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.     

Wild strawberry shows genetic variation in tolerance but not resistance to a generalist herbivore

Plants’ defenses against herbivores usually include both resistance and tolerance mechanisms. Their deployment has predominantly been studied in either single‐plant genotypes or multiple genotypes exposed to single herbivores. In natural situations, however, most plants are attacked by multiple herbivores. Therefore, aims of this study were to assess and compare the effects of single and multiple herbivores on plant resistance and tolerance traits, and the consequences for overall plant performance. For this, we exposed multiple genotypes of wild woodland strawberry (Fragaria vesca) to jasmonic acid (JA), to mimic chewing herbivory and induce the plants’ defense responses, and then introduced the generalist herbivore Spodoptera littoralis to feed on them. We found that woodland strawberry consistently showed resistance to S. littoralis herbivory, with no significant genetic variation between the genotypes. By contrast, the studied genotypes showed high variation in tolerance, suggesting evolutionary potential in this trait. Prior JA application did not alter these patterns, although it induced an even higher level of resistance in all tested genotypes. The study provides novel information that may be useful for breeders seeking to exploit tolerance and resistance mechanisms to improve strawberry crops’ viability and yields, particularly when multiple herbivores pose significant threats.     

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.     

Antiherbivore defenses alter natural selection on plant reproductive traits

While many studies demonstrate that herbivores alter selection on plant reproductive traits, little is known about whether antiherbivore defenses affect selection on these traits. We hypothesized that antiherbivore defenses could alter selection on reproductive traits by altering trait expression through allocation trade‐offs, or by altering interactions with mutualists and/or antagonists. To test our hypothesis, we used white clover, Trifolium repens, which has a Mendelian polymorphism for the production of hydrogen cyanide—a potent antiherbivore defense. We conducted a common garden experiment with 185 clonal families of T. repens that included cyanogenic and acyanogenic genotypes. We quantified resistance to herbivores, and selection on six floral traits and phenology via male and female fitness. Cyanogenesis reduced herbivory but did not alter the expression of reproductive traits through allocation trade‐offs. However, the presence of cyanogenic defenses altered natural selection on petal morphology and the number of flowers within inflorescences via female fitness. Herbivory influenced selection on flowers and phenology via female fitness independently of cyanogenesis. Our results demonstrate that both herbivory and antiherbivore defenses alter natural selection on plant reproductive traits. We discuss the significance of these results for understanding how antiherbivore defenses interact with herbivores and pollinators to shape floral evolution.     

Geographic variation and temporal changes in plant–herbivore interaction: Case studies with Solidago altissima in native and introduced ranges

Plants are subjected to environmental gradients and may encounter various herbivores, leading to geographic variation in defensive traits. The present review highlights that biological invasions are remarkable natural experiments for studying geographic variation in plant–herbivore interaction and tracking temporal dynamics in plant defense in response to environmental changes. Studies from this viewpoint can challenge various general topics in plant ecology, including the evolution of plant defense and indirect interactions among plants. First, I provide a brief overview on how the introduction of exotic herbivores drives rapid evolution after the establishment of exotic plants and its impacts on native plants. Second, I present a series of case studies investigating the patterns and mechanisms of geographic variation in the interaction between Solidago altissima and Corythucha marmorata (lace bug) in the native range in the United States and the introduced range in Japan. By combining biogeographical and experimental approaches, my collaborators and I unraveled the temporal dynamics of S. altissima's resistance to lace bugs and explored the drivers of differentiation in resistance between native and introduced ranges. These studies provide new insight into the geographic variation in exotic plant–herbivore interaction by unraveling the mechanisms and the temporal scale that cause the variation. These findings are vital not only for predicting invasiveness of exotic plants but also for understanding the evolution of plant–herbivore interaction in community contexts and under climate change.     

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.     

