Introduction
The enemy release hypothesis (ERH) is the most well-known hypothesis in invasion biology (Enders et al. 2018) and is frequently invoked to explain the success of exotic species in their non-native range (Mitchell & Power 2003; Torchin et al . 2003; Connolly et al. 2014). According to the ERH, invaders can leave their natural enemies behind when introduced beyond their home range, releasing them from enemy regulation and consequently enabling increased growth, reproduction, or survival in their invaded range (Keane & Crawley 2002; Prior et al. 2015; Mlynarek et al. 2017). The ERH has an intuitive mechanistic basis, seemingly straightforward tests and direct link with biosecurity and invasive species management. For example, when the ERH holds true, introduced specialist biocontrol agents can be a way of controlling populations of invasive species (Clewley et al.2012; Walsh et al. 2023). However, using the ERH to effectively prioritise or guide management requires identifying invasions (or potential future invaders) that have been (or may be) facilitated by enemy release.
Not all exotic species show evidence for the ERH or will benefit from enemy release, but it is currently unclear why some exotics benefit while others do not. For example, Reinhert et al. (2003) and te Beest et al. (2009) tested belowground enemy release with nearly identical experimental designs (though with different exotic species). The two studies reached opposite conclusions: Reinhert et al.(2003) showed that release from belowground pathogens promoted exotic success, while te Beest et al. (2009) found no release from soil-borne enemies. The context in which a test is carried out could explain why the occurrence or strength of enemy release can vary between studies (Catford et al. 2022; Chiuffo et al. 2022). However, relevant contexts are rarely reported in ERH studies, leaving no clear path for synthesising circumstances where enemy release promotes exotic success and potential invasive impacts. It is thus not possible to surmise why the exotic species in the Reinhert et al.(2003) study benefitted from enemy release while those examined by te Beest et al. (2009) did not. Individual contexts have previously been predicted to be important in determining the likelihood and strength of enemy release, such as resource levels (Blumenthal 2006), time since introduction (Hawkes 2007) or phylogenetic relatedness of exotic and native species (Mitchell et al. 2006). However, an overarching framework for integrating these contexts is absent, hampering effective predictions of when and how enemy release may affect invasion success (see inconsistencies in Table S1).
We propose a new framework for the ERH (Fig. 1). Our framework emphasises exotic performance as the key outcome of the ERH, explicitly linking enemy release with the relative success of exotic populations. We introduce three component factors – enemy diversity, enemy impact, and host adaptation – that influence exotic performance. We then show how effects of these factors are modulated by seven key ecological contexts: (i) time since introduction; (ii) resource availability; (iii) phylogenetic relatedness of exotic and native species; (iv) host-enemy asynchronicity; (v) number of introduction events; (vi) type of enemy; and (vii) the strength of growth-defence trade-offs. In later sections we outline three ways in which current understandings of the ERH are improved by our framework and provide recommendations to guide data collection and documentation when testing the ERH. Other frameworks have been suggested that propose splitting the ERH into sub-hypotheses (e.g. Schulz et al. 2019) or splitting the ERH according to how it is tested (e.g. Heger & Jeschke 2014). These frameworks ably highlight the complexity of the ERH. However, they do not attempt to propose the circumstances where one sub-hypothesis should be more likely than another, or why different tests may come to different conclusions. In contrast, by considering how factors interact with specific contexts, we provide a more mechanistic understanding of observed patterns. Our framework aids the prediction of circumstances when enemy release may facilitate invasion and assists effective synthesis of studies testing the ERH.