Rieta Gols

Jasmonic Acid and Herbivory Differentially Induce Carnivore-Attracting Plant Volatiles in Lima Bean Plants

Lima bean plants respond to feeding damage of two-spotted spider mites (Tetranychus urticae) with the emission of a complex blend of volatiles that are products of several different biosynthetic pathways. These volatiles attract the carnivorous mite Phytoseiulus persimilis, a specialist predator of the spider mites that exterminates entire prey populations, and thus the volatiles contribute indirectly to plant defense. The volatile blend constitutes information to the carnivores, and blend composition is an important factor in this. Jasmonic acid (JA) is involved in the signal transduction of this induced defense. Application of JA through the petiole of Lima bean plants induces a volatile blend that is similar, but not identical, to that emitted by spider mite-infested plants. The induced volatiles originate from the lipoxygenase pathway, the shikimic acid pathway, and the isoprenoid pathway. Among the induced bean plant volatiles are nitriles and oximes. Of a total of 61 components, 10 are emitted at significantly different rates. Among these are the terpene (E)-4,8-dimethyl-1,3,7-nonatriene and the phenolic methyl salicylate, two compounds that are known to attract P. persimilis. A crucial test for comparing the effect of spider mite damage and JA application on volatile induction is the response of P. persimilis. The carnivore is attracted by volatiles from JA-treated plants. Moreover, even treatment of Lima bean plants with methyl jasmonate vapor made the plants attractive to the carnivorous mites. However, the predators prefer the volatiles from spider-mite-infested Lima bean plants over those from JA-treated plants. Thus, chemical as well as behavioral analyses demonstrate that spider mite damage and JA treatment have similar, although not identical, effects on volatile induction in Lima bean plants.

Plant Interactions with Multiple Insect Herbivores: From Community to Genes

Every plant is a member of a complex insect community that consists of tens to hundreds of species that belong to different trophic levels. The dynamics of this community are critically influenced by the plant, which mediates interactions between community members that can occur on the plant simultaneously or at different times. Herbivory results in changes in the plants morphological or chemical phenotype that affect interactions with subsequently arriving herbivores. Changes in the plants phenotype are mediated by molecular processes such as phytohormonal signaling networks and transcriptomic rearrangements that are initiated by oral secretions of the herbivore. Processes at different levels of biological complexity occur at timescales ranging from minutes to years. In this review, we address plant-mediated interactions with multiple species of the associated insect community and their effects on community dynamics, and link these to the mechanistic effects that multiple attacks have on plant phenotypes.

GENETIC VARIATION IN DEFENSE CHEMISTRY IN WILD CABBAGES AFFECTS HERBIVORES AND THEIR ENDOPARASITOIDS

Populations of wild Brassica oleracea L. grow naturally along the Atlantic coastlines of the United Kingdom and France. Over a very small spatial scale (i.e., <15 km) these populations differ in the expression of the defensive compounds, glucosinolates (GS). Thus far, very few studies have examined interactions between genetically distinct populations of a wild plant species and associated consumers in a multitrophic framework. Here, we compared the development of a specialist (Pieris rapae) and a generalist (Mamestra brassicae) insect herbivore and their endoparasitoids (Cotesia rubecula and Microplitis mediator, respectively) on three wild populations and one cultivar of B. oleracea under controlled greenhouse conditions. Herbivore performance was differentially affected by the plant population on which they were reared. Plant population influenced only development time and pupal mass in P. rapae, whereas plant population also had a dramatic effect on survival of M. brassicae. Prolonged development time in P. rapae corresponded with high levels of the indole GS, neoglucobrassicin, whereas reduced survival in M. brassicae coincided with high levels of the aliphatic GS, gluconapin and sinigrin. The difference between the two species can be explained by the fact that the specialist P. rapae is adapted to feed on plants containing GS and has evolved an effective detoxification system against aliphatic GS. The different B. oleracea populations also affected development of the endoparasitoids. Differences in food-plant quality for the hosts were reflected in adult size in C. rubecula and survival in M. mediator, and further showed that parasitoid performance is also affected by herbivore diet.

Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations.

