Search

1. Maternal provisioning can reduce offspring vulnerability to predators by promoting offspring growth and eliciting of antipredator behaviours. Mothers perceiving predation risk may improve offspring survival if producing larger, higher‐quality offspring. However, empirical evidence suggests that offspring quality is often reduced, probably reflecting predator‐induced physiological costs, or a selfish maternal strategy aimed at producing more offspring by sacrificing their quality. While perception and impact of predators can vary across the prey's life stage, a majority of studies have focused on understanding how reproductive allocation decisions are influenced by the risk of predation during adulthood. 2. In this study, Leptinotarsa decemlineata beetles were used to examine if the risk of predation during the larval stage: (i) impacts the mother's physiological condition, including body mass and metabolic rate; and (ii) alters maternal allocation of reproductive resources to offspring quantity versus quality. 3. Results revealed that L. decemlineata mothers responded to perceived predation risk by producing clutches with fewer but larger eggs, thus increasing offspring provisioning. Surprisingly, while females that had faced predation risk as larva emerged with a similar body mass to control females, they exhibited lower metabolic rates. 4. Although predation risk in L. decemlineata larvae is known to impair their ability to acquire and maintain energy resources, adult females appeared to ameliorate such costs by improving their metabolic efficiency and by allocating more of their limited reproductive resources to produce fewer but better‐quality offspring.

Entomopathogenic nematodes (EPNs) have potential as an alternate means of controlling soil-dwelling pests in settings such as school athletic fields, where use of chemical pesticides is often restricted or prohibited. Athletic fields are also unique among turfgrass systems, as their distinct pattern of foot traffic can result in compaction and other soil properties varying across different areas of the field, potentially causing variability in EPN performance even within a single field, as many abiotic and biotic soil properties are known to influence EPN efficacy. We tested the efficacy of the EPNs Steinernema feltiae and Heterorhabditis bacteriophora against third-instar grubs of the Japanese beetle Popillia japonica in high-traffic and low-traffic areas of two soccer fields in New York State, one grown atop loam soil and the other atop loamy sand. Efficacy was low in the loam soil but modest for both species in the loamy sand, though the only significant increase over controls occurred in S. feltiae-inoculated plots within low traffic areas in 2016. Non-metric multidimensional scaling revealed positive associations between efficacy of both EPN species and soil sand content, suggesting that sandy soils are most optimal for curative applications against turfgrass pests. Soil biotic factors, such as microarthropod abundance, were not found to have an effect on EPNs. These results will aid turfgrass managers by improving knowledge of the conditions required for effective use of EPNs.

1. Although many vector-borne pathogens are transmitted by an array of vector species, most studies do not account for the potential effects of species interactions. 2. By manipulating conspecific and heterospecific vector density in small experimental mesocosms, this study disentangled the impact of vector density and community composition on vector movement and plant virus transmission in the potato virus Y system. 3. The following predictions were tested: (i) increasing aphid density will increase aphid movement and virus transmission; (ii) adding low-efficiency vectors and thereby decreasing the average transmission efficiency of the vector assemblage will decrease virus transmission; and (iii) aphid movement and the average vector transmission efficiency will mediate the effect of aphid density and community composition on virus transmission. 4. It was found that initial density positively affected aphid movement, but had no effect on virus transmission, and that conspecific density was more important than heterospecific density. Conversely, community composition affected both aphid movement and virus transmission. These effects were driven by species identity, rather than species richness per se. 5. The results of this study emphasise the importance of accounting for vector behaviour, and analysing it within the context of the wider vector assemblage.

Summary Landscape composition affects local arthropod biodiversity, including herbivorous insects and their predators, yet to date landscape effects on insect-vectored plant diseases have received little attention. Here, we examine how landscape composition affects the prevalence of a viral pathogen in host plants, and the role the arthropod vector assemblage plays in mediating landscape effects. We measured the effect of landscape composition (measured as percentage of cropland and unmanaged land) on the plant virus Potato virus Y (PVY), its aphid vectors, and their coccinellid predators during the 2012 and 2013 field seasons at 19 to 21 farms. In both years, we found a positive relationship between final virus prevalence and percentage of cropland within 500, 1000, and 1500 m surrounding study sites. Percentage of cropland also had a significant negative effect on aphid species richness, and the aphid community composition in turn affected PVY prevalence. By contrast, landscape composition had no measurable effect on coccinellid abundance or species richness in this study. Synthesis and applications. Our work demonstrates that landscape composition plays an important role in vector-borne pathogen spread, and that pathogen spread appears to be mediated by the effects of the landscape on the insect vector community. The small spatial scale (≤1500 m) of the effects seen in our study indicates that on-farm management practices have the potential to reduce virus prevalence on small-scale farms. Farmers may be able to reduce Potato virus Y prevalence by on-farm diversification, by isolating potato fields from other agricultural crops, and by not using saved potato seed. This article is protected by copyright. All rights reserved.

Agricultural intensification impacts local arthropod communities. The temporal and spatial variation of agricultural environments can have a significant impact on insect pest populations, yet little work has been done to date on the effect of intra-annual variation (within season) or spatiotemporal effects on arthropod functional community composition. The aim of this research was to evaluate the effects of intra-annual variation and landscape composition on the aphid community. To that end, we investigated the following research question: How do intra-annual variation and landscape composition affect aphid abun- dance, species richness, and functional community composition? In this study, we quantified landscape com- position as percent cropland, intra-annual variation as sampling week measured throughout the growing season, and aphid functional community composition as crop virus transmission—or vectoring—ability. We collected data in two agricultural regions: a diversified agricultural region in New York State (NY) and an agriculturally intense potato-growing region in Wisconsin (WI). We found that the interactive effect of land- scape composition and intra-annual variation significantly affected aphid abundance and species richness in both study regions, and functional community composition in NY. These results indicate that spatiotempo- ral shifts in agroecosystems have significant implications for aphid functional community composition.

Lethal predators and pathogens can reduce the size of pest populations and help regulate crop-damaging herbivores. Additionally, predators like the spined soldier bug (Podisus maculiventris) can elicit non-consumptive effects in herbivores such as the Colorado potato beetle (Leptinotarsa decemlineata), causing changes in prey behavior, physiology and life history. While it is known that lethal predators and pathogens interact, there is little known about the interaction of predator-induced non-consumptive effects and pathogens on their shared hosts. Using the spined soldier bug, which is known to elicit non-consumptive effects on potato beetles (e.g. reduced feeding), we studied the interaction of predator-induced non-consumptive effects and the fungal pathogen Beauveria bassiana on the survival of Colorado potato beetle larvae. In laboratory microcosms we found a 16–50% increase in survival of fungus-treated beetles held with non-lethal male stink bugs. We also studied the predator-fungus interaction on jasmonic acid-treated plants to assess whether elevated levels of host plant defenses made larvae more susceptible to fungal infection. Beetles’ susceptibility to fungal infection did not change when provided jasmonic-acid treated foliage as food. Finally, we determined that two volatile compounds (E-2-hexenal and alpha-terpineol), produced as part of the bugs’ aggregation pheromone, reduced conidial germination, resulting in higher levels of beetle survival. Our findings suggest that stink bug odors protect prey against fungal pathogens.

Herbivore-induced plant defences regulated by the phytohormones jasmonic acid (JA) and salicylic acid (SA) are predicted to influence herbivore population dynamics, in part because they can operate in a density-dependent manner. While there is ample evidence that herbivore-induced plant responses affect individual performance and growth of herbivores, whether they scale-up to regulate herbivore population dynamics is still unclear. We evaluated the consequences of variation in plant defences and herbivore density on herbivore development, reproduction and density-dependent population growth. We investigated potential mechanisms affecting the strength of herbivore density-dependent processes by manipulating jasmonate expression, quantifying plant defensive traits (phytohormones JA and SA and serine proteinase inhibitors) and adding aphids (Macrosiphum euphorbiae) at different densities to plants to simulate different initial population density and herbivore load. We manipulated jasmonate defences by using genetically modified lines of tomato plants (Solanum lycopersicum) with elevated or suppressed jasmonate-dependent defences. Jasmonate-insensitive plants cannot induce the defences regulated by the JA pathway, while jasmonate-overexpressing plants constitutively express jasmonate-dependent defences. We found that jasmonate defences provided resistance against aphids and influenced density-dependent processes. Jasmonate-overexpressing plants reduced aphid reproduction, prolonged developmental time, dampened aphid populations across all aphid densities and caused density-independent aphid population growth. Jasmonate-overexpressing plants showed high JA-dependent constitutive levels of resistance and were unable to activate the SA pathway in response to aphid feeding. In contrast, jasmonate-insensitive plants increased aphid reproduction, shortened developmental time, reduced population growth only at high initial densities and promoted strong negative density-dependent population growth. Aphid feeding on jasmonate-insensitive plants did not induce jasmonate-dependent defences, but induced the SA pathway in a density-dependent manner, which resulted in negative density-dependent aphid population growth. Aphid feeding on jasmonate-insensitive and jasmonate-overexpressing plants differentially activated the salicylate pathway, revealing a negative crosstalk between the defensive phytohormones JA and SA. By muting or enhancing jasmonate-mediated responses and quantifying SA phytohormone induction, we demonstrated that plant defences are a key factor driving not only the performance, but also the density dependence processes and population growth of herbivores.

