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1.  Differences in Volatile Profiles of Turnip Plants Subjected to Single and Dual Herbivory Above- and Belowground 
Journal of Chemical Ecology  2011;37(4):368-377.
Plants attacked by herbivorous insects emit volatile organic compounds that are used by natural enemies to locate their host or prey. The composition of the blend is often complex and specific. It may vary qualitatively and quantitatively according to plant and herbivore species, thus providing specific information for carnivorous arthropods. Most studies have focused on simple interactions that involve one species per trophic level, and typically have investigated the aboveground parts of plants. These investigations need to be extended to more complex networks that involve multiple herbivory above- and belowground. A previous study examined whether the presence of the leaf herbivore Pieris brassicae on turnip plants (Brassica rapa subsp. rapa) influences the response of Trybliographa rapae, a specialist parasitoid of the root feeder Delia radicum. It showed that the parasitoid was not attracted by volatiles emitted by plants under simultaneous attack. Here, we analyzed differences in the herbivore induced plant volatile (HIPV) mixtures that emanate from such infested plants by using Orthogonal Partial Least Squares-Discriminant Analysis (OPLS-DA). This multivariate model focuses on the differences between odor blends, and highlights the relative importance of each compound in an HIPV blend. Dual infestation resulted in several HIPVs that were present in both isolated infestation types. However, HIPVs collected from simultaneously infested plants were not the simple combination of volatiles from isolated forms of above- and belowground herbivory. Only a few specific compounds characterized the odor blend of each type of damaged plant. Indeed, some compounds were specifically induced by root herbivory (4-methyltridecane and salicylaldehyde) or shoot herbivory (methylsalicylate), whereas hexylacetate, a green leaf volatile, was specifically induced after dual herbivory. It remains to be determined whether or not these minor quantitative variations, within the background of more commonly induced odors, are involved in the reduced attraction of the root feeder’s parasitoid. The mechanisms involved in the specific modification of the odor blends emitted by dual infested turnip plants are discussed in the light of interferences between biosynthetic pathways linked to plant responses to shoot or root herbivory.
PMCID: PMC3197925  PMID: 21448706
Plant–insect interactions; Multiple herbivory; Volatile organic compounds; Parasitoid; Trybliographa rapae; Delia radicum; Pieris brassicae; Brassicaceae
2.  Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid 
Oecologia  2007;152(2):257-264.
The majority of studies exploring interactions between above- and below-ground biota have been focused on the effects of root-associated organisms on foliar herbivorous insects. This study examined the effects of foliar herbivory by Pieris brassicae L. (Lepidoptera: Pieridae) on the performance of the root herbivore Delia radicum L. (Diptera: Anthomyiidae) and its parasitoid Trybliographa rapae (Westwood) (Hymenoptera: Figitidae), mediated through a shared host plant Brassica nigra L. (Brassicaceae). In the presence of foliar herbivory, the survival of D. radicum and T. rapae decreased significantly by more than 50%. In addition, newly emerged adults of both root herbivores and parasitoids were significantly smaller on plants that had been exposed to foliar herbivory than on control plants. To determine what factor(s) may have accounted for the observed results, we examined the effects of foliar herbivory on root quantity and quality. No significant differences in root biomass were found between plants with and without shoot herbivore damage. Moreover, concentrations of nitrogen in root tissues were also unaffected by shoot damage by P. brassicae larvae. However, higher levels of indole glucosinolates were measured in roots of plants exposed to foliar herbivory, suggesting that the development of the root herbivore and its parasitoid may be, at least partly, negatively affected by increased levels of these allelochemicals in root tissues. Our results show that foliar herbivores can affect the development not only of root-feeding insects but also their natural enemies. We argue that such indirect interactions between above- and below-ground biota may play an important role in the structuring and functioning of communities.
PMCID: PMC1915602  PMID: 17334787
Above-/below-ground interactions; Delia radicum; Glucosinolates; Plant–insect interactions; Trybliographa rapae
3.  Identification of Biologically Relevant Compounds in Aboveground and Belowground Induced Volatile Blends 
Journal of Chemical Ecology  2010;36(9):1006-1016.
Plants under attack by aboveground herbivores emit complex blends of volatile organic compounds (VOCs). Specific compounds in these blends are used by parasitic wasps to find their hosts. Belowground induction causes shifts in the composition of aboveground induced VOC blends, which affect the preference of parasitic wasps. To identify which of the many volatiles in the complex VOC blends may explain parasitoid preference poses a challenge to ecologists. Here, we present a case study in which we use a novel bioinformatics approach to identify biologically relevant differences between VOC blends of feral cabbage (Brassica oleracea L.). The plants were induced aboveground or belowground with jasmonic acid (JA) and shoot feeding caterpillars (Pieris brassicae or P. rapae). We used Partial Least Squares—Discriminant Analysis (PLSDA) to integrate and visualize the relation between plant-emitted VOCs and the preference of female Cotesia glomerata. Overall, female wasps preferred JA-induced plants over controls, but they strongly preferred aboveground JA-induced plants over belowground JA-induced plants. PLSDA revealed that the emission of several monoterpenes was enhanced similarly in all JA-treated plants, whereas homoterpenes and sesquiterpenes increased exclusively in aboveground JA-induced plants. Wasps may use the ratio between these two classes of terpenes to discriminate between aboveground and belowground induced plants. Additionally, it shows that aboveground applied JA induces different VOC biosynthetic pathways than JA applied to the root. Our bioinformatic approach, thus, successfully identified which VOCs matched the preferences of the wasps in the various choice tests. Additionally, the analysis generated novel hypotheses about the role of JA as a signaling compound in aboveground and belowground induced responses in plants.
