Herbivory and jasmonate treatment affect reproductive traits in wild Lima bean, but without transgenerational effects.

PREMISE: Plant responses to herbivores and their elicitors include changes in traits associated with phenology, defense, and reproduction. Induced responses by chewing herbivores are known to be hormonally mediated by the jasmonate pathway and can cascade and affect late-season seed predators and pollinators. Moreover, herbivore-induced plant responses can be transmitted to the next generation. Whether herbivore-induced transgenerational effects also apply to phenological traits is less well understood. METHODS: Here, we explored responses of wild lima bean plants (Phaseolus lunatus) to herbivory and jasmonate treatment and possible transgenerational effects of herbivore-induced early flowering. In a controlled field experiment, we exposed lima bean plants to herbivory by leaf beetles or methyl jasmonate sprays (MJ). We then compared plant development, phenology, reproductive fitness and seed traits among these treatments and undamaged, untreated control plants. RESULTS: We found that MJ and leaf herbivory induced similar responses, with treated plants growing less, flowering earlier, and producing fewer seeds than undamaged plants. However, seed size, phenolics and cyanogenic glycosides concentrations did not differ among treatments. Seed germination rates and flowering time of the offspring were similar among maternal treatments. CONCLUSIONS: Overall, the results confirm that responses of lima bean to herbivory by leaf beetles are mediated by jasmonate; however, effects on phenological traits are not transmitted to the next generation. We discuss why transgenerational effects of herbivory might be restricted to traits that directly target herbivores.

Interpreting Temporal and Spatial Variation in Spotted-Wing Drosophila (Diptera: Drosophilidae) Trap Captures in Highbush Blueberries.

Integrated pest management (IPM) programs for the spotted-wing drosophila Drosophila suzukii (Diptera: Drosophilidae) rely on insecticide applications to reduce adult populations and prevent fruit infestation. Although monitoring traps are used for early D. suzukii adult detection to time the start of insecticide applications, it remains unclear whether trap counts can be used to determine the efficacy of these programs and predict the risk of fruit infestation. To address this, a 2-yr study (2016-2017) was conducted in highbush blueberries in New Jersey (USA) to interpret D. suzukii trap count variation in relation to the frequency of insecticide applications and proximity to forest habitats. We also correlated trap counts with fruit infestation and used traps to determine the maximum dispersive distance traveled by D. suzukii adults within blueberry fields by using mark-release-capture studies. Using a trapping network across nine farms, we demonstrated that insecticide applications reduce D. suzukii trap counts, but this varied according to seasonality, and that traps placed closer to forest habitats within farms had higher fly counts than those placed in farm interiors. Moreover, blueberry fields that had zero fruit infestation also had predictably lower trap counts than fields with infested fruit, and the maximum dispersive distance for D. suzukii within blueberry fields was 90 m. In summary, while D. suzukii trap counts in blueberry farms could predict the frequency of insecticide applications and fruit infestation, the predictive power of our trap data was too variable across the blueberry harvest period to make it a reliable tool.

Laboratory and Field Evaluation of Host-Related Foraging Odor-Cue Combinations to Attract Drosophila suzukii (Diptera: Drosophilidae).

The invasive spotted-wing drosophila, Drosophila suzukii (Matsumura), is a major pest of soft-skinned fruits. Since its introduction into North America and Europe, significant progress has been made in understanding the volatile cues used by this fly during food, oviposition site, and mate finding. Despite this progress, commercially available lures are non-selective. Here, we tested two Hanseniaspora uvarum (Niehaus) yeast compounds (isoamyl acetate and isobutyl acetate) and a leaf compound ß-cyclocitral alone and in combination with a blend of four fermentation compounds ('Fermentation lure': acetic acid, ethanol, methionol, and acetoin) to improve D. suzukii attraction and selectivity. In laboratory assays, males and females were attracted to all seven individual compounds, although in electrophysiological assays, their antennae exhibited a dose-dependent response to only four of these compounds. In two-choice cage studies, the Fermentation lure was more attractive to D. suzukii than water controls, whereas ß-cyclocitral and the mixture of isoamyl acetate and isobutyl acetate were not attractive in this larger-cage study. Moreover, adding the two-component H. uvarum compound blend to the Fermentation lure reduced D. suzukii attraction to the Fermentation blend. When these experiments were repeated in blueberry, raspberry, blackberry, and cherry orchards across several states in the United States over 2 yr, similar outcomes were observed: ß-cyclocitral or the mixture of the H. uvarum blend did not improve the attractiveness of the Fermentation lure or its selectivity. This study demonstrates that cues from different sources may interfere with each other and reduce D. suzukii attraction to otherwise attractive odor combinations.

