Information arms race explains plant-herbivore chemical communication in ecological communities

Zu, Pengjuan; Boege, Karina; del‐Val, Ek; Schuman, Meredith C.; Stevenson, Philip C.; Zaldívar‐Riverón, Alejandro; Saavedra, Serguei

doi:10.1126/science.aba2965

Cited by 74 publications

(94 citation statements)

References 47 publications

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“…Overall, plot diversity as well as the local neighbourhood has an impact on the metabolome of root exudates and leaves. Studies on tropical trees have linked metabolomic diversity to differences in insect community composition (Richards et al, 2015, Zu et al, 2020). Our observation that tree diversity affects leaf metabolomes thus may impact herbivore communities on trees of the same species, but growing in plots with different diversity levels.…”

Section: Resultsmentioning

confidence: 99%

Plot diversity differentially affects the chemical composition of leaves, roots and root exudates in four subtropical tree species

Weinhold

Döll

Liu

et al. 2020

Preprint

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Plants produce thousands of compounds, collectively called the metabolome, which mediate interactions with other organisms. The metabolome of an individual plant may change according to the number and nature of these interactions. We tested the hypothesis that tree diversity level affects the metabolome of four subtropical tree species in a biodiversity ecosystem-functioning experiment, BEF-China. We postulated that the chemical diversity of leaves, roots and root exudates increases with tree diversity. We expected the strength of this diversity effect to differ among leaf, root and root exudates samples. Considering their role in plant competition, we expected to find the strongest effects in root exudates.In an ecometabolomics approach, roots, root exudates and leaves of four tree species (Cinnamomum camphora, Cyclobalanopsis glauca, Daphniphyllum oldhamii, Schima superba) were sampled from selected plots in BEF-China. Samples were extracted and analysed using Liquid Chromatography-Time of Flight-Mass Spectrometry. The exudate metabolomes were normalized over their non-purgeable organic carbon level. Multivariate analyses were applied to identify the effect of both neighbouring (local) trees and plot diversity on tree metabolomes. The species and sample specific metabolites were assigned to major compound classes using the ClassyFire tool, whereas m/z features related to diversity effects were annotated manually.Individual tree species showed distinct leaf, root and root exudate metabolomes. The main compound class in leaves were the flavonoids, whereas carboxylic acids, prenol lipids and specific alkaloids were most prominent in root exudates and roots. Overall plot diversity had a stronger effect on metabolome profiles than the diversity of local, directly neighbouring trees. Leaf metabolomes responded more often to tree diversity level than exudates, whereas root metabolomes varied the least. We found not overall correlation between metabolite richness or diversity and tree diversity.Synthesis: Classification of metabolites supported initial ecological interpretation of differences among species and organs. Particularly the metabolomes of leaves and root exudates respond to differences in tree diversity. These responses were neither linear nor uniform and individual metabolites showed different dynamics. More controlled interaction experiments are needed to dissect the causes and consequences of the observed shifts in plant metabolomes.

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Section: Resultsmentioning

confidence: 99%

Plot diversity differentially affects the chemical composition of leaves, roots and root exudates in four subtropical tree species

Weinhold

Döll

Liu

et al. 2020

Preprint

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“…We previously showed that BPH preferentially oviposits on SSB-infested rice plants, thereby avoiding the attraction of the egg parasitoid Anagrus nilaparvatae 25 . These various examples confirm that insect herbivores not only can evolve the ability to use volatiles to identify host plants of better nutritional quality, but also plants where their offspring can escape natural enemies 50 .…”

Section: Discussionmentioning

confidence: 70%

Cooperative herbivory between two important pests of rice

Liu

et al. 2021

Preprint

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Normally, when different species of herbivorous arthropods feed on the same plant this leads to fitness reducing competition. We found this to be uniquely different for two of Asia's most destructive rice pests, the brown planthopper and the rice striped stem borer. Both insects directly and indirectly benefit from jointly attacking the same host plant. Double infestation improved plant quality, particularly for the stemborer because the planthopper fully suppresses caterpillar-induced production of proteinase inhibitors. It also drastically reduced the risk of egg parasitism, due to diminished parasitoid attraction. Females of both pests have adapted their oviposition behaviour accordingly. Their strong preference for plants infested by the other species even overrides their avoidance of plants already attacked by conspecifics. This uncovered cooperation between herbivores is telling of the exceptional adaptations resulting from the evolution of plant-insect interactions, and points out mechanistic vulnerabilities that can be targeted to control two major pests.

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“…For example, Zu et al. (2020) suggested that seemingly redundant volatile organic compounds play an important role in confusing herbivores at the community level. Konstantopoulou et al.…”

Section: Introductionmentioning

confidence: 99%

Plant volatiles mediate evolutionary interactions between plants and tephritid flies and are evolutionarily more labile than non‐volatile defenses

Wang

Zhou

et al. 2021

Journal of Animal Ecology

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Studies show that plant defenses influence the host‐use of herbivores and tend to be evolutionarily more labile than herbivore traits (e.g. feeding preferences). However, all previous studies have focused exclusively on non‐volatile plant defenses thereby overlooking the roles of plant volatiles. We hypothesized that volatiles are equally important determinants of herbivore host‐use and are evolutionarily more labile than herbivore traits. To test these hypotheses, the following experiments were conducted. We identified the volatiles and non‐volatiles of 17 Asteraceae species and measured their relative contents. We also used a highly resolved bipartite trophic network of the 17 host species and 20 herbivorous (pre‐dispersal seed predator) tephritid fly species to determine the evolutionary interactions between plants and herbivores. The chemical data showed that interspecific similarity in volatiles—but not non‐volatiles and phylogenetic distance—significantly accounted for the herbivore community across the plant species; this implies that plant volatiles—but not non‐volatile compounds and species identity—dictate plant‐tephritid fly interactions. Moreover, we observed phylogenetic signal for non‐volatiles but not for volatiles; therefore closely related herbivores do not necessarily use closely related host species with similar non‐volatiles, but do tend to attack plants producing similar volatiles. Thus, plant volatiles are evolutionarily more labile than non‐volatiles and herbivore traits associate with host use. These results show that the interactions between plants and herbivores are evolutionary asymmetric, shed light on the role of plant volatiles in plant–herbivore interactions, and highlight the need to include data for both volatiles and non‐volatiles when investigating plant–animal interactions.

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Information arms race explains plant-herbivore chemical communication in ecological communities

Cited by 74 publications

References 47 publications

Plot diversity differentially affects the chemical composition of leaves, roots and root exudates in four subtropical tree species

Plot diversity differentially affects the chemical composition of leaves, roots and root exudates in four subtropical tree species

Cooperative herbivory between two important pests of rice

Plant volatiles mediate evolutionary interactions between plants and tephritid flies and are evolutionarily more labile than non‐volatile defenses

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