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The transmission of resistance traits to herbivores across subsequent generations is an important strategy employed by plants to enhance their fitness in environments with high herbivore pressure. However, our understanding of the impact of maternal herbivory on direct and indirect induced chemical defenses of progeny, as well as the associated costs, is currently limited to herbivory by leaf-chewing insects. In this study, we investigated the transgenerational effects of a sap-feeding insect, the green peach aphid Myzus persicae, on direct and indirect chemical defenses of bell pepper plants (Capsicum annuum), and whether the effects entail costs to plant growth. Aphid herbivory on parental plants led to a reduced number of seeds per fruit, which exhibited lower germination rates and produced smaller seedlings compared to those from non-infested parental plants. In contrast, the progeny of aphid-infested plants were less preferred as hosts by aphids and less suitable than the progeny of non-infested plants. This enhanced resistance in the progeny of aphid-infested plants coincided with elevated levels of both constitutive and herbivore-induced total phenolic compounds, compared to the progeny of non-infested plants. Furthermore, the progeny of aphid-infested plants emitted herbivore-induced plant volatiles (HIPVs) that were more attractive to the aphid parasitoid Aphidius platensis than those emitted by the progeny of non-infested plants. Our results indicate that herbivory by sap-feeding insect induces transgenerational resistance on progeny bell pepper plants, albeit at the expense of vegetative growth., (© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

Evolutionary biologists have long sought to understand the ecological processes that generate plant reproductive diversity. Recent evidence indicates that constitutive antiherbivore defences can alter natural selection on reproductive traits, but it is unclear whether induced defences will have the same effect and whether reduced foliar damage in defended plants is the cause of this pattern. In a factorial field experiment using common milkweed, Asclepias syriaca L., we induced plant defences using jasmonic acid (JA) and imposed foliar damage using scissors. We found that JA-induced plants experienced selection for more inflorescences that were smaller in size (fewer flowers), whereas control plants only experienced a trend towards selection for larger inflorescences (more flowers); all effects were independent of foliar damage. Our results demonstrate that induced defences can alter both the strength and direction of selection on reproductive traits, and suggest that antiherbivore defences may promote the evolution of plant reproductive diversity., (© 2017 European Society For Evolutionary Biology. Journal of Evolutionary Biology © 2017 European Society For Evolutionary Biology.)

Background: Plants can respond to insect attack via defense mechanisms that reduce insect performance. In this study, we examined the effects of several treatments applied to two maize genotypes (one resistant, one susceptible) on the subsequent growth and survival of Sesamia nonagrioides Lef. (Mediterranean corn borer, MCB) larvae. The treatments were infestation with MCB larvae, application of MCB regurgitant upon wounding, wounding alone, or exposure to methyl jasmonate, and they were applied at the V6-V8 stage of maize development. We also monitored changes in the concentrations of compounds known to be involved in constitutive resistance, such as cell wall-bound hydroxycinnamates and benzoxazinoids., Results: In both maize genotypes, the leaves of plants pre-infested with MCB larvae were less suitable for larval development than those from untreated plants. Application of MCB regurgitant upon wounding, and wounding itself, resulted in leaf tissues becoming less suitable for larval growth than those of pre-infested plants, suggesting that there could be herbivore-associated effector molecules that suppress some wounding responses. A single application of MCB regurgitant did not seem to mimic feeding by MCB larvae, although the results suggested that regurgitant deposited during feeding may have enhanced ferulates and diferulates synthesis in infested vs. control plants. Jasmonic acid may play a role in mediating the maize response to MCB attack, but it did not trigger hydroxycinnamate accumulation in the leaves to a level comparable to that induced by larval leaf feeding. The EP39 maize genotype showed an increase in leaf cell wall strength by increasing hemicellulose cross-linking in response to MCB attack, while induced defenses in the EP42 plants appeared to reflect a broader array of resistance mechanisms., Conclusions: The results indicated that leaf feeding by MCB larvae can increase leaf antibiosis against MCB in two maize genotypes with contrasting levels of resistance against this borer. Also, the larval regurgitant played a positive role in eliciting a defense response. We determined the effects of the plant response on larval growth, and detected defense compounds related to borer resistance.

