Extreme acidity in a cynipid gall: a potential new defensive strategy against natural enemies.

The morphology of insect-induced galls contributes to defences of the gall-inducing insect species against its natural enemies. In terms of gall chemistry, the only defensive compounds thus far identified in galls are tannins that accumulate in many galls, preventing damage by herbivores. Intrigued by the fruit-like appearance of the translucent oak gall (TOG; Amphibolips nubilipennis, Cynipidae, Hymenoptera) induced on red oak (Quercus rubra), we hypothesized that its chemical composition may deviate from other galls. We found that the pH of the gall is between 2 and 3, making it among the lowest pH levels found in plant tissues. We examined the organic acid content of TOG and compared it to fruits and other galls using high-performance liquid chromatography and gas chromatography-mass spectrometry. Malic acid, an acid with particularly high abundance in apples, represents 66% of the organic acid detected in TOGs. The concentration of malic acid was two times higher than in other galls and in apples. Gall histology showed that the acid-containing cells were enlarged and vacuolized just like fruits mesocarp cells. Accumulation of organic acid in gall tissues is convergent with fruit morphology and may constitute a new defensive strategy against predators and parasitoids.

Oak Galls Exhibit Ant Dispersal Convergent with Myrmecochorous Seeds.

AbstractAnts disperse oak galls of some cynipid wasp species similarly to how they disperse seeds with elaiosomes. We conducted choice assays in field and laboratory settings with ant-dispersed seeds and wasp-induced galls found in ant nests and found that seed-dispersing ants retrieve these galls as they do myrmecochorous seeds. We also conducted manipulative experiments in which we removed the putative ant-attracting appendages ("kapéllos") from galls and found that ants are specifically attracted to kapéllos. Finally, we compared the chemical composition and histology of ant-attracting appendages on seeds and galls and found that they both have similar fatty acid compositions as well as morphology. We also observed seed-dispersing ants retrieving oak galls to their nests and rodents and birds consuming oak galls that were not retrieved by ants. These results suggest convergence in ant-mediated dispersal between myrmecochorous seeds and oak galls. Based on our observations, a protective advantage for galls retrieved to ant nests seems a more likely benefit than dispersal distance, as has also been suggested for myrmecochorous seeds. These results require reconsideration of established ant-plant research assumptions, as ant-mediated seed and gall dispersal appear strongly convergent and galls may be far more abundant in eastern North American deciduous forests than myrmecochorous seeds.

Early-season plant cover supports more effective pest control than insecticide applications.

Growing evidence suggests that conservation agricultural practices, like no-till and cover crops, help protect annual crops from insect pests by supporting populations of resident arthropod predators. While adoption of conservation practices is growing, most field crop producers are also using more insecticides, including neonicotinoid seed coatings, as insurance against early-season insect pests. This tactic may disrupt benefits associated with conservation practices by reducing arthropods that contribute to biological control. We investigated the interaction between preventive pest management (PPM) and the conservation practice of cover cropping. We also investigated an alternative pest management approach, integrated pest management (IPM), which responds to insect pest risk, rather than using insecticides prophylactically. In a 3-year corn (Zea mays mays L.)-soy (Glycine max L.) rotation, we measured the response of invertebrate pests and predators to PPM and IPM with and without a cover crop. Using any insecticide provided some small reduction to plant damage in soy, but no yield benefit. In corn, vegetative cover early in the season was key to reducing pest density and damage, likely by increasing the abundance of arthropod predators. Further, PPM in year 1 decreased predation compared to a no-pest-management control. Contrary to our expectation, the IPM strategy, which required just one insecticide application, was more disruptive to the predator community than PPM, likely because the applied pyrethroid was more acutely toxic to a wider range of arthropods than neonicotinoids. Promoting early-season cover was more effective at reducing pest density and damage than either intervention-based strategy. Our results suggest that the best pest management outcomes may occur when biological control is encouraged by planting cover crops and avoiding broad-spectrum insecticides as much as possible. As part of a conservation-based approach to farming, cover crops can promote natural-enemy populations that can help provide biological effective control of insect pest populations.

More phylogenetically diverse polycultures inconsistently suppress insect herbivore populations.