A growing number of studies have manipulated intraspecific plant diversity and found dramatic changes in the densities of associated insect herbivores and their predators. While these studies have been essential for quantifying the net ecological consequences of intraspecific plant diversity, they have been less effective at uncovering the ways in which plant diversity alters trophic interactions within arthropod communities. We manipulated intraspecific plant diversity and predation risk in the field in a factorial design to reveal how a mixture of plant genotypes changes the response of an herbivorous beetle (Leptinotarsa decemlineata) to a common stink bug predator (Podisus maculiventris). We repeated the manipulations twice across the ontogeny of the beetle to examine how the effects of diversity on the predator-prey interaction differ between larval and adult stages. We found that intraspecific plant diversity, mixtures of susceptible and resistant varieties of potato (Solanum tuberosum), reduced larval survival by 20% and adult oviposition by 34%, which surprisingly put survival and oviposition lower in the mixed-genotype plots than in the resistant monocultures. Moreover, we found that predation risk reduced larval survival 25% and 11% in resistant and susceptible monocultures, respectively, but had no effect in the mixture. This result indicated that our genotypic mixing treatment interacted nonadditively with predation risk such that plant diversity altered the predator-prey interaction by changing the responses of the beetles to their stink bug predators. In addition, even though predation risk reduced larval survival, it increased adult overwintering survival by 9%, independently of plant treatment, suggesting that these interactions change through ontogeny. A key implication of our study is that plant diversity influences arthropod communities not only by changing resource quality, as past studies have suggested, but also by changing interactions between species within the arthropod community.

In the study of insect-vectored plant viruses, colonizing vector species remain the focus. However, non-colonizing vector species, those that do not settle and reproduce on the viral plant host, are often the most abundant in the field and may be the largest contributors to disease spread. While non-colonists may have a substantial effect on disease prevalence, the factors influencing their movement and transmission on non-host plants have been little studied. Here we evaluated how a common biological control agent (Hippodamia convergens), host and non-host plant abundance, and plant spatial distribution impact the movement and density of a wingless non-colonizing vector [Rhopalosiphum padi (L.)] and transmission of potato virus Y (PVY) in potatoes in experimental arenas. The results of this work illustrate the importance of plant species function (host or non-host) and distribution to vector behavior and disease spread. Predation, host plant abundance, and plant spatial distribution interactively affected viral prevalence within infected arenas. Increasing the number of vector non-host plants increased the distance and frequency of aphid movement, and the effect was influenced by plant spatial distribution, the arrangement of plant species in the experimental arena. Increasing the number of vector host plants increased the density of aphids. Although the interaction of the plant and predator treatments affected the proportion of potato plants infected in arenas where infection occurred, and host abundance and spatial distribution impacted vector movement and viral prevalence, aphid movement did not appear to mediate the effect of plant and predator treatments on PVY prevalence. This work demonstrates that both wingless non-colonizing vector behavior and transmission are aggregated responses to multiple environmental drivers.

Many omnivorous insects are important biological control agents, and their success is influenced by both plant resistance and prey availability. The potential impact of these two factors is complicated by the fact that they may not be independent: Resistant plants also often support fewer herbivorous prey. We studied how lifetime development, growth, fecundity and preference of the omnivorous stink bug, Podisus maculiventris, was affected by jasmonate-induced plant defenses and amount of prey available. P. maculiventris survival was 70 % lower on high-resistance (jasmonate-overexpressing) plants compared to low-resistance (jasmonate-insensitive) plants. However, surviving P. maculiventris grew and achieved equal fecundity on low- and high-resistance plants. When given a choice, P. maculiventris preferred low-resistance plants, but did not differentiate between caterpillar prey reared on high- or low-resistance plants. Low prey availability impacted distinct aspects of P. maculiventris performance: Development time was lengthened, and nymphal and adult mass were reduced, but survival was not impacted. We did not detect any interactive effects between plant resistance and prey availability for any measure of P. maculiventris. Thus, we found remarkably compartmentalized impacts of plant resistance and prey availability for this omnivorous insect.

Predator–prey interactions primarily focus on prey life-stages that are consumed. However, animals in less vulnerable life-stages might also be influenced by the presence of a predator, making our understanding of predation-related impacts across all life-stages of prey essential. It has been previously demonstrated that Podisus maculiventris is a voracious predator of eggs and larvae of Leptinotarsa decemlineata, and that larvae will alter their behavior to avoid predation. However, the adult beetles are not readily consumed by P. maculiventris, raising the question of whether they will respond to predators to protect themselves or their offspring. Here, we examine the effect of predation risk by P. maculiventris, on three adult behaviors of L. decemlineata; colonization, oviposition, and feeding, and the resulting impact on host plant damage. In an open-field test, there was no difference in natural beetle colonization between plots with predation risk and control treatments. However, subsequent host plant damage by adult beetles was 63.9% less in predation risk treatments. Over the lifetime of adult beetles in field mesocosms, per capita feeding was 23% less in the predation risk treatment. Beetle oviposition was 37% less in the presence of predators in a short-term, greenhouse assay, and marginally reduced in longer term field mesocosms. Our results indicate that predation risk can drive relatively invulnerable adult herbivores to adjust behaviors that affect themselves (feeding) and their offspring (oviposition). Thus, the full impact of predator presence must be considered across the prey life cycle.

A consequence of plant diversity is that it can allow or force herbivores to consume multiple plant species, which studies indicate can have major effects on herbivore fitness. An underappreciated but potentially important factor modulating the consequences of multi-species diets is the extent to which herbivores can choose their diets versus being forced to consume specific host-plant sequences. We examined how host-selection behavior alters the effects of multi-species diets using the Colorado potato beetle (Leptinotarsa decemlineata) and diets of potato plants (Solanum tuberosum), tomato plants (S. lycopersicum), or both. When we gave beetles simultaneous access to both plants, allowing them to choose their diets, their final mass was within 0.1% of the average mass across both monocultures and 43.6% lower than mass on potato, the superior host in monoculture. This result indicates these beetles do not benefit from a mixed diet, and that the presence of tomato, an inferior but suitable host, makes it difficult to use potato. In contrast, when we forced beetles to switch between host species, their final mass was 37.8% less than the average of beetles fed constant diets of either host species and within 3.5% of the mass on tomato even though they also fed on potato. This indicates preventing host-selection behavior magnified the negative effects of this multi-species diet. Our results imply that ecological contexts that constrain host-selection or force host-switches, such as communities with competition or predation, will lead plant species diversity to reduce the performance of insect herbivores.

Because predation risk typically alters how prey forage for food, interactions between predation risk and food availability are commonly found. Less is known about how host plant quality and predation risk interact to affect prey behaviour and physiology. Using the caterpillar, Manduca sexta, and its predator, Podisus maculiventris, the effects of predation risk and host plant quality on caterpillar feeding, growth, assimilation efficiency, and resting metabolic rate were tested. Overall, caterpillars on low-resistance tomato plants (jasmonate-insensitive) gained 14% more mass than caterpillars on high-resistance plants (wild-type tomato). On low-resistance plants, the presence of predators caused caterpillars to eat 32% less, but they gained the same mass as unthreatened caterpillars (i.e. a 19% increase in assimilation efficiency). In addition, caterpillars showed a 17% increase in resting metabolic rate in the presence of predators. On high-resistance plants, predation risk caused a decrease in feeding, but did not alter assimilation efficiency or resting metabolic rate. The reduction in physiological responses to predation risk on high- versus low-resistance plants demonstrates a tradeoff between the ability to respond to predation risk and the ability to grow, especially on well-defended plants.