The spitting image of plant defenses: Effects of plant secondary chemistry on the efficacy of caterpillar regurgitant as an anti‐predator defense

In the arms race between plants, herbivores, and their natural enemies, specialized herbivores may use plant defenses for their own benefit, and variation in plant traits may affect the benefits that herbivores derive from these defenses. Pieris brassicae is a specialist herbivore of plants containing glucosinolates, a specific class of defensive secondary metabolites. Caterpillars of P. brassicae are known to actively spit on attacking natural enemies, including their main parasitoid, the braconid wasp Cotesia glomerata. Here, we tested the hypothesis that variation in the secondary metabolites of host plants affects the efficacy of caterpillar regurgitant as an anti‐predator defense. Using a total of 10 host plants with different glucosinolate profiles, we first studied natural regurgitation events of caterpillars on parasitoids. We then studied manual applications of water or regurgitant on parasitoids during parasitization events. Results from natural regurgitation events revealed that parasitoids spent more time grooming after attack when foraging on radish and nasturtium than on Brassica spp., and when the regurgitant came in contact with the wings rather than any other body part. Results from manual applications of regurgitant showed that all parameters of parasitoid behavior (initial attack duration, attack interruption, grooming time, and likelihood of a second attack) were more affected when regurgitant was applied rather than water. The proportion of parasitoids re‐attacking a caterpillar within 15 min was the lowest when regurgitant originated from radish‐fed caterpillars. However, we found no correlation between glucosinolate content and regurgitant effects, and parasitoid behavior was equally affected when regurgitant originated from a glucosinolate‐deficient Arabidopsis thaliana mutant line. In conclusion, host plant affects to a certain extent the efficacy of spit from P. brassicae caterpillars as a defense against parasitoids, but this is not due to glucosinolate content. The nature of the defensive compounds present in the spit remains to be determined, and the ecological relevance of this anti‐predator defense needs to be further evaluated in the field.     

An Ecological Genetic Approach to the Study of Coevolution

Almost forty years ago, Ehrlich and Raven (1964) hypothesizedthat the great diversity of plants and the herbivores that feedon them arose from a process of coevolution. Plants do possessan amazing diversity of traits that are easily imagined as havingarisen from an antagonistic interaction between plants and herbivores.Two basic assumptions lie at the root of most theories of coevolutionbetween plants and their herbivores. First, herbivores are agentsof natural selection on plant resistance traits. Second, plantsincur a significant fitness cost for possessing these resistancetraits. An ecological genetic approach can provide rigorousevidence for these coevolutionary assumptions. In this paper,I present new experimental work on the subject of costs of resistanceand review and discuss my own previous work bearing directlyon these questions. Using both field experiments on naturalpopulations of the mouse-ear cress (Arabidopsis thaliana) andlaboratory experiments using genetically modified plants, Idemonstrate that herbivores are exerting selection on both achemical and physical resistance trait and that there are significantfitness costs to possessing these two traits. These resultsprovide direct confirmation that our current models of the evolutionof plant defenses are appropriate.     

Increased reproductive capacity and physical defense but decreased tannin content in an invasive plant

Abstract Plant invasions create novel plant–insect interactions. The EICA (evolution of increased competitive ability) hypothesis proposes that invasive plants will reallocate resources from defense to growth and/or reproduction because they have escaped from their co‐evolved insect natural enemies. Testing multiple herbivory by monophagous and oligophagous herbivores and simultaneous measurement of various plant traits will provide new insights into the evolutionary change of invasive plants. In this context, we conducted a common garden experiment to compare plant growth and reproduction, chemical and physical defense, and plant responses to herbivory by different types of herbivores between invasive North American populations and native East Asian populations of mile‐a‐minute weed, Persicaria perfoliata. We found that invasive mile‐a‐minute exhibited lower biomass, flowered earlier and had greater reproductive output than plants from the native range. Compared with native populations, plants from invasive populations had lower tannin content, but exhibited higher prickle density on nodes and leaves. Thus our results partially support the EICA hypothesis. When exposed to the monophagous insect, Rhinoncomimus latipes and the oligophagous insects, Gallerucida grisescens and Smaragdina nigrifrons, more damage by herbivory was found on invasive plants than on natives. R. latipes, G. grisescens and S. nigrifrons had strong, moderate and weak impacts on the growth and reproduction of mile‐a‐minute, respectively. The results indicate that mile‐a‐minute may have evolved a higher reproductive capacity in the introduced range, and this along with a lack of oligophagous and monophagous herbivores in the new range may have contributed to its invasiveness in North America.     

