Can the enemy release hypothesis explain the success of Rumex (Polygonaceae) species in an introduced range?

Abstract

The enemy release hypothesis states that introduced plants have a competitive advantage due to their release from co-evolved natural enemies (i.e., herbivores and pathogens), which allows them to spread rapidly in new environments. This hypothesis has received mixed support to date, but previous studies have rarely examined the herbivore community, plant damage, and performance simultaneously and largely ignored below-ground herbivores. We tested for enemy release by conducting large scale field surveys of insect diversity and abundance in both the native (United Kingdom) and introduced (New Zealand) ranges of three dock (Rumex, Polygonaceae) species: R. conglomeratus Murray (clustered dock), R. crispus L. (curly dock) and R. obtusifolius L. (broad-leaved dock). We captured both above- and below-ground insect herbivores, measured herbivore damage, and plant biomass as an indicator for performance. In the introduced range, Rumex plants had a lower diversity of insect herbivores, all insect specialists present in the native range were absent and plants had lower levels of herbivore damage on both roots and leaves. Despite this, only R. crispus had greater fresh weight in the introduced range compared to the native range. This suggests that enemy release, particularly from below-ground herbivores, could be a driver for the success of R. crispus plants in New Zealand, but not for R. conglomeratus and R. obtusifolius.

Invertebrate herbivory damage of lowland plant species decreases after an experimental shift to higher altitudes

“…These results hold in comparison to control measurements of herbivory damage in plants naturally growing in both the lowland and the highland which revealed no significant difference in natural herbivory between the two altitudes. Our results thus provide support for the enemy release hypothesis (Costan et al, 2022; Kambo & Kotanen, 2014) in a new context, specifically as a potential mechanism facilitating the uphill shift of plants induced by climate change.…”

“…Two main mechanisms of enemy release have been documented. First, a plant can escape its specialised herbivores which occur in its native range but not in the invasive range (Keane & Crawley, 2002; Costan et al, 2022). It can still be consumed by generalised herbivores, but the overall herbivory damage is reduced because of the absence of specialised herbivores.…”

“…Causes and ecological consequences of the spread of plants to new geographic regions were studied mostly in invasive exotic species (Vilà et al, 2009; Simberloff et al, 2013). According to the enemy release hypothesis, their spread to new areas can be facilitated by the reduction of damage caused by herbivores or pathogens because the plants escape specialized natural enemies occurring in their native range (Kambo & Kotanen, 2014; Keane & Crawley, 2002; Costan et al, 2022). Herbivores attacking the exotic plants in their invasive range are usually generalists which may not be adapted to cope with chemical defences of the exotic plants (Cappuccino & Carpenter, 2005; Enge et al, 2012).…”

“…The main difference compared to invasive exotic species, which come from distant regions, is that mountain communities often contain species which are phylogenetically closely related to plants coming from the lowland. This raises the question whether the shifts of lowland plants to higher altitudes may be facilitated by reduced herbivory as observed in invasive exotic species (Kambo & Kotanen, 2014; Keane & Crawley, 2002; Costan et al, 2022). In addition, the abundance and activity of generalist herbivorous invertebrates often decreases with increasing elevation because of less favourable climate compared to the lowlands (Scheidel & Bruelheide, 2001; Scheidel et al, 2003; Moreira et al, 2017), which may result in lower herbivory damage at higher elevations (Reynolds & Crossley, 1997; Scheidel et al, 2003; Pellisier et al, 2014; Galmán et al, 2018).…”

Transgenerational herbivory effects on performance of clonal offspring of the invasive plant Alternanthera philoxeroides

“…The enemy release hypothesis (ERH) postulates that the rapid adaptation and competitive advantage of many alien species in invasive ranges can be attributed to the absence of coevolved native enemies, which greatly contributes to their invasion potential (Keane and Crawley 2002). This hypothesis, despite some supports (e.g., Lucero et al 2019;Xu et al 2021;Costan et al 2022), has also been challenged (Colautti et al 2004; Mitchell et al 2006;Liu and Stiling 2006;Meijer et al 2016). For instance, the performance of alien species may still be heavily in uenced by local herbivores in the invasive ranges after new plant-herbivore relationships have been established (Colautti et al 2004;Chun et al 2010).…”