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Podisus maculiventris (spined soldier bug) is a generalist predator studied for its biocontrol potential. This species has a large dorsal abdominal gland (DAG) that releases pheromones that can also be important semiochemicals for other organisms. Despite our growing understanding of gland development, the conditions that elicit releases are largely unknown. To determine if male age or gland development affects the chemical composition and release behavior, we dissected adult male bugs and profiled the chemical composition of the male DAG 1, 7, and 14 d post-eclosion. To determine if gland development is related to sexual maturity, we counted the number of sperm present in the seminal vesicles at the same time points. Finally, we measured the diurnal release patterns of different aged males and in various male-female combinations. We observed that newly eclosed adults have under-developed glands and male seminal vesicles contained few sperm. One week post-eclosion the DAG contained previously reported pheromone compounds and males contained many sperm. Mirroring the trend in reproductive maturation and gland development, the number of pheromone releases increased with age and the majority of releases followed a scotophase pattern unaffected by sexual composition. These findings link male age to 1) dorsal abdominal gland development 2) release behavior and 3) sexual maturity, which will help our understanding of when these olfactory cues are present for other organisms, like prey, to perceive.

Despite the ubiquity of parental effects and their potential impact on evolutionary dynamics, their contribution to the evolution of ecologically relevant adaptations remains poorly understood. Using quantitative genetics, here we demonstrate that parental effects contribute substantially to the evolutionary potential of larval antipredator responses in a leaf beetle (Leptinotarsa decemlineata). Previous research showed that larger L. decemlineata larvae elicit stronger antipredator responses, and mothers perceiving predators improved offspring responses by increasing intraclutch cannibalism –an extreme form of offspring provisioning. We now report substantial additive genetic variation underlying maternal ability to induce intraclutch cannibalism, indicating the potential of this adaptive maternal effect to evolve by natural selection. We also show that paternal size, a heritable trait, impacted larval responses to predation risk, but that larval responses themselves had little additive genetic variation. Together, these results demonstrate how larval responses to predation risk can evolve via two types of parental effects, both of which provide indirect sources of genetic variation for offspring traits.

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.

The risk of consumption is a pervasive aspect of ecology and recent work has focused on synthesis of consumer-resource interactions (e.g., enemy-victim ecology). Despite this, theories pertaining to the timing and magnitude of defenses in animals and plants have largely developed independently. However, both animals and plants share the common dilemma of uncertainty of attack, can gather information from the environment to predict future attacks and alter their defensive investment accordingly. Here, we present a novel, unifying framework based on the way an organism's ability to defend itself during an attack can shape their pre-attack investment in defense. This framework provides a useful perspective on the nature of information use and variation in defensive investment across the sequence of attack-related events, both within and among species. It predicts that organisms with greater proportional fitness loss if attacked will gather and respond to risk information earlier in the attack sequence, while those that have lower proportional fitness loss may wait until attack is underway. This framework offers a common platform to compare and discuss consumer effects and provides novel insights into the way risk information can propagate through populations, communities, and ecosystems.

Insect herbivores express tremendous ontogenetic variation in traits related to growth and maturation, but also as an evolutionary consequence of ecological interactions with plants and predators. These selective pressures can either reinforce or restrict expression of particular ontogenetic strategies, allowing herbivores to simultaneously cope with plant resistance and risk of predation through ontogenetic change. For example, whereas an increase in defense-sabotaging behavior, aposematism and sequestration along herbivore ontogeny seems to be reinforced by both bottom-up and top-down forces, some ontogenetic trends in anti-predator behavior can be limited by plant resistance. Communication among plants, herbivores and their natural enemies is also influenced by insect ontogenies. The study of ontogenetic strategies of herbivores requires the assessment of the genetic variation, heritability and adaptive value across herbivore development, considering the variation in plant quality and predation risk.

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.

Theory on condition-dependent risk-taking indicates that when prey are in poor condition, their anti-predator responses should be weak. However, variation in responses resulting from differences in condition is generally considered an incidental by-product of organisms living in a heterogeneous environment. Using Leptinotarsa decemlineata beetles and stinkbug (Podisus maculiventris) predators, we hypothesised that in response to predation risk, parents improve larval nutritional condition and expression of anti-predator responses by promoting intraclutch cannibalism. We showed that mothers experiencing predation risk increase production of unviable trophic eggs, which assures provisioning of an egg meal to the newly hatched offspring. Next, we experimentally demonstrated that egg cannibalism reduces L. decemlineata vulnerability to predation by improving larval nutritional condition and expression of anti-predator responses. Intraclutch cannibalism in herbivorous insects might be a ubiquitous strategy, aimed to overcome the dual challenge of feeding on protein-limited diets while living under constant predation threat.

