Dataset Information

Modulation of plant-mediated interactions between herbivores of different feeding guilds: Effects of parasitism and belowground interactions.

ABSTRACT: Herbivory affects subsequent herbivores, mainly regulated by the phytohormones jasmonic (JA) and salicylic acid (SA). Additionally, organisms such as soil microbes belowground or parasitoids that develop inside their herbivorous hosts aboveground, can change plant responses to herbivory. However, it is not yet well known how organisms of trophic levels other than herbivores, below- and above-ground, alter the interactions between insect species sharing a host plant. Here, we investigated whether the parasitoid Aphidius colemani and different soil microbial communities (created through plant-soil feedbacks) affect the JA and SA signalling pathways in response to the aphid Myzus persicae and the thrips Frankliniella occidentalis, as well as subsequent thrips performance. Our results show that the expression of the JA-responsive gene CaPINII in sweet pepper was more suppressed by aphids than by parasitised aphids. However, parasitism did not affect the expression of CaPAL1, a biosynthetic gene of SA. Furthermore, aphid feeding enhanced thrips performance compared with uninfested plants, but this was not observed when aphids were parasitised. Soils where different plant species were previously grown, did not affect plant responses or the interaction between herbivores. Our study shows that members of the third trophic level can modify herbivore interactions by altering plant physiology.

SUBMITTER: Vaello T

PROVIDER: S-EPMC6158277 | biostudies-other | 2018 Sep

REPOSITORIES: biostudies-other

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Modulation of plant-mediated interactions between herbivores of different feeding guilds: Effects of parasitism and belowground interactions.

Vaello Teresa T Sarde Sandeep J SJ Marcos-García Mª Ángeles MÁ de Boer Jetske G JG Pineda Ana A

Scientific reports 20180926 1

Herbivory affects subsequent herbivores, mainly regulated by the phytohormones jasmonic (JA) and salicylic acid (SA). Additionally, organisms such as soil microbes belowground or parasitoids that develop inside their herbivorous hosts aboveground, can change plant responses to herbivory. However, it is not yet well known how organisms of trophic levels other than herbivores, below- and above-ground, alter the interactions between insect species sharing a host plant. Here, we investigated whether ...[more]

PMID: 30258118

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Project description:Plants show ontogenetic variation in growth-defence strategies to maximize reproductive output within a community context. Most work on plant ontogenetic variation in growth-defence trade-offs has focussed on interactions with antagonistic insect herbivores. Plants respond to herbivore attack with phenotypic changes. Despite the knowledge that plant responses to herbivory affect plant mutualistic interactions with pollinators required for reproduction, indirect interactions between herbivores and pollinators have not been included in the evaluation of how ontogenetic growth-defence trajectories affect plant fitness.In a common garden experiment with the annual Brassica nigra, we investigated whether exposure to various herbivore species on different plant ontogenetic stages (vegetative, bud or flowering stage) affects plant flowering traits, interactions with flower visitors and results in fitness consequences for the plant.Effects of herbivory on flowering plant traits and interactions with flower visitors depended on plant ontogeny. Plant exposure in the vegetative stage to the caterpillar Pieris brassicae and aphid Brevicoryne brassicae led to reduced flowering time and flower production, and resulted in reduced pollinator attraction, pollen beetle colonization, total seed production and seed weight. When plants had buds, infestation by most herbivore species tested reduced flower production and pollen beetle colonization. Pollinator attraction was either increased or reduced. Plants infested in the flowering stage with P. brassicae or Lipaphis erysimi flowered longer, while infestation by any of the herbivore species tested increased the number of flower visits by pollinators.Our results show that the outcome of herbivore-flower visitor interactions in B. nigra is specific for the combination of herbivore species and plant ontogenetic stage. Consequences of herbivory for flowering traits and reproductive output were strongest when plants were attacked early in life. Such differences in selection pressures imposed by herbivores to specific plant ontogenetic stages may drive the evolution of distinct ontogenetic trajectories in growth-defence-reproduction strategies and include indirect interactions between herbivores and flower visitors. Synthesis. Plant ontogeny can define the direct and indirect consequences of herbivory. Our study shows that the ontogenetic stage of plant individuals determined the effects of herbivory on plant flowering traits, interactions with flower visitors and plant fitness.

Project description:Plants are often exposed to multiple herbivores and densities of these attackers (or corresponding damage intensities) often fluctuate greatly in the field. Plant-mediated interactions vary among herbivore species and with changing feeding intensity, but little is known about how herbivore identity and density interact to determine plant responses and herbivore fitness. Here, we investigated this question using Triadica sebifera (tallow) and two common and abundant specialist insect herbivores, Bikasha collaris (flea beetle) and Heterapoderopsis bicallosicollis (weevil). By manipulating densities of leaf-feeding adults of these two herbivore species, we tested how variations in the intensity of leaf damage caused by flea beetle or weevil adults affected the performance of root-feeding flea beetle larvae and evaluated the potential of induced tallow root traits to predict flea beetle larval performance. We found that weevil adults consistently decreased the survival of flea beetle larvae with increasing leaf damage intensities. In contrast, conspecific flea beetle adults increased their larval survival at low damage then decreased larval survival at high damage, resulting in a unimodal pattern. Chemical analyses showed that increasing leaf damage from weevil adults linearly decreased root carbohydrates and increased root tannin, whereas flea beetle adults had opposite effects as weevil adults at low damage and similar effects as them at high damage. Furthermore, across all feeding treatments, flea beetle larval survival correlated positively with concentrations of carbohydrates and negatively with concentration of tannin, suggesting that root primary and secondary metabolism might underlie the observed effects on flea beetle larvae. Our study demonstrates that herbivore identity and density interact to determine systemic plant responses and plant-mediated effects on herbivores. In particular, effects are species-specific at low densities, but converge at high densities. These findings emphasize the importance of considering herbivore identity and density simultaneously when investigating factors driving plant-mediated interactions between herbivores, which advances our understanding of the structure and composition of herbivore communities and terrestrial food webs.

Dataset Information

Modulation of plant-mediated interactions between herbivores of different feeding guilds: Effects of parasitism and belowground interactions.

Publications

Modulation of plant-mediated interactions between herbivores of different feeding guilds: Effects of parasitism and belowground interactions.

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