Evolutionary history predicts plant defense against an invasive pest

It has long been hypothesized that invasive pests may be facilitated by the evolutionary naïveté of their new hosts, but this prediction has never been examined in a phylogenetic framework. To address the hypothesis, we have been studying the invasive viburnum leaf beetle (Pyrrhalta viburni), which is decimating North American native species of Viburnum, a clade of worldwide importance as understory shrubs and ornamentals. In a phylogenetic field experiment using 16 species of Viburnum, we show that old-world Viburnum species that evolved in the presence of Pyrrhalta beetles mount a massive defensive wound response that crushes eggs of the pest insect; in contrast, naïve North American species that share no evolutionary history with Pyrrhalta beetles show a markedly lower response. This convergent continental difference in the defensive response of Viburnum spp. against insect oviposition contrasts with little difference in the quality of leaves for beetle larvae. Females show strong oviposition preferences that correspond with larval performance regardless of continental origin, which has facilitated colonization of susceptible North American species. Thus, although much attention has been paid to escape from enemies as a factor in the establishment and spread of nonnative organisms, the colonization of undefended resources seems to play a major role in the success of invasive species such as the viburnum leaf beetleViburnum phylogenetic studies were supported by National Science Foundation Grant IOS-0842800 (to M.J.D.). This study was supported by US National Science Foundation Grant DEB-0950231 (to A.A.A.) and Federal Formula Funds allocated by the Cornell University Agricultural Experiment Station (to A.A.A.)

The Arabidopsis Pep-PEPR system is induced by herbivore feeding and contributes to JA-mediated plant defence against herbivory

Dysfunction of the Pep-PEPR system and its interplay with JA signalling results in increased plant susceptibility towards herbivore attack indicating that endogenous signalling also contributes to herbivore defenc

Do plant defenses predict damage by an invasive herbivore? A comparative study of the viburnum leaf beetle

The impact of plant defenses on insect herbivores is widely accepted, but their relative effects on oviposition choice, survival, and larval growth in preventing pest damage, especially for invasive insects, is not fully understood. Here, we examined the potential for plant defenses to reduce the economic and environmental impacts of an invasive herbivore, the viburnum leaf beetle, VLB (Pyrrhalta viburni), on Viburnum species in North America. We used a common garden with 15 host Viburnum species of North American, European, and Asian origin and evaluated oviposition preferences, twig defense against oviposition (a reaction that crushes VLB eggs), larval performance in the lab and field, and foliar damage to mature shrubs in two consecutive years. VLB oviposition preference was the strongest predictor of plant damage, with twig defense and larval performance explaining little of the defoliation patterns. In particular, we showed that VLB females evade key defenses by choosing poorly defended twigs for oviposition; assays on the 15 Viburnum species revealed that adults laid over four times more eggs on dead (undefended) twigs than on living twigs. We additionally tested the hypothesis that shrubs with a higher proportion of dead twigs are preferentially chosen for oviposition, leading to more defoliation by larvae and increased dieback in the following year. We term this the infestation feedback hypothesis. Indeed, we report consistent positive correlations between percentage dieback, oviposition, and percentage defoliation across Viburnum species, and among individuals within two species tested separately (V. dentatum and V. opulus). Our results demonstrate that oviposition preference plays a major role in the susceptibility of Viburnum shrubs to the invasive VLB through adults choosing high?quality species for their larvae (a strong preference–performance correlation) and avoiding well?defended twigs among preferred species. More generally, where invasive insects can avoid plant defenses and when preference and performance are positively correlated, an infestation feedback loop can lead to persistent pest problems. Because dieback weakens Viburnum defenses by providing optimal oviposition sites, we recommend that Viburnum growers mechanically remove dead twigs from susceptible shrubs at the end of the growing season, especially in the early stages of VLB colonization.This work was funded by NSF DEB?1118783 and federal formula funds from USDA (Hatch project NYC?183453) to A. A. Agrawal

Trans-generational inheritance of herbivory-induced phenotypic changes in Brassica rapa

Biotic stress can induce plastic changes in fitness-relevant plant traits. Recently, it has been shown that such changes can be transmitted to subsequent generations. However, the occurrence and extent of transmission across different types of traits is still unexplored. Here, we assessed the emergence and transmission of herbivory-induced changes in Brassica rapa and their impact on interactions with insects. We analysed changes in morphology and reproductive traits as well as in flower and leaf volatile emission during two generations with leaf herbivory by Mamestra brassicae and Pieris brassicae and two subsequent generations without herbivory. Herbivory induced changes in all trait types, increasing attractiveness of the plants to the parasitoid wasp Cotesia glomerata and decreasing visitation by the pollinator Bombus terrestris, a potential trade-off. While changes in floral and leaf volatiles disappeared in the first generation after herbivory, some changes in morphology and reproductive traits were still measurable two generations after herbivory. However, neither parasitoids nor pollinators further discriminated between groups with different past treatments. Our results suggest that transmission of herbivore-induced changes occurs preferentially in resource-limited traits connected to plant growth and reproduction. The lack of alterations in plant-insect interactions was likely due to the transient nature of volatile changes

