Plant-insect Herbivore Interactions Research Articles

Oral secretions: A key molecular interface of plant-insect herbivore interactions

The oral secretions of insect herbivores are complex mixtures of organic and inorganic solutes and enzymes that are deposited onto plant tissues during the feeding process. Some specific components of insect oral secretions have been shown to confer important functions in mediating plant-insect interactions at the molecular level. In this review, we examined the biochemical studies of insect oral secretions to summarize the current knowledge of their compositions. We then moved beyond the functional studies of components of oral secretions, and focused on the literature that pinpointed specific molecular targets of these compounds. Finally, we highlighted the investigations of oral secretion components in the context of insect physiology, which shed light on the potential evolutionary trajectory of these multi-functional molecules.

Exchange of Microbiomes in Plant-Insect Herbivore Interactions

Prokaryotic and eukaryotic microbial symbiotic communities span through kingdoms. The vast microbial gene pool extends the host genome and supports adaptations to changing environmental conditions. Plants are versatile hosts for the symbionts, carrying microbes on the surface, inside tissues, and even within the cells. Insects are equally abundantly colonized by microbial symbionts on the exoskeleton, in the gut, in the hemocoel, and inside the cells. The insect gut is a prolific environment, but it is selective on the microbial species that enter with food. Plants and insects are often highly dependent on each other and frequently interact. Regardless of the accumulating evidence on the microbiomes of both organisms, it remains unclear how much they exchange and modify each other's microbiomes. In this review, we approach this question from the point of view of herbivores that feed on plants, with a special focus on the forest ecosystems. After a brief introduction to the subject, we concentrate on the plant microbiome, the overlap between plant and insect microbial communities, and how the exchange and modification of microbiomes affects the fitness of each host.

Bottom-up effects of fertilization and jasmonate-induced resistance independently affect the interactions between tomato plants and an insect herbivore

ABSTRACT Whether nutrient availability interacts with induced resistance to alter plant chemistry and, consequently, the preference and performance of herbivores on plants remains unclear. We hypothesized that changing fertilizer inputs modulates responses induced by exogenous application of the defensive phytohormone methyl jasmonate (MeJA) against Tuta absoluta, a devastating pest of tomatoes. We found that tomato plants grown at or 2-fold above optimal fertilizer rates had higher nutrient content and were more preferred by T. absoluta females for oviposition and were better hosts for their offspring. MeJA increased phenolic content and volatile emissions in plants, which correlated with lower T. absoluta oviposition preference and offspring performance. However, we found no significant interactions when fertilizer and MeJA were applied simultaneously, such that induced responses against T. absoluta in tomatoes were similar regardless of fertilizer rate. These results provide novel insights into the bottom-up effects of fertilization and induced resistance on plant-insect herbivore interactions.

Understanding the ecology of host plant–insect herbivore interactions in the fossil record through bipartite networks—Corrigendum

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Alternative developmental and transcriptomic responses to host plant water limitation in a butterfly metapopulation.

Predicting how climate change affects biotic interactions poses a challenge. Plant-insect herbivore interactions are particularly sensitive to climate change, as climate-induced changes in plant quality cascade into the performance of insect herbivores. Whereas the immediate survival of herbivore individuals depends on plastic responses to climate change-induced nutritional stress, long-term population persistence via evolutionary adaptation requires genetic variation for these responses. To assess the prospects for population persistence under climate change, it is therefore crucial to characterize response mechanisms to climate change-induced stressors, and quantify their variability in natural populations. Here, we test developmental and transcriptomic responses to water limitation-induced host plant quality change in a Glanville fritillary butterfly (Melitaea cinxia) metapopulation. We combine nuclear magnetic resonance spectroscopy on the plant metabolome, larval developmental assays and an RNA sequencing analysis of the larval transcriptome. We observed that responses to feeding on water-limited plants, in which amino acids and aromatic compounds are enriched, showed marked variation within the metapopulation, with individuals of some families performing better on control and others on water-limited plants. The transcriptomic responses were concordant with the developmental responses: families exhibiting opposite developmental responses also produced opposite transcriptomic responses (e.g. in growth-associated transcripts). The divergent responses in both larval development and transcriptome are associated with differences between families in amino acid catabolism and storage protein production. The results reveal intrapopulation variability in plasticity, suggesting that the Finnish M. cinxia metapopulation harbours potential for buffering against drought-induced changes in host plant quality.

