Biological Invasions

, Volume 17, Issue 5, pp 1283–1297 | Cite as

Insights from community ecology into the role of enemy release in causing invasion success: the importance of native enemy effects

  • Kirsten M. PriorEmail author
  • Thomas H. Q. Powell
  • Ashley L. Joseph
  • Jessica J. Hellmann
Perpectives and paradigms


The enemy release hypothesis (ERH) predicts that the success of invasive species is caused by reduced enemy pressure in species’ introduced ranges. The ERH is a highly-cited explanation for invasion success, yet rigorous evidence is lacking for most species and ecosystems. Most evidence comes from observations of enemies in native and introduced ranges. These studies assess one aspect of the ERH—“enemy loss.” They do not provide a direct test of the ERH and overlook the assumption of “native enemy effects.” This is a critical limitation as enemy release will not occur if enemies do not affect species in their native ranges, even if enemy loss occurs. Biogeographical experiments, providing a direct test of the ERH, are largely restricted to terrestrial plants. We present a synthesis of community ecology and invasion biology studies, including a novel meta-analysis of native enemy effects, to assess the potential for release for species in different taxonomic groups and ecosystems. We suggest that species that are subject to strong enemy effects in their native range will have a high potential for enemy release. We found that native enemy effects were stronger in aquatic systems than in terrestrial systems. They were particularly weak for terrestrial plants; and strong for marine organisms, and freshwater plants. Studies are needed for species that have strong potential for release, such as for aquatic invasive species. Alternative explanations should be explored for invasive species that are not affected by enemies in their native range, and future studies should emphasize native enemy effects rather than only enemy loss.


Community interactions Enemy release hypothesis Invasion success Invasive species Top-down effects Native and introduced range 



We thank G. Belovsky, D. Lodge and J. McLachlan for informative discussions. A.L. Joseph and T.H.Q. Powell were supported by GLOBES (NSF-IGERT 0504495). K.M. Prior received support from a Bayer Fellowship from the Center for Environmental Sciences and Technology at the University of Notre Dame, and a Departmental Postdoctoral Fellowship from the Department of Ecology and Evolutionary Biology at the University of Toronto.

Supplementary material

10530_2014_800_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 21 kb)
10530_2014_800_MOESM2_ESM.docx (51 kb)
Supplementary material 2 (DOCX 52 kb)
10530_2014_800_MOESM3_ESM.docx (28 kb)
Supplementary material 3 (DOCX 28 kb)
10530_2014_800_MOESM4_ESM.docx (21 kb)
Supplementary material 4 (DOCX 21 kb)
10530_2014_800_MOESM5_ESM.docx (46 kb)
Supplementary material 5 (DOCX 46 kb)