Early-season herbivory can cause plants to induce resistance to subsequent herbivores, and this ubiquitous plant defense strategy has been shown to be adaptive when subsequent vegetative-feeding herbivores impact plant fitness. However, a growing number of studies show that leaf herbivory can also induce defenses in plant reproductive tissues, which may deter mutualists such as pollinators and seed dispersers, or antagonists such as florivores and seed predators. Due to their direct interaction with plant reproductive tissues, deterrence of these mutualists or antagonists may have large negative or positive effects on plant fitness. Despite numerous predictions, we know little regarding the fitness consequences of leaf-to-reproductive tissue induction in nature. Here, using observations of natural populations and manipulative field experiments, we show that leaf herbivory by the invasive Japanese beetle (Popillia japonica) induces an accumulation of jasmonic acid and complex phenolics in reproductive tiss...

The cost of inbreeding (inbreeding depression, ID) is an important variable in the maintenance of reproductive variation. Ecological interactions such as herbivory could modulate this cost, provided that defence traits harbour deleterious mutations and herbivores are responsible for differences in fitness. In the field, we manipulated the presence of herbivores on experimentally inbred and outcrossed plants of Solanum carolinense (horsenettle) for three years. Damage was greater on inbred plants, and ID for growth and fitness was significantly greater under herbivory. Inbreeding reduced phenolic expression both qualitatively (phytochemical diversity) and quantitatively, indicating deleterious load at loci related to the biosynthesis of defence compounds. Our results indicate that inbreeding effects on plant-herbivore interactions are mediated by changes to functional plant metabolites, suggesting that variation in inbreeding could be a predictor of defence trait variation. The magnitude of herbivore-mediated, ecological ID indicates that herbivores could maintain outcrossing mating systems in nature.

Worldwide, many crops rely on insect pollination. Insufficient pollination can reduce fruit and seed set by directly reducing pollen deposition, and can also affect offspring quality, such as growth rate and resistance to herbivores, by limiting outcrossing opportunities. Both effects are important in fruit agroecosystems where fruit size and the quality of seeds for re-planting are dependent on sufficient pollination. We experimentally manipulated pollination of the cape gooseberry, Physalis peruviana L. (Solanaceae), to test the effects of honey and bumble bee pollination compared to manual outcrossing and autonomous self-pollination on fruit and offspring characteristics. Compared to manual and self-pollination, bee pollination increased fruit size, seed set and germination rates, supporting the hypothesis that sufficient pollination increases plant fitness. Interestingly, plant growth rate and herbivore resistance were significantly and marginally greater in manually outcrossed plants compared to self-pollinated offspring, suggesting that inbreeding reduces offspring quality. Herbivore resistance and plant growth did not differ between one honeybee visit and self-pollination suggesting that multiple pollinator visits are needed to prevent inbreeding events. Our data suggest that the quantity and quality of pollen deposited by bee visitation can significantly alter ecologically and economically relevant traits in this agroecosystem. Zusammenfassung Verschiedene Nutzpflanzen weltweit brauchen Insektenbestaubung, um hohe Ertrage zu erzielen. Ungenugende Bestaubung kann, vermittelt durch eine geringe Pollenablage, die Grosse von Fruchten und Samen reduzieren oder die Qualitat der Nachkommen durch Inzuchtdepression beeinflussen. Beide Effekte sind wichtig in Obst-Agrarokosystemen, wo Fruchtgrose und die Qualitat der Samen fur die Wiederbepflanzung eine grosse Rolle spielen und von ausreichender Bestaubung abhangig sind. Wir haben experimentell die Bestaubung von Physalis-Pflanzen (Physalis peruviana) manipuliert, um die Auswirkungen von Honigbienen- und Hummel-Bestaubung im Vergleich zu manueller Fremdbestaubung und Selbstbestaubung auf Frucht- und Nachkommeneigenschaften zu testen. ImVergleich zur manuellen und Selbstbestaubung, erhohte Bienenbestaubung sowohl Samenansatz und Fruchtgrose, als auch die Keimungsrate. Unsere Ergebnisse unterstutzen die Hypothese, dass Insektenbestaubung die Fitness der Pflanze erhoht und auch von Interesse fur die Produzenten von Physalis sein sollte. Beachtlich war, dass Nachkommen von manuell fremdbestaubten Fruchten eine marginal hohere Resistenz gegen Herbivorie aufwiesen

Aphids increase production of winged individuals as a generalized response to multiple threats, including predators, competitors, and poor host plant quality. While wing formation in response to these individual threats is well documented, few investigations have evaluated whether combined threats lead to additive or non-additive outcomes. We tested the interactive effects of predation risk and plant quality on population growth and wing induction in the potato aphid, Macrosiphum euphorbiae. Plant quality was varied using phytohormonal manipulations of tomato (Solanum lycopersicum) to elevate or suppress the jasmonate and salicylate defense pathways. Predation risk was altered by exposing aphids to lethal or risk (unable to feed) individuals of the convergent lady beetle, Hippodamia convergens. Phytohormonal treatments resulted in >4-fold variation in aphid population growth and thus strongly affected plant quality; however, the percentage of winged individuals was no different across plant types. Predators similarly reduced aphid abundance, but also elicited a ~3-fold increase in wing formation, an effect that was similar in magnitude when comparing lethal with risk predators. The overall impact of plants and predators on aphids was largely additive, an outcome that was unexpected given the likelihood for interactions between these two factors and our prior results with other herbivores in this system. We discuss this discrepancy in the context of phenotypic plasticity, non-lethal predator effects, and the ecological challenges faced by wing dimorphic insects.

Omnivorous plant-feeding predators have been predicted to both increase and decrease prey consumption on resistant host-plants because of behavioral shifts in food preferences and direct ingestion of phytotoxins, respectively. To help resolve this debate, we reviewed the published literature on plant defense-heteropteran interactions using both vote-counting and meta-analytical approaches. The Heteroptera are ideal for this analysis because as a group they are broadly omnivorous, critical in the biocontrol of crop pests, and frequently come in contact with plants varying in quality. We identified 37 studies that matched our search criteria, involving at least 16 species of Heteroptera. Overall, plant resistance lowered the abundance of heteropterans in the field, but had virtually no impact on their performance when reared in the lab (aside from a significant, albeit minor, increase in development time). Prey consumption was strongly affected by plant resistance; however, the outcome was extremely variable with near equal evidence for increasing (22 cases) vs. decreasing (21 cases) predation on resistant host-plants. Thus, prey consumption is far more variable across plant-types differing in quality when compared with either abundance or performance. Heteropteran family and developmental stage (adult vs. nymph) were poor predictors of the outcome for prey suppression. Our results indicate that the feeding ecology of omnivorous heteropterans is highly contingent on plant defense expression, more so than other ecologically-relevant traits, but the factors mediating behavioral shifts in prey consumption remain elusive.

Plant resistance and predation have strong independent and interacting eff ects on herbivore survival, behavior, and patterns of herbivory. Historically, research has emphasized variation in the consumption of herbivores by enemies. Recent work, however, demonstrates that predators also elicit important changes in the traits of their prey, but we do not know how this is infl uenced by plant quality. In this study, we quantify how the consumptive and non-consumptive eff ects of predators vary along a gradient of plant resistance using tomato plants (Solanum lycopersicum), tobacco hornworms (Manduca sexta), and predaceous stinkbugs (Podisus maculiventris). We manipulated resource quality using three tomato lines that vary in the expression of the jasmonate pathway, a phytohormonal pathway that is central in mediating resistance to insects. Resistant plants had higher levels of defensive proteins and glandular trichomes than low resistance plants. Th e consumptive and non-consumptive eff ects of predators were quantifi ed on the three tomato lines by comparing the impact of ‘lethal’ predators that both kill and scare prey with ‘risk’ predators whose mouthparts were surgically impaired to prevent killing. Across several fi eld experiments, the total cascading eff ect of predators on plant damage was 80.4% lower on jasmonate-overexpressing (highly resistant) plants compared to that on wild-type or jasmonate-insensitive (low resistance) plants. Th is dramatic attenuation of predator eff ects was due to a 66% reduction in consumption on high resistance plants, and also because of a 65% decline in non-consumptive eff ects. Numerous studies in natural and agricultural habitats have documented that predator eff ects tend to be weaker on well-defended plants; our results provide novel mechanistic insight into this pattern by demonstrating that plant resistance substantially weakens both the consumptive and non-consumptive impacts of predators.

