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Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance.

ABSTRACT: Insect herbivores are frequently reported to metabolize plant defense compounds, but the physiological and ecological consequences are not fully understood. It has rarely been studied whether such metabolism is genuinely beneficial to the insect, and whether there are any effects on higher trophic levels. Here, we manipulated the detoxification of plant defenses in the herbivorous pest diamondback moth (Plutella xylostella) to evaluate changes in fitness, and additionally examined the effects on a predatory lacewing (Chrysoperla carnea). Silencing glucosinolate sulfatase genes resulted in the systemic accumulation of toxic isothiocyanates in P. xylostella larvae, impairing larval development and adult reproduction. The predatory lacewing C. carnea, however, efficiently degraded ingested isothiocyanates via a general conjugation pathway, with no negative effects on survival, reproduction, or even prey preference. These results illustrate how plant defenses and their detoxification strongly influence herbivore fitness but might only subtly affect a third trophic level.

SUBMITTER: Sun R

PROVIDER: S-EPMC6934381 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance.

Sun Ruo R Jiang Xingcong X Reichelt Michael M Gershenzon Jonathan J Pandit Sagar Subhash SS Giddings Vassão Daniel D

eLife 20191216

Insect herbivores are frequently reported to metabolize plant defense compounds, but the physiological and ecological consequences are not fully understood. It has rarely been studied whether such metabolism is genuinely beneficial to the insect, and whether there are any effects on higher trophic levels. Here, we manipulated the detoxification of plant defenses in the herbivorous pest diamondback moth (<i>Plutella xylostella</i>) to evaluate changes in fitness, and additionally examined the eff ...[more]

PMID: 31841109

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Project description: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.

Project description:Plant-herbivore interactions are influenced by host plant quality which in turn is affected by plant growth conditions. Competition is the major biotic and nutrient availability a major abiotic component of a plant's growth environment. Yet, surprisingly few studies have investigated impacts of competition and nutrient availability on herbivore performance and reciprocal herbivore effects on plants. We studied growth of the specialist aphid, Macrosiphoniella tanacetaria, and its host plant tansy, Tanacetum vulgare, under experimental addition of inorganic and organic fertilizer crossed with competition by goldenrod, Solidago canadensis. Because of evidence that competition by goldenrod is mediated by allelopathic compounds, we also added a treatment with activated carbon. Results showed that fertilization increased, and competition with goldenrod decreased, plant biomass, but this was likely mediated by resource competition. There was no evidence from the activated carbon treatment that allelopathy played a role which instead had a fertilizing effect. Aphid performance increased with higher plant biomass and depended on plant growth conditions, with fertilization and AC increasing, and plant competition decreasing aphid numbers. Feedbacks of aphids on plant performance interacted with plant growth conditions in complex ways depending on the relative magnitude of the effects on plant biomass and aphid numbers. In the basic fertilization treatment, tansy plants profited from increased nutrient availability by accumulating more biomass than they lost due to an increased number of aphids under fertilization. When adding additional fertilizer, aphid numbers increased so high that tansy plants suffered and showed reduced biomass compared with controls without aphids. Thus, the ecological cost of an infestation with aphids depends on the balance of effects of growth conditions on plant and herbivore performance. These results emphasize the importance to investigate both perspectives in plant herbivore interactions and characterize the effects of growth conditions on plant and herbivore performance and their respective feedbacks.

Dataset Information

Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance.

Publications

Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance.

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