  1. 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 86:2979–2989CrossRefGoogle Scholar
  2. Atlegrim O (1998) Exclusion of birds from bilberry stands: impact on insect larval density and damage to the bilberry. Oecologia 7:136–139Google Scholar
  3. Bach CE (1994) Effects of a specialist herbivore (Altica suplicata) on Salix cordata and sand dune succession. Ecol Monogr 64:423–445CrossRefGoogle Scholar
  4. Barton AM (1986) Spatial variation in the effect of ants on an extrafloral nectary plant. Ecology 67:495–504CrossRefGoogle Scholar
  5. Bigger DS, Marvier MA (1999) How different would a world without herbivory be? A search for generality in ecology. Integr Biol 1:60–67CrossRefGoogle Scholar
  6. Blossey B, Nötzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants—a hypothesis. J Ecol 83:887–889CrossRefGoogle Scholar
  7. Blumenthal D (2006) Interactions between resource availability and enemy release in Plant invasion. Ecol Lett 9:887–895CrossRefPubMedGoogle Scholar
  8. Blumenthal D, Mitchell CE, Pysek P, Jarosik V (2009) Synergy between pathogen release and resource availability in plant invasion. Proc Natl Acad Sci USA 106:7899–7904CrossRefPubMedCentralPubMedGoogle Scholar
  9. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733CrossRefPubMedGoogle Scholar
  10. Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Lett 1:435–438CrossRefPubMedCentralPubMedGoogle Scholar
  11. Carlsson NO, Sarnelle O, Strayer DL (2009) Native predators and exotic prey –an acquired taste? Front Ecol Environ 7:525–532CrossRefGoogle Scholar
  12. Cebrian J, Shurin JB, Borer ET, Cardinale BJ, Ngai JT, Smith MD, Fagan WF (2009) Producer nutritional quality controls ecosystem trophic structure. PLoS ONE 4:e4929CrossRefPubMedCentralPubMedGoogle Scholar
  13. Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Earlbaum Associates, New JerseyGoogle Scholar
  14. Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558CrossRefPubMedGoogle Scholar
  15. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  16. Cornelissen T, Stiling P (2006) Responses of different herbivore guilds to nutrient addition and natural enemy exclusion. Ecoscience 13:66–74CrossRefGoogle Scholar
  17. Cornell HV, Hawkins BA (1993) Accumulation of native parasitoid species on introduced herbivores: a comparison of hosts as natives and hosts as invaders. Am Nat 141:847–865CrossRefPubMedGoogle Scholar
  18. Cripps MG, Schwarzländer M, McKenney JL, Hinz HL, Price WJ (2006) Biogeographical comparison of arthropod herbivore communities associated with Lepidium draba in its native, expanded and introduced ranges. J Biogeogr 33:2107–2119CrossRefGoogle Scholar
  19. D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Syst 23:63–87Google Scholar
  20. DeBach P, Rosen D (1991) Biological control by natural enemies. University Press, CambridgeGoogle Scholar
  21. DeWalt SJ, Denslow JS, Ickes K (2004) Natural enemy release facilitates habitat expansion of the invasive tropical shrub, Clidemia hirta. Ecology 85:471–483CrossRefGoogle Scholar
  22. Dobson A, Lodge D, Alder J, Cumming GS, Keymer J, McGlade J et al (2006) Habitat loss, trophic collapse, and the decline of ecosystem services. Ecology 87:1915–1924CrossRefPubMedGoogle Scholar
  23. Ebeling SK, Hensen I, Auge H (2008) The invasive shrub Buddleja davidii performs better in its introduced range. Divers Distrib 14:225–233CrossRefGoogle Scholar
  24. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonCrossRefGoogle Scholar
  25. Flecker AS (1992) Fish trophic guilds and the structure of a tropical stream: weak direct vs. strong indirect effects. Ecology 73:927CrossRefGoogle Scholar
  26. Floyd T (1996) Top-down impacts on Creosotebush herbivores in a spatially and temporally complex environment. Ecology 77:1544–1555CrossRefGoogle Scholar
  27. Forslund H, Wikström SA, Pavia H (2010) Higher resistance to herbivory in introduced compared to native populations of a seaweed. Oecologia 164:833–840CrossRefPubMedGoogle Scholar
  28. Fretwell SD (1977) Regulation of plant communities by food-chain exploiting them. Perspect Biol Med 20:169–185CrossRefGoogle Scholar
  29. Genton BJ, Kotanen PM, Cheptou P-O, Adolphe C, Shykoff JA (2005) Enemy release but no evolutionary loss of defence during ragweed invasion of France: an inter-continental reciprocal transplant experiment. Oecologia 146:404–414CrossRefPubMedGoogle Scholar
  30. Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80:1142–1149CrossRefGoogle Scholar
  31. Gurevitch J, Fox GA, Wardle GM, Inderjit, Taub D (2011) Emergent insights from synthesis of conceptual frameworks for biological invasions. Eco Lett 14:407–418CrossRefGoogle Scholar
  32. Haag JJ, Coupe MD, Cahill JF (2004) Antagonistic interactions between competition and insect herbivory on plant growth. J Ecol 92:156–167CrossRefGoogle Scholar
