Biological Invasions

, Volume 21, Issue 4, pp 1269–1281 | Cite as

Plant defense against generalist herbivores in the forest understory: a phylogenetic comparison of native and invasive species

  • Elise D. HinmanEmail author
  • Jason D. Fridley
  • Dylan Parry
Original Paper


Invasive woody plants from Europe and Asia tend to be more productive than co-occurring native species in deciduous forests of Eastern North America, but community-scale drivers of invasion success remain unknown. If increased productivity in invaders relative to natives comes at the expense of reduced relative allocation to defenses, generalist herbivores may preferentially consume invasive species, potentially reducing the effectiveness of invader growth advantage. We compared leaf traits related to herbivory (nitrogen concentration, total phenolics, cellulose and lignin concentrations, and leaf dry matter content) in 20 phylogenetically paired native and non-native, invasive species and evaluated species palatability to two generalist herbivores: one non-native (European gypsy moth, Lymantria dispar) and one native (fall webworm, Hyphantria cunia). We also evaluated potential physiological tradeoffs between defense-related leaf traits, leaf production, and carbon storage in this group of species. Invasive plants had higher leaf N and lignin concentrations than related native species (0.5% and 5%, respectively), but gypsy moth and fall webworm growth were not associated with plant nativity. Plant defense traits did not predict differences in gypsy moth growth, but fall webworm growth was marginally negatively associated with leaf N. We found no evidence of tradeoffs between defense-related leaf traits, leaf production, and carbon storage, indicating a limited role for carbon-based tradeoffs relating to growth and herbivory in these species, although other unmeasured carbon pools including reproduction may impact these relationships. Woody invaders continue to spread in Eastern North American forest understories, but we found no evidence of inhibition or facilitation by generalist insect herbivores, despite differences among species in leaf traits associated with defense.


Defense Generalists Herbivory Palatability Tradeoff Traits 



We thank A. Craddock and V. Hull for field assistance and S. Goetz, V. Hull, and T. Schlossnagle for feeding trial assistance. We thank N. Podpora, K. Martinez, and L. Woolhiser for lab assistance. We also thank D. Frank, D. Leopold, and M. Ritchie for contributions to the theoretical framework of this paper, and K. Martinez for manuscript comments. This work was supported by a United States National Science Foundation Doctoral Dissertation Improvement Grant (04293) to E. Hinman.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10530_2018_1898_MOESM1_ESM.docx (620 kb)
Supplementary material 1 (DOCX 620 kb)


