Evolutionary and environmental effects on the geographical adaptation of herbivory resistance in native and introduced <Emphasis Type="Italic">Solidago altissima</Emphasis> populations

To understand rapid evolution in plant resistance to herbivory, it is critical to determine how the genetic correlation among resistances varies genetically and/or environmentally. We conducted a reciprocal transplant experiment of tall goldenrod, Solidago altissima with multiple replicates within the native range (USA) and the introduced range (Japan) to explore the differences in phenotypic traits of resistance to multiple herbivorous insects and their relationships between and within the countries. The Japanese plants were more resistant to the lace bug, Corythucha marmorata, which had recently invaded Japan, but were more susceptible to other herbivorous insects compared to the USA plants. An antagonistic relationship was found between plant resistances to lace bugs and other herbivorous insects in both USA and Japanese plants. In addition, this relationship was more obvious in gardens with a high level of foliage damage than in gardens with a low level of foliage damage by other herbivorous insects. An antagonistic relationship between resistances to aphids and lace bugs was also observed in USA gardens, but not in Japanese garden. These results suggest that the strength of constraints on the evolution of plant resistance due to genetic trade-offs may differ among biotic environments, including community structure of herbivorous insects. Therefore, differences in herbivorous insect communities between the native and introduced ranges can result in the rapid evolution of greater resistance in plants in the introduced range than in the native range.     

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.     

Different effects of two exotic herbivores on the pollinator-mediated effect of an exotic plant on a native plant

Exotic plants can affect native plants indirectly through various biotic interactions. However, combinations of the multiple indirect effects of exotic plants on native plants have been rarely evaluated. Herbivory can either positively or negatively influence plant–pollinator interactions. Here, we addressed whether the pollinator-mediated plant interaction between exotic and native plants is altered through the introduction of exotic herbivores by conducting a 2-year common garden experiment. We compared the effects of pollinator-mediated indirect effects of an exotic plant, Solidago altissima, on the co-flowering native plant Aster microcephalus in geographically different populations reflecting differences in insect herbivore communities. We found a positive effect of co-flowering S. altissima on pollinator visitation of A. microcephalus, which varied between gardens and years. The co-flowering S. altissima did not significantly affect the seed set of A. microcephalus in the first year but had a negative effect in the second year. The facilitative effect of S. altissima on A. microcephalus pollination was suggested to be negatively affected by an exotic aphid, while it was not significantly affected by an exotic lace bug. Our study suggests that the phenology and feeding guilds of the herbivores may be critical for predicting the effect of exotic plants on native plants through herbivore–pollinator interactions. Integrated effects between plant interactions via multiple species interactions under different abiotic and biotic environments are necessary to understand the impact of exotic plants under complex interactions in nature.     

Herbivore‐induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack

1. Plant responses to herbivore attack may have community‐wide effects on the composition of the plant‐associated insect community. Thereby, plant responses to an early‐season herbivore may have profound consequences for the amount and type of future attack. 2. Here we studied the effect of early‐season herbivory by caterpillars of Pieris rapae on the composition of the insect herbivore community on domesticated Brassica oleracea plants. We compared the effect of herbivory on two cultivars that differ in the degree of susceptibility to herbivores to analyse whether induced plant responses supersede differences caused by constitutive resistance. 3. Early‐season herbivory affected the herbivore community, having contrasting effects on different herbivore species, while these effects were similar on the two cultivars. Generalist insect herbivores avoided plants that had been induced, whereas these plants were colonised preferentially by specialist herbivores belonging to both leaf‐chewing and sap‐sucking guilds. 4. Our results show that community‐wide effects of early‐season herbivory may prevail over effects of constitutive plant resistance. Induced responses triggered by prior herbivory may lead to an increase in susceptibility to the dominant specialists in the herbivorous insect community. The outcome of the balance between contrasting responses of herbivorous community members to induced plants therefore determines whether induced plant responses result in enhanced plant resistance.     