Management of green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), in bell pepper, Capsicum annuum L., was explored through a combination of plant growth-promoting rhizobacteria (PGPR) and endemic biological control in New York in 2006 and 2007. We hypothesized that by using PGPR-treated peppers 1) M. persicae infestations would be reduced via induced resistance, 2) natural enemies would be lured to plants through the elicitation of volatile organic compounds, and 3) yield amount and quality would be improved. Pepper seed was planted in soil containing the PGPR formulation BioYield or untreated soil. Plants were transplanted to field plots and then treated with an insecticide regimen designed to remove or conserve populations of natural enemies. Apterous aphids and natural enemies were counted weekly on plants and pepper fruit were harvested, graded and weighed three times. PGPR did not directly or indirectly reduce aphid densities in either year. In 2006, there were more natural enemies in PGPR-treated plots than untreated ones, but this was probably a density-dependent response to aphid densities rather than a response of natural enemies to volatiles from PGPR-treated plants. For the first harvest date in 2006, yield of all fruit grades, especially the premium Fancy Grade, was 1.7-2.3 times greater in PGPR-treated plots than in untreated plots. However, no differences in yield were observed for the other two harvest dates or overall yield in 2006; no differences in yield among treatments were detected in 2007. Our results suggest that PGPR will not significantly impact M. persicae infestations or natural enemy populations but could enhance yield and quality of pepper fruit in some years.

The non-consumptive (or trait-mediated) effects of predators on prey are known to contribute substantially to the negative impact of insect predators on herbivorous insects. Our goal now is to understand what factors alter the relative importance of the consumptive (or density-mediated) and non-consumptive components of the total predator impact. This is important both for understanding the effects of predators in natural systems as well as for successfully manipulating predators for biological control in agriculture. In this study, we tested whether herbivore ontogeny influenced the contribution of consumptive and non-consumptive effects of a predator on herbivore survivorship and plant damage by the herbivores. We addressed these questions using the native plant Solanum ptychanthum Dunal (Solanaceae), the predator Podisus maculiventris Say (Heteroptera: Pentatomidae), and first-, third-, and fourth-instar Manduca sexta L. (Lepidoptera: Sphingidae). In field cage experiments, we found that first- and third-instar M. sexta were more vulnerable to predators compared to fourth instars. In the presence of predators, M. sexta caterpillars spent less time on feeding compared to caterpillars in the absence of predators. The amount of damage the plants received was reduced in the presence of the predator and the consumptive and non-consumptive components contributed approximately equally to this reduction. Thus, the non-consumptive component of the predator is important for all of the herbivore stages vulnerable to predation in our study. We conclude with a discussion of possible implications of considering non-consumptive effects of predators in biological control of agricultural pests.

1. Herbivory can induce resistance in a plant and the induced phenotype may be disfavoured by subsequent herbivores. Yet, as the distance between plants in a population increases, limited mobility may make a herbivore more likely to feed and oviposit on host plants in its immediate surroundings. 2. The present study tested whether a herbivore’s preference and distribution across plants with different induced phenotypes was influenced by the spatial distribution of plants. A fragmented population of Solanum dulcamara plants was created. This consisted of discrete, spatially separated patches with different histories of damage, either herbivory from adult flea beetles (Psylliodes affinis), tortoise beetles (Plagiometriona clavata), or mechanical damage. Each patch was separated by 7 m and consisted of 12 plants that were spaced 30 cm apart. Then a fixed number of adult tortoise beetles were introduced to each patch, and movement and oviposition within and between spatially separate homogeneous patches (receiving one type of damage) were compared with movement and oviposition within heterogeneous patches (containing all three types of damage) over the growing season. 3. Flea beetle and tortoise beetle herbivory consistently induced different phytochemical responses in S. dulcamara (polyphenol oxidase and peroxidase), and adult tortoise beetles avoided oviposition on the flea beetle induced plants within heterogeneous patches. However, between homogeneous patches, plant phenotype did not influence oviposition. Colonisation by naturally occurring flea beetle adults followed a similar pattern. 4. These results suggest that the heterogeneity of plant phenotypes can influence herbivore choice and distribution at small but not large spatial scales.

Plants in nature are attacked sequentially by herbivores, and theory predicts that herbivore-specific responses allow plants to tailor their defenses. We present a novel field test of this hypothesis, and find that specific responses of Solanum dulcamara lead to season-long consequences for two naturally colonizing herbivores, irrespective of the second herbivore to attack plants. This result indicates that responses induced by the initial herbivore made plants less responsive to subsequent attack. We show that initial herbivory by flea beetles and tortoise beetles induce distinct plant chemical responses. Initial herbivory by flea beetles lowered the occurrence of conspecifics and tortoise beetles relative to controls. Conversely, initial herbivory by tortoise beetles did not influence future herbivory. Remarkably, the experimentally imposed second herbivore to feed on plants did not modify consequences (induced resistance or lack thereof) of the first attacker. Induction of plant chemical responses was consistent with these ecological effects; i.e. the second herbivore did not modify the plant's initial induced response. Thus, canalization of the plant resistance phenotype may constrain defensive responses in a rapidly changing environment.

Predators can affect herbivores both through direct consumption (density-mediated interactions) and by changing behavioural, physiological or morphological attributes of the prey (trait-mediated interactions). These effects on the herbivore can in turn affect the plant through density- and trait-mediated indirect interactions (DMIIs and TMIIs). While the effects of DMIIs and TMIIs imposed by predators has been shown to influence plant density and plant communities, we know little about the effects on plant quality. In addition, the DMII and TMII components of the predator may influence each other so that the total effect of the predator on the plant is not simply the sum of the DMII and TMII. We examined DMIIs and TMIIs between a stinkbug predator and a caterpillar, and show how these interactions affect plant quality, as measured by damage, resistance to herbivores, and a defence chemical, peroxidase. We used novel methods to estimate the independent and non-additive contribution of DMIIs and TMIIs to the plant phenotype. Both predator-induced DMIIs and TMIIs caused decreases in the amount of caterpillar herbivory on plants; a strong non-additive effect between the two resulted from redundancy in their effects. TMIIs initiated by the predator were primarily responsible for a decrease in induced plant resistance. However, DMIIs predominated for reducing the production of peroxidase. These data demonstrate how DMIIs and TMIIs initiated by predators cascade through tri-trophic interactions to affect plant damage and induced resistance.

Interspecific competition between phytophagous insects can occur when plant responses induced by an early-season herbivore alter host quality for later colonizers. Recent evidence for specificity in the elicitation of induced plant responses by different attackers suggests that dynamics of host use in the field may be more complex than previously anticipated, because host suitability for colonizing herbivores may depend on which herbivore species has initially damaged a plant. In each of two years, we manipulated the first herbivore to attack Solanum dulcamara plants in an experimental population using several different arthropod species and subsequently monitored colonization by natural herbivores over the course of the growing season. We additionally performed weekly herbivore counts in wild S. dulcamara populations following natural variation in herbivore arrival. Plant-mediated interactions occurred primarily between two leaf-feeding beetles, Psylliodes affinis and Plagiometriona clavata. In both manipulative and observational experiments, P. clavata oviposition was reduced on plants initially damaged by P. affinis (or a third leaf-feeding beetle, Lema trilinea) relative to plants that were initially undamaged. Lowered P. clavata occurrence continued through subsequent life-history stages, resulting in decreased emergence of second-generation P. clavata adults on these plants. The occurrence of P. affinis was also lowered on plants damaged by conspecifics in both manipulative and observational experiments. Resistance against P. affinis also followed applications of jasmonic acid, an elicitor of plant defensive responses. Conversely, early-season damage by P. clavata did not influence plant quality for either later conspecifics or P. affinis. Initial herbivory by the spittlebug Aphrophora saratogensis or generalist taildropper slugs (Prophysaon sp.) likewise had no influence on P. clavata and P. affinis colonization, whereas L. trilinea damage did not affect later arriving P. affinis. Hence, only a subset of early-season damagers influenced herbivore occurrence on S. dulcamara. Preference tests examining P. affinis feeding and P. clavata oviposition confirmed that specificity in elicitation of induced plant responses produced the divergent herbivore occurrence patterns observed in the field. Overall, the existence of plant-mediated competitive asymmetry between herbivore species on S. dulcamara highlights the dynamic nature of plant resistance and its potential role in organizing herbivore communities.

