Seasonality of herbivory and communication between individuals of sagebrush

Seasonal changes in herbivore numbers and in plant defenses are well known to influence plant–herbivore interactions. Some plant defenses are induced in response to herbivore attack or cues correlated with risk of attack although seasonal variation in these defenses is relatively poorly known. We previously reported that sagebrush becomes more resistant to its herbivores when neighboring plants have been experimentally clipped with scissors. In this study we asked whether herbivory to leaves of sagebrush varied seasonally and whether there was seasonal variation in natural levels of damage when neighbors were clipped. We found that sagebrush accumulated most chewing damage early in the season, soon after the spring flush of new leaves. This damage was caused by generalist grasshoppers, deer, specialist caterpillars, beetles, gall makers, and other less common herbivores. Sagebrush showed no evidence of preferentially abscising leaves that had been experimentally clipped. Experimental clipping by Trirhabda pilosa beetle larvae caused neighbors to accumulate less herbivore damage later that season, similar to results in which clipping was done with scissors. Induced resistance caused by experimentally clipping a neighbor was affected by season; plants with neighbors clipped in May accumulated less damage throughout the season relative to plants with unclipped neighbors or neighbors clipped later in the summer. We found a correlation between seasonal herbivore pressure, damage accumulated by plants, and induced responses to experimentally clipping neighbors. The causal mechanisms responsible for this correlation are unknown although a strong seasonal effect was clear.     

Volatile communication between plants that affects herbivory: a meta‐analysis

Volatile communication between plants causing enhanced defence has been controversial. Early studies were not replicated, and influential reviews questioned the validity of the phenomenon. We collected 48 well‐replicated studies and found overall support for the hypothesis that resistance increased for individuals with damaged neighbours. Laboratory or greenhouse studies and those conducted on agricultural crops showed stronger induced resistance than field studies on undomesticated species, presumably because other variation had been reduced. A cumulative analysis revealed that early, non‐replicated studies were more variable and showed less evidence for communication. Effects of habitat and plant growth form were undetectable. In most cases, the mechanisms of resistance and alternative hypotheses were not considered. There was no indication that some response variables were more likely to produce large effects. These results indicate that plants of diverse taxonomic affinities and ecological conditions become more resistant to herbivores when exposed to volatiles from damaged neighbours.     

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

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

Plant age, communication, and resistance to herbivores: young sagebrush plants are better emitters and receivers

Plants progress through a series of distinct stages during development, although the role of plant ontogeny in their defenses against herbivores is poorly understood. Recent work indicates that many plants activate systemic induced resistance after herbivore attack, although the relationship between resistance and ontogeny has not been a focus of this work. In addition, for sagebrush and a few other species, individuals near neighbors that experience simulated herbivory become more resistant to subsequent attack. Volatile, airborne cues are required for both systemic induced resistance among branches and for communication among individuals. We conducted experiments in stands of sagebrush of mixed ages to determine effects of plant age on volatile signaling between branches and individuals. Young and old control plants did not differ in levels of chewing damage that they experienced. Systemic induced resistance among branches was only observed for young plants. Young plants showed strong evidence of systemic resistance only if airflow was permitted among branches; plants with only vascular connections showed no systemic resistance. We also found evidence for volatile communication between individuals. For airborne communication, young plants were more effective emitters of cues as well as more responsive receivers of volatile cues.     

Methyl jasmonate does not induce changes in Eucalyptus grandis leaves that alter the effect of constitutive defences on larvae of a specialist herbivore

