, Volume 166, Issue 3, pp 843–851 | Cite as

Phylogenetic structure predicts capitular damage to Asteraceae better than origin or phylogenetic distance to natives

Community ecology - Original Paper


Exotic species more closely related to native species may be more susceptible to attack by native natural enemies, if host use is phylogenetically conserved. Where this is the case, the use of phylogenies that include co-occurring native and exotic species may help to explain interspecific variation in damage. In this study, we measured damage caused by pre-dispersal seed predators to common native and exotic plants in the family Asteraceae. Damage was then mapped onto a community phylogeny of this family. We tested the predictions that damage is phylogenetically structured, that exotic plants experience lower damage than native species after controlling for this structure, and that phylogenetically novel exotic species would experience lower damage. Consistent with our first prediction, 63% of the variability in damage was phylogenetically structured. When this structure was accounted for, exotic plants experienced significantly lower damage than native plants, but species origin only accounted for 3% of the variability of capitular damage. Finally, there was no support for the phylogenetic novelty prediction. These results suggest that interactions between exotic plants and their seed predators may be strongly influenced by their phylogenetic position, but not by their relationship to locally co-occurring native species. In addition, the influence of a species’ origin on the damage it experiences often may be small relative to phylogenetically conserved traits.


Asteraceae Darwin’s naturalization hypothesis Community phylogenetics Enemy release hypothesis Invasion biology 



This research was supported by NSERC Discovery and Equipment Grants (PMK), an NSERC PGS-D (SBH), and the Koffler Scientific Reserve at Jokers Hill. Thanks to Kateryna Kostyukova for her help, Andrew MacDonald and Megan Saunders for their support, discussions, and field assistance, and two anonymous reviewers for their comments. All of the experiments conducted in this study comply with the current laws of Canada. This is a publication of the Koffler Scientific Reserve.


