Leaf-chewing Herbivores Research Articles

No support for the optimal allocation to indirect plant defenses mediated by ant-hemipteran interactions

The Optimal Defense Theory (ODT) postulates that reproductive structures should be more heavily defended because they contribute the most to a plant's fitness and have the highest probability of being attacked by herbivores. Ants can provide indirect defense to plants through their mutualistic interactions with hemipteran insects. In this well-studied interaction, ants provide protection to hemipterans against their natural enemies (e.g., predators and parasitic wasps) in exchange for the sugar-rich honeydew secreted by hemipterans. In turn, ants attending hemipterans can indirectly benefit plants by suppressing other harmful herbivores. Despite the numerous investigations of this ant-hemipteran mutualism, patterns of optimal allocation to indirect plant defenses mediated by this mutualistic interaction have not been previously investigated. In this study, we evaluated whether allocation to indirect plant defenses mediated by ant-hemipteran interactions and the effectiveness of such indirect defenses differ between vegetative branches (with only leaves) and reproductive branches (with leaves and inflorescences) of the tropical shrub Solanum lycocarpum. For this, we selected plants with aggregations of the ant-tended hemipteran Enchenopa brasiliensis in both reproductive and vegetative branches. We then estimated indirect defenses (measured as the production of sugar in the plant sap and hemipteran honeydew, as well as ant attraction), and their effectiveness in terms of plant protection by ants (measured as the damage and survival of leaf-chewing herbivores). Supporting ODT predictions, we found that the sugar concentration in the plant sap, and consequently in hemipteran honeydew, was higher in reproductive than in vegetative branches. However, the increase in sugar concentration in hemipteran honeydew did not result in greater ant attraction to reproductive branches. Additionally, contrary to ODT predictions, we found that ants attending hemipterans did not enhance plant protection against leaf-chewing herbivores on reproductive branches. Overall, our study demonstrated that the patterns of allocation to indirect defenses mediated by ant-hemipteran interactions in S. lycocarpum plants did not support the predictions of the ODT.

Phloem-feeding insects create parasitoid-free space for caterpillars

Seemingly small ecological changes can have large, ramifying effects that defy expectations. Such are keystone effects in ecosystems. Phloem-feeding insect herbivores can act as keystone species by altering community structure and species interactions via plant-mediated or ant-mediated mechanisms. Plant responses triggered by phloem feeders can disrupt tri-trophic interactions induced by leaf-chewing herbivores, while ants that tend phloem feeders can deter or prey on other arthropods. Here, we investigate how phloem-feeding herbivores change caterpillar-parasitoid interactions on Quercus alba (white oak) trees in natural forests. We factorially manipulated the presence of phloem-feeding insects as well as ant access on Q.alba branches over multiple years and sites and measured parasitism rates of co-occurring caterpillars. While 19.3% of caterpillars were parasitized when phloem feeders were removed, the presence of phloem feeders completely suppressed parasitism of caterpillars (0%). This stark pattern was consistent across the diverse community of phloem feeders and caterpillars. Our manipulation of ant access had no effect on parasitism of caterpillars, implicating a plant-mediated mechanism. We further assessed the mechanistic hypothesis that phloem feeders suppress plant emission of caterpillar-induced volatile compounds, which could disrupt host-location behavior by parasitoids of caterpillars. Phloem feeders indeed reduced concentrations of four volatile compounds, consistent with the putative plant volatile-mediated mechanism. Given the important role of parasitoids in controlling herbivore populations, this keystone effect of phloem feeders offers novel insight into community dynamics in forests and potentially other terrestrial ecosystems.

Genotypic Variation and Potential Mechanisms of Resistance against Multiple Insect Herbivores in Cranberries.

