Biological Invasions

, Volume 8, Issue 7, pp 1535–1545 | Cite as

Testing the enemy release hypothesis: a review and meta-analysis

Article

Abstract

One of the most cited hypotheses explaining the inordinate success of a small proportion of introduced plants that become pests is the ‘natural enemies hypothesis’. This states that invasive introduced plants spread rapidly because they are liberated from their co-evolved natural enemies. This hypothesis had not been properly tested until recently. Previous reviews on this topic have been narrative and vote counting in nature. In this review, we carried out quantitative synthesis and meta-analysis using existing literature on plants and their herbivores to test the different components of the enemy release hypothesis. We found supporting evidence in that (1) insect herbivore fauna richness is significantly greater in the native than introduced ranges, and the reduction is skewed disproportionally towards specialists and insects feeding on reproductive parts; and (2) herbivore damage levels are greater on native plants than on introduced invasive congeners. However, herbivore damage levels are only marginally greater for plants in native than in introduced ranges, probably due to the small numbers of this type of study. Studies quantifying herbivore impacts on plant population dynamics are too scarce to make conclusions for either comparison of plants in native vs introduced ranges or of co-occurring native and introduced congeners. For future research, we advocate that more than two-way comparisons between plants in native and introduced ranges, or native and introduced congeners are needed. In addition, the use of herbivore exclusions to quantify the impacts of herbivory on complete sets of population vital rates of native vs introduced species are highly desirable. Furthermore, three-way comparisons among congeners of native plants, introduced invasive, and introduced non-invasive plants can also shed light on the importance of enemy release. Finally, simultaneously testing the enemy release hypothesis and other competing hypotheses will provide significant insights into the mechanisms governing the undesirable success of invasive species.

Keywords

co-evolution competitive advantage enemy release hypothesis ERH herbivore exclusion herbivore fauna IAS introduced species invasive alien species invasive plant invasive species non-indigenous species specialist herbivore weeds 

