Abstract
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.
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References
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
Atlegrim O (1998) Exclusion of birds from bilberry stands: impact on insect larval density and damage to the bilberry. Oecologia 7:136–139
Bach CE (1994) Effects of a specialist herbivore (Altica suplicata) on Salix cordata and sand dune succession. Ecol Monogr 64:423–445
Barton AM (1986) Spatial variation in the effect of ants on an extrafloral nectary plant. Ecology 67:495–504
Bigger DS, Marvier MA (1999) How different would a world without herbivory be? A search for generality in ecology. Integr Biol 1:60–67
Blossey B, Nötzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants—a hypothesis. J Ecol 83:887–889
Blumenthal D (2006) Interactions between resource availability and enemy release in Plant invasion. Ecol Lett 9:887–895
Blumenthal D, Mitchell CE, Pysek P, Jarosik V (2009) Synergy between pathogen release and resource availability in plant invasion. Proc Natl Acad Sci USA 106:7899–7904
Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733
Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Lett 1:435–438
Carlsson NO, Sarnelle O, Strayer DL (2009) Native predators and exotic prey –an acquired taste? Front Ecol Environ 7:525–532
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:e4929
Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Earlbaum Associates, New Jersey
Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558
Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733
Cornelissen T, Stiling P (2006) Responses of different herbivore guilds to nutrient addition and natural enemy exclusion. Ecoscience 13:66–74
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 141:847–865
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 33:2107–2119
D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Syst 23:63–87
DeBach P, Rosen D (1991) Biological control by natural enemies. University Press, Cambridge
DeWalt SJ, Denslow JS, Ickes K (2004) Natural enemy release facilitates habitat expansion of the invasive tropical shrub, Clidemia hirta. Ecology 85:471–483
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 87:1915–1924
Ebeling SK, Hensen I, Auge H (2008) The invasive shrub Buddleja davidii performs better in its introduced range. Divers Distrib 14:225–233
Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London
Flecker AS (1992) Fish trophic guilds and the structure of a tropical stream: weak direct vs. strong indirect effects. Ecology 73:927
Floyd T (1996) Top-down impacts on Creosotebush herbivores in a spatially and temporally complex environment. Ecology 77:1544–1555
Forslund H, Wikström SA, Pavia H (2010) Higher resistance to herbivory in introduced compared to native populations of a seaweed. Oecologia 164:833–840
Fretwell SD (1977) Regulation of plant communities by food-chain exploiting them. Perspect Biol Med 20:169–185
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 146:404–414
Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80:1142–1149
Gurevitch J, Fox GA, Wardle GM, Inderjit, Taub D (2011) Emergent insights from synthesis of conceptual frameworks for biological invasions. Eco Lett 14:407–418
Haag JJ, Coupe MD, Cahill JF (2004) Antagonistic interactions between competition and insect herbivory on plant growth. J Ecol 92:156–167
Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421
Halaj J, Wise DH (2001) Terrestrial trophic cascades: how much do they trickle? Am Nat 157:262–281
Hay ME (1991) Marine-terrestrial contrasts in the ecology of plant chemical defenses against herbivores. Trends Ecol Evol 6:362–365
Heger T, Jeschke JM (2014) The enemy release hypothesis as a hierarchy of hypotheses. Oikos 123:741–750
Hellmann JJ, Prior KM, Pelini SL (2012) The influence of species interactions on geographic range change under climate change. Ann NY Acad Sci 1249:18–28
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
Ho CK, Pennings SC (2008) Consequences of omnivory for trophic interactions on a marsh shrub. Ecol 89:1714–1722
Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258
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 84:2108–2118
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 73:724–732
Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528
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 14:1–20
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 111:4501–4506
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 1:199–204
Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989
Lewis SM (1986) The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol Monogr 56:183–200
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 89:475–484
Lodge DM (1991) Herbivory on freshwater macrophytes. Aquat Bot 41:195–224
Lodge DM, Kershner MW, Aloi JE, Covich AP (1994) Effects of an omnivorous crayfish (Orconectes rusticus) on a freshwater littoral food web. Ecology 75:1265–1281
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 162:977–986
Maron JL, Vila M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373
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 21:213–222
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 33:413–421
Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757
Miller TEX (2008) Bottom-up, top-down, and within-trophic level pressures on a cactus-feeding insect. Ecol Entomol 33:261–268
Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627
Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN et al (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740
Navarrete SA, Menge BA, Daley BA (2000) Species interactions in intertidal food webs: prey or predation regulation of intermediate predators? Ecology 81:2264–2277
Ostrofsky ML, Zettler ER (1986) Chemical defenses in aquatic plants. J Ecol 74:279–287
Parker JD (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461
Parker IM, Gilbert GS (2007) When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants. Ecology 88:1210–1224
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 94:985–994
Pimm SL (1991) The balance of nature?. University of Chicago Press, Chicago
Polis GA (1991) Complex trophic interactions in deserts: an empirical critique of food-web theory. Am Nat 138:123–155
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 185:19–31
Prior KM, Hellmann JJ (2010) Impact of an invasive oak gall wasp on a native butterfly: a test of plant-mediated competition. Ecology 91:3284–3293
Prior KM, Hellmann JJ (2013) Does enemy loss cause release? A biogeographical comparison of parasitoid effects on an introduced insect. Ecology 94:1015–1024
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, Chicago
Pyšek P, Richardson DM, Pergl J, Jarošík V, Sixtová Z, Weber E (2008) Geographical and taxonomic biases in invasion ecology. Trends Ecol Evol 23:237–244
Rosenberg MS, Adams DC, Gurevitch, J (2000) MetaWin: statistical software for meta-analysis, Version 2.0. Sinauer Associates, Massachusetts
Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge
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 56:451–468
Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176
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 5:785–791
Shurin JB, Gruner DS, Hillebrand H (2006) All wet or dried up? Real differences between aquatic and terrestrial food webs. Proc R Soc B 273:1–9
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 15:310–318
Sih A (1985) Predation, competition, and prey communities: a review of field experiments. Ann Rev Ecol Syst 16:269–311
Strong DR (1992) Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–754
Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago
Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190
Torchin ME, Lafferty KD, Kuris AM (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions 3:333–345
Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630
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 7:733–746
Verhoeven KJF, Biere A, Harvey JA, Van der Putten WH (2009) Plant invaders and their novel natural enemies: Who is naïve? Ecol Lett 12:107–117
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 11:1463–1474
Vos M, Vet LEM (2004) Geographic variation in host acceptance by an insect parasitoid: genotype versus experience. Evol Ecol Res 6:1021–1035
Williams JL, Auge H, Maron JL (2010) Testing hypotheses for exotic plant success: parallel experiments in the native and introduced ranges. Ecology 91:1355–1366
Wootton JT (1992) Indirect effects, prey susceptibility, and habitat selection: impacts of birds on limpets and algae. Ecology 73:981–991
Acknowledgments
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.
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Prior, K.M., Powell, T.H.Q., Joseph, A.L. et al. Insights from community ecology into the role of enemy release in causing invasion success: the importance of native enemy effects. Biol Invasions 17, 1283–1297 (2015). https://doi.org/10.1007/s10530-014-0800-4
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DOI: https://doi.org/10.1007/s10530-014-0800-4