Plant genotypes often exhibit varying resistance levels to herbivores. However, the impact of this genotypic variation on resistance against multiple herbivores remains poorly understood, especially in crops undergoing recent process of domestication. To address this gap, we studied the magnitude and mechanism of resistance in 12 cranberry (Vaccinium macrocarpon) genotypes to three leaf-chewing herbivores - Sparganothis fruitworm (Sparganothis sulfureana), spotted fireworm (Choristoneura parallela), and spongy moth (Lymantria dispar) - along a domestication gradient (native 'wild' genotypes, 'early hybrid' genotypes, and 'modern hybrid' genotypes). Like cranberries, S. sulfureana and C. parallela are native to the United Sates, while L. dispar is an invasive pest. We measured the survival and growth of larvae on each genotype, as well as variation in plant performance (height and biomass) and leaf defensive chemical traits (C/N ratio, total phenolics, total proanthocyanidins, and flavonols levels) in these genotypes to elucidate potential resistance mechanisms. We found differences in C. parallela and L. dispar larval performance across genotypes, with larvae performing better on the modern hybrid genotypes, while S. sulfureana showed no differences. Morphological and chemical traits varied among genotypes, with total phenolics being the only trait correlated with C. parallela and L. dispar larval performance. Notably, the wild genotypes 'McFarlin' and 'Potter' had higher total phenolics and were more resistant to both herbivores than the modern hybrids 'Demoranville' and 'Mullica Queen.' This research contributes to a comprehensive understanding of the impact of crop domestication on multiple insect herbivores, offering insights for future breeding efforts to enhance host-plant resistance against agricultural pests.

Legacy effects of premature defoliation in response to an extreme drought event modulate phytochemical profiles with subtle consequences for leaf herbivory in European beech.

Extreme droughts can have long-lasting effects on forest community dynamics and species interactions. Yet, our understanding of how drought legacy modulates ecological relationships is just unfolding. We tested the hypothesis that leaf chemistry and herbivory show long-term responses to premature defoliation caused by an extreme drought event in European beech (Fagus sylvatica L.). For two consecutive years after the extreme European summer drought in 2018, we collected leaves from the upper and lower canopy of adjacently growing drought-stressed and unstressed trees. Leaf chemistry was analyzed and leaf damage by different herbivore-feeding guilds was quantified. We found thatdrought had lasting impacts on leaf nutrients and on specialized metabolomic profiles. However, drought did not affect the primary metabolome. Drought-related phytochemical changes affected damage of leaf-chewing herbivores whereas damage caused by other herbivore-feeding guilds was largely unaffected. Drought legacy effects on phytochemistry and herbivory were often weaker than between-year or between-canopy strata variability. Our findings suggest that a single extreme drought event bears the potential to long-lastingly affect tree-herbivore interactions. Drought legacy effects likely become more important in modulating tree-herbivore interactions since drought frequency and severity are projected to globally increase in the coming decades.

Plant diversity and soil legacy independently affect the plant metabolome and induced responses following herbivory.

Plant and soil biodiversity can have significant effects on herbivore resistance mediated by plant metabolites. Here, we disentangled the independent effects of plant diversity and soil legacy on constitutive and herbivore-induced plant metabolomes of three plant species in two complementary microcosm experiments. First, we grew plants in sterile soil with three different plant diversity levels. Second, single plant species were grown on soil with different plant diversity-induced soil legacies. We infested a subset of all plants with Spodoptera exigua larvae, a generalist leaf-chewing herbivore, and assessed foliar and root metabolomes. Neither plant diversity nor soil legacy had significant effects on overall foliar, root, or herbivore-induced metabolome composition. Herbivore-induced metabolomes, however, differed from those of control plants. We detected 139 significantly regulated metabolites by comparing plants grown in monocultures with conspecifics growing in plant or soil legacy mixtures. Moreover, plant-plant and plant-soil interactions regulated 141 metabolites in herbivore-induced plants. Taken together, plant diversity and soil legacy independently alter the concentration and induction of plant metabolites, thus affecting the plant's defensive capability. This is a first step toward disentangling plant and soil biodiversity effects on herbivore resistance, thereby improving our understanding of the mechanisms that govern ecosystem functioning.

Age-dependent resistance of a perennial herb, Aristolochia contorta against specialist and generalist leaf-chewing herbivores.

