Root volatiles in plant–plant interactions II: Root volatiles alter root chemistry and plant–herbivore interactions of neighbouring plants

Volatile organic compounds (VOCs) emitted by plant roots can influence the germination and growth of neighbouring plants. However, little is known about the effects of root VOCs on plant–herbivore interactions of neighbouring plants. The spotted knapweed (Centaurea stoebe) constitutively releases high amounts of sesquiterpenes into the rhizosphere. Here, we examine the impact of C. stoebe root VOCs on the primary and secondary metabolites of sympatric Taraxacum officinale plants and the resulting plant‐mediated effects on a generalist root herbivore, the white grub Melolontha melolontha. We show that exposure of T. officinale to C.stoebe root VOCs does not affect the accumulation of defensive secondary metabolites but modulates carbohydrate and total protein levels in T. officinale roots. Furthermore, VOC exposure increases M. melolontha growth on T. officinale plants. Exposure of T. officinale to a major C. stoebe root VOC, the sesquiterpene (E)‐β‐caryophyllene, partially mimics the effect of the full root VOC blend on M. melolontha growth. Thus, releasing root VOCs can modify plant–herbivore interactions of neighbouring plants. The release of VOCs to increase the susceptibility of other plants may be a form of plant offense.     

Caterpillar‐induced plant volatiles attract conspecific herbivores and a generalist predator

Plants release volatiles in response to caterpillar feeding that attracts natural enemies of the herbivores, a tritrophic interaction which has been considered to be an indirect plant defence against herbivores. On the other hand, the caterpillar‐induced plant volatiles have been reported to either repel or attract conspecific adult herbivores. This work was undertaken to investigate the response of both herbivores and natural enemies to caterpillar‐induced plant volatiles in apple orchards. We sampled volatile compounds emitted from uninfested apple trees, and apple trees infested with generalist herbivore the pandemis leafroller moth, Pandemis pyrusana (Lepidoptera, Tortricidae) larvae using headspace collection and analysed by gas chromatography/mass spectrometry. Infested apple trees uniquely release six compounds (benzyl alcohol, phenylacetonitrile, phenylacetaldehyde, 2‐phenylethanol, indole and (E)‐nerolidol). These compounds were tested on two species of herbivores and one predator in apple orchards. Binary blends of phenylacetonitrile + acetic acid or 2‐phenylethanol + acetic acid attracted a large number of conspecific male and female adult herbivores. The response of pandemis leafroller to herbivore‐induced plant volatiles (HIPVs) was so pronounced that over one thousand and seven hundred conspecific male and female adult herbivores were caught in traps baited with HIPVs in three‐day trapping period. In addition, significantly higher number of male and female obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera, Tortricidae), was caught in traps baited a binary blend of 2‐phenylethanol + acetic acid, or a ternary blend contains 2‐phenylethanol and phenylacetonitrile + acetic acid. This result challenges the current paradigm hypothesized that HIPVs repel herbivores and question the indirect defensive function proposed for these compounds. On the other hand, a ternary blend of phenylacetonitrile and 2‐phenylethanol + acetic acid attracted the largest numbers of the general predator, the common green lacewing, Chrysoperla plorabunda. To our knowledge, this is the first record of the direct attraction of conspecific adult herbivores as well as a predator to the caterpillar‐induced plant volatiles in the field.     

Effects of quantitative and qualitative differences in volatiles from host‐ and non‐host‐infested maize on the attraction of the larval parasitoid Cotesia kariyai

