Invasion ecology is saturated with many hypotheses (Catford, Jansson & Nilsson, 2009). One of these is the Enemy Release Hypothesis (ERH) (Keane & Crawley, 2002), which posits that exotics become more abundant and distributed through relative release: greater natural enemy impact on natives than the exotic, in the introduced range. Despite the intuitive nature of the ERH, evidence for the hypothesis remains equivocal it (Jeschke et al., 2012). To the detriment of the ERH, studies are heavily driven to identify traits of invasiveness (Colautti et al., 2004). Studies have thus been rendered unable to fully explore the ERH. It is concluded that the ERH is in need of long-term exclusion experiments in invaded plant communities to address this issue. Exclusion experiments must be designed to investigate all the assumptions of the ERH, using population dynamics as a measure of enemy impact whilst long-term studies are highly desired to achieve greater certainty in the dynamics observed (Allan & Crawley, 2011).
What is the ERH?
The ERH states that exotic plants can become invasive by experiencing less regulation, than native plants, by enemies in their introduced habitat. This relative release allows the exotic species to increase in abundance and distribution (Keane & Crawley, 2002). Although widely used, the ERH remains a controversial topic in invasion ecology and no general consensus has been established on how to test it (Jeschke et al., 2012). How can such a seemingly simple hypothesis baffle the scientific community for so long? The aim of this literature review is not to debate the place the ERH has in invasion ecology, but to address the issues the ERH is currently facing. It is imperative that a consensus is reached on how to study the ERH, however, so that its viability as a tool in invasion ecology can be established. Ultimately, understanding the processes of invasion is vital to secure global biodiversity, as invasive plant species are regarded as one of the major culprits of global biodiversity loss (Vitousek et al., 1997).
Figure 1. A guide on exploring the assumptions of the ERH. Regulation refers to the regulation of population dynamics. Competitors are the native species in the introduced community. Positive changes in abundance and distribution are true measures of invasiveness.
Exploring the assumptions
The ERH has three assumptions: (1) natural enemies are important in the regulation of plant populations; (2) in the introduced community, the impact of enemies is greater on native plant populations than on exotic populations; and (3) exotic populations capitalise on this relatively lower enemy impact (relative release) through increased abundance and distribution (Keane & Crawley, 2002). When studying the ERH it is vital to incorporate all three assumptions into the experimental design (figure 1), otherwise the study would lack a full analysis of the ERH.
(1) Enemy regulation of plant population dynamics
There is a distinct lack of studies in invasion ecology that investigate how herbivores regulate plant population dynamics. Instead, enemy impact has often been measured by its effect on plant performance. Yet, Crawley (1989) has highlighted that although herbivores may lower the performance of their host plant, there may be no effect on plant population dynamics. The extrapolation of performance to population dynamics is unreliable, as it is highly context specific. For instance, the effects of granivory have no effect on plants whose populations are not seed-limited. More recently, Allan & Crawley (2011) have shown that the exclusion of insects in an English acid mesotrophic grassland decreased total plant species richness from an average of 12.5 species in 4-m2 control plots to 9.4 species (p = 0.019). Holcus mollis, by increasing in abundance, was the only species to benefit from insect exclusion. Therefore, insects regulated the abundance of H. mollis and this had positive effects on other grass species. Although molluscs and vertebrates were also excluded, the study did not aim to exclude all possible natural enemies, such as nematodes and fungal pathogens. These natural enemies could have significant effects on plants (Reinhart et al., 2003 and Callaway et al., 2004). The broad-spectrum nature of fungicides and some pesticides, however, risks upsetting mutualist and commensal interactions above and below the soil. Most illuminating of all, the effects of invertebrate exclusion only became apparent after 8 years (Allan & Crawley, 2011). In future, studies must aim for long-term investigation to ascertain the importance of insect regulation.
Studies of the ERH are short-term, focussing on damage (herbivore damage, attack rate, load and diversity) or performance of plants (usually expressed using population parameters) (Colautti et al., 2004; Liu & Stiling, 2006 and Chun, van Kleunen & Dawson, 2010). For example, a short-term insect exclusion by MacDonald & Kotanen (2010) has investigated the impact of insects on seedling germination and survivorship; and adult survivorship, growth and fecundity on common ragweed (Ambrosia artemisiifolia). They have concluded that natural enemies are likely to be ineffective in controlling common ragweed. As a short-term study, the certainty of their conclusion is doubtful, as previously shown (Allan & Crawley, 2011). Additionally, without linking performance to the population dynamics of the common ragweed, any conclusion on the effectiveness of insects controlling common ragweed is premature. The same can be said for all other short-term, damage and performance driven studies of the ERH.
(2) Relative release
The impact of natural enemies is assumed to be greater on native populations than on exotic populations because natural enemies in the introduced range lack the evolutionary history with which to locate, utilise the resources and tolerate the defences of the exotic. Studies testing the preference of native herbivores for exotics or natives have not found a consistent pattern (Agrawal & Kotanen, 2003; Parker & Gilbert, 2007; Proches et al., 2008; White, Sims & Clarke, 2008; and Parker et al., 2012). As for impact, studies are superficially equivocal (Agrawal & Kotanen, 2003; Cincotta, Adams & Holzapfel, 2009; Chun, van Kleunen & Dawson, 2010 and Jeschke et al., 2012). Unfortunately, population dynamics in response to herbivory were not used as a measure of impact.