Plants need to balance investments in growth and defense throughout their life to increase their fitness. To optimize fitness, levels of defense against herbivores in perennial plants may vary according to plant age and season. However, secondary plant metabolites often have a detrimental effect on generalist herbivores, while many specialists have developed resistance to them. Therefore, varying levels of defensive secondary metabolites depending on plant age and season may have different effects on the performance of specialist and generalist herbivores colonizing the same host plants. In this study, we analyzed concentrations of defensive secondary metabolites (aristolochic acids) and the nutritional value (C/N ratios) of 1st-, 2nd- and 3rd-year Aristolochia contorta in July (the middle of growing season) and September (the end of growing season). We further assessed their effects on the performances of the specialist herbivore Sericinus montela (Lepidoptera: Papilionidae) and the generalist herbivore Spodoptera exigua (Lepidoptera: Noctuidae). Leaves of 1st-year A. contorta contained significantly higher concentrations of aristolochic acids than those of older plants, with concentrations tending to decrease over the first-year season. Therefore, when first year leaves were fed in July, all larvae of S. exigua died and S. montela showed the lowest growth rate compared to older leaves fed in July. However, the nutritional quality of A. contorta leaves was lower in September than July irrespective of plant age, which was reflected in lower larval performance of both herbivores in September. These results suggest that A. contorta invests in the chemical defenses of leaves especially at a young age, while the low nutritional value of leaves seems to limit the performance of leaf-chewing herbivores at the end of the season, regardless of plant age.

Leaf-chewing herbivores affect preference and performance of a specialist root herbivore

Plants interact with a diversity of phytophagous insects above- and belowground. By inducing plant defence, one insect herbivore species can antagonize or facilitate other herbivore species feeding on the same plant, even when they are separated in space and time. Through systemic plant-mediated interactions, leaf-chewing herbivores may affect the preference and performance of root-feeding herbivores. We studied how six different leaf-chewing herbivore species of Brassica oleracea plants affected oviposition preference and larval performance of the root-feeding specialist Delia radicum. We expected that female D. radicum flies would oviposit where larval performance was highest, in accordance with the preference–performance hypothesis. We also assessed how the different leaf-chewing herbivore species affected defence-related gene expression in leaves and primary roots of B. oleracea, both before and after infestation with the root herbivore. Our results show that leaf-chewing herbivores can negatively affect the performance of root-feeding D. radicum larvae, although the effects were relatively weak. Surprisingly, we found that adult D. radicum females show a strong preference to oviposit on plants infested with a leaf-chewing herbivore. Defence-related genes in primary roots of B. oleracea plants were affected by the leaf-chewing herbivores, but these changes were largely overridden upon local induction by D. radicum. Infestation by leaf herbivores makes plants more attractive for oviposition by D. radicum females, while decreasing larval performance. Therefore, our findings challenge the preference–performance hypothesis in situations where other herbivore species are present.

Generalist herbivore response to volatile chemical induction varies along a gradient in soil salinization

Elevated soil salinity directly modifies plant physiology and indirectly alters the biotic interactions that shape plant performance. However, it is unclear how soil salinization interacts with plant defenses to alter patterns of leaf consumption or herbivore survival, development, and performance. In this study, we carried out laboratory feeding trials and a common garden experiment to investigate how gradients in soil salinization interact with plant induction status (modified via exogenous application of methyl jasmonate [MeJA]) to influence feeding consumption and performance of the generalist herbivore Spodoptera exigua on tomato (Solanum lycoperscium) plants. Our results showed that S. exigua consumed less leaf tissue from tomatoes treated with ≥ 50 mM NaCl; at these higher salinity treatments, these herbivores were less likely to pupate and died more quickly. Treatment with MeJA only reduced leaf consumption in the 0 mM NaCl treatment. Our common garden study demonstrated that natural populations of leaf chewing herbivores were less likely to damage tomatoes treated with > 50 mM NaCl solutions. Treatment with MeJA in the common garden reduced damage from natural populations of herbivores, but only for salt treatments at the 50 mM NaCl concentration level and we did observe variation in herbivore damage between cohorts in common garden trials. These results suggest that both soil salinization and volatile jasmonate signals may generate complementary shifts in decreased plant quality for herbivores. Overall, our study concludes that soil salinization could be a potential driver in spatial patterns of variation in both herbivory and herbivore demography.

