Chewing Herbivores Research Articles

Combining optimal defense theory and the evolutionary dilemma model to refine predictions regarding plant invasion

Optimal defense theory posits that plants with limited resources deploy chemical defenses based on the fitness value of different tissues and their probability of attack. However, what constitutes optimal defense depends on the identity of the herbivores involved in the interaction. Generalists, which are not tightly coevolved with their many host plants, are typically deterred by chemical defenses, while coevolved specialists are often attracted to these same chemicals. This imposes an "evolutionary dilemma" in which generalists and specialists exert opposing selection on plant investment in defense, thereby stabilizing defenses at intermediate levels. We used the natural shift in herbivore community composition that typifies many plant invasions to test a novel, combined prediction of optimal defense theory and the evolutionary dilemma model: that the within-plant distribution of defenses reflects both the value of different tissues (i.e., young vs. old leaves) and the relative importance of specialist and generalist herbivores in the community. Using populations of Verbascum thapsus exposed to ambient herbivory in its native range (where specialist and generalist chewing herbivores are prevalent) and its introduced range (where only generalist chewing herbivores are prevalent), we illustrate significant differences in the way iridoid glycosides are distributed among young and old leaves. Importantly, high-quality young leaves are 6.5x more highly defended than old leaves in the introduced range, but only 2x more highly defended in the native range. Additionally, defense levels are tracked by patterns of chewing damage, with damage restricted mostly to low-quality old leaves in the introduced range, but not the native range. Given that whole-plant investment in defense does not differ between ranges, introduced mullein may achieve increased fitness simply by optimizing its within-plant distribution of defense in the absence of certain specialist herbivores.

OsNPR1 negatively regulates herbivore‐induced JA and ethylene signaling and plant resistance to a chewing herbivore in rice

NPR1 (a non-expressor of pathogenesis-related genes1) has been reported to play an important role in plant defense by regulating signaling pathways. However, little to nothing is known about its function in herbivore-induced defense in monocot plants. Here, using suppressive substrate hybridization, we identified a NPR1 gene from rice, OsNPR1, and found that its expression levels were upregulated in response to infestation by the rice striped stem borer (SSB) Chilo suppressalis and rice leaf folder (LF) Cnaphalocrocis medinalis, and to mechanical wounding and treatment with jasmonic acid (JA) and salicylic acid (SA). Moreover, mechanical wounding induced the expression of OsNPR1 quickly, whereas herbivore infestation induced the gene more slowly. The antisense expression of OsNPR1 (as-npr1), which reduced the expression of the gene by 50%, increased elicited levels of JA and ethylene (ET) as well as of expression of a lipoxygenase gene OsHI-LOX and an ACC synthase gene OsACS2. The enhanced JA and ET signaling in as-npr1 plants increased the levels of herbivore-induced trypsin proteinase inhibitors (TrypPIs) and volatiles, and reduced the performance of SSB. Our results suggest that OsNPR1 is an early responding gene in herbivore-induced defense and that plants can use it to activate a specific and appropriate defense response against invaders by modulating signaling pathways.

Tradeoffs between foliar silicon and carbon‐based defences: evidence from vegetation communities of contrasting soil types

Silica is ubiquitous in plants and can constitute up to 10% of plant dry mass, varying with phylogeny and soil silicon availability. Plant silicon is an important alleviator of abiotic (salinity, heavy metal, drought) and biotic (herbivore and fungal pathogen) stress. As well as playing an important role in reducing the impact of abiotic stresses, silicon may be an alternative to carbon‐based and other chemical defences. Knowledge of silicon function is predominantly derived from agricultural species and model systems. We investigated the abundance and role of plant silicon at a community level by comparing leaf silicon concentration with defence chemicals, carbon compound concentrations and invertebrate assemblages in vegetation communities from two different soil types with contrasting levels of plant available silicon. We found that the concentrations of silicon in the leaves did not reflect the silicon availability in the soil at a community level. The leaf silica concentration range in the vegetation communities was comparable to other diverse communities reported in the literature, suggesting that the species rather than the environment determine leaf silica concentration. Across sites, leaf silica concentration was significantly negatively correlated with concentrations of carbon, total phenols and weakly with tannins but not with other measured defence compounds. Leaf silica concentration was also negatively correlated with Coleoptera abundance, but not the abundance of any other invertebrate groups measured. Our results suggest that tradeoffs exist between phenolic‐ and tannin‐based defences and provide evidence that leaf silicification may be a more effective defence against some chewing herbivore groups than others.