Cotesia kariyai Watanabe (Hymenoptera: Braconidae) is a specialist larval parasitoid of Mythimna separata Walker (Lepidoptera: Noctuidae). Cotesia kariyai wasps use herbivore‐induced plant volatiles (HIPVs) to locate hosts. However, complex natural habitats are full of volatiles released by both herbivorous host‐ and non‐host‐infested plants at various levels of intensity. Therefore, the presence of non‐hosts may affect parasitoid decisions while foraging. Here, the host‐finding efficiency of naive C. kariyai from HIPVs influenced by host‐ and non‐host‐infested maize [Zea mays L. (Poaceae)] plants was investigated with a four‐arm olfactometer. Ostrinia furnacalis Guenée (Lepidoptera: Crambidae) was selected as a non‐host species. One unit (1 U) of host‐ or non‐host‐infested plant was prepared by infesting a potted plant with five host or seven non‐host larvae. In two‐choice bioassays, host‐infested plants fed upon by different numbers of larvae, and various units of host‐ and non‐host‐infested plants (infestation units; 1 U, 2 U, and 3 U) were arranged to examine the effects of differences in volatile quantity and quality on the olfactory responses of C. kariyai with the assumption that volatile quantity and quality changes with differences in numbers of insects and plants. Cotesia kariyai was found to perceive quantitative differences in volatiles from host‐infested plants, preferring larger quantities of volatiles from larger numbers of larvae or plants. Also, the parasitoids discriminated between healthy plants, host‐infested plants, and non‐host‐infested plants by recognising volatiles released from those plants. Cotesia kariyai showed a reduced preference for host‐induced volatiles, when larger numbers of non‐host‐infested plants were present. Therefore, quantitative and qualitative differences in volatiles from host‐ and non‐host‐infested plants appear to affect the decision of C. kariyai during host‐habitat searching in multiple tritrophic systems.     

Similar Metabolic Changes Induced by HIPVs Exposure as Herbivore in Ammopiptanthus mongolicus

Herbivore-induced plant volatiles (HIPVs) are important compounds to prim neighboring undamaged plants; however, the mechanism for this priming process remains unclear. To reveal metabolic changes in plants exposed to HIPVs, metabolism of leaves and roots of Ammopiptanthus mongolicus seedlings exposed to HIPVs released from conspecific plants infested with larvae of Orgyia ericae were analyzed together with control and infested seedlings using nuclear magnetic resonance (NMR)-based metabolic technology and multi variate data analysis. Results presented showed that HIPVs exposure led to similar but specific metabolic changes compared with those induced by infestation in both leaves and roots. Furthermore, both HIPVs exposure and herbivore attack resulted in metabolic changes involving a series of primary and secondary metabolites in both leaves and roots. Taken together, these results suggested that priming of yet-damaged plants may be achieved by reconfiguring metabolic pathways in leaves and roots to make similar concentrations for all metabolites as those in seedlings infested. Therefore, we propose that improved readiness of defense induction of primed plants toward subsequent herbivore attack may be based on the similar metabolic profiling induced by HIPVs exposure as those caused by herbivore.     

Influence of volatile compounds from herbivore‐damaged soybean plants on searching behavior of the egg parasitoid Telenomus podisi

Parasitoids use herbivore‐induced plant volatiles (HIPVs) to locate their hosts. However, there are few studies in soybean showing the mechanisms involved in the attraction of natural enemies to their hosts and prey. The objective of this study was to evaluate the influence of volatile organic compounds (VOCs) of soybean, Glycine max (L.) Merr. (Fabaceae) (cv. Dowling), that were induced after injury caused by Euschistus heros (Fabricius) (Hemiptera: Pentatomidae), on the searching behavior of the egg parasitoid Telenomus podisi Ashmead (Hymenoptera: Scelionidae). Four HIPVs from soybean, (E,E)‐α‐farnesene, methyl salicylate, (Z)‐3‐hexenyl acetate, and (E)‐2‐octen‐1‐ol, were selected, prepared from standards at various concentrations (10^?6 to 10^?1 m ), and tested individually and in combinations using a two‐choice olfactometer (type Y). Telenomus podisi displayed a preference only for (E,E)‐α‐farnesene at 10^?5 m when tested individually and compared to hexane, but they did not respond to the other compounds tested individually at any concentration or when combinations of these compounds were tested. However, the parasitoids stayed longer in the olfactometer arm with the mixture of (E,E)‐α‐farnesene + methyl salicylate at 10^?5 m than in the arm containing hexane. The results suggest that (E,E)‐α‐farnesene and methyl salicylate might help T. podisi to determine the presence of stink bugs on a plant. In addition, bioassays were conducted to compare (E,E)‐α‐farnesene vs. the volatiles emitted by undamaged and E. heros‐damaged plants, to evaluate whether (E,E)‐α‐farnesene was the main cue used by T. podisi or whether other minor compounds from the plants and/or the background might also be used to locate its host. The results suggest that minor volatile compounds from soybean plants or from its surroundings are involved in the host‐searching behavior of T. podisi.     