Enhanced volatile emissions and anti-herbivore functions mediated by the synergism between jasmonic acid and salicylic acid pathways in tea plants.

The interaction between jasmonic acid (JA) and salicylic acid (SA) pathways, which affects plant stress resistance, is mainly considered to be antagonistic. Using an established theoretical model, we investigated how tea plant (Camellia sinensis) volatiles induced by exogenous elicitors of the JA and SA pathways are affected by the sequence of elicitor application, elicitor identity, and the applied concentrations. We also examined the effects of the volatiles mediated by the JA–SA synergistic interaction on the behaviors of a tea leaf-chewing herbivore (Ectropis grisescens) and its parasitic wasp (Apanteles sp.). The JA and SA pathway interactions were almost always reciprocally synergistic when the two pathways were elicited at different times, except at high JA elicitor concentrations. However, the JA pathway antagonized the SA pathway when they were elicited simultaneously. The elicitor identity affected the degree of JA–SA interaction. The volatiles induced by the JA pathway in the JA–SA reciprocal synergism treatments included up to 11 additional compounds and the total amount of volatiles was up to 7.9-fold higher. Similarly, the amount of emitted volatiles induced by the SA pathway in the reciprocal synergism treatments increased by up to 4.2-fold. Compared with the volatiles induced by either pathway, the enriched volatiles induced by the JA–SA reciprocal synergism similarly repelled E. grisescens, but attracted Apanteles sp. more strongly. Thus, non-simultaneous activation is important for optimizing the JA–SA reciprocal synergism. This reciprocal synergism enables plants to induce multifarious responses, leading to increased biotic stress resistance.

Tissue-specific systemic responses of the wild tobacco Nicotiana attenuata against stem-boring herbivore attack

BackgroundPlants are able to optimize defense responses induced by various herbivores, which have different feeding strategies. Local and systemic responses within a plant after herbivory are essential to modulate herbivore-specific plant responses. For instance, leaf-chewing herbivores elicit jasmonic acid signaling, which result in the inductions of toxic chemicals in the attacked leaf (tissue-specific responses) and also in the other unattacked parts of the plant (systemic responses). Root herbivory induces toxic metabolites in the attacked root and alters the levels of transcripts and metabolites in the unattacked shoot. However, we have little knowledge of the local and systemic responses against stem-boring herbivores. In this study, we examined the systemic changes in metabolites in the wild tobacco Nicotiana attenuata, when the stem-boring herbivore Trichobaris mucorea attacks.ResultsTo investigate the systemic responses of T. mucorea attacks, we measured the levels of jasmonic acid (JA), JA-dependent secondary metabolites, soluble sugars, and free amino acids in 7 distinct tissues of N. attenuata: leaf lamina with epidermis (LLE), leaf midrib (LM), stem epidermis (SE), stem pith (SP), stem vascular bundle (SV), root cortex with epidermis (RCE), and root vascular bundle (RV). The levels of JA were increased in all root tissues and in LM by T. mucorea attacks. The levels of chlorogenic acids (CGAs) and nicotine were increased in all stem tissues by T. mucorea. However, CGA was systematically induced in LM, and nicotine was systematically induced in LM and RCE. We further tested the resource allocation by measuring soluble sugars and free amino acids in plant tissues. T. mucorea attacks increased the level of free amino acids in all tissues except in LLE. The levels of soluble sugars were significantly decreased in SE and SP, but increased in RV.ConclusionsThe results reveal that plants have local- and systemic-specific responses in response to attack from a stem-boring herbivore. Interestingly, the level of induced secondary metabolites was not consistent with the systemic inductions of JA. Spatiotemporal resolution of plant defense responses against stem herbivory will be required to understand how a plant copes with attack from herbivores from different feeding guilds.