Community‐wide impact of an exotic aphid on introduced tall goldenrod

1. The aphid Uroleucon nigrotuberculatum Olive, which is specialised to the tall goldenrod, Solidago altissima L., in its native range, has become a dominant species on the introduced tall goldenrod in Japan. How this exotic aphid influenced arthropod communities on the introduced tall goldenrod in aphid‐present (spring) and aphid‐absent (autumn) seasons was examined, using an aphid removal experiment. 2. In spring, aphid presence increased ant abundance because aphid honeydew attracted foraging ant workers. A significant negative correlation was found between the numbers of ants and herbivorous insects other than aphids on the aphid‐exposed plants, but no significant correlation was detected on the aphid‐free plants. Thus, the aphid presence was likely to decrease the abundance of co‐occurring herbivorous insects through removal behaviour of the aphid‐tending ants. There were no significant differences in plant traits between the aphid‐exposed and aphid‐free plants. 3. In autumn, the numbers of lateral shoots and leaves, and the leaf nitrogen content were increased in response to the aphid infestation in spring. Because of the improvement of plant traits by aphid feeding, the abundance of leaf chewers increased on aphid‐exposed plants. In contrast, the abundance of sap feeders decreased on the aphid‐exposed plants. In particular, the dominant scale insect among sap feeders, Parasaissetia nigra Nietner, decreased, followed by a decrease in the abundance of ants attending P. nigra. Thus, aphid feeding may have attenuated the negative impacts of the tending ants on leaf chewers. 4. Aphid presence did not change herbivore species richness but changed the relative density of dominant herbivores, resulting in community‐wide effects on co‐occurring herbivores through ant‐mediated indirect effects, and on temporally separated herbivores through plant‐ and ant‐mediated indirect effects. The aphid also altered predator community composition by increasing and decreasing the relative abundance of aphid‐tending ants in the spring and autumn, respectively.     

Feeding preferences of Melanoplus femurrubrum grasshoppers on native and exotic grasses: behavioral and molecular approaches

Generalist insect herbivores, such as grasshoppers, may either avoid feeding on exotic plants, potentially enabling these plants to become invasive in the introduced range, or insects may incorporate exotic plants into their diet, contributing to the biotic resistance of native communities and potentially preventing plant invasions. Accurate determination of insect diet preferences with regard to native and exotic plants can be challenging, but this information is critical for understanding the interaction between native herbivores and exotic plants, and ultimately the mechanisms underlying plant invasions. To address this, we combined behavioral and molecular approaches to accurately compare food consumption of the polyphagous red‐legged grasshopper, Melanoplus femurrubrum (De Geer) (Orthoptera: Acrididae), on native [Andropogon gerardii Vitman and Bouteloua curtipendula (Michx.) Torr.] and exotic, potentially invasive grasses [Miscanthus sinensis Andersson and Bothriochloa ischaemum (L.) Keng] (all Poaceae). We found that M. femurrubrum grasshoppers demonstrated strong feeding preferences toward exotic grasses in experiments with intact plants under both field and greenhouse conditions, but they showed no preference in experiments with clipped leaves. Additionally, we sampled the gut contents of M. femurrubrum collected in the field and identified the ingested plant species based on DNA sequences for the non‐coding region of the chloroplast trnL (UAA) gene. We found that exotic plants were prevalent in the gut contents of grasshoppers collected at study sites in Ohio and Maryland, USA. These results suggest that the generalist herbivore M. femurrubrum does not avoid feeding on exotic grasses with which they do not share coevolutionary history. In addition, by demonstrating greater food consumption of exotic plants, these grasshoppers potentially provide biotic resistance should these grasses escape cultivation and become invasive in the introduced range.     