Understanding the ecology of host plant–insect herbivore interactions in the fossil record through bipartite networks

AbstractPlant–insect associations have been a significant component of terrestrial ecology for more than 400 Myr. Exploring these interactions in the fossil record through novel perspectives provides a window into understanding evolutionary and ecological forces that shaped these interactions. For the past several decades, researchers have documented, described, and categorized fossil evidence of these interactions. Drawing on powerful tools from network science, we propose here a bipartite network representation of fossilized plants and their herbivore-induced leaf damage to understand late Paleozoic plant–insect interactions at the local community level. We focus on four assemblages from north-central Texas, but the methods used in this work are general and can be applied to any well-preserved fossil flora. Network analysis can address key questions in the evolution of insect herbivory that often would be difficult to summarize using standard herbivory metrics.

Rich and Specialized Plant-Insect Associations in a Middle–Late Paleocene (58–60 Ma) Neotropical Rainforest (Bogotá Formation, Colombia)

Plant predation by insects is a major driver of high plant diversity in modern tropical forests. Previous reports of leaf damage in middle–late Paleocene Neotropical rainforests of Cerrejón, Colombia, show that leaf herbivory was abundant but of low diversity, mainly inflicted by generalized feeders. Here, we present and describe plant-insect associations in leaf fossils from the middle–late Paleocene Bogotá Formation, central Colombia, to test whether the high abundance and low richness of insect damage typified early evolving Neotropical rainforests. The Bogotá flora records the highest richness and frequency of insect-damage associations among comparable Paleocene floras in North America, Patagonia, and Europe, as well as the highest number of leaf mines and galling associations. These results indicate that by the middle–late Paleocene, plant-insect herbivore interactions were much more intense and host-specialized in Neotropical rainforests of the Bogotá region than elsewhere. The rich and frequent galling associations, a distinctive feature of the Bogotá flora, are consistent with the preferential use of canopy leaves by galling insects seen in modern Neotropical rainforests. Our results also indicate differences in plant-insect associations among Paleocene Neotropical rainforests, perhaps reflecting a geographically heterogeneous ecological recovery from the end-Cretaceous ecological crisis. Plant insect-associations in the Bogotá flora also suggest a deep historical context for negative density-dependence as a potential driver (and maintainer) of the high plant diversity observed in modern Neotropical rainforests.

Detection of herbivory: eDNA detection from feeding marks on leaves

AbstractMany techniques have been developed to investigate the interactions between plants and herbivorous insects in natural environments and are generally used to determine either (a) which plant species are eaten by a specific herbivorous insect or (b) which herbivorous insect species are herbivores of a specific plant. The former problem is usually addressed by the direct observation of feeding and microscopic observation of gut contents and excrements, as well as the application of DNA‐barcoding techniques. However, the latter problem has typically been addressed using time‐consuming methods, such as direct observation and rearing. Therefore, more efficient techniques are needed for identifying and quantifying the interactions of plants with herbivorous insects. The present study demonstrates that the environmental DNA (eDNA) of herbivorous insects can be recovered from leaves with external foliage feeding marks. Mitochondrial DNA fragments of herbivorous insects were detected from insect‐exposed leaves using primer sets that amplified the DNA of target species. The amplification rate of the herbivorous insect DNA was positively associated with the rim length of feeding marks, which suggests that most of the insect DNA came from the feeding marks. Additionally, we showed that this method has the potential to detect eDNA from field‐collected leaves. This time‐efficient approach will contribute to the detection of plant–insect herbivore interactions.

Insect herbivory and herbivores ofFicusspecies along a rain forest elevational gradient in Papua New Guinea

