Parasitism overrides herbivore identity allowing hyperparasitoids to locate their parasitoid host using herbivore-induced plant volatiles
Zhu, F. ; Broekgaarden, C. ; Weldegergis, B.T. ; Harvey, J.A. ; Vosman, B. ; Dicke, M. ; Poelman, E.H. - \ 2015
Molecular Ecology 24 (2015)1. - ISSN 0962-1083 - p. 2886 - 2899.
cabbage brassica-oleracea - time rt-pcr - nicotiana-attenuata - insect herbivores - gene-expression - trophic levels - defense - responses - specialist - generalist
Foraging success of predators profoundly depends on reliable and detectable cues indicating the presence of their often inconspicuous prey. Carnivorous insects rely on chemical cues to optimize foraging efficiency. Hyperparasitoids that lay their eggs in the larvae or pupae of parasitic wasps may find their parasitoid hosts developing in different herbivores. They can use herbivore-induced plant volatiles (HIPVs) to locate parasitized caterpillars. Because different herbivore species induce different HIPV emission from plants, hyperparasitoids may have to deal with large variation in volatile information that indicates host presence. In this study, we used an ecogenomics approach to first address whether parasitized caterpillars of two herbivore species (Pieris rapae and P. brassicae) induce similar transcriptional and metabolomic responses in wild Brassica oleracea plants and, second, whether hyperparasitoids Lysibia nana are able to discriminate between these induced plant responses to locate their parasitoid host in different herbivores under both laboratory and field conditions. Our study revealed that both herbivore identity and parasitism affect plant transcriptional and metabolic responses to herbivory. We also found that hyperparasitoids are able to respond to HIPVs released by wild B. oleracea under both laboratory and field conditions. In addition, we observed stronger attraction of hyperparasitoids to HIPVs when plants were infested with parasitized caterpillars. However, hyperparasitoids were equally attracted to plants infested by either herbivore species. Our results indicate that parasitism plays a major role in HIPV-mediated plant-hyperparasitoid interactions. Furthermore, these findings also indicate that plant trait-mediated indirect interaction networks play important roles in community-wide species interactions.
To be in time: egg deposition enhances plant-mediated detection of young caterpillars by parasitoids
Pashalidou, F.G. ; Gols, R. ; Berkhout, B.W. ; Weldegergis, B.T. ; Loon, J.J.A. van; Dicke, M. ; Fatouros, N.E. - \ 2015
Oecologia 177 (2015)2. - ISSN 0029-8549 - p. 477 - 486.
different larval instars - pieris-brassicae - specialist herbivore - volatile emissions - cotesia-glomerata - host location - oviposition - responses - maize - generalist
Animals use information from their environment while foraging for food or prey. When parasitic wasps forage for hosts, they use plant volatiles induced by herbivore activities such as feeding and oviposition. Little information is available on how wasps exploit specific plant volatiles over time, and which compounds indicate changes in host quality. In experiments investigating the role of herbivore-induced plant volatiles in wasp foraging, induction of plant response is usually achieved by placing larvae on clean plants instead of allowing the natural sequence of events: to let eggs deposited by the herbivore develop into larvae. We compared the attraction of the parasitoid Cotesia glomerata to volatiles emitted by black mustard (Brassica nigra) plants induced by eggs and successive larval stages of the Large Cabbage White butterfly (Pieris brassicae) to the attraction of this parasitoid to black mustard plant volatiles induced only by larval feeding in a wind tunnel setup. We show that wasps are attracted to plants infested with eggs just before and shortly after larval hatching. However, wasp preference changed at later time points towards plants induced only by larval feeding. These temporal changes in parasitoid attraction matched with changes in the chemical compositions of the blends of plant volatiles. Previous studies have shown that host quality/suitability decreases with caterpillar age and that P. brassicae oviposition induces plant defences that negatively affect subsequently feeding caterpillars. We investigated parasitoid performance in hosts of different ages. Wasp performance was positively correlated with preference. Moreover, parasitism success decreased with time and host stage. In conclusion, the behaviour of Cotesia glomerata is fine-tuned to exploit volatiles induced by eggs and early host stages that benefit parasitoid fitness.
Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance
Wang, M. ; Biere, A. ; Putten, W.H. van der; Bezemer, T.M. - \ 2014
Oecologia 175 (2014)1. - ISSN 0029-8549 - p. 187 - 198.
deterrent iridoid glycosides - mediated interactions - specialist herbivore - chemical defense - lanceolata l - induction - generalist - damage - age - chemistry
Plants are often simultaneously or sequentially attacked by multiple herbivores and changes in host plants induced by one herbivore can influence the performance of other herbivores. We examined how sequential feeding on the plant Plantago lanceolata by the aboveground herbivore Spodoptera exigua and the belowground herbivore Agriotes lineatus influences plant defense and the performance of both insects. Belowground herbivory caused a reduction in the food consumption by the aboveground herbivore independent of whether it was initiated before, at the same time, or after that of the aboveground herbivore. By contrast, aboveground herbivory did not significantly affect belowground herbivore performance, but significantly reduced the performance of later arriving aboveground conspecifics. Interestingly, belowground herbivores negated negative effects of aboveground herbivores on consumption efficiency of their later arriving conspecifics, but only if the belowground herbivores were introduced simultaneously with the early arriving aboveground herbivores. Aboveground–belowground interactions could only partly be explained by induced changes in an important class of defense compounds, iridoid glycosides (IGs). Belowground herbivory caused a reduction in IGs in roots without affecting shoot levels, while aboveground herbivory increased IG levels in roots in the short term (4 days) but only in the shoots in the longer term (17 days). We conclude that the sequence of aboveground and belowground herbivory is important in interactions between aboveground and belowground herbivores and that knowledge on the timing of exposure is essential to predict outcomes of aboveground–belowground interactions.
Microorganisms and nematodes increase levels of secondary metabolties in roots and root exudates of Plantago lanceolata
Wurst, S. ; Wagenaar, R. ; Biere, A. ; Putten, W.H. van der - \ 2010
Plant and Soil 329 (2010)1-2. - ISSN 0032-079X - p. 117 - 126.
deterrent iridoid glycosides - herbivore damage - responses - defense - generalist - specialist - induction - specificity - chemistry - growth
Plant secondary metabolites play an important role in constitutive and inducible direct defense of plants against their natural enemies. While induction of defense by aboveground pathogens and herbivores is well-studied, induction by belowground organisms is less explored. Here, we examine whether soil microorganisms and nematodes can induce changes in levels of the secondary metabolites aucubin and catalpol (iridoid glycosides, IG) in roots and root exudates of two full-sib families of Plantago lanceolata originating from lines selected for low and high constitutive levels of IG in leaves. Addition of soil microorganisms enhanced the shoot and root biomass, and the concentration of aucubin in roots of both Plantago lines without affecting IG levels in the rhizosphere. By contrast, nematode addition tended to reduce the root biomass and enhanced the stalk biomass, and increased the levels of aucubin and catalpol in root exudates of both Plantago lines, without affecting root IG concentrations. The Plantago lines did not differ in constitutive levels of aucubin and total IG in roots, while the concentration of catalpol was slightly higher in roots of plants originally selected for low constitutive levels of IG in leaves. Root exudates of "high IG line" plants contained significantly higher levels of aucubin, which might be explained by their higher root biomass. We conclude that soil microorganisms can induce an increase of aucubin concentrations in the roots, whereas nematodes (probably plant feeders) lead to an enhancement of aucubin and catalpol levels in root exudates of P. lanceolata. A potential involvement of secondary metabolites in belowground interactions between plants and soil organisms is discussed.
