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The Gastropod Menace: Slugs on Brassica Plants Affect Caterpillar Survival through Consumption and Interference with Parasitoid Attraction

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) 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 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.

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Acknowledgments

The authors thank Diane Laplanche, Antoine Guiguet, Leslie Mann, and Gabriel Marcacci for their help with rearing the animals used in the study and performing the predation experiments. Xu Hao and Marie-Jeanne Tschudi helped with growing the plants used, and Neil Villard helped with taking pictures and videos of the bioassays. M. A. Z. is grateful to Gerald Heckel for encouraging her to explore different aspects of the A. vulgaris invasion within a PhD project.

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Correspondence to Gaylord A. Desurmont.

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Desurmont, G.A., Zemanova, M.A. & Turlings, T.C.J. The Gastropod Menace: Slugs on Brassica Plants Affect Caterpillar Survival through Consumption and Interference with Parasitoid Attraction. J Chem Ecol 42, 183–192 (2016). https://doi.org/10.1007/s10886-016-0682-2

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  • DOI: https://doi.org/10.1007/s10886-016-0682-2

Keywords

  • Herbivore-induced plant volatiles
  • Indirect defense
  • Infochemical networks
  • Intraguild predation
  • Molluscan ecology
  • VOCs
  • Invasive slug