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Enemy release hypothesis

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The enemy release hypothesis is among the most widely proposed explanations for the dominance of exotic invasive species. In its native range, a species has co-evolved with pathogens, parasites and predators that limit its population. When it arrives in a new territory, it leaves these old enemies behind, while those in its introduced range are less effective at constraining the introduced species' population. The result is sometimes rampant growth that threatens native species and ecosystems.

Explanations for invasive species success

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Ecologists have identified many potential reasons for the success of invasive species, including higher growth rates or seed production than native species, more aggressive dispersal, tolerance of environmental heterogeneity, more efficient use of resources, and phenological advantages such as an earlier or longer flowering season.[1][2][3] Invasive species may have greater phenotypic plasticity in important traits than their native competitors, allowing them to tolerate more environmental variation,[4] or exhibit the ability to evolve rapidly to adapt to their new conditions.[5] In addition, some habitats, due to disturbances or other factors, may be more vulnerable to invasion than others.[6] Most exotic species do not become invasive,[7] and some authors suggest that those that do represent repeated and larger introductions that generate propagule pressure.[8] Among the many explanations for invasive success, however, the enemy release hypothesis has had the most support.[9]

Enemy release hypothesis

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The enemy release hypothesis (ERH) is most often applied to invasive plants, but there is evidence for its usefulness in other systems, including fish,[10] amphibians,[11] insects,[12] and crustaceans.[13] The ERH assumes that: (1) herbivores, pathogens and parasites suppress plant population growth, (2) these enemies plague native plants more than immigrating non-native species, and (3) non-native plants are able to leverage this advantage into more rapid population growth.[14]

An early study of the flowering plant Silene latifolia found that about 60% of its invasive populations in North America were free from herbivory, while 84% of those in its native Europe exhibited damage from at least one herbivore.[15] A study of almost 500 exotic plant species in the United States found that they were infected by 84% fewer fungi and 24% fewer virus species than in their native ranges.[16] And a meta-analysis covering 15 exotic plant studies found the number of insect herbivores on average to be greater in their native than in their introduced range, with overall damage greater on native plants than on the introduced species.[17]

Support for the theory, however, is not universal.[18] In some cases, native pathogens, parasites and herbivores present significant biotic resistance to potential invasive species,[19][20] as do non-native enemies that may have arrived prior to the exotic plant.[21] Enemy release may be weaker, too, when an exotic species is more closely related to native species in their introduced ranges, making them more likely to share herbivores or pathogens.[22] In a meta-analysis of 19 research studies involving 72 pairs of native and invasive plants, invasive exotic species did not incur less damage than their native counterparts and, in fact, exhibited lower relative growth rates.[23] In other cases, invasive success was due not to release from herbivory but greater tolerance of it.[24]

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The ERH is closely related to two other important theories for invasive species success: the evolution of increased competitive ability (EICA) and novel weapons hypotheses (NWH). EICA asserts that because exotic plants are released from the burden of defending themselves against herbivores in their native range, they evolve to reallocate those resources to traits, such as growth and seed production, that make them more formidable competitors in their introduced range.[25] ERH is an ecological mechanism, while EICA rests on evolutionary adaptation.[26] The experimental support for EICA is mixed.[27] For example, Solidago altissima plants artificially released from herbivory became more competitive against other plant species.[28] However, a meta-analysis of 30 studies that found evidence of evolutionary shifts in introduced species, showed no indication of a trade-off between herbivore defenses and growth.[26]

The novel weapons hypothesis (NWH) is another perspective on the enemy release hypothesis. Some plants evolve chemical defenses to compete in their original range. In their introduced range, the native species are highly vulnerable to these chemicals because they have no prior experience with them, giving the exotic species a competitive advantage.[29][30][31]

Practical applications

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A final argument for the ERH lies in the success of biological control of some invasive species, in which herbivores or other enemies from their native environment are introduced to suppress population growth in their adopted range.[32] For example, when conservationists sought to control the invasive St.-John's-wort (Hypericum perforatum) in North America, they imported a leaf herbivore (Chrysolina quadrigemina) from its native range in Europe.[33]

