Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods?

Plants that are damaged by herbivorous arthropods provide carnivorous enemies of the herbivores with important information. They emit an induced volatile blend that is highly detectable to the carnivores from a distance. Such detectable signals that indicate herbivore presence are important for the carnivores because herbivores themselves are under strong selection not to expose themselves. In addition, carnivores would benefit from a specificity of the induced plant volatiles. Whether herbivore-induced plant volatiles are reliable indicators of herbivore identity, however, has not been resolved unambiguously. Some studies support the reliability of herbivore-induced plant volatiles, while others do not. Different approaches have been used such as chemical analysis, behavioural analysis or a combination of the two. Based on the total of chemical studies one might conclude that in most cases herbivore-induced plant volatiles are not very specific for the herbivore that damages the plant. However, arthropod chemosensors are much more sensitive than the detectors of analytical instruments. Therefore, chemical analyses are not suitable to demonstrate whether or not herbivore-induced plant volatiles are reliable indicators of herbivore identity to carnivores. Behavioural studies should provide this information. In analysing carnivore behaviour it should be realised, however, that arthropod behaviour can be highly variable. Arthropod foraging decisions are affected by external and internal factors such as (a) abiotic environmental factors, (b) presence of competitors or enemies, (c) deprivation of food or oviposition sites, (d) specific deprivation of certain nutrients or (e) learning. In this paper their effect on discrimination of carnivores between volatile blends emitted by plants infested by different herbivores is reviewed. This provides testable hypotheses of why discrimination was not found in some studies. The ability of carnivores to discriminate is likely to be more common than is clear to date, which should invoke functional studies of the conditions that influence the occurrence of this discrimination.     

Non‐pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid‐induced plant volatiles via jasmonic acid signalling

Beneficial soil‐borne microbes, such as mycorrhizal fungi or rhizobacteria, can affect the interactions of plants with aboveground insects at several trophic levels. While the mechanisms of interactions with herbivorous insects, that is, the second trophic level, are starting to be understood, it remains unknown how plants mediate the interactions between soil microbes and carnivorous insects, that is, the third trophic level. Using Arabidopsis thaliana Col‐0 and the aphid Myzus persicae, we evaluate here the underlying mechanisms involved in the plant‐mediated interaction between the non‐pathogenic rhizobacterium Pseudomonas fluorescens and the parasitoid Diaeretiella rapae, by combining ecological, chemical and molecular approaches. Rhizobacterial colonization modifies the composition of the blend of herbivore‐induced plant volatiles. The volatile blend from rhizobacteria‐treated aphid‐infested plants is less attractive to an aphid parasitoid, in terms of both olfactory preference behaviour and oviposition, than the volatile blend from aphid‐infested plants without rhizobacteria. Importantly, the effect of rhizobacteria on both the emission of herbivore‐induced volatiles and parasitoid response to aphid‐infested plants is lost in an Arabidopsis mutant (aos/dde2‐2) that is impaired in jasmonic acid production. By modifying the blend of herbivore‐induced plant volatiles that depend on the jasmonic acid‐signalling pathway, root‐colonizing microbes interfere with the attraction of parasitoids of leaf herbivores.     

Contrasting patterns of herbivore and predator pressure on invasive and native plants

Invasive non-native plant species often harbor fewer herbivorous insects than related native plant species. However, little is known about how herbivorous insects on non-native plants are exposed to carnivorous insects, and even less is known on plants that have recently expanded their ranges within continents due to climate warming. In this study we examine the herbivore load (herbivore biomass per plant biomass), predator load (predator biomass per plant biomass) and predator pressure (predator biomass per herbivore biomass) on an inter-continental non-native and an intra-continental range-expanding plant species and two congeneric native species. All four plant species co-occur in riparian habitat in north-western Europe. Insects were collected in early, mid and late summer from three populations of all four species. Before counting and weighing the insects were classified to trophic guild as carnivores (predators), herbivores, and transients. Herbivores were further subdivided into leaf-miners, sap-feeders, chewers and gallers. Total herbivore loads were smaller on inter-continental non-native and intra-continental range-expanding plants than on the congeneric natives. However, the differences depended on time within growing season, as well as on the feeding guild of the herbivore. Although the predator load on non-native plants was not larger than on natives, both non-native plant species had greater predator pressure on the herbivores than the natives. We conclude that both these non-native plant species have better bottom-up as well as top-down control of herbivores, but that effects depend on time within growing season and (for the herbivore load) on herbivore feeding guild. Therefore, when evaluating insects on non-native plants, variation within season and differences among feeding guilds need to be taken into account.     

