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There is increasing evidence that plant-associated microorganisms play important roles in defending plants against insect herbivores through both direct and indirect mechanisms. While previous research has shown that these microbes can modify the behaviour and performance of insect herbivores and their natural enemies, little is known about their effect on egg parasitoids which utilize oviposition-induced plant volatiles to locate their hosts. In this study, we investigated how root inoculation of sweet pepper (Capsicum annuum) with the plant-beneficial fungi Beauveria bassiana ARSEF 3097 or Trichoderma harzianum T22 influences the olfactory behaviour of the egg parasitoid Trissolcus basalis following egg deposition by its host Nezara viridula. Olfactometer assays showed that inoculation by T. harzianum significantly enhanced the attraction of the egg parasitoid, while B. bassiana had the opposite effect. However, no variation was observed in the chemical composition of plant volatiles. Additionally, fitness-related traits of the parasitoids (wasp body size) were not altered by any of the two fungi, suggesting that fungal inoculation did not indirectly affect host quality. Altogether, our results indicate that plant inoculation with T. harzianum T22 can be used to enhance attraction of egg parasitoids, which could be a promising strategy in manipulating early plant responses against pest species and improving sustainable crop protection. From a more fundamental point of view, our findings highlight the importance of taking into account the role of microorganisms when studying the intricate interactions between plants, herbivores and their associated egg parasitoids. [ABSTRACT FROM AUTHOR]

Microorganisms living in and on macroorganisms may produce microbial volatile compounds (mVOCs) that characterise organismal odours. The mVOCs might thereby provide a reliable cue to carnivorous enemies in locating their host or prey. Parasitism by parasitoid wasps might alter the microbiome of their caterpillar host, affecting organismal odours and interactions with insects of higher trophic levels such as hyperparasitoids. Hyperparasitoids parasitise larvae or pupae of parasitoids, which are often concealed or inconspicuous. Odours of parasitised caterpillars aid them to locate their host, but the origin of these odours and its relationship to the caterpillar microbiome are unknown. Here, we analysed the odours and microbiome of the large cabbage white caterpillar Pieris brassicae in relation to parasitism by its endoparasitoid Cotesia glomerata. We identified how bacterial presence in and on the caterpillars is correlated with caterpillar odours and tested the attractiveness of parasitised and unparasitised caterpillars to the hyperparasitoid Baryscapus galactopus. We manipulated the presence of the external microbiome and the transient internal microbiome of caterpillars to identify the microbial origin of odours. We found that parasitism by C. glomerata led to the production of five characteristic volatile products and significantly affected the internal and external microbiome of the caterpillar, which were both found to have a significant correlation with caterpillar odours. The preference of the hyperparasitoid was correlated with the presence of the external microbiome. Likely, the changes in external microbiome and body odour after parasitism were driven by the resident internal microbiome of caterpillars, where the bacterium Wolbachia sp. was only present after parasitism. Micro-injection of Wolbachia in unparasitised caterpillars increased hyperparasitoid attraction to the caterpillars compared to untreated caterpillars, while no differences were found compared to parasitised caterpillars. In conclusion, our results indicate that host-parasite interactions can affect multi-trophic interactions and hyperparasitoid olfaction through alterations of the microbiome. Author summary: Bacteria living in and on macroorganisms produce the majority of their odours and thereby play an essential role in species interactions. For example, the hyperparasitoid enemies of parasitic wasps can reliably use odours of parasitised caterpillars to find the parasitic wasp larvae developing inside the caterpillar. We studied whether parasitism of caterpillars caused changes in caterpillar odours and associated internal and external bacterial communities to elucidate whether specific bacteria are responsible for the odours emitted by parasitised caterpillars. We identified which bacteria corresponded with odour production and whether hyperparasitoids could still find parasitised caterpillars that had their bacterial communities experimentally disrupted. We found that parasitised caterpillars have different odour profiles compared to unparasitised caterpillars and that bacteria in and on caterpillars correspond with these changes. The hyperparasitoid was less attracted to parasitised caterpillars with a disrupted skin microbiome. A characteristic bacterium, Wolbachia sp., which was only found inside parasitised caterpillars, may have initiated changes in the external microbiome and effects on odour emission. Furthermore, we show that micro-injection of Wolbachia in unparasitized caterpillars enhanced hyperparasitoid attraction. Hence, our results indicate that parasitoid wasps indirectly reveal themselves to their hyperparasitoid natural enemies by alteration of the bacterial communities of their host. [ABSTRACT FROM AUTHOR]

Symbiotic relationships may provide organisms with key innovations that aid in the establishment of new niches. For example, during oviposition, some species of parasitoid wasps, whose larvae develop inside the bodies of other insects, inject polydnaviruses into their hosts. These symbiotic viruses disrupt host immune responses, allowing the parasitoid's progeny to survive. Here we show that symbiotic polydnaviruses also have a downside to the parasitoid's progeny by initiating a multitrophic chain of interactions that reveals the parasitoid larvae to their enemies. These enemies are hyperparasitoids that use the parasitoid progeny as host for their own offspring. We found that the virus and venom injected by the parasitoid during oviposition, but not the parasitoid progeny itself, affected hyperparasitoid attraction toward plant volatiles induced by feeding of parasitized caterpillars. We identified activity of virus-related genes in the caterpillar salivary gland. Moreover, the virus affected the activity of elicitors of salivary origin that induce plant responses to caterpillar feeding. The changes in caterpillar saliva were critical in inducing plant volatiles that are used by hyperparasitoids to locate parasitized caterpillars. Our results show that symbiotic organismsmay be key drivers of multitrophic ecological interactions. We anticipate that this phenomenon is widespread in nature, because of the abundance of symbiotic microorganisms across trophic levels in ecological communities. Their role should be more prominently integrated in community ecology to understand organization of natural and managed ecosystems, as well as adaptations of individual organisms that are part of these communities. [ABSTRACT FROM AUTHOR]