PMCID: PMC2941087  PMID: 20737198
Aboveground-belowground interactions; Volatile organic compounds; Indirect defenses; Multivariate analysis; Terpenes; Jasmonic acid; Parasitoid preference; PLSDA
4.  Belowground induction by Delia radicum or phytohormones affect aboveground herbivore communities on field-grown broccoli 
Induced plant defence in response to phytophagous insects is a well described phenomenon. However, so far little is known about the effect of induced plant responses on subsequently colonizing herbivores in the field. Broccoli plants were induced in the belowground compartment using (i) infestation by the root-herbivore Delia radicum, (ii) root application of jasmonic acid (JA) or (iii) root application of salicylic acid (SA). The abundance of D. radicum and six aboveground herbivores displaying contrasting levels of host specialization were surveyed for 5 weeks. Our study showed that the response of herbivores was found to differ from one another, depending on the herbivore species, its degree of specialization and the root treatment. The abundance of the root herbivore D. radicum and particularly the number of emerging adults was decreased by both phytohormone treatments, while the number of D. radicum eggs was increased on conspecific infested plants. The root infestation exhibited moderate effects on the aboveground community. The abundance of the aphid Brevicoryne brassicae was strongly increased on D. radicum infested plants, but the other species were not impacted. Root hormone applications exhibited a strong effect on the abundance of specialist foliar herbivores. A higher number of B. brassicae and Pieris brassicae and a lower number of Plutella xylostella were found on JA treated plants. On SA treated plants we observed a decrease of the abundance of B. brassicae, Pi. rapae, and P. xylostella. Surprisingly, generalist species, Mamestra brassicae and Myzus persicae were not affected by root induction treatments. Finally, root treatments had no significant effect on either glucosinolate (GLS) profiles of the heads or on plant quality parameters. These results are discussed from the perspective of below- aboveground interactions and adaptations of phytophagous insects to induced plant responses according to their trophic specialization level.
PMCID: PMC3748748  PMID: 23970888
plant-mediated above-belowground interactions; induced plant defence; Brassica spp; root herbivory; phytohormones
5.  Tracing Hidden Herbivores: Time-Resolved Non-Invasive Analysis of Belowground Volatiles by Proton-Transfer-Reaction Mass Spectrometry (PTR-MS) 
Journal of Chemical Ecology  2012;38(6):785-794.
Root herbivores are notoriously difficult to study, as they feed hidden in the soil. However, root herbivores may be traced by analyzing specific volatile organic compounds (VOCs) that are produced by damaged roots. These VOCs not only support parasitoids in the localization of their host, but also may help scientists study belowground plant-herbivore interactions. Herbivore-induced VOCs are usually analyzed by gas-chromatography mass spectrometry (GC-MS), but with this off-line method, the gases of interest need to be preconcentrated, and destructive sampling is required to assess the level of damage to the roots. In contrast to this, proton-transfer-reaction mass spectrometry (PTR-MS) is a very sensitive on-line, non-invasive method. PTR-MS already has been successfully applied to analyze VOCs produced by aboveground (infested) plant parts. In this review, we provide a brief overview of PTR-MS and illustrate how this technology can be applied to detect specific root-herbivore induced VOCs from Brassica plants. We also specify the advantages and disadvantages of PTR-MS analyses and new technological developments to overcome their limitations.
PMCID: PMC3375075  PMID: 22592334
Chemical ecology; Root herbivory; Trace gas analysis; Induced indirect defense; Mass spectrometry; Volatile organic compound (VOC)
6.  Parasitoids select plants more heavily infested with their caterpillar hosts: a new approach to aid interpretation of plant headspace volatiles 
Plants produce volatile organic compounds (VOCs) in response to herbivore attack, and these VOCs can be used by parasitoids of the herbivore as host location cues. We investigated the behavioural responses of the parasitoid Cotesia vestalis to VOCs from a plant–herbivore complex consisting of cabbage plants (Brassica oleracea) and the parasitoids host caterpillar, Plutella xylostella. A Y-tube olfactometer was used to compare the parasitoids' responses to VOCs produced as a result of different levels of attack by the caterpillar and equivalent levels of mechanical damage. Headspace VOC production by these plant treatments was examined using gas chromatography–mass spectrometry. Cotesia vestalis were able to exploit quantitative and qualitative differences in volatile emissions, from the plant–herbivore complex, produced as a result of different numbers of herbivores feeding. Cotesia vestalis showed a preference for plants with more herbivores and herbivore damage, but did not distinguish between different levels of mechanical damage. Volatile profiles of plants with different levels of herbivores/herbivore damage could also be separated by canonical discriminant analyses. Analyses revealed a number of compounds whose emission increased significantly with herbivore load, and these VOCs may be particularly good indicators of herbivore number, as the parasitoid processes cues from its external environment.
