Gastropod Seed Dispersal: An Invasive Slug Destroys Far More Seeds in Its Gut than Native Gastropods

Seed dispersal is one of the most important mechanisms shaping biodiversity, and animals are one of the key dispersal vectors. Animal seed dispersal can directly or indirectly be altered by invasive organisms through the establishment of new or the disruption of existing seed dispersal interactions. So far it is known for a few gastropod species that they ingest and defecate viable plant seeds and consequently act as seed dispersers, referred to as gastropodochory. In a multi-species experiment, consisting of five different plant species and four different gastropod species, we tested with a fully crossed design whether gastropodochory is a general mechanism across native gastropod species, and whether it is altered by the invasive alien slug species Arion lusitanicus. Specifically, we hypothesized that a) native gastropod species consume the seeds from all tested plant species in equal numbers (have no preference), b) the voracious invasive alien slug A. lusitanicus – similarly to its herbivore behaviour – consumes a higher amount of seeds than native gastropods, and that c) seed viability is equal among different gastropod species after gut passage. As expected all tested gastropod species consumed all tested plant species. Against our expectation there was a difference in the amount of consumed seeds, with the largest and native mollusk Helix pomatia consuming most seeds, followed by the invasive slug and the other gastropods. Seed damage and germination rates did not differ after gut passage through different native species, but seed damage was significantly higher after gut passage through the invasive slug A. lusitanicus, and their germination rates were significantly reduced.

Locomotor activity of two sympatric slugs: implication for the invasion success of terrestrial invertebrates.

A central focus of invasion biology is to identify the traits that predict which introduced species will become invasive. Behavioral traits related to locomotor activity most likely play a pivotal role in determining a species’invasion success but have rarely been studied, particularly in terrestrial invertebrates. Here, we experimentally investigated the small-scale locomotor activity of two slug species with divergent invasion success in Europe, the highly invasive slug, Arion lusitanicus, and the closely related, non-invasive and native slug, Arion rufus. To do so, we used a multi-state capture-mark-recapture approach, and hypothesized that the invasive slug has a higher moving rate (keeps on moving) and leaving rate (leaves more frequently known places). A total of 221 invasive and 241 non-invasive slugs were individually marked using magnetic transponders and released in three study sites differing in habitat type. The slugs were recaptured using shelter traps, and moving and leaving rates were estimated. Both rates were significantly higher for the invasive slug, demonstrating a higher locomotor activity which might partly explain its invasion success. Our results provide evidence for the recently suggested idea that locomotor activity might be an important trait underlying animal invasions using for the first time terrestrial invertebrates.

The role of glucosinolates and the jasmonic acid pathway in resistance of Arabidopsis thaliana against molluscan herbivores

Although slugs and snails play important roles in terrestrial ecosystems and cause considerable damage on a variety of crop plants, knowledge about the mechanisms of plant immunity to molluscs is limited. We found slugs to be natural herbivores of Arabidopsis thaliana and therefore investigated possible resistance mechanisms of this species against several molluscan herbivores. Treating wounded leaves with the mucus residue (‘slime trail’) of the Spanish slug Arion lusitanicus increased wound-induced jasmonate levels, suggesting the presence of defence elicitors in the mucus. Plants deficient in jasmonate biosynthesis and signalling suffered more damage by molluscan herbivores in the laboratory and in the field, demonstrating that JA-mediated defences protect A. thaliana against slugs and snails. Furthermore, experiments using A. thaliana mutants with altered levels of specific glucosinolate classes revealed the importance of aliphatic glucosinolates in defending leaves and reproductive structures against molluscs. The presence in mollusc faeces of known and novel metabolites arising from glutathione conjugation with glucosinolate hydrolysis products suggests that molluscan herbivores actively detoxify glucosinolates. Higher levels of aliphatic glucosinolates were found in plants during the night compared to the day, which correlated well with the nocturnal activity rhythms of slugs and snails. Our data highlight the function of well-known antiherbivore defence pathways in resistance against slugs and snails and suggest an important role for the diurnal regulation of defence metabolites against nocturnal molluscan herbivores.

Development and characterization of novel microsatellite markers for Arion slug species

Seventeen polymorphic microsatellite markers were isolated and characterized in Arion vulgaris/lusitanicus, which belongs to the worst European slug pests with serious economic and ecological impact. These markers were tested on 23 individuals collected in a population in Switzerland. Numbers of alleles ranged from 2 to 14 per locus, observed and expected heterozygosities ranged from 0.174 to 0.87, and from 0.162 to 0.903, respectively. These loci were also successfully amplified and were polymorphic in the closely related species A. rufus and A. ater. These loci represent the first highly polymorphic nuclear markers described for A. vulgaris and pave the way for population genetics and molecular ecology research of the important Arion pest slugs.