Aphid-Induced Volatiles and Subsequent Attraction of Natural Enemies Varies among Sorghum Cultivars.

The production of herbivore-induced plant volatiles (HIPVs) is a type of indirect defense used by plants to attract natural enemies and reduce herbivory by insect pests. In many crops little is known about genotypic variation in HIPV production or how this may affect natural enemy attraction. In this study, we identified and quantified HIPVs produced by 10 sorghum (Sorghum bicolor) cultivars infested with a prominent aphid pest, the sorghum aphid (Melanaphis sorghi Theobald). Volatiles were collected using dynamic headspace sampling techniques and identified and quantified using GC-MS. The total amounts of volatiles induced by the aphids did not differ among the 10 cultivars, but overall blends of volatiles differed significantly in composition. Most notably, aphid herbivory induced higher levels of methyl salicylate (MeSA) emission in two cultivars, whereas in four cultivars, the volatile emissions did not change in response to aphid infestation. Dual-choice olfactometer assays were used to determine preference of the aphid parasitoid, Aphelinus nigritus, and predator, Chrysoperla rufilabris, between plants of the same cultivar that were un-infested or infested with aphids. Two aphid-infested cultivars were preferred by natural enemies, while four other cultivars were more attractive to natural enemies when they were free of aphids. The remaining four cultivars elicited no response from parasitoids. Our work suggests that genetic variation in HIPV emissions greatly affects parasitoid and predator attraction to aphid-infested sorghum and that screening crop cultivars for specific predator and parasitoid attractants has the potential to improve the efficacy of biological control.

Landscape Complexity has Mixed Effects on an Invasive Aphid and Its Natural Enemies in Sorghum Agroecosystems.

Landscapes with more complex composition and configuration are generally expected to enhance natural enemy densities and pest suppression. To evaluate this hypothesis for an invasive aphid pest of sorghum, Melanaphis sorghi Theobald (Hemiptera: Aphididae), sampling in sorghum fields for aphids and natural enemies was conducted over two years in a southern U.S. coastal production region. Landscape composition and configuration of crop and noncrop elements were assessed using correlation and multivariate regression modeling to detect relationships with insects at different spatial scales. Significant models found more complex landscape configuration, particularly the amount of habitat edges, was associated with increased aphid and natural enemy abundance. Composition associated with noncrop habitats had the opposite effect. Numerical response of natural enemies was taxa dependent, with parasitism lower as landscape complexity increased, while predator numerical response was not affected by landscape complexity. These results indicate landscape complexity may increase both aphid and natural enemy abundance, but with decreasing parasitism and little association with predator numerical response. These relationships are likely contingent on overall environmental suitability to aphid population increase as results were less evident in the second year when average aphid abundance regularly exceeded the economic threshold. This study supports the importance of configuration, especially habitat borders, as a critical metric for determining pest-natural enemy dynamics within a large-scale cereal agroecosystem.

The discrepancy between fire ant recruitment to and performance on rodent carrion.

Ants have not been considered important in the process of vertebrate carrion decomposition, but a recent literature review reported over 150 carrion-visiting ant species. Though many ant species have been observed to remove carrion tissue and consume carrion-exuded liquids, the significance of ant recruitment to vertebrate carrion is poorly understood. We conducted a combination of field and laboratory experiments to quantify red imported fire ant recruitment to rodent carrion and determine whether consuming rodent carrion is beneficial to ant colony performance. In the field, 100% of rat carcasses were rapidly colonized by fire ants at high abundances. In our laboratory experiment, the performance of mice-fed fire ant colonies was poor when compared to colonies that were fed mice and insects or insects only. Our results suggest that there is a discrepancy between high levels of fire ant recruitment to vertebrate carrion and the poor colony performance when fed carrion. We hypothesize that fire ants are attracted to vertebrate carrion not because it is a high-quality food, but rather because it hosts large numbers of other invertebrates that can serve as prey for fire ants, potentially showcasing an interesting case of tritrophic interaction in carrion ecology.

Distinct colony boundaries and larval discrimination in polygyne red imported fire ants (Solenopsis invicta).