References

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  1. ^ Estoup, Arnaud; Guillemaud, Thomas (2010-08-13). "Reconstructing routes of invasion using genetic data: why, how and so what?". Molecular Ecology. 19 (19): 4113–4130. Bibcode:2010MolEc..19.4113E. doi:10.1111/j.1365-294X.2010.04773.x. PMID 20723048. S2CID 8242098.
  2. ^ Pysek, Petr; Richardson, David M. (2007). "Traits associated with invasiveness in alient plants: Where do we stand?". In Nentwig, Wolfgang (ed.). Biological invasions. Vol. 193. Nentwig, Wolfgang, 1953-. Berlin: Springer. pp. 97–125. ISBN 978-3-540-36920-2. OCLC 184984594.
  3. ^ van Kleunen, Mark; Weber, Ewald; Fischer, Markus (2010). "A meta-analysis of trait differences between invasive and non-invasive plant species". Ecology Letters. 13 (2): 235–245. doi:10.1111/j.1461-0248.2009.01418.x. PMID 20002494.
  4. ^ Davidson, Amy Michelle; Jennions, Michael; Nicotra, Adrienne B. (2011). "Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis: Invasive species have higher phenotypic plasticity". Ecology Letters. 14 (4): 419–431. doi:10.1111/j.1461-0248.2011.01596.x. PMID 21314880.
  5. ^ Whitney, Kenneth D.; Gabler, Christopher A. (2008-04-15). "Rapid evolution in introduced species, 'invasive traits' and recipient communities: challenges for predicting invasive potential: Evolution and invasion predictions". Diversity and Distributions. 14 (4): 569–580. doi:10.1111/j.1472-4642.2008.00473.x.
  6. ^ Rejmanek, M.; Richardson, David M. (2005). "Plant invasion and the invasibility of plant communities". In Van der Marl, E.; Franklin, J. (eds.). Ecology of invasive plants: state of the art. Oxford, England: Blackwell. pp. 332–355.
  7. ^ Williamson, Mark; Fitter, Alastair (1996). "The Varying Success of Invaders". Ecology. 77 (6): 1661–1666. Bibcode:1996Ecol...77.1661W. doi:10.2307/2265769. JSTOR 2265769.
  8. ^ Simberloff, Daniel (2009). "The Role of Propagule Pressure in Biological Invasions". Annual Review of Ecology, Evolution, and Systematics. 40 (1): 81–102. doi:10.1146/annurev.ecolsys.110308.120304. ISSN 1543-592X. S2CID 85842323.
  9. ^ Flory, S. Luke; Clay, Keith (2013). Thrall, Peter (ed.). "Pathogen accumulation and long‐term dynamics of plant invasions". Journal of Ecology. 101 (3): 607–613. doi:10.1111/1365-2745.12078. ISSN 0022-0477. S2CID 86845671.
  10. ^ Sarabeev, Volodimir; Balbuena, Juan Antonio; Morand, Serge (2017). "Testing the enemy release hypothesis: abundance and distribution patterns of helminth communities in grey mullets (Teleostei: Mugilidae) reveal the success of invasive species". International Journal for Parasitology. 47 (10–11): 687–696. doi:10.1016/j.ijpara.2017.05.006. PMID 28694188.
  11. ^ Marr, Shenandoah R.; Mautz, William J.; Hara, Arnold H. (2008). "Parasite loss and introduced species: a comparison of the parasites of the Puerto Rican tree frog, (Eleutherodactylus coqui), in its native and introduced ranges". Biological Invasions. 10 (8): 1289–1298. Bibcode:2008BiInv..10.1289M. doi:10.1007/s10530-007-9203-0. ISSN 1387-3547. S2CID 43072717.
  12. ^ Aliabadi, Brianna W.; Juliano, Steven A. (2002). "Escape from gregarine parasites affects the competitive interactions of an invasive mosquito". Biological Invasions. 4 (3): 283–297. doi:10.1023/A:1020933705556. PMC 2748405. PMID 19777120.
  13. ^ Torchin, Mark E.; Lafferty, Kevin D.; Kuris, Armand M. (2001). "Release from parasites as natural enemies increased performance of a globally introduced marine crab". Biological Invasions. 3 (4): 333–345. doi:10.1023/A:1015855019360. S2CID 9445764.
  14. ^ Keane, R; Crawley, MJ (2002-04-01). "Exotic plant invasions and the enemy release hypothesis". Trends in Ecology & Evolution. 17 (4): 164–170. doi:10.1016/S0169-5347(02)02499-0.
  15. ^ Wolfe, Lorne M. (2002). "Why Alien Invaders Succeed: Support for the Escape‐from‐Enemy Hypothesis". The American Naturalist. 160 (6): 705–711. doi:10.1086/343872. ISSN 0003-0147. PMID 18707459. S2CID 205984290.
  16. ^ Mitchell, Charles E.; Power, Alison G. (2003). "Release of invasive plants from fungal and viral pathogens". Nature. 421 (6923): 625–627. Bibcode:2003Natur.421..625M. doi:10.1038/nature01317. ISSN 0028-0836. PMID 12571594. S2CID 4320245.
  17. ^ Liu, Hong; Stiling, Peter (2006). "Testing the enemy release hypothesis: a review and meta-analysis". Biological Invasions. 8 (7): 1535–1545. Bibcode:2006BiInv...8.1535L. CiteSeerX 10.1.1.453.9744. doi:10.1007/s10530-005-5845-y. ISSN 1387-3547. S2CID 35919248.