Pith-specific lignification in Nicotiana attenuata as a defense against a stem-boring herbivore.

Plants have developed tissue-specific defense strategies in response to various herbivores with different feeding habits. Although defense responses to leaf-chewing insects have been well studied, little is known about stem-specific responses, particularly in the pith, to stem-boring herbivores. To understand the stem-specific defense, we first conducted a comparative transcriptomic analysis of the wild tobacco Nicotiana attenuata before and after attack by the leaf-chewing herbivore Manduca sexta and the stem borer Trichobaris mucorea. When the stem-boring herbivore attacked, lignin-associated genes were upregulated specifically in the inner parenchymal cells of the stem, the pith; lignin also accumulated highly in the attacked pith. Silencing the lignin biosynthetic gene cinnamyl alcohol dehydrogenase enhanced the performance of the stem-boring herbivore but had no effect on the growth of the leaf-chewing herbivore. Two-dimensional nuclear magnetic resonance results revealed that lignified pith contains feruloyltyramine as an unusual lignin component in the cell wall, as a response against stem-boring herbivore attack. Pith-specific lignification induced by the stem-boring herbivore was modulated by both jasmonate and ethylene signaling. These results suggest that lignin provides a stem-specific inducible barrier, protecting plants against stem-boring insects.

Invertebrate functional traits and terrestrial nutrient cycling: Insights from a global meta-analysis.

Functional traits are useful for characterizing variation in community and ecosystem dynamics. Most advances in trait-based ecology to date centre on plant functional traits, although there is an increasing recognition that animal traits are also key contributors to processes operating at the community or ecosystem scale. Terrestrial invertebrates are incredibly diverse and ubiquitous animals with important roles in nutrient cycling. Despite their widespread influence on ecosystem processes, we currently lack a synthetic understanding of how invertebrate functional traits affect terrestrial nutrient cycling. We present a meta-analysis of 511 paired observations from 122 papers that examined how invertebrate functional traits affected litter decomposition rates, nitrogen pools and litter C:N ratios. Based on the available data, we specifically assessed the effects of feeding mode (bioturbation, detritus shredding, detritus grazing, leaf chewing, leaf piercing, ambush predators, active hunting predators) and body size (macro- and micro-invertebrates) on nutrient cycling. The effects of invertebrates on terrestrial nutrient cycling varied according to functional trait. The inclusion of both macro- (≥2mm) and micro-invertebrates (<2mm) increased litter decomposition by 20% and 19%, respectively. All detritivorous feeding modes enhanced litter decomposition rates, with bioturbators, detritus shredders and detritus grazers increasing decomposition by 28%, 22% and 15%, respectively. Neither herbivore feeding mode (e.g. leaf chewers and leaf piercers) nor predator hunting mode (ambush and active hunting) affected decomposition. We also revealed that bioturbators and detritus grazers increased soil nitrogen availability by 99% and 70%, respectively, and that leaf-chewing herbivores had a weak effect on litterfall stoichiometry via reducing C:N ratios by 11%. Although functional traits might be useful predictors of ecosystem processes, our findings suggest context-dependent effects of invertebrate traits on terrestrial nutrient cycling. Detritivore functional traits (i.e. bioturbators, detritus shredders and detritus grazers) are more consistent with increased rates of nutrient cycling, whereas our currently characterized predator and herbivore traits are less predictive. Future research is needed to identify, standardize and deliberately study the impacts of invertebrate functional traits on nutrient cycling in hopes of revealing the key functional traits governing ecosystem functioning worldwide.

