Herbivory of an invasive slug is affected by earthworms and the composition of plant communities

Abstract

BackgroundBiodiversity loss and species invasions are among the most important human-induced global changes. Moreover, these two processes are interlinked as ecosystem invasibility is considered to increase with decreasing biodiversity. In temperate grasslands, earthworms serve as important ecosystem engineers making up the majority of soil faunal biomass. Herbivore behaviour has been shown to be affected by earthworms, however it is unclear whether these effects differ with the composition of plant communities. To test this we conducted a mesocosm experiment where we added earthworms (Annelida: Lumbricidae) to planted grassland communities with different plant species composition (3 vs. 12 plant spp.). Plant communities had equal plant densities and ratios of the functional groups grasses, non-leguminous forbs and legumes. Later, Arion vulgaris slugs (formerly known as A. lusitanicus; Gastropoda: Arionidae) were added and allowed to freely choose among the available plant species. This slug species is listed among the 100 worst alien species in Europe. We hypothesized that (i) the food choice of slugs would be altered by earthworms’ specific effects on the growth and nutrient content of plant species, (ii) slug herbivory will be less affected by earthworms in plant communities containing more plant species than in those with fewer plant species because of a more readily utilization of plant resources making the impacts of earthworms less pronounced.ResultsSlug herbivory was significantly affected by both earthworms and plant species composition. Slugs damaged 60% less leaves when earthworms were present, regardless of the species composition of the plant communities. Percent leaf area consumed by slugs was 40% lower in communities containing 12 plant species; in communities containing only three species earthworms increased slug leaf area consumption. Grasses were generally avoided by slugs. Leaf length and number of tillers was increased in mesocosms containing more plant species but little influenced by earthworms. Overall shoot biomass was decreased, root biomass increased in plant communities with more plant species. Earthworms decreased total shoot biomass in mesocosms with more plant species but did not affect biomass production of individual functional groups. Plant nitrogen concentrations across three focus species were 18% higher when earthworms were present; composition of plant communities did not affect plant quality.ConclusionsGiven the important role that both herbivores and earthworms play in structuring plant communities the implications of belowground-aboveground linkages should more broadly be considered when investigating global change effects on ecosystems.

Misperceived invasion: theLusitanian slug (Arion lusitanicusauct. non‐Mabille orArion vulgarisMoquin‐Tandon 1855) is native toCentralEurope

“…Moreover, the species is used to test predictions on invasive species success, for example, regarding phenotypic plasticity (Knop and Reusser ) and diet choice (Zaller et al. ) or as an example of their impact (e.g. Blattmann et al.…”

“…Moss and Hermanutz 2010) or even eradication efforts crucially depend on whether a species is introduced or native (see respective paragraphs in, e.g., the Convention on Biological Diversity or the Convention on Migratory Species of Wild Animals). Moreover, the species is used to test predictions on invasive species success, for example, regarding phenotypic plasticity (Knop and Reusser 2012) and diet choice (Zaller et al 2013) or as an example of their impact (e.g. Blattmann et al 2013), which is questionable given the presented results.…”

Demographic responses of rare forest plants to multiple stressors: the role of deer, invasive species and nutrients

“…Zaller et al . () found that slug herbivory is affected by an interaction between earthworms and plant diversity. Plant communities varied across our study sites and were affected by earthworm abundance (A. Dávalos, V. Nuzzo & B. Blossey, unpubl.…”

“…Once again (see results for non-native plant and slug interaction on Agrimonia survival), we found that slug presence had a positive effect on survival in more stressful conditions only, in this case at low earthworm abundance sites (earthworms have a positive effect on Agrimonia). Zaller et al (2013) found that slug herbivory is affected by an interaction between earthworms and plant diversity. Plant communities varied across our study sites and were affected by earthworm abundance (A.…”

The role of invertebrates in seedling establishment in a heterocarpic plant, Atriplex sagittata

“…This species exhibits superior mobility (Honek & Martinkova, ; Knop et al, ) and is well adapted to warm and dry microclimates (Knop & Reusser, ); consequently, it survives well on farmland (Ryser et al, ). The presence of populations of this slug on degraded areas (construction sites, roadside margins) that are typical A. sagittata habitats is supplied by emigrants from near grassy sites (Honek & Martinkova, ) and might be favoured due to an impoverishment of the soil fauna (Zaller et al, ). The consequences of recent A. vulgaris invasion increase the risk of death for A. sagittata .…”