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.

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.

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.

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.

Variability in plant chemistry has long been believed to suppress populations of insect herbivores by constraining herbivore resource selection behavior in ways that make herbivores more vulnerable to predation. The focus on behavior, however, overlooks the pervasive physiological effects of plant variability on herbivores. Here we propose the plant variability-gut acclimation hypothesis, which posits that plant chemical variability constrains herbivore anti-predator defenses by frequently requiring herbivores to acclimate their guts to changing plant defenses and nutrients. Gut acclimation, including changes to morphology and detoxification enzymes, requires time and nutrients, and we argue these costs will constrain how and when herbivores can mount anti-predator defenses. A consequence of this hypothesis is stronger top-down control of herbivores in heterogeneous plant populations.

Chemical ecology is a mechanistic approach to understanding the causes and consequences of species interactions, distribution, abundance, and diversity. The promise of chemical ecology stems from its potential to provide causal mechanisms that further our understanding of ecological interactions and allow us to more effectively manipulate managed systems. Founded on the notion that all organisms use endogenous hormones and chemical compounds that mediate interactions, chemical ecology has flourished over the past 50 years since its origin. In this essay we highlight the breadth of chemical ecology, from its historical focus on pheromonal communication, plant-insect interactions, and coevolution to frontier themes including community and ecosystem effects of chemically mediated species interactions. Emerging approaches including the -omics, phylogenetic ecology, the form and function of microbiomes, and network analysis, as well as emerging challenges (e.g., sustainable agriculture and public health) are guiding current growth of this field. Nonetheless, the directions and approaches we advocate for the future are grounded in classic ecological theories and hypotheses that continue to motivate our broader discipline.

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.

One goal of phytohormonal ecology is to study the interactions between biotic and abiotic stress at hierarchical levels of biological organization. From an ecological perspective, exposure to one stress may alter the plant's probability of being exposed to another stress. From a mechanistic perspective, hormonal and biochemical signaling in- teractions between responses to each stress may influence the severity or ability to adaptively respond to the subsequent stress. In this article, we consider the relationship between plant water and salt stress and attack by pathogens and herbivores. Empirical data suggest that water stress and the probability of attack by pathogens and herbivores are correlated between habitats. Biochemical interactions between plant responses to water and salt stress and insect and pathogen attack are also interrelated. Initial biochemical models indicated that abscisic acid (ABA), an important hormone in responses to water and salt stress, had a synergistic positive role with jasmonate-induced defenses against herbivores and an an- tagonistic role with salicylate-based resistance to some pathogens. Based on this back- ground, we developed predictions about how water and salt stress would alter plant resis- tance to insects and pathogens and tested the predictions using tomato plants as a model system. We used polyphenol oxidase activity as a marker of the jasmonate response and pathogenesis-related protein P4 as a marker of the salicylate response. First, we examined levels of chemical defense in wild-type and ABA-deficient plants and the ability of these plants to resist insect and pathogen attack. In the second experiment, we exposed plants to short-term salinity stress and tested their subsequent resistance to a chewing insect Spodoptera exigua and the bacterial speck pathogen Pseudomonas syringae pv. tomato. We have two key findings. First, ABA-deficient plants had higher levels of salicylate-mediated responses and were more resistant to bacterial speck disease, consistent with the proposed role of salicylate in defense against pathogens. This suggests linkage between water avail- ability to the plant and salicylate action in pathogenesis through ABA signaling. ABA- deficient plants had reduced resistance to the insect Spodoptera exigua, suggesting a positive correlation between responses to water stress and herbivory. The lack of difference in chemical expression of the jasmonate (JA) response (polyphenol oxidase activity) between wild-type and ABA-deficient plants did not support the proposed mechanism of synergism with the jasmonate response. Second, salt stress reduced the chemical induction (e.g., pathogenesis-related protein P4) of the salicylate response, but this did not affect resistance to the pathogen. Salt stress did not alter resistance to the herbivore Trichoplusia ni, but did alter the negative signal interaction between the jasmonate and salicylate responses. Under control conditions, the jasmonate and salicylate responses are antagonistic to one another, with induction of one response reducing the inducibility of the other. Under salt stress conditions, the negative effect of salicylate on the jasmonate response was reduced. Thus, complex interactions occur between ABA, JA, and SA, hormones that are important regulators of abiotic and biotic stress responses. Phytohormonal ecology is attempting to link ecological and hormonal interactions to develop a predictive framework for how and why plants coordinate responses to the environment.