  33. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421CrossRefGoogle Scholar
  34. Halaj J, Wise DH (2001) Terrestrial trophic cascades: how much do they trickle? Am Nat 157:262–281CrossRefPubMedGoogle Scholar
  35. Hay ME (1991) Marine-terrestrial contrasts in the ecology of plant chemical defenses against herbivores. Trends Ecol Evol 6:362–365CrossRefPubMedGoogle Scholar
  36. Heger T, Jeschke JM (2014) The enemy release hypothesis as a hierarchy of hypotheses. Oikos 123:741–750CrossRefGoogle Scholar
  37. Hellmann JJ, Prior KM, Pelini SL (2012) The influence of species interactions on geographic range change under climate change. Ann NY Acad Sci 1249:18–28CrossRefPubMedGoogle Scholar
  38. 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 93:5–15CrossRefGoogle Scholar
  39. Ho CK, Pennings SC (2008) Consequences of omnivory for trophic interactions on a marsh shrub. Ecol 89:1714–1722CrossRefGoogle Scholar
  40. Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258CrossRefPubMedGoogle Scholar
  41. Huitu O, Koivula M, Korpimäki E, Klemola T, Norrdahl K (2003) Winter food supply limits growth of northern vole populations in the absence of predation. Ecology 84:2108–2118CrossRefGoogle Scholar
  42. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732Google Scholar
  43. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528CrossRefGoogle Scholar
  44. Jeschke JM, Aparicio LG, Haider S, Heger T, Lortie CJ, Pyšek P, Strayer DL (2012) Support for major hypotheses in invasion biology is uneven and declining. NeoBiota 14:1–20CrossRefGoogle Scholar
  45. Kalisz S, Spigler RB, Horvitz (2014) In a long-term experimental demography study, excluding ungulates reversed invader’s explosive population growth rate and restored natives. Proc Natl Acad Sci USA 111:4501–4506CrossRefPubMedCentralPubMedGoogle Scholar
  46. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  47. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 1:199–204CrossRefGoogle Scholar
  48. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989CrossRefGoogle Scholar
  49. Lewis SM (1986) The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol Monogr 56:183–200CrossRefGoogle Scholar
  50. Liu H, Stiling P, Pemberton RW, Peña J (2006) Insect herbivore faunal diversity among invasive, non-invasive and native Eugenia species: implications for the enemy release hypothesis. Fla Entomol 89:475–484CrossRefGoogle Scholar
  51. Lodge DM (1991) Herbivory on freshwater macrophytes. Aquat Bot 41:195–224CrossRefGoogle Scholar
  52. Lodge DM, Kershner MW, Aloi JE, Covich AP (1994) Effects of an omnivorous crayfish (Orconectes rusticus) on a freshwater littoral food web. Ecology 75:1265–1281CrossRefGoogle Scholar
  53. MacDonald AAM, Kotanen PM (2010) The effects of disturbance and enemy exclusion on performance of an invasive species, common ragweed, in its native range. Oecologia 162:977–986CrossRefPubMedGoogle Scholar
  54. Maron JL, Vila M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373CrossRefGoogle Scholar
  55. Memmott J, Fowler SV, Paynter Q, Sheppard AW, Syrett R (2000) The invertebrate fauna on broom, Cytisus scoparius, in two native and two exotic habitats. Acta Oecol 21:213–222CrossRefGoogle Scholar
  56. Menéndez R, Gonzáez-Megías A, Lewis OT, Shaw MR, Thomas CD (2008) Escape from natural enemies during climate-driven range expansion: a case study. Ecol Entomol 33:413–421CrossRefGoogle Scholar
  57. Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757CrossRefGoogle Scholar
  58. Miller TEX (2008) Bottom-up, top-down, and within-trophic level pressures on a cactus-feeding insect. Ecol Entomol 33:261–268CrossRefGoogle Scholar
  59. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627CrossRefPubMedGoogle Scholar
  60. Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN et al (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740CrossRefPubMedGoogle Scholar
  61. Navarrete SA, Menge BA, Daley BA (2000) Species interactions in intertidal food webs: prey or predation regulation of intermediate predators? Ecology 81:2264–2277CrossRefGoogle Scholar
  62. Ostrofsky ML, Zettler ER (1986) Chemical defenses in aquatic plants. J Ecol 74:279–287CrossRefGoogle Scholar
  63. Parker JD (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461CrossRefPubMedGoogle Scholar
  64. Parker IM, Gilbert GS (2007) When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants. Ecology 88:1210–1224CrossRefPubMedGoogle Scholar
  65. Parker JD, Torchin ME, Hufbauer RA, Lemoine NP, Alba C, Blumenthal DM et al (2013) Do invasive species perform better in their new ranges? Ecology 94:985–994CrossRefPubMedGoogle Scholar