Evaluating the factors that promote invasive ant abundance is critical to assess their ecological impact and inform their management. Many invasive ant species show reduced nestmate recognition and an absence of boundaries between unrelated nests, which allow populations to achieve greater densities due to reduced intraspecific competition. We examined nestmate discrimination and colony boundaries in introduced populations of the red imported fire ant (Solenopsis invicta; hereafter, fire ant). Fire ants occur in two social forms: monogyne (colonies with a single egg-laying queen) and polygyne (colonies with multiple egg-laying queens). In contrast with monogyne nests, polygyne nests are thought to be interconnected due to the reduced antagonism between non-nestmate polygyne workers, perhaps because polygyne workers habituate the colony to an odour unique to Gp-9b -carrying adults. However, colony boundaries and nestmate discrimination are poorly documented, particularly for worker-brood interactions. To delimit boundaries between field colonies, we correlated the exchange of a 15 N-glycine tracer dissolved in a sucrose solution with social form. We also evaluated nestmate discrimination between polygyne workers and larvae in the laboratory. Counter to our expectations, polygyne colonies behaved identically to monogyne colonies, suggesting both social forms maintain strict colony boundaries. Polygyne workers also preferentially fed larval nestmates and may have selectively cannibalized non-nestmates. The levels of relatedness among workers in polygyne colonies was higher than those previously reported in North America (mean ± standard error: 0.269 ± 0.037). Our study highlights the importance of combining genetic analyses with direct quantification of resource exchange to better understand the factors influencing ant invasions.

Crop and Semi-Natural Habitat Configuration Affects Diversity and Abundance of Native Bees (Hymenoptera: Anthophila) in a Large-Field Cotton Agroecosystem.

The cotton agroecosystem is one of the most intensely managed, economically and culturally important fiber crops worldwide, including in the United States of America (U.S.), China, India, Pakistan, and Brazil. The composition and configuration of crop species and semi-natural habitat can have significant effects on ecosystem services such as pollination. Here, we investigated the local-scale effect of crop and semi-natural habitat configuration in a large field (>200 ha in size) cotton agroecosystem on the diversity and abundance of native bees. The interfaces sampled included cotton grown next to cotton, sorghum or semi-natural habitat along with a natural habitat comparator. Collections of native bees across interface types revealed 32 species in 13 genera across 3 families. Average species richness metrics ranged between 20.5 and 30.5, with the highest (30.5) at the interface of cotton and semi-natural habitat. The most abundant species was Melissodes tepaneca Cresson (>4000 individuals, ~75% of bees collected) with a higher number of individuals found in all cotton-crop interfaces compared to the cotton interface with semi-natural habitat or natural habitat alone. It was also found that interface type had a significant effect on the native bee communities. Communities of native bees in the cotton-crop interfaces tended to be more consistent in species richness and abundance. While cotton grown next to semi-natural habitat had higher species richness, the number of bees collected varied. These data suggest that native bee communities persist in large-field cotton agroecosystems. Selected species dominate (i.e., M. tepaneca) and thrive in this large-field cotton system where cotton-crop interfaces are key local landscape features. These data have implications for potential pollination benefits to cotton production. The findings also contribute to a discussion regarding the role of large-field commercial cotton growing systems in conserving native bees.

Adding a Natural Enemy to Respond to Pest Immigration and Delayed Natural Enemy Releases in Augmentative Biological Control.

Whether increased natural enemy density or adding a second natural enemy species will provide superior pest suppression in greenhouse augmentative biological control is unknown for many commercially available natural enemy species. In this study, we use sweetpotato whiteflies, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), on poinsettias, Euphorbia pulcherrima Willd. ex Klotzsch (Malpighiales: Euphorbiaceae), to determine whether adding Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae) to Eretmocerus eremicus Rose and Zolnerowich (Hymenoptera: Aphelinidae) is better for B. tabaci suppression compared with either natural enemy alone, both with and without challenges with whitefly immigration or delayed natural enemy releases. The number of whiteflies on caged poinsettias treated with different natural enemy release rates (single or double rate), natural enemy species (one or two species), natural enemy delayed release (weeks 4 and 8), and whitefly immigration treatments (introduced at week 4 or week 8) was censused biweekly for 16 wk. Both species used in combination provided similar or better suppression of whiteflies compared with either natural enemy alone. Both species combined also provided superior suppression of whiteflies when challenged with whitefly immigration or delays in natural enemy releases compared with E. eremicus alone. Whitefly immigration or delays in E. eremicus releases did not increase whitefly populations, suggesting that suppression of whiteflies by E. eremicus alone is relatively robust. This study found no evidence for negative interactions between E. eremicus and A. swirskii for suppressing B. tabaci.

Generalising indirect defence and resistance of plants.