Variation in performance and resistance to parasitism of Plutella xylostella populations

Two major ecological factors determine the fitness of an insect herbivore: the ability to overcome plant resistance strategies (bottom-up effects) and the ability to avoid or resist attack by natural enemies such as predators and parasitoids (top-down effects). In response to differences in selection pressure, variation may exist in host-plant adaptation and immunity against parasitism among populations of an insect herbivore. We investigated the variation in larval performance of six different Plutella xylostella populations originating from four continents when feeding on a native Dutch plant species, Brassica rapa. One of the used populations has successfully switched its host plant, and is now adapted to pea. In addition, we determined the resistance to attack by the endoparasitoid Diadegma semiclausum originating from the Netherlands (where it is also native) and measured parasitoid performance as a proxy for host resistance against parasitism. Pupal mortality, immature development times, and adult biomass of P. xylostella differed significantly across populations when feeding on the same host plant species. In addition, parasitism success differed in terms of parasitoid adult emergence and their biomass, but not their development times. Variation among natural populations of insects should be considered more when studying interactions between plants and insects up the food chain.</p

Floral odors can interfere with the foraging behavior of parasitoids searching for hosts

Plants produce distinct blends of volatile compounds that attract pollinators (floral odors) or natural enemies of insect herbivores (herbivore-induced plant volatiles). The admixture of these blends in the atmosphere may alter the attraction of insect mutualists and ultimately affect plant fitness. Here, using synthetic blends of Brassica rapa floral volatiles and real B. rapa flowers, we investigated how floral odors impact the foraging behavior of parasitoids. In an olfactometer setting, floral odors reduced the attractiveness of plants infested by herbivores to parasitoids by 43.5% and affected four out of five parasitoid species tested. Additionally, experiments with the parasitoid Cotesia glomerata revealed that the effects of floral odors are dose-dependent and that floral odors were less disruptive under wind tunnel conditions than under olfactometer conditions. Electroantennogram recordings showed that C. glomerata antennae do respond to floral compounds, but that floral compounds do not inhibit antennal responses to herbivore-induced leaf volatiles. In conclusion, floral odors can act as background pollutants decreasing the attractiveness of chemical blends used by natural enemies to locate their hosts. Under natural conditions, such interferences could affect the outcome of tritrophic interactions and may play an important role in the evolution of plant volatile signaling

Can Estivation Preferences Be Used to Develop Novel Management Tools against Invasive Mediterranean Snails?

Terrestrial snails that live in hot and dry climates have developed strategies to cope with high summer temperatures. Several species estivate during the warmest months of the years by resting on vertical supports, typically in groups. Understanding how snails choose their estivation sites and aggregate may lead to the development of new management tools in areas where these snails are invasive. Here, we investigated the preferences of four snail species for vertical supports varying in widths and heights under laboratory and field conditions, and tested whether the presence of conspecifics or snails of other species affected these preferences. The results show that the snails strongly preferred wider supports in laboratory dual-choice tests, and one species (Theba&nbsp;pisana) showed a consistent preference for taller supports as well. These results were confirmed in the field, where more snails were found on wider and taller supports 24 h after being placed in test quadrats. The percentage of snails found in groups on a support was strongly density-dependent. The presence of conspecifics or their mucus did not affect the choices of the snails, nor did the presence of snails of other species or their mucus. Taken together, these results could lead to the development of attractive supports that could be used to mass-capture snails in the field

The Gastropod Menace: Slugs on Brassica Plants Affect Caterpillar Survival Through Consumption and Interference With Parasitoid Attraction

Terrestrial molluscs and insect herbivores play a major role as plant consumers in a number of ecosystems, but their direct and indirect interactions have hardly been explored. The omnivorous nature of slugs makes them potential disrupters of predator-prey relationships, as a direct threat to small insects and through indirect, plant-mediated effects. Here, we examined the effects of the presence of two species of slugs, Arion rufus (native) and A. vulgaris (invasive) on the survivorship of young Pieris brassicae caterpillars when feeding on Brassica rapa plants, and on plant attractiveness to the main natural enemy of P. brassicae, the parasitoid Cotesia glomerata. In two separate predation experiments, caterpillar mortality was significantly higher on plants co-infested with A. rufus or A. vulgaris. Moreover, caterpillar mortality correlated positively with slug mass and leaf consumption by A. vulgaris. At the third trophic level, plants infested with slugs and plants co-infested with slugs and caterpillars were far less attractive to parasitoids than plants damaged by caterpillars only, independently of slug species. Chemical analyses confirmed that volatile emissions, which provide foraging cues for parasitoids, were strongly reduced in co-infested plants. Our study shows that the presence of slugs has the potential to affect insect populations, directly via consumptive effects, and indirectly via changes in plant volatiles that result in a reduced attraction of natural enemies. The fitness cost for P. brassicae imposed by increased mortality in presence of slugs may be counterbalanced by the benefit of escaping its parasitoid