Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences

Plants and herbivores are thought to be engaged in a coevolutionary arms race: rising frequencies of plants with anti-herbivore defences exert pressure on herbivores to resist or circumvent these defences and vice versa. Owing to its frequency-dependent character, the arms race hypothesis predicts that herbivores exhibit genetic variation for traits that determine how they deal with the defences of a given host plant phenotype. Here, we show the existence of distinct variation within a single herbivore species, the spider mite Tetranychus urticae, in traits that lead to resistance or susceptibility to jasmonate (JA)-dependent defences of a host plant but also in traits responsible for induction or repression of JA defences. We characterized three distinct lines of T. urticae that differentially induced JA-related defence genes and metabolites while feeding on tomato plants (Solanum lycopersicum). These lines were also differently affected by induced JA defences. The first line, which induced JA-dependent tomato defences, was susceptible to those defences; the second line also induced JA defences but was resistant to them; and the third, although susceptible to JA defences, repressed induction. We hypothesize that such intraspecific variation is common among herbivores living in environments with a diversity of plants that impose diverse selection pressure.     

Plant defence as a complex and changing phenotype throughout ontogeny

Background and Aims Ontogenetic changes in anti-herbivore defences are common and result from variation in resource availability and herbivore damage throughout plant development. However, little is known about the simultaneous changes of multiple defences across the entire development of plants, and how such changes affect plant damage in the field. The aim of this study was to assess if changes in the major types of plant resistance and tolerance can explain natural herbivore damage throughout plant ontogeny.Methods An assessment was made of how six defensive traits, including physical, chemical and biotic resistance, simultaneously change across the major transitions of plant development, from seedlings to reproductive stages of Turnera velutina growing in the greenhouse. In addition, an experiment was performed to assess how plant tolerance to artificial damage to leaves changed throughout ontogeny. Finally, leaf damage by herbivores was evaluated in a natural population.Key Results The observed ontogenetic trajectories of all defences were significantly different, sometimes showing opposite directions of change. Whereas trichome density, leaf toughness, extrafloral nectary abundance and nectar production increased, hydrogen cyanide and compensatory responses decreased throughout plant development, from seedlings to reproductive plants. Only water content was higher at the intermediate juvenile ontogenetic stages. Surveys in a natural population over 3 years showed that herbivores consumed more tissue from juvenile plants than from younger seedlings or older reproductive plants. This is consistent with the fact that juvenile plants were the least defended stage.Conclusions The results suggest that defensive trajectories are a mixed result of predictions by the Optimal Defence Theory and the Growth–Differentiation Balance Hypothesis. The study emphasizes the importance of incorporating multiple defences and plant ontogeny into further studies for a more comprehensive understanding of plant defence evolution.     

Herbivores and plant defences affect selection on plant reproductive traits more strongly than pollinators

Pollinators and herbivores can both affect the evolutionary diversification of plant reproductive traits. However, plant defences frequently alter antagonistic and mutualistic interactions, and therefore, variation in plant defences may alter patterns of herbivore‐ and pollinator‐mediated selection on plant traits. We tested this hypothesis by conducting a common garden field experiment using 50 clonal genotypes of white clover (Trifolium repens) that varied in a Mendelian‐inherited chemical antiherbivore defence—the production of hydrogen cyanide (HCN). To evaluate whether plant defences alter herbivore‐ and/or pollinator‐mediated selection, we factorially crossed chemical defence (25 cyanogenic and 25 acyanogenic genotypes), herbivore damage (herbivore suppression) and pollination (hand pollination). We found that herbivores weakened selection for increased inflorescence production, suggesting that large displays are costly in the presence of herbivores. In addition, herbivores weakened selection on flower size but only among acyanogenic plants, suggesting that plant defences reduce the strength of herbivore‐mediated selection. Pollinators did not independently affect selection on any trait, although pollinators weakened selection for later flowering among cyanogenic plants. Overall, cyanogenic plant defences consistently increased the strength of positive directional selection on reproductive traits. Herbivores and pollinators both strengthened and weakened the strength of selection on reproductive traits, although herbivores imposed ~2.7× stronger selection than pollinators across all traits. Contrary to the view that pollinators are the most important agents of selection on reproductive traits, our data show that selection on reproductive traits is driven primarily by variation in herbivory and plant defences in this system.     

Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids

Direct and indirect plant defences are well studied, particularly in the Brassicaceae. Glucosinolates (GS) are secondary plant compounds characteristic in this plant family. They play an important role in defence against herbivores and pathogens. Insect herbivores that are specialists on brassicaceous plant species have evolved adaptations to excrete or detoxify GS. Other insect herbivores may even sequester GS and employ them as defence against their own antagonists, such as predators. Moreover, high levels of GS in the food plants of non-sequestering herbivores can negatively affect the growth and survival of their parasitoids. In addition to allelochemicals, plants produce volatile chemicals when damaged by herbivores. These herbivore induced plant volatiles (HIPV) have been demonstrated to play an important role in foraging behaviour of insect parasitoids. In addition, biosynthetic pathways involved in the production of HIPV are being unraveled using the model plant Arabidopsis thialiana. However, the majority of studies investigating the attractiveness of HIPV to parasitoids are based on experiments mainly using crop plant species in which defence traits may have changed through artificial selection. Field studies with both cultivated and wild crucifers, the latter in which defence traits are intact, are necessary to reveal the relative importance of direct and indirect plant defence strategies on parasitoid and plant fitness. Future research should also consider the potential conflict between direct and indirect plant defences when studying the evolution of plant defences against insect herbivory.     

Interactions between plants and herbivores: A review of plant defense

Ecologists have long ignored or underestimated the importance of plant–herbivore interactions owing to the diversities of herbivores, plant defensive strategies and ecological systems. In this review, we briefly discussed the categories of herbivores. Then we reviewed the major types of plant defenses against herbivores. Selective forces of herbivore pressures have led to the evolution of various defensive mechanisms in plants, which can be classified into (i) resistance traits that reduce the amount of damage received, including physical, chemical, and biotic traits; (ii) tolerance mechanisms that decrease the impact of herbivore damage, and (iii) escape strategies that reduce the probability of plants to be found by herbivores. These strategies have been studied at different levels from molecular genetics and genomics, to chemistry and physiology, to community and ecosystem ecology. We summarized the development of the methodology for studying plant defenses against herbivores. Particularly, 24 of those hypotheses and models, which are influential in the international community concerning the relationship between plants and herbivores, including the defensive mimicry hypothesis, the compensatory continuum hypothesis, the slow-growth-high-mortality hypothesis, etc, were introduced and grouped into four categories according to plant defense strategies in the present review. Finally, we also reviewed the research progress of plant–herbivore interactions in China, and discussed the perspectives of studies on plant–herbivore interactions.     

Evolutionary changes in plant tolerance against herbivory through a resurrection experiment

Both theoretical and empirical works have highlighted the difference in the evolutionary implications of host resistance and tolerance against their enemies. However, it has been difficult to show evolutionary changes in host defences in natural populations; thus, evaluating theoretical predictions of simultaneous evolution of defences remains a challenge. We studied the evolutionary changes in traits related to resistance and tolerance against herbivory in a natural plant population using seeds from two collections made in a period of 20 years. In a common garden experiment, we compared defensive traits of ancestral (1987) and descendant (2007) subpopulations of the annual plant Datura stramonium that shows genetic variation for tolerance and to which the specialist herbivore Lema daturaphila is locally adapted. We also examined the effects of different plant genotypes on the herbivore for testing the plant genetic variation in resistance. Based on the response to the contemporary herbivore populations, results revealed a nonsignificant response in plant resistance traits (herbivore consumption, foliar trichomes and tropane alkaloids), but a significant one in tolerance. The survival of herbivores in laboratory experiments depended on the plant genotype, which suggests genetic variation in plant resistance. Although we cannot identify the selective agent for the change nor exclude genetic drift, the results are consistent with the expectation that when resistance fails to control herbivory, tolerance should play a more important role in the evolution of the interaction.     

