Herbivore-Mediated Effects of Glucosinolates on Different Natural Enemies of a Specialist Aphid

Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands.
Journal of Chemical Ecology (Impact Factor: 2.75). 01/2012; 38(1):100-15. DOI: 10.1007/s10886-012-0065-2
Source: PubMed


The cabbage aphid Brevicoryne brassicae is a specialist herbivore that sequesters glucosinolates from its host plant as a defense against its predators. It is unknown to what extent parasitoids are affected by this sequestration. We investigated herbivore-mediated effects of glucosinolates on the parasitoid wasp Diaeretiella rapae and the predator Episyrphus balteatus. We reared B. brassicae on three ecotypes of Arabidopsis thaliana that differ in glucosinolate content and on one genetically transformed line with modified concentrations of aliphatic glucosinolates. We tested aphid performance and the performance and behavior of both natural enemies. We correlated this with phloem and aphid glucosinolate concentrations and emission of volatiles. Brevicoryne brassicae performance correlated positively with concentrations of both aliphatic and indole glucosinolates in the phloem. Aphids selectively sequestered glucosinolates. Glucosinolate concentration in B. brassicae correlated negatively with performance of the predator, but positively with performance of the parasitoid, possibly because the aphids with the highest glucosinolate concentrations had a higher body weight. Both natural enemies showed a positive performance-preference correlation. The predator preferred the ecotype with the lowest emission of volatile glucosinolate breakdown products in each test combination, whereas the parasitoid wasp preferred the A. thaliana ecotype with the highest emission of these volatiles. The study shows that there are differential herbivore-mediated effects of glucosinolates on a predator and a parasitoid of a specialist aphid that selectively sequesters glucosinolates from its host plant.