Because the diet of many herbivorous insects is restricted to closely related taxa with similar chemistry, intercropping with diverse plant communities may reduce both pest populations and reliance on chemical pesticides in agroecosystems. We tested whether the effectiveness of intercropping against herbivorous insects depends on the phylogenetic relatedness of neighboring crops, using butternut squash (Cucurbita moschata) as a focal crop species in a series of different intercropping combinations. We found that increased phylogenetic divergence of neighboring plants could reduce abundance of herbivorous insects, but the effect was only detectable mid-season. In addition, we tested two hypothesized mechanisms for a negative association between phylogenetic distance of neighboring plants and reduced herbivore populations: one, we tested using Y-tube olfactometer and choice cage trials whether diverse volatile cues impede host-plant location by the dominant pest of butternut squash in our experiment, striped cucumber beetle Acalymma vittatum. Two, we recorded predator and parasitoid abundance relative to crop phylodiversity to test whether diverse crops support larger natural-enemy populations that can better control pest species. Our results, however, did not support either hypothesis. Striped cucumber beetles preferentially oriented toward non-host-plant volatiles, and predator populations more often decreased with phylodiversity than increased. Thus, the mechanisms driving associations in the field between phylogenetic divergence and herbivore populations remain unclear.

Wild bees as winners and losers: Relative impacts of landscape composition, quality, and climate.

Wild bees, like many other taxa, are threatened by land-use and climate change, which, in turn, jeopardizes pollination of crops and wild plants. Understanding how land-use and climate factors interact is critical to predicting and managing pollinator populations and ensuring adequate pollination services, but most studies have evaluated either land-use or climate effects, not both. Furthermore, bee species are incredibly variable, spanning an array of behavioral, physiological, and life-history traits that can increase or decrease resilience to land-use or climate change. Thus, there are likely bee species that benefit, while others suffer, from changing climate and land use, but few studies have documented taxon-specific trends. To address these critical knowledge gaps, we analyzed a long-term dataset of wild bee occurrences from Maryland, Delaware, and Washington DC, USA, examining how different bee genera and functional groups respond to landscape composition, quality, and climate factors. Despite a large body of literature documenting land-use effects on wild bees, in this study, climate factors emerged as the main drivers of wild-bee abundance and richness. For wild-bee communities in spring and summer/fall, temperature and precipitation were more important predictors than landscape composition, landscape quality, or topography. However, relationships varied substantially between wild-bee genera and functional groups. In the Northeast USA, past trends and future predictions show a changing climate with warmer winters, more intense precipitation in winter and spring, and longer growing seasons with higher maximum temperatures. In almost all of our analyses, these conditions were associated with lower abundance of wild bees. Wild-bee richness results were more mixed, including neutral and positive relationships with predicted temperature and precipitation patterns. Thus, in this region and undoubtedly more broadly, changing climate poses a significant threat to wild-bee communities.

Small-Grain Cover Crops Have Limited Effect on Neonicotinoid Contamination from Seed Coatings.

Neonicotinoids from insecticidal seed coatings can contaminate soil in treated fields and adjacent areas, posing a potential risk to nontarget organisms and ecological function. To determine if cover crops can mitigate neonicotinoid contamination in treated and adjacent areas, we measured neonicotinoid concentrations for three years in no-till corn-soybean rotations, planted with or without neonicotinoid seed coatings, and with or without small grain cover crops. Although neonicotinoids were detected in cover crops, high early season dissipation provided little opportunity for winter-planted cover crops to absorb significant neonicotinoid residues; small grain cover crops failed to mitigated neonicotinoid contamination in either treated or untreated plots. As the majority of neonicotinoids from seed coatings dissipated shortly after planting, residues did not accumulate in soil, but persisted at concentrations below 5 ppb. Persistent residues could be attributed to historic neonicotinoid use and recent, nearby neonicotinoid use. Tracking neonicotinoid concentrations over time revealed a large amount of local interplot movement of neonicotinoids; in untreated plots, contamination was higher when plots were less isolated from treated plots.

Balancing Disturbance and Conservation in Agroecosystems to Improve Biological Control.

