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.

     

Solar ultraviolet-B radiation alters the attractiveness of Arabidopsis plants to diamondback moths (Plutella xylostella L.): impacts on oviposition and involvement of the jasmonic acid pathway

Solar ultraviolet-B radiation (UV-B) can have large impacts on the interactions between plants and herbivorous insects. Several studies have documented effects of UV-B-induced changes in plant tissue quality on the feeding performance of insect larvae. In contrast, the effects of UV-B-induced plant responses on the behavior of adult insects have received little attention. We carried out a series of field and glasshouse experiments using the model plant Arabidopsis thaliana L. and the crucifer-specialist insect Plutella xylostella L. (diamondback moth) to investigate the effects of UV-B on natural herbivory and plant–insect interactions. Natural herbivory under field conditions was less severe on plants exposed to ambient UV-B than on plants grown under filters that attenuated the UV-B component of solar radiation. This reduced herbivory could not be accounted for by effects of UV-B on larval feeding preference and performance, as P. xylostella caterpillars did not respond to changes in plant quality induced by UV-B. In contrast, at the adult stage, the insects presented clear behavioral responses: P. xylostella moths deposited significantly more eggs on plants grown under attenuated UV-B levels than on plants exposed to ambient UV-B. The deterring effect of UV-B exposure on insect oviposition was absent in jar1-1, a mutant with impaired jasmonic acid (JA) sensitivity, but it was conserved in mutants with altered ethylene signaling. The jar1-1 mutant also presented reduced levels of UV-absorbing phenolic compounds than the other genotypes that we tested. Our results suggest that variations in UV-B exposure under natural conditions can have significant effects on insect herbivory by altering plant traits that female adults use as sources of information during the process of host selection for oviposition. These effects of natural UV-B on plant quality appear to be mediated by activation of signaling circuits in which the defense-related hormone JA plays a functional role.     

Silicon‐mediated resistance against specialist insects in sap‐sucking and leaf‐chewing guilds in the Si non‐accumulator collard

Soil amendment with Silicon (Si) can increase plant resistance against insect herbivores, but the underlying mechanisms remain unclear. The mechanical resistance hypothesis (MRH) states that Si accumulated in epidermal cells directly and passively protects against herbivores by creating a mechanical barrier. The physiological resistance hypothesis (PRH) states that Si enhances resistance by activating plant biochemical and physiological processes. We tested both hypotheses by manipulating Si fertilization of the Si non‐accumulator collard, Brassica oleracea L. cv. acephala (Brassicaceae). Then, we assessed functional and ultrastructural plant responses and the developmental and reproductive performance of the leaf‐chewing larvae of the diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae), and the sap‐sucking cabbage aphid, Brevicoryne brassicae L. (Hemiptera: Aphididae). There was a 20% increase in leaf Si content. Silicon deposition in epidermal cells was identified by confocal microscopy and directly coincided with lower performance of P. xylostella, but did not affect B. brassicae. On the other hand, we found no unequivocal evidence that Si‐mediated changes in primary and secondary metabolism improved plant resistance against the insects. Negative mechanical effects of Si on the insects may have masked beneficial effects of increased water, nitrogen, and mineral contents in Si‐treated collards. Silicon did not change leaf contents of hemicellulose, cellulose, and lignin. Although Si‐mediated increases in leaf glucosinolates (GLS) correlated with lower larval performance and higher oviposition preference of P. xylostella, both P. xylostella and B. brassicae are highly specialized in overcoming such secondary metabolites. Thus, mechanical resistance may have impaired P. xylostella, rather than the Si‐mediated increase in GLS. We suggest that the PRH may depend on the degree of insect feeding specialization, so that toxic Si‐mediated defenses may be more efficient against unadapted polyphagous herbivores. For them, a toxic barrier may be added to the mechanical resistance.     