Through artificial selection, domesticated plants often contain modified levels of primary and secondary metabolites compared to their wild progenitors. It is hypothesized that the changed chemistry of cultivated plants will affect the performance of insects associated with these plants. In this paper, the development of several specialist and generalist herbivores and their endoparasitoids were compared when reared on a wild and cultivated population of cabbage, Brassica oleracea, and a recently established feral Brassica species. Irrespective of insect species or the degree of dietary specialization, herbivores and parasitoids developed most poorly on the wild population. For the specialists, plant population influenced only development time and adult body mass, whereas for the generalists, plant populations also affected egg-to-adult survival. Two parasitoid species, a generalist (Diadegma fenestrale) and a specialist (D. semiclausum), were reared from the same host (Plutella xylostella). Performance of D. semiclausum was closely linked to that of its host, whereas the correlation between survival of D. fenestrale and host performance was less clear. Plants in the Brassicaceae characteristically produce defense-related glucosinolates (GS). Levels of GS in leaves of undamaged plants were significantly higher in plants from the wild population than from the domesticated populations. Moreover, total GS concentrations increased significantly in wild plants after herbivory, but not in domesticated or feral plants. The results of this study reveal that a cabbage cultivar and plants from a wild cabbage population exhibit significant differences in quality in terms of their effects on the growth and development of insect herbivores and their natural enemies. Although cultivated plants have proved to be model systems in agroecology, we argue that some caution should be applied to evolutionary explanations derived from studies on domesticated plants, unless some knowledge exists on the history of the system under investigation.

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

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

INDUCTION OF DIRECT AND INDIRECT PLANT RESPONSES BY JASMONIC ACID, LOW SPIDER MITE DENSITIES, OR A COMBINATION OF JASMONIC ACID TREATMENT AND SPIDER MITE INFESTATION

Jasmonic acid (JA) and the octadecanoid pathway are involved in both induced direct and induced indirect plant responses. In this study, the herbivorous mite, Tetranychus urticae, and its predator, Phytoseiulus persimilis, were given a choice between Lima bean plants induced by JA or spider mites and uninduced control plants. Infestation densities resulting in the induction of predator attractants were much lower than thus far assumed, i.e., predatory mites were significantly attracted to plants that were infested for 2 days with only one or four spider mites per plant. Phytoseiulus persimilis showed a density-dependent response to volatiles from plants that were infested with different numbers of spider mites. Similarly, treating plants with increasing concentrations of JA also led to increased attraction of P. persimilis. Moreover, the duration of spider mite infestation was positively correlated with the proportion of predators that were attracted to mite-infested plants. A pretreatment of the plants with JA followed by a spider mite infestation enhanced the attraction of P. persimilis to plant volatiles compared to attraction to volatiles from plants that were only infested with spider mites and did not receive a pretreatment with JA. The herbivore, T. urticae preferred leaf tissue that previously had been infested with conspecifics to uninfested leaf tissue. In the case of choice tests with JA-induced and control leaf tissue, spider mites slightly preferred control leaf tissue. When spider mites were given a choice between leaf discs induced by JA and leaf discs damaged by spider mite feeding, they preferred the latter. The presence of herbivore induced chemicals and/or spider mite products enhanced settlement of the mites, whereas treatment with JA seemed to impede settlement.

Development of the parasitoid, Cotesia rubecula (Hymenoptera: Braconidae) in Pieris rapae and Pieris brassicae (Lepidoptera: Pieridae): evidence for host regulation

Several recent models examining the developmental strategies of parasitoids attacking hosts which continue feeding and growing after parasitism (=koinobiont parasitoids) assume that host quality is a non-linear function of host size at oviposition. We tested this assumption by comparing the growth and development of males of the solitary koinobiont endoparasitoid, Cotesia rubecula, in first (L1) to third (L3) larval instars of its preferred host, Pieris rapae and in a less preferred host, Pieris brassicae. Beginning 3 days after parasitism, hosts were dissected daily, and both host and parasitoid dry mass was determined. Using data on parasitoid dry mass, we measured the mean relative growth rate of C. rubecula, and compared the trajectories of larval growth of the parasitoid during the larval and pupal stages using non-linear equations. Parasitoids generally survived better, completed development faster, and grew larger in earlier than in later instars of both host species, and adult wasps emerging from P. rapae were significantly larger than wasps emerging from all corresponding instars of P. brassicae. During their early larval stages, parasitoids grew most slowly in L1 P. rapae, whereas in all other host classes of both host species growth to pupation proceeded fairly uniformly. The growth of both host species was markedly reduced after parasitism compared with controls, with the development of P. brassicae arrested at an earlier stage, and at a smaller body mass, than P. rapae. Our results suggest that C. rubecula regulates certain biochemical processes more effectively in P. rapae than in P. brassicae, in accordance with its own nutritional and physiological requirements. Furthermore, we propose that, for parasitoids such as C. rubecula, which do not consume all host tissues prior to pupation, that parasitoid size and host quality may vary independently of host size at oviposition and at larval parasitoid egression.