Disturbances associated with agricultural intensification reduce our ability to achieve sustainable crop production. These disturbances stem from crop-management tactics and can leave crop fields more vulnerable to insect outbreaks, in part because natural-enemy communities often tend to be more susceptible to disturbance than herbivorous pests. Recent research has explored practices that conserve natural-enemy communities and reduce pest outbreaks, revealing that different components of agroecosystems can influence natural-enemy populations. In this review, we consider a range of disturbances that influence pest control provided by natural enemies and how conservation practices can mitigate or counteract disturbance. We use four case studies to illustrate how conservation and disturbance mitigation increase the potential for biological control and provide co-benefits for the broader agroecosystem. To facilitate the adoption of conservation practices that improve top-down control across significant areas of the landscape, these practices will need to provide multifunctional benefits, but should be implemented with natural enemies explicitly in mind.

Costs of plant defense priming: exposure to volatile cues from a specialist herbivore increases short-term growth but reduces rhizome production in tall goldenrod (Solidago altissima).

BACKGROUND: By sensing environmental cues indicative of pathogens or herbivores, plants can "prime" appropriate defenses and deploy faster, stronger responses to subsequent attack. Such priming presumably entails costs-else the primed state should be constitutively expressed-yet those costs remain poorly documented, in part due to a lack of studies conducted under realistic ecological conditions. We explored how defence priming in goldenrod (Solidago altissima) influenced growth and reproduction under semi-natural field conditions by manipulating exposure to priming cues (volatile emissions of a specialist herbivore, Eurosta solidaginis), competition between neighbouring plants, and herbivory (via insecticide application). RESULTS: We found that primed plants grew faster than unprimed plants, but produced fewer rhizomes, suggesting reduced capacity for clonal reproduction. Unexpectedly, this effect was apparent only in the absence of insecticide, prompting a follow-up experiment that revealed direct effects of the pesticide esfenvalerate on plant growth (contrary to previous reports from goldenrod). Meanwhile, even in the absence of pesticide, priming had little effect on herbivore damage levels, likely because herbivores susceptible to the primed defences were rare or absent due to seasonality. CONCLUSIONS: Reduced clonal reproduction in primed plants suggest that priming can entail significant costs for plants. These costs, however, may only become apparent when priming cues fail to provide accurate information about prevailing threats, as was the case in this study. Additionally, our insecticide data indicate that pesticides or their carrier compounds can subtly, but significantly, affect plant physiology and may interact with plant defences.

Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences.

To fuel their activities and rear their offspring, foraging bees must obtain a sufficient quality and quantity of nutritional resources from a diverse plant community. Pollen is the primary source of proteins and lipids for bees, and the concentrations of these nutrients in pollen can vary widely among host-plant species. Therefore we hypothesized that foraging decisions of bumble bees are driven by both the protein and lipid content of pollen. By successively reducing environmental and floral cues, we analyzed pollen-foraging preferences of Bombus impatiens in (i) host-plant species, (ii) pollen isolated from these host-plant species, and (iii) nutritionally modified single-source pollen diets encompassing a range of protein and lipid concentrations. In our semifield experiments, B impatiens foragers exponentially increased their foraging rates of pollen from plant species with high protein:lipid (P:L) ratios; the most preferred plant species had the highest ratio (∼4.6:1). These preferences were confirmed in cage studies where, in pairwise comparisons in the absence of other floral cues, B impatiens workers still preferred pollen with higher P:L ratios. Finally, when presented with nutritionally modified pollen, workers were most attracted to pollen with P:L ratios of 5:1 and 10:1, but increasing the protein or lipid concentration (while leaving ratios intact) reduced attraction. Thus, macronutritional ratios appear to be a primary factor driving bee pollen-foraging behavior and may explain observed patterns of host-plant visitation across the landscape. The nutritional quality of pollen resources should be taken into consideration when designing conservation habitats supporting bee populations.

A Maize Inbred Exhibits Resistance Against Western Corn Rootwoorm, Diabrotica virgifera virgifera.