Plants employ a variety of defence mechanisms, some of which act directly by having a negative effect on herbivores and others that act indirectly by attracting natural enemies of herbivores. In this study we asked if a common jasmonate-signalling pathway links the regulation of direct and indirect defences in plants. We examined the performance of herbivores (direct defence) and the attraction of natural enemies of herbivores (indirect defence) to wild-type tomato plants and mutant plants that are deficient in the production of the signalling hormone jasmonic acid. Wild-type plants supported lower survivorship of caterpillars compared with jasmonic acid-deficient plants. Damaged wild-type plants were more attractive to predaceous mites compared with undamaged wild-type plants, whereas damaged jasmonate-deficient plants were not more attractive to predators. Damaged wild-type plants induced a greater production of volatile compounds (primarily the sesquiterpene β-caryophyllene and the monoterpenes α-pinene, β-pinene, 2-carene and β-phellandrene) compared with damaged jasmonatedeficient plants. Treating jasmonate-deficient plants with exogenous jasmonic acid restored both the direct and indirect defence capabilities, demonstrating that jasmonic acid is an essential regulatory component for the expression of direct and indirect plant defence.

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.

Herbivores can greatly reduce plant fitness. Error management theory (EMT) predicts the evolution of adaptive plant defensive strategies that err towards making less-costly errors so as to avoid making rare, costly errors. EMT provides a common framework for understanding observed levels of variation in plant defense among and within species.

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.

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.

Plant defenses are plastic when a single genotype can produce different phenotypes depending upon the environment. Plastic responses might be favored by selection only if plants can respond appropriately to reliable information in their environments. Recent findings indicate that when information is accurate, plants can benefit by changing their defenses appropriately but, when information is inaccurate they produce inappropriate defenses and have lower fitness. Plants can potentially use a variety of cues to adjust their defensive phenotypes appropriately. The relationship between the information about risk of herbivory and plant defense can be evaluated by determining if the information available to plants is reliable enough to support the evolution of plastic-induced defenses.

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.

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

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.

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.

Biodiversity loss is proceeding at an unprecedented rate, yet we lack a thorough understanding of the consequences of losing diversity at different scales. While species diversity is known to impact community and ecosystem processes, genotypic diversity is assumed to have relatively smaller effects. Nonetheless, a few recent studies suggest that genotypic diversity may have quantitatively similar ecological consequences compared to species diversity. Here we show that increasing either genotypic diversity of common evening primrose (Oenothera biennis) or species diversity of old-field plant species resulted in nearly equivalent increases (approximately 17%) in aboveground primary production. The predominant mechanism explaining this effect, niche complementarity, was similar for each type of diversity. Arthropod species richness also increased with both types of plant diversity, but the mechanisms leading to this effect differed: abundance-driven accumulation of arthropod species was important in plant genotypic polycultures, whereas resource specialization was important in plant species polycultures. Thus, similar increases in primary productivity differentially impacted higher trophic levels in response to each type of plant diversity. These results highlight important ecological similarities and differences between genotypic and species diversity and suggest that genotypic diversity may play a larger role in community and ecosystem processes than previously realized.

Biodiversity is quantified via richness (e.g., the number of species), evenness (the relative abundance dis- tribution of those species), or proportional diversity (a combination of richness and evenness, such as the Shannon index, H 0 ). While empirical studies show no consistent relationship between these aspects of biodiversity within communities, the mechanisms leading to inconsistent relationships have received little attention. Here, using common evening primrose (Oenothera biennis) and its associated arthropod community, we show that relation- ships between arthropod richness, evenness, and propor- tional diversity are altered by plant genotypic richness. Arthropod richness increased with O. biennis genotypic richness due to an abundance-driven accumulation of species in response to greater plant biomass. Arthropod evenness and proportional diversity decreased with plant genotypic richness due to a nonadditive increase in abun- dance of a dominant arthropod, the generalist florivore/ omnivore Plagiognathas politus (Miridae). The greater quantity of flowers and buds produced in polycultures— which resulted from positive complementarity among O. biennis genotypes—increased the abundance of this dominant insect. Using choice bioassays, we show that floral quality did not change in plant genotypic mixtures. These results elucidate mechanisms for how plant geno- typic richness can modify relationships between arthropod richness, evenness, and proportional diversity. More broadly, our results suggest that trophic interactions may be a previously underappreciated factor controlling relation- ships between these different aspects of biodiversity.

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.