Response of mirid predators to synthetic herbivore‐induced plant volatiles

Zoophytophagous plant bugs feed on plant tissue as a source of water and nutrients, besides feeding on prey. By phytophagy, mirid predators activate plant defense responses through different pathways, resulting, among others, in the release of herbivore‐induced plant volatiles (HIPVs). These compounds could repel herbivores and attract parasitoids and predators, and synthetic versions could potentially be used in biological control. Nevertheless, little is known about the influence of synthetic volatiles on mirid attraction. Using Y‐tube olfactometer trials, we evaluated the responses of Nesidiocoris tenuis (Reuter), Macrolophus pygmaeus (Rambur), and Dicyphus bolivari Lindberg (Hemiptera: Miridae), important natural enemies used to control various greenhouse pests, to 10 synthetic versions of HIPVs released from tomato (Solanum lycopersicum L., Solanaceae) plants induced by N. tenuis and M. pygmaeus. Nesidiocoris tenuis responded to five of the 10 HIPVs, whereas M. pygmaeus and D. bolivari responded to four of the 10 HIPVs. Two green leaf volatiles, (Z)‐3‐hexenyl propanoate and (Z)‐3‐hexenyl acetate, and the ester methyl salicylate (MeSA) were attractive to all three mirid predator species. Our results demonstrate that the volatiles released by tomato plants activated by N. tenuis and M. pygmaeus phytophagy are attractive to their conspecifics and also to D. bolivari. Further studies should evaluate the potential of these compounds to attract predatory mirids in the field.     

Intraspecific variation in herbivore‐induced plant volatiles influences the spatial range of plant–parasitoid interactions

Chemical information influences the behaviour of many animals, thus affecting species interactions. Many animals forage for resources that are heterogeneously distributed in space and time, and have evolved foraging behaviour that utilizes information related to these resources. Herbivore‐induced plant volatiles (HIPVs), emitted by plants upon herbivore attack, provide information on herbivory to various animal species, including parasitoids. Little is known about the spatial scale at which plants attract parasitoids via HIPVs under field conditions and how intraspecific variation in HIPV emission affects this spatial scale. Here, we investigated the spatial scale of parasitoid attraction to two cabbage accessions that differ in relative preference of the parasitoid Cotesia glomerata when plants were damaged by Pieris brassicae caterpillars. Parasitoids were released in a field experiment with plants at distances of up to 60 m from the release site using intervals between plants of 10 or 20 m to assess parasitism rates over time and distance. Additionally, we observed host‐location behaviour of parasitoids in detail in a semi‐field tent experiment with plant spacing up to 8 m. Plant accession strongly affected successful host location in field set‐ups with 10 or 20 m intervals between plants. In the semi‐field set‐up, plant finding success by parasitoids decreased with increasing plant spacing, differed between plant accessions, and was higher for host‐infested plants than for uninfested plants. We demonstrate that parasitoids can be attracted to herbivore‐infested plants over large distances (10 m or 20 m) in the field, and that stronger plant attractiveness via HIPVs increases this distance (up to at least 20 m). Our study indicates that variation in plant traits can affect attraction distance, movement patterns of parasitoids, and ultimately spatial patterns of plant–insect interactions. It is therefore important to consider plant‐trait variation in HIPVs when studying animal foraging behaviour and multi‐trophic interactions in a spatial context.     

Variability and stability of tea weevil‐induced volatile emissions from tea plants with different weevil densities,photoperiod and infestation duration