Plants respond to herbivore damage by inducing defences that can affect the abundance of herbivores and predators. These tritrophic interactions may be influenced by heterogeneity in plant neighbourhood. 2. In the present study, the effects of induced responses on the abundance of herbivores (flea beetles and aphids), omnivores (pirate bugs and thrips), and predators (lady beetles and spiders) on individual plants and their neighbours between and within patches composed of three tomato plants was investigated. 3. Herbivore damage was manipulated to create homogeneous patches where either all or none of the plants had defences induced by herbivore damage, and heterogeneous patches where only one of the plants was induced. 4. Arthropod abundance on plants at different scales was compared by testing between patch effects (patch level), for neighbourhood effects at the plant pheno- type level (neighbourhood level), and between near and far plants (within patch position). 5. At the patch level, plants in homogeneously induced patches contained fewer flea beetles and pirate bugs, but more lady beetles, compared with homogeneously non-induced patches. There was no effect of patch type on the abundance of aphids, thrips, and spiders on plants. 6. At the neighbourhood level, induced plants in heterogeneous patches contained more flea beetles and pirate bugs compared with induced plants in homogeneous patches, indicating that the abundance of some herbivores and omnivores on induced plants varied depending on the phenotype of the other plants within the patch. Within patch position, there was no evidence that the abundance of herbivores or predators on non-induced plants was affected by proximity to an induced plant. 7. Therefore, variation in plant neighbourhood generated by induced plant responses affected the abundance of three arthropods from three feeding guilds.

Plants defend themselves against attack from insects and pathogens with various resistance strategies. The jasmonate and salicylate signaling pathways are two induced responses that protect plants against these attackers. Knowledge of the range of organisms that are affected by each response is important for understanding how plants coordinate their defenses against multiple attackers and the generality of effect of different resistance mechanisms. The jasmonate response is known to protect plants against a wide range of insect herbivores; in this study, we examined the role of the jasmonate response in susceptibility to eight pathogens with diverse lifestyles in the laboratory and field. Recent biochemical models suggest that the lifestyle of the pathogen (necrotroph versus biotroph) should predict whether the jasmonate response will be involved in resistance. We tested this by examining the susceptibility of wild-type (cv Castlemart with no known genes for resistance to the pathogens used) and jasmonate-deficient mutant tomato (Lycopersicon esculentum) plants (def1) and by employing rescue treatments of the mutant. Plant susceptibility to five of the eight pathogens we examined was reduced by the jasmonate response, including two bacteria (Pseudomonas syringae and Xanthomonas campestris), two fungi (Verticillium dahliae and Fusarium oxysporum f. sp. lycopersici), and an oomycete (Phytophthora infestans). Susceptibility to three fungi was unaffected (Cladosporium fulvum, Oidium neolycopersici, and Septoria lycopersici). Our results indicate that the jasmonate response reduces damage by a wide range of pathogens from different lifestyles, a result that contrasts with the emerging picture of diseases on Arabidopsis. Thus, the generality of jasmonate-based resistance of tomato challenges the view that ecologically distinct plant parasites are resisted via different mechanisms.

Summary 1 Plant traits can act as defences against herbivores both by reducing herbivore performance directly and by increasing the effectiveness of the natural enemies of herbivores. Natural enemy performance and rate of parasitism can be affected by plant traits and/or changes in herbivore quality. 2 Jasmonic acid is responsible for the induction of many changes in plant resistance that occur following herbivore attack. This study examines the effects of jasmonate-induced defences on the abundance and performance of natural enemies, as well as the interaction between induced plant responses and parasitism in their ability to kill herbivores. 3 In a tomato field containing plants induced with jasmonic acid and control plants, the abundance of natural enemies was counted using several census techniques. Induced resistance affected the abundance of natural enemies of herbivores differently. One predator of aphids, syrphid flies, was negatively affected by the decrease in herbivore abundance on induced plants. One parasitoid of caterpillars, Hyposoter exiguae Viereck, was not affected by induced resistance in this study although it was positively affected in a previous study. Two other natural enemies, a parasitoid of aphids and ladybeetle predators, were not affected by induced resistance. 4 Induced resistance and parasitism both reduced the survivorship of herbivores. In a 2 × 2 factorial design with induced resistance crossed by parasitism, the interaction between the effects of induced resistance and parasitism on herbivore survival was tested. Two trials of this experiment were conducted; one where induced resistance affected both herbivore quantity and quality and one where induced resistance only affected herbivore quality (herbivore density was equalized). 5 Parasitoids were more effective at killing herbivores feeding on control plants than herbivores on induced plants. This difference was due to a difference in herbivore quality, not herbivore quantity. Herbivores feeding on induced plants have lower mass than herbivores on control plants and this appears to be a major factor reducing the performance of developing parasitic wasps. 6 Thus, jasmonate-induced responses influence natural enemies species in differing ways, sometimes reducing the density of herbivores and sometimes reducing the quality of herbivores for natural enemies.

The jasmonate (JA) and salicylate (SA) signaling pathways in plants provide resistance to herbivorous insects and pathogens. It is known that these pathways interact, sometimes resulting in antagonism between the pathways. We tested how the timing and concentration of elicitation of each pathway influenced the interaction between the jasmonate and salicylate pathways measured in terms of five biochemical responses and biological resistance to caterpillars and bacteria. The salicylate pathway had a stronger effect on the jasmonate pathway than did the reverse. The negative signal interaction was generated by two distinct paths in the plant. A negative interaction in the biochemical expression of the two pathways was most consistent in the simultaneous elicitation experiments compared to when the elicitors were temporally separated by two days. Herbivore bioassays with Spodoptera exigua also consistently reflected an interaction between the two pathways in the simultaneous elicitation experiments. The negative signal interaction reducing biological resistance to the herbivore was also demonstrated in some temporally separated treatment combinations where attenuation of the biochemical response was not evident. Concentration of the elicitors had an effect on the pathway interaction with consistent biochemical and biological antagonism in the high concentration experiments and inconsistent antagonism in the low concentration experiments. The bacterial pathogen, Pseudomonas syringae pv. tomato (Pst), consistently showed reduced lesion development on plants with SA responses activated and, in some experiments, on JA-elicited plants. Resistance to Pst was not reduced or enhanced in dual-elicited plants. Thus, signal interaction is most consistent when elicitors are applied at the same time or when applied at high doses. Signal interaction affected the herbivore S. exigua, but not the pathogen Pst.

Plant quality and predators are important factors affecting herbivore population growth, but how they interact to regulate herbivore populations is not well understood. We manipulated jasmonate-induced plant resistance, exposure to the natural predator community and herbivore density to test how these factors jointly and independently affect herbivore population growth. On low-resistance plants, the predator community was diverse and abundant, promoting high predator consumption rates. On high-resistance plants, the predator community was less diverse and abundant, resulting in low predator consumption rate. Plant resistance only directly regulated aphid population growth on predator-excluded plants. When predators were present, plant resistance indirectly regulated herbivore population growth by changing the impact of predators on the herbivorous prey. A possible mechanism for the interaction between plant resistance and predation is that methyl salicylate, a herbivore-induced plant volatile attractive to predators, was more strongly induced in low-resistance plants. Increased plant resistance reduced predator attractant lures, preventing predators from locating their prey. Low-resistance plants may regulate herbivore populations via predators by providing reliable information on prey availability and increasing the effectiveness of predators.