Insect resistance against root herbivores like the western corn rootworm (WCR, Diabrotica virgifera virgifera) is not well understood in non-transgenic maize. We studied the responses of two American maize inbreds, Mp708 and Tx601, to WCR infestation using biomechanical, molecular, biochemical analyses, and laser ablation tomography. Previous studies performed on several inbreds indicated that these two maize genotypes differed in resistance to pests including fall armyworm (Spodoptera frugiperda) and WCR. Our data confirmed that Mp708 shows resistance against WCR, and demonstrates that the resistance mechanism is based in a multi-trait phenotype that includes increased resistance to cutting in nodal roots, stable root growth during insect infestation, constitutive and induced expression of known herbivore-defense genes, including ribosomal inhibitor protein 2 (rip2), terpene synthase 23 (tps23) and maize insect resistance cysteine protease-1 (mir1), as well high constitutive levels of jasmonic acid and production of (E)-ß-caryophyllene. In contrast, Tx601 is susceptible to WCR. These findings will facilitate the use of Mp708 as a model to explore the wide variety of mechanisms and traits involved in plant defense responses and resistance to herbivory by insects with several different feeding habits.

Inter-varietal interactions among plants in genotypically diverse mixtures tend to decrease herbivore performance.

Much research has explored the effects of plant species diversity on herbivore populations, but far less has considered effects of plant genotypic diversity, or how abiotic stressors, like drought, can modify effects. Mechanisms by which plant genotypic diversity affects herbivore populations remain largely unresolved. We used greenhouse studies with a model system of wheat (Triticum aestivum L.) and bird cherry-oat aphid (Rhopalosiphum padi L.) to determine whether the genotypic diversity of a plant's neighborhood influences performance and fitness of herbivores on a focal plant and if drought changes the influence of neighborhood diversity. Taken across all varieties we tested, plant-plant interactions in diverse neighborhoods reduced aphid performance and generated associational resistance, although effects on aphids depended on variety identity. In diverse mixtures, drought stress greatly diminished the genotypic diversity-driven reduction in aphid performance. Neighborhood diversity influenced mother aphid size, and appeared to partially explain how plant-plant interactions reduced the number of offspring produced in mixtures. Plant size did not mediate effects on aphid performance, although neighborhood diversity reduced plant mass across varieties and watering treatments. Our results suggest inter-varietal interactions in genotypic mixtures can affect herbivore performance in the absence of herbivore movement and that abiotic stress may diminish any effects. Accounting for how neighborhood diversity influences resistance of an individual plant to herbivores will help aid development of mixtures of varieties for managing insect pests and clarify the role of plant genotypic diversity in ecosystems.

Exposure of Solidago altissima plants to volatile emissions of an insect antagonist (Eurosta solidaginis) deters subsequent herbivory.

Recent work indicates that plants respond to environmental odors. For example, some parasitic plants grow toward volatile cues from their host plants, and other plants have been shown to exhibit enhanced defense capability after exposure to volatile emissions from herbivore-damaged neighbors. Despite such intriguing discoveries, we currently know relatively little about the occurrence and significance of plant responses to olfactory cues in natural systems. Here we explore the possibility that some plants may respond to the odors of insect antagonists. We report that tall goldenrod (Solidago altissima) plants exposed to the putative sex attractant of a closely associated herbivore, the gall-inducing fly Eurosta solidaginis, exhibit enhanced defense responses and reduced susceptibility to insect feeding damage. In a field study, egg-laying E. solidaginis females discriminated against plants previously exposed to the sex-specific volatile emissions of males; furthermore, overall rates of herbivory were reduced on exposed plants. Consistent with these findings, laboratory assays documented reduced performance of the specialist herbivore Trirhabda virgata on plants exposed to male fly emissions (or crude extracts), as well as enhanced induction of the key defense hormone jasmonic acid in exposed plants after herbivory. These unexpected findings from a classic ecological study system provide evidence for a previously unexplored class of plant-insect interactions involving plant responses to insect-derived olfactory cues.

Herbivore exploits orally secreted bacteria to suppress plant defenses.