The up-regulation of secondary metabolic pathways following herbivore attack and the subsequent reduction in herbivore performance have been identified in numerous woody plant species. Eucalypts constitutively express many secondary metabolites in the leaves, including terpenes and formylated phloroglucinol compounds (FPCs). We used clonal ramets from six clones of Eucalyptus grandis and two clones of E. grandis x camaldulensis to determine if methyl jasmonate (MeJA) treatment could induce changes in the foliar concentrations of either of these groups of compounds. We also used bioassays to determine if any changes in the performance of larvae of Paropsis atomaria, a chrysomelid leaf beetle, could be detected in treated ramets versus the untreated controls, thus indicating whether MeJA induced the up-regulation of defences other than terpenes or FPCs. We found no significant effects of MeJA treatment on either the foliar concentrations of terpenes and FPCs or on herbivore performance. We did, however, detect dramatic differences in larval performance between Eucalyptus clones, thereby demonstrating large variations in the levels of constitutive defence. Larval feeding on clones resistant to P. atomaria resulted in high first instar mortality and disruption of normal gregarious feeding behaviour in surviving larvae. Histological examination of larvae feeding on a resistant clone revealed damage to the midgut consistent with the action of a toxin. These findings concur with mounting evidence that most evergreen perennial plants lack foliar-induced defences and suggest that constitutively expressed secondary metabolites other than those commonly examined in studies of interactions between insect herbivores and Eucalyptus may be important in plant defence.     

Compensation and resistance to herbivory in seagrasses: induced responses to simulated consumption by fish

Herbivory can induce changes in plant traits that may involve both tolerance mechanisms that compensate for biomass loss and resistance traits that reduce herbivore preference. Seagrasses are marine vascular plants that possess many attributes that may favour tolerance and compensatory growth, and they are also defended with mechanisms of resistance such as toughness and secondary metabolites. We quantified phenotypic changes induced by herbivore damage on the temperate seagrass Posidonia oceanica in order to identify specific compensatory and resistance mechanisms in this plant, and to assess any potential trade-offs between these two strategies of defence. We simulated three natural levels of fish herbivory by repeatedly clipping seagrass leaves during the summer period of maximum herbivory. Compensatory responses were determined by measuring shoot-specific growth, photosynthetic rate, and the concentration of nitrogen and carbon resources in leaves and rhizomes. Induced resistance was determined by measuring the concentration of phenolic secondary metabolites and by assessing the long-term effects of continued clipping on herbivore feeding preferences using bioassays. Plants showed a significant ability to compensate for low and moderate losses of leaf biomass by increasing aboveground growth of damaged shoots, but this was not supported by an increase in photosynthetic capacity. Low levels of herbivory induced compensatory growth without any measurable effects on stored resources. In contrast, nitrogen reserves in the rhizomes played a crucial role in the plant’s ability to compensate and survive herbivore damage under moderate and high levels of herbivory, respectively. We found no evidence of inducibility of long-term resistance traits in response to herbivory. The concentration of phenolics decreased with increasing compensatory growth despite all treatments having similar carbon leaf content, suggesting reallocation of these compounds towards primary functions such as cell-wall construction.     

Airborne signals of communication in sagebrush: a pharmacological approach

When plants receive volatiles from a damaged plant, the receivers become more resistant to herbivory. This phenomenon has been reported in many plant species and called plant-plant communication. Lab experiments have suggested that several compounds may be functioning as airborne signals. The objective of this study is to identify potential airborne signals used in communication between sagebrush (Artemisia tridentata) individuals in the field. We collected volatiles of one branch from each of 99 sagebrush individual plants. Eighteen different volatiles were detected by GC-MS analysis. Among these, 4 compounds; 1.8-cineol, β-caryophyllene, α-pinene and borneol, were investigated as signals of communication under natural conditions. The branches which received either 1,8-cineol or β-caryophyllene tended to get less damage than controls. These results suggested that 1,8-cineol and β-caryophyllene should be considered further as possible candidates for generalized airborne signals in sagebrush.     