PMCID: PMC3136836  PMID: 21270031
herbivore-induced plant volatiles; Hymenoptera; Lepidoptera; parasitoid host location; tritrophic; volatile organic compounds
7.  Herbivore-induced maize leaf volatiles affect attraction and feeding behavior of Spodoptera littoralis caterpillars 
Plants under herbivore attack emit volatile organic compounds (VOCs) that can serve as foraging cues for natural enemies. Adult females of Lepidoptera, when foraging for host plants to deposit eggs, are commonly repelled by herbivore-induced VOCs, probably to avoid competition and natural enemies. Their larval stages, on the other hand, have been shown to be attracted to inducible VOCs. We speculate that this contradicting behavior of lepidopteran larvae is due to a need to quickly find a new suitable host plant if they have fallen to the ground. However, once they are on a plant they might avoid the sites with fresh damage to limit competition and risk of cannibalism by conspecifics, as well as exposure to natural enemies. To test this we studied the effect of herbivore-induced VOCs on the attraction of larvae of the moth Spodoptera littoralis and on their feeding behavior. The experiments further considered the importance of previous feeding experience on the responses of the larvae. It was confirmed that herbivore-induced VOCs emitted by maize plants are attractive to the larvae, but exposure to the volatiles decreased the growth rate of caterpillars at early developmental stages. Larvae that had fed on maize previously were more attracted by VOCs of induced maize than larvae that had fed on artificial diet. At relatively high concentrations synthetic green leaf volatiles, indicative of fresh damage, also negatively affected the growth rate of caterpillars, but not at low concentrations. In all cases, feeding by the later stages of the larvae was not affected by the VOCs. The results are discussed in the context of larval foraging behavior under natural conditions, where there may be a trade-off between using available host plant signals and avoiding competitors and natural enemies.
PMCID: PMC3695448  PMID: 23825475
Spodoptera littoralis; green leaf volatiles; maize; larval foraging behavior; host plant suitability
8.  The Composite Effect of Transgenic Plant Volatiles for Acquired Immunity to Herbivory Caused by Inter-Plant Communications 
PLoS ONE  2011;6(10):e24594.
A blend of volatile organic compounds (VOCs) emitted from plants induced by herbivory enables the priming of defensive responses in neighboring plants. These effects may provide insights useful for pest control achieved with transgenic-plant-emitted volatiles. We therefore investigated, under both laboratory and greenhouse conditions, the priming of defense responses in plants (lima bean and corn) by exposing them to transgenic-plant-volatiles (VOCos) including (E)-β-ocimene, emitted from transgenic tobacco plants (NtOS2) that were constitutively overexpressing (E)-β-ocimene synthase. When lima bean plants that had previously been placed downwind of NtOS2 in an open-flow tunnel were infested by spider mites, they were more defensive to spider mites and more attractive to predatory mites, in comparison to the infested plants that had been placed downwind of wild-type tobacco plants. This was similarly observed when the NtOS2-downwind maize plants were infested with Mythimna separata larvae, resulting in reduced larval growth and greater attraction of parasitic wasps (Cotesia kariyai). In a greenhouse experiment, we also found that lima bean plants (VOCos-receiver plants) placed near NtOS2 were more attractive when damaged by spider mites, in comparison to the infested plants that had been placed near the wild-type plants. More intriguingly, VOCs emitted from infested VOCos-receiver plants affected their conspecific neighboring plants to prime indirect defenses in response to herbivory. Altogether, these data suggest that transgenic-plant-emitted volatiles can enhance the ability to prime indirect defenses via both plant-plant and plant-plant-plant communications.
PMCID: PMC3192036  PMID: 22022359
9.  Flower vs. Leaf Feeding by Pieris brassicae: Glucosinolate-Rich Flower Tissues are Preferred and Sustain Higher Growth Rate 
Journal of Chemical Ecology  2007;33(10):1831-1844.
Interactions between butterflies and caterpillars in the genus Pieris and plants in the family Brassicaceae are among the best explored in the field of insect–plant biology. However, we report here for the first time that Pieris brassicae, commonly assumed to be a typical folivore, actually prefers to feed on flowers of three Brassica nigra genotypes rather than on their leaves. First- and second-instar caterpillars were observed to feed primarily on leaves, whereas late second and early third instars migrated via the small leaves of the flower branches to the flower buds and flowers. Once flower feeding began, no further leaf feeding was observed. We investigated growth rates of caterpillars having access exclusively to either leaves of flowering plants or flowers. In addition, we analyzed glucosinolate concentrations in leaves and flowers. Late-second- and early-third-instar P. brassicae caterpillars moved upward into the inflorescences of B. nigra and fed on buds and flowers until the end of the final (fifth) instar, after which they entered into the wandering stage, leaving the plant in search of a pupation site. Flower feeding sustained a significantly higher growth rate than leaf feeding. Flowers contained levels of glucosinolates up to five times higher than those of leaves. Five glucosinolates were identified: the aliphatic sinigrin, the aromatic phenyethylglucosinolate, and three indole glucosinolates: glucobrassicin, 4-methoxyglucobrassicin, and 4-hydroxyglucobrassicin. Tissue type and genotype were the most important factors affecting levels of identified glucosinolates. Sinigrin was by far the most abundant compound in all three genotypes. Sinigrin, 4-hydroxyglucobrassicin, and phenylethylglucosinolate were present at significantly higher levels in flowers than in leaves. In response to caterpillar feeding, sinigrin levels in both leaves and flowers were significantly higher than in undamaged plants, whereas 4-hydroxyglucobrassicin leaf levels were lower. Our results show that feeding on flower tissues, containing higher concentrations of glucosinolates, provides P. brassicae with a nutritional benefit in terms of higher growth rate. This preference appears to be in contrast to published negative effects of volatile glucosinolate breakdown products on the closely related Pieris rapae.