▪ Abstract Plant-mediated interactions between pathogenic microorganisms and arthropod herbivores occur when arthropod infestation or pathogen infection changes the shared host plant in ways that affect a subsequent attacker of the opposite type. Interest in such “tripartite” interactions has increased as the ecological and plant physiological framework for understanding and contextualizing them has developed. The outcomes of plant-mediated interactions are variable, and only a few provisional patterns can be identified at present. However, these interactions can have important consequences not only for individual pathogens and herbivores, but also for the population dynamics of both types of organisms in managed and natural ecosystems. Research has focused on the role of two plant response pathways in mediating tripartite interactions, one involving jasmonic acid and the other salicylic acid. Further studies of plant-mediated interactions will facilitate an understanding of how plants coordinate and integrate their defenses against multiple biotic threats.

Herbivore-induced plants responses can affect the preference and performance of herbivores and their natural enemies. These responses may vary depending on the identity and number of herbivore species feeding on the plant so that when herbivores from different guilds feed on plants, the interactions between plants, herbivores, and natural enemies may be disrupted. Tomato plants were damaged either by the caterpillar Spodoptera exigua, or the aphid Macrosiphum euphorbiae, or damaged by both herbivores, or undamaged controls. We measured the preference and performance of S. exigua and its parasitoid Cotesia marginiventris, and activity of proteinase inhibitors (PI) as an indicator of induced resistance. Compared to undamaged plants, caterpillar damage reduced the number of eggs laid by S. exigua adults, reduced growth, consumption, and survival of larval S. exigua and C. marginiventris, and increased activity of PIs 43%; but did not increase attraction of C. marginiventris. While pupal mass of S. exigua was not affected, the pupal mass of C. marginiventris decreased on caterpillar-damaged plants compared to controls. In contrast, plants damaged by aphids were preferred for oviposition by S. exigua, and had increased larval consumption and survival, compared to controls. Aphid feeding did not affect the preference or performance of C. marginiventris, or PI activity, compared to controls. While oviposition was deterred on caterpillar-damaged plants, plants damaged by both herbivores received the same amount of oviposition as controls. The attraction of C. marginiventris to plants damaged by caterpillars and aphids was increased compared to controls. However, plants damaged by both herbivores had similar PI activity, larval growth and survival of S. exigua and C. marginiventris, as plants singly damaged by caterpillars. Overall, the preference component for both the herbivore and parasitoid was more strongly affected by damage due to multiple herbivores than the performance component.

In this study, we used plant vascular architecture as a framework from which to predict induced changes in resource quality for Lema trilinea feeding on the host plant Solanum dulcamara at both low and high levels of herbivory. The systemic patterns of allocation of dye from a capillary tube inserted onto the petiole of the first true leaf and sections of the stem were used to establish the degree of vascular connectivity among different leaf positions. Induced changes in the activity of two defensive proteins, proteinase inhibitor (PI) and polyphenol oxidase (PPO), as well as larval L. trilinea performance, were measured in weakly or strongly connected leaves on plants with the first leaf damaged or undamaged by adult L. trilinea. At high levels of herbivory, larval performance decreased on the sixth leaf, which has strong vascular connections to the first leaf, yet increased on the fifth leaf, which has weak vascular connections to the first leaf. PPO activity increased in both the fifth and sixth leaf, while PI activity decreased in the fifth leaf although remaining unchanged in the sixth leaf. At low levels of herbivory, a decrease in larval performance was observed in the sixth leaf, but no change occurred in the weakly connected fifth leaf. Hence, plant vascular architecture clearly predicted within-plant changes in resource quality following only small amounts of herbivore damage.

Plants are often attacked by many herbivorous insects and pathogens at the same time. Two important suites of responses to attack are mediated by plant hormones, jasmonate and salicylate, which independently provide resistance to herbivorous insects and pathogens, respectively. Several lines of evidence suggest that there is negative cross-talk between the jasmonate and salicylate response pathways. This biochemical link between general plant defense strategies means that deploying defenses against one attacker can positively or negatively affect other attackers. In this study, we tested for cross-talk in the jasmonate and salicylate signaling pathways in a wild tomato and examined the effects of cross-talk on an array of herbivores of cultivated tomato plants. In the wild cultivar, induction of defenses signaled by salicylate reduced biochemical expression of the jasmonate pathway but did not influence performance of S. exigua caterpillars. This indicates that the signal interaction is not a result of agricultural selection. In cultivated tomato, biochemical attenuation of the activity of a defense protein (polyphenol oxidase) in dual-elicited plants resulted in increased of performance of cabbage looper caterpillars, but not thrips, spider mites, hornworm caterpillars or the bacteria Pseudomonas syringae pv. tomato. In addition, we tested the effects of jasmonate-induced resistance on the ability of thrips to vector tomato spotted wilt virus. Although thrips fed less on induced plants, this did not affect the level of disease. Thus, the negative interaction between jasmonate and salicylate signaling had biological consequences for two lepidopteran larvae but not for several other herbivores tested or on the spread of a disease.