Predicting the outcomes of a tri‐trophic interaction between an indigenous parasitoid and an exotic herbivorous pest and its host plants

Understanding the novel ecological interactions that result from biological invasions is a critical issue in modern ecology and evolution as well as pest management. Introduced herbivorous insects may interact with native plants and indigenous natural enemies, creating novel tri‐trophic interactions. To help predict the potential outcomes of novel interactions, we investigated the behavioural and physiological responses of an indigenous generalist parasitoid (Habrobracon gelechiae) to an introduced generalist herbivore (the light brown apple moth, Epiphyas postvittana) and its new host plants in California. We first examined the parasitoid's host location and acceptance on a range of nine common host plants of the moth representing distinctly different geographic origins and morphologies (to examine the effect of a known toxic plant on the parasitoid's performance, an additional toxic plant species was also tested that the moth consumes in the laboratory but does not naturally attack). The parasitoid was able to locate the host larvae on all plants equally well, although clutch size was affected by host plant. We then determined fitness of the moth and the parasitoid on four representative plants. The moth larvae suffered higher mortality and a slower developmental rate on the known toxic plant than on the other three plants, but the parasitoid's fitness correlates did not differ between the host food plants. These results show a high level of plasticity in the indigenous generalist parasitoid in its ability to exploit the exotic host on a wide range of host plants, generating an invasion‐driven novel tri‐trophic interaction.     

Proportion of exotics and relatedness of host species mediate the positive effect of plant richness on the species richness of fruit flies

1. All else being equal, the greater the local species richness of plants, the greater the number of associated herbivore species. Because most herbivore insects feed on a subset of closely related plant species, plant phylogenetic diversity is expected to play a key role in determining the number of herbivore species. What is not well known, however, is how an increase in the species richness of exotic plants affects the species richness of herbivores. 2. In this study, we used plant–fruit fly interactions to investigate the influence of the proportion and species richness of exotic host plants on the species richness of herbivorous insects. We also tested whether the phylogenetic diversity of host plants increases when the number of exotic plant species increases. 3. We found that the species richness of fruit flies is more accurately predicted by the richness of native host plants than by total plant species richness (including both native and exotic species). The proportion of exotic host species and the phylogenetic diversity of host plants had negative and positive effects, respectively, on the species richness of fruit flies. 4. Our findings suggest that a positive effect of plant richness on herbivore richness occurs only when an increase in plant diversity involves plant species with which native herbivores share some evolutionary history.     

Phytophagous insect fauna tracks host plant responses to exotic grass invasion

The high dependence of herbivorous insects on their host plants implies that plant invaders can affect these insects directly, by not providing a suitable habitat, or indirectly, by altering host plant availability. In this study, we sampled Asteraceae flower heads in cerrado remnants with varying levels of exotic grass invasion to evaluate whether invasive grasses have a direct effect on herbivore richness independent of the current disturbance level and host plant richness. By classifying herbivores according to the degree of host plant specialization, we also investigated whether invasive grasses reduce the uniqueness of the herbivorous assemblages. Herbivorous insect richness showed a unimodal relationship with invasive grass cover that was significantly explained only by way of the variation in host plant richness. The same result was found for polyphagous and oligophagous insects, but monophages showed a significant negative response to the intensity of the grass invasion that was independent of host plant richness. Our findings lend support to the hypothesis that the aggregate effect of invasive plants on herbivores tends to mirror the effects of invasive plants on host plants. In addition, exotic plants affect specialist insects differently from generalist insects; thus exotic plants affect not only the size but also the structural profile of herbivorous insect assemblages.     

Non‐pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid‐induced plant volatiles via jasmonic acid signalling