Experimental Manipulation of Grassland Plant Diversity Induces Complex Shifts in Aboveground Arthropod Diversity

Changes in producer diversity cause multiple changes in consumer communities through various mechanisms. However, past analyses investigating the relationship between plant diversity and arthropod consumers focused only on few aspects of arthropod diversity, e.g. species richness and abundance. Yet, shifts in understudied facets of arthropod diversity like relative abundances or species dominance may have strong effects on arthropod-mediated ecosystem functions. Here we analyze the relationship between plant species richness and arthropod diversity using four complementary diversity indices, namely: abundance, species richness, evenness (equitability of the abundance distribution) and dominance (relative abundance of the dominant species). Along an experimental gradient of plant species richness (1, 2, 4, 8, 16 and 60 plant species), we sampled herbivorous and carnivorous arthropods using pitfall traps and suction sampling during a whole vegetation period. We tested whether plant species richness affects consumer diversity directly (i), or indirectly through increased productivity (ii). Further, we tested the impact of plant community composition on arthropod diversity by testing for the effects of plant functional groups (iii). Abundance and species richness of both herbivores and carnivores increased with increasing plant species richness, but the underlying mechanisms differed between the two trophic groups. While higher species richness in herbivores was caused by an increase in resource diversity, carnivore richness was driven by plant productivity. Evenness of herbivore communities did not change along the gradient in plant species richness, whereas evenness of carnivores declined. The abundance of dominant herbivore species showed no response to changes in plant species richness, but the dominant carnivores were more abundant in species-rich plant communities. The functional composition of plant communities had small impacts on herbivore communities, whereas carnivore communities were affected by forbs of small stature, grasses and legumes. Contrasting patterns in the abundance of dominant species imply different levels of resource specialization for dominant herbivores (narrow food spectrum) and carnivores (broad food spectrum). That in turn could heavily affect ecosystem functions mediated by herbivorous and carnivorous arthropods, such as herbivory or biological pest control.     

Trophic Cascades in Terrestrial Systems: A Review of the Effects of Carnivore Removals on Plants

We present a quantitative synthesis of trophic cascades in terrestrial systems using data from 41 studies, reporting 60 independent tests. The studies covered a wide range of taxa in various terrestrial systems with varying degrees of species diversity. We quantified the average magnitude of direct effects of carnivores on herbivore prey and indirect effects of carnivores on plants. We examined how the effect magnitudes varied with type of carnivores in the study system, food web diversity, and experimental protocol. A metaanalysis of the data revealed that trophic cascades were common among the studies. Exceptions to this general trend did arise. In some cases, trophic cascades were expected not to occur, and they did not. In other cases, the direct effects of carnivores on herbivores were stronger than the indirect effects of carnivores on plants, indicating that top-down effects attenuated. Top-down effects usually attenuated whenever plants contained antiherbivore defenses or when herbivore species diversity was high. Conclusions about the strength of top-down effects of carnivores varied with the type of carnivore and with the plant-response variable measured. Vertebrate carnivores generally had stronger effects than invertebrate carnivores. Carnivores, in general, had stronger effects when the response was measured as plant damage rather than as plant biomass or plant reproductive output. We caution, therefore, that conclusions about the strength of top-down effects could be an artifact of the plant-response variable measured. We also found that mesocosm experiments generally had weaker effect magnitudes than open-plot field experiments or observational experiments. Trophic cascades in terrestrial systems, although not a universal phenomenon, are a consistent response throughout the published studies reviewed here. Our analysis thus suggests that they occur more frequently in terrestrial systems than currently believed. Moreover, the mechanisms and strengths of top-down effects of carnivores are equivalent to those found in other types of systems (e.g., aquatic environments).     

Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host

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.     

Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals

It is widely reported that plants emit volatile compounds when they are attacked by herbivorous insects, which may be used by parasitoids and predators to locate their host or prey. The study of herbivore-induced plant volatiles and their role in mediating interactions between plants, herbivores and their natural enemies have been primarily based on aboveground systems, generally ignoring the potential interactions between above and belowground infochemical- and food webs. This study examines whether herbivory by Delia radicum feeding on roots of Brassica nigra (black mustard) affects the behaviour of Cotesia glomerata , a parasitoid of the leaf herbivore Pieris brassicae , mediated by changes in plant volatiles. In a semi-field experiment with root-damaged and root-undamaged plants C. glomerata prefers to oviposit in hosts feeding on root-undamaged plants. In addition, in a flight-cage experiment the parasitoid also prefers to search for hosts on plants without root herbivores. Plants exposed to root herbivory were shown to emit a volatile blend characterized by high levels of specific sulphur volatile compounds, which are reported to be highly toxic for insects, combined with low levels of several compounds, i.e. beta-farnesene, reported to act as attractants for herbivorous and carnivorous insects. Our results provide evidence that the foraging behaviour of a parasitoid of an aboveground herbivore can be influenced by belowground herbivores through changes in the plant volatile blend. Such indirect interactions may have profound consequences for the evolution of host selection behaviour in parasitoids, and may play an important role in the structuring and functioning of communities.     

Terrestrial trophic cascades: how much do they trickle?

Although more consensus is now emerging on the magnitude and frequency of cascading trophic effects in aquatic communities, the debate over their terrestrial counterparts continues. We used meta-analysis to analyze field experiments on trophic cascades in terrestrial arthropod-dominated food webs to evaluate the overall magnitude of trophic cascades and conditions affecting their occurrence and strength. We found extensive support for the presence of trophic cascades in terrestrial communities. In the majority of experiments, predator removal led to increased densities of herbivorous insects and higher levels of plant damage. Cascades in which removing predators led to decreased herbivory also were detected but were less frequent and weaker, suggesting a predominantly three-trophic-level behavior of arthropod-dominated terrestrial food webs. Despite the clear evidence that cascades often decreased plant damage, residual effects of predation produced either no or only minimal changes in overall plant biomass. Agricultural systems and natural communities exhibited similarly strong effects of predation on herbivore abundance. However, resulting effects on plant damage and community-wide effects of trophic cascades on plant biomass usually were highly variable, and only in the managed agricultural systems did predators occasionally have strong indirect effects on plant biomass. Our meta-analysis suggests that the effects of trophic cascades on the biomass of primary producers are weaker in terrestrial than aquatic food webs.     

Differential induction of plant chemical defenses by parasitized and unparasitized herbivores: consequences for reciprocal,multitrophic interactions

Insect parasitoids can play ecologically important roles in virtually all terrestrial plant–insect herbivore interactions, yet whether parasitoids alter the defensive traits that underlie interactions between plants and their herbivores remains a largely unexplored question. Here, we examined the reciprocal trophic interactions among populations of the wild cabbage Brassica oleracea that vary greatly in their production of defensive secondary compounds – glucosinolates (GSs), a generalist herbivore, Trichoplusia ni, and its polyembryonic parasitoid Copidosoma floridanum. In a greenhouse environment, plants were exposed to either healthy (unparasitized), parasitized, or no herbivores. Feeding damage by herbivores induced higher levels of the indole GSs, glucobrassicin and neoglucobrassicin, but not any of the other measured GSs. Herbivores parasitized by C. floridanum induced cabbage plants to produce 1.5 times more indole GSs than levels induced by healthy T. ni and five times more than uninduced plants. As a gregarious endoparasitoid, C. floridanum causes its host T. ni to feed more than unparasitized herbivores resulting in increased induction of indole GSs. In turn, herbivore fitness parameters (including differential effects on male and female contributions to lifetime fecundity in the herbivore) were negatively correlated with the aliphatic GSs, sinigrin and gluconapin, whereas parasitoid fitness parameters were negatively correlated with the indole GSs, glucobrassicin and neoglucobrassicin. That herbivores and their parasitoids appear to be affected by different sets of GSs was unexpected given the intimate developmental associations between host and parasitoid. This study is the first to demonstrate that parasitoids, through increasing feeding by their herbivorous hosts, can induce higher levels of non‐volatile plant chemical defenses. While parasitoids are widely recognized to be ubiquitous in most terrestrial insect herbivore communities, their role in influencing plant–insect herbivore relationships is still vastly underappreciated.     

