Enemy Release Hypothesis

The enemy release hypothesis (ERH) is a central biogeographical and community-level mechanism in invasion ecology proposing that plant, animal, or microbial species translocated across geographic barriers into an exotic range leave behind the majority of their co-evolved natural enemies—particularly host-specific specialist herbivores, parasitoids, viral and fungal pathogens, and helminth parasites—and therefore experience a demographic release from top-down consumer regulation that enables rapid population expansion and competitive dominance over native species. First articulated qualitatively by Charles Darwin (1859) and Charles S. Elton in The Ecology of Invasions by Animals and Plants (1958), and formalized into testable predictions by Ryan M. Keane and Michael J. Crawley (2002), Charles E. Mitchell and Alison G. Power (2003), and Mark E. Torchin et al. (2003), the enemy release hypothesis provides the theoretical foundation for both classical biological control (re-associating an invasive pest with its co-evolved specialist enemies from its native home range) and the Evolution of Increased Competitive Ability (EICA) hypothesis (Blossey & Nötzold, 1995; Keane & Crawley, 2002; Liu & Stiling, 2006).

As formalized by Keane & Crawley (2002), the enemy release hypothesis rests on three testable ecological premises that must hold simultaneously in the introduced range:

1. Natural Enemies Strongly Regulate Plant and Animal Populations: Herbivores, seed predators, parasitoids, and pathogens significantly depress per-capita survival, somatic growth rate, or lifetime fecundity (R₀) in terrestrial and aquatic food webs.
2. Coevolved Specialist Enemies Are Absent in the Introduced Range: During long-distance human-mediated transport (often as a small bottlenecked founder cohort of dry seeds, ballast-water larvae, or dormant eggs), an introduced species leaves behind its native monophagous and oligophagous specialists—both because small founder stages rarely harbor all native parasite taxa ("parasite sampling bottleneck") and because parasites requiring complex multi-host life cycles cannot complete transmission in the new habitat (Torchin et al., 2003).
3. Resident Generalist Enemies Impact Native Competitors More Heavily Than Exotic Invaders: While native polyphagous generalists in the recipient community (such as mammalian browsers, generalist grasshoppers, or broad-host-range soil oomycetes) can attack both native and exotic species, they typically inflict greater per-capita damage on familiar native hosts than on evolutionarily novel invaders whose secondary metabolites or phenology they have not adapted to detoxify.

Mathematically, if native species N and exotic invader I compete for a shared limiting resource R while suffering mortality from specialist enemies (E_spec) and generalist enemies (E_gen), the per-capita net growth rate of species i is:

dN_i / (N_i dt) = f_i(R) − m_0,i − a_spec,i E_spec,i − a_gen,i E_gen

In the native range, a_spec,I E_spec,I > 0 holds the invader's equilibrium resource requirement R_I^* (see Resource-Ratio Hypothesis) at a moderate value consistent with coexistence. Upon translocation to the exotic range where E_spec,I = 0 and a_gen,I ≤ a_gen,N, the invader's total mortality rate drops sharply, lowering its effective break-even resource requirement (R_I,exotic^* < R_N^*) and allowing it to draw down ambient resources or overtop native competitors (Keane & Crawley, 2002; Shea & Chesson, 2002).

Ecological tests of enemy release are divided into biogeographical comparisons (comparing enemy richness and damage on the same species between its native home range and its invaded range) and community comparisons (comparing enemy damage on an invasive species vs. co-occurring native congeneric species within the same recipient habitat; Colautti et al., 2004):

When an invasive population remains free of co-evolved specialist herbivores over tens to hundreds of generations, natural selection reshapes its secondary metabolic allocation:

1. Evolution of Increased Competitive Ability (EICA Hypothesis, Blossey & Nötzold, 1995): Formulated originally for purple loosestrife (Lythrum salicaria) invading North American wetlands, EICA predicts that because constitutive chemical and physical defenses against specialist enemies (such as tannins, glucosinolates, furanocoumarins, and trichomes) are metabolically expensive to synthesize, natural selection in an enemy-free exotic range favors genotypes that downregulate costly anti-herbivore defenses and reallocate carbon and nitrogen into rapid vegetative growth, taller stature, and higher seed output. Common-garden experiments confirm that invasive North American genotypes of Lythrum salicaria and Chinese tallow tree (Triadica sebifera, Siemann & Rogers, 2001) grow larger and produce more seeds than native Eurasian genotypes, but are poorly defended when re-exposed to native specialist beetles (Galerucella).
2. The Shifting Defense Hypothesis (SDH, Müller-Schärer et al., 2004; Doorduin & Vrieling, 2011): Refines EICA by distinguishing between qualitative toxins (cheap, low-molecular-weight alkaloids, pyrrolizidine alkaloids, and glucosinolates that deter non-adapted generalist herbivores, which specialist insects use as oviposition cues) and quantitative digestibility reducers (expensive, high-concentration tannins, lignins, and proteinase inhibitors needed to slow down co-adapted specialists). SDH predicts that invasive plants in their new range reduce expensive anti-specialist digestibility reducers while increasing cheap qualitative toxins to repel resident generalists—verified in invasive ragwort (Jacobaea vulgaris) and garlic mustard (Alliaria petiolata).
3. Synergy with the Novel Weapons Hypothesis (Callaway & Ridenour, 2004) and Biotic Resistance (Parker et al., 2006): Whereas the Novel Weapons Hypothesis explains how root exudates mediating allelopathy (such as 8-hydroxyquinoline or catechin in Centaurea knapweeds and sinigrin in Alliaria petiolata) disrupt naive native mycorrhizal fungi and competitors, Biotic Resistance occurs in the opposite case where an introduced species encounters a voracious native generalist herbivore (such as North American beavers, crayfish, or native caterpillars) against which it lacks evolutionary defenses—explaining why many introduced plants fail to become invasive. Finally, over 100 to 300 years of residence time, native herbivores and pathogens gradually adapt to host-shift onto the invader (pathogen accumulation, Hawkes, 2007; Mitchell et al., 2010), slowly eroding the initial enemy release advantage.

1. Blossey, B., & Nötzold, R. (1995). Evolution of increased competitive ability in invasive nonindigenous plants: A hypothesis. Journal of Ecology, 83(5), 887–889. https://doi.org/10.2307/2261425
2. Keane, R. M., & Crawley, M. J. (2002). Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution, 17(4), 164–170. https://doi.org/10.1016/S0169-5347(02)02499-002499-0)
3. Mitchell, C. E., & Power, A. G. (2003). Release of invasive plants from fungal and viral pathogens. Nature, 421(6923), 625–627. https://doi.org/10.1038/nature01317
4. Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J., & Kuris, A. M. (2003). Introduced species and their missing parasites. Nature, 421(6923), 628–630. https://doi.org/10.1038/nature01346
5. Colautti, R. I., Ricciardi, A., Grigorovich, I. A., & MacIsaac, H. J. (2004). Is invasion success explained by the enemy release hypothesis? Ecology Letters, 7(8), 721–733. https://doi.org/10.1111/j.1461-0248.2004.00616.x
6. Liu, H., & Stiling, P. (2006). Testing the enemy release hypothesis: A review and meta-analysis. Biological Invasions, 8(7), 1535–1545. https://doi.org/10.1007/s10530-005-5845-y
7. Doorduin, L. J., & Vrieling, K. (2011). A review of the phytochemical support for the shifting defence hypothesis. Phytochemistry Reviews, 10(1), 99–106. https://doi.org/10.1007/s11101-010-9195-8