PMCID: PMC2039843  PMID: 17828429
Herbivory; Lepidoptera; Pieridae; Myrosinase; Isothiocyanates; Nutrition; Brassica nigra
10.  Priming of Production in Maize of Volatile Organic Defence Compounds by the Natural Plant Activator cis-Jasmone 
PLoS ONE  2013;8(6):e62299.
cis-Jasmone (CJ) is a natural plant product that activates defence against herbivores in model and crop plants. In this study, we investigated whether CJ could prime defence in maize, Zea mays, against the leafhopper, Cicadulina storeyi, responsible for the transmission of maize streak virus (MSV). Priming occurs when a pre-treatment, in this case CJ, increases the potency and speed of a defence response upon subsequent attack on the plant. Here, we tested insect responses to plant volatile organic compounds (VOCs) using a Y-tube olfactometer bioassay. Our initial experiments showed that, in this system, there was no significant response of the herbivore to CJ itself and no difference in response to VOCs collected from unexposed plants compared to CJ exposed plants, both without insects. VOCs were then collected from C. storeyi-infested maize seedlings with and without CJ pre-treatment. The bioassay revealed a significant preference by this pest for VOCs from infested seedlings without the CJ pre-treatment. A timed series of VOC collections and bioassays showed that the effect was strongest in the first 22 h of insect infestation, i.e. before the insects had themselves induced a change in VOC emission. Chemical analysis showed that treatment of maize seedlings with CJ, followed by exposure to C. storeyi, led to a significant increase in emission of the defensive sesquiterpenes (E)-(1R,9S)-caryophyllene, (E)-α-bergamotene, (E)-β-farnesene and (E)-4,8-dimethyl-1,3,7-nonatriene, known to act as herbivore repellents. The chemical analysis explains the behavioural effects observed in the olfactometer, as the CJ treatment caused plants to emit a blend of VOCs comprising more of the repellent components in the first 22 h of insect infestation than control plants. The speed and potency of VOC emission was increased by the CJ pre-treatment. This is the first indication that CJ can prime plants for enhanced production of defensive VOCs antagonist towards herbivores.
PMCID: PMC3694093  PMID: 23840295
11.  Degree of herbivore feeding damage as an important contributor to multitrophic plant-parasitoid signaling under climate change 
Plant Signaling & Behavior  2009;4(3):249-251.
Biogenic volatile organic compounds (VOCs) serve as signals mediating information between plants and their higher trophic level beneficials, such as parasitoids and predators of herbivores. We recently demonstrated with oilseed rape (Brassica napus L.) plants, herbivorous diamond-back moth (Plutella xylostella L. (Lepidoptera: Yponomeutidae)) larvae and Cotesia vestalis (Haliday) (Hymenoptera: Braconidae) parasitoids that atmospheric pollution, i.e., elevated ozone (O3), can disturb attraction of natural enemies by plant-emitted host-induced volatile cues. Additionally, we found that the degree of herbivore feeding damage is an important contributor to this O3 interference. Low feeding damage in herbivore-resistant plants was sufficient to attract C. vestalis females to host-damaged plants under ambient air, but this tritrophic signaling turned non-functional in the combination of low feeding damage and high O3 concentration. Here we present some additional data of how climate change factors may modify feeding patterns and growth of herbivores. We further discuss how the degree of herbivore feeding damage and the tritrophic signaling interaction relaying on the herbivore-induced VOCs from attacked plants might change through direct and indirect effects of increased levels of carbon dioxide, temperature and O3.
PMCID: PMC2652544  PMID: 19721765
volatile organic compounds; carbon dioxide; ozone; herbivore feeding; tritrophic interactions; oilseed rape; Lepidoptera; parasitoids; climate change
12.  Canopy light cues affect emission of constitutive and methyl jasmonate-induced volatile organic compounds in Arabidopsis thaliana 
The New Phytologist  2013;200(3):861-874.
The effects of plant competition for light on the emission of plant volatile organic compounds (VOCs) were studied by investigating how different light qualities that occur in dense vegetation affect the emission of constitutive and methyl-jasmonate-induced VOCs.Arabidopsis thaliana Columbia (Col-0) plants and Pieris brassicae caterpillars were used as a biological system to study the effects of light quality manipulations on VOC emissions and attraction of herbivores. VOCs were analysed using gas chromatography–mass spectrometry and the effects of light quality, notably the red : far red light ratio (R : FR), on expression of genes associated with VOC production were studied using reverse transcriptase–quantitative PCR.The emissions of both constitutive and methyl-jasmonate-induced green leaf volatiles and terpenoids were partially suppressed under low R : FR and severe shading conditions. Accordingly, the VOC-based preference of neonates of the specialist lepidopteran herbivore P. brassicae was significantly affected by the R : FR ratio.We conclude that VOC-mediated interactions among plants and between plants and organisms at higher trophic levels probably depend on light alterations caused by nearby vegetation. Studies on plant–plant and plant–insect interactions through VOCs should take into account the light quality within dense stands when extrapolating to natural and agricultural field conditions.
PMCID: PMC4283982  PMID: 23845065
Arabidopsis thaliana; herbivory; light quality; phytochrome; shade avoidance; volatile organic compounds (VOCs)
13.  The role of spatial scale and intraspecific variation in secondary chemistry in host-plant location by Ceutorhynchus assimilis (Coleoptera: Curculionidae). 