Nutrient-limited food webs with up to three trophic levels: feasibility, stability, assembly rules, and effects of nutrient enrichment

Community structure is controlled, among multiple factors, by competition and predation. Using the R* rule and graphical analysis, we analyse here the feasibility, stability and assembly rules of resource-based food webs with up to three trophic levels. In particular, we show that (1) the stability of a food web with two plants and two generalist herbivores does not require that plants' resource exploitation abilities trade-off with resistance to the two herbivores, and (2) food webs with two plants and either one generalist herbivore and a carnivore or two generalist herbivores and two generalist carnivores are not feasible because of cascade competition between top consumers. The relative strength of species interactions and the relative impacts of plants and herbivores on factors which control their growth also play a critical role. We discuss how community structure constrains assembly rules and yields cascades of extinctions in food webs.     

Parasitic wasp‐associated symbiont affects plant‐mediated species interactions between herbivores

Microbial mutualistic symbiosis is increasingly recognised as a hidden driving force in the ecology of plant–insect interactions. Although plant‐associated and herbivore‐associated symbionts clearly affect interactions between plants and herbivores, the effects of symbionts associated with higher trophic levels has been largely overlooked. At the third‐trophic level, parasitic wasps are a common group of insects that can inject symbiotic viruses (polydnaviruses) and venom into their herbivorous hosts to support parasitoid offspring development. Here, we show that such third‐trophic level symbionts act in combination with venom to affect plant‐mediated interactions by reducing colonisation of subsequent herbivore species. This ecological effect correlated with changes induced by polydnaviruses and venom in caterpillar salivary glands and in plant defence responses to herbivory. Because thousands of parasitoid species are associated with mutualistic symbiotic viruses in an intimate, specific relationship, our findings may represent a novel and widespread ecological phenomenon in plant–insect interactions.     

Quantifying the impact of above‐ and belowground higher trophic levels on plant and herbivore performance by modeling1

Growing empirical evidence suggests that aboveground and belowground multitrophic communities interact. However, investigations that comprehensively explore the impacts of above‐ and belowground third and higher trophic level organisms on plant and herbivore performance are thus far lacking. We tested the hypotheses that above‐ and belowground higher trophic level organisms as well as decomposers affect plant and herbivore performance and that these effects cross the soil–surface boundary. We used a well‐validated simulation model that is individual‐based for aboveground trophic levels such as shoot herbivores, parasitoids, and hyperparasitoids while considering belowground herbivores and their antagonists at the population level. We simulated greenhouse experiments by removing trophic levels and decomposers from the simulations in a factorial design. Decomposers and above‐ and belowground third trophic levels affected plant and herbivore mortality, root biomass, and to a lesser extent shoot biomass. We also tested the effect of gradual modifications of the interactions between different trophic level organisms with a sensitivity analysis. Shoot and root biomass were highly sensitive to the impact of the fourth trophic level. We found effects that cross the soil surface, such as aboveground herbivores and parasitoids affecting root biomass and belowground herbivores influencing aboveground herbivore mortality. We conclude that higher trophic level organisms and decomposers can strongly influence plant and herbivore performance. We propose that our modelling framework can be used in future applications to quantitatively explore the possible outcomes of complex above‐ and belowground multitrophic interactions under a range of environmental conditions and species compositions.     

Effect of pollen supplement on intraguild predatory interactions between two omnivores: The importance of spatial dynamics

Arthropods often engage in complex trophic interactions such as intraguild predation (IGP), true omnivory (i.e., feeding on plants and prey), and apparent competition. Theoretical treatments of the effects of such interactions on herbivore populations have been concerned almost entirely with equilibrium conditions. Yet these interactions are common in non-equilibrium settings such as agroecosystems, where they are likely to have a strong influence on pest populations. We therefore tested short-term effects of IGP and food supplementation on interactions between two predators (the phytoseiid mite Neoseiulus cucumeris and the anthocorid bug Orius laevigatus) and their shared prey, Frankliniella occidentalis, on strawberry plants. All three consumers feed on strawberry pollen, both mites and bugs prey on thrips, and the bug also feeds on the mites (IGP). Strong IGP on mites (IG prey) by the bugs (IG predator) was recorded in structurally-simple arenas. In a more complex setting (whole-plants), however, the intensity of IGP differed among plant structures. Likewise, pollen supplementation reduced both IGP and predation on thrips in a structurally simple setting. In the whole-plant experiment, IGP was more intense on pollen-bearing than pollen-free flowers. The study illustrated how spatial dynamics, generated when consumers track food sources differently in the habitat and possibly when herbivorous and IG prey alter their distribution to escape predation, led to site-specific configuration of interacting populations. The intensity of resulting trophic interactions was weakened by food supplementation and by increased complexity of the habitat.     

