Evolution of signal emission by uninfested plants to help nearby infested relatives

Herbivory by arthropods often induces the emission of plant volatiles, which attract natural enemies of the herbivores. This induced emission of volatiles is considered to be a strategy of plants to effectively defend against herbivores by employing bodyguards. Recent empirical research has revealed that these volatiles can also affect neighboring undamaged plants and cause them to emit volatiles secondarily. Provided that signal emission imposes some cost on plants, the evolutionary advantage to undamaged plants in the emission of such secondary signals is unclear. We hypothesized that plants have evolved to emit a secondary signal to help nearby relatives by promoting the recruitment of natural enemies, whereby they increase inclusive fitness. We constructed a simulation model to evaluate this hypothesis. Our simulations suggest that a secondary signal evolves if the following five conditions are met: the cost of the signal is low; the potential risk of infestation is high; the attractiveness of the signal to natural enemies is highly positively correlated with the local density of the signal chemical; dispersal of offspring is spatially restricted, causing population viscosity, and; sufficient vacant space is available, allowing the population to be elastic.     

Evolution of talking plants in a tritrophic context: conditions for uninfested plants to attract predators prior to herbivore attack

Herbivory induces plants to emit volatile chemicals that attract enemies of the herbivores (bodyguards of plants). In this way, the plant acquires protection and the bodyguards gain food. These plant signals cause neighboring plants, not under attack, to release signals as well. We hypothesize that such "secondary" signals help to reduce damage from future herbivore attacks by the protection received from the bodyguards. By modeling we explore the conditions for such secondary signals to evolve. Three kinds of strategies are considered: plants of the first strategy always emit a signal, those of the second strategy emit a signal only when infested, and those of the third strategy emit a signal not only when infested, but also when a certain number of neighbors are infested (i.e. secondary signaling). When signaling is much less (much more) costly than damage from herbivory, the first (second) strategy will be favored by selection, whereas for intermediate costs the third strategy, i.e. secondary signaling, will evolve. However, secondary signaling will not evolve when the primary signals lure the bodyguards too effectively. This is because the undamaged plant gains associational defense when the infested individual is defending very well; therefore, the need for secondary signaling decreases.     

Olfactory response of four aphidophagous insects to aphid- and caterpillar-induced plant volatiles

Plants damaged by herbivores emit blends of volatile organic compounds (VOCs) that attract the herbivore’s natural enemies. Most work has focussed on systems involving one plant, one herbivore and one natural enemy, though, in nature, plants support multiple herbivores and multiple natural enemies of these herbivores. Our study aimed to understand how different aphid natural enemies respond to aphid-induced VOCs, and whether attraction of the natural enemies that responded to aphid-induced VOCs was altered by simultaneous damage by a chewing herbivore. We used a model system based on Brassica juncea (Brassicaceae), Myzus persicae (Hemiptera: Aphididae) and Plutella xylostella (Lepidoptera: Plutellidae). Ceraeochrysa cubana (Neuroptera: Chrysopidae) did not show preferences for any plant odour, while Cycloneda sanguinea (Coleoptera: Coccinellidae) responded to undamaged plants over air but not to aphid-damaged plants over undamaged plants. Therefore, no further tests were carried out with these two species. Chrysoperla externa (Neuroptera: Chrysopidae) preferred aphid-damaged plants, but not caterpillar-damaged plants, over undamaged plants, and preferred plants damaged by both herbivores over both undamaged plants and aphid-damaged plants. When tested for responses against undamaged plants, Aphidius colemani (Hymenoptera: Braconidae) preferred aphid-damaged plants but not plants damaged by caterpillars. Plants damaged by both herbivores attracted more parasitoids than undamaged plants, but not more than aphid-damaged plants. Thus, multiply damaged plants were equally attractive to A. colemani and more attractive to C. externa than aphid-damaged plants, while C. cubana and C. sanguinea did not respond to aphid-induced VOCs, highlighting how different natural enemies can have different responses to herbivore-damaged plants.     