Induced plant defenses in response to herbivore attack are modulated by cross-talk between jasmonic acid (JA)- and salicylic acid (SA)-signaling pathways. Oral secretions from some insect herbivores contain effectors that overcome these antiherbivore defenses. Herbivores possess diverse microbes in their digestive systems and these microbial symbionts can modify plant-insect interactions; however, the specific role of herbivore-associated microbes in manipulating plant defenses remains unclear. Here, we demonstrate that Colorado potato beetle (Leptinotarsa decemlineata) larvae exploit bacteria in their oral secretions to suppress antiherbivore defenses in tomato (Solanum lycopersicum). We found that antibiotic-untreated larvae decreased production of JA and JA-responsive antiherbivore defenses, but increased SA accumulation and SA-responsive gene expression. Beetles benefit from down-regulating plant defenses by exhibiting enhanced larval growth. In SA-deficient plants, suppression was not observed, indicating that suppression of JA-regulated defenses depends on the SA-signaling pathway. Applying bacteria isolated from larval oral secretions to wounded plants confirmed that three microbial symbionts belonging to the genera Stenotrophomonas, Pseudomonas, and Enterobacter are responsible for defense suppression. Additionally, reinoculation of these bacteria to antibiotic-treated larvae restored their ability to suppress defenses. Flagellin isolated from Pseudomonas sp. was associated with defense suppression. Our findings show that the herbivore exploits symbiotic bacteria as a decoy to deceive plants into incorrectly perceiving the threat as microbial. By interfering with the normal perception of herbivory, beetles can evade antiherbivore defenses of its host.

Large-scale deployment of seed treatments has driven rapid increase in use of neonicotinoid insecticides and preemptive pest management in US field crops.

Neonicotinoids are the most widely used class of insecticides worldwide, but patterns of their use in the U.S. are poorly documented, constraining attempts to understand their role in pest management and potential nontarget effects. We synthesized publicly available data to estimate and interpret trends in neonicotinoid use since their introduction in 1994, with a special focus on seed treatments, a major use not captured by the national pesticide-use survey. Neonicotinoid use increased rapidly between 2003 and 2011, as seed-applied products were introduced in field crops, marking an unprecedented shift toward large-scale, preemptive insecticide use: 34-44% of soybeans and 79-100% of maize hectares were treated in 2011. This finding contradicts recent analyses, which concluded that insecticides are used today on fewer maize hectares than a decade or two ago. If current trends continue, neonicotinoid use will increase further through application to more hectares of soybean and other crop species and escalation of per-seed rates. Alternatively, our results, and other recent analyses, suggest that carefully targeted efforts could considerably reduce neonicotinoid use in field crops without yield declines or economic harm to farmers, reducing the potential for pest resistance, nontarget pest outbreaks, environmental contamination, and harm to wildlife, including pollinator species.

Shared genes related to aggression, rather than chemical communication, are associated with reproductive dominance in paper wasps (Polistes metricus).

BACKGROUND: In social groups, dominant individuals may socially inhibit reproduction of subordinates using aggressive interactions or, in the case of highly eusocial insects, pheromonal communication. It has been hypothesized these two modes of reproductive inhibition utilize conserved pathways. Here, we use a comparative framework to investigate the chemical and genomic underpinnings of reproductive dominance in the primitively eusocial wasp Polistes metricus. Our goals were to first characterize transcriptomic and chemical correlates of reproductive dominance and second, to test whether dominance-associated mechanisms in paper wasps overlapped with aggression or pheromone-related gene expression patterns in other species. To explore whether conserved molecular pathways relate to dominance, we compared wasp transcriptomic data to previous studies of gene expression associated with pheromonal communication and queen-worker differences in honey bees, and aggressive behavior in bees, Drosophila, and mice. RESULTS: By examining dominant and subordinate females from queen and worker castes in early and late season colonies, we found that cuticular hydrocarbon profiles and genome-wide patterns of brain gene expression were primarily associated with season/social environment rather than dominance status. In contrast, gene expression patterns in the ovaries were associated primarily with caste and ovary activation. Comparative analyses suggest genes identified as differentially expressed in wasp brains are not related to queen pheromonal communication or caste in bees, but were significantly more likely to be associated with aggression in other insects (bees, flies), and even a mammal (mice). CONCLUSIONS: This study provides the first comprehensive chemical and molecular analysis of reproductive dominance in paper wasps. We found little evidence for a chemical basis for reproductive dominance in P. metricus, and our transcriptomic analyses suggest that different pathways regulate dominance in paper wasps and pheromone response in bees. Furthermore, there was a substantial impact of season/social environment on gene expression patterns, indicating the important role of external cues in shaping the molecular processes regulating behavior. Interestingly, genes associated with dominance in wasps were also associated with aggressive behavior in bees, solitary insects and mammals. Thus, genes involved in social regulation of reproduction in Polistes may have conserved functions associated with aggression in insects and other taxa.