Reversal of fortune: plant suppression and recovery after vole herbivory

It is not clear how plant species preferred as forage by rodents persist in prairie vegetation. To test permanence of suppression of wet-mesic prairie vegetation by vole (Microtus pennsylvanicus) herbivory in synthetic experimental communities, access treatments were reversed after 9 years of vole exclusion or access. Between 1996 and 2004, rye grass Elymus virginicus (Poaceae) and tick-trefoil Desmodium canadense (Fabaceae) achieved mean cover of up to 30 and 25%, respectively, in plots where voles were excluded, but disappeared from plots where voles had access. To determine whether these species remained vulnerable to vole herbivory as established adults, and to determine whether the species could recover if vole herbivory were removed, access treatments were reversed at the end of the 2004 growing season and monitored through 2007. Repeated measures ANOVA demonstrated dramatic vole suppression of established E. virginicus, but not D. canadense, indicating continuing vulnerability of the grass but not of the adult legume. Release from vole herbivory resulted in re-growth of rye, but not tick-trefoil, which was apparently suppressed by established vegetation. Two additional common planted species did not respond to treatment reversal, nor did 11 much less common planted species that comprised a minor portion of the vegetation. Dominant perennial black-eyed Susan Rudbeckia subtomentosa (Asteraceae) did not change in plant numbers by year or treatment, but expanded or contracted in stems per plant and cover as E. virginicus was suppressed or released by vole herbivory or its absence. Results indicate that preferred food plants may persist through capacity to quickly recover during periods of relative vole scarcity, or reach a refuge in maturity.     

Root and shoot glucosinolates: a comparison of their diversity, function and interactions in natural and managed ecosystems

The role of glucosinolates in aboveground plant–insect and plant–pathogen interactions has been studied widely in both natural and managed ecosystems. Fewer studies have considered interactions between root glucosinolates and soil organisms. Similarly, data comparing local and systemic changes in glucosinolate levels after root- and shoot-induction are scarce. An analysis of 74 studies on constitutive root and shoot glucosinolates of 29 plant species showed that overall, roots have higher concentrations and a greater diversity of glucosinolates than shoots. Roots have significantly higher levels of the aromatic 2-phenylethyl glucosinolate, possibly related to the greater effectiveness and toxicity of its hydrolysis products in soil. In shoots, the most dominant indole glucosinolate is indol-3-ylglucosinolate, whereas roots are dominated by its methoxyderivatives. Indole glucosinolates were the most responsive after jasmonate or salicylate induction, but increases after jasmonate induction were most pronounced in the shoot. In general, root glucosinolate levels did not change as strongly as shoot levels. We postulate that roots may rely more on high constitutive levels of glucosinolates, due to the higher and constant pathogen pressure in soil communities. The differences in root and shoot glucosinolate patterns are further discussed in relation to the molecular regulation of glucosinolate biosynthesis, the within-tissue distribution of glucosinolates in the roots, and the use of glucosinolate-containing crops for biofumigation. Comparative studies of tissue-specific biosynthesis and regulation in relation to the biological interactions in aboveground and belowground environments are needed to advance investigations of the evolution and further utilization of glucosinolates in natural and managed ecosystems. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Delayed induced responses of birch glandular trichomes and leaf surface lipophilic compounds to mechanical defoliation and simulated winter browsing

Changes in morphology and chemistry of leaf surface in response to herbivore damage may increase plant resistance to subsequent herbivore attack; however, there is lack of studies on induced responses of glandular trichomes and their exudates in woody plants and on effects of these changes on herbivores. We studied delayed induced responses in leaf surface traits of five clones of silver birch (Betula pendula Roth) subjected to various types of mechanical defoliation and simulated winter browsing. Glandular trichome density and concentrations of the majority of surface lipophilic compounds increased in trees defoliated during the previous summer. This induced response was systemic, since control branches in branch defoliated trees responded to the treatments similarly to defoliated branches, but differently from control trees. In contrast to defoliation treatments, simulated winter browsing reduced glandular trichome density on the following summer and had fewer effects on individual surface lipophilic compounds. Moreover, constitutive density of glandular trichomes was negatively correlated with induced total amount of lipophilic compounds per trichome, indicating a trade-off between constitutive and induced resistance in silver birch. Induced changes in leaf surface traits had no significant effect on leaf damage by chewers, miners and gall mites, but increased susceptibility of birch trees to aphids. However, leaf damage by chewers, miners and gall mites in defoliated (but not in control) trees was correlated with concentrations of some fatty acids and triterpenoids, although the direction of relationships varied among herbivore species. This indicates that induction of surface lipophilic compounds may influence birch resistance to herbivores. Our study thus demonstrated both specificity of elicitation of induced responses of birch leaf surface traits by different types of damage and specificity of the effects of these responses on different types of herbivores.Electronic Supplementary Material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Plant regrowth response to a stem-boring insect: a swift moth-willow system