  1. Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6:712–715CrossRefGoogle Scholar
  2. Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153:51–68CrossRefGoogle Scholar
  3. Brändle M, Brandl R (2006) Is the composition of phytophagous insects and parasitic fungi among trees predictable? Oikos 113:296–304CrossRefGoogle Scholar
  4. Cadotte MW, Hamilton MA, Murray BR (2009) Phylogenetic relatedness and plant invader success across two spatial scales. Divers Distrib 15:481–488CrossRefGoogle Scholar
  5. Cahill JF, Kembel SW, Lamb EG, Keddy PA (2008) Does phylogenetic relatedness influence the strength of competition among vascular plants? Perspect Plant Ecol 10:41–50CrossRefGoogle Scholar
  6. Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Lett 1:435–438PubMedCrossRefGoogle Scholar
  7. Chun YJ, van Kleunen M, Dawson W (2010) The role of enemy release, tolerance and resistance in plant invasions: linking damage to performance. Ecol Lett 13:937–946PubMedGoogle Scholar
  8. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  9. Crawley MJ (1989) Insect herbivores and plant population dynamics. Annu Rev Ecol Syst 34:531–564Google Scholar
  10. Crawley MJ (2007) The R book. Wiley, New YorkCrossRefGoogle Scholar
  11. Daehler CC (2001) Darwin’s naturalization hypothesis revisited. Am Nat 158:324–330PubMedCrossRefGoogle Scholar
  12. Darwin C (1859) On the origin of species by means of natural selection. Murray, LondonGoogle Scholar
  13. Dawson W, Burslem D, Hulme PE (2009) Herbivory is related to taxonomic isolation, but not to invasiveness of tropical alien plants. Divers Distrib 15:141–147CrossRefGoogle Scholar
  14. de Candolle ALP (1855) Géographie botanique raissoné. Masson, ParisGoogle Scholar
  15. Desdevises Y, Legendre P, Azouzi L, Morand S (2003) Quantifying phylogenetically structured environmental variation. Evolution 57:2647–2652PubMedGoogle Scholar
  16. Diez JM, Sullivan JJ, Hulme PE, Edwards G, Duncan RP (2008) Darwin’s naturalization conundrum: dissecting taxonomic patterns of species invasions. Ecol Lett 11:674–681PubMedCrossRefGoogle Scholar
  17. Diniz-Filho JAF, de Sant’Ana CER (1998) An eigenvector method for estimating phylogenetic inertia. Evolution 52:1247–1262CrossRefGoogle Scholar
  18. Duncan RP, Williams PA (2002) Darwin’s naturalization hypothesis challenged. Nature 417:608–609PubMedCrossRefGoogle Scholar
  19. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  20. Fenner M, Lee WG (2001) Lack of pre-dispersal seed predators in introduced Asteraceae in New Zealand. N Z J Ecol 25:95–99Google Scholar
  21. Fenner M, Cresswell JE, Hurley RA (2002) Relationship between capitulum size and pre-dispersal seed predation by insect larvae in common Asteraceae. Oecologia 130:72–77Google Scholar
  22. Frenzel M, Brandl R (2001) Hosts as habitats: faunal similarity of phytophagous insects between host plants. Ecol Entomol 26:594–601CrossRefGoogle Scholar
  23. Funk VA, Bayer RJ, Kelley S, Chan R, Watson L, Gemeinholzer B, Schilling E, Panero JL, Baldwin BG, Garcia-Jacas N, Susanna A, Jansen RK (2005) Everywhere but Antarctica: using a supertree to understand the diversity and distribution of the Compositae. Biol Skr 55:343–374Google Scholar
  24. Gaskin JF, Wilson LM (2007) Phylogenetic relationships among native and naturalized Hieracium (Asteraceae) in Canada and the United States based on plastid DNA sequences. Syst Bot 32:478–485CrossRefGoogle Scholar
  25. Gilbert GS, Webb CO (2007) Phylogenetic signal in plant pathogen-host range. Proc Natl Acad Sci USA 104:4979–4983PubMedCrossRefGoogle Scholar
  26. Gross RS, Werner PA, Hawthorn WR (1980) The biology of Canadian weeds 38: Arctium minus (Hill) Bernh. and A. lappa L. Can J Plant Sci 60:621–634CrossRefGoogle Scholar
  27. Hawkes CV (2007) Are invaders moving targets? The generality and persistence of advantages in size, reproduction, and enemy release in invasive plant species with time since introduction. Am Nat 170:832–843PubMedCrossRefGoogle Scholar
  28. Hawthorn WD, Hayne PD (1978) Seed production and pre-dispersal seed predation in the biennial composite species, Arctium minus (Hill) Bernh. and A. lappa L. Oecologia 34:283–295CrossRefGoogle Scholar
  29. Hill SB, Kotanen PM (2009) Evidence that phylogenetically novel non-indigenous plants experience less herbivory. Oecologia 161:581–590PubMedCrossRefGoogle Scholar
  30. Hill SB, Kotanen PM (2010) Phylogenetically structured damage on Asteraceae: susceptibility of native and exotic species to foliar herbivores. Biol Invasions 12:3333–3342CrossRefGoogle Scholar
  31. Holt RD (1977) Predation, apparent competition, and structure of prey communities. Theor Popul Biol 12:197–229PubMedCrossRefGoogle Scholar
  32. Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8:704–714CrossRefGoogle Scholar
  33. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  34. Kim KJ, Choi KS, Jansen RK (2005) Two chloroplast DNA inversions originated simultaneously during the early evolution of the sunflower family (Asteraceae). Mol Biol Evol 22:1783–1792PubMedCrossRefGoogle Scholar
  35. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989CrossRefGoogle Scholar