Abstract After herbivore attack, many plants emit herbivore‐induced plant volatiles (HIPVs). HIPVs can attract carnivores and/or repel herbivores, thereby mediating tritrophic plant–herbivore–carnivore interactions. HIPVs act as chemical information between organisms; hence, their variability and stability are vital. In the present study, variations in the volatile emissions, from the tea plant Camellia sinensis (O. Ktze) damaged by the tea weevil Myllocerinus aurolineatus (Voss) (Coleoptera: Curculionidae), with weevil densities, photoperiod and infestation duration, were investigated. The volatiles induced by high‐density weevils were more abundant in composition and amount than those induced by low‐density weevils, whether at noon, night or after weevil removal. The induced volatile emissions were similar on the second and third day after infestation, and the emissions of the major induced compounds displayed diurnal cycles. Linalool, (E,E)‐α‐farnesene, and benzyl nitrile were emitted mainly at noon, whereas 1,3,8‐p‐menthatriene and (E)‐β‐ocimene were maximally emitted at night. Given the different emission dynamics, significant differences were found between noon‐ and night‐induced volatiles. In summary, tea plants damaged by different weevil densities emitted a relatively stable signal at a particular time. This stability could be attributed to the similarities under the two densities of the main induced volatile compounds, their relative ratios and the emission dynamics of the induced volatiles.     

A Latex Metabolite Benefits Plant Fitness under Root Herbivore Attack

Plants produce large amounts of secondary metabolites in their shoots and roots and store them in specialized secretory structures. Although secondary metabolites and their secretory structures are commonly assumed to have a defensive function, evidence that they benefit plant fitness under herbivore attack is scarce, especially below ground. Here, we tested whether latex secondary metabolites produced by the common dandelion (Taraxacum officinale agg.) decrease the performance of its major native insect root herbivore, the larvae of the common cockchafer (Melolontha melolontha), and benefit plant vegetative and reproductive fitness under M. melolontha attack. Across 17 T. officinale genotypes screened by gas and liquid chromatography, latex concentrations of the sesquiterpene lactone taraxinic acid β-D-glucopyranosyl ester (TA-G) were negatively associated with M. melolontha larval growth. Adding purified TA-G to artificial diet at ecologically relevant concentrations reduced larval feeding. Silencing the germacrene A synthase ToGAS1, an enzyme that was identified to catalyze the first committed step of TA-G biosynthesis, resulted in a 90% reduction of TA-G levels and a pronounced increase in M. melolontha feeding. Transgenic, TA-G-deficient lines were preferred by M. melolontha and suffered three times more root biomass reduction than control lines. In a common garden experiment involving over 2,000 T. officinale individuals belonging to 17 different genotypes, high TA-G concentrations were associated with the maintenance of high vegetative and reproductive fitness under M. melolontha attack. Taken together, our study demonstrates that a latex secondary metabolite benefits plants under herbivore attack, a result that provides a mechanistic framework for root herbivore driven natural selection and evolution of plant defenses below ground.     

L-DOPA functions as a plant pheromone for belowground anti-herbivory communication

While mechanisms of plant–plant communication for alerting neighbouring plants of an imminent insect herbivore attack have been described aboveground via the production of volatile organic compounds (VOCs), we are yet to decipher the specific components of plant–plant signalling belowground. Using bioassay-guided fractionation, we isolated and identified the non-protein amino acid l -DOPA, released from roots of Acyrtosiphon pisum aphid-infested Vicia faba plants, as an active compound in triggering the production of VOCs released aboveground in uninfested plants. In behavioural assays, we show that after contact with l -DOPA, healthy plants become highly attractive to the aphid parasitoid (Aphidius ervi), as if they were infested by aphids. We conclude that l -DOPA, originally described as a brain neurotransmitter precursor, can also enhance immunity in plants.     

Volatile organic compounds released by maize following herbivory or insect extract application and communication between plants