Jasmonate-deficient plants have reduced direct and indirect defences against herbivores

Plants employ a variety of defence mechanisms, some of which act directly by having a negative effect on herbivores and others that act indirectly by attracting natural enemies of herbivores. In this study we asked if a common jasmonate‐signalling pathway links the regulation of direct and indirect defences in plants. We examined the performance of herbivores (direct defence) and the attraction of natural enemies of herbivores (indirect defence) to wild‐type tomato plants and mutant plants that are deficient in the production of the signalling hormone jasmonic acid. Wild‐type plants supported lower survivorship of caterpillars compared with jasmonic acid‐deficient plants. Damaged wild‐type plants were more attractive to predaceous mites compared with undamaged wild‐type plants, whereas damaged jasmonate‐deficient plants were not more attractive to predators. Damaged wild‐type plants induced a greater production of volatile compounds (primarily the sesquiterpene β‐caryophyllene and the monoterpenes α‐pinene, β‐pinene, 2‐carene and β‐phellandrene) compared with damaged jasmonate‐deficient plants. Treating jasmonate‐deficient plants with exogenous jasmonic acid restored both the direct and indirect defence capabilities, demonstrating that jasmonic acid is an essential regulatory component for the expression of direct and indirect plant defence.     

Aphid responses to volatile cues from turnip plants (Brassica rapa) infested with phloem-feeding and chewing herbivores

Herbivore-induced plant volatiles provide foraging cues for herbivores and for herbivores’ natural enemies. Aphids induce plant volatile emissions and also utilize plant-derived olfactory volatile cues, but the chemical ecology of aphids and other phloem-feeding insects is less extensively documented than that of chewing insects. Here, we characterize the volatile cues emitted by turnip plants (Brassica rapa) under attack by an aphid (Myzus persicae) or by the chewing lepidopteran larva Heliothis virescens. We also tested the behavioral responses of M. persicae individuals to the odors of undamaged and herbivore-damaged plants presented singly or in combination, as well as to the odor of crushed conspecifics (simulating predation). Gas chromatographic analysis of the volatile blend of infested turnips revealed distinct profiles for both aphid- and caterpillar-induced plants, with induced compounds including green-leaf alcohols, esters, and isothiocyanates. In behavioral trials, aphids exhibited increased activity in the presence of plant odors and positive attraction to undamaged turnip plants. However, aphids exhibited a strong preference for the odors of healthy versus plants subjected to herbivore damage, and neither aphid- or caterpillar-damaged plants were attractive compared to clean-air controls. Reduced aphid attraction to herbivore-infested plants may be mediated by changes in the volatile blend constituent composition, including large amounts of isothiocyanates and green-leaf volatiles or, in the case of aphid-infested plants, of the aphid alarm pheromone, (E)-β-farnesene.     

Fall Armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), Female Moths Respond to Herbivore-Induced Corn Volatiles

In response to herbivore attack, plants release herbivore-induced plant volatiles (HIPVs) that represent important chemical cues for herbivore natural enemies. Additionally, HIPVs have been shown to mediate other ecological interactions with herbivores. Differently from natural enemies that are generally attracted to HIPVs, herbivores can be either attracted or repelled depending on several biological and ecological parameters. Our study aimed to assess the olfactory response of fall armyworm-mated female moths toward odors released by mechanically and herbivore-induced corn at different time intervals. Results showed that female moths strongly respond to corn volatiles, although fresh damaged corn odors (0?C1?h) are not recognized by moths. Moreover, females preferred volatiles released by undamaged plant over herbivore-induced plants at 5?C6?h. This preference for undamaged plants may reflect an adaptive strategy of moths to avoid competitors and natural enemies for their offspring. We discussed our results based on knowledge about corn volatile release pattern and raise possible explanations for fall armyworm moth behavior.     