To examine plastic willow regrowth response to herbivory, we studied the effect of a boring insect, the swift moth Endoclita excrescens (Hepialidae: Lepidoptera), which does not remove apical meristems, on shoot growth in three willow species—Salix gilgiana, S. eriocarpa, and S. serissaefolia−by direct observations and experiments in the field. We hypothesized that the stem-boring could initiate new lateral bud activation, and result in secondary shoot regrowth without the removal of the primary apical meristems. There were significantly more lateral shoots on naturally attacked than unattacked stems, and a significant positive correlation between lateral shoot density and the number of swift moth tunnels per tree was observed for all three willow species. Artificial boring, and larval infestation, resulted in an increase in the number of lateral shoots, but did not affect growth of current-year shoots. The length of lateral shoots differed between species, being significantly longer in S. gilgiana than S. eriocarpa and S. serissaefolia. The results of this study show that compensatory regrowth can result even if herbivory does not remove the apical meristem. We argue that this type of plant compensatory response is probably widespread, given that the stem-boring is a common feeding type of insect herbivores.     

Impact of floral herbivory by <Emphasis Type="Italic">Coleotechnites eryngiella</Emphasis> Bottimer (Lepidoptera: Gelechiidae) on the reproductive output of <Emphasis Type="Italic">Eryngium yuccifolium</Emphasis> Michaux (Apiaceae): a test of the reserve ovary model

The reserve ovary model is a key hypothesis proposed to explain why plants produce surplus flowers and posits that plants may utilize surplus flowers to compensate for losses from floral herbivory. We tested this hypothesis in the prairie plant Eryngium yuccifolium and its floral herbivore Coleotechnites eryngiella. At five Illinois tallgrass prairie sites, we collected central, primary lateral, and secondary lateral inflorescences from E. yuccifolium to determine whether damage by the larvae of C. eryngiella to the flowers in earlier developing inflorescences would be compensated for in later developing inflorescences. Coleotechnites eryngiella does extensive damage to the central and primary inflorescences and little damage to the secondary inflorescences. Later maturing inflorescences did not compensate for early damage by increasing seed production in later inflorescences. The secondary inflorescences of E. yuccifolium may only compensate for catastrophic damage done to the central and primary inflorescences early on in development, serve as additional advertisements for pollinators, act as pollen donors, or allow the plant to take advantage of “ecological windows” of high pollinator and low herbivore abundance. Our findings were spatially and temporally consistent and did not support the predictions of the reserve ovary model in the E. yuccifolium–C. eryngiella system suggesting that in this system, alternate, proximate, and ultimate causes need to be explored for the production of surplus flowers.     

Variation in plant quality and the population dynamics of herbivores: there is nothing average about aphids

In the attempt to use results from small-scale studies to make large-scale predictions, it is critical that we take into account the greater spatial heterogeneity encountered at larger spatial scales. An important component of this heterogeneity is variation in plant quality, which can have a profound influence on herbivore population dynamics. This influence is particularly relevant when we consider that the strength of density dependence can vary among host plants and that the strength of density dependence determines the difference between exponential and density- dependent growth. Here, we present some simple models and analyses designed to examine the impact of variable plant quality on the dynamics of insect herbivore populations, and specifically the consequences of variation in the strength of density dependence among host plants. We show that average values of herbivore population growth parameters, calculated from plants that vary in quality, do not predict overall population growth. Furthermore, we illustrate that the quality of a few individual plants within a larger plant population can dominate herbivore population growth. Our results demonstrate that ignoring spatial heterogeneity that exists in herbivore population growth on plants that differ in quality can lead to a misunderstanding of the mechanisms that underlie population dynamics.     