  18. ^ Jeschke, Jonathan; Gómez Aparicio, Lorena; Haider, Sylvia; Heger, Tina; Lortie, Christopher; Pyšek, Petr; Strayer, David (2012-08-22). "Support for major hypotheses in invasion biology is uneven and declining". NeoBiota. 14: 1–20. doi:10.3897/neobiota.14.3435. hdl:10261/56814. ISSN 1314-2488.
  19. ^ Parker, Ingrid M.; Gilbert, Gregory S. (2007). "When there is no escape: The effects of natural enemies on native, invasive and non-invasive plants". Ecology. 88 (5): 1210–1224. Bibcode:2007Ecol...88.1210P. doi:10.1890/06-1377. ISSN 0012-9658. PMID 17536407. S2CID 41013635.
  20. ^ Maron, John L.; Vila, Montserrat (2001). "When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses". Oikos. 95 (3): 361–373. Bibcode:2001Oikos..95..361M. doi:10.1034/j.1600-0706.2001.950301.x. ISSN 0030-1299. S2CID 17449132.
  21. ^ Powell, Kristin I.; Chase, Jonathan M.; Knight, Tiffany M. (2011). "A synthesis of plant invasion effects on biodiversity across spatial scales". American Journal of Botany. 98 (3): 539–548. doi:10.3732/ajb.1000402. PMID 21613145.
  22. ^ Hill, Steven Burton; Kotanen, Peter M. (2009). "Evidence that phylogenetically novel non-indigenous plants experience less herbivory". Oecologia. 161 (3): 581–590. Bibcode:2009Oecol.161..581H. doi:10.1007/s00442-009-1403-0. hdl:1807/73981. ISSN 0029-8549. PMID 19585153. S2CID 12619010.
  23. ^ Chun, Young Jin; Van Kleunen, Mark; Dawson, Wayne (2010-06-10). "The role of enemy release, tolerance and resistance in plant invasions: linking damage to performance: Invasive plants and enemy release". Ecology Letters. 13 (8): 937–46. doi:10.1111/j.1461-0248.2010.01498.x. PMID 20545733.
  24. ^ Ashton, Isabel W.; Lerdau, Manuel T. (2007-10-04). "Tolerance to herbivory, and not resistance, may explain differential success of invasive, naturalized, and native North American temperate vines: Resistance and tolerance of invasive vines". Diversity and Distributions. 14 (2): 169–178. doi:10.1111/j.1472-4642.2007.00425.x. S2CID 83429134.
  25. ^ Blossey, Bernd; Notzold, Rolf (1995). "Evolution of Increased Competitive Ability in Invasive Nonindigenous Plants: A Hypothesis". The Journal of Ecology. 83 (5): 887. Bibcode:1995JEcol..83..887B. doi:10.2307/2261425. JSTOR 2261425. S2CID 15256369.
  26. ^ a b Felker-Quinn, Emmi; Schweitzer, Jennifer A.; Bailey, Joseph K. (2013). "Meta-analysis reveals evolution in invasive plant species but little support for Evolution of Increased Competitive Ability (EICA)". Ecology and Evolution. 3 (3): 739–751. doi:10.1002/ece3.488. PMC 3605860. PMID 23531703.
  27. ^ Joshi, J.; Vrieling, K. (2005-04-28). "The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores: Evolutionary change in invasive ragwort". Ecology Letters. 8 (7): 704–714. doi:10.1111/j.1461-0248.2005.00769.x.
  28. ^ Uesugi, Akane; Kessler, André (2013). "Herbivore exclusion drives the evolution of plant competitiveness via increased allelopathy". New Phytologist. 198 (3): 916–924. doi:10.1111/nph.12172. PMID 23437810.
  29. ^ Callaway, Ragan M.; Ridenour, Wendy M.; Laboski, Trevor; Weir, Tiffany; Vivanco, Jorge M. (2005). "Natural selection for resistance to the allelopathic effects of invasive plants". Journal of Ecology. 93 (3): 576–583. Bibcode:2005JEcol..93..576C. doi:10.1111/j.1365-2745.2005.00994.x. ISSN 0022-0477.
  30. ^ Cappuccino, Naomi; Arnason, J.Thor (2006). "Novel chemistry of invasive exotic plants". Biology Letters. 2 (2): 189–193. doi:10.1098/rsbl.2005.0433. ISSN 1744-9561. PMC 1618907. PMID 17148359.
  31. ^ Inderjit; Callaway, Ragan M.; Vivanco, Jorge M. (2006). "Can plant biochemistry contribute to understanding of invasion ecology?". Trends in Plant Science. 11 (12): 574–580. doi:10.1016/j.tplants.2006.10.004. PMID 17092763.
  32. ^ Clewley, Gary D.; Eschen, René; Shaw, Richard H.; Wright, Denis J. (2012). Sheppard, Andy (ed.). "The effectiveness of classical biological control of invasive plants". Journal of Applied Ecology. 49 (6): 1287–1295. Bibcode:2012JApEc..49.1287C. doi:10.1111/j.1365-2664.2012.02209.x.
  33. ^ DeLoach, C.J. (1997). "Biological control of weeds in the United States and Canada". In Luken, James O.; Thieret, John W. (eds.). Assessment and Management of Plant Invasions. New York: Springer New York. pp. 172–194. ISBN 978-1-4612-1926-2. OCLC 840278263.
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