The volatile emission of Eurosta solidaginis primes herbivore-induced volatile production in Solidago altissima and does not directly deter insect feeding.

BACKGROUND: The induction of plant defenses in response to herbivory is well documented. In addition, many plants prime their anti-herbivore defenses following exposure to environmental cues associated with increased risk of subsequent attack, including induced volatile emissions from herbivore-damaged plant tissues. Recently, we showed in both field and laboratory settings that tall goldenrod plants (Solidago altissima) exposed to the putative sex attractant of a specialist gall-inducing fly (Eurosta solidaginis) experienced less herbivory than unexposed plants. Furthermore, we observed stronger induction of the defense phytohormone jasmonic acid in exposed plants compared to controls. These findings document a novel class of plant-insect interactions mediated by the direct perception, by plants, of insect-derived olfactory cues. However, our previous study did not exclude the possibility that the fly emission (or its residue) might also deter insect feeding via direct effects on the herbivores. RESULTS: Here we show that the E. solidaginis emission does not (directly) deter herbivore feeding on Cucurbita pepo or Symphyotrichum lateriflorum plants--which have no co-evolutionary relationship with E. solidaginis and thus are not expected to exhibit priming responses to the fly emission. We also document stronger induction of herbivore-induced plant volatiles (HIPV) in S. altissima plants given previous exposure to the fly emission relative to unexposed controls. No similar effect was observed in maize plants (Zea mays), which have no co-evolutionary relationship with E. solidaginis. CONCLUSIONS: Together with our previous findings, these results provide compelling evidence that reduced herbivory on S. altissima plants exposed to the emission of male E. solidaginis reflects an evolved plant response to olfactory cues associated with its specialist herbivore and does not involve direct effects of the fly emission on herbivore feeding behavior. We further discuss mechanisms by which the priming of HIPV responses documented here might contribute to enhanced S. altissima defense against galling.

Phytohormone dynamics associated with gall insects, and their potential role in the evolution of the gall-inducing habit.

While plant galls can be induced by a variety of organisms, insects produce the most diverse and complex galls found in nature; yet, how these galls are formed is unknown. Phytohormones have long been hypothesized to play a key role in gall production, but their exact role, and how they influence galls, has been unclear. Research in the past decade has provided better insight into the role of plant hormones in gall growth and plant defenses. We review and synthesize recent literature on auxin, cytokinins, and abscisic, jasmonic, and salicylic acids to provide a broader understanding of how these phytohormones might effect gall production, help plants defend against galls, and/or allow insects to overcome host-plant defenses. After reviewing these topics, we consider the potential for phytohormones to have facilitated the evolution of insect galls. More specialized research is needed to provide a mechanistic understanding of how phytohormones operate in gall-insect-plant interactions, but current evidence strongly supports phytohormones as key factors determining the success and failure of insect galls.

Illuminating patterns of firefly abundance using citizen science data and machine learning models.

