Abstract
Author SummaryIn nature, plants often release volatiles in response to damage by herbivores (e.g., by caterpillars), and these can indirectly help defend the plants. Indeed, it is well documented that volatiles can recruit the natural enemies of herbivores, such as predators and parasitoid wasps, whose offspring feed on and develop within their caterpillar hosts. However, such induced plant odours can also be detected by other organisms. One important group of organisms, hyperparasitoids, the enemies of the parasitoids that indirectly benefit the plants, have not been included in this trophic web because so little is known about their foraging behaviour. Here, using a combination of laboratory and field experiments, we demonstrate that hyperparasitoid wasps also take advantage of the odours that plants produce in response to the feeding by caterpillars. The larvae of parasitic wasps developing inside the caterpillar alter the composition of the oral secretions of their herbivorous host and thereby affect the cocktail of volatiles the plant produces. The hyperparasitoids on the lookout for their parasitoid prey can preferentially detect infected caterpillars, although not all parasitoid wasps gave away their presence through this host–plant interaction. We conclude that herbivore-induced plant volatiles can affect the interaction among parasitoids and their enemies and thereby may reduce the indirect defence accrued for the plant.
Highlights
Plant volatiles play a profoundly important role in the structure and function of ecological communities [1,2,3,4,5,6]
In line with differences in the size of their hosts, we found that L. nana wasps were about 35% smaller when emerging from C. glomerata than C. rubecula cocoons (Table 1; Figure 2)
When we offered cocoons of C. rubecula in a group, to match the cocoon mass of a brood of C. glomerata cocoons, we found that L. nana females more often first encountered the group of C. rubecula cocoons than the clutch of C. glomerata cocoons (n = 47, p = 0.003) (Figure 3)
Summary
Plant volatiles play a profoundly important role in the structure and function of ecological communities [1,2,3,4,5,6]. Volatiles make a plant and its condition apparent to community members at different trophic levels [6,7] and may, thereby, mediate interactions between organisms at higher trophic levels [8,9] Nowhere has this been better investigated than for interactions between insect herbivores and their natural enemies, such as primary parasitic wasps (or ‘‘parasitoids’’) at the third trophic level. Little is known about foraging behaviour of the enemies of parasitoids (i.e., hyperparasitoids) that are an important group of fourth-trophic-level organisms, because hyperparasitoids have not been included in the debate on the fitness benefit of volatile release by plants [15]
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