Indirect defence, the adaptive top-down control of herbivores by plant traits that enhance predation, is a central component of plant-herbivore interactions. However, the scope of interactions that comprise indirect defence and associated ecological and evolutionary processes has not been clearly defined. We argue that the range of plant traits that mediate indirect defence is much greater than previously thought, and we further organise major concepts surrounding their ecological functioning. Despite the wide range of plant traits and interacting organisms involved, indirect defences show commonalities when grouped. These categories are based on whether indirect defences boost natural enemy abundance via food or shelter resources, or, alternatively, increase natural enemy foraging efficiency via information or alteration of habitat complexity. The benefits of indirect defences to natural enemies should be further explored to establish the conditions in which indirect defence generates a plant-natural enemy mutualism. By considering the broader scope of plant-herbivore-natural enemy interactions that comprise indirect defence, we can better understand plant-based food webs, as well as the evolutionary processes that have shaped them.

Sugar Feeding Patterns for Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae) Mosquitoes in South Texas.

Effective mosquito surveillance and management depend on a thorough understanding of the biology and feeding patterns unique to species and sex. Given that a propensity to sugar feed is necessary for some mosquito surveillance and newer control strategies, we sought to document the amount of total sugar in wild Aedes aegypti (L.) and Culex quinquefasciatus (Say) captured from five different locations in the Lower Rio Grande Valley (LRGV) of South Texas over 2 yr. We used Biogents Sentinel 2 (BGS2) traps in year 1 and aspirators, BGS2, and CDC resting traps in years 2 and 3 to collect adult mosquitoes. The hot anthrone test was used to quantify total sugar content in each mosquito. Additionally, the cold and hot anthrone tests were used to distinguish fructose content from total sugars for mosquitoes captured in 2019. Overall, Ae. aegypti females had significantly lower total sugar content than Ae. aegypti males as well as both sexes of Cx. quinquefasciatus. However, the percentage of Ae. aegypti positive for fructose consumption was four to eightfold higher than Ae. aegypti previously reported in other regions. The difference between locations was significant for males of both species, but not for females. Seasonality and trapping method also revealed significant differences in sugar content of captured mosquitoes. Our results reinforce that sugar feeding in female Ae. aegypti is less than Cx. quinquefasciatus, although not absent. This study provides necessary data to evaluate the potential effectiveness of sugar baits in surveillance and control of both Ae. aegypti and Cx. quinquefasciatus mosquitoes.

Red imported fire ant (Solenopsis invicta) aggression influences the behavior of three hard tick species.

Few studies have documented the indirect effects of predators on tick behavior. We conducted behavioral assays in the laboratory to quantify the effects of a highly abundant predator, the red imported fire ant (Solenopsis invicta), on three species of ticks endemic to the southern USA: the lone star tick (Amblyomma americanum), the Gulf Coast tick (A. maculatum), and the Cayenne tick (A. mixtum). We documented ant aggression toward ticks (biting, carrying, and stinging) and determined the effects of ants on tick activity. Ticks were significantly less active in the presence of fire ants, and tick activity was negatively associated with ant aggression, but in many cases the effects of fire ants on ticks varied by tick species, stage, and engorgement status. For example, fire ants took half as long (~ 62 s) to become aggressive toward unfed A. americanum adults compared with unfed A. maculatum, and only ~ 8 s to become aggressive toward engorged A. maculatum nymphs. Correspondingly, the activity of unfed A. americanum adults and engorged A. maculatum nymphs was reduced by 67 and 93%, respectively, in the presence of fire ants. This reduction in tick activity translated to less questing by unfed ticks and less time spent walking by engorged nymphs. Our results suggest that fire ants may have important non-consumptive effects on ticks and demonstrate the importance of measuring the indirect effects of predators on tick behavior.

Neonicotinoid Insecticides Alter the Transcriptome of Soybean and Decrease Plant Resistance.

Neonicotinoids are widely used systemic insecticides that have been associated with spider mite outbreaks on diverse plants. These insecticides have complex effects on plant physiology, which have been speculated to drive enhanced performance of spider mites. We used RNA-Seq to explore how neonicotinoids modify gene expression in soybean thereby lowering plant resistance. We exposed soybean (Glycine max L.) to two neonicotinoid insecticides, thiamethoxam applied to seeds and imidacloprid applied as a soil drench, and we exposed a subset of these plants to spider mites (Tetranychus cinnabarinus). Applications of both insecticides downregulated genes involved in plant-pathogen interactions, phytohormone pathways, phenylpropanoid pathway, and cell wall biosynthesis. These effects were especially pronounced in plants exposed to thiamethoxam. Introduction of spider mites restored induction of genes in these pathways in plants treated with imidacloprid, while expression of genes involved in phenylpropanoid synthesis, in particular, remained downregulated in thiamethoxam-treated plants. Our outcomes indicate that both insecticides suppress genes in pathways relevant to plant⁻arthropod interactions, and suppression of genes involved in cell wall synthesis may explain lower plant resistance to spider mites, cell-content feeders. These effects appear to be particularly significant when plants are exposed to neonicotinoids applied to soybean seeds.

