Tri-trophic consequences of plant-to-plant volatile signalling and its contingency on plant relatedness in wild cotton

Background and Aims Plant volatile organic compounds (VOCs) induced by herbivory boost defences in neighbouring plants. These effects have been shown primarily for direct plant defences and are often stronger when emitter and receiver plants are genetically related. However, we know much less about how plant indirect defence is affected by VOC signalling. To address this, we conducted field experiments controlling for plant relatedness, testing the effects of VOC signalling on extrafloral nectar (EFN) production, a key indirect defence, and its impact on ant recruitment and attacks on herbivores of wild cotton (Gossypium hirsutum) plants. Methods Experiments consisted of plant triplets, where one individual acted as an emitter of VOCs and two as receivers. One receiver shared the same mother plant as the emitter, and the other was descended from a different mother. Half of the emitter plants were induced using the specialist caterpillar Alabama argillacea, and VOCs were collected. We then induced receivers and measured their EFN production as well as ant abundance and attack on sentinel caterpillars. Immediately after, we excluded ants from half of the receivers to test for ant-mediated effects on natural herbivory occurring over the following weeks. Key Results Receivers exposed to VOCs of damaged emitters produced a greater volume and concentration of EFN in response to herbivory relative to those exposed to undamaged emitters, and, accordingly, showed higher rates of ant attack on sentinel caterpillars but there were no differences in ant abundance. These effects were not contingent on emitter-receiver relatedness. In addition, we found no effect of ant exclusion on natural herbivory levels on receiver plants, though damage was overall very low. Conclusions These findings provide insight into inter-plant VOC signalling effects on multitrophic interactions by revealing indirect defence induction that leads to herbivore reduction by ants independently of the emitter-receiver relatedness.