Coincidental intraguild predation by caterpillars on spider mites.

Intraguild predation (IGP) is defined as the killing and eating of prey species by a predator that also can utilize the resources of the prey. It is mainly reported among carnivores that share common herbivorous prey. However, a large chewing herbivore could prey upon sedentary and/or micro herbivores in addition to utilizing a host plant. To investigate such coincidental IGP, we observed the behavioral responses of the polyphagous mite Tetranychus kanzawai Kishida (Acari: Tetranychidae) when its host plant Cayratia japonica (Thunb.) Gagnep. (Vitaceae) was attacked by hornworms, Theretra japonica Boisduval (Sphingidae) and T. oldenlandiae Fabricius (Sphingidae). We also examined an interaction between the oligophagous mite Panonychus citri McGregor (Acari: Tetranychidae) and caterpillars of the swallowtail Papilio xuthus L. (Papilionidae) that share citrus plants as their main food source. Although all T. kanzawai and some active stage P. citri tried to escape from the coincidental IGP, some were consumed together with eggs, quiescent mites, and host plant leaves, suggesting that coincidental IGP occurs on spider mites in the wild. Moreover, neither hornworms nor swallowtail caterpillars distinguished between spider mite-infested and uninfested leaves, suggesting that the mite-infested leaves do not discourage caterpillar feeding. The reasons that the mites have no effective defense against coincidental IGP other than escaping are discussed.

Emergent Impacts of Ant and Spider Interactions: Herbivory Reduction in a Tropical Savanna Tree

AbstractMultiple predators often have effects on their common prey populations that cannot be predicted by summing the effects of each predator at a time. When predators forage on the same vegetation substrate, intraguild interactions might cause emergent outcomes for the plants on which the predators co‐occur. We experimentally evaluated the effects of spiders and ants on herbivory and reproduction in the extrafloral nectary‐bearing tree Qualea multiflora (Vochysiaceae). Plants were divided in four experimental groups, depending on the presence or absence of ants and spiders. We compared the effects of each treatment on richness and abundance of chewing and sucking herbivores and on herbivory (leaf area loss). We also evaluated the impact of predators on the production of buds, fruits and seeds, and weight of the fruits. The presence of ants reduced the abundance and richness of spiders, but spiders did not affect the abundance and richness of ants. Only the removal of ants resulted in a significant increase in the abundance of herbivores and herbivore richness. Herbivory, however, was also affected by spiders. In addition, we found a significant interaction effect of ants and spiders on herbivory, indicating an emergent multiple predator effect. Neither ants nor spiders had an impact on the number of buds produced, number of fruits per bud, and seeds per fruits or fruit weight. This study highlights the importance of evaluating the effect of the predator fauna as a whole and not only one specific group on herbivory.

Bottom‐up multitrophic effects in resprouting plants

Severe damage often provokes compensatory resprouting of plants, which commonly modify plant morphological and phenological traits. Rapid plant growth often results in poorly defended nutrient-rich foliage, which is more susceptible to foliar-chewing herbivores. It is less known how other guilds of arthropods are affected by plant regrowth. We tested the hypotheses that clipping-induced resprouting and nutrient availability, separately and in combination, would (1) influence plant traits, (2) benefit chewing herbivores, sap-suckers, gallers, and pre-dispersal seed predators, and (3) cascade up to the third trophic level by positively affecting herbivores. Resprouted plants were morphologically and phenologically different from undamaged plants; as a result, seed predation, infestation rate, richness, and diversity of seed predators increased, and species composition was altered. Leaf consumption by chewing herbivores was four times higher on resprouted plants. The number of galls decreased, whereas the abundance of sap-sucking and leaf-chewing insects was not affected. The incidence of predators and parasitoids was also higher on resprouted plants and on plants with nutrients added, but the increase was less pronounced compared to the herbivores they feed on. Thus, the effects of resprouting, contingent on nutrient availability, can propagate simultaneously through two independent tri-trophic level pathways.