To understand the ecological role of secondary plant compounds in host location by phytophagous insects it is important to consider attraction at different scales in natural populations. The cabbage seed weevil, Ceutorhynchus assimilis, which lays eggs in pods of crucifers where the larvae feed on seed, is attracted to purified extracts of specific glucosinolate-derived volatiles. We considered the possibility that C. assimilis adults are attracted to and preferentially attack patches of plants and/or individual plants producing these volatiles. Using discrete natural populations of Brassica oleracea and Brassica nigra, we found that oviposition was highest in populations of B. oleracea producing high amounts of 3-butenylglucosinolate. No links were found between the other glucosinolates, 2-propenylglucosinolate, 2-hydroxy-3-butenylglucosinolate, 1-indolylmethylglucosinolate or 1-methoxy-3-indolylmethylglucosinolate, and oviposition in B. oleracea. B. nigra, which contains only 2-propenylglucosinolate, was not attacked by C. assimilis. Within populations of B. oleracea, neither oviposition nor the number of seeds eaten was related to the glucosinolate profiles of individual plants. We suggest that C. assimilis adults use 3-butenylglucosinolate-derived volatiles to locate host populations, whereas other cues determine oviposition on individual plants. The consequences of these results for natural selection of glucosinolate phenotypes are discussed.
PMCID: PMC1088779  PMID: 11487403
14.  Do Leaf Cutting Ants Cut Undetected? Testing the Effect of Ant-Induced Plant Defences on Foraging Decisions in Atta colombica 
PLoS ONE  2011;6(7):e22340.
Leaf-cutting ants (LCAs) are polyphagous, yet highly selective herbivores. The factors that govern their selection of food plants, however, remain poorly understood. We hypothesized that the induction of anti-herbivore defences by attacked food plants, which are toxic to either ants or their mutualistic fungus, should significantly affect the ants' foraging behaviour. To test this “induced defence hypothesis,” we used lima bean (Phaseolus lunatus), a plant that emits many volatile organic compounds (VOCs) upon herbivore attack with known anti-fungal or ant-repellent effects. Our results provide three important insights into the foraging ecology of LCAs. First, leaf-cutting by Atta ants can induce plant defences: Lima bean plants that were repeatedly exposed to foraging workers of Atta colombica over a period of three days emitted significantly more VOCs than undamaged control plants. Second, the level to which a plant has induced its anti-herbivore defences can affect the LCAs' foraging behaviour: In dual choice bioassays, foragers discriminated control plants from plants that have been damaged mechanically or by LCAs 24 h ago. In contrast, strong induction levels of plants after treatment with the plant hormone jasmonic acid or three days of LCA feeding strongly repelled LCA foragers relative to undamaged control plants. Third, the LCA-specific mode of damaging leaves allows them to remove larger quantities of leaf material before being recognized by the plant: While leaf loss of approximately 15% due to a chewing herbivore (coccinelid beetle) was sufficient to significantly increase VOC emission levels after 24 h, the removal of even 20% of a plant's leaf area within 20 min by LCAs did not affect its VOC emission rate after 24 h. Taken together, our results support the “induced defence hypothesis” and provide first empirical evidence that the foraging behaviour of LCAs is affected by the induction of plant defence responses.
PMCID: PMC3140513  PMID: 21799831
15.  Epichloë Endophytes Alter Inducible Indirect Defences in Host Grasses 
PLoS ONE  2014;9(6):e101331.
Epichloë endophytes are common symbionts living asymptomatically in pooid grasses and may provide chemical defences against herbivorous insects. While the mechanisms underlying these fungal defences have been well studied, it remains unknown whether endophyte presence affects the host's own defences. We addressed this issue by examining variation in the impact of Epichloë on constitutive and herbivore-induced emissions of volatile organic compounds (VOC), a well-known indirect plant defence, between two grass species, Schedonorus phoenix (ex. Festuca arundinacea; tall fescue) and Festuca pratensis (meadow fescue). We found that feeding by a generalist aphid species, Rhopalosiphum padi, induced VOC emissions by uninfected plants of both grass species but to varying extents, while mechanical wounding failed to do so in both species after one day of damage. Interestingly, regardless of damage treatment, Epichloë uncinata-infected F. pratensis emitted significantly lower quantities of VOCs than their uninfected counterparts. In contrast, Epichloë coenophiala-infected S. phoenix did not differ from their uninfected counterparts in constitutive VOC emissions but tended to increase VOC emissions under intense aphid feeding. A multivariate analysis showed that endophyte status imposed stronger differences in VOC profiles of F. pratensis than damage treatment, while the reverse was true for S. phoenix. Additionally, both endophytes inhibited R. padi population growth as measured by aphid dry biomass, with the inhibition appearing greater in E. uncinata-infected F. pratensis. Our results suggest, not only that Epichloë endophytes may play important roles in mediating host VOC responses to herbivory, but also that the magnitude and direction of such responses may vary with the identity of the Epichloë–grass symbiosis. Whether Epichloë-mediated host VOC responses will eventually translate into effects on higher trophic levels merits future investigation.
PMCID: PMC4076332  PMID: 24978701
16.  From Plants to Birds: Higher Avian Predation Rates in Trees Responding to Insect Herbivory 
PLoS ONE  2008;3(7):e2832.
An understanding of the evolution of potential signals from plants to the predators of their herbivores may provide exciting examples of co-evolution among multiple trophic levels. Understanding the mechanism behind the attraction of predators to plants is crucial to conclusions about co-evolution. For example, insectivorous birds are attracted to herbivore-damaged trees without seeing the herbivores or the defoliated parts, but it is not known whether birds use cues from herbivore-damaged plants with a specific adaptation of plants for this purpose.