Geographic association and temporal variation of chemical and physical defense and leaf damage in Datura stramonium

The evolution of plant defense traits has traditionally been explained trough the “coevolutionary arms race” between plants and herbivores. According to this, specialist herbivores have evolved to cope effectively with the defensive traits of their host plants and may even use them as a cue for host location. We analyzed the geographic association between leaf trichomes, two tropane alkaloids (putative resistance traits), and leaf damage by herbivores in 28 populations of Datura stramonium in central Mexico. Since the specialist leaf beetles Epitrix parvula and Lema trilineata are the main herbivores of D. stramonium in central Mexico, we predicted a positive association between plant defense and leaf damage across populations. Also, if physical environmental conditions (temperature or precipitation) constrain the expression of plant defense, then the geographic variation in leaf damage should be explained partially by the interaction between defensive traits and environmental factors. Furthermore, we studied the temporal and spatial variation in leaf trichome density and leaf damage in five selected populations of D. stramonium sampled in two periods (1997 vs. 2007). We found a positive association between leaf trichomes density and atropine concentration with leaf damage across populations. The interaction between defensive traits and water availability in each locality had a significant effect on the geographic variation in leaf damage. Differences among populations in leaf trichome density are maintained over time. Our results indicate that local plant–herbivore interaction plays an important role in shaping the geographic and temporal variation in plant defense in D. stramonium.     

Plant age and the inducibility of extrafloral nectaries in Vicia faba

Insect herbivory imposes a strong selection pressure on plants. As a result, plants have evolved a wide array of defences, including resistance traits that help them reduce the negative impact of herbivores. Along one axis of variation, these traits can be divided into direct resistance (physical and chemical defences) and indirect resistance (the recruitment of natural enemies of the herbivore via extrafloral nectar and other incentives). Along a second axis of variation, resistance can be split into constitutive resistance, which is always present, and induced resistance, which is expressed more strongly following damage to plant tissues. Interestingly, the strength and efficacy of all of constitutive-direct, constitutive-indirect, induced-direct, and induced-indirect resistance can vary with plant age and ontological stage. Here, we examine the effect of plant age on an induced-indirect resistance trait, the deployment of extrafloral nectaries (EFNs) to attract pugnacious ants, in a short-lived annual, broad bean (Vicia faba L.). We demonstrate that in severely damaged plants, the induction of EFNs is greater in older plants (5?C6?weeks) than in younger plants (2?C4?weeks); however, in more moderately damaged plants, the induction of EFNs is unaffected by plant age. This suggests the hypothesis that a plant??s ability to induce extrafloral nectar, and therefore recruit more ant ??bodyguards,?? may be related to the interaction of plant age and severity of damage.     

Silicon-augmented resistance of plants to herbivorous insects: a review

Silicon (Si) is one of the most abundant elements in the earth's crust, although its essentiality in plant growth is not clearly established. However, the importance of Si as an element that is particularly beneficial for plants under a range of abiotic and biotic stresses is now beyond doubt. This paper reviews progress in exploring the benefits at two‐ and three‐trophic levels and the underlying mechanism of Si in enhancing the resistance of host plants to herbivorous insects. Numerous studies have shown an enhanced resistance of plants to insect herbivores including folivores, borers, and phloem and xylem feeders. Silicon may act directly on insect herbivores leading to a reduction in insect performance and plant damage. Various indirect effects may also be caused, for example, by delaying herbivore establishment and thus an increased chance of exposure to natural enemies, adverse weather events or control measures that target exposed insects. A further indirect effect of Si may be to increase tolerance of plants to abiotic stresses, notably water stress, which can in turn lead to a reduction in insect numbers and plant damage. There are two mechanisms by which Si is likely to increase resistance to herbivore feeding. Increased physical resistance (constitutive), based on solid amorphous silica, has long been considered the major mechanism of Si‐mediated defences of plants, although there is recent evidence for induced physical defence. Physical resistance involves reduced digestibility and/or increased hardness and abrasiveness of plant tissues because of silica deposition, mainly as opaline phytoliths, in various tissues, including epidermal silica cells. Further, there is now evidence that soluble Si is involved in induced chemical defences to insect herbivore attack through the enhanced production of defensive enzymes or possibly the enhanced release of plant volatiles. However, only two studies have tested for the effect of Si on an insect herbivore and third trophic level effects on the herbivore's predators and parasitoids. One study showed no effect of Si on natural enemies, but the methods used were not favourable for the detection of semiochemical‐mediated effects. Work recently commenced in Australia is methodologically and conceptually more advanced and an effect of Si on the plants' ability to generate an induced response by acting at the third trophic level was observed. This paper provides the first overview of Si in insect herbivore resistance studies, and highlights novel, recent hypotheses and findings in this area of research. Finally, we make suggestions for future research efforts in the use of Si to enhance plant resistance to insect herbivores.     