Finish line plant–insect interactions mediated by insect feeding mode and plant interference: a case study of Brassica interactions with diamondback moth and turnip aphid

There are gaps in our understanding of plant responses under different insect phytophagy modes and their subsequent effects on the insect herbivores’ performance at late season. Here we compared different types of insect feeding by an aphid, Lipaphis erysimi, and a lepidopteran, Plutella xylostella, and how this affected defensive metabolites in leaves of 2 Brassica species when plants gain maturity. Thiocyanate concentrations after P. xylostella and L. erysimi feeding activities were the same. Total phenolics was higher after the phloem feeder feeding than the folivore activity. The plants compensatory responses (i.e., tolerance) to L. erysimi feeding was significantly higher than the responses to P. xylostella. This study showed that L. erysimi had higher carbon than P. xylostella whereas nitrogen in P. xylostella was 1.42 times that in L. erysimi. Population size of the phloem feeder was not affected by plant species or insect coexistence. However, there was no correlation between plant defensive metabolites and both insects’ population size and biomass. This suggests that plant root biomass and tolerance index after different insect herbivory modes are not necessarily unidirectional. Importantly, the interaction between the folivore and the phloem feeder insects is asymmetric and the phloem feeder might be a trickier problem for plants than the folivore. Moreover, as both plants’ common and special defenses decreased under interspecific interference, we suggest that specialist insect herbivores can be more challenged in ecosystems in which plants are not involved in interspecific interference.     

An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores

A general prediction of the specialist/generalist paradigm indicates that plant responses to insect herbivores may depend on the degree of ecological specialization of the insect attacker. However, results from a single greenhouse experiment evaluating the responses of the model plant Arabidopsis thaliana to three specialist (Plutella xylostella, Pieris rapae, and Brevicoryne brassicae) and three generalist (Trichoplusia ni, Spodoptera exigua, and Myzus persicae) insect species did not support the previous prediction. Using an ecological genomic approach, we assessed plant responses in terms of herbivore-induced changes in genome-wide gene expression, defense-related pathways, and concentrations of glucosinolates (i.e., secondary metabolites that are ubiquitously present in cruciferous plants). Our results showed that plant responses were not influenced by the degree of specialization of insect herbivores. In contrast, responses were more strongly shaped by insect taxa (i.e., aphid vs. lepidopteran species), likely due to their different feeding modes. Interestingly, similar patterns of plant responses were induced by the same insect herbivore species in terms of defense signaling (jasmonic acid pathway), aliphatic glucosinolate metabolism (at both the gene expression and phenotypic levels) and genome-wide responses. Furthermore, plant responses to insect herbivores belonging to the same taxon (i.e., four lepidopteran species) were not explained by herbivore specialization or phylogenetic history. Overall, this study suggests that different feeding modes of insect taxa as well as herbivore-specific plant responses, which may result from distinct ecological/evolutionary interactions between A. thaliana (or a close relative) and each of the lepidopteran species, may explain why observed responses deviate from those predicted by the specialist/generalist paradigm.     

Response of Brassica oleracea to temporal variation in attack by two herbivores affects preference and performance of a third herbivore

1. Plants are frequently under attack by multiple insect herbivores, which may interact indirectly through herbivore‐induced changes in the plant's phenotype. The identity, order, and timing of herbivore arrivals may influence the outcome of interactions between two herbivores. How these aspects affect, in turn, subsequently arriving herbivores that feed on double herbivore‐induced plants has not been widely investigated. 2. This study tested whether the order and timing of arrival of two inducing herbivores from different feeding guilds affected the preference and performance of a subsequently arriving third herbivore, caterpillars of Mamestra brassicae L. (Lepidoptera: Noctuidae). Aphids [Brevicoryne brassicae L. (Hemiptera: Aphididae)] and caterpillars [Plutella xylostella L. (Lepidoptera: Yponomeutidae)] were introduced onto wild Brassica oleracea L. (Brassicaceae) plants in different sequences and with different arrival times. The effects of these plant treatments on M. brassicae caterpillars were assessed in pairwise preference tests and no‐choice performance tests. 3. The caterpillars of M. brassicae preferred to feed from undamaged plants rather than double herbivore‐induced plants. Compared with undamaged plants, they preferred plant material on which aphids had arrived first followed by caterpillars, whereas they avoided plant material with the reverse order of herbivore arrival. Performance of the caterpillars increased with increasing arrival time between herbivore infestations in double herbivore‐induced plants. Although M. brassicae grew faster on plants induced by aphids than on those induced by caterpillars alone, its performance was not affected by the order of previous herbivore arrival. 4. These results imply that the timing of colonisation by multiple herbivores determines the outcome of plant‐mediated herbivore–herbivore interactions.     