We examined whether signals from damaged trees attract avian predators in the wild and whether birds could use volatile organic compound (VOC) emissions or net photosynthesis of leaves as cues to detect herbivore-rich trees. We conducted a field experiment with mountain birches (Betula pubescens ssp. czerepanovii), their main herbivore (Epirrita autumnata) and insectivorous birds. Half of the trees had herbivore larvae defoliating trees hidden inside branch bags and half had empty bags as controls. We measured predation rate of birds towards artificial larvae on tree branches, and VOC emissions and net photosynthesis of leaves.
Principal Findings and Significance
The predation rate was higher in the herbivore trees than in the control trees. This confirms that birds use cues from trees to locate insect-rich trees in the wild. The herbivore trees had decreased photosynthesis and elevated emissions of many VOCs, which suggests that birds could use either one, or both, as cues. There was, however, large variation in how the VOC emission correlated with predation rate. Emissions of (E)-DMNT [(E)-4,8-dimethyl-1,3,7-nonatriene], β-ocimene and linalool were positively correlated with predation rate, while those of highly inducible green leaf volatiles were not. These three VOCs are also involved in the attraction of insect parasitoids and predatory mites to herbivore-damaged plants, which suggests that plants may not have specific adaptations to signal only to birds.
PMCID: PMC2475509  PMID: 18665271
17.  Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host 
PLoS Biology  2012;10(11):e1001435.
Parasitic wasps that develop inside herbivorous hosts alter the volatiles produced by plants in response to the damage, thus giving away the presence of the parasitoid larvae to their hyperparasitoid enemies.
Plants respond to herbivory with the emission of induced plant volatiles. These volatiles may attract parasitic wasps (parasitoids) that attack the herbivores. Although in this sense the emission of volatiles has been hypothesized to be beneficial to the plant, it is still debated whether this is also the case under natural conditions because other organisms such as herbivores also respond to the emitted volatiles. One important group of organisms, the enemies of parasitoids, hyperparasitoids, has not been included in this debate because little is known about their foraging behaviour. Here, we address whether hyperparasitoids use herbivore-induced plant volatiles to locate their host. We show that hyperparasitoids find their victims through herbivore-induced plant volatiles emitted in response to attack by caterpillars that in turn had been parasitized by primary parasitoids. Moreover, only one of two species of parasitoids affected herbivore-induced plant volatiles resulting in the attraction of more hyperparasitoids than volatiles from plants damaged by healthy caterpillars. This resulted in higher levels of hyperparasitism of the parasitoid that indirectly gave away its presence through its effect on plant odours induced by its caterpillar host. Here, we provide evidence for a role of compounds in the oral secretion of parasitized caterpillars that induce these changes in plant volatile emission. Our results demonstrate that the effects of herbivore-induced plant volatiles should be placed in a community-wide perspective that includes species in the fourth trophic level to improve our understanding of the ecological functions of volatile release by plants. Furthermore, these findings suggest that the impact of species in the fourth trophic level should also be considered when developing Integrated Pest Management strategies aimed at optimizing the control of insect pests using parasitoids.
Author Summary
In nature, plants often release volatiles in response to damage by herbivores (e.g., by caterpillars), and these can indirectly help defend the plants. Indeed, it is well documented that volatiles can recruit the natural enemies of herbivores, such as predators and parasitoid wasps, whose offspring feed on and develop within their caterpillar hosts. However, such induced plant odours can also be detected by other organisms. One important group of organisms, hyperparasitoids, the enemies of the parasitoids that indirectly benefit the plants, have not been included in this trophic web because so little is known about their foraging behaviour. Here, using a combination of laboratory and field experiments, we demonstrate that hyperparasitoid wasps also take advantage of the odours that plants produce in response to the feeding by caterpillars. The larvae of parasitic wasps developing inside the caterpillar alter the composition of the oral secretions of their herbivorous host and thereby affect the cocktail of volatiles the plant produces. The hyperparasitoids on the lookout for their parasitoid prey can preferentially detect infected caterpillars, although not all parasitoid wasps gave away their presence through this host–plant interaction. We conclude that herbivore-induced plant volatiles can affect the interaction among parasitoids and their enemies and thereby may reduce the indirect defence accrued for the plant.
PMCID: PMC3507920  PMID: 23209379
18.  Odor Uniformity among Tomato Individuals in Response to Herbivore Depends on Insect Species 
PLoS ONE  2013;8(10):e77199.
Plants produce specific volatile organic compound (VOC) blends in response to herbivory. Herbivore-induced blends may prime the plant for future attack or attract carnivorous insects; these responses have been considered adaptive for plants. If herbivores differentially modify the VOC emission among individuals within a group of plants they feed upon, then plant responses to herbivores will not only produce specific blends but also variation in odor among individuals, i.e. individuals smell the same, then having a uniform odor. We investigated the VOC emission variation or uniformity among tomato individuals (Solanum lycopersicum L. cv. Castlemart) in response to moderate wounding by (1) nymphs of the psyllid Bactericera cockerelli (Sulc.) (TP); (2) Lepidoptera chewing-feeding larvae of Fall Armyworm (Spodoptera frugiperda Smith) (FAW) and (3) of Cabbage Looper (Trichoplusia ni Hübner) (CL), and (4) mechanical damage (MD). We used a ratio-based analysis to compare the fold-change in concentration from constitutive to induced VOC emission. We also used size and shape analysis to compare the emission of damaged and non-damaged individuals. Aside of finding herbivore-specific blends in line with other studies, we found patterns not described previously. We detected constitutive and induced odor variation among individuals attacked by the same herbivore, with the induced odor uniformity depending on the herbivore identity. We also showed that the fold-change of VOCs from constitutive to induced state differed among individuals independently of the uniformity of the blends before herbivore attack. We discuss our findings in the context of the ecological roles of VOCs in plant-plant and plant-carnivore insects’ interactions.