integration of physiological responses has received less attention. This is the subject of this special issue.Prey physiological responses are important at all stages of the predator–prey interaction. They are a major part of the prey’s primary, fight or flight, response, are mechanis-tic drivers of behavioral and morphological changes, help prepare prey for future attack, and secondarily respond to changes caused by primary responses. We are beginning to understand how, in the initial steps of predator detection, sensory systems, such as visual and olfactory ones, may act synergistically to gather information regarding risk (Kats and Dill 1998; Hartman and Abrahams 2000). Following detection, the physiological status of the prey (Koivula et al. 1995; Martin and Lopez 1999), prey genotype (Den-nis et al. 2010), and personality (Sih et al. 2004) influence whether and how they respond. Physiological responses also aid in defense once the predator initiates attack. For example, tadpoles previously exposed to predator cues have adaptive morphological changes linked to elevated stress hormone levels giving them an advantage in escap-ing predation (Hossie et al. 2010), dragonfly predators select for higher arginine kinase enzyme that powers faster swimming speed and escape performance in damselfly prey (Strobbe et al. 2010), and caterpillars can increase digestive efficiency to compensate for reductions in feeding (Thaler et al. 2012). Finally, parental exposure to predation risk can influence offspring behavior, morphology, and physiol-ogy (Agrawal et al. 1999; Sheriff et al. 20092010, ; Storm and Lima 2010; Zanette et al. 2011) and these effects may lead to adaptive phenotypes dependent upon the match between the maternal and offspring environment (Sheriff and Love 2013). Given that the primary response of prey to the immediate threat of predation is the “stress response” (Sapolsky et al. 2000) and central to this is the activation of the hypothalamic–pituitary–adrenal axis, much work has

Predators can affect prey in two ways-by reducing their density (consumptive effects) or by changing their behavior, physiology or other phenotypic traits (non-consumptive effects). Understanding the cues and sensory modalities prey use to detect predators is critical for predicting the strength of non-consumptive effects and the outcome of predator-prey encounters. While predator-associated cues have been well studied in aquatic systems, less is known about how terrestrial prey, particularly insect larvae, detect their predators. We evaluated how Colorado potato beetle, Leptinotarsa decemlineata, larvae perceive predation risk by isolating cues from its stink bug predator, the spined soldier bug, Podisus maculiventris. When exposed to male "risk" predators that were surgically manipulated so they could hunt but not kill, beetles reduced feeding 29% compared to controls. Exposure to risk females caused an intermediate response. Beetles ate 24% less on leaves pre-exposed to predators compared to leaves never exposed to predators, indicating that tactile and visual cues are not required for the prey's response. Volatile odor cues from predators reduced beetle feeding by 10% overall, although male predators caused a stronger reduction than females. Finally, visual cues from the predator had a weak effect on beetle feeding. Because multiple cues appear to be involved in prey perception of risk, and because male and female predators have differential effects, beetle larvae likely experience tremendous variation in the information about risk from their local environment.

Herbivores are squeezed between the two omnipresent threats of variable food quality and natural enemy attack, but these two factors are not independent of one another. The mechanisms by which organisms navigate the dual challenges of foraging while avoiding predation are poorly understood. We tested the effects of plant defense and predation risk on herbivory in an assemblage of leaf-chewing insects on Solanum lycopersicum (tomato) that included two Solanaceae specialists (Manduca sexta and Leptinotarsa decemlineata) and one generalist (Trichoplusia ni). Defenses were altered using genetic manipulations of the jasmonate phytohormonal cascade, whereas predation risk was assessed by exposing herbivores to cues from the predaceous stink bug, Podisus maculiventris. Predation risk reduced herbivore food intake by an average of 29% relative to predator-free controls. Interestingly, this predator-mediated impact on foraging behavior largely attenuated when quantified in terms of individual growth rate. Only one of the three species experienced lower body weight under predation risk and the magnitude of this effect was small (17% reduction) compared with effects on foraging behavior. Manduca sexta larvae, compensated for their predator-induced reduction in food intake by more effectively converting leaf tissue to body mass. They also had higher whole-body lipid content when exposed to predators, suggesting that individuals convert energy to storage forms to draw upon when risk subsides. In accordance with expectations based on insect diet breadth, plant defenses tended to have a stronger impact on consumption and growth in the generalist than the two specialists. These data both confirm the ecological significance of predators in the foraging behavior of herbivorous prey and demonstrate how sophisticated compensatory mechanisms allow foragers to partially offset the detrimental effects of reduced food intake. The fact that these mechanisms operated across a wide range of plant resistance phenotypes suggests that compensation is not always constrained by reduced food quality.

1. The impact of predators on prey has traditionally been attributed to the act of consumption. Prey responses to the presence of the predator (non-consumptive effects), however, can be as important as predation itself. While plant defences are known to influence predator-prey interactions, their relative effects on consumptive vs. non-consumptive effects are not well understood. 2. We evaluated the consequences of plant resistance and predators (Hippodamia convergens) on the mass, number of nymphs, population growth, density and dispersal of aphids (Macrosiphum euphorbiae). We tested for the effects of plant resistance on non-consumptive and consumptive effects of predators on aphid performance and dispersal using a combination of path analysis and experimental manipulation of predation risk. 3. We manipulated plant resistance using genetically modified lines of tomato (Solanum lycopersicum) that vary incrementally in the expression of the jasmonate pathway, which mediates induced resistance to insects and manipulated aphid exposure to lethal and risk predators. Predation risk predators had mandibles impaired to prevent killing. 4. Plant resistance reduced predation rate (consumptive effect) on high resistance plants. As a consequence, predators had no impact on the number of nymphs, aphid density or population growth on high resistance plants, whereas on low resistance plants, predators reduced aphid density by 35% and population growth by 86%. Path analysis and direct manipulation of predation risk showed that predation risk rather than predation rate promoted aphid dispersal and varied with host plant resistance. Aphid dispersal in response to predation risk was greater on low compared to high resistance plants. The predation risk experiment also showed that the number of aphid nymphs increased in the presence of risk predators but did not translate into increased population growth. 5. In conclusion, the consumptive and non-consumptive components of predators affect different aspects of prey demography, acting together to shape prey population dynamics. While predation risk accounts for most of the total effect of the predator on aphid dispersal and number of nymphs, the suppressive effect of predators on aphid population occurred largely through consumption. These effects are strongly influenced by plant resistance levels, suggesting that they are context dependent.

Summary 1. The negative effect of induced plant resistance on the preference and performance of herbivores is a well-documented ecological phenomenon that is thought to be important for both plants and herbivores. This study links the well-developed mechanistic understanding of the biochemistry of induced plant resistance in the tomato system with an examination of how these mechanisms affect the community of herbivores in the field. 2. Several proteins that are induced in tomato foliage following herbivore damage have been linked causally to reductions in herbivore performance under laboratory conditions. Application of jasmonic acid, a natural elicitor of these defensive proteins, to tomato foliage stimulates induced responses to herbivory. 3. Jasmonic acid was sprayed on plants in three doses to generate plants with varying levels of induced responses, which were measured as increases in the activities of proteinase inhibitors and polyphenol oxidase. 4. Field experiments conducted over 3 years indicated that induction of these defensive proteins is associated with decreases in the abundance of all four naturally abundant herbivores, including insects in three feeding guilds, caterpillars, flea beetles, aphids, and thrips. Induced resistance killed early instars of noctuid caterpillars. Adult flea beetles strongly preferred control plants over induced plants, and this effect on host plant preference probably contributed to differences in the natural abundance of flea beetles. 5. The general nature of the effects observed in this study suggests that induced resistance will suppress many members of the herbivore community. By linking plant biochemistry, insect preference, performance, and abundance, tools can be developed to manipulate plant resistance sensibly and to predict its outcome under field conditions.

Plants are often simultaneously challenged by pathogens and insects capable of triggering an array of responses that may be beneficial or detrimental to the plant. The efficacy of resistance mechanisms can be strongly influenced by the mix of signals generated by biotic stress as well as abiotic stress such as drought, nutrient limitation or high soil salinity. An understanding of their biochemical nature, and knowledge of the specificity and compatibility of the signaling systems that regulate the expression of inducible responses could optimize the utilization of these responses in crop protection. Signaling conflicts and synergies occur during a plant's response to pathogens and insect herbivores, and much of the research on defense signaling has focused on salicylate- and jasmonate-mediated responses. We will review our results using tomato (Lycopersicon esculentum) in greenhouse and field studies that illustrate a trade-off between salicylate- and jasmonate-mediated signaling, and discuss research on strategies to minimize the trade-off that can occur following the application of chemical elicitors of resistance. In addition, there is evidence of another signaling system that mediates endogenous levels of ceramide in the plant. This signal is associated with programmed cell death and protection of tomato against the fungal pathogen Alternaria alternata f. sp. lycopersici.