Overcompensation for insect herbivory: a review and meta-analysis of the evidence.

Not all herbivory is detrimental to plants. In some cases, plants can compensate for herbivory, maintain growth and fitness following damage, or even overcompensate for herbivory and perform better than if left undamaged. Examples of overcompensation to vertebrate herbivory are well known, but here we review the literature for examples of reproductive overcompensation (i.e., increased production of traits associated with fitness) and increased vegetative growth (i.e., vegetative overcompensation) following insect herbivory. We used a meta-analysis to explore the effects of plant growth form, evolutionary history, herbivore feeding guild, and other plant and insect traits on the expression of reproductive and vegetative overcompensation by plants. Our literature search revealed 86 studies documenting examples of overcompensation for insect herbivory by 67 plant species representing 26 families. These plants included monocots and dicots, annuals and perennials, and woody and herbaceous plants. We also found that varied insect herbivores induce overcompensation, including 75 insect species in six orders representing 27 families and myriad feeding guilds. In our meta-analysis, we calculated 53 effect sizes from 21 publications documenting reproductive overcompensation and 89 effect sizes from 40 publications documenting vegetative overcompensation. Variation in reproductive overcompensation was seen among plant growth forms, functional groups, cultivation, herbivore feeding sites, and plant and herbivore families. Variation in vegetative overcompensation was seen among plant families, herbivore families, and latitudinal gradients. We suggest overcompensation for insect herbivory may be far more prevalent than previously thought. Additional research focusing on the mechanisms, patterns, and ecological and evolutionary consequences of overcompensation for insect herbivory is likely to provide exciting new insights into this poorly understood and largely overlooked outcome of plant-insect interactions.

Colony-level behavioural variation correlates with differences in expression of the foraging gene in red imported fire ants.

Among social insects, colony-level variation is likely to be widespread and has significant ecological consequences. Very few studies, however, have documented how genetic factors relate to behaviour at the colony level. Differences in expression of the foraging gene have been associated with differences in foraging and activity of a wide variety of organisms. We quantified expression of the red imported fire ant foraging gene (sifor) in workers from 21 colonies collected across the natural range of Texas fire ant populations, but maintained under standardized, environmentally controlled conditions. Colonies varied significantly in their behaviour. The most active colonies had up to 10 times more active foragers than the least active colony and more than 16 times as many workers outside the nest. Expression differences among colonies correlated with this colony-level behavioural variation. Colonies with higher sifor expression in foragers had, on average, significantly higher foraging activity, exploratory activity and recruitment to nectar than colonies with lower expression. Expression of sifor was also strongly correlated with worker task (foraging vs. working in the interior of the nest). These results provide insight into the genetic and physiological processes underlying collective differences in social behaviour. Quantifying variation in expression of the foraging gene may provide an important tool for understanding and predicting the ecological consequences of colony-level behavioural variation.

Decreased small mammal and on-host tick abundance in association with invasive red imported fire ants (Solenopsis invicta).

Invasive species may impact pathogen transmission by altering the distributions and interactions among native vertebrate reservoir hosts and arthropod vectors. Here, we examined the direct and indirect effects of the red imported fire ant (Solenopsis invicta) on the native tick, small mammal and pathogen community in southeast Texas. Using a replicated large-scale field manipulation study, we show that small mammals were more abundant on treatment plots where S. invicta populations were experimentally reduced. Our analysis of ticks on small mammal hosts demonstrated a threefold increase in the ticks caught per unit effort on treatment relative to control plots, and elevated tick loads (a 27-fold increase) on one common rodent species. We detected only one known human pathogen (Rickettsia parkeri), present in 1.4% of larvae and 6.7% of nymph on-host Amblyomma maculatum samples but with no significant difference between treatment and control plots. Given that host and vector population dynamics are key drivers of pathogen transmission, the reduced small mammal and tick abundance associated with S. invicta may alter pathogen transmission dynamics over broader spatial scales.

Summer and fall ants have different physiological responses to food macronutrient content.

