Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants

Many plant species respond to herbivory with increased emission of volatile organic compounds (VOCs): these attract carnivorous arthropods and thereby function as an indirect defence mechanism. Whether neighbouring plants can 'eavesdrop' on such airborne cues and tailor their defences accordingly, remains controversial. We used Lima bean plants (Phaseolus lunatus) to investigate whether herbivore-induced VOCs induce another indirect defence strategy, i.e. the secretion of extrafloral nectar (EFN) in conspecific plant neighbours, and whether this enhances the defence status of the receiving plant under natural conditions. EFN secretion was induced by VOCs released from herbivore-damaged bean tendrils as well as by a synthetic VOC mixture resembling the natural one. One constituent of the herbivore-induced blend - the green leaf volatile (3Z)-hex-3-enyl acetate - was sufficient to elicit the defence reaction. A long-term experiment comparing the defensive effect of EFN alone with the VOC-mediated effect (EFN induction plus attraction of plant defenders) suggested that Lima bean benefits from both indirect defences. Repeated treatment of tendrils with either an artificial blend of VOCs or with EFN led to the attraction of a higher cumulative number of predatory and parasitoid insects (i.e. ants and wasps) as well as to less herbivore damage and an increased production of inflorescences and leaves. Our results demonstrate that one indirect defence mechanism can induce another one in conspecific plants, and that Lima bean plants can benefit from this VOC-induced EFN secretion under natural conditions. Both extrafloral nectaries and the capability to release VOCs upon herbivory are present in many plant taxa and airborne signalling may thus represent a common mechanism for regulating the secretion of EFN in plant parts which face an increased risk of herbivory.