Theory predicts that the balance of nutritional needs, food availability, and the quality of particular food items are important factors in the feeding decisions of om- nivorous animals. In this study we investigate factors that affect the feeding decisions of an omnivorous thrips (Frankliniella occidentalis) that eats both animal prey and plant foliage. In the presence of prey (mite eggs), adult and larval thrips consumed nearly half the amount of plant tissue as did thrips without prey. We manipulated host-plant quality by exposing plants to spider mite feeding. In the absence of prey, systemically induced plant responses following herbivory reduced the amount of feeding by thrips compared to that on uninduced control plants. In the presence of prey, induced responses caused a shift in the feeding preferences of thrips: thrips consumed half the amount of plant material and twice the number of prey on induced plants as did thrips on uninduced control plants. Our findings are relevant to understanding the complex factors that shape food-web interactions in nature. Variation in host-plant quality and availability of prey can exert a strong influence on the feeding preferences of omnivores. In addition, induced resistance may be a partic- ularly useful biological-control strategy because it reduces herbivorous pest populations directly, and indirectly by causing a shift toward predation in naturally occurring omnivores.

All plants pass through a series of predictable developmental stages during their lives, called phase changes. The phase change from juvenile to adult leaves is known to be associated with changes in resistance against plant pathogens and herbivores in several species. Virtually nothing is known about changes in resistance associated with the transition from embryonic tissue to autotrophic tissue in seedlings. We studied the consequences of transitions from cotyledons to juvenile true leaves to adult true leaves in cotton seedlings (Gossypium hirsutum) for their resistance to spider mites (Tetranychus urticae). Mite populations grew much more rapidly on cotyledons than on true leaves. However, there was no detectable difference in the population growth of mites on juvenile vs. adult true leaves. We suggest that population growth of mites is positively affected by the high rates of photosynthesis of cotyledons relative to true leaves, or by some process or attribute correlated with photosynthesis. Conditions that caused increased rates of photosynthesis (exposure to light and elevated concentrations of CO2) caused mite populations to increase. Greater mite population growth on cotyledons was not associated with stored reserves in the cotyledons, as the mites did poorly on cotyledons kept in the dark. This study indicates that phase changes can have profound effects on plant resistance to herbivores. Because the seedling stage is so vulnerable to herbivory and so critical to understanding plant population dynamics, a broader consideration of phase changes associated with seedlings is warranted.

Pathogens and insects can elicit different sets of plant host responses, supporting the hypothesis for control by different signaling pathways. To evaluate the potential for signal interaction in plants attacked by pathogens and insects, the mRNA abundance for lipoxygenase (LOX), a wound-inducible proteinase inhibitor (PINII), and a pathogenesis-related protein (P4) was evaluated in tomato leaves following challenge with a variety of agents. PINII and P4 expression was determined as these proteins are induced in tomato leaves characteristically following attack by certain insects or pathogens, respectively. Expression studies of LOX, PINII, and P4 indicate that their induction in tomato does not follow a strict pattern based on the type of biologic inducer (insect vs. pathogen) or chemical treatment, with each specific treatment inducing a distinct pattern of gene expression. However, plants induced to express disease resistance with the synthetic salicylate mimic benzothiadiazole-7-carbothioic acid S-methyl ester were compromised in their expression of the wound- or jasmonate-activated PINII, consistent with an observed increase in susceptibility to insect herbivory reported in a companion study. The results do not support the hypothesis for a strict dichotomy of signaling by insects and pathogens of LOX, PINII and P4 in tomato, but point to a potential vulnerability of acquired resistance evident at the levels of gene expression and response to insect attack.

Plants can be treated with natural plant elicitors to induce resistance to herbivores. To use elicitors in agriculture we must know the net effects of induction on plant yield. For 4 yr, I induced plant resistance to insect herbivores in tomato plants using the natural plant hormone jasmonic acid. Foliar jasmonic acid application increased levels of polyphenol oxidase, an oxidative enzyme implicated in resistance against several insect herbivores. Induced plants received 60% less leaf damage than did control plants. I then looked at the effects of this induction on seedling survivorship, phenology, fruit production, and plant biomass in the presence and absence of herbivores. Induced plants produced fewer flowers than control plants, but this did not translate into differences in yield between treatments. In addition, there was no difference in yield between induced and control plants under natural and experimentally reduced herbivore levels. This lack of effect on yield may have been caused by low levels of herbivory in the unmanipulated controls. Thus, it appears that jasmonic acid induces resistance in tomato plants and that this resistance produces no measurable costs to tomato plants. Elicitors such as jasmonic acid may be valuable pest management tools, especially when there are high densities of herbivores that can reduce yield.

Two signaling pathways, one involving salicylic acid and another involving jasmonic acid, participate in the expression of plant resistance to pathogens and insect herbivores. In this study, we report that stimulation of systemic acquired resistance in field-grown tomato plants with the salicylate mimic, benzothiadiazole: (1) attenuates the jasmonate-induced expression of the antiherbivore defense-related enzyme polyphenol oxidase, and (2) compromises host-plant resistance to larvae of the beet armyworm, Spodoptera exigua. Conversely, treatment of plants with jasmonic acid at concentrations that induce resistance to insects reduces pathogenesis-related protein gene expression induced by benzothiadiazole, and partially reverses the protective effect of benzothiadiazole against bacterial speck disease caused by Pseudomonas syringae pv. tomato. We conclude that effective utilization of induced plant resistance to the multiple pests typically encountered in agriculture will require understanding potential signaling conflicts in plant defense responses.

Plant defenses are assumed to play a critical role in directing the evolution of interactions between plants and their herbivores (Dethier 1954; Fraenkel 1959; Ehrlich and Raven 1964; Futuyma 1983; Feeny 1992; Futuyma and Keese 1992). Unfortunately, evaluating this assumption has proven to be exceedingly difficult. We know that plant traits can have strong effects on herbivores and that herbivores can exert strong selection on plants, but we have little evidence that plants have actually responded to that selection. The most obvious place to look for information about the evolutionary history of plant-herbivore interactions is the fossil record, but the fossil record is poor for plants and insects and provides few clues about the traits that plants have employed to defend themselves. A phylogenetic analysis can potentially provide some insight into how often and under what conditions resistance to herbivores may have evolved. For example, if a phylogenetic analysis revealed that plants in environments with more herbivory had evolved more defense, this would be valuable evidence indeed. Surprisingly few phylogenetic analyses of secondary compounds or other plant defenses have been attempted. We have performed an analysis of the distribution of induced and constitutive resistance of members of the genus Gossypium against a generalist and ubiquitous herbivore. Induced resistance differs from constitutive resistance in that induced resistance is activated or expressed only after the plant is attacked or otherwise injured; constitutive resistance is expressed independently of injury. Induced plant resistance against herbivores is a widespread phenomenon, having been reported for over a hundred plant species (Karban and Baldwin 1997). However, relatively little is known about the evolution of this phenomenon. Most evolutionary models of induced resistance treat it as a special, derived form of constitutive resistance, the presumed ancestral state (reviewed in Karban and Adler 1996; Karban and Baldwin 1997). However, the relationship between constitutive re

While plant species diversity can reduce herbivore densities and herbivory, little is known regarding how plant genotypic diversity alters resource utilization by herbivores. Here, we show that an invasive folivore—the Japanese beetle ( Popillia japonica )—increases 28 per cent in abundance, but consumes 24 per cent less foliage in genotypic polycultures compared with monocultures of the common evening primrose ( Oenothera biennis ). We found strong complementarity for reduced herbivore damage among plant genotypes growing in polycultures and a weak dominance effect of particularly resistant genotypes. Sequential feeding by P. japonica on different genotypes from polycultures resulted in reduced consumption compared with feeding on different plants of the same genotype from monocultures. Thus, diet mixing among plant genotypes reduced herbivore consumption efficiency. Despite positive complementarity driving an increase in fruit production in polycultures, we observed a trade-off between complementarity for increased plant productivity and resistance to herbivory, suggesting costs in the complementary use of resources by plant genotypes may manifest across trophic levels. These results elucidate mechanisms for how plant genotypic diversity simultaneously alters resource utilization by both producers and consumers, and show that population genotypic diversity can increase the resistance of a native plant to an invasive herbivore.