To protect themselves from herbivory, plants have evolved an arsenal of physical and chemical defences and release a variety of volatile organic compounds (VOCs). By releasing these VOCs, a signalling plant can both reduce herbivory, sometimes by more than 90%, and also warn neighbouring plants about an attack. The aim of this study was to assess the influence of herbivory and insect extract application on VOC release by damaged/treated and nearby undamaged/untreated maize plants. We confirmed that European corn borer (Ostrinia nubilalis) larvae attack or larvae extract application induced maize VOC release. Greater amounts of (Z)‐3‐hexenal, (E)‐2‐hexenal, (Z)‐3‐hexen‐1‐ol, (E)‐2‐hexen‐1‐ol, β‐myrcene, (Z)‐3‐hexen‐1‐yl acetate, 1‐hexyl acetate, (Z)‐ocimene, linalool, benzyl acetate, methyl salicylate, indole, methyl anthranilate, geranyl acetate, β‐caryophyllene, (E)‐β‐farnesene and (Z)‐3‐hexenal, (Z)‐3‐hexen‐1‐ol, (Z)‐3‐hexen‐1‐yl acetate, (Z)‐ocimene, linalool, indole, methyl anthranilate, geranyl acetate, β‐caryophyllene and (E)‐β‐farnesene were released as a result of biotic stress after insect attack or insect extract application. The amounts of each VOC released were qualitatively and quantitatively distinct and dependent on time after biotic stress exposure. However, for all biotic stresses, significantly lower VOC induction was measured when leaves were damaged/treated for three days, as compared to seven days. Our work also demonstrated that undamaged/untreated neighbouring plants also release significant amounts of VOCs. This suggests that VOC emission by a damaged/treated plant stimulates VOC induction in nearby undamaged/untreated plants. However, the concentrations of all VOCs released by neighbouring undamaged/untreated maize plants were lower than those from damaged/treated plants and were negatively correlated with distance from a damaged/treated plant. Still, significant VOC induction occurred in undamaged/untreated plants even at 3 m distance from a damaged/infected plant. Our work suggests that maize plant protective defence responses (VOC emission) can be induced via application of European corn borer extracts.     

Odour-mediated responses of a predatory mirid bug and its prey, the two-spotted spider mite

It has been shown that many natural enemies of herbivorous arthropods use herbivore induced plant volatiles (HIPVs) to locate their prey. Herbivores can also exploit cues emitted by plants infested with heterospecifics or conspecifics. A study was conducted to test whether green bean HIPVs as well as odours emitted directly by spider mites influenced the orientation behaviour of the predatory mirid bug, Macrolophus caliginosus and its prey, Tetranychus urticae in a Y-tube olfactometer. Our results show that both spider mites and M. caliginosus preferred spider mite infested green bean plants to uninfested plants. For M. caliginosus this response was mediated by HIPVs whereas for T. urticae it was mediated through a composite response to both HIPVs and odours emitted directly by the conspecifics (and their associated products). The results may be of use in practical biocontrol situations, through e.g., plant breeding for improved HIPV production, conditioning of mass-reared predators to appropriate cues, and employment of “push–pull-strategies” by using HIPVs.     

An ecogenomic analysis of herbivore‐induced plant volatiles in Brassica juncea

Upon herbivore feeding, plants emit complex bouquets of induced volatiles that may repel insect herbivores as well as attract parasitoids or predators. Due to differences in the temporal dynamics of individual components, the composition of the herbivore‐induced plant volatile (HIPV) blend changes with time. Consequently, the response of insects associated with plants is not constant either. Using Brassica juncea as the model plant and generalist Spodoptera spp. larvae as the inducing herbivore, we investigated herbivore and parasitoid preference as well as the molecular mechanisms behind the temporal dynamics in HIPV emissions at 24, 48 and 72 h after damage. In choice tests, Spodoptera litura moth preferred undamaged plants, whereas its parasitoid Cotesia marginiventris favoured plants induced for 48 h. In contrast, the specialist Plutella xylostella and its parasitoid C. vestalis preferred plants induced for 72 h. These preferences matched the dynamic changes in HIPV blends over time. Gene expression analysis suggested that the induced response after Spodoptera feeding is mainly controlled by the jasmonic acid pathway in both damaged and systemic leaves. Several genes involved in sulphide and green leaf volatile synthesis were clearly up‐regulated. This study thus shows that HIPV blends vary considerably over a short period of time, and these changes are actively regulated at the gene expression level. Moreover, temporal changes in HIPVs elicit differential preferences of herbivores and their natural enemies. We argue that the temporal dynamics of HIPVs may play a key role in shaping the response of insects associated with plants.     

