Harmony under threat: does resource-mediated stress affect the (caste-based) social network of leaf-cutting ant colonies?

BACKGROUND: Managing pest species of eusocial insects, such as leaf-cutting ants, poses significant challenges. Controlling them requires understanding of how toxic plant substrates and ant baits are recognized by foragers, transported to the nest, shared among workers and managed by gardeners cultivating the symbiont fungus garden. Despite this, little is known about how unsuitable resources might impact social interactions within ant colonies. This study aims to investigate whether the provision of a suitable substrate (copperleaf) and a toxic substrate (nasturtium leaves) affects the social network dynamics within colonies of two leaf-cutting ant species: Acromyrmex molestans and Acromyrmex subterraneus. The interactions between castes were recorded and subjected to social network analyses. RESULTS: Initial foraging duration increased for A. subterraneus provided with copperleaf, although no difference was observed for the other species and resource combinations. The social network structure was similar for both species when copperleaf leaves were provided as a substrate. However, notable alterations occurred with nasturtium leaf provision, leading to higher integration of gardeners in interactions and noticeable changes in the generalist worker network centrality, particularly in A. subterraneus. DISCUSSION: The observed changes in social interactions, particularly in A. subterraneus, suggest that increasing gardener interactions with other castes expedites the movement of the substrate within the colony. This maximizes the potential toxic effect on the colony. © 2024 Society of Chemical Industry.

Reimagining agrochemical pollution mitigation: Leveraging hormesis for sustainable environmental solutions.

Emerging evidence reveals that low doses of stress stimulate, and high doses suppress, organism responses - a phenomenon known as hormesis. Here, we propose a framework for harnessing hormesis principles to optimize agrochemical use and mitigate pollution. We discuss how hormesis can be applied in agrochemical context and highlight challenges and needs beyond scientific research, offering a perspective for sustainable environmental solutions.

Nasturtium leaf compounds, diphenyl disulfide and lyral, against Atta sexdens (Hymenoptera: Formicidae) and their symbiotic fungi.

Social insect pests, particularly leaf-cutting ants, present a considerable challenge in terms of control. Leaf-cutting ants are significant agricultural, forestry, and pasture pests, and understanding their behavior and defense mechanisms is essential for managing their colonies effectively. While toxic ant baits are a primary control method, the limited availability of effective insecticides and concerns over their hazardous nature has spurred the search for alternative solutions, particularly natural compounds, which aligns with the goals of forest certification groups. In the light of previous evidence demonstrating the efficacy of nasturtium leaves (Tropaeolum majus L. (Brassicales: Tropaeolaceae)) in suppressing leaf-cutting ant colonies, this study investigates 2 active components of nasturtium leaf extracts: diphenyl disulfide and lyral. We tested their impact on Atta sexdens (L.) (Hymenoptera: Formicidae), the most prevalent leaf-cutter ant species in Brazil, and their symbiotic fungus, Leucoagaricus gongylophorus (Möller) Singer (Agaricales: Agaricaceae). We conducted experiments with increasing concentrations of diphenyl disulfide and lyral, assessing their effects on the symbiotic fungus and on forager workers and gardeners of A. sexdens colonies. Our findings revealed no fungicidal activity, and ant mortality was minimal in both topical and ingestion bioassays with the exception of gardeners topically exposed to diphenyl sulfide. Furthermore, the compounds did not affect leaf ingestion, but diphenyl disulfide did increase interactions among foragers. These results suggest that neither diphenyl disulfide nor lyral are the primary contributors to the suppression of leaf-cutting ant colonies by nasturtium leaves. However, they may enhance the formicidal activity of other compounds present in nasturtium leaves.

Tetraniliprole risk assessment: Unveiling a hidden threat for managing a generalist herbivore.

Insecticide resistance poses a significant challenge in managing generalist herbivores such as the tobacco cutworm (TCW), Spodoptera litura. This study investigates the potential risks associated with using the novel diamide insecticide tetraniliprole to control TCW. A tetraniliprole-resistant strain was developed through twelve generations of laboratory selection, indicating an intermediate risk of resistance development. Field monitoring in China revealed a significant incidence of resistance, particularly in the Nanchang (NC) population (>100-fold). Tetraniliprole showed moderate to high cross-resistance to multiple insecticides and was autosomally inherited with incomplete dominance, controlled by multiple genes, some of which belong to the cytochrome P450 family associated with enhanced detoxification. Life table studies indicated transgenerational hormesis, stimulating TCW female fecundity and increasing population net reproduction rates (R0). These findings suggest a potential for pest resurgence under tetraniliprole use. The integrated risk assessment provides a basis for the sustainable management of TCW using tetraniliprole.

