2002) Distribution and abundance of Cryptorhynchus lapathi on Salix spp. in British Columbia. Can J For Res 32:561–568

    Article  Google Scholar 

  • Chapin FS III, McKendrick JD, Johnson DA (1986) Seasonal changes in carbon fractions in Alaskan tundra plants of differing growth form: implications for herbivory. J Ecol 74:707–731

    Article  CAS  Google Scholar 

  • Crawley MJ (1985) Reduction of oak fecundity by low-density herbivore populations. Nature 314:163–164

    Google Scholar 

  • Danell K, Bergstrom R, Edenius L (1994) Effects of large mammalian browsers on architecture, biomass, and nutrients of woody plants. J Mammal 75:833–844

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Eyles A, Pinkard EA, Mohammed C (2009) Shifts in biomass and resource allocation patterns following defoliation in Eucalyptus globulus growing with varying water and nutrient supplies. Tree Phys 29:753–764

    Article  CAS  Google Scholar 

  • Faber M (2002) Soil survey of Dutchess County. US Department of Agriculture, Natural Resources Conservation Service, Millbrook

  • Fineblum WL, Rausher MD (1995) Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377:517–520

    Article  CAS  Google Scholar 

  • Fornoni J (2011) Ecological and evolutionary implications of plant tolerance to herbivory. Funct Ecol 25:399–407

    Article  Google Scholar 

  • Fornoni J, Valverde PL, Núñez-Farfán J (2003) Quantitative genetics of plant tolerance and resistance against natural enemies of two natural populations of Datura stramonium. Evol Ecol Res 5:1049–1065

    Google Scholar 

  • Fornoni J, Núñez-Farfán J, Valverde PL, Rausher MD (2004) Evolution of mixed strategies of plant defense allocation against natural enemies. Evolution 58:1685–1695

    PubMed  Google Scholar 

  • Fritz RS, Simms EL (eds) (1992) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. The University of Chicago Press, Chicago

  • 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

    Article  Google Scholar 

  • Fritz RS, Hochwender CG, Brunsfeld SJ, Roche BM (2003) Genetic architecture of susceptibility to herbivores in hybrid willows. J Evol Biol 16:1115–1126

    Article  PubMed  CAS  Google Scholar 

  • Fritz RS, Hochwender CG, Albrectsen BR, Czesak ME (2006) Fitness and genetic architecture of parent and hybrid willows in common gardens. Evolution 60:1215–1227

    PubMed  Google Scholar 

  • Hardig TM, Brunsfeld SJ, Fritz RS, Morgan M, Orians CM (2000) Morphological and molecular evidence for hybridization and introgression in a willow (Salix) hybrid zone. Mol Ecol 9:9–24

    Article  PubMed  CAS  Google Scholar 

  • Harms KE, Dalling JW (1997) Damage and herbivory tolerance through resprouting as an advantage of large seed size in tropical trees and lianas. J Trop Ecol 13:617–621

    Article  Google Scholar 

  • Haukioja E, Koricheva J (2000) Tolerance to herbivory in woody versus herbaceous plants. Evol Ecol 14:551–562

    Article  Google Scholar 

  • Hendrix SD (1979) Compensatory reproduction in a biennial herb following insect defloration. Oecologia 42:107–118

    Google Scholar 

  • Hjältén J, Price PW (1996) The effect of pruning on willow growth and sawfly population densities. Oikos 77:549–555

    Article  Google Scholar 

  • Hochwender CG, Fritz RS, Orians CM (2000a) Using hybrid systems to explore the evolution of tolerance to damage. Evol Ecol 14:521–590

    Article  Google Scholar 

  • Hochwender CG, Marquis RJ, Stowe KA (2000b) The potential for and constraints on the evolution of compensatory ability in Asclepias syriaca. Oecologia 122:361–370

    Article  Google Scholar 

  • Hochwender CG, Sork VL, Marquis RJ (2003) Fitness consequences of herbivory on Quercus alba. Am Midl Nat 150:246–253

    Article  Google Scholar 

  • Hochwender CG, Janson EM, Cha DH, Fritz RS (2005) Community structure of insect herbivores in a hybrid system: examining the effects of browsing damage and plant genetic variation. Ecol Ent 30:170–175

    Article  Google Scholar 

  • Hódar JA, Zamora R, Castro J, Gómez JM, Garcia D (2008) Biomass allocation and growth responses of Scots pine saplings to simulated herbivory depend on plant age and light availability. Plant Ecol 197:229–238

    Article  Google Scholar 

  • Houle G, Simard G (1996) Additive effects of genotype, nutrient availability and type of tissue damage on the compensatory response of Salix planifolia ssp planifolia to simulated herbivory. Oecologia 107:373–378

    Article  Google Scholar 

  • Jones CG, Hare JD, Compton SJ (1989) Measuring plant protein with the Bradford assay: evaluation and a standard method. J Chem Ecol 15:979–992