Do Leaf Cutting Ants Cut Undetected? Testing the Effect of Ant-Induced Plant Defences on Foraging Decisions in Atta colombica

Leaf-cutting ants (LCAs) are polyphagous, yet highly selective herbivores. The factors that govern their selection of food plants, however, remain poorly understood. We hypothesized that the induction of anti-herbivore defences by attacked food plants, which are toxic to either ants or their mutualistic fungus, should significantly affect the ants' foraging behaviour. To test this “induced defence hypothesis,” we used lima bean (Phaseolus lunatus), a plant that emits many volatile organic compounds (VOCs) upon herbivore attack with known anti-fungal or ant-repellent effects. Our results provide three important insights into the foraging ecology of LCAs. First, leaf-cutting by Atta ants can induce plant defences: Lima bean plants that were repeatedly exposed to foraging workers of Atta colombica over a period of three days emitted significantly more VOCs than undamaged control plants. Second, the level to which a plant has induced its anti-herbivore defences can affect the LCAs' foraging behaviour: In dual choice bioassays, foragers discriminated control plants from plants that have been damaged mechanically or by LCAs 24 h ago. In contrast, strong induction levels of plants after treatment with the plant hormone jasmonic acid or three days of LCA feeding strongly repelled LCA foragers relative to undamaged control plants. Third, the LCA-specific mode of damaging leaves allows them to remove larger quantities of leaf material before being recognized by the plant: While leaf loss of approximately 15% due to a chewing herbivore (coccinelid beetle) was sufficient to significantly increase VOC emission levels after 24 h, the removal of even 20% of a plant's leaf area within 20 min by LCAs did not affect its VOC emission rate after 24 h. Taken together, our results support the “induced defence hypothesis” and provide first empirical evidence that the foraging behaviour of LCAs is affected by the induction of plant defence responses.

Tri-trophic level interactions affect host plant development and abundance of insect herbivores

Understanding the interactions among plants, hemipterans, and ants has provided numerous insights into a range of ecological and evolutionary processes. In these systems, however, studies concerning the isolated direct and indirect effects of aphid colonies on host plant and other herbivores remain rare at best. The aphid Uroleucon erigeronensis forms dense colonies on the apical shoots of the host plant Baccharis dracunculilfolia (Asteraceae). The honeydew produced by these aphids attracts several species of ants that might interfere with other herbivores. Four hypotheses were tested in this system: (1) ants tending aphids reduce the abundance of other herbivores; (2) the effects of ants and aphids upon herbivores differ between chewing and fluid-sucking herbivores; (3) aphids alone reduce the abundance of other herbivores; and (4), the aphid presence negatively affects B. dracunculifolia shoot growth. The hypotheses were evaluated with ant and aphid exclusion experiments, on isolated plant shoots, along six consecutive months. We adjusted linear mixed-effects models for longitudinal data (repeated measures), with nested spatial random effect. The results showed that: (1) herbivore abundance was lower on shoots with aphids than on shoots without aphids, and even lower on shoots with aphids and ants; (2) both chewing and fluid-sucking insects responded similarly to the treatment, and (3) aphid presence affected negatively B. dracunculifolia shoot growth. Thus, since aphids alone changed plant growth and the abundance of insect herbivores, we suggest that the ant–aphid association is important to the organization of the system B. dracunculifolia-herbivorous insects.

Belowground rhizobia positively affect abundances of aboveground sap feeding and leaf chewing herbivores

Belowground rhizobia positively affect abundances of aboveground sap feeding and leaf chewing herbivores.

Elevated CO2 influences nematode-induced defense responses of tomato genotypes differing in the JA pathway.