Effects of prohydrojasmon‐treated corn plants on attractiveness to parasitoids and the performance of their hosts

We investigated the effect of prohydrojasmon [propyl (1RS,2RS)‐(3‐oxo‐ 2‐pentylcyclopentyl) acetate] (PDJ) treatment of intact corn plants, on their attractiveness to the specialist endoparasitoid, Cotesia kariyai Watanabe (Hymenoptera: Braconidae), and on the performance of the common armyworm, Mythimna separata (Walker) (Lepidoptera: Noctuidae) under laboratory conditions. Attractiveness of C. kariyai to PDJ‐treated plants was studied in a wind tunnel, whereas performance of M. separata larvae was tested in plastic cages. The attractiveness of the treated plants increased with concentrations of PDJ increasing to 2 mm , which was equivalent to the attractiveness of host‐infested plants. PDJ‐treated corn plants emitted 16 volatile compounds (α‐pinene, β‐myrcene, (Z)‐3‐hexenyl acetate, limonene, (E)‐β‐ocimene, linalool, (E)‐4,8‐dimethyl‐1,3,7‐nonatriene, (+)‐cyclosativene, ylangene, (E)‐β‐farnesene, (E, E)‐4,8,12‐trimethyl‐1,3,7,11‐tridecatetraene, α‐bergamotene, γ‐cadinene, δ‐cadinene, α‐muulolene and nerolidol), most of which were observed in the headspace of host‐infested corn plants with some quantitative and qualitative differences. We also tested the effects of PDJ treatment on the performance of M. separata larvae. The survival rates of the larval and pupal stages were significantly lower at 2 mm level of PDJ. A significant decrease in weight at 6th stadium larvae was observed only at 2 mm level of PDJ. In contrast, PDJ treatment at all PDJ concentration levels caused significant reduction in weight of pupal stage as compared to control. These data suggested that PDJ, originally developed as a plant growth regulator, especially to induce coloring of fruits, has the potential to induce direct and indirect defenses in corn plants against common armyworm, M. separata.     

Associative learning of host presence in non‐host environments influences parasitoid foraging

1. Parasitoids are known to utilise learning of herbivore‐induced plant volatiles (HIPVs) when foraging for their herbivorous host. In natural situations these hosts share food plants with other, non‐suitable herbivores (non‐hosts). Simultaneous infestation of plants by hosts and non‐hosts has been found to result in induction of HIPVs that differ from host‐infested plants. Each non‐host herbivore may have different effects on HIPVs when sharing the food plant with hosts, and thus parasitoids may learn that plants with a specific non‐host herbivore also contain the host. 2. This study investigated the adaptive nature of learning by a foraging parasitoid that had acquired oviposition experience on a plant infested with both hosts and different non‐hosts in the laboratory and in semi‐field experiments. 3. In two‐choice preference tests, the parasitoid Cotesia glomerata shifted its preference towards HIPVs of a plant–host–non‐host complex previously associated with an oviposition experience. It could, indeed, learn that the presence of its host is associated with HIPVs induced by simultaneous feeding of its host Pieris brassicae and either the non‐host caterpillar Mamestra brassicae or the non‐host aphid Myzus persicae. However, the learned preference found in the laboratory did not translate into parasitisation preferences for hosts accompanying non‐host caterpillars or aphids in a semi‐field situation. 4. This paper discusses the importance of learning in parasitoid foraging, and debates why observed learned preferences for HIPVs in the laboratory may cancel out under some field experimental conditions.     

Responses of Thrips tabaci to odours of herbivore‐induced cotton seedlings

Herbivore‐induced changes in plants have been widely viewed as defensive responses against further insect attack. However, changes in plants as a consequence of herbivore feeding can elicit various responses in herbivores; these are variable, context dependent, and often unpredictable. In this laboratory study, the responses of Thrips tabaci Lindeman (Thysanoptera: Thripidae) to volatiles emitted by intact and herbivore‐damaged or mechanically damaged cotton seedlings [Gossypium hirsutum L. (Malvaceae)] were investigated in dual‐choice olfactometer assays. Thrips tabaci showed increased attraction to seedlings subject to foliar mechanical damage and those with foliar damage inflicted by conspecifics or Tetranychus urticae Koch (Acari: Tetranychidae), upon which it preys. However, T. tabaci did not discriminate between intact seedlings and those with foliar damage inflicted by Helicoverpa armigera Hübner (Lepidoptera: Noctuidae), two other species of thrips, Frankliniella schultzei Trybom and Frankliniella occidentalis Pergrande (Thysanoptera: Thripidae), or those with root damage inflicted by Tenebrio molitor L. (Coleoptera: Tenebrionidae). Attraction of T. tabaci was also affected by herbivore density on damaged plants. That is, seedlings damaged by higher densities of T. urticae or T. tabaci were more attractive than seedlings damaged by lower densities of the corresponding arthropod. Although attracted to plants damaged by conspecifics or T. urticae, T. tabaci showed greater attraction to seedlings damaged by T. urticae than to seedlings damaged by conspecifics. Results are discussed in the context of the responses of F. schultzei and F. occidentalis to herbivore‐induced cotton seedlings, highlighting the complexity, variability, and unpredictability of the responses of even closely related species of insects to plants under herbivore attack.     