  1. Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6:712–715CrossRefGoogle Scholar
  2. Agrawal AA, Weber MG (2015) On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds. Ecol Lett 18(10):985–991CrossRefGoogle Scholar
  3. Agrawal AA, Kotanen PM, Mitchell CE, Power AG, Godsoe W, Klironomos J (2005) Enemy release? An experiment with congeneric plant pairs and diverse above-and belowground enemies. Ecology 86(11):2979–2989CrossRefGoogle Scholar
  4. Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. Nat Protoc 2(4):875CrossRefGoogle Scholar
  5. Ashton IW, Lerdau MT (2008) Tolerance to herbivory, and not resistance, may explain differential success of invasive, naturalized, and native North American temperate vines. Divers Distrib 14(2):169–178CrossRefGoogle Scholar
  6. Ayres MP, Lombardero MJ (2000) Assessing the consequences of global change for forest disturbance from herbivores and pathogens. Sci Total Environ 262(3):263–286CrossRefGoogle Scholar
  7. Barbosa P, Krischik VA (1987) Influence of alkaloids on feeding preference of eastern deciduous forest trees by the gypsy moth Lymantria dispar. Am Nat 130(1):53–69CrossRefGoogle Scholar
  8. Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37(1):58–67CrossRefGoogle Scholar
  9. Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83(5):887–889CrossRefGoogle Scholar
  10. Blumenthal DM (2006) Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9(7):887–895CrossRefGoogle Scholar
  11. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2(8):436–443CrossRefGoogle Scholar
  12. Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Lett 1(4):435–438CrossRefGoogle Scholar
  13. Carmona D, Fornoni J (2013) Herbivores can select for mixed defensive strategies in plants. New Phytol 197(2):576–585CrossRefGoogle Scholar
  14. Chapin FS III, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21(1):423–447CrossRefGoogle Scholar
  15. Cincotta CL, Adams JM, Holzapfel C (2009) Testing the enemy release hypothesis: a comparison of foliar insect herbivory of the exotic Norway maple (Acer platanoides L.) and the native sugar maple (A. saccharum L.). Biol Invasions 11(2):379–388CrossRefGoogle Scholar
  16. Coley PD (1988) Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74(4):531–536CrossRefGoogle Scholar
  17. Davis MA (2009) Invasion biology. Oxford University Press, OxfordGoogle Scholar
  18. Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65:667–687CrossRefGoogle Scholar
  19. Doorduin LJ, Vrieling K (2011) A review of the phytochemical support for the shifting defence hypothesis. Phytochem Rev 10(1):99–106CrossRefGoogle Scholar
  20. Dostál P, Allan E, Dawson W, Kleunen M, Bartish I, Fischer M (2013) Enemy damage of exotic plant species is similar to that of natives and increases with productivity. J Ecol 101(2):388–399CrossRefGoogle Scholar
  21. Dudt JF, Shure DJ (1994) The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology 75(1):86–98CrossRefGoogle Scholar
  22. Elkinton JS, Liebhold AM (1990) Population dynamics of gypsy moth in North America. Annu Rev Entomol 35(1):571–596CrossRefGoogle Scholar
  23. Elton CS (1958) The ecology of invasions by animals and plants. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  24. Endara MJ, Coley PD (2011) The resource availability hypothesis revisited: a meta-analysis. Funct Ecol 25(2):389–398CrossRefGoogle Scholar
  25. Eschtruth AK, Battles JJ (2009) Acceleration of exotic plant invasion in a forested ecosystem by a generalist herbivore. Conserv Biol 23(2):388–399CrossRefGoogle Scholar
  26. Feng YL, Lei YB, Wang RF, Callaway RM, Valiente-Banuet A, Li YP, Zheng YL (2009) Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. Proc Natl Acad Sci 106(6):1853–1856CrossRefGoogle Scholar
  27. Fine PV, Miller ZJ, Mesones I, Irazuzta S, Appel HM, Stevens MHH, Sääksjärvi I, Schultz JC, Coley PD (2006) The growth–defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87(7):S150–S162CrossRefGoogle Scholar
  28. Fraser LH, Grime JP (1999) Interacting effects of herbivory and fertility on a synthesized plant community. J Ecol 87(3):514–525CrossRefGoogle Scholar
  29. Fridley JD (2008) Of Asian forests and European fields: eastern US plant invasions in a global floristic context. PLoS ONE 3(11):e3630CrossRefGoogle Scholar
  30. Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485(7398):359CrossRefGoogle Scholar
  31. Fridley JD, Craddock A (2015) Contrasting growth phenology of native and invasive forest shrubs mediated by genome size. New Phytol 207(3):659–668CrossRefGoogle Scholar
  32. Gelman A, Hill J (2007) Data analysis using regression and multi-level hierarchical models, vol 1. Cambridge University Press, New YorkGoogle Scholar
  33. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–472CrossRefGoogle Scholar
  34. Haack RA, Byler JW (1993) Insects and pathogens: regulators of forest ecosystems. J For 91(9):32–37Google Scholar
  35. Heberling JM, Fridley JD (2013) Resource-use strategies of native and invasive plants in Eastern North American forests. New Phytol 200(2):523–533CrossRefGoogle Scholar
  36. Heberling JM, Fridley JD (2016) Invaders do not require high resource levels to maintain physiological advantages in a temperate deciduous forest. Ecology 97(4):874–884Google Scholar
  37. Hinman ED, Fridley JD (2018) To spend or to save? Assessing energetic growth-storage tradeoffs in native and invasive woody plants. Oecologia 188(3):659–669CrossRefGoogle Scholar
  38. Huang W, Siemann E, Wheeler GS, Zou J, Carrillo J, Ding J (2010) Resource allocation to defence and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. J Ecol 98(5):1157–1167CrossRefGoogle Scholar