Can imitation companion planting interfere with host selection by Brassica pest insects?

• 1 Companion planting with nonhosts may offer a non‐insecticidal means of controlling pests, although the results of studies can be variable and species‐dependent.
• 2 The effect of companion planting on two pests of Brassica crops, Plutella xylostella (L.) and Brevicoryne brassicae (L.), was examined using Brussels sprout as the host plant and imitation cereal plants made from green plastic as the nonhost. For P. xylostella, the effect of nonhost density was also investigated.
• 3 Oviposition (P. xylostella) and abundance (B. brassicae) were lower on Brussels sprout plants presented on a background of high‐density imitation cereal plants (reductions of 59% and 85%, respectively).
• 4 The results are discussed in the context of host location by pest insects and the selection of nonhost companion plants for pest management.
• 5 It is concluded that nonhost plants interfere with pest host selection through disruption to visual host location processes.

     

Performance of specialist and generalist herbivores feeding on cabbage cultivars is not explained by glucosinolate profiles

Plants display a wide range of chemical defences that may differ in effectiveness against generalist and specialist insect herbivores. Host plant‐specific secondary chemicals such as glucosinolates (GS) in Brassicaceae typically reduce the performance of generalist herbivores, whereas specialists have adaptations to detoxify these compounds. The concentration of glucosinolates may also alter upon herbivory, allowing the plant to tailor its response to specifically affect the performance of the attacking herbivore. We studied the performance of three Lepidoptera species, two specialists [Pieris rapae L. (Pieridae), Plutella xylostella L. (Yponomeutidae)] and one generalist [Mamestra brassicae L. (Noctuidae)], when feeding on eight cultivars of Brassica oleracea L. and a native congener (Brassica nigra L.) and related this to the GS content. We tested the hypotheses (i) that a generalist herbivore is more affected by high GS concentrations, and (ii) that generalist feeding has a stronger effect on GS levels. Although performance of the three herbivores was different on the B. oleracea cultivars, M. brassicae and P. xylostella had a similar ranking order of performance on the eight cultivars. In most of the cultivars, the concentration of indole GS was significantly higher after feeding by P. rapae or M. brassicae than after P. xylostella feeding. As a consequence, the total concentration of GS in the cultivars showed a different ranking order for each herbivore species. The generalist M. brassicae performed equally well as the specialist P. xylostella on cultivars with high concentrations of GS. Our findings suggest that secondary metabolites other than GSs or differences in nutrient levels affect performance of the species studied.     

