Biological Invasions

, Volume 11, Issue 4, pp 1005–1016 | Cite as

A cross-continental test of the Enemy Release Hypothesis: leaf herbivory on Acer platanoides (L.) is three times lower in North America than in its native Europe

  • Jonathan M. Adams
  • Wei Fang
  • Ragan M. Callaway
  • Don Cipollini
  • Elizabeth Newell
  • Transatlantic Acer platanoides Invasion Network (TRAIN)
Original Paper


Acer platanoides (Norway maple) is a widespread native tree species in Europe. It has been introduced to North America where it has often established dense stands in both secondary woodlands and relatively undisturbed mature woodlands. In Europe A. platanoides is also extending its original range, but generally seems to exist at much lower densities. One explanation for the ‘aggressiveness’ of invasive plants such as A. platanoides is that they have left behind pests and diseases which limit their population densities in their native lands (the enemy release hypothesis or ERH). To assess the ERH for Norway maple, a large network of collaborators assessed leaf herbivory rates in populations throughout Europe and North America. We found significantly lower total leaf herbivory (1.6% ± 0.19, n = 21 vs. 7.4% ± 1.94, n = 34) and lower fungal damage (1.0% ± 0.35, n = 13 vs. 3.7% ± 0.85, n = 34) in North America than in Europe over a 2 year period, which is consistent with the predictions of the Enemy Release Hypothesis. Across years, the average total leaf herbivory was significantly correlated with average annual temperature of the site (< 0.05), although this was mostly due to sites in Europe (< 0.001), and not sites in North America (> 0.05). Furthermore, only populations in Europe showed very high levels of herbivory (e.g., nine sites had total leaf herbivory ranging from 10.0 to 51.2% in at least 1 year) or leaf fungal damage (only one site in North America showed high levels of fungal damage in 1 year), suggesting the possibility of more frequent episodic outbreaks in the native range. Leaf herbivory and fungal damage are only two aspects of consumer pressure and we do not know whether the differences reported here are enough to actually elicit release from top-down population control, but such large scale biogeographic differences in herbivory contribute towards understanding exotic invasions.


Biological invasion Acer platanoides Enemy release hypothesis North America Europe 



Data collection in Slovakia was supported by the grant VEGA No 2/5152/25, and in Montana by the Sponsored Research Office of The University of Montana.