Preference of Neoseiulus californicus (Acari: Phytoseiidae) for volatiles of Bt maize induced by multiple herbivory

Plant indirect induced defenses against herbivores are characterized by the production of plant volatiles that to attract natural enemies. The objective of this study was to evaluate whether the attack of the two-spotted spider mite Tetranychus urticae or the multiple herbivory of T. urticae together with the fall armyworm Spodoptera frugiperda are able to elicit indirect induced defense in conventional and Bt maize plants. The experiment was carried out in the laboratory using Y-tube olfactometer, evaluating the predatory mite Neoseiulus californicus olfactory preference for plant volatiles. The treatments involved: Clean Conventional Plant; Conventional Plant Infested with T. urticae; Clean Bt Plant; Bt Plant Infested with T. urticae; Conventional Plant Infested with T. urticae + fall armyworm; Bt Plant Infested with T. urticae + fall armyworm. For the chemical analyzes the Trace GC Ultra gas chromatograph was used, paired with the Polaris Q mass spectrometer, GCMS system. Neoseiulus californicus was also unable to distinguish between volatiles from both conventional and Bt infested maize plants. Moreover, there was no discrimination of the predator mite between plants under single and multiple infestations, both in conventional and Bt maize. When comparing conventional and Bt plants, both with multiple infestation, the predator mite N. californicus had no preference among these sources of odors. However, there was observed chemical changes of the volatiles among the groups of plants studied. Thus, it is suggested that the groups of plants under study have chemical modifications, but they are not able to attract N. californicus. In addition, Bt plants response was similar to conventional plants on attracting N. californicus.     

Members only: induced systemic resistance to herbivory in a clonal plant network

The stoloniferous herb Trifolium repens was used to study the expression of induced systemic resistance (ISR) to the generalist caterpillar Spodoptera exigua in interconnected ramets of clonal fragments. The ISR was assessed as caterpillar preference in dual choice tests between control and systemically induced plants. The ISR was detected in young ramets, after inducing older sibling ramets on the same stolon by a controlled herbivore attack. However, older ramets did not receive a defense induction signal from younger ramets unless the predominant phloem flow was reversed by means of basal shading. This provides evidence for the notion that in T. repens the clone-internal expression of ISR is coupled to phloem transport and follows source–sink gradients. The inducibility of the genotypes was not linked to their constitutive ability to produce cyanide, implying the absence of a trade-off between these two defense traits. To our knowledge, this is the first study that explores ISR to herbivory in the context of physiological integration in potentially extensive clonal plant networks.     

Impact of volcanic activity on a plant-pollinator module in an island ecosystem: the example of the association of <Emphasis Type="Italic">Camellia japonica</Emphasis> and <Emphasis Type="Italic">Zosterops japonica</Emphasis>

Volcanic activity provides an indispensable opportunity to study the ecological responses of organisms to environmental devastation. We examined the reproductive success of Camellia trees to identify how volcanic activity affects the processes of leaf survival, flowering activity, fruit and seed production, pollinator abundance, pollinator visitation frequency, pollination rate, and fruit and seed maturation at different damage sites on Miyake-jima, which experienced an eruption in the summer of 2000. Volcanic gases negatively affect leaf survival and reduce flowering activity in heavily damaged areas. Pollen transfer was sufficient to ensure that higher pollination rates (83%) occurred in heavily damaged areas than in less damaged areas (26–45%), but pollinator densities were lower in response to reduced flower resources. Fruit abortion rates were greater in heavily damaged sites (78%) than in less-damaged sites (53–63%). Consequently, fruit-set rates (16–29%) did not differ significantly among sites. Seed set rates tended to increase with increasing volcanic damage. The negative correlation between seed-set rates and seed mass suggests that the decreased seed mass in severely damaged sites was attributable to the better pollination rates observed there. These results indicate that compensation mechanisms ensure better reproductive success at sites that are more strongly affected by volcanic activity.     

