A comparative study of plant volatiles induced by insect and gastropod herbivory.

Insect and gastropod herbivores are major plant consumers and their importance in the evolution of plant defensive traits is broadly recognized. However, their respective effects on plant responses have rarely been compared. Here we focused on plant volatile emissions (VOCs) following herbivory and compared the effects of herbivory by caterpillars of the generalist insect Spodoptera littoralis and by generalist slugs of the genus Arion on the VOCs emissions of 14 cultivated plant species. Results revealed that plants consistently produced higher amounts of volatiles and responded more specifically to caterpillar than to slug herbivory. Specifically, plants released on average 6.0 times more VOCs (total), 8.9 times more green leaf volatiles, 4.2 times more terpenoids, 6.0 times more aromatic hydrocarbons, and 5.7 times more other VOCs in response to 1 cm2 of insect damage than to 1 cm2 of slug damage. Interestingly, four of the plant species tested produced a distinct blend of volatiles following insect damage but not slug damage. These findings may result from different chemical elicitors or from physical differences in herbivory by the two herbivores. This study is an important step toward a more inclusive view of plant responses to different types of herbivores.

Evolutionary changes in an invasive plant support the defensive role of plant volatiles.

It is increasingly evident that plants interact with their outside world through the production of volatile organic compounds,1-5 but whether the volatiles have evolved to serve in plant defense is still a topic of considerable debate.3,6-8 Unharmed leaves constitutively release small amounts of volatiles, but when the leaves are damaged by herbivorous arthropods, they emit substantially more volatiles. These herbivore-induced plant volatiles (HIPVs) attract parasitoids and predators that kill insect herbivores,9-12 and this can benefit the plants.13,14 As yet, however, there is no tangible evolutionary evidence that this tritrophic interplay contributes to the selection forces that have shaped the volatile emissions of plants.2,3,5-8,15 With this in mind, we investigated the evolutionary changes in volatile emissions in invasive common ragwort and the respective defensive roles of its constitutive and inducible volatiles. This Eurasian plant has invaded other continents, where it evolved for many generations in the absence of specialized herbivores and their natural enemies. We found that, compared to native ragworts, invasive plants release higher levels of constitutive volatiles but considerably lower levels of herbivore-induced volatiles. As a consequence, invasive ragwort is more attractive to a specialist moth but avoided by an unadapted generalist moth. Importantly, conforming to the indirect defense hypothesis, a specialist parasitoid was much more attracted to caterpillar-damaged native ragwort, which was reflected in higher parasitism rates in a field trial. The evolution of foliar volatile emissions appears to be indeed driven by their direct and indirect roles in defenses against insects.

Spodoptera frugiperda Caterpillars Suppress Herbivore-Induced Volatile Emissions in Maize.

The vast spectrum of inducible plant defenses can have direct negative effects on herbivores, or indirect effects, for instance in the form of herbivore-induced plant volatiles (HIPVs) that attract natural enemies. Various arthropods have evolved ways to suppress plant defenses. To test whether this is the case for caterpillar-induced HIPVs, we compared the volatile induction by Spodoptera frugiperda (Lepidoptera: Noctuidae), which is particularly well adapted to feed on maize (Zea mays), with the induction by three more generalist noctuid larvae. We tested the hypothesis that S. frugiperda suppresses HIPV emissions in maize, and thereby reduces attractiveness to natural enemies. HIPV emissions triggered by S. frugiperda when feeding on maize were indeed found to be significantly weaker than by Spodoptera littoralis, Spodoptera exigua, and Helicoverpa armigera. The suppression seems specific for maize, as we found no evidence for this when S. frugiperda caterpillars fed on cotton (Gossypium herbaceum). Artificially damaged maize plants treated with larval regurgitant revealed that HIPV suppression may be related to factors in the caterpillars' oral secretions. We also found evidence that differential physical damage that the caterpillars inflict on maize leaves may play a role. The suppressed induction of HIPVs had no apparent consequences for the attraction of a common parasitoid of S. frugiperda, Cotesia marginiventris (Hymenoptera: Braconidae). Nevertheless, the ability to manipulate the defenses of its main host plant may have contributed to the success of S. frugiperda as a major pest of maize, especially in Africa and Asia, which it has recently invaded.

With or without you: Effects of the concurrent range expansion of an herbivore and its natural enemy on native species interactions.