Changes in plant growth and seed production in wild lima bean in response to herbivory are attenuated by parasitoids.

Lima bean plants (Phaseolus lunatus) exhibit compensatory growth responses to herbivory. Among the various factors that have been identified to affect plant compensatory growth are the extent and type of tissue damage, the herbivore's feeding mode and the time of damage. Another factor that can greatly impact plant responses to herbivory, but has been largely ignored in previous studies, is the action of parasitoids. In most cases, parasitoids halt or slow down the development of herbivorous hosts, which, can result in decreased leaf damage, thereby affecting plant responses and ultimately plant fitness. Here, we investigated the effects of two koinobiont parasitoids on the amount of leaf damage inflicted by the Southern armyworm Spodoptera latifascia to wild lima bean, and the consequences of this for plant growth and seed production in the field. We specifically tested the hypothesis that the action of parasitoids will reduce plant damage and that this reduction will alter plant growth responses and seed production. Indeed, we found that in the presence of parasitoids plants suffered less damage than plants with only herbivores. As a consequence, compensatory growth was reduced and more and heavier seeds were produced earlier in the season, compared to plants exposed to only herbivores.

Tempo-Spatial Dynamics of Adult Plum Curculio (Coleoptera: Curculionidae) Based on Semiochemical-Baited Trap Captures in Blueberries.

Plum curculio, Conotrachelus nenuphar (Herbst), has become an important pest of highbush blueberries in the northeastern United States. Here, we conducted experiments in 2010-2013 to compare the efficacy of semiochemical-baited traps for C. nenuphar versus conventional (beating cloth) sampling methods in blueberries, and to understand the seasonal abundance and distribution of C. nenuphar adults within and among blueberry fields using these traps. Black pyramid traps baited with the C. nenuphar aggregation pheromone grandisoic acid and the fruit volatile benzaldehyde caught three to four times more adults than unbaited traps without causing an increase in injury to berries in neighboring bushes. Numbers of adult weevils caught in traps correlated with those on bushes (beating cloth samples), indicating that trap counts can predict C. nenuphar abundance in the field. Early in the season, traps placed 20 m from field edges near a forest caught higher C. nenuphar numbers than traps placed at farther distances, suggesting movement of overwintered weevils from outside fields. Using a trapping network across multiple fields in an organic farm, we found evidence of C. nenuphar aggregation in "hotspots"; early in the season, C. nenuphar numbers in traps were higher in the middle of fields, and there was a correlation between these numbers and distance from the forest in 2013 but not in 2012. These results show that semiochemical-baited traps are effective in capturing C. nenuphar adults in blueberries, and that these traps should be placed in the interior of fields preferably, but not exclusively, near wooded habitats to maximize their efficacy.

Effects of plant intraspecific diversity across three trophic levels: Underlying mechanisms and plant traits.

PREMISE OF STUDY: Although there is increasing recognition of the effects of plant intraspecific diversity on consumers, the mechanisms by which such effects cascade-up to higher trophic levels remain elusive. METHODS: We evaluated the effects of plant (lima bean, Phaseolus lunatus) intraspecific diversity on a suite of insect herbivores (leaf-chewers, aphids, and seed-eating beetles) and their third trophic-level associates (parasitoids and aphid-tending ants). We established plots of three plants, classified as monocultures of one population source or polycultures with mixtures of three of the four population sources (N = 16 plots per level of diversity). Within each plot, plants were individually placed in pots and canopy contact was prevented, therefore eliminating diversity effects on consumers arising from changes in plant traits due to plant physical interactions. KEY RESULTS: Plant diversity reduced damage by leaf-chewers as well as aphid abundance, and the latter effect in turn reduced ant abundance. In contrast, plant diversity increased the abundance of seed-eating beetles, but did not influence their associated parasitoids. There were no effects of diversity on seed traits potentially associated with seed predation, suggesting that differences in early season herbivory between monocultures and polycultures (a likely mechanism of diversity effects on plants since plant interactions were prevented) did not drive concomitant changes in plant traits. CONCLUSIONS: This study emphasizes that effects of plant intraspecific diversity on consumers are contingent upon differences in associate responses within and among higher trophic levels and suggests possible mechanisms by which such effects propagate up this food web.