Stimulation of insect vectors of pathogens by sublethal environmental contaminants: A hidden threat to human and environmental health?

Sublethal stimulation and hormetic responses are increasingly identified and acknowledged in scientific research. However, the occurrence and characteristics of such responses in insect vectors of pathogens are little explored and poorly understood. Here, we collate significant evidence from the scientific literature showing that sublethal doses of environmental contaminants, such as pesticides, microplastics, and plasticizers, induce stimulation and hormetic responses in insect vectors of pathogens of agricultural and public health importance, including mosquitoes, other dipterans, psyllids, aphids, and planthoppers. Physiological, behavioral, and demographic traits can be enhanced by exposure to lower subtoxic contaminant doses while being inhibited by higher toxic doses. Energetic trade-offs can also occur, especially at sublethal doses higher than the no-observed-adverse-effect level (NOAEL). The relevant literature is limited and so are the number of doses commonly included in the studies, precluding firm conclusions and enhanced understanding. Nevertheless, these effects are significant and could undermine human and environmental health, and thus sustainability agendas, if ultimately the transmission of pathogens and disease spread and severity are increased. Further research is urgently needed to tackle these phenomena, especially under field conditions. The findings discussed here are relevant to chemical risk assessment and chemical safety evaluations, in which all possible effects from the lowest to higher doses should be considered.

Sublethal chemical stimulation of arthropod parasitoids and parasites of agricultural and environmental importance.

An increasing number of studies have reported stimulation of various organisms in the presence of environmental contaminants. This has created a need to critically evaluate sublethal stimulation and hormetic responses of arthropod parasitoids and parasites following exposure to pesticides and other contaminants. Examining this phenomenon with a focus on arthropods of agricultural and environmental importance serves as the framework for this literature review. This review shows that several pesticides, with diverse chemical structures and different modes of action, applied individually or in combination at sublethal doses, commonly stimulate an array of arthropod parasitoids and parasites. Exposure at sublethal doses can enhance responses related to physiology (e.g., respiration, total lipid content, and total protein content), behavior (e.g., locomotor activity, antennal drumming frequency, host location, and parasitization), and fitness (longevity, growth, fecundity, population net and gross reproduction). Concordantly, the parasitic potential (e.g., infestation efficacy, parasitization rate, and parasitoid/parasite emergence) can be increased, and as a result host activities inhibited. There is some evidence illustrating hormetic dose-responses, but the relevant literature commonly included a limited number and range of doses, precluding a robust differentiation between sub- and superNOAEL (no-observed-adverse-effect level) stimulation. These results reveal a potentially significant threat to ecological health, through stimulation of harmful parasitic organisms by environmental contaminants, and highlight the need to include sublethal stimulation and hormetic responses in relevant ecological pesticide risk assessments. Curiously, considering a more utilitarian view, hormesis may also assist in optimizing mass rearing of biological control agents for field use, a possibility that also remains neglected.

Acaricide exposure impairs predatory behavior of the phytoseiid mite Neoseiulus idaeus (Acari: Phytoseiidae).

Predation is an important interaction that can change the structure of arthropod communities across both temporal and spatial scales. In agricultural systems predation can reduce the population levels of several arthropod pest species of a community. This predator-prey interaction involves the predator searching and handling behaviors. Several factors can affect this interaction, such as pesticide exposure, which is a frequent feature in agroecosystems. Thus, the hypothesis of our study is that the predatory behavior of the phytoseiid mite Neoseiulus idaeus Denmark & Muma, an important natural enemy of spider mites, is affected by acaricide exposure. To test that hypothesis, the predatory mite was exposed to the acaricides abamectin, fenpyroximate, and azadirachtin in 4 exposure scenarios. The predatory behavior of N. idaeus was negatively affected by acaricide exposure when the leaf surface containing both prey and predator was sprayed leading to a reduction in the frequency of transitions between predator walking and meeting preys. Prey handling and consumption were also compromised by acaricide exposure through contaminated leaf surface and prey, and contaminated leaf surface, prey, and predator. Abamectin compromised predation regardless of the exposure scenario. Acaricide-exposure reduced the number of prey found, number of attacks, and number prey killed by N. idaeus. Moreover, partial prey consumption was observed with acaricide-exposed mites. Thus, caution is necessary while attempting to integrate acaricide applications and mass release of N. idaeus for spider mite management.