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    • "Herbivorous insects are well-documented biotic factors that affect the emission of plant volatile blends (Van Poecke, 2007; Dicke et al., 2009; Holopainen and Gershenzon, 2010; Kos et al., 2012; Louis et al., 2012). Of these, phloem-feeding insects can cause minor damage to plant foliage following infestations due to their salivary chemicals and/or proteins that act as signaling factors to affect the biosynthesis of volatile compounds by plants (Walling, 2000; De Vos and Jander, 2009). "
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    ABSTRACT: Emissions of volatile organic compounds (VOCs) by water-controlled or water-stressed Arabidopsis thaliana infested or not infested with Myzus persicae were evaluated by headspace solid phase microextraction (HS-SPME) coupled with gas chromatography-mass spectrometry (GC-MS). The infestations were maintained for 0–24 h, 24–48 h, and 48–72 h, and the emission profile for each time period was determined. Under these controlled conditions, the proportion of 4-methylpentyl isothiocyanate and dimethyl disulfide emitted by aphid-infested, water-stressed Arabidopsis was greater than that for aphid-infested water-controlled Arabidopsis over the 48–72 h sampling period. The proportion of terpene emitted by aphid-infested water-stressed plants also significantly increased compared with the other treatments over the three assayed sampling periods. In contrast, the proportion of 2-ethylhexanal (the only detected aldehyde) and ketones for the water-controlled plants generally remained high following aphid infestation. Taken together, these original data ascertain that abiotic factors can greatly interact to biotic stresses to alter the VOC emission profiles of plants.
    Full-text · Article · Dec 2014
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    • "An earlier study showed that Myzus persicae also induced 4- methoxyglucobrassicin levels in A. thaliana, which enhanced resistance to this generalist aphid species (Kim and Jander 2007). It is not known whether 4-methoxyglucobrassicin or its breakdown products (Agerbirk et al. 2009) could affect this specialist aphid, but in a multivariate analysis, Kos et al. (2012) found a positive correlation between 4-methoxyglucobrassicin and aphid adult weight as well as number of offspring. Nematodes did not affect 4-methoxyglucobrassicin, but changed the levels of several other glucosinolates in the shoots. "
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    ABSTRACT: Aboveground and belowground herbivore species modify plant defense responses differently. Simultaneous attack can lead to non-additive effects on primary and secondary metabolite composition in roots and shoots. We previously found that aphid (Brevicoryne brassicae) population growth on Brassica oleracea was reduced on plants that were infested with nematodes (Heterodera schachtii) prior (4 weeks) to aphid infestation. Here, we examined how infection with root-feeding nematodes affected primary and secondary metabolites in the host plant and whether this could explain the increase in aphid doubling time from 3.8 to 6.7 days. We hypothesized that the effects of herbivores on plant metabolites would depend on the presence of the other herbivore and that nematode-induced changes in primary metabolites would correlate with reduced aphid performance. Total glucosinolate concentration in the leaves was not affected by nematode presence, but the composition of glucosinolates shifted, as gluconapin concentrations were reduced, while gluconapoleiferin concentrations increased in plants exposed to nematodes. Aphid presence increased 4-methoxyglucobrassicin concentrations in leaves, which correlated positively with the number of aphids per plant. Nematodes decreased amino acid and sugar concentrations in the phloem. Aphid population doubling time correlated negatively with amino acids and glucosinolate levels in leaves, whereas these correlations were non-significant when nematodes were present. In conclusion, the effects of an herbivore on plant metabolites were independent of the presence of another herbivore. Nematode presence reduced aphid population growth and disturbed feeding relations between plants and aphids. Electronic supplementary material The online version of this article (doi:10.1007/s10886-013-0338-4) contains supplementary material, which is available to authorized users.
    Full-text · Article · Sep 2013 · Journal of Chemical Ecology
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    • "Herbivore host size is considered a key factor influencing parasitoid performance (Bukovinszky et al., 2012; Ode, 2006; Vinson and Iwantsch, 1980), and large compared to small hosts are expected to offer more resources for development of parasitoid offspring (Häckermann et al., 2007). Under ambient CO 2 , it has most recently been shown that feeding on plants containing higher phloem glucosinolate contents resulted in larger aphids, sustaining high performance of the same parasitoid (Kos et al., 2012). However, we show that under elevated CO 2 , feeding on plants containing higher leaf glucosinolate contents resulted in smaller aphids, sustaining lower performance of the parasitoid. "
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    ABSTRACT: Elevated concentrations of atmospheric carbon dioxide (CO2), a consequence of anthropogenic global change, may profoundly interfere with tritrophic interactions. Such effects with a focus on parasitoids as natural antagonists of herbivores have rarely been investigated. In particular, studies on effects of secondary metabolites induced by crop plant acclimation to elevated CO2 on higher trophic levels were yet missing. We used the system composed of Brassica plants, the aphid Brevicoryne brassicae and the endoparasitoid Diaeretiella rapae, which is specialized on aphids feeding on brassicacean plants, to compare effects of elevated CO2 (800 ppm) versus ambient CO2 (400 ppm). Plants were exposed to the CO2 concentrations for up to 10 weeks, aphids for 2–3 generations, and parasitoids for 1 generation, to allow for acclimation. Concomitant bioassays with herbivore-infested plants and parasitoids showed a significantly lower proportion of hosts parasitized under elevated compared to ambient CO2 after a 10-week plant exposure. Parasitoid progeny emerged earlier but offspring adults were shorter lived. Plant glucosinolate concentrations were higher under elevated compared to ambient CO2, whereas, contrary to expectation, aphid glucosinolate concentrations were significantly lower. Likewise aphid body mass remained approximately 20% lower under elevated compared to ambient CO2. Thus, elevated CO2 seems to have enhanced plant direct defense by an increase of natural plant defense compounds, however, it led to a decrease in indirect defense, likely due to the reduced host size. Our results point, for the first time, to a conflict between bottom-up and top-down control under elevated CO2.
    Full-text · Article · Jul 2013 · Biological Control
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