Instar-specific sensitivity of specialist Manduca sexta larvae to induced defences in their host plant Nicotiana attenuata

1. The time delay associated with the activation of induced defences is thought to be a liability for this type of defence because it allows herbivores to remove biomass before the defence is fully induced. When defences are costly and plants grow with competitors, however, it may be more advantageous not to induce defences too fast and motivate the herbivore to move to the neighbour when it is most voracious. 2. Such a strategy can only work when the costs for the herbivore of moving to a neighbouring plant are smaller than the costs of staying on a fully induced plant. For lepidopteran herbivores, both the sensitivity to induced defences and the costs of moving may vary considerably between instars and this variation may constrain the plant's defensive opportunities. 3. This study was designed to examine whether the cost of moving, mimicked by a starvation period of 8 h, was larger than the cost of staying on a fully induced plant for each larval instar of the specialist Manduca sexta feeding on induced and control tissues of Nicotiana attenuata. 4. For first‐ and second‐instar larvae, the costs of moving were larger than the costs of staying on a fully induced plant. In contrast, feeding on induced plant material retarded development in third‐instar larvae more than did starvation, indicating that in this instar the costs of leaving are smaller than the costs of staying on an induced plant. More than 98% of the lifetime leaf mass consumed by a M. sexta larva is consumed during the fourth and fifth instars, and during these instars larval development was not affected by either induced defences or starvation. Thus the third instar, the stage just before larvae cause the majority of damage, represents a window of sensitivity to induced defences during which larvae can be motivated to change plants. 5. These results suggest that N. attenuata plants, which commonly compete with conspecifics in nature, have the opportunity to manipulate the behaviour of the specialist herbivore M. sexta to minimise the fitness effects of inducing defences when these defences are most costly, i.e. when plants grow under intraspecific competition.     

Generalising indirect defence and resistance of plants

Indirect defence, the adaptive top‐down control of herbivores by plant traits that enhance predation, is a central component of plant–herbivore interactions. However, the scope of interactions that comprise indirect defence and associated ecological and evolutionary processes has not been clearly defined. We argue that the range of plant traits that mediate indirect defence is much greater than previously thought, and we further organise major concepts surrounding their ecological functioning. Despite the wide range of plant traits and interacting organisms involved, indirect defences show commonalities when grouped. These categories are based on whether indirect defences boost natural enemy abundance via food or shelter resources, or, alternatively, increase natural enemy foraging efficiency via information or alteration of habitat complexity. The benefits of indirect defences to natural enemies should be further explored to establish the conditions in which indirect defence generates a plant–natural enemy mutualism. By considering the broader scope of plant–herbivore–natural enemy interactions that comprise indirect defence, we can better understand plant‐based food webs, as well as the evolutionary processes that have shaped them.     

Above‐ and belowground herbivory jointly impact defense and seed dispersal traits in Taraxacum officinale

Plants are able to cope with herbivores by inducing defensive traits or growth responses that allow them to reduce or avoid the impact of herbivores. Since above‐ and belowground herbivores differ substantially in life‐history traits, for example feeding types, and their spatial distribution, it is likely that they induce different responses in plants. Moreover, strong interactive effects on defense and plant growth are expected when above‐ and belowground herbivores are jointly present. The strengths and directions of these responses have been scarcely addressed in the literature. Using Taraxacum officinale, the root‐feeding nematode Meloidogyne hapla and the locust Schistocerca gregaria as a model species, we examined to what degree above‐ and belowground herbivory affect (1) plant growth responses, (2) the induction of plant defensive traits, that is, leaf trichomes, and (3) changes in dispersal‐related seed traits and seed germination. We compared the performance of plants originating from different populations to address whether plant responses are conserved across putative different genotypes. Overall, aboveground herbivory resulted in increased plant biomass. Root herbivory had no effect on plant growth. Plants exposed to the two herbivores showed fewer leaf trichomes than plants challenged only by one herbivore and consequently experienced greater aboveground herbivory. In addition, herbivory had effects that reached beyond the individual plant by modifying seed morphology, producing seeds with longer pappus, and germination success.     