Beneficial soil‐borne microbes, such as mycorrhizal fungi or rhizobacteria, can affect the interactions of plants with aboveground insects at several trophic levels. While the mechanisms of interactions with herbivorous insects, that is, the second trophic level, are starting to be understood, it remains unknown how plants mediate the interactions between soil microbes and carnivorous insects, that is, the third trophic level. Using Arabidopsis thaliana Col‐0 and the aphid Myzus persicae, we evaluate here the underlying mechanisms involved in the plant‐mediated interaction between the non‐pathogenic rhizobacterium Pseudomonas fluorescens and the parasitoid Diaeretiella rapae, by combining ecological, chemical and molecular approaches. Rhizobacterial colonization modifies the composition of the blend of herbivore‐induced plant volatiles. The volatile blend from rhizobacteria‐treated aphid‐infested plants is less attractive to an aphid parasitoid, in terms of both olfactory preference behaviour and oviposition, than the volatile blend from aphid‐infested plants without rhizobacteria. Importantly, the effect of rhizobacteria on both the emission of herbivore‐induced volatiles and parasitoid response to aphid‐infested plants is lost in an Arabidopsis mutant (aos/dde2‐2) that is impaired in jasmonic acid production. By modifying the blend of herbivore‐induced plant volatiles that depend on the jasmonic acid‐signalling pathway, root‐colonizing microbes interfere with the attraction of parasitoids of leaf herbivores.     

Experimental assemblage of novel plant–herbivore interactions: ecological host shifts after 40 million years of isolation

Geographic isolation is the first step in insect herbivore diet specialization. Such specialization is postulated to increase insect fitness, but may simultaneously reduce insect ability to colonize novel hosts. During the Paleocene‐Eocene, plants from the order Zingiberales became isolated either in the Paleotropics or in the Neotropics. During the Cretaceous, rolled‐leaf beetles diversified in the Neotropics concurrently with Neotropical Zingiberales. Using a community of Costa Rican rolled‐leaf beetles and their Zingiberales host plants as study system, we explored if previous geographic isolation precludes insects to expand their diets to exotic hosts. We recorded interactions between rolled‐leaf beetles and native Zingiberales by combining DNA barcodes and field records for 7450 beetles feeding on 3202 host plants. To determine phylogenetic patterns of diet expansions, we established 20 experimental plots in the field, in which we planted plots five exotic Zingiberales, recording beetles feeding on these exotic hosts. In the laboratory, using both native and exotic host plants, we reared a subset of insect species that had expanded their diets to the exotic plants. The original plant–herbivore community comprised 24 beetle species feeding on 35 native hosts, representing 103 plant–herbivore interactions. After exotic host plant introduction, 20 percent of the beetle species expanded their diets to exotic Zingiberales. Insects only established on exotic hosts that belong to the same plant family as their native hosts. Laboratory experiments show that beetles are able to complete development on these novel hosts. In conclusion, rolled‐leaf beetles are preadapted to expand their diets to novel host plants even after millions of years of geographic isolation.     

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.     

Plant‐mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage

• Plants are part of biodiverse communities and frequently suffer from attack by multiple herbivorous insects. Plant responses to these herbivores are specific for insect feeding guilds: aphids and caterpillars induce different plant phenotypes. Moreover, plants respond differentially to single or dual herbivory, which may cascade into a chain of interactions in terms of resistance to other community members. Whether differential responses to single or dual herbivory have consequences for plant resistance to yet a third herbivore is unknown.
• We assessed the effects of single or dual herbivory by Brevicoryne brassicae aphids and/or Plutella xylostella caterpillars on resistance of plants from three natural populations of wild cabbage to feeding by caterpillars of Mamestra brassicae. We measured plant gene expression and phytohormone concentrations to illustrate mechanisms involved in induced responses.
• Performance of both B. brassicae and P. xylostella was reduced when feeding simultaneously with the other herbivore, compared to feeding alone. Gene expression and phytohormone concentrations in plants exposed to dual herbivory were different from those found in plants exposed to herbivory by either insect alone. Plants previously induced by both P. xylostella and B. brassicae negatively affected growth of the subsequently arriving M. brassicae. Furthermore, induced responses varied between wild cabbage populations.
• Feeding by multiple herbivores differentially activates plant defences, which has plant‐mediated negative consequences for a subsequently arriving herbivore. Plant population‐specific responses suggest that plant populations adapt to the specific communities of insect herbivores. Our study contributes to the understanding of plant defence plasticity in response to multiple insect attacks.

