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

1. 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 defenses is
unclear.  2. 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 defense.  3. We show that low WA initially
increases total HIPV emission by tomatoes 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 behavioral assays indicates that changes
in HIPV emissions by low WA compromise the ability of tomato plants to
attract natural enemies.  4. 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 defenses but
enhances plant direct defense against herbivores.