  1. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7 (8):721–733CrossRefGoogle Scholar
  2. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335. doi: 10.1146/annurev.ecolsys.27.1.305 CrossRefGoogle Scholar
  3. Cranshaw W (2004) Garden insects of North America. Princeton University Press, PrincetonGoogle Scholar
  4. Crawley MJ (1983) Herbivory, the dynamics of animal-plant interactions. Blackwell, OxfordGoogle Scholar
  5. DeWalt SJ, Denslow JS, Ickes K (2004) Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 85:471–483. doi: 10.1890/02-0728 CrossRefGoogle Scholar
  6. Dunster K (1990) Exotic plant species management plan, Point Pelee National Park, Report prepared for Parks Canada, Ontario RegionGoogle Scholar
  7. Fang W (2005) Spatial analysis of an invasion front Acer platanoides: dynamic inferences from static data. Ecography 28:1–12. doi: 10.1111/j.0906-7590.2005.04052.x CrossRefGoogle Scholar
  8. Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15. doi: 10.1111/j.0022-0477.2004.00953.x CrossRefGoogle Scholar
  9. Hudler GW, Banik MT, Miller S (1987) Unusual epidemic of tar spot on Norway maple in upstate New York. Plant Dis 71:65–68. doi: 10.1094/PD-71-0065 CrossRefGoogle Scholar
  10. Hudler GW, Jensen-Tracy S, Banik MT (1998) Rhytisma americanum sp. nov.: a previously undescribed species of Rhytisma on maples (Acer spp.). Mycotaxon 68:405–416Google Scholar
  11. Jactel HJ, Brockerhoff E, Duelli P (2005) A test of the biodiversity—stability theory: meta-analysis of tree species diversity effects on insect pest infestations, and re-examination of responsible factors. In: Scherer-Lorenzen M, Körner CH, Schulze ED (eds) Forest diversity and function. Temperate and boreal systems. Ecological studies, vol 176. Springer, Berlin, pp 235–262Google Scholar
  12. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. doi: 10.1016/S0169-5347(02)02499-0 CrossRefGoogle Scholar
  13. Martin PH (1999) Norway maple (Acer platanoides) invasion of natural forest stand: understory consequence and regeneration pattern. Biol Invasions 1:215–222. doi: 10.1023/A:1010084421858 CrossRefGoogle Scholar
  14. Martin PH, Marks PL (2006) Intact forests provide only weak resistance to a shade-tolerant invasive Norway maple. J Ecol 94:1070–1079. doi: 10.1111/j.1365-2745.2006.01159.x CrossRefGoogle Scholar
  15. Muller MJ (1982) Selected climate data for a global set of standard stations for vegetation science. Dr W. Junk Publishers, The Hague, pp 1–12Google Scholar
  16. Nowak DJ, Rowntree RA (1990) History and range of Norway maple. J Arboricult 16:291–296Google Scholar
  17. Prism (2004) Spatial Climate Analysis Service, Oregon State University. Created 4 Feb 2004
  18. Reinhart KO, Callaway RM (2004) Soil biota facilitate exotic Acer invasions in Europe and North America. Ecol Appl 14:1737–1745. doi: 10.1890/03-5204 CrossRefGoogle Scholar
  19. Reinhart KO, Greene E, Callaway RM (2005) Effects of Acer platanoides invasion on understory plant communities and tree generation in the northern Rocky Mountains. Ecography 28:573–582. doi: 10.1111/j.2005.0906-7590.04166.x CrossRefGoogle Scholar
  20. Reinhart KO, Gurnee J, Tirado R, Callaway RM (2006) Invasion through quantitative effects: intense shade as a driver of invasive success and native decline. Ecol Appl 16:1821–1831. doi: 10.1890/1051-0761(2006)016[1821:ITQEIS]2.0.CO;2 PubMedCrossRefGoogle Scholar
  21. Roques A, Auger-Rozenberg MA, Boivin S (2006) A lack of native congeners may limit colonization of introduced conifers by indigenous insects in Europe. Can J Res 36:299–313. doi: 10.1139/x05-277 CrossRefGoogle Scholar
  22. Siska EL, Pennings SC, Buck TL, Hanisak MD (2002) Latitudinal variation in palatability of salt-marsh plants: which traits are responsible? Ecology 83:3369–3381CrossRefGoogle Scholar
  23. Spongberg SA (1990) A reunion of trees: the discovery of exotic plants and their introduction into North American and European landscapes. Harvard University Press, CambridgeGoogle Scholar
  24. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630. doi: 10.1038/nature01346 PubMedCrossRefGoogle Scholar
  25. Vila M, Maron JL, Marco L (2005) Evidence for the enemy release hypothesis in Hypericum perforatum. Oecologia 142:474–479. doi: 10.1007/s00442-004-1731-z PubMedCrossRefGoogle Scholar
  26. Webb SL, Kaunzinger CK (1993) Biological invasion of the Drew University (New Jersey) forest preserve by Norway maple (Acer platanoides L.). Bull Torrey Bot Club 120:343–349. doi: 10.2307/2996999 CrossRefGoogle Scholar
  27. Webb SL, Dwyer M, Kaunzinger CK, Wyckoff PH (2000) The myth of the resilient forest: case study of the invasive Norway maple (Acer platanoides). Rhodora 102:332–354Google Scholar
  28. Whittaker JB, Warrington S (1985) An experimental field study of different levels of insect herbivory induced by Formica rufa predation on Sycamore (Acer pseudoplatanus) III. Effects on tree growth. J Appl Ecol 22:797–811. doi: 10.2307/2403230 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Jonathan M. Adams
    • 1
  • Wei Fang
    • 2
  • Ragan M. Callaway
    • 3
  • Don Cipollini
    • 4
  • Elizabeth Newell
    • 5
  • Transatlantic Acer platanoides Invasion Network (TRAIN)
    • 6
  1. 1.Department of Biological SciencesRutgers UniversityNewarkUSA
  2. 2.Department of BiologyLong Island UniversityBrookvilleUSA
  3. 3.University of MontanaMissoulaUSA
  4. 4.Wright State UniversityDaytonUSA
  5. 5.Hobart and William Smith CollegesGenevaUSA
  6. 6.CamdenUSA

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