PMCID: PMC3793962  PMID: 24130855
19.  Heterodera schachtii Nematodes Interfere with Aphid-Plant Relations on Brassica oleracea 
Journal of Chemical Ecology  2013;39(9):1193-1203.
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.
PMCID: PMC3790247  PMID: 24014097
Heterodera; Brevicoryne; Brassica; Glucosinolates; Phloem; EDTA
20.  Root and shoot jasmonic acid applications differentially affect leaf chemistry and herbivore growth 
Plant Signaling & Behavior  2008;3(2):91-98.
Many induced responses in plants are systemic. Therefore, root-induced responses may alter leaf quality for shoot herbivores. Previously, we found that root and shoot application of jasmonic acid (JA) to feral Brassica oleracea both induced glucosinolates in the leaves. However, the types of glucosinolates that increased in root- and shoot induced plants were different. Here we analyse whether primary metabolites, such as sugars and amino acids, are also differentially affected. Moreover, we test whether chemical differences in root- and shoot-induced plants differentially affect growth of the generalist Mamestra brassicae and the specialist Pieris rapae. Comprehensive analysis of glucosinolates, amino acid and sugars with principal component analysis revealed that leaf chemical profiles were affected both by JA application and by the organ that was induced. Shoot-induction increased indole glucosinolates, whereas root-induction induced aliphatic glucosinolates in the leaves. Leaves of shoot-induced plants had lower total sugar and total amino acid levels, whereas in root-induced plants only total sugar levels were significantly decreased. (Iso)leucine responded significantly different from the general trend, which allowed us to discuss the potential role of Myb transcription factors which are coordinating JA-induced glucosinolate and amino acid responses in Arabidopsis thaliana. Both M. brassicae and P. rapae grew the slowest on leaves of shoot-induced plants. M. brassicae growth and survival was also reduced on root-induced plants, whereas P. rapae growth on these plants was similar to that on controls. Specialist and generalist herbivores thus are differentially affected by the chemical changes after root and shoot-JA application.
PMCID: PMC2633990  PMID: 19516980
above-below ground interactions; amino acids; Brassica oleracea; glucosinolates; induced responses; jasmonic acid; Mamestra brassicae; Pieris rapae; sugars
21.  Plant defence responses in oilseed rape MINELESS plants after attack by the cabbage moth Mamestra brassicae  
Journal of Experimental Botany  2015;66(2):579-592.
The larvae of Mamestra brassicae feed less and show reduced growth on plants with ablated myrosin cells, which raises questions about the role of defence cells in Brassicaceae plants.
The Brassicaceae family is characterized by a unique defence mechanism known as the ‘glucosinolate–myrosinase’ system. When insect herbivores attack plant tissues, glucosinolates are hydrolysed by the enzyme myrosinase (EC into a variety of degradation products, which can deter further herbivory. This process has been described as ‘the mustard oil bomb’. Additionally, insect damage induces the production of glucosinolates, myrosinase, and other defences. Brassica napus seeds have been genetically modified to remove myrosinase-containing myrosin cells. These plants are termed MINELESS because they lack myrosin cells, the so-called toxic mustard oil mines. Here, we examined the interaction between B. napus wild-type and MINELESS plants and the larvae of the cabbage moth Mamestra brassicae. No-choice feeding experiments showed that M. brassicae larvae gained less weight and showed stunted growth when feeding on MINELESS plants compared to feeding on wild-type plants. M. brassicae feeding didn’t affect myrosinase activity in MINELESS plants, but did reduce it in wild-type seedlings. M. brassicae feeding increased the levels of indol-3-yl-methyl, 1-methoxy-indol-3-yl-methyl, and total glucosinolates in both wild-type and MINELESS seedlings. M. brassicae feeding affected the levels of glucosinolate hydrolysis products in both wild-type and MINELESS plants. Transcriptional analysis showed that 494 and 159 genes were differentially regulated after M. brassicae feeding on wild-type and MINELESS seedlings, respectively. Taken together, the outcomes are very interesting in terms of analysing the role of myrosin cells and the glucosinolate–myrosinase defence system in response to a generalist cabbage moth, suggesting that similar studies with other generalist or specialist insect herbivores, including above- and below-ground herbivores, would be useful.
PMCID: PMC4286410  PMID: 25563968
Brassica napus (oilseed rape); defence cells; generalist; glucosinolate; jasmonates; myrosinase; plant–insect interaction; transcriptional profiling.
22.  Drought and Root Herbivory Interact to Alter the Response of Above-Ground Parasitoids to Aphid Infested Plants and Associated Plant Volatile Signals 
PLoS ONE  2013;8(7):e69013.