AbstractClassic research on elevational gradients in plant–herbivore interactions holds that insect herbivore pressure is stronger under warmer climates of low elevations. However, recent work has questioned this paradigm, arguing that it oversimplifies the ecological complexity in which plant–insect herbivore interactions are embedded. Knowledge of antagonistic networks of plants and herbivores is however crucial for understanding the mechanisms that govern ecosystem functioning. We examined herbivore damage and insect herbivores of eight species of genusFicus(105 saplings) and plant constitutive defensive traits of two of these species, along a rain forest elevational gradient of Mt. Wilhelm (200–2,700 m a.s.l.), in tropical Papua New Guinea. We report overall herbivore damage 2.4% of leaf area, ranging from 0.03% inFicus endochaeteat 1,700 m a.s.l. to 6.1% inF. hombronianaat 700 m a.s.l. Herbivore damage and herbivore abundances varied significantly with elevation, as well as among the tree species, and between the wet and dry season. Community‐wide herbivore damage followed a hump‐shaped pattern with the peak between 700 and 1,200 m a.s.l. and this pattern corresponded with abundance of herbivores. For two tree species surveyed in detail, we observed decreasing and hump‐shaped patterns in herbivory, in general matching the trends found in the set of plant defenses measured here. Our results imply that vegetation growing at mid‐elevations of the elevational gradient, that is at the climatically most favorable elevations where water is abundant, and temperatures still relatively warm, suffers the maximum amount of herbivorous damage which changes seasonally, reflecting the water availability.

Inducibility of chemical defences in young oak trees is stronger in species with high elevational ranges.

Elevational gradients have been highly useful for understanding the underlying forces driving variation in plant traits and plant-insect herbivore interactions. A widely held view from these studies has been that greater herbivory under warmer and less variable climatic conditions found at low elevations has resulted in stronger herbivore selection on plant defences. However, this prediction has been called into question by conflicting empirical evidence, which could be explained by a number of causes such as an incomplete assessment of defensive strategies (ignoring other axes of defence such as defence inducibility) or unaccounted variation in abiotic factors along elevational clines. We conducted a greenhouse experiment testing for inter-specific variation in constitutive leaf chemical defences (phenolic compounds) and their inducibility in response to feeding by gypsy moth larvae (Lymantria dispar L., Lepidoptera) using saplings of 18 oak (Quercus, Fagaceae) species. These species vary in their elevational distribution and together span >2400 m in elevation, therefore allowing us to test for among-species elevational clines in defences based on the elevational range of each species. In addition, we further tested for elevational gradients in the correlated expression of constitutive defences and their inducibility and for associations between defences and climatic factors potentially underlying elevational gradients in defences. Our results showed that oak species with high elevational ranges exhibited a greater inducibility of phenolic compounds (hydrolysable tannins), but this gradient was not accounted for by climatic predictors. In contrast, constitutive defences and the correlated expression of constitutive phenolics and their inducibility did not exhibit elevational clines. Overall, this study builds towards a more robust and integrative understanding of how multivariate plant defensive phenotypes vary along ecological gradients and their underlying abiotic drivers.

Elevational gradients in plant defences and insect herbivory: recent advances in the field and prospects for future research

Classic research on elevational gradients in plant–herbivore interactions holds that insect herbivore pressure is stronger under warmer, less seasonal climates characteristic of low elevations, and that this in turn selects for increased defence in low‐ (relative to high‐) elevation plants. However, recent work has questioned this paradigm, arguing that it overly simplifies the ecological complexity in which plant–insect herbivore interactions are embedded along elevational gradients. Numerous biotic and abiotic factors vary with elevation, and their simultaneous influences are the focus of current work on elevational gradients in insect herbivory and plant defences. The present review 1) synthesizes current knowledge on elevational gradients in plant–insect herbivore interactions; 2) critically analyses research gaps and highlights recent advances that contribute to filling these gaps; and 3) outlines new research opportunities to uncover underlying mechanisms and build towards a unified theory on elevational gradients. We conclude that the next generation of studies should embrace community complexity – including multi‐trophic dynamics and the multivariate nature of plant defence – and to do so by combining observational data, manipulative experiments and emerging analytical tools.

Does Plant Cultivar Difference Modify the Bottom-Up Effects of Resource Limitation on Plant-Insect Herbivore Interactions?

Variation in resource input to plants triggers bottom-up effects on plant-insect herbivore interactions. However, variation in plant intrinsic traits in response to resource availability may modify the bottom-up effects. Furthermore, the consequences also may depend on the feeding strategy of insect herbivores belonging to different feeding guilds. We evaluated the performance of two insect herbivores from distinct feeding guilds, the leaf miner Tuta absoluta and the phloem feeder Bemisia tabaci. We offered the insects two tomato cultivars growing under optimal nitrogen input vs. nitrogen limitation, or under optimal water input vs. water limitation. We found that: (i) the two cultivars differed in their responses to nitrogen and water limitation by regulating primary (leaf-gas exchange related parameters, leaf nitrogen content, and leaf C/N ratio) and secondary metabolism (main defensive compounds: glycoalkaloids); (ii) for both plant cultivars, nitrogen or water limitation significantly affected T. absoluta survival and development, while B. tabaci survival was affected only by nitrogen limitation; and surprisingly (iii) plant cultivar differences did not modify the negative bottom-up effects of resource limitation on the two insect herbivores. In conclusion, the negative effects of resource limitation cascaded up to insect herbivores even though plant cultivars exhibited various adaptive traits to resource limitation.