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References

  1. Agrawal, AA, Kotanen, PM 2003Herbivores and success of exotic plants: a phylogenetically controlled experimentEcology Letters6712715CrossRefGoogle Scholar
  2. Baloch, GM, Mohyuddin, AI, Ghani, MA 1968 Xanthium strumarium L. – insects and other organisms associated with it in west PakistanTechnical Bulletin of the Commonwealth Institute for Biological Control Technical Bulletin10103111Google Scholar
  3. Blossey, B, Nuzzo, V, Hinz, H, Gerber, E 2001Developing biological control of Alliaria petolata (M. Bieb.) Cavara and Grande (garlic mustard)Natural Area Journal21357367Google Scholar
  4. Briese, DT 1989Natural enemies of carduine thistles in New South WalesJournal of the Australian Entomological Society28125134Google Scholar
  5. Briese, DT, Sheppard, AW, Zwolfer, H, Boldt, PE 1994Structure of the phytophagous insect fauna of Onopordum thistles in the northern Mediterranean basinBiological Journal of the Linnean Society53231253CrossRefGoogle Scholar
  6. Bürki, CB, Nentwig, W 1997Comparison of herbivore insect communities of Heracleum sphondylium and H. mantegazzianum in Switzerland (Spermatophyta: Apicaceae)Entomologia Generalis22147155Google Scholar
  7. Colautti, RI, Ricciardi, A, Grigorovich, IA, Maclsaac, HJ 2004Is invasion success explained by the enemy release hypothesis?Ecology Letters7721733CrossRefGoogle Scholar
  8. Connor, EF, Faeth, SH, Simberloff, D, Opler, PA 1980Taxonomic isolation and the accumulation of herbivorous insects: a comparison of introduced and native treesEcological Entomology5205211CrossRefGoogle Scholar
  9. Crawley, MJ 1997Plant EcologyBlackwell ScienceOxfordGoogle Scholar
  10. DeWalt, SJ, Denslow, JS, Ickes, K 2004Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta Ecology85471483Google Scholar
  11. Goeden, RD 1971The phytophagous insect fauna of milk thistle in southern CaliforniaJournal of Economic Entomology6411011104Google Scholar
  12. Goeden, RD 1973Comparative survey of the phytophagous insect faunas of Italian thistle, Carduus pycnocephalus, in southern California and southern Europe relative to biological weed controlEnvironmental Entomology3464474Google Scholar
  13. Hilgendorf, JH, Geoden, RD 1982Phytophagous insects reported worldwide from the noxious weeds spiny clotbur, Xanthium spinosum, and cocklebur, X. strumarium Bulletin of the Entomological Society of America28147152Google Scholar
  14. Hinz, HL, Gerber, E 1998Investigations on Potential Biological Control Agents of Garlic Mustard, Alliaria petiolata (Bieb.) Cavara & Grande. Annual Report for 1998CABI BioscienceDelemontGoogle Scholar
  15. Jobin, A, Schaffner, U, Nentwig, W 1996The structure of the phytophagous insect fauna on the introduced weed Solidago altissima in SwizerlandEntomologia Experimentalis et Applicata793342CrossRefGoogle Scholar
  16. Keane, RM, Crawley, MJ 2002Exotic plant invasions and the enemy release hypothesisTrends in Ecology and Evolution17164169CrossRefGoogle Scholar
  17. Levine, JM, Adler, PB, Yelenik, SG 2004A meta-analysis of biotic resistance to exotic plant invasionsEcology Letters7975989CrossRefGoogle Scholar
  18. Lindelöw, A, Björkman, C 2001Insects on lodgepole pine in Sweden – current knowledge and potential risksForest Ecology and Management141107116CrossRefGoogle Scholar
  19. Maron, JL, Vilà, M 2001When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypothesesOikos95361373CrossRefGoogle Scholar
  20. Memmott, J, Fowler, SV, Paynter, Q, Sheppard, AW, Syrett, P 2000The invertebrate fauna on broom, Cytisus scoparius, in two native and two exotic habitatsActa Oecologica21213222CrossRefGoogle Scholar
  21. Mitchell, CE, Power, AG 2003Release of invasive plants from fungal and viral pathogensNature421625627PubMedCrossRefGoogle Scholar
  22. Myers, JH, Basely, DR 2003Ecology and Control of Introduced Plants, pp 20–23Cambridge University PressCambridge2023Google Scholar
  23. Radho-Toly, S, Majer, JD, Yates, C 2001Impact of fire on leaf nutrients, arthropod fauna and herbivory of native and exotic eucalypts in Kings Park, Perth, Western AustraliaAustralia Journal of Ecology26500506CrossRefGoogle Scholar
  24. Rosenberg, MS, Adams, DC, Gurevitch, J 2000MetaWin: Statistical software for Meta-Analysis Version 2.0Sinauer AssociatesSunderlandGoogle Scholar
  25. Schierenbeck, KA, Mack, RN, Sharitz, RR 1994Effects of herbivory on growth and biomass allocation in native and introduced species of Lonicera Ecology7516611672CrossRefGoogle Scholar
  26. Southwood, TRE, Moran, VC, Kennedy, CEJ 1982The richness, abundance and biomsass of the arthropod communities on treesJournal of Animal Ecology51635649CrossRefGoogle Scholar
  27. Strong, DR, Lawton, JH, Southwood, R 1984Insects on Plants: Community Patterns and MechanismsBlackwell Scientific PublicationsOxfordGoogle Scholar
  28. Szentesi, A 1999Predispersal seed predation of the introduced false indigo, Amorpha fruticosa L. in HungaryActa Zoologica Academiae Scientiarum Hungaricae45125141Google Scholar
  29. Torchin, ME, Mitchell, CE 2004Parasites, pathogens, and invasions by plants and animalsFrontiers in Ecology and Environment2183190Google Scholar
  30. Wilson, CG, Flanagan, GJ 1990The phytophagous insect fauna of the introduced shrubs Sida acuta Burm. F. and Sida cordifolia L. in the northern territory, AustraliaAustralian Entomological Magazine17715Google Scholar
  31. Wilson, CG, Flanagan, GJ 1993Phytophagous insect fauna of the introduced noxious weed Xanthium occidentale in northern Australia and its relevance to biological controlBiological Control2254261Google Scholar
  32. Wilson, CG, Flanagan, GJ, Gillett, JD 1990The phytophagous fauna of the introduced shrub Mimosa pigra in northern Australia and its relevance to biological controlEnvironmental Entomology19776784Google Scholar
  33. Wolfe, LM 2002Why alien invaders succeed: support for the escape-from-enemy hypothesisAmerican Naturalists160705711CrossRefGoogle Scholar
  34. Yela, JL, Lawton, JH 1997Insect herbivore loads on native and introduced plants: a preliminary studyEntomological Experimentalis et Applicata85275279CrossRefGoogle Scholar
  35. Zwölfer, H 1965Preliminary list of phytophagous insects attacking wild Cynareae (Compositae) in EuropeTechnical Bulletin of the Commonwealth Institute for Biological Control Technical Bulletin681154Google Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of South FloridaTampaUSA
  2. 2.C/o U.S. Department of Agriculture, Agricultural Research Service, Invasive Plant Research LaboratoryUniversity of Florida, IFASLauderdaleUSA

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