Friend or foe?: a plant's induced response to an omnivore

Omnivorous natural enemies of herbivores consume plant-based resources and may elicit induced resistance in their host plant. A greater induction threshold for damage produced by omnivorous predators than for strict herbivores might be expected if omnivore performance is enhanced on noninduced plants, allowing them to reduce future levels of herbivory. Currently, it is not known if a plant responds to feeding by omnivorous predators and by herbivores similarly. To examine this question, we chose herbivore and omnivore species that produce the same kind of quantifiable damage to cotton leaves, enabling us to control statistically for the intensity of plant damage, and ask whether plant responses differed depending on the identity of the damaging species. We first compared changes in plant peroxidase activity, gossypol gland number and density, and leaf area in response to feeding by the spider mite Tetranychus turkestani (Ugarov and Nikolski) (an herbivore) and by one of the mite's principal natural enemies, the western flower thrips Frankliniella occidentalis (Pergande) (an omnivore). Both species increased the activity of peroxidase, but when we controlled for the amount of damage, the peroxidase activity of mite-damaged plants was higher than that of thrips-damaged plants. We also found that thrips, but not spider mites, increased the density of gossypol glands in the second true leaf. In a second experiment we included an additional herbivore, the bean thrips Caliothrips fasciatus (Pergande), to see if the different responses of cotton to thrips and mite herbivory we first observed were attributable to differences in trophic function (herbivore versus omnivore) or to other differences in feeding generated by thrips versus mites. Cotton plants exhibited the same pattern of induced responses (elevated peroxidase, increased number of glands, reduced leaf area) to herbivory generated by the bean thrips (an herbivore) and western flower thrips (an omnivore), suggesting that trophic function was not a key determinant of plant response. Thrips-damaged plants again showed a significantly higher density of gossypol glands than did mite-damaged plants. Overall, our results suggest that (1) an omnivorous predator systemically induces resistance traits in cotton and (2) whereas there is evidence of taxonomic specificity (thrips versus mites), there is little support for trophic specificity (herbivorous thrips versus omnivorous thrips) in the elicitation of induced responses.     

Effects of environmental stress cascade up through four trophic levels in a salt marsh study system

1. Although in recent years there have been a number of studies demonstrating trophic cascades in terrestrial systems, it is still unclear what environmental conditions enable or enhance such cascades, especially among four trophic levels. 2. In this study, the influence of environmental stress (increased soil pore water salinity) on a four trophic level study system in a Florida salt marsh was examined by experimentally increasing soil pore water salinity. Effects of increased salinity on the quality of the host plant, Batis maritima, were assessed, as were resulting effects on the lepidopteran herbivore Ascia monuste, and the primary parasitoids and hyperparasitoids of its caterpillars. 3. Increased salinity altered host‐plant quality, which subsequently affected the consumer species. These effects of altered plant quality cascaded up through the herbivore and primary parasitoid to the hyperparasitoid Hypopteromalus inimicus, influencing its density, sex ratio, body size, and initial egg load. 4. These results demonstrate how heterogeneity in environmental stress can result in effects that cascade up through four trophic levels. We suggest that such strong effects at higher trophic levels may be more likely in systems in which relationships are more specific and intimate such as those among hosts, parasitoids, and hyperparasitoids.     

Early herbivore alert matters: plant‐mediated effects of egg deposition on higher trophic levels benefit plant fitness

Induction of plant defences, specifically in response to herbivore attack, can save costs that would otherwise be needed to maintain defences even in the absence of herbivores. However, plants may suffer considerable damage during the time required to mount these defences against an attacker. This could be resolved if plants could respond to early cues, such as egg deposition, that reliably indicate future herbivory. We tested this hypothesis in a field experiment and found that egg deposition by the butterfly Pieris brassicae on black mustard (Brassica nigra) induced a plant response that negatively affected feeding caterpillars. The effect cascaded up to the third and fourth trophic levels (larval parasitoids and hyperparasitoids) by affecting the parasitisation rate and parasitoid performance. Overall, the defences induced by egg deposition had a positive effect on plant seed production and may therefore play an important role in the evolution of plant resistance to herbivores.     

