Abstract
BackgroundPlants have evolved an astonishing array of survival strategies. To defend against insects, for example, damaged plants emit volatile organic compounds that attract the herbivore’s natural enemies. So far, plant volatile responses have been studied extensively in conjunction with leaf chewing and sap sucking insects, yet little is known about the relationship between plant volatiles and gall-inducers, the most sophisticated herbivores. Here we describe a new role for volatiles as gall-insects were found to benefit from this plant defence.ResultsChemical analyses of galls triggered by the gregarious aphid Slavum wertheimae on wild pistachio trees showed that these structures contained and emitted considerably higher quantities of plant terpenes than neighbouring leaves and fruits. Behavioural assays using goats as a generalist herbivore confirmed that the accumulated terpenes acted as olfactory signals and feeding deterrents, thus enabling the gall-inducers to escape from inadvertent predation by mammals.ConclusionsIncreased emission of plant volatiles in response to insect activity is commonly looked upon as a “cry for help” by the plant to attract the insect’s natural enemies. In contrast, we show that such volatiles can serve as a first line of insect defences that extends the ‘extended phenotype’ represented by galls, beyond physical boundaries. Our data support the Enemy hypothesis insofar that high levels of gall secondary metabolites confer protection against natural enemies.
Highlights
Plants have evolved an astonishing array of survival strategies
In this study we have focused on the role of volatile terpenes in the conspicuous cauliflower-shaped galls that are induced by the aphid Slavum wertheimae (Pemphigidae) on the lateral buds of Pistacia atlantica (Anacardiaceae) trees (Figure 1) [24,25]
To further assess the functions of plant volatiles in tritrophic interactions with galls, we explored the following questions: (1) Does gall formation by S. wertheimae lead to enhanced concentrations of volatile compounds in the gall? (2) Does increased storage and emission of volatile compounds protect the gall and the insects inside from damage? Individuals of Capra hircus hircus (Damascus goat) were used to explore the defensive role of gall volatiles
Summary
Plants have evolved an astonishing array of survival strategies. To defend against insects, for example, damaged plants emit volatile organic compounds that attract the herbivore’s natural enemies. The proposed advantages of the galling habit fall into three main categories [2,6]: (1) Microclimatic stabilization: galls protect the insects from unfavourable abiotic conditions such as high temperature and low humidity (2) Nutrition: gall tissue provides an abundance of high quality nutrients and (3) Defence: morphology and chemistry of the gall tissue protect the inducing insect from various natural enemies, including predators, parasitoids, pathogens and other herbivores. This notion has been termed the Enemy hypothesis [2]
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