A molecular approach to unravel trophic interactions between parasitoids and hyperparasitoids associated with pecan aphids.

Advances in molecular ecology can overcome many challenges in understanding host-parasitoid interactions. Genetic characterization of the key-players in systems helps to confirm species and identify trophic linkages essential for ecological service delivery by biological control agents; however, relatively few agroecosystems have been explored using this approach. Pecan production consists of a large tree perennial system containing an assortment of seasonal pests and natural enemies. As a first step to characterizing host-parasitoid associations in pecan food webs, we focus on aphid species and their parasitoids. Based on DNA barcoding of field-collected and reared specimens, we confirmed the presence of 3 species of aphid, one family of primary parasitoids, and 5 species of hyperparasitoids. By applying metabarcoding to field-collected aphid mummies, we were able to identify multiple species within each aphid mummy to unravel a complex food web of 3 aphids, 2 primary parasitoids, and upward of 8 hyperparasitoid species. The results of this study demonstrate that multiple hyperparasitoid species attack a single primary parasitoid of pecan aphids, which may have negative consequences for successful aphid biological control. Although further research is needed on a broader spatial scale, our results suggest multiple species exist in this system and may suggest a complex set of interactions between parasitoids, hyperparasitoids, and the 3 aphid species. This was the first time that many of these species have been characterized and demonstrates the application of novel approaches to analyze the aphid-parasitoid food webs in pecans and other tree crop systems.

Potential of Ocotea indecora Essential Oil for Controlling Drosophila suzukii: Molecular Predictions for Toxicity and Selectivity to Beneficial Arthropods.

The protection of soft-skinned fruits against Drosophila suzukii has relied primarily on the efficacy of a few synthetic molecules. Despite their short-term efficacy, these molecules can cause environmental pollution, unintendedly affect non-target organisms, and fail to provide sustainable control. The shortfalls of using synthetic pesticides warrant the search for alternatives, such as essential oils extracted from plants, with greater eco-friendlier properties. Here, we chemically characterized and evaluated the toxicity of the essential oil extracted from leaves of Ocotea indecora (Schott) Mez (Lauraceae) against D. suzukii via two exposure pathways (ingestion and contact). We also assessed the selectivity of the essential oil to two predatory natural enemies, Eriopis connexa and Chrysoperla externa and two pollinator bees, Apis mellifera and Partamona helleri. In addition, we conducted in silico predictions to investigate potential interactions between the major compound of the essential oil and the insects' transient receptor potential (TRP) channels. Our chromatographic analysis revealed sesquirosefuran (87%) as the major compound. Higher toxicity to adults of D. suzukii was observed in contact exposure (LC50 = 0.43 µL mL-1) compared to ingestion (LC50 = 0.72 µL mL-1). However, the essential oil did not cause mortality to the non-target organisms tested here, even when applied at 2.20 µL mL-1. Molecular predictions demonstrated that sesquirosefuran binds more stably to the TRP channels of D. suzukii than to those expressed in beneficial arthropods. Collectively, our findings provide the initial framework for the potential use of O. indecora essential oil as a sustainable alternative for managing D. suzukii infestations.

Bayesian Multi-Targets Strategy to Track Apis mellifera Movements at Colony Level.

Interactive movements of bees facilitate the division and organization of collective tasks, notably when they need to face internal or external environmental challenges. Here, we present a Bayesian and computational approach to track the movement of several honey bee, Apis mellifera, workers at colony level. We applied algorithms that combined tracking and Kernel Density Estimation (KDE), allowing measurements of entropy and Probability Distribution Function (PDF) of the motion of tracked organisms. We placed approximately 200 recently emerged and labeled bees inside an experimental colony, which consists of a mated queen, approximately 1000 bees, and a naturally occurring beehive background. Before release, labeled bees were fed for one hour with uncontaminated diets or diets containing a commercial mixture of synthetic fungicides (thiophanate-methyl and chlorothalonil). The colonies were filmed (12 min) at the 1st hour, 5th and 10th days after the bees' release. Our results revealed that the algorithm tracked the labeled bees with great accuracy. Pesticide-contaminated colonies showed anticipated collective activities in peripheral hive areas, far from the brood area, and exhibited reduced swarm entropy and energy values when compared to uncontaminated colonies. Collectively, our approach opens novel possibilities to quantify and predict potential alterations mediated by pollutants (e.g., pesticides) at the bee colony-level.

