Slug Herbivory Induces Systemic Redox and Volatile Responses in Cabbage That Drive Chemotaxis of Slug-Parasitic Nematodes

Abstract

Slug herbivory is an important but poorly explored driver of plant defence and belowground multitrophic interactions. This study examined how aboveground feeding by Arion vulgaris and Deroceras reticulatum affects oxidative status, photosynthetic pigments, and volatile organic compound (VOC) emissions in cabbage (Brassica oleracea L. var. capitata), and whether these changes influence slug-parasitic nematodes. Slug feeding induced strong oxidative stress in leaves and roots, reflected by depletion of total ascorbate and glutathione contents and increased proportions of their oxidized forms, indicating a systemic redox imbalance. Photosynthetic pigments were also markedly affected, characterized by decreased chlorophylls and carotenoids and activation of the xanthophyll cycle towards more zeaxanthin, particularly in plants attacked by D. reticulatum. Headspace SPME–GC–MS analysis revealed tissue-specific, herbivory-induced shifts in VOC profiles. Based on these changes, three VOCs—3-phenylpropionitrile, allyl isothiocyanate, and 2-hexenal—were selected for chemotaxis assays. Behavioural experiments showed that VOC identity and nematode species markedly influenced motility and chemotactic responses. Phasmarhabditis papillosa exhibited the strongest attraction to 3-phenylpropionitrile, whereas allyl isothiocyanate acted as a weak repellent to P. papillosa, Oscheius myriophilus, and Oscheius onirici. In contrast, 2-hexenal elicited no consistent directional response. These results demonstrate that slug herbivory alters cabbage metabolism and volatile signalling, shaping species-specific nematode behaviour and highlighting its potential for sustainable slug management.