Spatially separated aboveground (AG) and belowground (BG) herbivores are closely linked through shared host plants, and both patterns of AG-BG interactions and plant responses may vary among plant genotypes. We subjected invasive (USA) and native (China) genotypes of tallow tree (Triadica sebifera) to herbivory by the AG specialist leaf-rolling weevil Heterapoderopsis bicallosicollis and/or the root-feeding larvae of flea beetle Bikasha collaris. We measured leaf damage and leaves rolled by weevils, quantified beetle survival, and analyzed flavonoid and tannin concentrations in leaves and roots. AG and BG herbivores formed negative feedbacks on both native and invasive genotypes. Leaf damage by weevils and the number of beetle larvae emerging as adults were higher on invasive genotypes. Beetles reduced weevil damage and weevils reduced beetle larval emergence more strongly for invasive genotypes. Invasive genotypes had lower leaf and root tannins than native genotypes. BG beetles decreased leaf tannins of native genotypes but increased root tannins of invasive genotypes. AG herbivory increased root flavonoids of invasive genotypes while BG herbivory decreased leaf flavonoids. Invasive genotypes had lower AG and BG herbivore resistance, and negative AG-BG herbivore feedbacks were much stronger for invasive genotypes. Lower tannin concentrations explained overall better AG and BG herbivore performances on invasive genotypes. However, changes in tannins and flavonoids affected AG and BG herbivores differently. These results suggest that divergent selection on chemical production in invasive plants may be critical in regulating herbivore performances and novel AG and BG herbivore communities in new environments.

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.

Key message: Corymbia citriodora subsp. variegata altered the expression of secondary metabolites in response to Paropsis atomaria larval feeding and mechanical wounding but did not alter leaf toughness and leaf trichomes. Plants have evolved strategies against herbivore pressure, relying on constitutive or induced traits that create physical and chemical barriers, which may influence herbivore performance. We evaluated the physical and chemical responses of Corymbia citriodora subsp. variegata, an important hardwood plantation taxon, to feedings by Paropsis atomaria larvae, a pest that causes severe defoliation in young trees. This was undertaken to obtain insights into plant–herbivore interactions, aiming to identify parameters that may improve plant fitness and/or protection that may benefit pest management in forestry plantations. Seedlings of C. citriodora subsp. variegata were submitted to the following treatments: no damage, mechanical wounding, and P. atomaria larval feeding damage. Foliar samples were collected during and after treatment at day 15 and 22, respectively, from damaged and undamaged leaves to detect: local, systemic, or delayed induced responses. Leaf samples were analysed to determine whether there were induced physical (leaf toughness, trichome density) or chemical (secondary metabolite profiles) responses to damage. No physical response in any of the treatments was evident in C. citriodora subsp. variegata foliage at day 15 or 22. Systemic chemical responses were observed for the larval feeding and mechanical treatments, with, a delayed response evident in the larval feeding treatment only. The proportion of long chain hydrocarbons were reduced in these treatments relative to the control, whereas the proportion of monounsaturated hydrocarbons and monoterpenes increased. When analysed across treatments, larval mortality was negatively correlated with long chain hydrocarbons and positively correlated with monounsaturated hydrocarbons. These findings suggest that CCV systemic chemical responses induced by both larval feeding and mechanical damage but only larval feeding induced delayed response, suggesting that CCV responses to herbivory may be associated with plant defence strategies. [ABSTRACT FROM AUTHOR]

1. Ants are recognized as induced biotic defence in mutualistic relationships with myrmecophytic plants. Pseudomyrmex concolor is an aggressive Amazonian ant that works as an anti‐herbivory agent for its host plant Tachigali myrmecophila. However, it is not known how this ant maintains the plant on low levels of herbivory. 2. Tachigali myrmecophila provides no food for P. concolor making this model appropriate to test the hypothesis that ants associated with myrmecophytes act as induced biotic defence by herbivory. Based on Optimal Defence Theory, we tested whether the response to herbivory and the ant daily activity rhythm is more frequent in most valuable parts of the plant, such as young leaves. 3. Ants were observed in young and mature leaves exposed to herbivory by experimental manipulation. Results suggest that ants act as induced biotic defence in T. myrmecophila: number of ants was significantly higher in manipulated leaflets, as well as the daily activity rhythm was increased in young leaves. The time to detect herbivory in young and mature leaves did not differ. However, leaf extracts signs were identified more quickly by the ants. 4. Induced ant responses in the ant–myrmecophytic plants system can be considered constitutive defence because ants are present throughout the development of their host plant from seedling to adulthood, responding aggressively to any intruder. In the Pseudomyrmex–Tachigali system, the presence of ants on the plants is, per se, a constitutive defence. However, the patrolling activity is an induced response, being the result of several plant‐related cues (chemical and physical) associated with herbivory activity. Pseudomyrmex concolor is an aggressive Amazonian ant that works as an anti‐herbivory agent for its host plant Tachigali myrmecophila. However, it is not known how this ant maintains the plant at low levels of herbivory.Based on Optimal Defence Theory, we tested whether the response to herbivory and the ant daily activity rhythm is more frequent in most valuable parts of the plant, such as young leaves.In the Pseudomyrmex–Tachigali system, the presence of ants on the plants is, per se, a constitutive defence, yet the patrolling activity is an induced response, being the result of several plant‐related cues (chemical and physical) associated with herbivore activity. [ABSTRACT FROM AUTHOR]