Floral plasticity: Herbivore‐species‐specific‐induced changes in flower traits with contrasting effects on pollinator visitation

Plant phenotypic plasticity in response to antagonists can affect other community members such as mutualists, conferring potential ecological costs associated with inducible plant defence. For flowering plants, induction of defences to deal with herbivores can lead to disruption of plant–pollinator interactions. Current knowledge on the full extent of herbivore‐induced changes in flower traits is limited, and we know little about specificity of induction of flower traits and specificity of effect on flower visitors. We exposed flowering Brassica nigra plants to six insect herbivore species and recorded changes in flower traits (flower abundance, morphology, colour, volatile emission, nectar quantity, and pollen quantity and size) and the behaviour of two pollinating insects. Our results show that herbivory can affect multiple flower traits and pollinator behaviour. Most plastic floral traits were flower morphology, colour, the composition of the volatile blend, and nectar production. Herbivore‐induced changes in flower traits resulted in positive, negative, or neutral effects on pollinator behaviour. Effects on flower traits and pollinator behaviour were herbivore species‐specific. Flowers show extensive plasticity in response to antagonist herbivores, with contrasting effects on mutualist pollinators. Antagonists can potentially act as agents of selection on flower traits and plant reproduction via plant‐mediated interactions with mutualists.     

Can genetically based clines in plant defence explain greater herbivory at higher latitudes?

Greater plant defence is predicted to evolve at lower latitudes in response to increased herbivore pressure. However, recent studies question the generality of this pattern. In this study, we tested for genetically based latitudinal clines in resistance to herbivores and underlying defence traits of Oenothera biennis. We grew plants from 137 populations from across the entire native range of O. biennis. Populations from lower latitudes showed greater resistance to multiple specialist and generalist herbivores. These patterns were associated with an increase in total phenolics at lower latitudes. A significant proportion of the phenolics were driven by the concentrations of two major ellagitannins, which exhibited opposing latitudinal clines. Our analyses suggest that these findings are unlikely to be explained by local adaptation of herbivore populations or genetic variation in phenology. Rather greater herbivory at high latitudes can be explained by latitudinal clines in the evolution of plant defences.     

Herbivore-induced coexistence of competing plant species

We study a series of spatially implicit lottery models in which two competing plant species, with and without defensive traits, are grazed by a herbivore in a homogeneous habitat. One species (palatable) has no defensive traits, while the other (defended) has defensive traits but suffers reduced reproduction as the result of an assumed trade-off. Not surprisingly, coexistence of these plants cannot occur when the herbivore density is very low (the palatable plant always wins) or very high (the defended plant wins). At intermediate densities, however, herbivory can mediate plant coexistence, even in a homogeneous environment. If the herbivore eats several plants per bite, and its forage-selection depends on the average palatability of the plants it eats, then palatable species in the immediate neighbourhood of defended plants may be more likely to persist (associational resistance) even at higher grazing pressure. If the herbivore shows a positive numerical response to the average palatability of the habitat as a whole, then both plant populations are stabilized and coexistence is promoted, because both species obtain a minority advantage through the negative feedback caused by herbivory. If the herbivore exhibits both of these traits, the system may have at most two non-trivial equilibria, one of which is stable and the other unstable. This means that coexistence in such a system is vulnerable to large fluctuations in herbivore density and identity, and this has implications for conservation in systems where large herbivores are managed to promote plant diversity.     

Indirect plant defense against insect herbivores: a review

Plants respond to herbivore attack by launching 2 types of defenses: direct defense and indirect defense. Direct defense includes all plant traits that increase the resistance of host plants to insect herbivores by affecting the physiology and/or behavior of the attackers. Indirect defense includes all traits that by themselves do not have significant direct impact on the attacking herbivores, but can attract natural enemies of the herbivores and thus reduce plant loss. When plants recognize herbivore‐associated elicitors, they produce and release a blend of volatiles that can attract predators, parasites, and other natural enemies. Known herbivore‐associated elicitors include fatty acid–amino acid conjugates, sulfur‐containing fatty acids, fragments of cell walls, peptides, esters, and enzymes. Identified plant volatiles include terpenes, nitrogenous compounds, and indoles. In addition, constitive traits including extrafloral nectars, food bodies, and domatia can be further induced to higher levels and attract natural enemies as well as provide food and shelter to carnivores. A better understanding of indirect plant defense at global and componential levels via advanced high throughput technologies may lead to utilization of indirect defense in suppression of herbivore damage to plants.     