The effect of direct and indirect defenses in two wild brassicaceous plant species on a specialist herbivore and its gregarious endoparasitoid
Gols, R. ; Witjes, L.M.A. ; Loon, J.J.A. van; Posthumus, M.A. ; Dicke, M. ; Harvey, J.A. - \ 2008
Entomologia Experimentalis et Applicata 128 (2008)1. - ISSN 0013-8703 - p. 99 - 108.
parasitoid diaeretiella-rapae - cotesia-rubecula - pieris-rapae - trophic level - host-plant - sequestration - infochemicals - domestication - generalist - induction
Most studies on plant defenses against insect herbivores investigate direct and indirect plant defenses independently. However, these defenses are not necessarily mutually exclusive. Plant metabolites can be transmitted through the food chain and can also affect the herbivore's natural enemies. A conflict may arise when a natural enemy is attracted to a plant that is suboptimal in terms of its own fitness. In addition, plant defenses are often studied in cultivated plant species in which artificial selection may have resulted in reduced resistance against insect herbivores. In this study, we investigated both direct and indirect plant defenses in two closely related wild brassicaceous plant species, Brassica nigra L. and Sinapis arvensis L. The herbivore Pieris brassicae L. (Lepidoptera: Pieridae), which is specialized on brassicaceous plant species, developed faster and attained higher pupal mass when reared on B. nigra than on S. arvensis. In contrast, Cotesia glomerata L. (Hymenoptera: Braconidae), which is a gregarious endoparasitoid of P. brassicae caterpillars, developed equally well on P. brassicae irrespective of the food plant on which its host had been reared. The feeding strategy of the parasitoid larvae, that is, selectively feeding on hemolymph and fat body, is likely to allow for a much wider host-size range without affecting the size or development time of the emerging parasitoids. In flight chamber experiments, C. glomerata, which had an oviposition experience in a host that fed on Brussels sprout, exhibited significant preference for host-damaged B. nigra over host-damaged S. arvensis plants. Headspace analysis revealed quantitative and qualitative differences in volatile emissions between the two plant species. This parasitoid species may use a range of cues associated with the host and the host's food plant in order to recognize the different plant species on which the host can feed. These results show that there is no conflict between direct and indirect plant defenses for this plant¿host¿parasitoid complex.
Increased risk of parasitism as ecological costs of using aggregation pheromones: laboratory and field study of Drosophila-Leptopilina interaction
Wertheim, B. ; Vet, L.E.M. ; Dicke, M. - \ 2003
Oikos 100 (2003)2. - ISSN 0030-1299 - p. 269 - 282.
reliability-detectability problem - heterotoma thomson hymenoptera - foraging behavior - host location - melanogaster - exploitation - eucoilidae - information - generalist - kairomones
Information conveyance plays an important role in parasitoid-host interactions. Several sources of information are available for searching parasitoids and exploitation of that information during the different phases of host location depends on its reliability, detectability and accuracy. One source of information especially suitable for exploitation by parasitoids is a host aggregation pheromone, because this often combines all three aspects. In laboratory and field experiments we studied the behavioural responses of the parasitoid Leptopilina heterotoma to the aggregation pheromone of the fruit fly Drosophila melanogaster, both for substrate selection and the behaviour on host snbstrates. Our results show that substrates with increasing dose of the host's aggregation pheromone attract increasingly more parasitoids, whereas we found no significant effects of pheromone on parasitoid searching behaviour on the substrates. Parasitoid searching behaviour on substrates was influenced by other host cues (e.g. larval exerements, traces of adults other than aggregation pheromone), which is discussed in relation to the expectations from reliability-detectability theory. The responses of the parasitoids were further influenced by substrate quality (i.e. yeast concentration) and the microscale distribution of pheromone. In several field experiments, the fraction of fruit fly larvae that was parasitised was significantly higher in substrates with aggregation pheromone than in control substrates, indicating an ecological cost to the use of aggregation pheromones in adult D. melanogaster.