    Article  CAS  Google Scholar 

  • Juenger T, Bergelson J (2000) The evolution of compensation to herbivory in scarlet gilia, Ipomopsis aggregata: herbivore-imposed natural selection and the quantitative genetics of tolerance. Evolution 54:764–777

    PubMed  CAS  Google Scholar 

  • Kaitaniemi P, Neuvonen S, Nyyssönen T (1999) Effects of cumulative defoliations on growth, reproduction, and insect resistance in mountain birch. Ecology 80:524–532

    Article  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, Chicago

    Google Scholar 

  • Katjiua MJL, Ward D (2006) Resistance and tolerance of Terminalia sericea trees to simulated herbivore damage under different soil nutrient and moisture conditions. J Chem Ecol 32:1431–1443

    Article  PubMed  CAS  Google Scholar 

  • Lambers H, Poorter H (1992) Inherent variation in growth-rate between higher-plants: a search for physiological causes and ecological consequences. Adv Ecol Res 23:187–261

    Article  CAS  Google Scholar 

  • Lennartsson T, Nilsson P, Tuomi J (1998) Induction of overcompensation in the field gentian, Gentianella campestris. Ecology 79:1061–1072

    Google Scholar 

  • Marquis RJ (1984) Leaf herbivores decrease fitness of a tropical plant. Science 226:537–539

    Article  PubMed  CAS  Google Scholar 

  • Marquis RJ (1996) Plant architecture, sectoriality and plant tolerance to herbivores. Vegetatio 127:85–97

    Article  Google Scholar 

  • Marquis RJ, Newell EA, Villegas AC (1997) Non-structural carbohydrate accumulation and use in an understorey rain-forest shrub and relevance for the impact of leaf herbivory. Funct Ecol 11:636–643

    Article  Google Scholar 

  • Maschinski J, Whitham TG (1989) The continuum of plant responses to herbivory: the influence of plant association, nutrient availability, and timing. Am Nat 134:1–19

    Article  Google Scholar 

  • Mauricio R, Rausher MD, Burdick DS (1997) Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78:1301–1311

    Article  Google Scholar 

  • Mosseler A (1990) Hybrid performance and species crossability relationships in willows (Salix). Can J Botany 68:2329–2338

    Google Scholar 

  • Murtaugh PA (2009) Performance of several variable-selection methods applied to real ecological data. Ecol Lett 12:1061–1068

    Article  PubMed  Google Scholar 

  • Myers JA, Kitajima K (2007) Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. J Ecol 95:383–395

    Article  CAS  Google Scholar 

  • Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153:375–380

    CAS  Google Scholar 

  • Nichols-Orians CM, Fritz RS, Clausen TP (1993) The genetic basis for variation in the concentration of phenolic glycosides in Salix sericea: clonal variation and sex-based differences. Biochem Syst Ecol 21:535–542

    Article  CAS  Google Scholar 

  • Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Syst 38:541–566

    Article  Google Scholar 

  • Ogren E (1999) Fall frost resistance in willows used for biomass production. I. Characterization of seasonal and genetic variation. Tree Phys 19:749–754

    Article  Google Scholar 

  • Orians CM, Griffiths ME, Roche BM, Fritz RS (2000) Phenolic glycosides and condensed tannins in Salix sericea, S. eriocephala and their F1 hybrids: not all hybrids are created equal. Biochem Syst Ecol 28:619–632

    Article  PubMed  CAS  Google Scholar 

  • Paige KN, Whitham TG (1987) Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am Nat 129:407–416

    Article  Google Scholar 

  • Pilson D, Decker KL (2002) Compensation for herbivory in wild sunflower: response to simulated damage by the head-clipping weevil. Ecology 83:3097–3107

    Article  Google Scholar 

  • Pratt PD, Rayamajhi MB, Van TK, Center TD, Tipping PW (2005) Herbivory alters resource allocation and compensation in the invasive tree Melaleuca quinquenervia. Ecol Ent 30:316–326

    Article  Google Scholar 

  • Rogers WE, Siemann E (2002) Effects of simulated herbivory and resource availability on native and invasive exotic tree seedlings. Basic Appl Ecol 3:297–307

    Article  Google Scholar 

  • Roininen H, Price PW, Bryant JP (1997) Response of galling insects to natural browsing by mammals in Alaska. Oikos 80:481–486

    Article  Google Scholar 

  • Rosenthal GA, Berenbaum MR (eds) (1992) Herbivores: their interactions with secondary plant metabolites, vol II: evolutionary and ecological processes. Academic, New York

  • Rosenthal JP, Welter SC (1995) Tolerance to herbivory by a stemboring caterpillar in architecturally distinct maizes and wild relatives. Oecologia 102:146–155

    Article  Google Scholar 

  • Roy BA, Kirchner JW (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51–63

    PubMed  CAS  Google Scholar 

  • Ryser P, Lambers H (1995) Root and leaf attributes accounting for the performance of fast-growing and slow-growing grasses at different nutrient supply. Plant Soil 170:251–265