Water stress and kaolin spray affect herbivorous insects’ success on cotton

Ecological hypotheses of plant–insect herbivore interactions suggest that insects perform better on weakened plants and plants grown under optimal conditions are less damaged. This study tested the hypothesis that the colonization and oviposition rates by pests with different feeding strategies and levels of specialization are affected in different ways by two conditions commonly faced by commercially grown plants–water deficit and application of kaolin sprays, a reducer of abiotic plant stressors. We used four major pests of cotton as insect herbivore models. Three were chewing Lepidoptera: Alabama argillacea (Hub.), a monophagous pest on cotton; Heliothis virescens (Fabr.), which is polyphagous, but with cotton as a primary host; and Chrysodeixis includens (Walk.), which is polyphagous, with cotton as secondary host. The fourth pest was a sap-sucking species, the polyphagous whitefly Bemisia tabaci (Gen.). In both choice and no-choice trials, the three chewing pests oviposited significantly less upon water-stressed plants; the greatest effect was observed for C. includens (>90 % reduction in oviposition under choice and >58 % under no-choice conditions). In contrast, the sap-sucking B. tabaci exhibited statistically more colonization and oviposition on water-stressed plants. Application of kaolin sprays reduced colonization and oviposition by all herbivore species tested, irrespective of irrigation regime and feeding strategies.

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.

Interactive effects of multiple climate change variables on trophic interactions: a meta-analysis

Climate change is expected to simultaneously alter many of the abiotic qualities of ecosystems as well as biotic interactions, especially trophic interactions. However, research to date has mostly focused on elucidating the effects of single climate change variables on individual species. Here, we use established meta-analysis techniques to synthesize the existing literature on the interactive effects of multiple climate change variables on trophic interactions. Most of the studies included in our meta-analysis examined plant-insect herbivore interactions. We found that the majority of trophic interaction response variables (55%) displayed multiplicative reactions to interacting climate change variables while 36% and 9% displayed antagonistic and synergistic reactions, respectively. We also found that only one of six climate change variable pairings had consistent positive or negative effects on trophic relationships, largely because interaction type and magnitude were both highly context dependent across the pairings. Most notably, males and females frequently responded differently to interacting climate change variables, and the response strength frequently varied with the underlying nutrient load of the system. Our results suggest that trophic interactions commonly respond antagonistically to interacting climate change variables whereas synergistic and simple additive/multiplicative reactions are less common than previously thought. In addition, response type and magnitude are highly context dependent. These findings further suggest that in many cases, future ecosystem responses to climate change, whether positive or negative, may be dampened relative to predictions based on experiments that investigate the effects of single climate change variables on single species. However, there is a paucity of work that has focused on the effects of interacting climate change variables on dynamic biotic relationships, likely because such research requires complex experimentation. Increasing the complexity of climate change research is necessary for accurately predicting ecosystem responses.

Will chemical defenses become more effective against specialist herbivores under elevated CO2?

Elevated atmospheric CO2 is known to affect plant-insect herbivore interactions. Elevated CO2 causes leaf nitrogen to decrease, the ostensible cause of herbivore compensatory feeding. CO2 may also affect herbivore consumption by altering chemical defenses via changes in plant hormones. We considered the effects of elevated CO2, in conjunction with soil fertility and damage (simulated herbivory), on glucosinolate concentrations of mustard (Brassica nigra) and collard (B. oleracea var. acephala) and the effects of leaf nitrogen and glucosinolate groups on specialist Pieris rapae consumption. Elevated CO2 affected B. oleracea but not B. nigra glucosinolates; responses to soil fertility and damage were also species-specific. Soil fertility and damage also affected B. oleracea glucosinolates differently under elevated CO2. Glucosinolates did not affect P. rapae consumption at either CO2 concentration in B. nigra, but had CO2-specific effects on consumption in B. oleracea. At ambient CO2, leaf nitrogen had strong effects on glucosinolate concentrations and P. rapae consumption but only gluconasturtiin was a feeding stimulant. At elevated CO2, direct effects of leaf nitrogen were weaker, but glucosinolates had stronger effects on consumption. Gluconasturtiin and aliphatic glucosinolates were feeding stimulants and indole glucosinolates were feeding deterrents. These results do not support the compensatory feeding hypothesis as the sole driver of changes in P. rapae consumption under elevated CO2. Support for hormone-mediated CO2 response (HMCR) was mixed; it explained few treatment effects on constitutive or induced glucosinolates, but did explain patterns in SEMs. Further, the novel feeding deterrent effect of indole glucosinolates under elevated CO2 in B. oleracae underscores the importance of defensive chemistry in CO2 response. We speculate that P. rapae indole glucosinolate detoxification mechanisms may have been overwhelmed under elevated CO2 forcing slowed consumption. Specialists may have to contend with hosts with poorer nutritional quality and more effective chemical defenses under elevated CO2.