Herbivore-herbivore interactions complicate links between soil fertility and pest resistance

Soil fertility is tightly linked with herbivore pressure because it affects the nutritional status of host plants as well as the production of anti-herbivore defenses. This in turn can influence whether herbivores in different feeding guilds render plants more or less susceptible to one another. Thus, growers’ fertility management choices may impact herbivores through a variety of indirect channels. We examined relationships between soil fertility and interactions between phloem-feeding and leaf-chewing herbivores on broccoli (Brassica oleracea) plants in the greenhouse, taking advantage of natural variation in nitrogen (N) and phosphorus (P) in soils from 20 working organic vegetable farms. Next, we experimentally fertilized soil in a field trial with N and/or P to examine the consequences of these nutrients for growth of and interactions between specialist and generalist herbivores. Soils on our cooperating farms varied widely in P and N concentrations, with 40% exceeding recommended pre-plant N concentrations and 90% exceeding P recommendations. In single-herbivore infestations, augmenting N in the soil increased caterpillar (Pieris rapae) growth, augmented N and P additively enhanced generalist green peach aphid (Myzus persicae) colonization, and augmented P (but not N) increased specialist cabbage aphid (Brevicoryne brassicae) growth. In dual-guild herbivore infestations, caterpillars facilitated specialist cabbage aphid growth in the absence of fertilizer, but this pattern disappeared under augmented N, and reversed under augmented P. We found that a complex web of indirect effects linked soil fertility to herbivore performance, depending on the identity of the nutrients being altered, the ecological roles of responding herbivore species (i.e., specialist versus generalist), and indirect interactions between chewing and sucking herbivores. More generally, we highlight that successful use of fertility management to improve pest resistance requires careful consideration of herbivore feeding niches and herbivore-herbivore interactions.

Volatiles of pathogenic and non-pathogenic soil-borne fungi affect plant development and resistance to insects

Plants are ubiquitously exposed to a wide diversity of (micro)organisms, including mutualists and antagonists. Prior to direct contact, plants can perceive microbial organic and inorganic volatile compounds (hereafter: volatiles) from a distance that, in turn, may affect plant development and resistance. To date, however, the specificity of plant responses to volatiles emitted by pathogenic and non-pathogenic fungi and the ecological consequences of such responses remain largely elusive. We investigated whether Arabidopsis thaliana plants can differentiate between volatiles of pathogenic and non-pathogenic soil-borne fungi. We profiled volatile organic compounds (VOCs) and measured CO2 emission of 11 fungi. We assessed the main effects of fungal volatiles on plant development and insect resistance. Despite distinct differences in VOC profiles between the pathogenic and non-pathogenic fungi, plants did not discriminate, based on plant phenotypic responses, between pathogenic and non-pathogenic fungi. Overall, plant growth was promoted and flowering was accelerated upon exposure to fungal volatiles, irrespectively of fungal CO2 emission levels. In addition, plants became significantly more susceptible to a generalist insect leaf-chewing herbivore upon exposure to the volatiles of some of the fungi, demonstrating that a prior fungal volatile exposure can negatively affect plant resistance. These data indicate that plant development and resistance can be modulated in response to exposure to fungal volatiles.

Plant trichomes and a single gene GLABRA1 contribute to insect community composition on field-grown Arabidopsis thaliana

BackgroundGenetic variation in plants alters insect abundance and community structure in the field; however, little is known about the importance of a single gene among diverse plant genotypes. In this context, Arabidopsis trichomes provide an excellent system to discern the roles of natural variation and a key gene, GLABRA1, in shaping insect communities. In this study, we transplanted two independent glabrous mutants (gl1–1 and gl1–2) and 17 natural accessions of Arabidopsis thaliana to two localities in Switzerland and Japan.ResultsFifteen insect species inhabited the plant accessions, with the insect community composition significantly attributed to variations among plant accessions. The total abundance of leaf-chewing herbivores was negatively correlated with trichome density at both field sites, while glucosinolates had variable effects on leaf chewers between the sites. Interestingly, there was a parallel tendency for the abundance of leaf chewers to be higher on gl1–1 and gl1–2 than on their different parental accessions, Ler-1 and Col-0, respectively. Furthermore, the loss of function in the GLABRA1 gene significantly decreased the resistance of plants to the two predominant chewers; flea beetles and turnip sawflies.ConclusionsOverall, our results indicate that insect community composition significantly varies among A. thaliana accessions across two distant field sites, with GLABRA1 playing a key role in altering the abundance of leaf-chewing herbivores. Given that such a trichome variation is widely observed in Brassicaceae plants, the present study exemplifies the community-wide effect of a single plant gene on crucifer-feeding insects in the field.

