Reciprocally beneficial interactions between introduced plants and ants are induced by the presence of a third introduced species

Abstract

Interspecific interactions play an important role in the success of introduced species. For example, the ‘enemy release’ hypothesis posits that introduced species become invasive because they escape top–down regulation by natural enemies while the ‘invasional meltdown’ hypothesis posits that invasions may be facilitated by synergistic interactions between introduced species. Here, we explore how facilitation and enemy release interact to moderate the potential effect of a large category of positive interactions – protection mutualisms. We use the interactions between an introduced plant (Japanese knotweed Fallopia japonica), an introduced herbivore (Japanese beetle Popillia japonica), an introduced ant (European red ant Myrmica rubra), and native ants and herbivores in riparian zones of the northeastern United States as a model system. Japanese knotweed produces sugary extrafloral nectar that is attractive to ants, and we show that both sugar reward production and ant attendance increase when plants experience a level of leaf damage that is typical in the plants’ native range. Using manipulative experiments at six sites, we demonstrate low levels of ant patrolling, little effect of ants on herbivory rates, and low herbivore pressure during midsummer. Herbivory rates and the capacity of ants to protect plants (as evidenced by effects of ant exclusion) increased significantly when plants were exposed to introduced Japanese beetles that attack plants in the late summer. Beetles were also associated with greater on‐plant foraging by ants, and among‐plant differences in ant‐foraging were correlated with the magnitude of damage inflicted on plants by the beetles. Last, we found that sites occupied by introduced M. rubra ants almost invariably included Japanese knotweed. Thus, underlying variation in the spatiotemporal distribution of the introduced herbivore influences the provision of benefits to the introduced plant and to the introduced ant. More specifically, the presence of the introduced herbivore converts an otherwise weak interaction between two introduced species into a reciprocally beneficial mutualism. Because the prospects for facilitation are linked to the prospects for enemy release in protection mutualisms, species introductions can have complex effects on existing species interactions, between both native and introduced species.

Novel plant–insect interactions in an urban environment: enemies, protectors, and pollinators of invasive knotweeds

“…These EFN produce nectar rich in fructose and glucose during early-season development and in response to herbivory. Ness et al (2013) observed ant-plant interactions between Fallopia japonica in its invasive range and the likewise invasive Eurasian ant Myrmica rubra, which protected F. japonica in response to P. japonica herbivory in the northeastern United States. Increased EFN production and associated increase in ant patrolling have been observed in Fallopia japonica following leaf damage by herbivory (Kawano et al 1999, Ness et al 2013, indicating a link between nectar rewards and protection in this relationship.…”

“…Ant foragers attracted to this nectar have been shown to strongly react to and chase away herbivores (Kawano et al 1999, Ness et al 2013. These EFN produce nectar rich in fructose and glucose during early-season development and in response to herbivory.…”

“…Where the invasive ranges of these species overlap in North America, it is an herbivore of Fallopia spp. (Fleming 1976, Ness et al 2013. P. japonica has re-established its relation to Fallopia taxa as a natural enemy in their overlapping invasive range.…”

The community ecology of invasive species: where are we and what's next?

“…Many introduced species rely on multi‐trophic mutualisms in their new habitats to become naturalized (Traveset and Richardson ). Mutualisms can be important at all stages of the introduction‐naturalization‐invasion continuum: 1) for establishment via symbioses between plant roots and microbiota (Pringle et al , Dickie et al , Rodríguez‐Echeverría , Bennett ) or plant–ant protection (Ness et al ), 2) for reproduction via animal‐mediated pollination (Burns et al ), and 3) for dispersal via animal seed dispersers (Sun et al , Traveset and Richardson ). Invasive species may also benefit from predator or parasite release in the invaded ranges (Van Kleunen et al , Hill and Kotanen , but see Levine et al ), or compete with the native species via the sharing of mutualistic partners (Burns et al , Gibson et al ).…”

Mutualism between co-introduced species facilitates invasion and alters plant community structure

“…Myrmica rubra occurs in various habitats, including forests, nesting at the roots of plants, in soil and within rotten wood [40]. Although M. rubra is considered invasive because of its dense populations and painful sting [34,40], little is known about its ecological effects in its introduced ranges (except see [45]). …”