Plant defense: warding off attack by pathogens, herbivores, and parasitic plants

Plant defense: warding off attack by pathogens, herbivores, and parasitic plants

Testing the efficiency of three 15N‐labeled nitrogen compounds for indirect labeling of grasshoppers via plants in the field

AbstractIn field studies of plant–insect herbivore interactions it is often difficult to establish which herbivore has fed on a particular plant. We investigated the suitability of three different 15N‐labeled nitrogen compounds (ammonium, nitrate, and glycine) for indirect marking of three grasshopper species [Omocestus viridulus (L.), Chorthippus parallelus (Zett.), and Chorthippus biguttulus (L.) (Orthoptera: Acrididae)] through labeling their food plants in the field. In two short‐term experiments grassland plots of 1 m2 were separately labeled with either one of the different nitrogen compounds. Grasshoppers were caged on three food‐plant species [Dactylis glomerata L., Holcus lanatus L. (Poaceae), and Trifolium repens L. (Fabaceae)] present in these plots for 72 h. Significantly enriched δ15N values in grasshoppers were found in all plant/grasshopper combinations. Enrichment in grasshoppers was positively correlated with the enrichment of plants and labeling with nitrate resulted in highest 15N enrichment. In a long‐term experiment, individuals of C. biguttulus were placed in a cage covering an area of 1 m2 for 37 days, with sampling of grasshoppers at regular intervals. δ15N values of the grasshopper and a common food plant, D. glomerata, increased steadily over time, up to 40‐fold by the end of the experiment. Our results demonstrate that 15N‐labeling of plants is an appropriate tool for the investigation of insect–plant interactions under natural conditions.

Effects of foliar and soil insecticide applications on the collembolan community of an early set-aside arable field

Effects of foliar and soil insecticide applications on collembolan density and community structure were investigated in an early set-aside arable field. Insecticides were applied separately and in combination to the soil surface (chlorpyrifos) and vegetation (dimethoate). The treatments were established to investigate effects of above- and below-ground insects on plant succession. Starting in 1997, the insecticides were applied from April to November at 2-week (dimethoate) or monthly intervals (chlorpyrifos). Samples were taken in 2000 prior to and after insecticide application in March and June, respectively. Both insecticides are lethal to Collembola and insecticide applications resulted in a strong decline in the density of total Collembola. Application of chlorpyrifos reduced collembolan density to a greater extent than dimethoate; the effect of the combined application on total collembolan numbers was similar to that of chlorpyrifos only. Collembolan numbers recovered after the insecticide applications in 1999, but in the treated plots populations were still reduced in March 2000 before the re-application of insecticide treatments in that year. The insecticide applications changed the dominance structure of the collembolan community, but had no effects on species composition. The results may be of relevance for the interpretation of studies on plant–insect herbivore interactions using insecticides.

Elemental microanalysis in ecophysiology using ion microbeam

A few recent applications of elemental microanalysis based on proton beam in ecophysiology and ecotoxicology are shown. They are related to biofiltering capabilities of mycorrhiza (symbiosis between fungi and plant roots) and to plant–insect herbivore interactions. The reported results were obtained at iThemba LABS, South Africa. PIXE and BS techniques were simultaneously used. True elemental maps were generated using a VMS version and PC version of GeoPIXE (GeoPIXE I and II). Further analysis was performed using PIXE and BS spectra extracted from list-mode data and corresponding to specific organs of an insect or a plant.