Insect eggs suppress plant defence against chewing herbivores

Plants activate direct and indirect defences in response to insect egg deposition. However, whether eggs can manipulate plant defence is unknown. In Arabidopsis thaliana, oviposition by the butterfly Pieris brassicae triggers cellular and molecular changes that are similar to the changes caused by biotrophic pathogens. In the present study, we found that the plant defence signal salicylic acid (SA) accumulates at the site of oviposition. This is unexpected, as the SA pathway controls defence against fungal and bacterial pathogens and negatively interacts with the jasmonic acid (JA) pathway, which is crucial for the defence against herbivores. Application of P. brassicae or Spodoptera littoralis egg extract onto leaves reduced the induction of insect‐responsive genes after challenge with caterpillars, suggesting that egg‐derived elicitors suppress plant defence. Consequently, larval growth of the generalist herbivore S. littoralis, but not of the specialist P. brassicae, was significantly higher on plants treated with egg extract than on control plants. In contrast, suppression of gene induction and enhanced S. littoralis performance were not seen in the SA‐deficient mutant sid2‐1, indicating that it is SA that mediates this phenomenon. These data reveal an intriguing facet of the cross‐talk between SA and JA signalling pathways, and suggest that insects have evolved a way to suppress the induction of defence genes by laying eggs that release elicitors. We show here that egg‐induced SA accumulation negatively interferes with the JA pathway, and provides an advantage for generalist herbivores.     

Differential effects of foliar endophytic fungi on insect herbivores attacking a herbaceous plant

Foliar endophytic fungi appear to be ubiquitous in nature, occurring in a very wide range of herbaceous plants. However, their ecological role within forbs is very poorly known and interactions with foliar-feeding insects virtually unexplored. In this study, leaves of Cirsium arvense were infected with different combinations of endophyte fungi that had been previously isolated from this plant species. Two months later, leaf material was fed to larvae of a generalist insect, Mamestra brassicae, and adults of a specialist feeder, Cassida rubiginosa. Endophytes had different effects on the two insects; one species, Chaetomium cochliodes, reduced growth of M. brassicae but increased feeding by C. rubiginosa. Another species, Cladosporium cladosporioides, increased beetle feeding also, but had no effect on M. brassicae. Interactions were also seen between fungal species and dual infection with C. cladosporioides and Trichoderma viride greatly reduced beetle feeding. It is concluded that endophytes have significant effects on foliar feeding insects that differ with degree of specialism of the herbivore. We suggest that these effects are due to chemical changes in the host, brought about by fungal infection. These fungi have received remarkably little attention in the study of insect–plant interactions and yet could be important determinants of insect growth and even population dynamics.     

Bottom‐up effects mediated by an organic soil amendment on the cabbage aphid pests Myzus persicae and Brevicoryne brassicae

Earthworm‐produced compost or vermicompost has been shown to increase resistance of plants to a variety of insect pests, but it is still unclear whether this resistance is dose dependent and whether the mechanisms responsible are the same for insect species with differing feeding habits and preferences. Therefore, we tested the effects of plants grown in various vermicompost concentrations (0, 20, 40, and 60%) on the preference and performance of generalist, Myzus persicae L., and specialist, Brevicoryne brassicae L. (both Hemiptera: Aphididae), aphid pests. Preference was evaluated with leaf disk (apterous) and whole plant (alate) choice assays. After 24 h of feeding, there was no significant negative effect on the feeding preference noted for apterae of either species of any of the treatments tested. To the contrary, apterae B. brassicae showed a significant preference for vermicompost treatments over control leaf disks. Alate M. persicae preferred alighting on control plants over vermicompost‐grown plants, but B. brassicae showed no preference toward any of the treatments tested. Both aphid species deposited significantly more nymphs on control plants than on those grown in 20% vermicompost. Furthermore, plants grown in soil amended with 20% vermicompost significantly suppressed mass accumulation, as well as numbers of adults and nymphs of both aphid species compared to controls. These data clearly show that vermicompost soil amendments can significantly influence pest aphid preference and performance on plants and that these effects are not dose dependent, but rather species and morph dependent.     

