Low water availability enhances volatile-mediated direct defences but disturbs indirect defences against herbivores

Interactions between plants and natural enemies of insect herbivores influence plant productivity and survival by reducing herbivory. Plants attract natural enemies via herbivore-induced plant volatiles (HIPVs), but how water availability (WA) influences HIPV-mediated defences is unclear. We use tomato, Solanum lycopersicum, tomato fruitworm, Helicoverpa zea and two natural enemies, the parasitoid wasp, Microplitis croceipes and the predator spined soldier bug, Podisus maculiventris, to investigate the effect of WA on HIPV emission dynamics and associated plant defence. We show that low WA initially increases total HIPV emission by tomato on the first day of herbivore exposure and, in contrast, reduces HIPV emission on the second day. Low WA enhances HIPVs that are mostly found in tomato trichomes. Notably, some volatiles inhibited by low WA are known attractants of natural enemies. Evidence from Y-tube and in-cage behavioural assays indicates that changes in HIPV emissions by low WA compromise the ability of tomato plants to attract natural enemies. Synthesis. Based on our results, we propose a hypothesis where plants respond to low WA by enhancing repellent HIPV emissions and reducing the emission of HIPVs that attract natural enemies, which disrupts natural enemy-mediated plant indirect defences, but enhances plant direct defence against herbivores.