Rising atmospheric CO2 concentrations can affect the induced defense of plants against chewing herbivores but little is known about whether elevated CO2 can change the induced defense of plants against parasitic nematodes. This study examined the interactions between the root-knot nematode Meloidogyne incognita and three isogenic tomato (Lycopersicon esculentum) genotypes grown under ambient (390 ppm) and elevated (750 ppm) CO2 in growth chambers. In a previous study with open-top chambers in the field, we reported that elevated CO2 increased the number of nematode-induced root galls in a JA-defense-dominated genotype but not in a wild-type or JA-defense-recessive genotype. In the current study, we tested the hypothesis that elevated CO2 will favor the salicylic acid (SA)-pathway defense but repress the jasmonic acid (JA)-pathway defense of plants against plant-parasitic nematodes. Our data showed that elevated CO2 reduced the JA-pathway defense against M. incognita in the wild-type and in a genotype in which defense is dominated by the JA pathway (a JA-defense-dominated genotype) but up-regulated the SA-pathway defense in the wild type and in a JA-defense-recessive genotype (jasmonate-deficient mutant). Our results suggest that, in terms of defense genes, secondary metabolites, and volatile organic compounds, induced defense of nematode-infected plants could be affected by elevated CO2, and that CO2-induced changes of plant resistance may lead to genotype-specific responses of plants to nematodes under elevated CO2. The changes in resistance against nematodes, however, were small relative to those reported for chewing insects.

The effect of nitrogen additions on bracken fern and its insect herbivores at sites with high and low atmospheric pollution

The impact of atmospheric pollution, including nitrogen deposition, on bracken fern herbivores has never been studied. Bracken fern is globally distributed and has a high potential to accumulate nitrogen in plant tissue. We examined the response of bracken fern and its herbivores to N fertilization at a high and low pollution site in forests downwind of Los Angeles, California. Foliage from the high pollution site had higher total N and nitrate than the low pollution site. Bracken fern biomass, foliar N and herbivore abundance were all affected by fertilization treatments. Biomass and herbivore responses were greatest during a year of high precipitation. N additions at the low pollution site were primarily associated with decreased fern biomass, and with transient impacts on herbivore abundance. N additions significantly affected bracken fern and its herbivores at the high pollution site where foliar N and nitrate decreased in response to N addition treatments, while biomass and herbivore abundance increased. High atmospheric deposition and fertilization were both associated with increased herbivore richness. Herbivore abundance was most impacted by fertilization during the early expansion of fern fronds. The most abundant chewing herbivore, a sawfly, was positively associated with plant nitrogen at the low pollution site, but negatively associated with plant nitrogen at the high pollution site, where concentrations of both total N and nitrate were high. While overall growth and herbivore impacts in this xeric location were limited, the variable response we observed associated with rainfall, may indicate impacts could be larger in more mesic environments.

The role of jasmonic acid and ethylene crosstalk in direct defense of Nicotiana attenuata plants against chewing herbivores

We examined performance of herbivores on plants lacking either jasmonate (JA, asLOX3) or ethylene (ET, mETR1) signaling, or both (mETR1asLOX3). Plant defenses against Manduca sexta caterpillars were strongly impaired in JA-deficient asLOX3 plants; however, making asLOX3 plants ethylene insensitive did not further increase the performance of the larvae on a mETR1asLOX3 genetic cross. This result demonstrates the dominant role of JA over ET in the regulation of plant defenses against herbivores. However, ET-insensitivity combined with otherwise normal levels of JA in mETR1 plants promoted faster caterpillar growth, which correlated with reduced accumulation of the alkaloidal direct defense nicotine in mETR1 compared to WT plants. Our data points to an important accessory function of ET in the activation of JA-regulated plant defenses against herbivores at the level of alkaloid biosynthesis in the roots and/or accumulation in the leaves.

Why do many galls have conspicuous colours? An alternative hypothesis revisited

It has been proposed that the colour of many plant galls evolved as an aposematic signal to protect the contained gall-maker from attack by chewing herbivores. But the evidence would suggest the more likely hypothesis is that the colour is caused by the galler inducing the gall to senesce early, thus releasing nutrients from the dying tissues of the gall to the benefit of the gall-maker. External agents, like chewing herbivores or natural enemies of the gall-maker, may subsequently learn to use these colours as signals.