Potential of Ficus carica extracts against Euschistus heros: Toxicity of major active compounds and selectivity against beneficial insects.

BACKGROUND: Using plant-based extracts and their constituents has been suggested as an alternative tool to replace or integrate with the synthetic compounds used to manage insect pests. Here, we evaluated the potential of extracts obtained from Ficus carica Linn (Moraceae) branches and leaves against the Neotropical brown stink bug, Euschistus heros, one of the most prevalent insect pests in soybean fields. We further isolated and evaluated the toxicity of the extracts' major components against E. heros. Additionally, by using computational docking analysis and toxicological approaches, we assessed the physiological basis for the selectivity of these extracts against beneficial insects such as pollinator bees (i.e. Apis mellifera and the Neotropical stingless bee Partamona helleri), ladybeetles (Eriopis connexa and Coleomegilla maculata), and lacewings (Chrysoperla externa). RESULTS: Our results demonstrate that branch (LC50  = 5.9 [4.7-7.1] mg mL-1 ) and leaf (LC50  = 14.1 [12.5-15.4] mg mL-1 ) extracts exhibited similar toxicity against E. heros. Our phytochemical analysis revealed psoralen and bergapten furanocoumarins as the major components of the extract. Based on our computational predictions, these molecules' differential abilities to physically interact with the acetylcholinesterases of E. heros and beneficial insects play relevant roles in their selectivity actions. The estimated LC90 values of branch (30.0 mg mL-1 ) and leaf (30.0 mg mL-1 ) extracts killed less than 12% of the beneficial insects. CONCLUSION: Overall, our findings revealed that furanocoumarin-rich extracts obtained from F. carica extracts have the potential to be used as alternative tools in the integrated management of stink bug pests. © 2021 Society of Chemical Industry.

Identifying Molecular-Based Trophic Interactions as a Resource for Advanced Integrated Pest Management.

Biodiversity is an essential attribute of sustainable agroecosystems. Diverse arthropod communities deliver multiple ecosystem services, such as biological control, which are the core of integrated pest management programs. The molecular analysis of arthropod diets has emerged as a new tool to monitor and help predict the outcomes of management on the functioning of arthropod communities. Here, we briefly review the recent molecular analysis of predators and parasitoids in agricultural environments. We focus on the developments of molecular gut content analysis (MGCA) implemented to unravel the function of community members, and their roles in biological control. We examine the agricultural systems in which this tool has been applied, and at what ecological scales. Additionally, we review the use of MGCA to uncover vertebrate roles in pest management, which commonly receives less attention. Applying MGCA to understand agricultural food webs is likely to provide an indicator of how management strategies either improve food web properties (i.e., enhanced biological control), or adversely impact them.

Sublethal agrochemical exposures can alter honey bees' and Neotropical stingless bees' color preferences, respiration rates, and locomotory responses.