  36. Lewinsohn TM, Novotny V, Basset Y (2005) Insects on plants: diversity of herbivore assemblages revisited. Annu Rev Ecol Syst 36:597–620CrossRefGoogle Scholar
  37. Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545CrossRefGoogle Scholar
  38. Liu H, Stiling P, Pemberton RW (2007) Does enemy release matter for invasive plants? evidence from a comparison of insect herbivore damage among invasive, non-invasive and native congeners. Biol Invasions 9:773–781CrossRefGoogle Scholar
  39. Louda SM (1983) Seed predation and seedling mortality in the recruitment of a shrub, Haplopappus venetus (Asteraceae), along a climatic gradient. Ecology 64:511–521CrossRefGoogle Scholar
  40. Louda SM, O’Brien CW (2002) Unexpected ecological effects of distributing the exotic weevil, Larinus planus (F.), for the biological control of Canada thistle. Conserv Biol 16:717–727CrossRefGoogle Scholar
  41. Louda SM, Potvin MA (1995) Effect of inflorescence-feeding insects in the demography and lifetime fitness of a native plant. Ecology 76:229–245CrossRefGoogle Scholar
  42. Louda SM, Kendall D, Connor J, Simberloff D (1997) Ecological effects of an insect introduced for the biological control of weeds. Science 277:1088–1090CrossRefGoogle Scholar
  43. Louda SM, Pemberton RW, Johnson MT, Follett PA (2003) Nontarget effects—the Achilles’ heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annu Rev Entomol 48:365–396PubMedCrossRefGoogle Scholar
  44. Mack RN (1996) Predicting the identity and fate of plant invaders: emergent and emerging approaches. Biol Conserv 78:107–121CrossRefGoogle Scholar
  45. Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373CrossRefGoogle Scholar
  46. Mason PG, Huber JT (2002) Biological control programmes in Canada 1981–2000. CABI, OttawaGoogle Scholar
  47. Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG, Seabloom EW, Torchin ME, Vazquez DP (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740PubMedCrossRefGoogle Scholar
  48. Moore RJ (1975) The biology of Canadian weeds, 13. Cirsium arvense (L.) Scop. Can J Plant Sci 55:1033–1048CrossRefGoogle Scholar
  49. Morton JK, Venn JM (1990) A checklist of the flora of Ontario: vascular plants. University of Waterloo Biology Series 34, Waterloo, ONGoogle Scholar
  50. Noyes RD (2000) Biogeographical and evolutionary insights on Erigeron and allies (Asteraceae) from ITS sequence data. Plant Syst Evol 220:93–114CrossRefGoogle Scholar
  51. Odegaard F, Diserud OH, Ostbye K (2005) The importance of plant relatedness for host utilization among phytophagous insects. Ecol Lett 8:612–617CrossRefGoogle Scholar
  52. Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Stevens MHH, Wagner H (2009) vegan: community ecology package. R package version 1.15-4. http://CRAN.R-project.org/package=vegan
  53. Parker IM, Gilbert GS (2007) When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants. Ecology 88:1210–1224PubMedCrossRefGoogle Scholar
  54. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967CrossRefGoogle Scholar
  55. Pearse IS, Hipp AL (2009) Phylogenetic and trait similarity to a native species predict herbivory on non-native oaks. Proc Nat Acad Sci USA 106:18097–18102PubMedCrossRefGoogle Scholar
  56. SAS (2002) JMP. SAS Institute, CaryGoogle Scholar
  57. Semple JC, Cook RE (2006) Solidago. In: Committee FNAE (ed) Flora of North America. Oxford University Press, Oxford, pp 107–166Google Scholar
  58. Strauss SY, Webb CO, Salamin N (2006) Exotic taxa less related to native species are more invasive. Proc Natl Acad Sci USA 103:5841–5845PubMedCrossRefGoogle Scholar
  59. Strong DR, Lawton JH, Southwood R (1984) Insects on plants. Harvard University Press, CambridgeGoogle Scholar
  60. R Development core team (2006) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org
  61. Thuiller W, Gallien L, Boulangeat I, de Bello F, Münkemüller T, Roquet C, Lavergne S (2010) Resolving Darwin’s naturalization conundrum: a quest for evidence. Diversity Distrib 16:461–475CrossRefGoogle Scholar
  62. Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190CrossRefGoogle Scholar
  63. Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183CrossRefGoogle Scholar
  64. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505CrossRefGoogle Scholar
  65. Weiblen GD, Webb CO, Novotny V, Basset Y, Miller SE (2006) Phylogenetic dispersion of host use in a tropical insect herbivore community. Ecology 87:S62–S75PubMedCrossRefGoogle Scholar
  66. Whitton J, Wallace RS, Jansen RK (1995) Phylogenetic-relationships and patterns of character change in the tribe Lactuceae (Asteraceae) based on chloroplast DNA restriction site variation. Can J Bot 73:1058–1073CrossRefGoogle Scholar
  67. Zuefle ME, Brown WP (2008) Tallamy DW (2008) Effects of non-native plants on the native insect community of Delaware. Biol Invasions 10:1159–1169CrossRefGoogle Scholar
  68. Zwölfer H (1998) Evolutionary and ecological relationships of the insect fauna of thistles. Annu Rev Entomol 33:103–122CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of Toronto at MississaugaMississaugaCanada

Personalised recommendations