Overcompensating plants: their expression of resistance traits and effects on herbivore preference and performance

Overcompensation is a plant tolerance response in which plants have higher fitness after herbivory than without damage. Although it has been demonstrated that plants are able to simultaneously express resistance and tolerance traits, it remains unclear whether overcompensating plants are also inducing resistance‐mediating secondary metabolite production and how herbivores perform on plants that overcompensate. Our previous work has shown that a potato variety [Solanum tuberosum L. cv. Pastusa Suprema (Solanaceae)] from Colombia can express overcompensatory responses to damage by larvae of the Guatemalan potato moth, Tecia solanivora Povolny (Lepidoptera: Gelechiidae). Here we investigated (1) whether potatoes that express overcompensatory responses also induce resistance traits and (2) how the previous damage affects Guatemalan potato moth preference and performance. Our results show that larval feeding not only systemically induces higher tuber biomass but also an increased production of resistance‐related compounds, such as phenolics and proteinase inhibitors. Pupal mass increased with increasing tuber size, whereas changes in tuber secondary metabolism did not correlate with any metric of larval performance. Oviposition preference did not change between induced and undamaged plants. Our data show that potato plants expressing overcompensatory responses also induce secondary compounds known to increase resistance against herbivores. However, the induced response was relatively small, reducing the opportunities for a negative effect on the herbivore. Hypotheses for why larvae perform better in larger tubers and are not affected by the secondary metabolism are discussed. From an ecological and agricultural point of view, our results suggest that the expression of overcompensatory traits could have positive effects on herbivore performance.     

Herbivore induced plant volatiles: Their role in plant defense for pest management

Plants respond to herbivory through different defensive mechanisms. The induction of volatile emission is one of the important and immediate response of plants to herbivory. Herbivore-induced plant volatiles (HIPVs) are involved in plant communication with natural enemies of the insect herbivores, neighboring plants, and different parts of the damaged plant. Release of a wide variety of HIPVs in response to herbivore damage and their role in plant-plant, plant-carnivore and intraplant communications represents a new facet of the complex interactions among different trophic levels. HIPVs are released from leaves, flowers, and fruits into the atmosphere or into the soil from roots in response to herbivore attack. Moreover, HIPVs act as feeding and/or oviposition deterrents to insect pests. HIPVs also mediate the interactions between the plants and the microorganisms. This review presents an overview of HIPVs emitted by plants, their role in plant defense against herbivores and their implications for pest management.     

Direct and indirect adverse effects of tomato on the predatory mite Neoseiulus californicus feeding on the spider mite Tetranychus evansi

Plants may defend themselves against herbivores via morphological traits, chemical traits, or a combination of both. Herbivores that overcome the defensive mechanisms of a plant tend to specialize on this plant due to enhanced protection from natural enemies. Well‐known examples of plants possessing a suite of defensive mechanisms are found in nightshades (Solanaceae), especially in the tomato genus Lycopersicon. The spider mite Tetranychus evansi Baker and Pritchard (Acari: Tetranychidae) is specialized on solanaceous plants and is an invasive pest of tomato in Europe and Africa. Biological control of T. evansi with currently available natural enemies, such as the predatory mites Phytoseiulus persimilis Athias‐Henriot and Neoseiulus californicus McGregor (both Acari: Phytoseiidae), is unsuccessful, with the underlying mechanisms only vaguely known. We hypothesized that T. evansi is a key pest of tomato because this host plant provides a two‐pronged protection from natural enemies. Direct adverse effects of tomato on predators may arise from morphological traits and/or trichome exudates, whereas indirect effects are prey‐mediated through the accumulation of toxic plant compounds. Using a 2 × 3 factorial design, we assessed and separated direct and indirect effects of tomato on the life history of N. californicus feeding on two strains of T. evansi (reared on bean or tomato) on three substrates (tomato leaf, bean leaf, and an artificial cage). Developmental time and oviposition rate of N. californicus were both directly and indirectly negatively affected by tomato whereas offspring sex ratio and survival of juveniles and adult females were unaffected. The direct and indirect, prey‐mediated adverse effects of tomato on N. californicus with T. evansi prey had similar magnitudes and were additive. We conclude that T. evansi per se is a suitable prey species for N. californicus and discuss the results with respect to the potential use of N. californicus as biological control agent of T. evansi on tomato and other host plants.     

Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities

Background Plants are hotbeds for parasites such as arthropod herbivores, which acquire nutrients and energy from their hosts in order to grow and reproduce. Hence plants are selected to evolve resistance, which in turn selects for herbivores that can cope with this resistance. To preserve their fitness when attacked by herbivores, plants can employ complex strategies that include reallocation of resources and the production of defensive metabolites and structures. Plant defences can be either prefabricated or be produced only upon attack. Those that are ready-made are referred to as constitutive defences. Some constitutive defences are operational at any time while others require activation. Defences produced only when herbivores are present are referred to as induced defences. These can be established via de novo biosynthesis of defensive substances or via modifications of prefabricated substances and consequently these are active only when needed. Inducibility of defence may serve to save energy and to prevent self-intoxication but also implies that there is a delay in these defences becoming operational. Induced defences can be characterized by alterations in plant morphology and molecular chemistry and are associated with a decrease in herbivore performance. These alterations are set in motion by signals generated by herbivores. Finally, a subset of induced metabolites are released into the air as volatiles and function as a beacon for foraging natural enemies searching for prey, and this is referred to as induced indirect defence.Scope The objective of this review is to evaluate (1) which strategies plants have evolved to cope with herbivores and (2) which traits herbivores have evolved that enable them to counter these defences. The primary focus is on the induction and suppression of plant defences and the review outlines how the palette of traits that determine induction/suppression of, and resistance/susceptibility of herbivores to, plant defences can give rise to exploitative competition and facilitation within ecological communities “inhabiting” a plant.Conclusions Herbivores have evolved diverse strategies, which are not mutually exclusive, to decrease the negative effects of plant defences in order to maximize the conversion of plant material into offspring. Numerous adaptations have been found in herbivores, enabling them to dismantle or bypass defensive barriers, to avoid tissues with relatively high levels of defensive chemicals or to metabolize these chemicals once ingested. In addition, some herbivores interfere with the onset or completion of induced plant defences, resulting in the plant’s resistance being partly or fully suppressed. The ability to suppress induced plant defences appears to occur across plant parasites from different kingdoms, including herbivorous arthropods, and there is remarkable diversity in suppression mechanisms. Suppression may strongly affect the structure of the food web, because the ability to suppress the activation of defences of a communal host may facilitate competitors, whereas the ability of a herbivore to cope with activated plant defences will not. Further characterization of the mechanisms and traits that give rise to suppression of plant defences will enable us to determine their role in shaping direct and indirect interactions in food webs and the extent to which these determine the coexistence and persistence of species.     

Simultaneous inbreeding modifies inbreeding depression in a plant–herbivore interaction

Because inbreeding is common in natural populations of plants and their herbivores, herbivore‐induced selection on plants, and vice versa, may be significantly modified by inbreeding and inbreeding depression. In a feeding assay with inbred and outbred lines of both the perennial herb, Vincetoxicum hirundinaria, and its specialist herbivore, Abrostola asclepiadis, we discovered that plant inbreeding increased inbreeding depression in herbivore performance in some populations. The effect of inbreeding on plant resistance varied among plant and herbivore populations. The among‐population variation is likely to be driven by variation in plant secondary compounds across populations. In addition, inbreeding depression in plant resistance was substantial when herbivores were outbred, but diminished when herbivores were inbred. These findings demonstrate that in plant–herbivore interactions expression of inbreeding depression can depend on the level of inbreeding of the interacting species. Furthermore, our results suggest that when herbivores are inbred, herbivore‐induced selection against self‐fertilisation in plants may diminish.     