An ecological cost of plant defence: attractiveness of bitter cucumber plants to natural enemies of herbivores

Plants produce defences that act directly on herbivores and indirectly via the attraction of natural enemies of herbivores. We examined the pleiotropic effects of direct chemical defence production on indirect defence employing near‐isogenic varieties of cucumber plants (Cucumis sativus) that differ qualitatively in the production of terpenoid cucurbitacins, the most bitter compounds known. In release–recapture experiments conducted in greenhouse common gardens, blind predatory mites were attracted to plants infested by herbivorous mites. Infested sweet plants (lacking cucurbitacins), however, attracted 37% more predatory mites than infested bitter plants (that produce constitutive and inducible cucurbitacins). Analysis of the headspace of plants revealed that production of cucurbitacins was genetically correlated with large increases in the qualitative and quantitative spectrum of volatile compounds produced by plants, including induced production of (E )‐β‐ocimene (3E )‐4,8‐dimethyl‐1,3,7‐nonatriene, (E,E)‐α‐farnesene, and methyl salicylate, all known to be attractants of predators. Nevertheless, plants that produced cucurbitacins were less attractive to predatory mites than plants that lacked cucurbitacins and predators were also half as fecund on these bitter plants. Thus, we provide novel evidence for an ecological trade‐off between direct and indirect plant defence. This cost of defence is mediated by the effects of cucurbitacins on predator fecundity and potentially by the production of volatile compounds that may be repellent to predators.     

Do plants use airborne cues to recognize herbivores on their neighbours?

Plants show defensive responses after exposure to volatiles from neighbouring plants infested by herbivores. When a plant’s neighbours host only species of herbivores that do not feed on the plant itself, the plant can conserve energy by maintaining a low defence level. An intriguing question is whether plants respond differently to volatiles from plants infested by herbivores that pose greater or lesser degrees of danger. We examined the secretion of extrafloral nectar (EFN) in lima bean plants exposed to volatiles from cabbage plants infested by common cutworm, two-spotted spider mites, or diamondback moth larvae. Although the first two herbivore species feed on lima bean plants, diamondback moth larvae do not. As a control, lima bean plants were exposed to volatiles from uninfested cabbage plants. Only when exposed to volatiles from cabbage plants infested by spider mites did lima bean plants significantly increase their EFN secretion compared with the control. Increased EFN secretion can function as an indirect defence by supplying the natural enemies of herbivores with an alternative food source. Of the three herbivore species, spider mites were the most likely to move from cabbage plants to lima bean plants and presumably posed the greatest threat. Although chemical analyses showed differences among treatments in volatiles produced by herbivore-infested cabbage plants, which compounds or blends triggered the increased secretion of EFN by lima bean plants remains unclear. Thus, our results show that plants may tune their defence levels according to herbivore risk level.     

Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabidopsis thaliana induced by Myzus persicae

In response to herbivory by insects, several plant species have been shown to produce volatiles that attract the natural enemies of those herbivores. Using a Y‐tube olfactometer, we investigated responses of the aphid parasitoid Diaeretiella rapae MacIntosh (Hymenoptera: Aphidiidae) to volatiles from Arabidopsis thaliana Columbia (Brassicaceae) plants that were either undamaged, infested by the peach‐potato aphid, Myzus persicae Sulzer (Homoptera: Aphididae), or mechanically damaged, as well as to volatiles from just the aphid or its honeydew. In dual‐choice experiments, female D. rapae given oviposition experience on A. thaliana infested with M. persicae were significantly attracted to volatiles from A. thaliana infested with M. persicae over volatiles from undamaged A. thaliana and similarly were significantly attracted to plants that had been previously infested by M. persicae, but from which the aphids were removed, over undamaged plants. Diaeretiella rapae did not respond to volatiles from M. persicae alone, their honeydew, or plants mechanically damaged with either a pin or scissors. We conclude that an interaction between the plant and the aphid induces A. thaliana to produce volatiles, which D. rapae can learn and respond to. Poor responses of D. rapae to volatiles from an A. thaliana plant that had two leaves infested with M. persicae, with the two infested leaves being removed before testing, suggested the possibility that, at this stage of infestation, the majority of volatile production induced by M. persicae may be localized to the infested tissues of the plant. We conclude that this tritrophic interaction is a suitable model system for future investigations of the biochemical pathways involved in the production of aphid‐induced volatiles attractive to natural enemies.     

Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush

The possibility of communication between plants was proposed nearly 20 years ago, although previous demonstrations have suffered from methodological problems and have not been widely accepted. Here we report the first rigorous, experimental evidence demonstrating that undamaged plants respond to cues released by neighbors to induce higher levels of resistance against herbivores in nature. Sagebrush plants that were clipped in the field released a pulse of an epimer of methyl jasmonate that has been shown to be a volatile signal capable of inducing resistance in wild tobacco. Wild tobacco plants with clipped sagebrush neighbors had increased levels of the putative defensive oxidative enzyme, polyphenol oxidase, relative to control tobacco plants with unclipped sagebrush neighbors. Tobacco plants near clipped sagebrush experienced greatly reduced levels of leaf damage by grasshoppers and cutworms during three field seasons compared to unclipped controls. This result was not caused by an altered light regime experienced by tobacco near clipped neighbors. Barriers to soil contact between tobacco and sagebrush did not reduce the difference in leaf damage although barriers that blocked air contact negated the effect. Received: 15 February 2000 / Accepted: 1 April 2000     

Attractiveness of Michigan native plants to arthropod natural enemies and herbivores

The use of plants to provide nectar and pollen resources to natural enemies through habitat management is a growing focus of conservation biological control. Current guidelines frequently recommend use of annual plants exotic to the management area, but native perennial plants are likely to provide similar resources and may have several advantages over exotics. We compared a set of 43 native Michigan perennial plants and 5 frequently recommended exotic annual plants for their attractiveness to natural enemies and herbivores for 2 yr. Plant species differed significantly in their attractiveness to natural enemies. In year 1, the exotic annual plants outperformed many of the newly established native perennial plants. In year 2, however, many native perennial plants attracted higher numbers of natural enemies than exotic plants. In year 2, we compared each flowering plant against the background vegetation (grass) for their attractiveness to natural enemies and herbivores. Screening individual plant species allowed rapid assessment of attractiveness to natural enemies. We identified 24 native perennial plants that attracted high numbers of natural enemies with promise for habitat management. Among the most attractive are Eupatorium perfoliatum L., Monarda punctata L., Silphium perfoliatum L., Potentilla fruticosa auct. non L., Coreopsis lanceolata L., Spiraea alba Duroi, Agastache nepetoides (L.) Kuntze, Anemone canadensis L., and Angelica atropurpurea L. Subsets of these plants can now be tested to develop a community of native plant species that attracts diverse natural enemy taxa and provides nectar and pollen throughout the growing season.     

Searching behaviour of an omnivorous predator for novel and native host plants of its herbivores: a study on arthropod colonization of eucalyptus in Brazil

Adaptation to novel host plants is a much‐studied process in arthropod herbivores, but not in their predators. This is surprising, considering the attention that has been given to the role of predators in host range expansion in herbivores; the enemy‐free space hypothesis suggests that plants may be included in the host range of herbivores because of lower predation and parasitism rates on the novel host plants. This effect can only be important if natural enemies do not follow their prey to the novel host plant, at least not immediately, thus allowing the herbivores to adapt to the novel host plant. Hence, depending on the speed with which natural enemies follow their prey to a new host plant, enemy‐free space on novel host plants may only exist for a limited period. This situation may presently be occurring in a system consisting of the herbivorous moth Thyrinteina arnobia Stoll (Lepidoptera: Geometridae) that attacks various species of Myrtaceae, such as guava (Psidium guajava L.) and jaboticaba (Myrciaria spp.), in Brazil. Since the introduction of eucalyptus (Myrtaceae) species into this country some 100 years ago, the moth has included this plant species in its host range and frequently causes outbreaks, a phenomenon that does not occur on the native host plant species. This suggests that the natural enemies that attack the herbivore on native species are not very effective on the novel host. We tested this hypothesis by studying the searching behaviour of one of the natural enemies, the omnivorous predatory bug Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae). When offered a choice between plants of the two species, the predators (originally collected in eucalyptus plantations) preferred guava to eucalyptus when both plant species were clean, infested with herbivores, or damaged by herbivores but with herbivores removed prior to the experiments. The bugs preferred herbivore‐damaged to clean guava, and showed a slight preference for damaged to clean eucalyptus. These results may explain the lack of impact of predatory arthropods on herbivore populations on eucalyptus and suggests that eucalyptus may offer an enemy‐free space for herbivores.     