Habitat fragmentation resulting in overgrazing by herbivores

Habitat fragmentation sometimes results in outbreaks of herbivorous insect and causes an enormous loss of primary production. It is hypothesized that the driving force behind such herbivore outbreaks is disruption of natural enemy attack that releases herbivores from top-down control. To test this hypothesis I studied how trophic community structure changes along a gradient of habitat fragmentation level using spatially implicit and explicit models of a tri-trophic (plant, herbivore and natural enemy) food chain. While in spatially implicit model number of trophic levels gradually decreases with increasing fragmentation, in spatially explicit model a relatively low level of habitat fragmentation leads to overgrazing by herbivore to result in extinction of the plant population followed by a total system collapse. This provides a theoretical support to the hypothesis that habitat fragmentation can lead to overgrazing by herbivores and suggests a central role of spatial structure in the influence of habitat fragmentation on trophic communities. Further, the spatially explicit model shows (i) that the total system collapse by the overgrazing can occur only if herbivore colonization rate is high; (ii) that with increasing natural enemy colonization rate, the fragmentation level that leads to the system collapse becomes higher, and the frequency of the collapse is lowered.     

Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels

Plants release volatiles induced by herbivore feeding that may affect the diversity and composition of plant-associated arthropod communities. However, the specificity and role of plant volatiles induced during the early phase of attack, i.e. egg deposition by herbivorous insects, and their consequences on insects of different trophic levels remain poorly explored. In olfactometer and wind tunnel set-ups, we investigated behavioural responses of a specialist cabbage butterfly (Pieris brassicae) and two of its parasitic wasps (Trichogramma brassicae and Cotesia glomerata) to volatiles of a wild crucifer (Brassica nigra) induced by oviposition of the specialist butterfly and an additional generalist moth (Mamestra brassicae). Gravid butterflies were repelled by volatiles from plants induced by cabbage white butterfly eggs, probably as a means of avoiding competition, whereas both parasitic wasp species were attracted. In contrast, volatiles from plants induced by eggs of the generalist moth did neither repel nor attract any of the tested community members. Analysis of the plant's volatile metabolomic profile by gas chromatography-mass spectrometry and the structure of the plant-egg interface by scanning electron microscopy confirmed that the plant responds differently to egg deposition by the two lepidopteran species. Our findings imply that prior to actual feeding damage, egg deposition can induce specific plant responses that significantly influence various members of higher trophic levels.     

Experimental Infection of Plants with an Herbivore-Associated Bacterial Endosymbiont Influences Herbivore Host Selection Behavior

Although bacterial endosymbioses are common among phloeophagous herbivores, little is known regarding the effects of symbionts on herbivore host selection and population dynamics. We tested the hypothesis that plant selection and reproductive performance by a phloem-feeding herbivore (potato psyllid, Bactericera cockerelli) is mediated by infection of plants with a bacterial endosymbiont. We controlled for the effects of herbivory and endosymbiont infection by exposing potato plants (Solanum tuberosum) to psyllids infected with “Candidatus Liberibacter solanacearum” or to uninfected psyllids. We used these treatments as a basis to experimentally test plant volatile emissions, herbivore settling and oviposition preferences, and herbivore population growth. Three important findings emerged: (1) plant volatile profiles differed with respect to both herbivory and herbivory plus endosymbiont infection when compared to undamaged control plants; (2) herbivores initially settled on plants exposed to endosymbiont-infected psyllids but later defected and oviposited primarily on plants exposed only to uninfected psyllids; and (3) plant infection status had little effect on herbivore reproduction, though plant flowering was associated with a 39% reduction in herbivore density on average. Our experiments support the hypothesis that plant infection with endosymbionts alters plant volatile profiles, and infected plants initially recruited herbivores but later repelled them. Also, our findings suggest that the endosymbiont may not place negative selection pressure on its host herbivore in this system, but plant flowering phenology appears correlated with psyllid population performance.