Crop Domestication and Its Impact on Naturally Selected Trophic Interactions

Crop domestication is the process of artificially selecting plants to increase their suitability to human requirements: taste, yield, storage, and cultivation practices. There is increasing evidence that crop domestication can profoundly alter interactions among plants, herbivores, and their natural enemies. Overall, little is known about how these interactions are affected by domestication in the geographical ranges where these crops originate, where they are sympatric with the ancestral plant and share the associated arthropod community. In general, domestication consistently has reduced chemical resistance against herbivorous insects, improving herbivore and natural enemy performance on crop plants. More studies are needed to understand how changes in morphology and resistance-related traits arising from domestication may interact with environmental variation to affect species interactions across multiple scales in agroecosystems and natural ecosystems.

Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Hellén)

Differences in allelochemistry of plants may influence their ability to attract parasitoids.We studied responses of Diadegma semiclausum (Hellén), a parasitoid of the diamondback moth (Plutella xylostella L.), to inter- and intraspecific variation in odor blends of crucifers and a non-crucifer species. Uninfested Brussels sprout (Brassica oleracea L. gemmifera), white mustard (Sinapis alba L.), a feral Brassica oleracea, and malting barley (Hordeum vulgare L.) were compared for their attractivity to D. semiclausum in a Y-tube bioassay. Odors from all plants were more attractive to the parasitoid than clean air. However, tested against each other, parasitoids preferred the volatile blend from the three cruciferous species over that of malting barley.Wasps also discriminated between uninfested crucifers: mustard was as attractive as feral B. oleracea, and both were more attractive than Brussels sprout. Attractivity of uninfested plants was compared with that of plants infested by larvae of the host P. xylostella. Host-infested mustard and Brussels sprout were more attractive than uninfested conspecifics. Interestingly, the volatile blends of uninfested white mustard and infested Brussels sprout were equally attractive.We also compared the volatile composition of different plant sources by collecting headspace samples and analysing them with GC-MS. Similarities of volatile profiles were determined by hierarchic clustering and non-metric scaling based on the Horn-index. Due to the absence of several compounds in its blend, the volatile profile of barley showed dissimilarities from blends of crucifers. The odor profile of white mustard was distinctly different from the two Brassicaceae.Feral Brassica oleracea odor profile was different from infested Brussels sprout, but showed overlap with uninfested Brussels sprout. Odor blends from infested and uninfested Brussels sprout were similar, and mainly quantitative differences were found. D. semiclausum appears to discriminate based on subtle differences in volatile composition of odor blends from infested and uninfested plants.

Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism.

The mechanisms through which trophic interactions between species are indirectly mediated by distant members in a food web have received increasing attention in the field of ecology of multitrophic interactions. Scarcely studied aspects include the effects of varying plant chemistry on herbivore immune defences against parasitoids. We investigated the effects of constitutive and herbivore-induced variation in the nutritional quality of wild and cultivated populations of cabbage (Brassica oleracea) on the ability of small cabbage white Pieris rapae (Lepidoptera, Pieridae) larvae to encapsulate eggs of the parasitoid Cotesia glomerata (Hymenoptera, Braconidae). Average encapsulation rates in caterpillars parasitised as first instars were low and did not differ among plant populations, with caterpillar weight positively correlating with the rates of encapsulation. When caterpillars were parasitised as second instar larvae, encapsulation of eggs increased. Caterpillars were larger on the cultivated Brussels sprouts plants and exhibited higher levels of encapsulation compared with caterpillars on plants of either of the wild cabbage populations. Observed differences in encapsulation rates between plant populations could not be explained exclusively by differences in host growth on the different Brassica populations. Previous herbivore damage resulted in a reduction in the larval weight of subsequent herbivores with a concomitant reduction in encapsulation responses on both Brussels sprouts and wild cabbage plants. To our knowledge this is the first study demonstrating that constitutive and herbivore-induced changes in plant chemistry act in concert, affecting the immune response of herbivores to parasitism. We argue that plant-mediated immune responses of herbivores may be important in the evaluation of fitness costs and benefits of herbivore diet on the third trophic level.