Keystone mutualism strengthens top-down effects by recruiting large-bodied ants.

Determining the impacts of mutualistic interactions and predator diversity on food webs are two important goals in community ecology. In this study, we examined how predator community variation mediates the strength of top-down effects in the presence and absence of mutualistic interactions. We examined the impacts of predatory ant species that simultaneously prey on leaf-chewing herbivores (Lepidoptera) and engage in food-for-protection mutualisms with sap-feeding herbivores (Hemiptera) in the lower canopy of Connecticut forests. In this 2-year study, we examined three hypothetical mechanisms by which mutualisms can alter the top-down effects of ants: (1) sap feeders increase ant abundance, thus strengthening predatory effects; (2) sap feeders increase the relative abundance of a species that has stronger predatory effects; and (3) changes to predator diversity (species richness) are caused by sap feeders mediating top-down effects of the ant community. Experiments revealed that host plants occupied by sap feeders favored large-bodied ant species in the genus Camponotus, but there were no changes to community-wide ant abundance or ant species richness. Fitting predictions of predation strength based on the functional trait of body size, large-bodied Camponotus suppressed caterpillars and reduced leaf herbivory. This work shows that the ant-hemipteran mutualism, which has been characterized as a keystone interaction, can generate strong top-down effects on leaf-chewing herbivores and herbivory via increasing the relative abundance of species with functional traits relevant to predation, such as body size. Therefore, the emergence of specific ants as keystone predators in a community can be contingent upon their mutualism with sap-feeding Hemiptera.

Does mycorrhizal status alter herbivore-induced changes in whole-plant resource partitioning?

Both mycorrhizae and herbivore damage cause rapid changes in source-sink dynamics within a plant. Mycorrhizae create long-term sinks for carbon within the roots while damage by leaf-chewing herbivores causes temporary whole-plant shifts in carbon and nitrogen allocation. Thus, induced responses to herbivory might depend on the presence or absence of mycorrhizae. We examined the effects of mycorrhizal presence on induced resource partitioning in tomato (Solanum lycopersicon) in response to cues from a specialist herbivore Manduca sexta. Differences in plant size, growth and in the concentrations of carbon-based (soluble sugars and starch) and nitrogen-based (protein and total nitrogen) resources in three tissue types (apex, stem and roots) were quantified. Both mycorrhizae and simulated herbivory altered the concentrations of carbon- and nitrogen-based resources. Mycorrhizae promoted plant growth, altered sugar and starch levels. Simulated herbivory resulted in lower concentrations of most resources (sugar, starch and protein) in the rapidly growing apex tissue, while causing an increase in stem protein. There was only one interactive effect; the effects of simulated herbivory were much stronger on the sugar concentration in the apex of non-mycorrhizal plants. This clearly demonstrates that both mycorrhizal colonization and herbivore cues cause shifts in carbon- and nitrogen-based resources and further shows there is little interference by mycorrhizae on the direction and magnitude of plant responses to herbivory. Overall, our results suggest that herbivore cues, regardless of mycorrhizal status, reduce allocation to the growing apex while inducing protein storage in the stem, a possible mechanism that could increase the tolerance of plants to damage.

Tree species richness attenuates the positive relationship between mutualistic ant-hemipteran interactions and leaf chewer herbivory.