Genetic variation in plant volatile emission does not result in differential attraction of natural enemies in the field

Volatile organic chemical (VOC) emission by plants may serve as an adaptive plant defense by attracting the natural enemies of herbivores. For plant VOC emission to evolve as an adaptive defense, plants must show genetic variability for the trait. To date, such variability has been investigated primarily in agricultural systems, yet relatively little is known about genetic variation in VOCs emitted by natural populations of native plants. Here, we investigate intraspecific variation in constitutive and herbivore-induced plant VOC emission using the native common milkweed plant (Asclepias syriaca) and its monarch caterpillar herbivore (Danaus plexippus) in complementary field and common garden greenhouse experiments. In addition, we used a common garden field experiment to gauge natural enemy attraction to milkweed VOCs induced by monarch damage. We found evidence of genetic variation in the total constitutive and induced concentrations of VOCs and the composition of VOC blends emitted by milkweed plants. However, all milkweed genotypes responded similarly to induction by monarchs in terms of their relative change in VOC concentration and blend. Natural enemies attacked decoy caterpillars more frequently on damaged than on undamaged milkweed, and natural enemy visitation was associated with higher total VOC concentrations and with VOC blend. Thus, we present evidence that induced VOCs emitted by milkweed may function as a defense against herbivores. However, plant genotypes were equally attractive to natural enemies. Although milkweed genotypes diverge phenotypically in their VOC concentrations and blends, they converge into similar phenotypes with regard to magnitude of induction and enemy attraction.     

Preference for outbred host plants and positive effects of inbreeding on egg survival in a specialist herbivore

Inbreeding can profoundly affect the interactions of plants with herbivores as well as with the natural enemies of the herbivores. We studied how plant inbreeding affects herbivore oviposition preference, and whether inbreeding of both plants and herbivores alters the probability of predation or parasitism of herbivore eggs. In a laboratory preference test with the specialist herbivore moth Abrostola asclepiadis and inbred and outbred Vincetoxicum hirundinaria plants, we discovered that herbivores preferred to oviposit on outbred plants. A field experiment with inbred and outbred plants that bore inbred or outbred herbivore eggs revealed that the eggs of the outbred herbivores were more likely to be lost by predation, parasitism or plant hypersensitive responses than inbred eggs. This difference did not lead to differences in the realized fecundity as the number of hatched larvae did not differ between inbred and outbred herbivores. Thus, the strength of inbreeding depression in herbivores decreases when their natural enemies are involved. Plant inbreeding did not alter the attraction of natural enemies of the eggs. We conclude that inbreeding can significantly alter the interactions of plants and herbivores at different life-history stages, and that some of these alterations are mediated by the natural enemies of the herbivores.     

Chemical interaction between undamaged plants--effects on herbivores and natural enemies

Most research on plant-plant chemical interactions has focussed on events following herbivore or pathogen attack. However, undamaged plants also interact chemically as a natural facet of their behaviour, and this may have consequences for insects that use the plants as hosts. In this review, the links between allelopathy and insect behaviour are outlined. Findings on how chemical interactions between different plant species and genotypes affect aphid herbivores and their natural enemies are reviewed, and the role of plant diversity and chemical interaction for trophic interactions in crops is discussed.     

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.     

