Skip to main content
SpringerLink
Log in

Evidence that phylogenetically novel non-indigenous plants experience less herbivory

  • Community ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The degree to which biotic interactions influence invasion by non-indigenous species may be partly explained by the evolutionary relationship of these invaders with natives. Darwin’s naturalization hypothesis controversially proposes that non-native plants are more likely to invade if they lack close relatives in their new range. A possible mechanism for this pattern is that exotics that are more closely related to natives are more likely to share their herbivores, and thus will suffer more damage than phylogenetically isolated species. We tested this prediction using exotic plants in Ontario, Canada. We measured herbivore damage to 32 species of exotic plants in a common garden experiment, and 52 in natural populations. We estimated their phylogenetic distances from locally occurring natives in three ways: as mean distance (age) to all native plants, mean distance to native members of the same family, and distance to the closest native species. In the common garden, the proportion of leaves damaged and the average proportion of leaf area damaged declined with mean phylogenetic distance to native family relatives by late summer. Distance to native confamilials was a better predictor of damage than distance to the closest native species, while mean distance to the entire native plant community failed to predict damage. No significant patterns were detected for plants in natural populations, likely because uncontrolled site-to-site variation concealed these phylogenetic trends. To the extent that herbivory has negative demographic impacts, these results suggest that exotics that are more phylogenetically isolated from native confamilials should be more invasive; conversely, native communities should be more resistant to invasion if they harbor close familial relatives of potential invaders. However, the large scatter in this relationship suggests that these often are likely to be weak effects; as a result, these effects often may be difficult to detect in uncontrolled surveys of natural populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6:712–715

    Article  Google Scholar 

  • 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 86:2979–2989

    Article  Google Scholar 

  • Bailey CD, Koch MA, Mayer M, Mummenhoff K, O’Kane SL Jr, Warwick SI, Windham MD, Al-Shehbaz IA (2006) Toward a global phylogeny of the Brassicaceae. Mol Biol Evol 23:2142–2160

    Article  PubMed  CAS  Google Scholar 

  • Burnham KD, Anderson DA (2002) Model selection and multi-model inference, 2nd edn. Springer, New York

    Google Scholar 

  • Cahill JF, Kembel SW, Lamb EG, Keddy PA (2008) Does phylogenetic relatedness influence the strength of competition among vascular plants? Plant Ecol Evol Syst 10:41–50

    Article  Google Scholar 

  • Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Lett 1:435–438

    Article  PubMed  Google Scholar 

  • Cavender-Bares J, Ackerly DD, Baum DA, Bazzaz FA (2004) Phylogenetic overdispersion in Floridian oak communities. Am Nat 163:823–843

    Article  PubMed  CAS  Google Scholar 

  • Cavender-Bares J, Keen A, Miles B (2006) Phylogenetic structure of Floridian plant communities depends on taxonomic and spatial scale. Ecology 87:S109–S122

    Article  PubMed  Google Scholar 

  • Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

    Article  Google Scholar 

  • Crall AW, Meyerson LA, Stohlgren TJ, Jarnevich CS, Newman GJ, Graham J (2006) Show me the numbers: what data currently exist for non-native species in the USA? Front Ecol Environ 4:414–418

    Article  Google Scholar 

  • Daehler CC (2001) Darwin’s naturalization hypothesis revisited. Am Nat 158:324–330

    Article  PubMed  CAS  Google Scholar 

  • Darwin C (1859) On the origin of species by means of natural selection. Murray, London

    Google Scholar 

  • Dawson W, Burslem DFRP, Hulme PE (2009) Herbivory is related to taxonomic isolation, but not to invasiveness of tropical alien plants. Divers Distrib 15:141–147

    Article  Google Scholar 

  • Dewalt SJ, Denslow JS, Ickes K (2004) Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 85:471–483

    Article  Google Scholar 

  • Diez JM, Sullivan JJ, Hulme PE, Edwards G, Duncan RP (2008) Darwin’s naturalization conundrum: dissecting taxonomic patterns of species invasions. Ecol Lett 11:674–681

    Article  PubMed  Google Scholar 

  • Downie SR, Katz-Downie DS, Watson MF (2000) A phylogeny of the flowering plant family Apiaceae based on chloroplast DNA rpl16 and rpoCl intron sequences: towards a suprageneric classification of subfamily Apioideae. Am J Bot 87:273–292