Interactions across trophic levels influence plant diversity effects on ecosystem functions, but the complexity of these interactions remains poorly explored. For example, the interplay between different interactions (e.g. mutualism, predation) might be an important moderator of biodiversity-ecosystem function relationships. We tested for relationships between trophobioses (facultative ant-hemipteran mutualism) and leaf chewer herbivory in a subtropical forest biodiversity experiment. We analysed trophobiosis and herbivory data of more than 10 000 trees along a tree species richness gradient. Against expectations, chewing damage was higher on trees with trophobioses. However, the net positive relationship between trophobioses and overall herbivory depended on tree species richness, being most pronounced at low richness. Our results point to indirect, positive effects of ant-tended sap suckers on leaf chewers, potentially by altering plant defences. Direct antagonistic relationships of trophobiotic ants and leaf-chewing herbivores-frequently reported to drive community-wide effects of trophobioses in other ecosystems-seemed less relevant. However, antagonistic interactions likely contributed to the attenuating effect of tree species richness, because trophobiotic ant and herbivore communities changed from monocultures to species-rich mixtures. Our findings, therefore, suggest that biodiversity loss might lead to complex changes in higher trophic level effects on ecosystem functions, mediated by both trophic and non-trophic interactions.

Antagonism between two root-associated beneficial Pseudomonas strains does not affect plant growth promotion and induced resistance against a leaf-chewing herbivore.

Plant growth-promoting microbes residing on the roots may cooperate or compete, thereby affecting their collective benefit to the host plant. Pseudomonas simiae WCS417r (formerly known as P. fluorescens WCS417r) and Pseudomonas fluorescens SS101 are well known for their ability to induce systemic resistance in Arabidopsis. Here, we evaluate how these species interact on the roots of Arabidopsis thaliana Col-0 and how their co-inoculation affects plant defense to the leaf-chewing herbivore Mamestra brassicae and plant growth promotion. WCS417r and SS101, applied individually to root tips or at two different positions along the roots, established similar population densities on Arabidopsis roots. When co-inoculated at the same position on the roots, however, WCS417r established significantly higher population densities than SS101. Both upon single inoculation and co-inoculation, the two pseudomonads induced the same level of induced systemic resistance against the caterpillar M. brassicae and the same increase in plant biomass. These results suggest that combined inoculation of both Pseudomonas strains does not significantly modify the plant's defensive capacity compared to individual inoculation, resulting in a similar effect on performance of the generalist herbivore M. brassicae.

Jasmonic Acid and Ethylene Signaling Pathways Regulate Glucosinolate Levels in Plants During Rhizobacteria-Induced Systemic Resistance Against a Leaf-Chewing Herbivore.

Beneficial soil microbes can promote plant growth and induce systemic resistance (ISR) in aboveground tissues against pathogens and herbivorous insects. Despite the increasing interest in microbial-ISR against herbivores, the underlying molecular and chemical mechanisms of this phenomenon remain elusive. Using Arabidopsis thaliana and the rhizobacterium Pseudomonas simiae WCS417r (formerly known as P. fluorescens WCS417r), we here evaluate the role of the JA-regulated MYC2-branch and the JA/ET-regulated ORA59-branch in modulating rhizobacteria-ISR to Mamestra brassicae by combining gene transcriptional, phytochemical, and herbivore performance assays. Our data show a consistent negative effect of rhizobacteria-mediated ISR on the performance of M. brassicae. Functional JA- and ET-signaling pathways are required for this effect, as shown by investigating the knock-out mutants dde2-2 and ein2-1. Additionally, whereas herbivory mainly induces the MYC2-branch, rhizobacterial colonization alone or in combination with herbivore infestation induces the ORA59-branch of the JA signaling pathway. Rhizobacterial colonization enhances the synthesis of camalexin and aliphatic glucosinolates (GLS) compared to the control, while it suppresses the herbivore-induced levels of indole GLS. These changes are associated with modulation of the JA-/ET-signaling pathways. Our data show that the colonization of plant roots by rhizobacteria modulates plant-insect interactions by prioritizing the JA/ET-regulated ORA59-branch over the JA-regulated MYC2-branch. This study elucidates how microbial plant symbionts can modulate the plant immune system to mount an effective defense response against herbivorous plant attackers.Electronic supplementary materialThe online version of this article (doi:10.1007/s10886-016-0787-7) contains supplementary material, which is available to authorized users.