Seasonally, long-lived animals exhibit changes in behavior and physiology in response to shifts in environmental conditions, including food abundance and nutritional quality. Ants are long-lived arthropods that, at the colony level, experience such seasonal shifts in their food resources. Previously we reported summer- and fall-collected ants practiced distinct food collection behavior and nutrient intake regulation strategies in response to variable food protein and carbohydrate content, despite being reared in the lab under identical environmental conditions and dietary regimes. Seasonally distinct responses were observed for both no-choice and choice dietary experiments. Using data from these same experiments, our objective here is to examine colony and individual-level physiological traits, colony mortality and growth, food processing, and worker lipid mass, and how these traits change in response to variable food protein-carbohydrate content. For both experiments we found that seasonality per se exerted strong effects on colony and individual level traits. Colonies collected in the summer maintained total worker mass despite high mortality. In contrast, colonies collected in the fall lived longer, and accumulated lipids, including when reared on protein-biased diets. Food macronutrient content had mainly transient effects on physiological responses. Extremes in food carbohydrate content however, elicited a compensatory response in summer worker ants, which processed more protein-biased foods and contained elevated lipid levels. Our study, combined with our previously published work, strongly suggests that underlying physiological phenotypes driving behaviors of summer and fall ants are likely fixed seasonally, and change circannually.

Intraspecific Variation among Social Insect Colonies: Persistent Regional and Colony-Level Differences in Fire Ant Foraging Behavior.

Individuals vary within a species in many ecologically important ways, but the causes and consequences of such variation are often poorly understood. Foraging behavior is among the most profitable and risky activities in which organisms engage and is expected to be under strong selection. Among social insects there is evidence that within-colony variation in traits such as foraging behavior can increase colony fitness, but variation between colonies and the potential consequences of such variation are poorly documented. In this study, we tested natural populations of the red imported fire ant, Solenopsis invicta, for the existence of colony and regional variation in foraging behavior and tested the persistence of this variation over time and across foraging habitats. We also reared single-lineage colonies in standardized environments to explore the contribution of colony lineage. Fire ants from natural populations exhibited significant and persistent colony and regional-level variation in foraging behaviors such as extra-nest activity, exploration, and discovery of and recruitment to resources. Moreover, colony-level variation in extra-nest activity was significantly correlated with colony growth, suggesting that this variation has fitness consequences. Lineage of the colony had a significant effect on extra-nest activity and exploratory activity and explained approximately half of the variation observed in foraging behaviors, suggesting a heritable component to colony-level variation in behavior.

Effect of Carbohydrate Supplementation on Investment into Offspring Number, Size, and Condition in a Social Insect.

Resource availability can determine an organism's investment strategies for growth and reproduction. When nutrients are limited, there are potential tradeoffs between investing into offspring number versus individual offspring size. In social insects, colony investment in offspring size and number may shift in response to colony needs and the availability of food resources. We experimentally manipulated the diet of a polymorphic ant species (Solenopsis invicta) to test how access to the carbohydrate and amino acid components of nectar resources affect colony investment in worker number, body size, size distributions, and individual percent fat mass. We reared field-collected colonies on one of four macronutrient treatment supplements: water, amino acids, carbohydrates, and amino acid and carbohydrates. Having access to carbohydrates nearly doubled colony biomass after 60 days. This increase in biomass resulted from an increase in worker number and mean worker size. Access to carbohydrates also altered worker body size distributions. Finally, we found a negative relationship between worker number and size, suggesting a tradeoff in colony investment strategies. This tradeoff was more pronounced for colonies without access to carbohydrate resources. The monopolization of plant-based resources has been implicated in the ecological success of ants. Our results shed light on a possible mechanism for this success, and also have implications for the success of introduced species. In addition to increases in colony size, our results suggest that having access to plant-based carbohydrates can also result in larger workers that may have better individual fighting ability, and that can withstand greater temperature fluctuations and periods of food deprivation.

Interactions between insect herbivores and plant mating systems.

Self-pollination is common in plants, and limited seed and pollen dispersal can create localized inbreeding even within outcrossing plants. Consequently, insects regularly encounter inbred plants in nature. Because inbreeding results in elevated homozygosity, greater expression of recessive alleles, and subsequent phenotypic changes in inbred plants, inbreeding may alter plant-insect interactions. Recent research has found that plant inbreeding alters resistance and tolerance to herbivores, alters the attraction and susceptibility of plants to insects that vector plant pathogens, and alters visitation rates of insect pollinators. These results suggest that interactions with insects can increase or decrease inbreeding depression (the loss of fitness due to self-fertilization) and subsequently alter the evolution of selfing within plant populations. Future work needs to focus on the mechanisms underlying genetic variation in the effects of inbreeding on plant-insect interactions and the consequences of altered plant-insect interactions on the evolution of plant defense and plant mating systems.