Conservation of an Ant–plant Mutualism in Native Forests and Ecologically‐managed Tree Monocultures

The Brazilian Atlantic Forest has been replaced by homogeneous tree monocultures with potentially drastic effect on ecological interactions. We expect that ecologically‐managed tree monocultures, however, can help to mitigate this impact. Here, we carried out an experiment with Inga vera (Fabaceae), an extrafloral nectary bearing plant, to test if the efficiency of ants as anti‐herbivory defense is affected by the replacement of its natural habitat (Araucaria Forest) by ecologically‐managed tree monocultures (plantations of Araucaria, Pinus, and Eucalyptus). Seedlings of Inga vera were transplanted to three patches of each habitat and ants were excluded from half of the plants. The abundance of ants and herbivores was low, similar among habitats, and exhibited temporal asynchrony. Number of herbivores and accumulated herbivory levels were lower in plant with ants. Rates of herbivory were extremely low and lower for young leaves than for mature leaves. The presence of ants did not affect plant performance traits measured by their growth in height, and their final numbers of leaves and leaflets. Contrary to what might be expected, ant‐protected plants produced fewer leaves and leaflets than unprotected ones. In conclusion, Inga vera‐ant interaction was similar between its natural habitat and the tree monocultures, indicating that potentially both species diversity and ecological processes can be conserved in ecologically‐managed tree monocultures.     

Effects of cotton cultivars differing in gossypol content on the quality of Aphis gossypii as prey for two species of Coccinellidae

Plants can have detrimental effects on biological control agents by affecting their prey or host quality. Thus, it is important to understand the tri-trophic interactions between plants, herbivores and natural enemies when implementing biological control programmes. Studies have shown that both morphological and chemical traits of host plants can affect the third trophic level. Cotton plants are known to produce alkaloids such as gossypol, a sesquiterpene aldehyde that can confer resistance against herbivorous arthropods. Nevertheless, little is known about the effect of gossypol on biological control agents. In this study, we investigated how three cotton cultivars (BRS Rubi, BRS Safira and BRS Verde) differing in gossypol content affect development and growth of predatory coccinellids, Eriopis connexa and Harmonia axyridis, feeding on the cotton aphid Aphis gossypii reared on those cultivars. The results show that the cultivar BRS Rubi (highest gossypol content) had a sub-lethal effect on the development and growth of both Coccinellidae species compared with the other cultivars. Overall, the cultivar BRS Rubi reduced slightly fecundity, net reproductive rate and intrinsic rate of natural increase for both Coccinellidae species. However, because aphid populations stay short periods of time in the field, and adult coccinellids may supplement its diet with alternative prey and plant material this sub-lethal indirect effect of gossypol may not have a detrimental effect on field biological control of cotton aphid by either E. connexa or H. axyridis, thus suggesting a compatibility between plant resistance and biological control agents.     

Trade-offs among anti-herbivore resistance traits: insights from Gossypieae (Malvaceae)

Plant defense theories commonly predict negative correlations among anti-herbivore resistance traits. Although this prediction has been widely accepted, the majority of empirical studies have failed to account for similarities among species due to common ancestry, thus risking pseudoreplication. Wild cotton plants possess traits conferring both direct resistance (toxic leaf glands and trichomes) and indirect resistance (extrafloral nectaries that reward enemies of herbivores). The evidence for negative phenotypic correlations among these resistance traits was examined at two levels: within Gossypium thurberi (wild cotton) and across species in the cotton clade (Gossypieae). A phylogenetic analysis controlled for shared ancestry among species. Across the Gossypieae, a strong negative correlation emerged between the direct resistance traits, leaf gland and trichomes. This correlation may reflect costs of these traits, a negative genetic correlation, or redundancy in their actions against herbivores. In contrast, the direct resistance traits (glands and trichomes) were not correlated with the indirect resistance trait of extrafloral nectar, either within or across species. The robust lack of correlation suggests that these direct and indirect resistance mechanisms evolve independently over evolutionary time scales. This conclusion conflicts with both predictions of plant defense theory and the majority of prior comparisons of direct and indirect resistance traits and may reflect the facultative nature of indirect resistance in Gossypieae.     

