Biological Invasions

, Volume 17, Issue 12, pp 3419–3432 | Cite as

Multitrophic enemy escape of invasive Phragmites australis and its introduced herbivores in North America

  • Warwick J. AllenEmail author
  • Randee E. Young
  • Ganesh P. Bhattarai
  • Jordan R. Croy
  • Adam M. Lambert
  • Laura A. Meyerson
  • James T. Cronin
Original Paper


One explanation for why invasive species are successful is that they escape natural enemies from their native range or experience lower attack from natural enemies in the introduced range relative to native species (i.e., the enemy-release hypothesis). However, little is known about how invasive plants interact with co-introduced herbivores or natural enemies of the introduced herbivores. We focus on Phragmites australis, a wetland grass native to Europe (EU) and North America (NA). Within the past 100–150 years, invasive European genotypes of P. australis and several species of specialist Lipara gall flies have spread within NA. On both continents we surveyed P. australis patches for Lipara infestation (proportion of stems infested) and Lipara mortality from natural enemies. Our objectives were to assess evidence for enemy-release in the invaded (NA) versus native (EU) range and whether Lipara infestation or mortality differed between invasive and native P. australis genotypes in NA. Enemy-release varied regionally; Lipara were absent throughout most of NA, supporting enemy-release of Phragmites. However, where Lipara were present, the proportion of invasive P. australis stems infested with Lipara was higher in the introduced (11 %) than native range (<1 %). This difference may be explained by the absence of Lipara parasitoids in our NA survey, strongly supporting enemy-release of Lipara. In NA, native P. australis genotypes exhibited higher Lipara infestation (32 %) than invasive genotypes (11 %), largely driven by L. rufitarsis. We attribute genotypic differences in infestation to a combination of Lipara exhibiting 34 % greater performance (gall diameter) and suffering four times less vertebrate predation on native than invasive genotypes. Our study suggests that complex interactions can result from the co-introduction of plants and their herbivores, and that a multitrophic perspective is required for investigating how biotic interactions influence invasion success.


Biotic resistance Chloropidae Enemy release Invasive plants Invasional meltdown Lipara spp. natural enemies 



Thanks to the stakeholders and landowners who allowed us access: Rachel Carson National Wildlife Refuge, Choptank Nature Conservancy, Palm Beach County Parks Department, Rockefeller Wildlife Refuge, Alice Welford, Mackay Island National Wildlife Refuge, Pettipaug Yacht Club, Sheepscot Valley Conservation Association, and Estell Manor State Park. Thanks also to B. Elderd, R. Andrews, A. Chow, A. Hunt, A. Flora, J. Maynard, H. Baldwin, D. Cummings, J. Anderson, M. Burger, C. Meyerson, M. Meyerson, F. Meyerson, C. Lambertini, and H. Brix for lab and field assistance. We also thank C. Rohal, E. Hazelton, and T. Reader for useful discussion, and the two anonymous reviewers for their comments which improved the quality of this manuscript. This project was funded by NSF grant numbers DEB 1050084 (to J.T.C.) and 1049914 (to L.A.M.), the Louisiana Environmental Education Commission (to W.J.A.), and the University of Rhode Island Agricultural Experiment Station grant number RI00H-332, 311000-6044 (to L.A.M.).

Supplementary material

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Supplementary material 1 (DOCX 133 kb)
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Supplementary material 4 (DOCX 32 kb)


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Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Warwick J. Allen
    • 1
    Email author
  • Randee E. Young
    • 1
  • Ganesh P. Bhattarai
    • 1
  • Jordan R. Croy
    • 1
  • Adam M. Lambert
    • 2
  • Laura A. Meyerson
    • 3
  • James T. Cronin
    • 1
  1. 1.Department of Biological SciencesLouisiana State UniversityBaton RougeUSA
  2. 2.UCSB Marine Science InstituteUniversity of California at Santa BarbaraSanta BarbaraUSA
  3. 3.Natural Resources ScienceUniversity of Rhode IslandKingstonUSA

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