Global climatic changes may lead to the arrival of multiple range-expanding species from different trophic levels into new habitats, either simultaneously or in quick succession, potentially causing the introduction of manifold novel interactions into native food webs. Unraveling the complex biotic interactions between native and range-expanding species is critical to understand the impact of climate change on community ecology, but experimental evidence is lacking. In a series of laboratory experiments that simulated direct and indirect species interactions, we investigated the effects of the concurrent arrival of a range-expanding insect herbivore in Europe, Spodoptera littoralis, and its associated parasitoid Microplitis rufiventris, on the native herbivore Mamestra brassicae, and its associated parasitoid Microplitis mediator, when co-occurring on a native plant, Brassica rapa. Overall, direct interactions between the herbivores were beneficial for the exotic herbivore (higher pupal weight than the native herbivore), and negative for the native herbivore (higher mortality than the exotic herbivore). At the third trophic level, both parasitoids were unable to parasitize the herbivore they did not coexist with, but the presence of the exotic parasitoid still negatively affected the native herbivore (increased mortality) and the native parasitoid (decreased parasitism rate), through failed parasitism attempts and interference effects. Our results suggest different interaction scenarios depending on whether S. littoralis and its parasitoid arrive to the native tritrophic system separately or concurrently, as the negative effects associated with the presence of the parasitoid were dependent on the presence of the exotic herbivore. These findings illustrate the complexity and interconnectedness of multitrophic changes resulting from concurrent species arrival to new environments, and the need for integrating the ecological effects of such arrivals into the general theoretical framework of global invasion patterns driven by climatic change.

The spitting image of plant defenses: Effects of plant secondary chemistry on the efficacy of caterpillar regurgitant as an anti-predator defense.

In the arms race between plants, herbivores, and their natural enemies, specialized herbivores may use plant defenses for their own benefit, and variation in plant traits may affect the benefits that herbivores derive from these defenses. Pieris brassicae is a specialist herbivore of plants containing glucosinolates, a specific class of defensive secondary metabolites. Caterpillars of P. brassicae are known to actively spit on attacking natural enemies, including their main parasitoid, the braconid wasp Cotesia glomerata. Here, we tested the hypothesis that variation in the secondary metabolites of host plants affects the efficacy of caterpillar regurgitant as an anti-predator defense. Using a total of 10 host plants with different glucosinolate profiles, we first studied natural regurgitation events of caterpillars on parasitoids. We then studied manual applications of water or regurgitant on parasitoids during parasitization events. Results from natural regurgitation events revealed that parasitoids spent more time grooming after attack when foraging on radish and nasturtium than on Brassica spp., and when the regurgitant came in contact with the wings rather than any other body part. Results from manual applications of regurgitant showed that all parameters of parasitoid behavior (initial attack duration, attack interruption, grooming time, and likelihood of a second attack) were more affected when regurgitant was applied rather than water. The proportion of parasitoids re-attacking a caterpillar within 15 min was the lowest when regurgitant originated from radish-fed caterpillars. However, we found no correlation between glucosinolate content and regurgitant effects, and parasitoid behavior was equally affected when regurgitant originated from a glucosinolate-deficient Arabidopsis thaliana mutant line. In conclusion, host plant affects to a certain extent the efficacy of spit from P. brassicae caterpillars as a defense against parasitoids, but this is not due to glucosinolate content. The nature of the defensive compounds present in the spit remains to be determined, and the ecological relevance of this anti-predator defense needs to be further evaluated in the field.

Combined use of herbivore-induced plant volatiles and sex pheromones for mate location in braconid parasitoids.

Herbivore-induced plant volatiles (HIPVs) are important cues for female parasitic wasps to find hosts. Here, we investigated the possibility that HIPVs may also serve parasitoids as cues to locate mates. To test this, the odour preferences of four braconid wasps - the gregarious parasitoid Cotesia glomerata (L.) and the solitary parasitoids Cotesia marginiventris (Cresson), Microplitis rufiventris Kokujev and Microplitis mediator (Haliday) - were studied in olfactometers. Each species showed attraction to pheromones but in somewhat different ways. Males of the two Cotesia species were attracted to virgin females, whereas females of M. rufiventris were attracted to virgin males. Male and female M. mediator exhibited attraction to both sexes. Importantly, female and male wasps of all four species were strongly attracted by HIPVs, independent of mating status. In most cases, male wasps were also attracted to intact plants. The wasps preferred the combination of HIPVs and pheromones over plant odours alone, except M. mediator, which appears to mainly use HIPVs for mate location. We discuss the ecological contexts in which the combined use of pheromones and HIPVs by parasitoids can be expected. To our knowledge, this is the first study to show that braconid parasitoids use HIPVs and pheromones in combination to locate mates.

Floral volatiles interfere with plant attraction of parasitoids: ontogeny-dependent infochemical dynamics in Brassica rapa.

BACKGROUND: 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 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 Cotesia glomerata, a parasitoid of the herbivore Pieris brassicae, and examined the blends of volatile compounds emitted by plants at each developmental stage. RESULTS: Pieris-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. CONCLUSION: Our 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.