  39. Huot B, Yao J, Montgomery BL, He SY (2014) Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7(8):1267–1287CrossRefGoogle Scholar
  40. Jo I, Fridley JD, Frank DA (2015) Linking above-and belowground resource use strategies for native and invasive species of temperate deciduous forests. Biol Invasions 17(5):1545–1554CrossRefGoogle Scholar
  41. Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8(7):704–714CrossRefGoogle Scholar
  42. Karban R, Myers JH (1989) Induced plant responses to herbivory. Annu Rev Ecol Syst 20(1):331–348CrossRefGoogle Scholar
  43. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17(4):164–170CrossRefGoogle Scholar
  44. Kirichenko N, Péré C, Baranchikov Y, Schaffner U, Kenis M (2013) Do alien plants escape from natural enemies of congeneric residents? Yes but not from all. Biol Invasions 15(9):2105–2113CrossRefGoogle Scholar
  45. Knight TM, Caswell H, Kalisz S (2009) Population growth rate of a common understory herb decreases non-linearly across a gradient of deer herbivory. For Ecol Manag 257(3):1095–1103CrossRefGoogle Scholar
  46. Lamarque LJ, Delzon S, Lortie CJ (2011) Tree invasions: a comparative test of the dominant hypotheses and functional traits. Biol Invasions 13(9):1969–1989CrossRefGoogle Scholar
  47. Lieurance D, Cipollini D (2012) Damage levels from arthropod herbivores on Lonicera maackii suggest enemy release in its introduced range. Biol Invasions 14(4):863–873CrossRefGoogle Scholar
  48. Lieurance D, Cipollini D (2013) Exotic Lonicera species both escape and resist specialist and generalist herbivores in the introduced range in North America. Biol Invasions 15(8):1713–1724CrossRefGoogle Scholar
  49. Mack RN (2003) Plant naturalizations and invasions in the eastern United States: 1634–1860. Ann Mo Bot Gard 90(1):77–90CrossRefGoogle Scholar
  50. Martinez KA, Fridley JD (2018) Acclimation of leaf traits in seasonal light environments: are non-native species more plastic? J Ecol 106(5):2019–2030CrossRefGoogle Scholar
  51. Mattson WJ Jr (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11(1):119–161CrossRefGoogle Scholar
  52. Meijer K, Schilthuizen M, Beukeboom L, Smit C (2016) A review and meta-analysis of the enemy release hypothesis in plant–herbivorous insect systems. PeerJ 4:e2778CrossRefGoogle Scholar
  53. Morrison JA, Mauck K (2007) Experimental field comparison of native and non-native maple seedlings: natural enemies, ecophysiology, growth and survival. J Ecol 95(5):1036–1049CrossRefGoogle Scholar
  54. Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19(8):417–422CrossRefGoogle Scholar
  55. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967CrossRefGoogle Scholar
  56. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018) nlme: Linear and nonlinear mixed effects models. R package version 3.1-137.
  57. Post KH, Parry D (2011) Non-target effects of transgenic blight-resistant American chestnut (Fagales: Fagaceae) on insect herbivores. Environ Entomol 40(4):955–963CrossRefGoogle Scholar
  58. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  59. Rhoades DF (1985) Offensive-defensive interactions between herbivores and plants: their relevance in herbivore population dynamics and ecological theory. Am Nat 125(2):205–238CrossRefGoogle Scholar
  60. Rogers WE, Siemann E (2005) Herbivory tolerance and compensatory differences in native and invasive ecotypes of Chinese tallow tree (Sapium sebiferum). Plant Ecol 181(1):57–68CrossRefGoogle Scholar
  61. Rossell CR Jr, Gorsira B, Patch S (2005) Effects of white-tailed deer on vegetation structure and woody seedling composition in three forest types on the Piedmont Plateau. For Ecol Manag 210(1–3):415–424CrossRefGoogle Scholar
  62. Schierenbeck KA, Mack RN, Sharitz RR (1994) Effects of herbivory on growth and biomass allocation in native and introduced species of Lonicera. Ecology 75(6):1661–1672CrossRefGoogle Scholar
  63. Schowalter TD, Hargrove W, Crossley DA Jr (1986) Herbivory in forested ecosystems. Annu Rev Entomol 31(1):177–196CrossRefGoogle Scholar
  64. Schultheis EH, Berardi AE, Lau JA (2015) No release for the wicked: enemy release is dynamic and not associated with invasiveness. Ecology 96(9):2446–2457CrossRefGoogle Scholar
  65. Su YS, Yajima M (2015) R2jags: Using R to run ‘JAGS’. R package version 0.5-7Google Scholar
  66. Tilghman NG (1989) Impacts of white-tailed deer on forest regeneration in northwestern Pennsylvania. J Wildl Manag 53:524–532CrossRefGoogle Scholar
  67. USDA, NRCS (2018) The PLANTS Database., 26 May 2018. National Plant Data Team, Greensboro, NC 27401-4901 USA
  68. van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13(2):235–245CrossRefGoogle Scholar
  69. van Kleunen M, Bossdorf O, Dawson W (2018) The ecology and evolution of alien plants. Ann Rev Ecol Evol Syst 49:25–47CrossRefGoogle Scholar
  70. Wein A, Bauhus J, Bilodeau-Gauthier S, Scherer-Lorenzen M, Nock C, Staab M (2016) Tree species richness promotes invertebrate herbivory on congeneric native and exotic tree saplings in a young diversity experiment. PLoS ONE 11(12):e0168751CrossRefGoogle Scholar
  71. Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distrib 14(4):569–580CrossRefGoogle Scholar
  72. Wolfe LM (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am Nat 160(6):705–711Google Scholar
  73. Züst T, Agrawal AA (2017) Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annu Rev Plant Biol 68:513–534CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Biology DepartmentSyracuse UniversitySyracuseUSA
  2. 2.Department of Environmental and Forest BiologySUNY College of Environmental Science and ForestrySyracuseUSA

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