Fine‐tuning of defences and counter‐defences in a specialised plant–herbivore system

1. The plant–herbivore arms race has been postulated to be a major driver for generating biological and biochemical diversity on Earth. Herbivore feeding is reduced by the production of chemical and physical barriers, but increases plant resistance against subsequent attack. Accordingly, specialisation is predicted to be an outcome of herbivores being able to circumvent plant‐induced defences. 2. Using a specialised plant–herbivore system, in which adult chrysomelid beetles (Chrysochus auratus) feed on leaves and larvae feed on roots of dogbane (Apocynum spp.), this study investigated whether root latex and cardenolides are effective against the soil‐dwelling larvae, and whether such defences could be circumvented by the herbivore. 3. Across two Apocynum species, C. auratus larvae were not affected by latex production or cardenolide amounts and diversity. By contrast, cardenolide apolarity was detrimental to larval growth. Yet larval feeding decreased average root cardenolide apolarity in A. cannabinum and larvae performed better on those plants. Finally, above‐ground induction rendered the plants more toxic by increasing root cardenolide apolarity and maintaining it, even during subsequent larval herbivory. 4. Therefore, the intimate relationship and interaction between Chrysochus and Apocynum are maintained by a delicate balance of herbivore manipulation and plant chemical induction.     

Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack

The roots of most land plants are colonised by mycorrhizal fungi that provide mineral nutrients in exchange for carbon. Here, we show that mycorrhizal mycelia can also act as a conduit for signalling between plants, acting as an early warning system for herbivore attack. Insect herbivory causes systemic changes in the production of plant volatiles, particularly methyl salicylate, making bean plants, Vicia faba, repellent to aphids but attractive to aphid enemies such as parasitoids. We demonstrate that these effects can also occur in aphid‐free plants but only when they are connected to aphid‐infested plants via a common mycorrhizal mycelial network. This underground messaging system allows neighbouring plants to invoke herbivore defences before attack. Our findings demonstrate that common mycorrhizal mycelial networks can determine the outcome of multitrophic interactions by communicating information on herbivore attack between plants, thereby influencing the behaviour of both herbivores and their natural enemies.     

Function of defensive volatiles in pedunculate oak (Quercus robur) is tricked by the moth Tortrix viridana

The indirect defences of plants are comprised of herbivore‐induced plant volatiles (HIPVs) that among other things attract the natural enemies of insects. However, the actual extent of the benefits of HIPV emissions in complex co‐evolved plant‐herbivore systems is only poorly understood. The observation that a few Quercus robur L. trees constantly tolerated (T‐oaks) infestation by a major pest of oaks (Tortrix viridana L.), compared with heavily defoliated trees (susceptible: S‐oaks), lead us to a combined biochemical and behavioural study. We used these evidently different phenotypes to analyse whether the resistance of T‐oaks to the herbivore was dependent on the amount and scent of HIPVs and/or differences in non‐volatile polyphenolic leaf constituents (as quercetin‐, kaempferol‐ and flavonol glycosides). In addition to non‐volatile metabolic differences, typically defensive HIPV emissions differed between S‐oaks and T‐oaks. Female moths were attracted by the blend of HIPVs from S‐oaks, showing significantly higher amounts of (E)‐4,8‐dimethyl‐1,3,7‐nonatriene (DMNT) and (E)‐β‐ocimene and avoid T‐oaks with relative high fraction of the sesquiterpenes α‐farnesene and germacrene D. Hence, the strategy of T‐oaks exhibiting directly herbivore‐repellent HIPV emissions instead of high emissions of predator‐attracting HIPVs of the S‐oaks appears to be the better mechanism for avoiding defoliation.