Stingless bees such as Partamona helleri Friese play important roles in pollination of native plants and agricultural crops in the Neotropics. Global concerns about declining bee populations due to agrochemical pollutants have, however, been biased towards the honey bee, Apis mellifera Linnaeus. Here, we analysed the unintended effects of commercial formulations of a neonicotinoid insecticide, imidacloprid, and a fungicide mixture of thiophanate-methyl and chlorothalonil on color preference, respiration rates and group locomotory activities of both P. helleri and A. mellifera. Our results revealed that P. helleri foragers that were not exposed to pesticides changed their color preference during the course of a year. By contrast, we found that pesticide exposure altered the color preference of stingless bees in a concentration-dependent manner. In addition, imidacloprid decreased the overall locomotion of both bee species, whereas the fungicide mixture increased locomotion of only stingless bees. The fungicide mixture also reduced respiration rates of forager bees of both species. Forager bees of both species altered their color preference, but not their locomotory and respiration rates, when exposed to commercial formulations of each fungicidal mixture component (i.e., chlorothalonil and thiophanate-methyl). Our findings emphasize the importance of P. helleri as a model for Neotropical wild pollinator species in pesticide risk assessments, and also the critical importance of including groups of agrochemicals that are often considered to have minimal impact on pollinators, such as fungicides.

Disentangling the ecotoxicological selectivity of clove essential oil against aphids and non-target ladybeetles.

The plant-based biopesticides have been proposed as insect pest control tools that seem to be safer for the environment and human health when compared to synthetic conventional molecules. However, such assumptions are generally made without considering the absence of detrimental effects on sublethally-exposed non-target organisms or showing the physiological basis of the selective action of such botanical products. Thus, by using in silico-based and in vivo toxicological approaches, the present investigation aimed to disentangle the ecotoxicological selectivity of clove, Syzygium aromaticum, essential oil against the aphid Rhopalosiphum maidis and the non-target ladybeetle, Coleomegilla maculata. We also investigated whether the sublethal exposure to clove essential oil would affect the locomotory and predatory abilities of C. maculata. We found that the clove essential oil concentration estimated to kill 95% (LC95: 0.17 µL/cm2) of the aphids was lethal to <18% of C. maculata. Indeed, our in silico results reinforced such differential susceptibility, as it predicted that eugenol and ß-caryophyllene (i.e., the clove essential oil major components) bound to three potential molecular targets (i.e., transient receptor potential (TRP) channels, octopamine, and gamma-aminobutyric acid (GABA) receptors) of the aphids but only to the octopamine receptors of the ladybeetles. Additionally, the ladybeetles that were exposure to the clove essential oil exhibited unaffected abilities to locomote and to prey upon R. maidis aphids when compared to unexposed ladybeetles. Thus, by displaying lower toxicity against the ladybeetles, the clove essential oil represents a safer alternative tool to be integrated into programs aiming to manage aphid infestations.

Essential oil from Negramina (Siparuna guianensis) plants controls aphids without impairing survival and predatory abilities of non-target ladybeetles.

Plant essential oils are regarded as interesting alternative tools to be integrated into the management of pest insects. However, as they generally consist of mixtures of numerous molecules, the physiological basis for their action is unresolved. Here, we evaluated the effects of essential oil of the Neotropical plant Siparuna guianensis Aubl., commonly known as Negramina, against an important pest insect: the green peach aphid Myzus persicae (Sulzer), and also in two non-target natural enemies: the ladybeetle predators Coleomegilla maculata (DeGeer) and Eriopis connexa (Germar). In addition, we conducted a computational docking analysis for predicting the physical interactions between the two Negramina essential oil major constituents: ß-myrcene and 2-undocanone, and the transient receptor potential (TRP) channels as potential binding receptors in the aphid and ladybeetles. As the most important results, Negramina essential oil caused mortality in M. persicae aphids with an LC95 = 1.08 mg/cm2, and also significantly repelled the aphids at concentrations as low as 0.14 mg/cm2. Our computational docking analysis reinforced such selectivity actions as the Negramina essential oil major compounds (i.e., ß-myrcene and 2-undocanone) bound to the TRP channels of M. persicae but not to ladybeetle-related TRP channels. Interestingly, the exposure to the Negramina essential oil did not affect the predatory abilities of C. maculata but increased the abilities of E. connexa to prey upon M. persicae. Collectively, our findings provided a physiological basis for the insecticidal and selectivity potential of Negramina essential oil, reinforcing its potential as a tool to be used in integrated pest control programs.