Insect eggs suppress plant defence against chewing herbivores

Plants activate direct and indirect defences in response to insect egg deposition. However, whether eggs can manipulate plant defence is unknown. In Arabidopsis thaliana, oviposition by the butterfly Pieris brassicae triggers cellular and molecular changes that are similar to the changes caused by biotrophic pathogens. In the present study, we found that the plant defence signal salicylic acid (SA) accumulates at the site of oviposition. This is unexpected, as the SA pathway controls defence against fungal and bacterial pathogens and negatively interacts with the jasmonic acid (JA) pathway, which is crucial for the defence against herbivores. Application of P. brassicae or Spodoptera littoralis egg extract onto leaves reduced the induction of insect-responsive genes after challenge with caterpillars, suggesting that egg-derived elicitors suppress plant defence. Consequently, larval growth of the generalist herbivore S. littoralis, but not of the specialist P. brassicae, was significantly higher on plants treated with egg extract than on control plants. In contrast, suppression of gene induction and enhanced S. littoralis performance were not seen in the SA-deficient mutant sid2-1, indicating that it is SA that mediates this phenomenon. These data reveal an intriguing facet of the cross-talk between SA and JA signalling pathways, and suggest that insects have evolved a way to suppress the induction of defence genes by laying eggs that release elicitors. We show here that egg-induced SA accumulation negatively interferes with the JA pathway, and provides an advantage for generalist herbivores.

Gross vs. net income: How plant toughness affects performance of an insect herbivore

Leaf biomechanical properties are thought to impose a significant obstacle to herbivores and as such influence patterns of herbivory more than leaf chemistry. However, evidence for the role of structural traits in influencing herbivore food choice and performance has come from correlative studies, whereas the underlying mechanisms have been given little attention. By manipulating the biomechanical properties of a host grass species through a combination of lyophilization and milling, and providing water separately, we were able to compare behavioral, physiological, and developmental responses of the Australian plague locust, Chortoicetes terminifera, to the biomechanical properties of plant food (exemplified by toughness) independently of the food's macronutrient content and the insect's demand for water. Increasing leaf toughness was associated with reduced rates of locust growth and prolonged development, with potential ecological consequences. Poorer performance on the tougher foods was primarily a consequence of a reduced rate of nutrient supply, which occurred as a result of (1) smaller meals being eaten more slowly, (2) slowed gut passage rates, which limited how quickly the next meal could be taken, and (3) reduced efficiency of assimilation of nutrients from food in the gut. In addition, there were deleterious changes in the ratio of protein to carbohydrate assimilated from the gut. Prolonged development time was associated with increased total nutrient demands throughout the extended developmental period. Because these demands could not be met by increased consumption, there was a decreased efficiency of conversion of assimilated nutrients to growth. By disentangling the effects of biomechanical properties from macronutrient and water content we have shown that leaf biomechanical traits can influence chewing herbivores independently of leaf chemical traits.

Silencing OsHI‐LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder

The jasmonic acid (JA) pathway plays a central role in plant defense responses against insects. Some phloem-feeding insects also induce the salicylic acid (SA) pathway, thereby suppressing the plant's JA response. These phenomena have been well studied in dicotyledonous plants, but little is known about them in monocotyledons. We cloned a chloroplast-localized type 2 13-lipoxygenase gene of rice, OsHI-LOX, whose transcripts were up-regulated in response to feeding by the rice striped stem borer (SSB) Chilo suppressalis and the rice brown planthopper (BPH) Niaparvata lugens, as well as by mechanical wounding and treatment with JA. Antisense expression of OsHI-LOX (as-lox) reduced SSB- or BPH-induced JA and trypsin protease inhibitor (TrypPI) levels, improved the larval performance of SBB as well as that of the rice leaf folder (LF) Cnaphalocrocis medinalis, and increased the damage caused by SSB and LF larvae. In contrast, BPH, a phloem-feeding herbivore, showed a preference for settling and ovipositing on WT plants, on which they consumed more and survived better than on as-lox plants. The enhanced resistance of as-lox plants to BPH infestation correlated with higher levels of BPH-induced H(2)O(2) and SA, as well as with increased hypersensitive response-like cell death. These results imply that OsHI-LOX is involved in herbivore-induced JA biosynthesis, and plays contrasting roles in controlling rice resistance to chewing and phloem-feeding herbivores. The observation that suppression of JA activity results in increased resistance to an insect indicates that revision of the generalized plant defense models in monocotyledons is required, and may help develop novel strategies to protect rice against insect pests.