     

虫害诱导植物间接防御反应的激发与信号转导途径

植物通过产生和释放挥发性物质增加植食性昆虫的天敌对其寄主或猎物的定位,减少植食性昆虫对植物的取食,从而达到间接防御的目的。植物对植食性昆虫所做出间接防御反应激发因子和信号转导途径的研究,对应用虫害诱导植物挥发物引诱害虫天敌,并进一步从植物、植食性昆虫及其天敌间三级营养关系,研究动植物协同进化机理和病虫害防治具有深远意义。本文根据国内外最新研究进展,对虫害诱导植物间接防御反应的激发因子,昆虫取食信号的转导途径及对植物间接防御相关基因的激活等方面进行了系统地综述。     

Urban landscape and forest vegetation regulate the range expansion of an exotic lace bug Corythucha marmorata (Hemiptera: Tingidae)

Landscapes and vegetation are critical factors in dispersion of exotic insects and expansion of their range. However, few studies have addressed how the surrounding landscape affects the establishment of exotic insects. We assessed the relationship between establishment of an exotic lace bug Corythucha marmorata (Uhler) and the surrounding landscape in the northern edge of the lace bug's expanded range. We found that the lace bugs showed variability in their density among populations. Urban areas had a positive effect, while the natural forest vegetation had a negative effect on lace bug density, with a buffer range of 1–2 km. Moreover, their abundance decreased with distance from the source population. Our results suggest that natural forest landscapes in urban areas may inhibit the range expansion of invasive insects that feed on exotic plants growing in human‐disturbed habitats.     

硅对植物抗虫性的影响及其机制

硅不是植物必需营养元素,但硅在提高植物对一系列非生物和生物胁迫的抗性方面都具有重要作用。综述了硅对植物抗虫性的影响及其机制。在多数植物中,增施硅肥可增强其抗虫性;所增强的抗性与硅肥种类和施用方式之间存在关系。植物组织中沉积的硅可增加其硬度和耐磨度,降低植物可消化性,从而增强植物组成性防御,包括延缓昆虫生长发育、降低繁殖力、减轻植物受害程度;植物体内的硅含量以及硅沉积的位点和排列方式影响组成性防御作用的强度。此外,硅可以调节植物诱导性防御,包括直接防御和间接防御,直接防御涉及增加有毒物质含量、产生局部过敏反应或系统获得抗性、产生有毒化合物和防御蛋白,从而延缓昆虫发育;间接防御主要通过释放挥发性化合物吸引植食性昆虫的捕食性和寄生性天敌而导致植食性昆虫种群下降。     

Gone with the wind: trembling leaves may deter herbivory

Plants employ various defensive tactics against herbivores but are rarely considered to use rapid movements to resist predation. However, the aboveground parts of plants are often forcefully moved by wind and rain. This passive movement has been overlooked as an anti‐herbivore trait. The leaves of many plant species, such as aspens, Indian sacred fig, bamboos, and palms, tremble even in a slight breeze. Leaves that are easily moved by gentle winds can sometimes resist strong winds and may have other benefits as well. In the present study, it is proposed that the movement of such plant leaves physically deters arthropod herbivory and pathogen infection by repelling colonization and oviposition by herbivorous insects. This leads to herbivores and pathogens being dislodged from the plants, and the ensuing death of the herbivores on the ground or at least their recolonization to other plants, as well as the interruption of feeding, intraspecific communication and the mating behaviour of herbivores, thus lowering their performance on the plant or increasing enemy attack of the herbivores. In addition, passive leaf movements may undermine herbivore camouflage and expose them to predation, and may also allow plant volatiles to diffuse efficiently to repel herbivores and attract natural enemies. Thus, the mechanistic properties of these leaves may have anti‐herbivore effects in the wind and rain. This hypothesis can also be applied to aquatic plants that tremble in gentle water currents. In addition, genetic manipulation of the tendency for leaf movement may be beneficial for the management of pest insects and pathogens with reduced pesticides in forestry and agriculture. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 738–747.     

