Abstract
BackgroundThe role of plant ontogeny on investment in direct defense against herbivores is well accepted, but the transition from the vegetative to the reproductive stage can also affect indirect resistance traits (i.e. attraction of the natural enemies of plant attackers). Here, we conducted behavioral bioassays in olfactometers to determine whether the developmental stage (vegetative, pre-flowering, and flowering) of Brassica rapa plants affects attraction of Cotesiaglomerata, a parasitoid of the herbivore Pieris brassicae, and examined the blends of volatile compounds emitted by plants at each developmental stage.ResultsPieris-infested plants were always more attractive to parasitoids than control plants and plants infested by a non-host herbivore, independently of plant developmental stage. On the other hand, the relative attractiveness of Pieris-infested plants was ontogeny dependent: Pieris-infested plants were more attractive at the pre-flowering stage than at the vegetative stage, and more attractive at the vegetative stage than at the flowering stage. Chemical analyses revealed that the induction of leaf volatiles after herbivory is strongly reduced in flowering plants. The addition of synthetic floral volatiles to infested vegetative plants decreased their attractiveness to parasitoids, suggesting a trade-off between signaling to pollinators and parasitoids.ConclusionOur results show that putative indirect resistance traits are affected by plant development, and are reduced during B. rapa reproductive stage. The effects of ontogenetic shifts in resource allocation on the behavior of members of the third trophic level may have important implications for the evolution of plant defense strategies against herbivores.Electronic supplementary materialThe online version of this article (doi:10.1186/s12898-015-0047-7) contains supplementary material, which is available to authorized users.
Highlights
The role of plant ontogeny on investment in direct defense against herbivores is well accepted, but the transition from the vegetative to the reproductive stage can affect indirect resistance traits
Tests conducted in 4-arm olfactometers with vegetative plants and flowering plants separately showed significant differences in attractiveness between the treatments (χ2 = 42.2, P < 0.0001, and χ2 = 49.9, P < 0.0001, respectively, df = 3). For both developmental stages, infested plants were more attractive than control plants: infested vegetative plants were five times more attractive than controls, and infested flowering plants twice as attractive as controls (Figure 2A, B)
In B. rapa, attractiveness to parasitoids decreases as plants enter the flowering stage, due to a reduced investment in herbivore-induced volatiles and to the interfering effect of floral volatiles on parasitoid attraction. Despite this reduced investment in volatiles, infested flowering plants remain more attractive to parasitoids than undamaged plants, and the blend emitted retains its specificity to Pieris infestation
Summary
The role of plant ontogeny on investment in direct defense against herbivores is well accepted, but the transition from the vegetative to the reproductive stage can affect indirect resistance traits (i.e. attraction of the natural enemies of plant attackers). Investment in secondary metabolism can vary tremendously through the lifetime of single plants [3] Such temporal changes can be separated in two categories: changes driven by fluctuating environmental conditions are referred to as seasonal, and changes associated with the development of the plant are referred to as ontogenetic [4]. Both types of temporal variation can play an important role in plant defense and insect–plant interactions. Plants may not have the same needs for defenses or equal amounts of resources to invest in defensive compounds
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