As insect populations decline in many regions, conservation biologists are increasingly tasked with identifying factors that threaten insect species and developing effective strategies for their conservation. One insect group of global conservation concern are fireflies (Coleoptera: Lampyridae). Although quantitative data on firefly populations are lacking for most species, anecdotal reports suggest that some firefly populations have declined in recent decades. Researchers have hypothesized that North American firefly populations are most threatened by habitat loss, pesticide use, and light pollution, but the importance of these factors in shaping firefly populations has not been rigorously examined at broad spatial scales. Using data from >24,000 surveys (spanning 2008-16) from the citizen science program Firefly Watch, we trained machine learning models to evaluate the relative importance of a variety of factors on bioluminescent firefly populations: pesticides, artificial lights at night, land cover, soil/topography, short-term weather, and long-term climate. Our analyses revealed that firefly abundance was driven by complex interactions among soil conditions (e.g., percent sand composition), climate/weather (e.g., growing degree days), and land cover characteristics (e.g., percent agriculture and impervious cover). Given the significant impact that climactic and weather conditions have on firefly abundance, there is a strong likelihood that firefly populations will be influenced by climate change, with some regions becoming higher quality and supporting larger firefly populations, and others potentially losing populations altogether. Collectively, our results support hypotheses related to factors threatening firefly populations, especially habitat loss, and suggest that climate change may pose a greater threat than appreciated in previous assessments. Thus, future conservation of North American firefly populations will depend upon 1) consistent and continued monitoring of populations via programs like Firefly Watch, 2) efforts to mitigate the impacts of climate change, and 3) insect-friendly conservation practices.

Abscisic Acid: A Potential Secreted Effector Synthesized by Phytophagous Insects for Host-Plant Manipulation.

Abscisic acid (ABA) is an isoprenoid-derived plant signaling molecule involved in a wide variety of plant processes, including facets of growth and development as well as responses to abiotic and biotic stress. ABA had previously been reported in a wide variety of animals, including insects and humans. We used high-performance liquid chromatography-electrospray ionization tandem mass spectrometry (HPLC-(ESI)-MS/MS) to examine concentrations of ABA in 17 species of phytophagous insects, including gall- and non-gall-inducing species from all insect orders with species known to induce plant galls: Thysanoptera, Hemiptera, Lepidoptera, Coleoptera, Diptera, and Hymenoptera. We found ABA in insect species in all six orders, in both gall-inducing and non-gall-inducing species, with no tendency for gall-inducing insects to have higher concentrations. The concentrations of ABA in insects often markedly exceeded those typically found in plants, suggesting it is highly improbable that insects obtain all their ABA from their host plant via consumption and sequestration. As a follow-up, we used immunohistochemistry to determine that ABA localizes to the salivary glands in the larvae of the gall-inducing Eurosta solidaginis (Diptera: Tephritidae). The high concentrations of ABA, combined with its localization to salivary glands, suggest that insects are synthesizing and secreting ABA to manipulate their host plants. The pervasiveness of ABA among both gall- and non-gall-inducing insects and our current knowledge of the role of ABA in plant processes suggest that insects are using ABA to manipulate source-sink mechanisms of nutrient allocation or to suppress host-plant defenses. ABA joins the triumvirate of phytohormones, along with cytokinins (CKs) and indole-3-acetic acid (IAA), that are abundant, widespread, and localized to glandular organs in insects and used to manipulate host plants.

Insecticide-contaminated honeydew: risks for beneficial insects.

Honeydew is the sugar-rich excretion of phloem-feeding hemipteran insects such as aphids, mealybugs, whiteflies, and psyllids, and can be a main carbohydrate source for beneficial insects in some ecosystems. Recent research has revealed that water-soluble, systemic insecticides contaminate honeydew excreted by hemipterans that feed on plants treated with these insecticides. This contaminated honeydew can be toxic to beneficial insects, such as pollinators, parasitic wasps and generalist predators that feed on it. This route of exposure has now been demonstrated in three plant species, for five systemic insecticides and four hemipteran species; therefore, we expect this route to be widely available in some ecosystems. In this perspective paper, we highlight the importance of this route of exposure by exploring: (i) potential pathways through which honeydew might be contaminated with insecticides; (ii) hemipteran families that are more likely to excrete contaminated honeydew; and (iii) systemic insecticides with different modes of action that might contaminate honeydew through the plant. Furthermore, we analyse several model scenarios in Europe and/or the USA where contaminated honeydew could be problematic for beneficial organisms that feed on this ubiquitous carbohydrate source. Finally, we explain why this route of exposure might be important when exotic, invasive, honeydew-producing species are treated with systemic insecticides. Overall, this review opens a new area of research in the field of ecotoxicology to understand how insecticides can reach non-target beneficial insects. In addition, we aim to shed light on potential undescribed causes of insect declines in ecosystems where honeydew is an important carbohydrate source for insects, and advocate for this route of exposure to be included in future environmental risk assessments.