  66. Pimm SL (1991) The balance of nature?. University of Chicago Press, ChicagoGoogle Scholar
  67. Polis GA (1991) Complex trophic interactions in deserts: an empirical critique of food-web theory. Am Nat 138:123–155CrossRefGoogle Scholar
  68. Posey M, Powell C, Cahoon L, Lindquist D (1995) Top down vs. bottom up control of benthic community composition on an intertidal tideflat. J Exp Mar Biol Ecol 185:19–31CrossRefGoogle Scholar
  69. Prior KM, Hellmann JJ (2010) Impact of an invasive oak gall wasp on a native butterfly: a test of plant-mediated competition. Ecology 91:3284–3293CrossRefPubMedGoogle Scholar
  70. Prior KM, Hellmann JJ (2013) Does enemy loss cause release? A biogeographical comparison of parasitoid effects on an introduced insect. Ecology 94:1015–1024CrossRefGoogle Scholar
  71. Prior KM, Hellmann JJ (2015) Does enemy release contribute to the success of invasive species? A review of the enemy release hypothesis. In: Keller R, Cadotte M, Sandiford G (eds) Invasive species in a globalized world. University of Chicago Press, ChicagoGoogle Scholar
  72. Pyšek P, Richardson DM, Pergl J, Jarošík V, Sixtová Z, Weber E (2008) Geographical and taxonomic biases in invasion ecology. Trends Ecol Evol 23:237–244CrossRefPubMedGoogle Scholar
  73. Rosenberg MS, Adams DC, Gurevitch, J (2000) MetaWin: statistical software for meta-analysis, Version 2.0. Sinauer Associates, MassachusettsGoogle Scholar
  74. Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  75. Roy HE, Lawson Handley LJ, Schönrogge K, Poland RL, Purse BV (2011) Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? Biocontrol 56:451–468CrossRefGoogle Scholar
  76. Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153CrossRefPubMedGoogle Scholar
  77. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176CrossRefGoogle Scholar
  78. Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B et al (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:785–791CrossRefGoogle Scholar
  79. Shurin JB, Gruner DS, Hillebrand H (2006) All wet or dried up? Real differences between aquatic and terrestrial food webs. Proc R Soc B 273:1–9CrossRefPubMedCentralPubMedGoogle Scholar
  80. Shwartz A, Strubbe D, Butler CJ, Matthysen E, Kark S (2009) The effect of enemy-release and climate conditions on invasive birds: a regional test using the rose-ringed parakeet (Psittacula krameri) as a case study. Divers Distrib 15:310–318CrossRefGoogle Scholar
  81. Sih A (1985) Predation, competition, and prey communities: a review of field experiments. Ann Rev Ecol Syst 16:269–311CrossRefGoogle Scholar
  82. Strong DR (1992) Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–754CrossRefGoogle Scholar
  83. Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, ChicagoGoogle Scholar
  84. Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190CrossRefGoogle Scholar
  85. Torchin ME, Lafferty KD, Kuris AM (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions 3:333–345CrossRefGoogle Scholar
  86. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630CrossRefPubMedGoogle Scholar
  87. Van der Putten WH, Yeates GW, Duyts H, Schreck Reis C, Karssen G (2005) Invasive plants and their escape from root herbivory: a worldwide comparison of the root-feeding nematode communities of the dune grass Ammophila arenaria in natural and introduced ranges. Biol Invasions 7:733–746CrossRefGoogle Scholar
  88. Verhoeven KJF, Biere A, Harvey JA, Van der Putten WH (2009) Plant invaders and their novel natural enemies: Who is naïve? Ecol Lett 12:107–117CrossRefPubMedGoogle Scholar
  89. Vermeij MJA, Smith TB, Dailer ML, Smith CM (2009) Release from native herbivores facilitates the persistence of invasive marine algae: a biogeographical comparison of the relative contribution of nutrients and herbivory to invasion success. Biol Invasions 11:1463–1474CrossRefGoogle Scholar
  90. Vos M, Vet LEM (2004) Geographic variation in host acceptance by an insect parasitoid: genotype versus experience. Evol Ecol Res 6:1021–1035Google Scholar
  91. Williams JL, Auge H, Maron JL (2010) Testing hypotheses for exotic plant success: parallel experiments in the native and introduced ranges. Ecology 91:1355–1366CrossRefPubMedGoogle Scholar
  92. Wootton JT (1992) Indirect effects, prey susceptibility, and habitat selection: impacts of birds on limpets and algae. Ecology 73:981–991CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Kirsten M. Prior
    • 1
    • 2
    Email author
  • Thomas H. Q. Powell
    • 1
    • 3
  • Ashley L. Joseph
    • 1
  • Jessica J. Hellmann
    • 1
  1. 1.Department of Biological SciencesUniversity of Notre DameNotre DameUSA
  2. 2.Department of BiologyUniversity of FloridaGainesvilleUSA
  3. 3.Department of Entomology and NematologyUniversity of FloridaGainesvilleUSA

Personalised recommendations