Jasmonate-mediated induced plant resistance affects a community of herbivores

1. The negative effect of induced plant resistance on the preference and performance of herbivores is a well‐documented ecological phenomenon that is thought to be important for both plants and herbivores. This study links the well‐developed mechanistic understanding of the biochemistry of induced plant resistance in the tomato system with an examination of how these mechanisms affect the community of herbivores in the field. 2. Several proteins that are induced in tomato foliage following herbivore damage have been linked causally to reductions in herbivore performance under laboratory conditions. Application of jasmonic acid, a natural elicitor of these defensive proteins, to tomato foliage stimulates induced responses to herbivory. 3. Jasmonic acid was sprayed on plants in three doses to generate plants with varying levels of induced responses, which were measured as increases in the activities of proteinase inhibitors and polyphenol oxidase. 4. Field experiments conducted over 3 years indicated that induction of these defensive proteins is associated with decreases in the abundance of all four naturally abundant herbivores, including insects in three feeding guilds, caterpillars, flea beetles, aphids, and thrips. Induced resistance killed early instars of noctuid caterpillars. Adult flea beetles strongly preferred control plants over induced plants, and this effect on host plant preference probably contributed to differences in the natural abundance of flea beetles. 5. The general nature of the effects observed in this study suggests that induced resistance will suppress many members of the herbivore community. By linking plant biochemistry, insect preference, performance, and abundance, tools can be developed to manipulate plant resistance sensibly and to predict its outcome under field conditions.     

Plant structural traits and their role in anti-herbivore defence

We consider the role that key structural traits, such as spinescence, pubescence, sclerophylly and raphides, play in protecting plants from herbivore attack. Despite the likelihood that many of these morphological characteristics may have evolved as responses to other environmental stimuli, we show that each provides an important defence against herbivore attack in both terrestrial and aquatic ecosystems. We conclude that leaf-mass–area is a robust index of sclerophylly as a surrogate for more rigorous mechanical properties used in herbivory studies. We also examine herbivore counter-adaptations to plant structural defence and illustrate how herbivore attack can induce the deployment of intensified defensive measures. Although there have been few studies detailing how plant defences vary with age, we show that allocation to structural defences is related to plant ontogeny. Age-related changes in the deployment of structural defences plus a paucity of appropriate studies are two reasons why relationships with other plant fitness characteristics may be obscured, although we describe studies where trade-offs between structural defence and plant growth, reproduction, and chemical defences have been demonstrated. We also show how resource availability influences the expression of structural defences and demonstrate how poorly our understanding of plant structural defence fits into contemporary plant defence theory. Finally, we suggest how a better understanding of plant structural defence, particularly within the context of plant defence syndromes, would not only improve our understanding of plant defence theory, but enable us to predict how plant morphological responses to climate change might influence interactions at the individual (plant growth trade-offs), species (competition), and ecosystem (pollination and herbivory) levels.     

Mechanisms of plant defense against insect herbivores

Plants respond to herbivory through various morphological, biochemicals, and molecular mechanisms to counter/offset the effects of herbivore attack. The biochemical mechanisms of defense against the herbivores are wide-ranging, highly dynamic, and are mediated both by direct and indirect defenses. The defensive compounds are either produced constitutively or in response to plant damage, and affect feeding, growth, and survival of herbivores. In addition, plants also release volatile organic compounds that attract the natural enemies of the herbivores. These strategies either act independently or in conjunction with each other. However, our understanding of these defensive mechanisms is still limited. Induced resistance could be exploited as an important tool for the pest management to minimize the amounts of insecticides used for pest control. Host plant resistance to insects, particularly, induced resistance, can also be manipulated with the use of chemical elicitors of secondary metabolites, which confer resistance to insects. By understanding the mechanisms of induced resistance, we can predict the herbivores that are likely to be affected by induced responses. The elicitors of induced responses can be sprayed on crop plants to build up the natural defense system against damage caused by herbivores. The induced responses can also be engineered genetically, so that the defensive compounds are constitutively produced in plants against are challenged by the herbivory. Induced resistance can be exploited for developing crop cultivars, which readily produce the inducible response upon mild infestation, and can act as one of components of integrated pest management for sustainable crop production.     

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.