Indirect cost of a defensive trait: variation in trichome type affects the natural enemies of herbivorous insects on <Emphasis Type="Italic">Datura wrightii</Emphasis>

The costs and benefits of defensive traits in plants can have an ecological component that arises from the effect of defenses on the natural enemies of herbivores. We tested if glandular trichomes in Datura wrightii, a trait that confers resistance to several species of herbivorous insects, impose an ecological cost by decreasing rates of predation by the natural enemies of herbivores. For two common herbivores of D. wrightii, Lema daturaphila and Tupiocoris notatus, several generalized species of natural enemies exhibited lower rates of predation on glandular compared to non-glandular plants. Lower rates of predation were associated with reductions in the residence time and foraging efficiency of natural enemies on plants with glandular trichomes, but not with direct toxic effects of glandular exudate. Our results suggest that the benefit of resistance to herbivores conferred by glandular trichomes might be offset by the detrimental effect of this trait on the natural enemies of herbivores, and that the fitness consequences of this trichome defense might depend on the composition and abundance of the natural-enemy community.     

Decreased resistance and increased tolerance to native herbivores of the invasive plant Sapium sebiferum

Release from natural enemies may favor invasive plants evolving traits associated with reduced herbivore‐resistance and faster‐growth in introduced ranges. Given a genetic trade‐off between resistance and tolerance, invasive plants could also become more tolerant to herbivory than conspecifics in the native range. We conducted a field common garden study in the native range of Sapium sebiferum using seeds from native Chinese populations and invasive North American populations to compare their growth and herbivory resistance. We also performed a cage‐pot experiment to compare their resistance and tolerance to Bikasha collaris beetles that are specialist feeders on S. sebiferum trees in China. Results of the common garden study showed that Sapium seedlings of invasive populations relative to native populations were more frequently attacked by native herbivores. Growth and leaf damage were significantly higher for invasive populations than for native populations. Growth of invasive populations was not significantly affected by insecticide spray, but insecticide spray benefited that of native populations. In the bioassay trial, beetles preferentially consumed leaf tissue of invasive populations compared to native populations when beetles had a choice between them. Regression of percent leaf damage on biomass showed that invasive populations tolerated herbivory more effectively than native populations. Our results suggest that S. sebiferum from the introduced range had lower resistance but higher tolerance to specialist herbivores. Both defense strategies could have evolved as a response to the escape from natural enemies in the introduced range.     

The molecular bases of plant resistance and defense responses to aphid feeding: current status

Plant genes participating in the recognition of aphid herbivory in concert with plant genes involved in defense against herbivores mediate plant resistance to aphids. Several such genes involved in plant disease and nematode resistance have been characterized in detail, but their existence has only recently begun to be determined for arthropod resistance. Hundreds of different genes are typically involved and the disruption of plant cell wall tissues during aphid feeding has been shown to induce defense responses in Arabidopsis, Triticum, Sorghum, and Nicotiana species. Mi‐1.2, a tomato gene for resistance to the potato aphid, Macrosiphum euphorbiae (Thomas), is a member of the nucleotide‐binding site and leucine‐rich region Class II family of disease, nematode, and arthropod resistance genes. Recent studies into the differential expression of Pto‐ and Pti1‐like kinase genes in wheat plants resistant to the Russian wheat aphid, Diuraphis noxia (Mordvilko), provide evidence of the involvement of the Pto class of resistance genes in arthropod resistance. An analysis of available data suggests that aphid feeding may trigger multiple signaling pathways in plants. Early signaling includes gene‐for‐gene recognition and defense signaling in aphid‐resistant plants, and recognition of aphid‐inflicted cell damage in both resistant and susceptible plants. Furthermore, signaling is mediated by several compounds, including jasmonic acid, salicylic acid, ethylene, abscisic acid, giberellic acid, nitric oxide, and auxin. These signals lead to the development of direct chemical defenses against aphids and general stress‐related responses that are well characterized for a number of abiotic and biotic stresses. In spite of major plant taxonomic differences, similarities exist in the types of plant genes expressed in response to feeding by different species of aphids. However, numerous differences in plant signaling and defense responses unique to specific aphid–plant interactions have been identified and warrant further investigation.