Are Laguncularia racemosa galled leaves less attractive to chewing herbivores

Evolutionary interactions between herbivores and plants have resulted in an impressive variety of adaptations, and herbivory pressure has led to the evolution of chemical, mechanical and phenological defense in plants. Coastal mangrove forests provide a very tractable system in which to study the dynamics of herbivory. The objective of this work was to evaluate if galled leaves of the mangrove tree Laguncularia racemosa (L.) Gaerten (Combretaceae) are less consumed by chewing insects. Monthly excursions were carried to the Maracaipe Mangrove in Pernambuco, to collect adult leaves from 60 plants of L. racemosa: 240 ungalled leaves consumed by chewing insects (CL), 240 galled leaves consumed by chewing insects (CLG) and 240 galled leaves not consumed by chewing herbivores (LG). Other leaves were collected in August, in order to quantify total phenolic concentration: 40 intact leaves of individuals with low rate of infestation by galls (LL) and 40 of individuals with high infestation (HL) were thus collected. CLG displayed a lesser loss of foliar area to chewing herbivores. The results show a signifi cant amount of phenols in HL (35.63 mg) and LG (32.7 mg). This high phenol concentration is probably repelling chewing phytophagous. It is known that herbivores tend to avoid leaves that were previously predated by another herbivore. Possibly galls are infl uencing the feeding performance of the chewing insects.

Are Laguncularia racemosa galled leaves less attractive to chewing herbivores?

Are Laguncularia racemosa galled leaves less attractive to chewing herbivores?

Symbiotic soil microorganisms as players in aboveground plant-herbivore interactions - the role of rhizobia

Rhizobia play a key role for performance of leguminous plants and ecosystem productivity. However, no studies to date have investigated the importance of the rhizobial symbiosis for legume–herbivore interactions. The additional nitrogen provided by the rhizobia improves the nutritional quality of plants, but may also be used for the synthesis of defence compounds. We performed greenhouse experiments with nodulating and non-nodulating, as well as cyanogenic and acyanogenic strains of Trifolium repens to study the effects of rhizobia Rhizobium leguminosarum on plant growth and the performance of the chewing herbivore Spodoptera littoralis and the phloem-sucking aphid Myzus persicae. We demonstrate that for nodulating strains of T. repens rhizobia increased plant growth and the performance of Spodoptera littoralis. However, this positive effect of rhizobia on the caterpillars did not occur in a cyanogenic clover strain. Reproduction of the phloem-sucking aphid Myzus persicae was inconsistently affected by rhizobia. Our study provides evidence that the additional nitrogen provided by the rhizobia may be used for the production of nitrogen-based defence compounds, thereby counteracting positive effects on the performance of chewing herbivores. The symbiosis with rhizobia is therefore an important driver of legume–herbivore interactions.

Symbiotic soil microorganisms as players in aboveground plant–herbivore interactions – the role of rhizobia

Rhizobia play a key role for performance of leguminous plants and ecosystem productivity. However, no studies to date have investigated the importance of the rhizobial symbiosis for legume–herbivore interactions. The additional nitrogen provided by the rhizobia improves the nutritional quality of plants, but may also be used for the synthesis of defence compounds. We performed greenhouse experiments with nodulating and non‐nodulating, as well as cyanogenic and acyanogenic strains of Trifolium repens to study the effects of rhizobia Rhizobium leguminosarum on plant growth and the performance of the chewing herbivore Spodoptera littoralis and the phloem‐sucking aphid Myzus persicae. We demonstrate that for nodulating strains of T. repens rhizobia increased plant growth and the performance of Spodoptera littoralis. However, this positive effect of rhizobia on the caterpillars did not occur in a cyanogenic clover strain. Reproduction of the phloem‐sucking aphid Myzus persicae was inconsistently affected by rhizobia. Our study provides evidence that the additional nitrogen provided by the rhizobia may be used for the production of nitrogen‐based defence compounds, thereby counteracting positive effects on the performance of chewing herbivores. The symbiosis with rhizobia is therefore an important driver of legume–herbivore interactions.