In plant–arthropod associations, the first herbivores to colonise a plant may directly or indirectly affect community assembly on that particular plant. Whether the order of arrival of different arthropod species further modulates community assembly and affects plant fitness remains unclear. Using wild Brassica oleracea plants in the field, we manipulated the order of arrival of early‐season herbivores that belong to different feeding guilds, namely the aphid Brevicoryne brassicae and caterpillars of Plutella xylostella. We investigated the effect of herbivore identity and order of arrival on community assembly on two B. oleracea plant populations during two growth seasons. For this perennial plant, we evaluated whether foliar herbivory also affected herbivore communities on the flowers and if these interactions affected plant seed production. Aphid infestation caused an increase in parasitoid abundance, but caterpillars modulated these effects, depending on the order of herbivore infestation and plant population. In the second growth season, when plants flowered, the order of infestation of leaves with aphids and caterpillars more strongly affected abundance of herbivores feeding on the flowers than those feeding on leaves. Infestation with caterpillars followed by aphids caused an increase in flower‐feeding herbivores compared to the reversed order of infestation in one plant population, whereas the opposite effects were observed for the other plant population. The impact on plant seed set in the first reproductive year was limited. Our work shows that the identity and arrival order of early season herbivores may have long‐term consequences for community composition on individual plants and that these patterns may vary among plant populations. We discuss how these community processes may affect plant fitness and speculate on the implications for evolution of plant defences. [ABSTRACT FROM AUTHOR]

Abstract: Intraspecific variation in plant defense phenotype is common and has wide‐ranging ecological consequences. Yet prevailing theories of plant defense allocation, which primarily account for interspecific differences in defense phenotype, often fail to predict intraspecific patterns. Furthermore, although individual variation in defense phenotype is often attributed to ecological interactions, few general mechanisms have been proposed to explain the ubiquity of variable defense phenotype within species. Here, we show experimentally that associational refuges and induced resistance interact to create predictable intraspecific variation in defense phenotype in African savanna plants. Physically defended species from four families (Acanthaceae, Asparagaceae, Cactaceae, and Solanaceae) growing in close association with spinescent Acacia trees had 39–78% fewer spines and thorns than did isolated conspecifics. For a subset of these species, we used a series of manipulative experiments to show that this variability is maintained primarily by a reduction in induced responses among individuals that seldom experience mammalian herbivory, whether due to association with Acacia trees or to experimental herbivore exclusion. Unassociated plants incurred 4‐ to 16‐fold more browsing damage than did associated individuals and increased spine density by 16–38% within one month following simulated browsing. In contrast, experimental clipping induced no net change in spine density among plants growing beneath Acacia canopies or inside long‐term herbivore exclosures. Associated and unassociated individuals produced similar numbers of flowers and seeds, but seedling recruitment and survival were vastly greater in refuge habitats, suggesting a net fitness benefit of association. We conclude that plant‐plant associations consistently decrease defense investment in this system by reducing both the frequency of herbivory and the intensity of induced responses, and that inducible responses enable plants to capitalize on such associations in heterogeneous environments. Given the prevalence of associational and induced defenses in plant communities worldwide, our results suggest a potentially general mechanism by which biotic interactions might predictably shape intraspecific variation in plant defense phenotype. [ABSTRACT FROM AUTHOR]

Coevolution is among the most important evolutionary processes that generate biological diversity. Plant-pollinator interactions play a prominent role in the evolution of reproductive traits in flowering plants. Likewise, plant-herbivore interactions select for myriad defenses that protect plants from damage. These mutualistic and antagonistic interactions, respectively, have traditionally been considered in isolation from one another. Here, we consider whether reproductive traits and antiherbivore defenses are interdependent as a result of pollinator- and herbivore-mediated selection. The evolution of floral traits, self-fertilization, and separate sexes frequently affects the expression and evolution of plant defenses. In turn, the evolution of defense can affect allocation to reproductive traits, and herbivores often impose strong selection directly on floral traits. Theory and empirical evidence suggest that herbivores can influence the evolution of selfing from outcrossing and potentially the evolution of separate sexes from combined sexes. We identify several areas in which future research is needed to increase our understanding of the evolutionary interplay between reproduction and defense in plants. [ABSTRACT FROM AUTHOR]