Induced resistance to Mexican bean beetles in soybean: variation among genotypes and lack of correlation with constitutive resistance

Fourteen genotypes (varieties) of soybean (Glycine max) were screened for levels of induced resistance to Mexican bean beetle (Epilachna varivestis) damage, and a subset of 6 of those varieties was screened for levels of constitutive resistance to Mexican bean beetles. Experiments were carried out in the greenhouse, with damage imposed by Mexican bean beetle larvae, and levels of resistance measured by a choice test bioassay with adult beetles. We found significant variation among soybean genotypes in levels of both induced and constitutive resistance. We found no significant correlation between levels of induced and constitutive resistance measured in the same genotypes. We compare these results to past work on resistance in the soybean-Mexican bean beetle system, consider the implications of variation in both types of resistance for plant-herbivore interactions in agricultural and natural systems, and discuss the relationship between induced and constitutive resistance. Received: 30 November 1998 / Accepted: 25 June 1999     

Use of silenced plants in allelopathy bioassays: a novel approach

Volatile phytohormones or other chemicals can affect processes in distal plant parts but may also influence neighboring plants, and thereby function allelopathically. While this hypothesis has been widely discussed, rigorous tests are lacking. Transgenic plants, silenced in the production of an emitted chemical, are ideal tools to test the hypothesis that the release of a chemical can negatively influence the growth of neighbors (allelopathy). We used isogenic wild type (WT) and genetically transformed plants that lacked the ability to produce ethylene (ir-aco), as both “emitters” and “receivers” of this volatile phytohormone in experiments where receiver plants were only exposed to the headspace of WT or ir-aco emitters, in order to evaluate if natural ethylene releases can function allelopathically. Root growth (a proxy of plant fitness) of WT receivers correlated negatively with the number of WT emitters and headspace ethylene concentrations. Reducing ethylene concentrations in the headspace with the ethylene scrubber, KMnO₄, and using ir-aco seedlings as emitters restored root growth of WT receiver seedlings. 1-Aminocyclopropane-1-carboxylic acid (ethylene biosynthesis substrate) supplementation to WT but not ir-aco emitters inhibited root growth of ir-aco, but not WT receivers, suggesting increased sensitivity to exogenous ethylene of ir-aco seedlings. We conclude that plants genetically silenced in the production of a putative allelochemical are useful in determining if the emitted chemical functions allelopathically. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Chlorophyll fluorescence imaging for disease-resistance screening of sugar beet

Both biotic and abiotic stresses cause considerable crop yield losses worldwide (Chrispeels, Sadava Plants, genes, and crop biotechnology 2003; Oerke, Dehne Crop Prot 23:275–285 2004). To speed up screening assays in stress resistance breeding, non-contact techniques such as chlorophyll fluorescence imaging can be advantageously used in the quantification of stress-inflicted damage. In comparison with visual spectrum images, chlorophyll fluorescence imaging reveals cell death with higher contrast and at earlier time-points. This technique has the potential to automatically quantify stress-inflicted damage during screening applications. From a physiological viewpoint, screening stress-responses using attached plant leaves is the ideal approach. However, leaf growth and circadian movements interfere with time-lapse monitoring of leaves, making it necessary to fix the leaves to be studied. From this viewpoint, a method to visualise the evolution of chlorophyll fluorescence from excised leaf pieces kept in closed petri dishes offers clear advantages. In this study, the plant–fungus interaction sugar beet–Cercospora beticola was assessed both in attached leaf and excised leaf strip assays. The attached leaf assay proved to be superior in revealing early, pre-visual symptoms and to better discriminate between the lines with different susceptibility to Cercospora.