    Article  CAS  Google Scholar 

  • SAS Institute (2001) JMP statistics and graphics guide, version 4. SAS Institute, Cary

  • Schierenbeck KA, Mack RN, Sharitz RR (1994) Effects of herbivory on growth and biomass allocation in native and introduced species of Lonicera. Ecology 75:1661–1672

    Article  Google Scholar 

  • Siemens DH, Lischke H, Maggiulli N, Schürch S, Roy BA (2003) Cost of resistance and tolerance under competition: the defense-stress benefit hypothesis. Evol Ecol 17:247–263

    Article  Google Scholar 

  • Simms EL, Triplett J (1994) Costs and benefits of plant responses to disease: resistance and tolerance. Evolution 48:1973–1985

    Article  Google Scholar 

  • Somogyi M (1952) Notes on sugar determination. J Biol Chem 195:19–23

    CAS  Google Scholar 

  • Stevens MT, Waller DM, Lindroth RL (2007) Resistance and tolerance in Populus tremuloides: genetic variation, costs, and environmental dependency. Evol Ecol 21:829–847

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Annu Rev Ecol Syst 31:565–595

    Article  Google Scholar 

  • Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185

    Article  PubMed  Google Scholar 

  • Tiffin P (2000) Mechanisms of tolerance to herbivore damage: what do we know? Evol Ecol 14:523–536

    Article  Google Scholar 

  • Tilmon KJ (ed) (2008) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley

  • van der Meijden E, Wijn M, Verkaar HJ (1988) Defense and regrowth: alternative plant strategies in the struggle against herbivores. Oikos 51:355–363

    Article  Google Scholar 

  • van der Meijden E, Boer NJ, van der Veen-van Wijk CAM (2000) Pattern of storage and regrowth in ragwort. Evol Ecol 14:457–489

    Article  Google Scholar 

  • Vandenberghe C, Freléchoux F, Buttler A (2008) The influence of competition from herbaceous vegetation and shade on simulated browsing tolerance of coniferous and deciduous saplings. Oikos 117:415–423

    Article  Google Scholar 

  • Weinig C, Stinchcombe JR, Schmitt J (2003) Evolutionary genetics of resistance and tolerance to natural herbivory in Arabadopsis thaliana. Evolution 57:1270–1280

    PubMed  Google Scholar 

  • Wise MJ, Abrahamson WG (2005) Beyond the compensatory continuum: environmental resource levels and plant tolerance of herbivory. Oikos 109:417–428

    Article  Google Scholar 

  • Wise MJ, Abrahamson WG (2008) Applying the limiting resource model to plant tolerance of apical meristem damage. Am Nat 172:635–647

    Article  PubMed  Google Scholar 

  • Wise MJ, Carr DE (2008) On quantifying tolerance of herbivory for comparative analyses. Evolution 62:2429–2434

    Article  PubMed  Google Scholar 

  • Wright IJ, Westoby M (1999) Differences in seedling growth behaviour among species: trait correlations across species, and trait shifts along nutrient compared to rainfall behavior. J Ecol 87:85-97

    Google Scholar 

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Acknowledgments

This work has been supported by NSF Grants DEB 01-27369 to CGH and DEB 99-81406 to RSF. We thank the Sosnowskis and M. Membrino, who have permitted us to conduct research on their property. We received logistical support from the Biology Department at Hartwick College. We thank the following people for help with field work: S.D. Bodach, R.D. Fritz, R.G. Gale, S. Irwin, M.J. Knee, J. Mann, B. Mock, B. Murray, M. Rasher, N. Rice, E. Sedgwick, and L. Spiller. We thank B. Mock and J. Rudolph for help with grinding the root and shoot samples. We give special thanks to C.M. Orians for guidance with phenolic glycoside analyses and for chemical standards. We thank anonymous reviewers for comments on earlier drafts of this manuscript.

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  1. Dong H. Cha

    Present address: Yakima Agricultural Research Laboratory, USDA-ARS, 5230 Konnowac Pass Road, Wapato, WA, 98951, USA

Authors and Affiliations

  1. Department of Biology, University of Evansville, Evansville, IN, 47722, USA

    Cris G. Hochwender & Dong H. Cha

  2. Department of Biology, Vassar College, Poughkeepsie, NY, 12604, USA

    Mary Ellen Czesak & Robert S. Fritz

  3. Department of Chemistry, University of Evansville, Evansville, IN, 47722, USA

    Arlen D. Kaufman, Brandi Warren & Ashley Neuman

  4. Department of Entomology, Cornell University, Ithaca, NY, 14853, USA

    Rebecca R. Smyth

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  1. Cris G. Hochwender
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Correspondence to Cris G. Hochwender.

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Communicated by Colin Orians.

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Hochwender, C.G., Cha, D.H., Czesak, M.E. et al. Protein storage and root:shoot reallocation provide tolerance to damage in a hybrid willow system. Oecologia 169, 49–60 (2012). https://doi.org/10.1007/s00442-011-2176-9

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