Many metabolomics studies aim to find 'biomarkers': sets of molecules that are consistently elevated or decreased upon experimental manipulation. Biological effects, however, often manifest themselves along a continuum of individual differences between the biological replicates in the experiment. Such differences are overlooked or even diminished by methods in standard use for metabolomics, although they may contain a wealth of information on the experiment. Properly understanding individual differences is crucial for generating knowledge in fields like personalised medicine, evolution and ecology. We propose to use simultaneous component analysis with individual differences constraints (SCA-IND), a data analysis method from psychology that focuses on these differences. This method constructs axes along the natural biochemical differences between biological replicates, comparable to principal components. The model may shed light on changes in the individual differences between experimental groups, but also on whether these differences correspond to, e.g., responders and non-responders or to distinct chemotypes. Moreover, SCA-IND reveals the individuals that respond most to a manipulation and are best suited for further experimentation. The method is illustrated by the analysis of individual differences in the metabolic response of cabbage plants to herbivory. The model reveals individual differences in the response to shoot herbivory, where two 'response chemotypes' may be identified. In the response to root herbivory the model shows that individual plants differ strongly in response dynamics. Thereby SCA-IND provides a hitherto unavailable view on the chemical diversity of the induced plant response, that greatly increases understanding of the system. [ABSTRACT FROM AUTHOR]

Although exogenous treatment of plants with jasmonic acid (JA) may result in induced responses similar to plant defences induced by herbivory, few studies have compared the details of insect herbivory and JA-mimicked responses. We compared volatiles of two crucifer species, Cardamine impatiens and Lepidium virginicum, in response to Plutella xylostella larval feeding and exogenous application of JA, over the entire period of time when induced changes were detectable. Significant differences in the composition and timing of volatiles occurred between herbivory and JA treatments in both plants. The quantity of nitrile and isothiocyanate released in response to herbivory was significantly larger than that upon JA treatment. In each of the two plant species, most volatile components were emitted immediately upon larval feeding and their quantity dropped rapidly once feeding ceased. In contrast, the emission of volatiles in response to JA treatment lasted for a longer period of time, and the maximum emission rate was recorded 2 and 3 days after JA treatment in L. virginicum and C. impatiens respectively. These findings are discussed in the context of signal-transduction pathways and mechanisms involved in induced emissions of plant volatiles, as well as induced defences mediated by plant volatiles. [ABSTRACT FROM AUTHOR]

Insect herbivores by necessity have to deal with a large arsenal of plant defence metabolites. The levels of defence compounds may be increased by insect damage. These induced plant responses may also affect the metabolism and performance of successive insect herbivores. As the chemical nature of induced responses is largely unknown, global metabolomic analyses are a valuable tool to gain more insight into the metabolites possibly involved in such interactions. This study analyzed the interaction between feral cabbage ( Brassica oleracea) and small cabbage white caterpillars ( Pieris rapae) and how previous attacks to the plant affect the caterpillar metabolism. Because plants may be induced by shoot and root herbivory, we compared shoot and root induction by treating the plants on either plant part with jasmonic acid. Extracts of the plants and the caterpillars were chemically analysed using Ultra Performance Liquid Chromatography/Time of Flight Mass Spectrometry (UPLCT/MS). The study revealed that the levels of three structurally related coumaroylquinic acids were elevated in plants treated on the shoot. The levels of these compounds in plants and caterpillars were highly correlated: these compounds were defined as the ‘metabolic interface’. The role of these metabolites could only be discovered using simultaneous analysis of the plant and caterpillar metabolomes. We conclude that a metabolomics approach is useful in discovering unexpected bioactive compounds involved in ecological interactions between plants and their herbivores and higher trophic levels. [ABSTRACT FROM AUTHOR]

1. The shade-tolerant conifer Abies alba Mill. (European silver fir) is a favoured browse species of several large herbivores. We performed an experiment to investigate how sun or shade conditions influence the recovery of A. alba saplings following simulated browsing. The browsing treatment involved clipping the leader and/or lateral shoots. For two growing seasons after applying the treatment, we recorded various measures of plant growth including bud development and the origin of new leaders. We then harvested the trees to determine patterns of above-ground biomass allocation. In the discussion, we consider the physiological basis for the observed responses to damage and evaluate the hypothesis that they represent an evolved defensive strategy against herbivory. 2. After 2 years, most saplings in the sun had compensated for lost height due to leader clipping, whereas saplings in the shade lagged 1 year behind. The degree of height recovery was influenced less by the length of the new leader than by its mode of origin; thus, there was overcompensation if the new leader developed from a side-shoot turning upwards (‘flagging’), while there was undercompensation if it was produced from an interwhorl or a secondary whorl bud. Leader origin, in turn, proved to be light-dependent, with flagging occurring twice as often in sun as in shade. Some trees, mostly in the shade, produced no leader in the first year but several leaders from secondary whorl buds in the second year (i.e. multiple stemming). Clipping of the leader also induced local bud development and led to greater allocation of resources to new leaders than in unclipped trees. Clipping of lateral shoots had no effect on either height increment or growth of lateral branches. 3. We conclude that, by influencing how the new leader is produced, light availability also affects the degree to which A. alba can compensate for loss in height from browsing. A possible interpretation of the overcompensation under high-light is as a defensive reaction to escape future browsing. However, an alternative explanation is that overcompensation and other morphological reactions, for example, multiple leaders, are merely contrasting physiological responses to release from apical dominance under different environmental conditions. [ABSTRACT FROM AUTHOR]