Performance of Danaini larvae is affected by both exotic host plants and abiotic conditions

The consequences of the introduction of invasive plants for the diet of herbivorous insects have been little explored in nature where, potentially, abiotic and biotic factors operate. In this study, we examined the larval performance of two Neotropical Danaini butterflies when using either a native or an exotic Apocynaceae species as host plant in both field and laboratory experiments. Hosts greatly differ in their amount of latex exudation and other physicochemical traits, as well as in the amount of evolutionary time they have interacted with herbivores. First, herbivore performance on the hosts was investigated under laboratory conditions. Larvae of both Danaini species took more time to develop on the exotic host; larval survivorship did not vary between hosts. Second, first instar survivorship on both hosts was evaluated in two field sites, one site per host. To do so, in both sites half of the larvae were bagged (protected against both abiotic and biotic factors) while the remainder were nonbagged (exposed). The interaction between larval exposure with the use of the exotic host reduced larval survival. We concluded that the combined effects of host plant traits and abiotic factors reduced survival of herbivores in field conditions. Therefore, the performance of herbivores when using hosts of different origins should be considered together with the multiple ecological factors found in natural environments, as these factors can modify the result of plant–herbivore interactions.     

An experimental test of the evolution of increased competitive ability hypothesis in goldenrod, <Emphasis Type="Italic">Solidago gigantea</Emphasis>

The mechanisms that allow introduced plants to become invasive are poorly understood. Here, we present a test of the evolution of increased competitive ability hypothesis, which holds that because specialized natural enemies may be absent from the introduced range, exotic plants may evolve to invest less in anti-herbivore defenses and thereby gain a competitive advantage over native plants. We grew Solidago gigantea plants derived from both the native range (North America) and the invasive range (Europe) in a common garden in the native range for 2 years. Half the plants were treated with insecticide to protect them from insect herbivores and the other half were exposed to insects that colonized the garden from nearby fields. Insect herbivore biomass was significantly higher on European plants than US plants in the first year but not the second. European plants were more heavily attacked by pathogens in both years of the study. When exposed to insect herbivores, US plants produced more seed than European plants, but when plants were protected from herbivores, seed production was equivalent between US plants and European plants. The presence of insect herbivores suppressed seed production of European plants much more than that of US plants, even though the level of herbivory experienced by European and US plants was similar in the second year, suggesting that the ability to tolerate herbivory was diminished in European plants. These results partially support the EICA hypothesis: plants from the introduced range were more susceptible to some natural enemies and benefited more from insect removal than plants from the native range. The prediction that European plants would perform better than US plants in the absence of insect herbivores was not supported. Electronic Supplementary Material Supplementary material is available for this article at     

Effects of biodiversity in agricultural landscapes on the protective microbiome of insects – a review

Symbiotic bacteria in herbivorous insects can have strong beneficial impacts on their host's survival, including conferring resistance to natural enemies such as parasitoid wasps or pathogens, while also imposing energetic costs on the host, resulting in cost‐benefit trade‐offs. Whether these trade‐offs favour the hosting of symbionts depends on the growth environment of the herbivore. Long‐term experimental grassland studies have shown that increasing plant species richness leads to an increased diversity of associated herbivores and their natural enemies. Such a change in natural enemy diversity, related to changes in plant diversity, could also drive changes in the community of symbionts hosted by the herbivorous insects. Aphids are one model system for studying symbionts in insects, and effects of host‐plant species and diversity on aphid‐symbiont interactions have been documented. Yet, we still understand little of the mechanisms underlying such effects. We review the current state of knowledge of how biodiversity can impact aphid‐symbiont communities and the underlying drivers. Then, we discuss this in the framework of sustainable agriculture, where increased plant biodiversity, in the form of wildflower strips, is used to recruit natural enemies to crop fields for their pest control services. Although aphid symbionts have the potential to reduce biological control effectiveness through conferring protection for the host insect, we discuss how increasing plant and natural enemy biodiversity can mitigate these effects and identify future research opportunities. Understanding how to promote beneficial interactions in ecological systems can help in the development of more sustainable agricultural management strategies.