The effects of multiple insect attacks on herbivore-induced plant volatiles and carnivorous arthropods are increasingly studied. Phytopathogens also represent an important threat to plants, and plant defence strategies against pathogens and insects are strongly interconnected, yet the potential impact of pathogens on insect-induced volatiles has been largely overlooked, and degree of pathogenicity is rarely considered., We investigated how pathogen challenge, with virulent and avirulent strains of Xanthomonas campestris either alone or with simultaneous Pieris brassicae caterpillar herbivory, affected the volatile emissions of Brassica nigra plants. The impact of these volatiles on the foraging behaviour of Cotesia glomerata parasitoids wasps was then assessed., Pathogens themselves induced volatiles that were highly attractive to parasitoids, and enhanced the attractiveness of host-infested plant volatiles. Chemical analyses revealed that virulent and avirulent strains differentially induced plant volatiles, with primarily sesquiterpene, homoterpene and green leaf volatile compounds contributing to the differences. Strong similarities were found in the blends induced by the virulent strain and caterpillar herbivory., Challenge by either virulent or avirulent pathogens has a significant impact on plant chemistry and its interactions with other community members, demonstrating the importance of integrating pathogen- and insect-based research to broaden our knowledge of plant defences under conditions of increasing complexity., A is available for this article. [ABSTRACT FROM AUTHOR]

Plants respond to herbivory with the emission of plant volatiles, which can be used by the herbivores' natural enemies to locate their hosts or prey. In nature, plants are often simultaneously confronted with insect herbivores and phytopathogens, potentially interfering with the attraction of the herbivores' enemies as a result of modifications of the induced volatile blend. Here, we investigated parasitoid ( C otesia glomerata) attraction to volatiles of plants challenged by different attackers, either alone or in combination with P ieris brassicae caterpillars, hosts of C . glomerata. We used a natural system consisting of B rassica nigra plants, eggs and larvae of P . brassicae, B revicoryne brassicae aphids and the bacterial phytopathogen X anthomonas campestris pv. campestris. In all cases, parasitoids successfully located host-infested plants, and wasp foraging behaviour was unaffected by the simultaneous presence of a non-host attacker or host eggs. Analysis of the volatile emissions show that the volatile blends of caterpillar-infested treatments were different from those without caterpillars. Furthermore, dually attacked plants could not be separated from those with only caterpillars, regardless of non-host identity, supporting the behavioural data. Our results suggest that, in this system, indirect plant defences may be more resistant to interference than is generally assumed, with volatiles induced during dual attack remaining reliable indicators of host presence for parasitoids. [ABSTRACT FROM AUTHOR]

ABSTRACT Beneficial soil-borne microbes, such as mycorrhizal fungi or rhizobacteria, can affect the interactions of plants with aboveground insects at several trophic levels. While the mechanisms of interactions with herbivorous insects, that is, the second trophic level, are starting to be understood, it remains unknown how plants mediate the interactions between soil microbes and carnivorous insects, that is, the third trophic level. Using Arabidopsis thaliana Col-0 and the aphid Myzus persicae, we evaluate here the underlying mechanisms involved in the plant-mediated interaction between the non-pathogenic rhizobacterium Pseudomonas fluorescens and the parasitoid Diaeretiella rapae, by combining ecological, chemical and molecular approaches. Rhizobacterial colonization modifies the composition of the blend of herbivore-induced plant volatiles. The volatile blend from rhizobacteria-treated aphid-infested plants is less attractive to an aphid parasitoid, in terms of both olfactory preference behaviour and oviposition, than the volatile blend from aphid-infested plants without rhizobacteria. Importantly, the effect of rhizobacteria on both the emission of herbivore-induced volatiles and parasitoid response to aphid-infested plants is lost in an Arabidopsis mutant ( aos/dde2-2) that is impaired in jasmonic acid production. By modifying the blend of herbivore-induced plant volatiles that depend on the jasmonic acid-signalling pathway, root-colonizing microbes interfere with the attraction of parasitoids of leaf herbivores. [ABSTRACT FROM AUTHOR]

BACKGROUND: Most insect-resistant transgenic crops employ toxins to control pests. A novel approach is to enhance the effectiveness of natural enemies by genetic engineering of the biosynthesis of volatile organic compounds (VOCs). Before the commercialisation of such transgenic plants can be pursued, detailed fundamental studies of their effects on herbivores and their natural enemies are necessary. The linalool/nerolidol synthase gene FaNES1 was constitutively expressed from strawberry in three Arabidopsis thaliana accessions, and the behaviour of the aphid Brevicoryne brassicae L., the parasitoid Diaeretiella rapae McIntosh and the predator Episyrphus balteatus de Geer was studied. RESULTS: Transgenic FaNES1-expressing plants emitted ( E)-nerolidol and larger amounts of ( E)-DMNT and linalool. Brevicoryne brassicae was repelled by the transgenic lines of two of the accessions, whereas its performance was not affected. Diaeretiella rapae preferred aphid-infested transgenic plants over aphid-infested wild-type plants for two of the accessions. In contrast, female E. balteatus predators did not differentiate between aphid-infested transgenic or wild-type plants. CONCLUSION: The results indicate that the genetic engineering of plants to modify their emission of VOCs holds considerable promise for facilitating biological control of herbivores. Validation for crop plants is a necessary next step to assess the usefulness of modified volatile emission in integrated pest management. Copyright © 2012 Society of Chemical Industry [ABSTRACT FROM AUTHOR]