Natural selection drives chemical resistance of Datura stramonium.

Plant resistance to herbivores involves physical and chemical plant traits that prevent or diminish damage by herbivores, and hence may promote coevolutionary arm-races between interacting species. Although Datura stramonium's concentration of tropane alkaloids is under selection by leaf beetles, it is not known whether chemical defense reduces seed predation by the specialist weevil, Trichobaris soror, and if it is evolving by natural selection. We measured infestation by T. soror as well as the concentration of the plants' two main tropane alkaloids in 278 D. stramonium plants belonging to 31 populations in central Mexico. We assessed whether the seed predator exerted preferences on the levels of both alkaloids and whether they affect plant fitness. Results show great variation across populations in the concentration of scopolamine and atropine in both leaves and seeds of plants of D. stramonium, as well as in the intensity of infestation and the proportion of infested fruits by T. soror. The concentration of scopolamine in seeds and leaves are negatively associated across populations. We found that scopolamine concentration increases plant fitness. Our major finding was the detection of a positive relationship between the population average concentrations of scopolamine with the selection differentials of scopolamine. Such spatial variation in the direction and intensity of selection on scopolamine may represent a coevolutionary selective mosaic. Our results support the view that variation in the concentration of scopolamine among-populations of D. stramonium in central Mexico is being driven, in part, by selection exerted by T. soror, pointing an adaptive role of tropane alkaloids in this plant species.

Adaptive divergence in resistance to herbivores in Datura stramonium.

Defensive traits exhibited by plants vary widely across populations. Heritable phenotypic differentiation is likely to be produced by genetic drift and spatially restricted gene flow between populations. However, spatially variable selection exerted by herbivores may also give rise to differences among populations. To explore to what extent these factors promote the among-population differentiation of plant resistance of 13 populations of Datura stramonium, we compared the degree of phenotypic differentiation (P ST) of leaf resistance traits (trichome density, atropine and scopolamine concentration) against neutral genetic differentiation (F ST) at microsatellite loci. Results showed that phenotypic differentiation in defensive traits among-population is not consistent with divergence promoted by genetic drift and restricted gene flow alone. Phenotypic differentiation in scopolamine concentration was significantly higher than F ST across the range of trait heritability values. In contrast, genetic differentiation in trichome density was different from F ST only when heritability was very low. On the other hand, differentiation in atropine concentration differed from the neutral expectation when heritability was less than or equal to 0.3. In addition, we did not find a significant correlation between pair-wise neutral genetic distances and distances of phenotypic resistance traits. Our findings reinforce previous evidence that divergent natural selection exerted by herbivores has promoted the among-population phenotypic differentiation of defensive traits in D. stramonium.

Specificity of induced defenses, growth, and reproduction in lima bean (Phaseolus lunatus) in response to multispecies herbivory.

UNLABELLED: • PREMISE OF THE STUDY: Following herbivore attack, plants can either reduce damage by inducing defenses or mitigate herbivory effects through compensatory growth and reproduction. It is increasingly recognized that such induced defenses in plants are herbivore-specific, but less is known about the specificity of compensatory responses. Damage by multiple herbivores may also lead to synergistic effects on induction and plant fitness that differ from those caused by a single herbivore species. Although largely unstudied, the order of arrival and damage by different herbivore species might also play an important role in the impacts of herbivory on plants.• METHODS: We investigated the specificity of defense induction (phenolics) and effects on growth (number of stems and leaves) and reproduction (number of seeds, seed mass, and germination rate) from feeding by two generalist leaf-chewing herbivores (Spodoptera eridania and Diabrotica balteata) on Phaseolus lunatus plants and evaluated whether simultaneous attack by both herbivores and their order of arrival influenced such dynamics.• KEY RESULTS: Herbivory increased levels of leaf phenolics, but such effects were not herbivore-specific. In contrast, herbivory enhanced seed germination in an herbivore-specific manner. For all variables measured, the combined effects of both herbivore species did not differ from their individual effects. Finally, the order of herbivore arrival did not influence defense induction, plant growth, or seed number but did influence seed mass and germination.• CONCLUSIONS: Overall, this study highlights novel aspects of the specificity of plant responses induced by damage from multiple species of herbivores and uniquely associates such effects with plant lifetime fitness.