Interaction webs in agroecosystems: beyond who eats whom.

Studies of insect communities in agroecosystems have historically focused on a food web approach: who eats whom. Recent research has highlighted the importance of indirect effects in determining the abundance and distribution of insects and their effects on other insects and plants. These indirect interactions include apparent competition where an herbivore indirectly suppresses another herbivore by attracting shared predators, cases where predators or even other herbivores alter the behavior and/or physiology of herbivores in ways that result in decreased plant consumption, and mutualisms that can generate a network of indirect effects that alter the abundance of many species within a community. The consequences of these indirect interactions have been modeled and proof-of-concept studies have demonstrated their potential importance, but studies of the consequences of these interactions on crop yield are sorely needed. Documenting the prevalence and consequences of these indirect effects in multiple crops will allow researchers to compare and contrast responses across systems and identify key species or characteristics of agroecosystems that dictate when and where these effects are important. This research will ultimately allow growers to manipulate these interactions to increase ecosystem services provided by insects and increase crop yield.

The effect of diet and opponent size on aggressive interactions involving caribbean crazy ants (Nylanderia fulva).

Biotic interactions are often important in the establishment and spread of invasive species. In particular, competition between introduced and native species can strongly influence the distribution and spread of exotic species and in some cases competition among introduced species can be important. The Caribbean crazy ant, Nylanderia fulva, was recently introduced to the Gulf Coast of Texas, and appears to be spreading inland. It has been hypothesized that competition with the red imported fire ant, Solenopsis invicta, may be an important factor in the spread of crazy ants. We investigated the potential of interspecific competition among these two introduced ants by measuring interspecific aggression between Caribbean crazy ant workers and workers of Solenopsis invicta. Specifically, we examined the effect of body size and diet on individual-level aggressive interactions among crazy ant workers and fire ants. We found that differences in diet did not alter interactions between crazy ant workers from different nests, but carbohydrate level did play an important role in antagonistic interactions with fire ants: crazy ants on low sugar diets were more aggressive and less likely to be killed in aggressive encounters with fire ants. We found that large fire ants engaged in fewer fights with crazy ants than small fire ants, but fire ant size affected neither fire ant nor crazy ant mortality. Overall, crazy ants experienced higher mortality than fire ants after aggressive encounters. Our findings suggest that fire ant workers might outcompete crazy ant workers on an individual level, providing some biotic resistance to crazy ant range expansion. However, this resistance may be overcome by crazy ants that have a restricted sugar intake, which may occur when crazy ants are excluded from resources by fire ants.

Neonicotinoid insecticides alter induced defenses and increase susceptibility to spider mites in distantly related crop plants.

BACKGROUND: Chemical suppression of arthropod herbivores is the most common approach to plant protection. Insecticides, however, can cause unintended, adverse consequences for non-target organisms. Previous studies focused on the effects of pesticides on target and non-target pests, predatory arthropods, and concomitant ecological disruptions. Little research, however, has focused on the direct effects of insecticides on plants. Here we demonstrate that applications of neonicotinoid insecticides, one of the most important insecticide classes worldwide, suppress expression of important plant defense genes, alter levels of phytohormones involved in plant defense, and decrease plant resistance to unsusceptible herbivores, spider mites Tetranychus urticae (Acari: Tetranychidae), in multiple, distantly related crop plants. METHODOLOGY/PRINCIPAL FINDINGS: Using cotton (Gossypium hirsutum), corn (Zea mays) and tomato (Solanum lycopersicum) plants, we show that transcription of phenylalanine ammonia lyase, coenzyme A ligase, trypsin protease inhibitor and chitinase are suppressed and concentrations of the phytohormone OPDA and salicylic acid were altered by neonicotinoid insecticides. Consequently, the population growth of spider mites increased from 30% to over 100% on neonicotinoid-treated plants in the greenhouse and by nearly 200% in the field experiment. CONCLUSIONS/SIGNIFICANCE: Our findings are important because applications of neonicotinoid insecticides have been associated with outbreaks of spider mites in several unrelated plant species. More importantly, this is the first study to document insecticide-mediated disruption of plant defenses and link it to increased population growth of a non-target herbivore. This study adds to growing evidence that bioactive agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when the ecological costs of insecticides are evaluated.