The gastropod menace: slugs on Brassica plants affect caterpillar survival through consumption and interference with parasitoid attraction

Authors: DESURMONT, GAYLORD - European Biological Control Laboratory (EBCL); ZEMANOVA, MYRIAM - University Of Berne; TURLINGS, TED - Neuchatel University - Switzerland

Submitted to: Journal of Chemical Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/10/2016
Publication Date: 3/20/2016
Citation: Desurmont, G., Zemanova, M., Turlings, T.C. 2016. The gastropod menace: slugs on Brassica plants affect caterpillar survival through consumption and interference with parasitoid attraction. Journal of Chemical Ecology. Vol 42, Issue 3, Pages 183-192.

Interpretive Summary: Slugs are major plant pests of many crops including cole crops. The genus Arion includes several species of slug that are invasive pests worldwide. However it is not well known how slugs interact with their host plants or with other insects that attack the same plant. We studied the effects of slugs on the attack by caterpillars of the large cabbage white butterfly (Pieris brassicae). We also measured odors produced by field mustard (Brassica rapa) in response to attack by the slugs and/or caterpillars to determine how they might affect the ability of parasites to find the caterpillars. Our results showed firstly that some caterpillars were directly killed by slugs. Secondly, plants damaged by slugs and caterpillars became unattractive to a parasite of the caterpillar (the parasitoid Cotesia glomerata) whereas those damaged only by the caterpillar were attractive. Thus the slugs tended to reduce the impact of caterpillars by directly killing them, but also tended to also reduce the ability of caterpillar parasites to attack the caterpillars, thus increasing their potential impact on the mustard plants. These results show that slugs should not be considered only as plant pests, but that they can also interact with insect herbivores and the natural enemies that help to control their populations.

Technical Abstract: Terrestrial molluscs and insect herbivores play a major role as plant consumers in a number of ecosystems, but their direct and indirect interactions have hardly been explored. The omnivorous nature of slugs makes them potential disrupters of predator-prey relationships, as a direct threat to small insects and through indirect, plant-mediated effects. Here we examined the effects of the presence of two species of slugs, Arion rufus (native to Switzerland) and A. vulgaris (invasive) on the survivorship of young Pieris brassicae caterpillars when feeding on Brassica rapa plants, and on plant attractiveness to the main natural enemy of P. brassicae, the parasitoid Cotesia glomerata. In two separate predation experiments, caterpillar mortality was significantly higher on plants co-infested with A. rufus or A. vulgaris. Moreover, caterpillar mortality correlated positively with slug mass and leaf consumption by A. vulgaris. At the third trophic level, plants infested with slugs and plants co-infested with slugs and caterpillars were far less attractive to parasitoids than plants damaged by caterpillars only, independently of slug species. Chemical analyses confirmed that volatile emissions, which provide important foraging cues for parasitoids, were strongly reduced in co-infested plants. Our study shows that the presence of slugs has the potential to affect insect populations, directly via consumptive effects and indirectly via changes in plant volatiles that result in a reduced attraction of natural enemies. The fitness cost for P. brassicae imposed by increased mortality in presence of slugs may be counterbalanced by the benefit of escaping its parasitoids.