Herbivore-induced volatile blends with both “fast” and “slow” components provide robust indirect defence in nature

Plants emit volatile blends specific to particular herbivore interactions, which predators and parasitoids learn to associate with prey, increasing herbivore mortality and thereby plant fitness in a phenomenon termed indirect defence. Herbivore-induced plant volatile blends commonly include both rapid, transient green leaf volatiles (GLVs) and delayed, enduring sesquiterpenes. A few laboratory studies indicate that insects can use plant volatiles to time behaviour, but it is not known whether and how the temporal dynamics of plant volatile blends influence their function in indirect defence. We characterized the activity of the native herbivores Manduca sexta and Tupiocoris notatus and their predators, Geocoris spp., on their host plant Nicotiana attenuata in their natural habitat. Diurnal predator activity only partially overlapped with variable herbivore activity, and herbivore attack at the beginning or end of the photophase elicited plant volatile blends with distinct GLV and sesquiterpene profiles. In field trials, day-active Geocoris spp. predators preferred morning- over evening-typical GLV blends. Using plants genetically transformed so as to be unable to produce specific volatiles, we found that GLVs increased predation after dawn elicitations, whereas sesquiterpenes increased predation after dusk elicitations in field trials. We conclude that predators respond to temporal differences in plant volatile blends, and that the different dynamics of specific volatiles permit effective indirect defence despite variable herbivore activity in nature. A plain language summary is available for this article.