(3) Relative release leads to invasiveness
To establish that a species’ invasiveness is caused by the ERH, it is vital to demonstrate that relative enemy release has led to increased abundance and distribution. Keane & Crawley (2002) have proposed an empirical model by which to encompass all assumptions of the ERH. The model proposes that enemy exclusion can be used to measure enemy release (table 1). Since the ERH provides exotic species with a competitive advantage when enemy regulation is relatively lower than natives, there should be no competitive advantage for the exotics when all enemies in the community are excluded. Thus, in an exclusion plot, expect the invasive to have a lower abundance relative to the control plot, if it benefits from ERH.
Table 1. Keane & Crawley’s (2002) empirical model for testing the enemy release hypothesis. Exclosure treatments must exclude all enemies. The abundance of exotic species is compared between control and exclosure treatments. The level of enemy release is determined when the abundance of the exclosure exotic species is subtracted from that of the control exotic species. The role of enemy release in the exotic plant invasion is revealed when the level of enemy release is compared to the abundance of the exotic as found in the introduced community.
Impact in biogeographic and community studies
Over the last decade, studies have not employed the empirical model (table 1). Instead, the usual biogeographic and community studies have persisted (Colautti et al., 2004; DeWalt, Denslow & Ickes, 2004; Genton et al., 2005; Liu & Stiling, 2006; Ebeling, Hensen & Auge, 2008; Adams et al., 2009; Chun, Kleunen & Dawson, 2010; and Jeschke et al., 2012). Biogeographic studies compare native and introduced populations of a species and have the potential to answer: does a species have an intraspecific difference in natural enemy impact in its native and introduced range (Liu & Stiling, 2006)? The intraspecific nature of biogeographic comparisons mean that biotic interactions in the introduced community cannot be studied, thus assumptions 2 and 3 are left unsatisfied. Community studies compare the invasive species to other native species in the introduced community and have the potential to answer: does an invasive species have an interspecific difference in natural enemy impact in its introduced range (Liu & Stiling, 2006)? In the light of the ERH assumptions, it becomes clear that only community studies have the potential to explore them all, because community studies have the potential to explore biotic interactions between the invasive and the species in the introduced community (figure 1).
To date, all ERH studies have been short-term and use population parameters as indicators of impact (Chun, van Kleunen & Dawson, 2010 and Jeschke et al., 2012). A point and a fault much laboured; no matter how intriguing the trait differences may be, whether intraspecific or interspecific, they do not fit in the scheme of the ERH because these traits do not necessarily grant increased abundance and distribution (Crawley, 1989). With respect to intraspecific trait comparison, trait differences may occur due to enemy release or various other competing mechanisms: phenotypic plasticity, founder effects, evolution of increased competitive ability, abiotic factors or a combination of these (Liu & Stiling, 2006). Finally, the use of traits as opposed to population dynamics renders current community studies only able to answer: do invasive species have different traits than native species?
The empirical model
The empirical model (Keane & Crawley, 2002) is able to study the population dynamics of the invasive species and of the native community. Being able to track the population dynamics of the invasive allows one to determine whether the invasive species satisfies assumption 1. Through the use of enemy exclusion, one can determine whether enemy release granted the invasive species a competitive advantage or not, assumption 2. Finally, assumption 3 is determined through the determination of the level of enemy release (table 1) (Keane & Crawley, 2002). However, exclusion treatments must attempt not to interfere with commensals and mutualists (Allan & Crawley, 2011). Exclusion of vertebrates is easily achieved through fencing. However, species-specific pesticides are lacking and so the exclusion of arthropod enemies without non-target influence may be difficult to achieve for some plant communities. Furthermore, exclusion treatments may require almost a decade to illuminate population dynamics (Allan & Crawley, 2011).
The long-term nature of the empirical model is most pressing in a world of rapid globalisation and species loss (Purvis & Hector, 2000). Despite this, future studies in invasion ecology should focus on employing the long-term empirical model because the fruits of its research will aid in determining whether the use of biological control may be feasible on a given invasive, especially when the risks of biological control are not yet fully understood (Simberloff & Siling, 1996). There is no need to risk a community with biological control, if the invasive species is unlikely to be regulated by natural enemies. Ultimately, the empirical model will yield full evaluation of the ERH after which it becomes possible for the invasion ecology community to answer: how useful is the ERH in predicting invasion?
The focus of ERH studies must shift away from intraspecific biogeographic comparisons and the habit of measuring enemy impact using population parameter or other traits. Studies must begin to focus on: long-term community studies of the population dynamics of the invasive and its competitors in response to the inclusion/exclusion of natural enemies. When enough data accrues, the usefulness of the ERH in predicting invasion can finally be determined.
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