Insect-resistant transgenic plants in a multi-trophic context

So far, genetic engineering of plants in the context of insect pest control has involved insertion of genes that code for toxins, and may be characterized as the incorporation of biopesticides into classical plant breeding. In the context of pesticide usage in pest control, natural enemies of herbivores have received increasing attention, because carnivorous arthropods are an important component of insect pest control. However, in plant breeding programmes, natural enemies of herbivores have largely been ignored, although there are many examples that show that plant breeding affects the effectiveness of biological control. Negative influences of modified plant characteristics on carnivorous arthropods may induce population growth of new, even more harmful pest species that had no pest status prior to the pesticide treatment. Sustainable pest management will only be possible when negative effects on non-target, beneficial arthropods are minimized. In this review, we summarize the effects of insect-resistant crops and insect-resistant transgenic crops, especially Bt crops, from a food web perspective. As food web components, we distinguish target herbivores, non-target herbivores, pollinators, parasitoids and predators. Below-ground organisms such as Collembola, nematodes and earthworms should also be included in risk assessment studies, but have received little attention. The toxins produced in Bt plants retain their toxicity when bound to the soil, so accumulation of these toxins is likely to occur. Earthworms ingest the bound toxins but are not affected by them. However, earthworms may function as intermediaries through which the toxins are passed on to other trophic levels. In studies where effects of insect-resistant (Bt) plants on natural enemies were considered, positive, negative and no effects have been found. So far, most studies have concentrated on natural enemies of target herbivores. However, Bt toxins are structurally rearranged when they bind to midgut receptors, so that they are likely to lose their toxicity inside target herbivores. What happens to the toxins in non-target herbivores, and whether these herbivores may act as intermediaries through which the toxins may be passed on to the natural enemies, remains to be studied.     

Investigations into plant biochemical wound-response pathways involved in the production of aphid-induced plant volatiles

Feeding damage to plants by insect herbivores induces the production of plant volatiles, which are attractive to the herbivores natural enemies. Little is understood about the plant biochemical pathways involved in aphid-induced plant volatile production. The aphid parasitoid Diaeretiella rapae can detect and respond to aphid-induced volatiles produced by Arabidopsis thaliana. When given experience of those volatiles, it can learn those cues and can therefore be used as a novel biosensor to detect them. The pathways involved in aphid-induced volatile production were investigated by comparing the responses of D. rapae to volatiles from a number of different transgenic mutants of A. thaliana, mutated in their octadecanoid, ethylene or salicylic acid wound-response pathways and also from wild-type plants. Plants were either undamaged or infested by the peach-potato aphid, Myzus persicae. It is demonstrated that the octadecanoid pathway and specifically the COI1 gene are required for aphid-induced volatile production. The presence of salicylic acid is also involved in volatile production. Using this model system, in combination with A. thaliana plants with single point gene mutations, has potential for the precise dissection of biochemical pathways involved in the production of aphid-induced volatiles.     

Indirect cost of a defensive trait: variation in trichome type affects the natural enemies of herbivorous insects on <Emphasis Type="Italic">Datura wrightii</Emphasis>

The costs and benefits of defensive traits in plants can have an ecological component that arises from the effect of defenses on the natural enemies of herbivores. We tested if glandular trichomes in Datura wrightii, a trait that confers resistance to several species of herbivorous insects, impose an ecological cost by decreasing rates of predation by the natural enemies of herbivores. For two common herbivores of D. wrightii, Lema daturaphila and Tupiocoris notatus, several generalized species of natural enemies exhibited lower rates of predation on glandular compared to non-glandular plants. Lower rates of predation were associated with reductions in the residence time and foraging efficiency of natural enemies on plants with glandular trichomes, but not with direct toxic effects of glandular exudate. Our results suggest that the benefit of resistance to herbivores conferred by glandular trichomes might be offset by the detrimental effect of this trait on the natural enemies of herbivores, and that the fitness consequences of this trichome defense might depend on the composition and abundance of the natural-enemy community.