Wounding increases the levels and activities of several defense-related proteins in the foliage of the tomato plant,Lycopersicon esculentum Mill. Evidence indicates that two of these responses, the systemic increases in polyphenol oxidase and proteinase inhibitors, are regulated by an octadecanoid-based signalling pathway which includes the wound hormone, jasmonic acid. It is not known whether other responses to wounding are also regulated by this same signalling pathway. In this paper, we show that application of jasmonates (jasmonic acid or its volatile derivative, methyl jasmonate) in low concentrations to foliage of young tomato plants induced, in a dose-dependent manner, the same protein responses-polyphenol oxidase, proteinase inhibitors, lipoxygenase, and peroxidase-as doesHelicoverpa zea Boddie feeding. Application of jasmonic acid to a single leaflet of four-leaf tomato plants induced these four proteins in a spatial pattern nearly identical to that produced by localized feeding ofH. zea. Exogenous jasmonic acid also decreased suitability of foliage for the beet armyworm,Spodoptera exigua Hubner in the laboratory. Based on these results, we conducted an experiment to measure the effects of jasmonic acid spray under field conditions. We provide the first evidence that jasmonic acid spray on field plants induces production of chemical defenses above the levels found in unsprayed controls. Exogenous jasmonic acid sprayed on plants in agricultural plots increased levels of polyphenol oxidase and proteinase inhibitors. Because application of jasmonic acid induces these defensive compounds at low concentrations in a manner similar to natural wounding, it may prove to be a useful tool for stimulating plant resistance to insects in the field.

We observed the number of predatory mites (Phytoseiidae:Typhlodromus caudiglans) on the foliage of 20 North American species of grapes (Vitis spp) plus the domesticated EuropeanVitis vinifera, all grown in a common garden. We found relatively few phytophagous mites. The numbers of phytophagous mites were not correlated with the plant characteristics that we measured. We found approximately five times as many predatory mites as phytophagous mites and the numbers of these phytoseiid predators were not affected by the availability of prey. Similarly, numbers of phytoseiids were unaffected by plant gender and, hence, the availability of pollen, another source of food. The numbers of phytoseiids were not clustered according to the taxonomic grouping of the tested plant species. Leaf surface characteristics explained over 25% of the variance in the numbers of phytoseiids. Numbers of phytoseiids were positively associated with the density of vein hairs, the density of bristles in leaf axils, and the presence of leaf domatia. These results suggest that sheltered habitats rather than food availability may limit the numbers of phytoseiid mites on grapevines.

Plants are frequently attacked by both pathogens and insects, and an attack from one can induce plant responses that affect resistance to the other. However, we currently lack a predictive framework for understanding how pathogens, their vectors, and other herbivores interact. To address this gap, we have investigated the effects of a viral infection in the host plant on both its aphid vector and non-vector herbivores. We tested whether the infection by three different strains of Potato virus Y (PVY(NTN), PVY(NO) and PVY(O)) on tomato plants affected: (1) the induced plant defense pathways; (2) the abundance and fecundity of the aphid vector (Macrosiphum euphorbiae); and (3) the performance of two non-vector species: a caterpillar (Trichoplusia ni) and a beetle (Leptinotarsa decemlineata). While infection by all three strains of PVY induced the salicylate pathway, PVY(NTN) induced a stronger and longer response. Fecundity and density of aphids increased on all PVY-infected plants, suggesting that the aphid response is not negatively associated with salicylate induction. In contrast, the performance of non-vector herbivores positively correlated with the strength of salicylate induction. PVY(NTN) infection decreased plant resistance to both non-vector herbivores, increasing their growth rates. We also demonstrated that the impact of host plant viral infection on the caterpillar results from host plant responses and not the effects of aphid vector feeding. We propose that pathogens chemically mediate insect-plant interactions by activating the salicylate pathway and decreasing plant resistance to chewing insects, which has implications for both disease transmission and insect community structure.

Plants employ hormone-mediated signaling pathways to defend against pathogens and insects. We tested predictions about the relative effect of jasmonate and salicylate pathways and how they mediate interactions between pathogens and herbivores. We employed two pathogens of tomato, Pseudomonas syringae (Pst) and tobacco mosaic virus (TMV), that are known to elicit distinct components of the two pathways, and we address the consequences of their induction for resistance in wild-type and salicylate-deficient transgenic plants in field experiments. We report that Pst infection induced jasmonic acid and proteinase inhibitors (PIs), and reduced the growth of Spodoptera exigua caterpillars on wild-type and salicylate-deficient plants. Pst and TMV both induced salicylic acid in wild-type but not salicylate-deficient plants. Although TMV did not affect jasmonic acid or PIs, infection increased caterpillar growth on wild-type plants, but not on salicylate-deficient plants. Aphid population growth was higher on salicylate-deficient compared to wild-type plants, and lower on salicylate-induced plants compared to controls. Natural aphid colonization was reduced on TMV-infected wild types, but not on salicylate-deficient plants. In sum, jasmonate-mediated resistance is induced by some pathogens, independent of salicylate, and salicylate-mediated induction by other pathogens results in induced susceptibility to a chewer and resistance to an aphid. We conclude with a predictive model for the expression of defense pathways and their consequences.

Previous work identified aphids and caterpillars as having distinct effects on plant responses to herbivory. We sought to decipher these interactions across different levels of biological organization, i.e., molecular, biochemical, and organismal, with tomato plants either damaged by one 3rd-instar beet armyworm caterpillar (Spodoptera exigua), damaged by 40 adult potato aphids (Macrosiphum euphorbiae), simultaneous damaged by both herbivores, or left undamaged (controls). After placing insects on plants, plants were transferred to a growth chamber for 5 d to induce a systemic response. Subsequently, individual leaflets from non-damaged parts of plants were excised and used for gene expression analysis (microarrays and quantitative real-time PCR), C/N analysis, total protein analysis, proteinase inhibitor (PI) analysis, and for performance assays. At the molecular level, caterpillars up-regulated 56 and down-regulated 29 genes systemically, while aphids up-regulated 93 and down-regulated 146 genes, compared to controls. Although aphids induced more genes than caterpillars, the magnitude of caterpillar-induced gene accumulation, particularly for those associated with plant defenses, was often greater. In dual-damaged plants, aphids suppressed 27% of the genes regulated by caterpillars, while caterpillars suppressed 66% of the genes regulated by aphids. At the biochemical level, caterpillars induced three-fold higher PI activity compared to controls, while aphids had no effects on PIs either alone or when paired with caterpillars. Aphid feeding alone reduced the foliar C/N ratio, but not when caterpillars also fed on the plants. Aphid and caterpillar feeding alone had no effect on the amount of protein in systemic leaves; however, both herbivores feeding on the plant reduced the amount of protein compared to aphid-damaged plants. At the organismal level, S. exigua neonate performance was negatively affected by prior caterpillar feeding, regardless of whether aphids were present or absent. This study highlights areas of concordance and disjunction between molecular, biochemical, and organismal measures of induced plant resistance when plants are attacked by multiple herbivores. In general, our data produced consistent results when considering each herbivore separately but not when considering them together.

In many plants, defence systems against herbivores are induced through the octadecanoid pathway1,2, which may also be involved in recruiting natural enemies of herbivores3. This pathway can beinduced by treating plants with jasmonic acid4 or by natural herbivory, and increases resistance against herbivorous insects intomato plants5, in part by causing production of toxic and antinutritive proteinase inhibitors and oxidative enzymes6,7,8. Herbivore-infested tomato plants release increased amounts of volatiles9 and attract natural enemies of the herbivores10, as do other plants11,12,13,14,15. The octadecanoid pathway may regulate production of these volatiles, which attract host-seeking parasitic wasps16,17. However, plant resistance compounds can adversely affect parasitoids as well as herbivores18. It is unclear whether the combination of increased retention and/or attractiveness of parasitic wasps to induced plants and the adverse effects of plant defence compounds on both caterpillars and parasitoids results in a net increase in parasitization of herbivores feeding on induced plants.Here I show that inducing plants with jasmonic acid increases parasitism of caterpillar pests in an agricultural field twofold. Thus, elicitors of plant resistance may become useful in agriculture.