    Article  PubMed  CAS  Google Scholar 

  • Duncan RP, Williams PA (2002) Ecology—Darwin’s naturalization hypothesis challenged. Nature 417:608–609

    Article  PubMed  CAS  Google Scholar 

  • Freudenstein JV, van den Berg C, Goldman DH, Kores PJ, Molvray M, Chase MW (2004) An expanded plastid DNA phylogeny of Orchidaceae and analysis of jackknife branch support strategy. Am J Bot 91:149–157

    Article  CAS  Google Scholar 

  • 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 55:343–374

    Google Scholar 

  • Gilbert GS, Webb CO (2007) Phylogenetic signal in plant pathogen–host range. Proc Natl Acad Sci USA 104:4979–4983

    Article  PubMed  CAS  Google Scholar 

  • 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 170:832–843

    Article  PubMed  Google Scholar 

  • Hillis DM (1987) Molecular versus morphological approaches to systematics. Annu Rev Ecol Syst 18:23–42

    Article  Google Scholar 

  • Holt RD (1977) Predation, apparent competition, and structure of prey communities. Theor Popul Biol 12:197–229

    Article  PubMed  CAS  Google Scholar 

  • Holt RD, Lawton JH (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25:495–520

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Långström E, Chase MW (2002) Tribes of Boraginoideae (Boraginaceae) and placement of Antiphytum, Echiochilon, Ogastemma, and Sericostoma: a phylogenetic analysis based on atpB plastid DNA sequence data. Plant Syst Evol 234:137–153

    Article  Google Scholar 

  • Lewinsohn TM, Novotny V, Basset Y (2005) Insects on plants: diversity of herbivore assemblages revisited. Annu Rev Ecol Syst 36:597–620

    Article  Google Scholar 

  • Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545

    Article  Google Scholar 

  • 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 9:773–781

    Article  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Maron JL, Vila M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373

    Article  Google Scholar 

  • Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627

    Article  PubMed  CAS  Google Scholar 

  • 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 9:726–740

    Article  PubMed  Google Scholar 

  • Morton JK, Venn JM (1990) A checklist of the flora of Ontario: vascular plants. University of Waterloo biology series. University of Waterloo, Waterloo

    Google Scholar 

  • Natali A, Manen J-F, Ehrendorfer F (1995) Phylogeny of the Rubiaceae–Rubioideae, in particular the tribe Rubieae: evidence from a non-coding chloroplast DNA sequence. Ann Mo Bot Gard 82:428–439

    Article  Google Scholar 

  • Novotny V, Basset Y (2005) Host specificity of insect herbivores in tropical forests. Proc R Soc Lond B Biol Sci 272:1083–1090

    Article  Google Scholar 

  • Novotny V, Basset Y, Miller SE, Weiblen GD, Bremer B, Cizek L, Drozd P (2002) Low host specificity of herbivorous insects in a tropical forest. Nature 416:841–844

    Article  PubMed  CAS  Google Scholar 

  • Odegaard F, Diserud OH, Ostbye K (2005) The importance of plant relatedness for host utilization among phytophagous insects. Ecol Lett 8:612–617

    Article  Google Scholar 

  • Olmstead RA, dePamphilis CW, Wolfe AD, Young ND, Ellisons WJ, Reeves PA (2001) Disintegration of the Scrophulariaceae. Am J Bot 88:348–361

    Article  PubMed  CAS  Google Scholar 

  • Oxelman B, Lidén M, Berglund D (1996) Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Plant Syst Evol 206:393–410

    Article  Google Scholar 

  • Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967

    Article  Google Scholar 

  • Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461

    Article  PubMed  CAS  Google Scholar 

  • Paton AJ, Springate D, Suddee S, Otieno D, Grayer RJ, Harley MM, Willis F, Simmonds MSJ, Powell MP, Savolainen V (2004) Phylogeny and evolution of basils and allies (Ocimeae, Labiatae) based on three plastid DNA regions. Mol Phylogenet Evol 31:277–299