Influence of presence and spatial arrangement of belowground insects on host‐plant selection of aboveground insects: a field study

Abstract 1. Several studies have shown that above‐ and belowground insects can interact by influencing each others growth, development, and survival when they feed on the same host‐plant. In natural systems, however, insects can make choices on which plants to oviposit and feed. A field experiment was carried out to determine if root‐feeding insects can influence feeding and oviposition preferences and decisions of naturally colonising foliar‐feeding insects. 2. Using the wild cruciferous plant Brassica nigra and larvae of the cabbage root fly Delia radicum as the belowground root‐feeding insect, naturally colonising populations of foliar‐feeding insects were monitored over the course of a summer season. 3. Groups of root‐infested and root‐uninfested B. nigra plants were placed in a meadow during June, July, and August of 2006 for periods of 3 days. The root‐infested and the root‐uninfested plants were either dispersed evenly or placed in clusters. Once daily, all leaves of each plant were carefully inspected and insects were removed and collected for identification. 4. The flea beetles Phyllotreta spp. and the aphid Brevicoryne brassicae were significantly more abundant on root‐uninfested (control) than on root‐infested plants. However, for B. brassicae this was only apparent when the plants were placed in clusters. Host‐plant selection by the generalist aphid M. persicae and oviposition preference by the specialist butterfly P. rapae, however, were not significantly influenced by root herbivory. 5. The results of this study show that the presence of root‐feeding insects can affect feeding and oviposition preferences of foliar‐feeding insects, even under natural conditions where many other interactions occur simultaneously. The results suggest that root‐feeding insects play a role in the structuring of aboveground communities of insects, but these effects depend on the insect species as well as on the spatial distribution of the root‐feeding insects.     

Contrary effects of jasmonate treatment of two closely related plant species on attraction of and oviposition by a specialist herbivore

Elevated jasmonic acid (JA) concentrations in response to herbivory can induce wounded plants to produce defences against herbivores. In laboratory and field experiments we compared the effects of exogenous JA treatment to two closely related cabbage species on the host‐searching and oviposition preference of the diamondback moth (DBM), Plutella xylostella. JA‐treated Chinese cabbage (Brassica campestris) was less attractive than untreated Chinese cabbage to ovipositing DBM, while JA‐treatment of common cabbage (B. oleracea) made plants more attractive than untreated controls for oviposition by this insect. Similar effects were observed when plants of the two species were damaged by DBM larvae. In the absence of insect‐feeding, or JA application, Chinese cabbage is much more attractive to DBM than common cabbage. Inducible resistance therefore appears to occur in a more susceptible plant and induced susceptibility appears to occur in a more resistant plant, suggesting a possible balance mechanism between constitutive and inducible defences to a specialist herbivore.     

Influence of water stress on the glucosinolate profile of Brassica oleracea var. italica and the performance of Brevicoryne brassicae and Myzus persicae

Drought stress alters the chemical composition of plants, which can influence their tolerance to insect herbivory. To evaluate plant chemical responses to drought stress, broccoli, Brassica oleracea L. var. italica Plenck (Brassicaceae), was grown under well‐watered, drought, and water‐logged conditions. The glucosinolate (GS) levels and the performance of two aphid species, the specialist Brevicoryne brassicae (L.) and the generalist Myzus persicae (Sulzer) (both Hemiptera: Aphididae), in relation to water stress conditions were studied. High Performance Liquid Chromatography analysis showed that water stress changed the levels of GS in broccoli plants. Plants grown for 2 weeks under drought stress were significantly smaller and showed decreased levels of total GS when compared with GS contents of well‐watered plants, whereas water‐logged conditions led to a slight increase in the GS contents. A substantial decrease in indolyl GS was detected in water‐deficient plants, whereas aliphatic GS decreased slightly. Analysis of sugar levels in phloem sap of broccoli plants revealed that plants under water‐logged conditions contained the highest amounts of sugars followed by drought‐stressed and well‐watered plants. The two aphid species responded differently to water stress‐induced changes in their host plants. Significantly larger populations of M. persicae were recorded on plants with a limited water supply than on plants grown under well‐watered or water‐logged conditions. Brevicoryne brassicae was less affected by water stress, and similar population sizes were found on plants that were subject to different treatments. Analysis of covariance showed a significant effect of the plants’ water condition but no significant effect of GS content on the performance of M. persicae. However, the specialist B. brassicae remained unaffected by changes induced under water stress conditions.