Multitrophic interactions are likely to be altered by climate change but there is little empirical evidence relating the responses of herbivores and parasitoids to abiotic factors. Here we investigated the effects of drought on an above/below-ground system comprising a generalist and a specialist aphid species (foliar herbivores), their parasitoids, and a dipteran species (root herbivore).We tested the hypotheses that: (1) high levels of drought stress and below-ground herbivory interact to reduce the performance of parasitoids developing in aphids; (2) drought stress and root herbivory change the profile of volatile organic chemicals (VOCs) emitted by the host plant; (3) parasitoids avoid ovipositing in aphids feeding on plants under drought stress and root herbivory. We examined the effect of drought, with and without root herbivory, on the olfactory response of parasitoids (preference), plant volatile emissions, parasitism success (performance), and the effect of drought on root herbivory. Under drought, percentage parasitism of aphids was reduced by about 40–55% compared with well watered plants. There was a significant interaction between drought and root herbivory on the efficacy of the two parasitoid species, drought stress partially reversing the negative effect of root herbivory on percent parasitism. In the absence of drought, root herbivory significantly reduced the performance (e.g. fecundity) of both parasitoid species developing in foliar herbivores. Plant emissions of VOCs were reduced by drought and root herbivores, and in olfactometer experiments parasitoids preferred the odour from well-watered plants compared with other treatments. The present work demonstrates that drought stress can change the outcome of interactions between herbivores feeding above- and below-ground and their parasitoids, mediated by changes in the chemical signals from plants to parasitoids. This provides a new insight into how the structure of terrestrial communities may be affected by drought.
PMCID: PMC3716814  PMID: 23894394
23.  The Venus flytrap attracts insects by the release of volatile organic compounds 
Journal of Experimental Botany  2014;65(2):755-766.
Does Dionaea muscipula, the Venus flytrap, use a particular mechanism to attract animal prey? This question was raised by Charles Darwin 140 years ago, but it remains unanswered. This study tested the hypothesis that Dionaea releases volatile organic compounds (VOCs) to allure prey insects. For this purpose, olfactory choice bioassays were performed to elucidate if Dionaea attracts Drosophila melanogaster. The VOCs emitted by the plant were further analysed by GC-MS and proton transfer reaction-mass spectrometry (PTR-MS). The bioassays documented that Drosophila was strongly attracted by the carnivorous plant. Over 60 VOCs, including terpenes, benzenoids, and aliphatics, were emitted by Dionaea, predominantly in the light. This work further tested whether attraction of animal prey is affected by the nutritional status of the plant. For this purpose, Dionaea plants were fed with insect biomass to improve plant N status. However, although such feeding altered the VOC emission pattern by reducing terpene release, the attraction of Drosophila was not affected. From these results it is concluded that Dionaea attracts insects on the basis of food smell mimicry because the scent released has strong similarity to the bouquet of fruits and plant flowers. Such a volatile blend is emitted to attract insects searching for food to visit the deadly capture organ of the Venus flytrap.
PMCID: PMC3904726  PMID: 24420576
Carnivorous plants; Dionaea muscipula; Drosophila melanogaster; nitrogen status; olfactory bioassay; plant–animal interaction; VOC emissions.
24.  Herbivore-Mediated Effects of Glucosinolates on Different Natural Enemies of a Specialist Aphid 
Journal of Chemical Ecology  2012;38(1):100-115.
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.
Electronic supplementary material
The online version of this article (doi:10.1007/s10886-012-0065-2) contains supplementary material, which is available to authorized users.
PMCID: PMC3268984  PMID: 22258357
Arabidopsis thaliana; Brevicoryne brassicae; Diaeretiella rapae; Episyrphus balteatus; Parasitoid wasp; Predator; Sequestration
25.  Herbivory by the insect diaphorina citri induces greater change in citrus plant volatile profile than does infection by the bacterium, Candidatus Liberibacter asiaticus 
Plant Signaling & Behavior  2013;8(10):e25677.
The volatile organic compound (VOC) profile in plant leaves often changes after biotic and abiotic stresses. Monitoring changes in VOCs in plant leaves could provide valuable information about multitrophic interactions. In the current study, we investigated the effect of Asian citrus psyllid (ACP) infestation, citrus greening pathogen (Candidatus Liberibacter asiaticus [CLas]) infection, and simultaneous attack by ACP and CLas on the VOC content of citrus leaves. Leaf volatiles were extracted using hexane and analyzed with gas chromatography-mass spectrometry (GC-MS). Although ACP is a phloem-sucking insect that causes minimal damage to plant tissues, the relative amount of 21 out of the 27 VOCs increased 2- to 10-fold in ACP-infested plants. The relative amount of d-limonene, β-phelandrene, citronellal, and undecanal were increased 4- to 20- fold in CLas-infected plants. A principle component analysis (PCA) and cluster analysis (CA) showed that VOC patterns of ACP-infested and CLas-infected plants were different from each other and were also different from the controls, while the VOC pattern of double-attacked plants was more like that of the controls than that of ACP-infested or CLas-infected plants. VOC amounts from leaves were compromised when plants were attacked by ACP and CLas. The results of this study showed that a simple direct extraction of citrus leaf volatiles could be successfully used to discriminate between healthy and CLas-infected plants. Information about the effects of insect and pathogen attack on the VOC content profile of plants might contribute to a better understanding of biotic stress.
PMCID: PMC4091108  PMID: 23857364
Diaphorina citri; Candidatus Liberibacter asiaticus; citrus greening; Huanglongbing; asain citrus psyllid; volatiles; herbivory; piecing-sucking insects

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