    Article  PubMed  CAS  Google Scholar 

  • Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • Potter D, Erickson T, Evans RC, Oh S, Smedmark JEE, Morgan DR, Kerr M, Robertson KR, Arsenault M, Dickinson TA, Campbell CS (2007) Phylogeny and classification of Rosaceae. Plant Syst Evol 266:5–43

    Article  Google Scholar 

  • Proches S, Wilson JRU, Richardson DM, Rejmanek M (2008) Searching for phylogenetic pattern in biological invasions. Glob Ecol Biogeogr 17:5–10

    Google Scholar 

  • Rejmanek M (1996) A theory of seed plant invasiveness: the first sketch. Biol Conserv 78:171–181

    Article  Google Scholar 

  • Ro K-E, Keener CS, McPheron BA (1997) Molecular phylogenetic study of the Ranunculaceae: utility of the nuclear 26S ribosomal DNA in inferring intrafamilial relationships. Mol Phylogenet Evol 8:117–127

    Article  PubMed  CAS  Google Scholar 

  • Ronsted N, Chase MW, Albach DC, Bello MA (2002) Phylogenetic relationships within Plantago (Plantaginaceae): evidence from nuclear ribosomal ITS and plastid trnL-F sequence data. Bot J Linn Soc 139:323–338

    Article  Google Scholar 

  • SAS Institute (2002) JMP version 50. SAS Institute, Cary

    Google Scholar 

  • Smedmark JEE, Erickson T (2002) Phylogenetic relationships of Geum (Rosaceae) and relatives inferred from the nrITS and trnL-trnF regions. Syst Bot 27:303–317

    Google Scholar 

  • Smissen RD, Clement JC, Garnock-Jones PJ, Chambers GK (2002) Subfamilial relationships within Caryophyllaceae as inferred from 5′ ndhF sequences. Am J Bot 89:1336–1341

    Article  CAS  Google Scholar 

  • Strauss SY, Webb CO, Salamin N (2006) Exotic taxa less related to native species are more invasive. PNAS 15:5841–5845

    Article  Google Scholar 

  • Strong DR, Lawton JH, Southwood R (1984) Insects on plants. Harvard University Press, Cambridge

    Google Scholar 

  • Swenson NG, Enquist BJ, Thompson J, Zimmerman JK (2007) The influence of spatial and size scale on phylogenetic relatedness in tropical forest communities. Ecology 88:1770–1780

    Article  PubMed  Google Scholar 

  • R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://wwwR-projectorg

  • Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190

    Article  Google Scholar 

  • Wagstaff SJ, Hickerson L, Spangler R, Reeves PA, Olmsted RA (1998) Phylogeny in Labiatae s l inferred from cpDNA sequences. Plant Syst Evol 209:265–274

    Article  CAS  Google Scholar 

  • Webb CO (2000) Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat 156:145–155

    Article  PubMed  Google Scholar 

  • Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183

    Article  Google Scholar 

  • Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  • Webb CO, Gilbert GS, Donoghue MJ (2006) Phylodiversity-dependent seedling mortality, size structure, and disease in a Bornean rain forest. Ecology 87:S123–S131

    Article  PubMed  Google Scholar 

  • 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–S75

    Article  PubMed  Google Scholar 

  • Wikstrom N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proc R Soc Lond B Biol Sci 268:2211–2220

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by NSERC Research and Equipment Grants (P. M. K.), an NSERC PGS-D (S. B. H), and the KSR at Jokers Hill. Thanks to Kateryna Kostyukova for her continuous help, to Nathalie Taraban-Lagois, Gilbert Tang, James McKay, and Andrew MacDonald for their support, discussions, and field assistance, and to two anonymous reviewers for valuable suggestions on an earlier version of this manuscript. This is a publication of the KSR. All of the experiments conducted in this study comply with the current laws of Canada.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Toronto at Mississauga, 3359 Mississauga Road N, Mississauga, ON, L5L 1C6, Canada

    Steven Burton Hill & Peter M. Kotanen

Authors
  1. Steven Burton Hill
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter M. Kotanen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Steven Burton Hill.

Additional information

Communicated by Bernhard Schmid.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hill, S.B., Kotanen, P.M. Evidence that phylogenetically novel non-indigenous plants experience less herbivory. Oecologia 161, 581–590 (2009). https://doi.org/10.1007/s00442-009-1403-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1403-0

Keywords

Search

Navigation