Herbivory of an invasive slug in a model grassland community can be affected by earthworms and mycorrhizal fungi

Abstract

Invasion of non-native species is among the top threats for the biodiversity and functioning of native and agricultural ecosystems worldwide. We investigated whether the herbivory of the slug Arion vulgaris (formerly Arion lusitanicus; Gastropoda), that is listed among the 100 worst alien species in Europe, is affected by soil organisms commonly present in terrestrial ecosystems (i.e. earthworms—Annelida: Lumbricidae and arbuscular mycorrhizal fungi—AMF, Glomerales). We hypothesized that slug herbivory would be affected by soil organisms via altered plant nutrient availability and plant quality. In a greenhouse experiment, we created a simple plant community consisting of a grass, a forb, and a legume species and inoculated these systems with either two earthworm species and/or four AMF taxa. Slugs were introduced after plants were established. Earthworms significantly reduced total slug herbivory in AMF-inoculated plant communities (P = 0.013). Across plant species, earthworms increased leaf total N and secondary metabolites, AMF decreased leaf thickness. Mycorrhizae induced a shift in slug feeding preference from non-legumes to legumes; the grass was generally avoided by slugs. AMF effects on legume herbivory can partly be explained by the AMF-induced increase in total N and decrease in C/N ratio; earthworm effects are less clear as no worm-induced alterations of legume plant chemistry were observed. The presence of earthworms increased average AMF colonization of plant roots by 140 % (P < 0.001). Total shoot mass was significantly increased by AMF (P < 0.001). These data suggest that the feeding behavior of this invasive slug is altered by a belowground control of plant chemical quality and community structure.

Glyphosate-based herbicides reduce the activity and reproduction of earthworms and lead to increased soil nutrient concentrations

“…First, the role of earthworms as important ecological engineers in agroecosystems and gardens can be compromised 10 . Reductions in mixing of organic litter within the soil will limit long-term soil microbial activity 9 , effects of earthworms on aboveground herbivores 37 38 39 , soil nutrient cycling and availability, all of which may lead to reductions in plant productivity 40 . Second, pulses of nitrate and phosphate availability following herbicide application could increase the risk of leaching or surface runoff of these nutrients into groundwater systems or adjacent aquatic ecosystems, as long as the crop cover is not yet re-established.…”

Earthworms affect plant growth and resistance against herbivores: A meta‐analysis

“…We found that the effects of earthworms on growth and resistance of plants under herbivory were overall negatively correlated ( Figure 4a), as would be predicted by classic plant defence theory (Herms & Mattson, 1992;Züst & Agrawal, 2017). An increasing number of studies indicate that earthworms could indirectly influence the performance of herbivores such as phloem-feeders by predominantly affecting plant size, vigour and nutrient content (Eisenhauer & Scheu, 2008;Scheu et al, 1999;Trouve et al, 2014), and to a lesser extent by changes in plant secondary chemistry (Francis, Lognay, Wathelet, & Haubruge, 2001;Katsanis, Rasmann, & Mooney, 2016;. For example, Cao et al (2016) showed that the green peach aphid (Myzus persicae) performed better on an enhanced amino acid:…”

“…In addition to these proven growth-promoting effects (e.g. van Groenigen et al, 2014), recent studies have highlighted that earthworms can also benefit plants by increasing their ability to resist herbivore attacks (Lohmann, Scheu, & Muller, 2009;Trouve, Drapela, Frank, Hadacek, & Zaller, 2014;Wurst, 2013;Wurst, Allema, Duyts, & Van Der Putten, 2008).…”

Occurrence of the invasive Spanish slug in gardens: can a citizen science approach help deciphering underlying factors?

“…Additionally, the time of day [ 25 , 26 ] and the availability of suitable shelters affect slug activity [ 25 , 27 ]. Some studies also observed that earthworms [ 28 , 29 ] or plant diversity [ 30 ] affected the extent of herbivory by slugs.…”