Phenotypic plasticity describes the capacity of a genotype to exhibit a range of phenotypes in response to variation in the environment. Environmental variation encompasses both abiotic and biotic components of the environment, including interactions among organisms. The strength and outcome of many ecological interactions, ranging from antagonism to mutualism, are mediated through the phenotypically plastic responses of one or more players in the interaction. Herein, three broadly defined, non-mutually exclusive, evolutionary consequences of ecological interactions mediated through phenotypic plasticity are discussed. (1) The predictable plastic response of one partner can favor behaviors, physiological responses, and life history traits of an interacting partner that manipulate, circumvent, or ameliorate the response of that partner. (2) Phenotypic plasticity can generate substantial spatial and temporal variation within and among populations. Such phenotypic variation can depend on the density and identity of interacting players in an ecological community, and can ultimately affect the evolutionary outcome of ecological interactions. (3) Phenotypic plasticity affects the strength and direction of natural selection. Ecological interactions mediated through phenotypic plasticity are ubiquitous in nature, and the potential evolutionary consequences of these interactions illustrate the complexity inherent in understanding evolution in a community context. [ABSTRACT FROM AUTHOR]

The role of induced responses of tomato, Lycopersicon esculentum, in interspecific interactions between two polyphagous herbivores, the silverleaf whitefly, Bemisia argentifolii (WF), and the vegetable leafminer, Liriomyza trifolii (LM), was characterized in laboratory and field experiments. Feeding by LMs and WFs induced local and systemic production of putative defensive proteins, i.e., chitinases, peroxidases, β-1,3-glucanases, and lysozymes. The magnitude of the induction for each defensive protein varied between species. Unlike WFs, LMs caused a 33% local reduction in total foliar protein content. In a whole-plant choice experiment, adult LM feeding, oviposition, and larval survival were reduced by 47.7%, 30.7%, and 26.5%, respectively, for the WF-infested host compared with the controls. Early WF infestations also had negative systemic (plant-mediated) effects on LMs. Adult LMs preferred leaves from control plants to leaves of plants that had been previously infested with WFs; no reciprocal effect of LMs on WFs were found. Feeding by Helicoverpa zea larvae, which has been shown previously to affect LM performance, had no effect on WF survival and development. LM natural population dynamics were monitored on WF-preinfested and control plants in a field experiment. WF-infested plants were less suitable for LM development with an overall 41% reduction in LM population density. These results demonstrate asymmetric direct and plant-mediated interspecific interactions between generalist herbivores feeding simultaneously on the same host. Possible mechanisms by which WFs overcome plant defenses are suggested. This ability may also contribute to WF success that makes them a major pest worldwide. The study supports the idea that over an evolutionary time scale, herbivores sharing the same host plant will automatically compete. [ABSTRACT FROM AUTHOR]

We compare the dynamic nature of anti-herbivore defense in ant-plants to other plant-herbivore systems. Previous studies have neglected the dynamic nature of defense in ant-plants. Changes in environmental cues can trigger modifications in a plantis defensive strategy (induced responses). In ant-plants, many cues and signals controlled by theplant and the environment can enhance defense by influencing recruitment, patrolling, and persistence of ants. Leaf damage may trigger plant signals such as the release of plant sap or green leaf volatiles that attract ant defenders. Similarly, disturbance and mammalian breath may themselves induce ants to recruit. We also review studies thathave looked for changes in extrafloral nectar production induced by herbivory. Induced responses to herbivory that stimulate changes in nectar volume, sugar concentration, and amino acid concentration of extrafloral nectar have been reported. This should increase patrolling by defending ants. We propose that non-nectary mediated ant recruitment should also occur, but may be restricted to tightly linked ant-plant systems. We suggest that induced responses to herbivory are commonin ant-plants. [ABSTRACT FROM AUTHOR]