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.)

Combined use of herbivore-induced plant volatiles and sex pheromones for mate location in braconid parasitoids

Herbivore-induced plant volatiles (HIPVs) are important cues for female parasitic wasps to find hosts. Here, we investigated the possibility that HIPVs may also serve parasitoids as cues to locate mates. To test this, the odour preferences of four braconid wasps – the gregarious parasitoid Cotesia glomerata (L.) and the solitary parasitoids Cotesia marginiventris (Cresson), Microplitis rufiventris Kokujev and Microplitis mediator (Haliday) – were studied in olfactometers. Each species showed attraction to pheromones but in somewhat different ways.Males of the two Cotesia species were attracted to virgin females, whereas females of M. rufiventriswere attracted to virginmales. Male and female M.mediator exhibited attraction to both sexes. Importantly, female and male wasps of all four species were strongly attracted by HIPVs, independent of mating status. In most cases, male wasps were also attracted to intact plants. The wasps preferred the combination of HIPVs and pheromones over plant odours alone, except M.mediator, which appears to mainly use HIPVs for mate location. We discuss the ecological contexts in which the combined use of pheromones and HIPVs by parasitoids can be expected. To our knowledge, this is the first study to show that braconid parasitoids use HIPVs and pheromones in combination to locate mates

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

Oviposition Of Viburnum Leaf Beetle [Pyrrhalta Viburni (Paykull)]: From Ecology To Biological Control Of An Emerging Landscape Pest

Pyrrhalta viburni (Coleoptera: Chrysomelidae), an invasive chrysomelid native to Eurasia, is a major pest of viburnums in the northeastern U.S. and southern Canada. P. viburni oviposition behavior was observed under laboratory and field conditions. The time cost of producing an egg mass was 135.3 + 6 min, chewing the egg cavity being the most time consuming part of the process. Choice-tests showed that females laid more eggs in twigs already infested by conspecifics than in non-infested twigs, and positioned their egg masses adjacent to existing ones. P. viburni oviposition behavior is therefore aggregative. An observational study showed that wound response, the main plant defense against P. viburni oviposition, decreased with increasing levels of egg infestation, suggesting a potential benefit of aggregative oviposition. A field study confirmed that there is a realized fitness benefit of aggregative oviposition on three host species: V. dentatum, V. opulus, and V. x bodnantense. Egg survivorship was higher on twigs with high and very high levels of infestation than on lightly or moderately infested twigs and wound response decreased with increasing levels of infestation. Twig mortality was positively correlated with level of infestation, and egg survivorship was higher on dead twigs than on living twigs. P. viburni oviposition on twigs that had died naturally occurred more frequently if the twigs had been infested the previous year, and the probability of new infestation was correlated with the number of old egg masses present in the twig. A study was conducted under quarantine conditions to determine the longevity and host specificity of Aprostocetus sp. (Hymenoptera: Eulophidae), a Eurasian egg parasitoid of P. viburni. Aprostocetus sp. females lived 53.8 days on average, the maximum longevity being 133 days. Aprostocetus sp. successfully parasitized the following non-target species: Galerucella nymphaea, G. pusilla/G. calmariensis, and Plagiometriona clavata (Coleoptera: Chrysomelidae). Due to its lack of host specificity, I think that the egg parasitoid Aprostocetus sp. should not be considered for introduction as a biological control agent against P. viburni in North America. The implications of this research for management of P. viburni in North America are discussed

Switched after Birth: Performance of the Viburnum Leaf Beetle [Pyrrhalta viburni (Paykull)] after Transfer to a Suboptimal Host Plant

Host plant switching is common among phytophagous insects. Once optimal food sources have been depleted, immature insects may resort to use of suboptimal hosts in order to complete their development. Such host switching may have dramatic consequences for insect fitness. Here we investigate the effects of host switching in larvae of the viburnum leaf beetle, Pyrrhalta viburni, an invasive landscape pest in North America. Specifically, we examine how transfer of 3rd instar larvae from the optimal host Viburnum dentatum to three suboptimal hosts (V. lentago, V. carlesii, and V sieboldii) affects larval development and survivorship to the adult stage. Larval survivorship, pupal weight, and adult weight were overall lower for P. viburni larvae that switched hosts, independently of the suboptimal host tested. This decrease in performance corresponds to a decreased feeding rate on suboptimal hosts. Subsequent choice tests showed that 3rd instar larvae become less choosy as they approach pupation, and discriminate less between optimal and suboptimal hosts past a certain weight threshold. In conclusion, P. viburni larvae are able to complete their development on suboptimal hosts, but host switching negatively impacts several fitness correlates. Mixed ornamental gardens containing both optimal and suboptimal Viburnum species may provide to outbreaking P. viburni populations opportunities to survive the depletion of their preferred food sources

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

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

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