Low-dose chemical stimulation and pest resistance threaten global crop production.

Pesticide resistance increases and threatens crop production sustainability. Chemical contamination contributes to the development of pest resistance to pesticides, in part by causing stimulatory effects on pests at low sub-toxic doses and facilitating the spread of resistance genes. This article discusses hormesis and low-dose biological stimulation and their relevance to crop pest resistance. It highlights that a holistic approach is needed to tackle pest resistance to pesticides and reduce imbalance in accessing food and improving food security in accordance with the UN's Sustainable Development Goals. Among others, the effects of sub-toxic doses of pesticides should be considered when assessing the impact of synthetic and natural pesticides, while the promotion of alternative agronomical practices is needed to decrease the use of agrochemicals. Potential alternative solutions include camo-cropping, exogenous application of phytochemicals that are pest-suppressing or -repelling and/or attractive to carnivorous arthropods and other pest natural enemies, and nano-technological innovations. Moreover, to facilitate tackling of pesticide resistance in poorer countries, less technology-demanding and low-cost practices are needed. These include mixed cropping systems, diversification of cultures, use of 'push-pull cropping', incorporation of flower strips into cultivations, modification of microenvironment, and application of beneficial microorganisms and insects. However, there are still numerous open questions, and more research is needed to address the ecological and environmental effects of many of these potential solutions, with special reference to trophic webs.

Research Trends, Biases, and Gaps in Phytochemicals as Insecticides: Literature Survey and Meta-Analysis.

A 76-year literature survey and meta-analyses were carried out to recognize the trends, biases, and knowledge gaps of studies focusing on major groups of compounds of botanical origin, or phytochemicals, as insecticides. The survey found that the main phytochemicals prospected as insecticides belong to the following major chemical groups: terpenoids, terpenes, and carbonyl, all of which were tested, mainly against beetles (Coleoptera), caterpillars (i.e., larvae of Lepidoptera), and mosquitoes and other flies (i.e., Diptera). These studies are burgeoning at an exponential rate, with an evident focus on mortality endpoint estimates, but they are also neglecting sublethal assessments. China and India in Asia, as well as Brazil in the Americas, were responsible for most studies. The majority of the papers used stored grain insects as experimental models, which limits the applicability and representativeness of the findings. As a result, the main modes of exposure tested were fumigation and contact, which leads to the prevalence of estimates of lethal concentration in these studies. Therefore, a broader range of insect species deserves testing, with suitable modes of exposure identifying and characterizing the main molecules responsible for the insecticidal activity, which is seldom performed. Attention to these needs will circumvent current biases and allow the recognition of the main patterns of association between the origin and structure of phytochemicals and their insecticidal effects.

Disentangling a Neotropical pest species complex: genetic diversity and population structure of the native rice stink bug Oebalus poecilus and the invasive O. ypsilongriseus.

BACKGROUND: A first step in any pest management initiative is recognizing the existing problem - identifying the pest species and its abundance and dispersal capacities. This is not simple and even more challenging when insidious (invasive) species are involved constituting a pest complex. Understanding a species' population diversity and structure can provide a better understanding of its adaptation and relative pest potential. Such is the need for the native rice stink bug Oebalus poecilus and the invasive O. ypsilongriseus in low and high flatlands of South America. RESULTS: The genetic structure differed between both rice stink bug species (FST  = 0.157, P = 0.001), where 84% of the overall genetic variability takes place within species and three genetic groups were recognized through Bayesian approach (K = 3). Oebalus poecilus exhibited slightly higher genetic diversity (HE  = 0.253) and structuring (FST  = 0.050, P = 0.001) than the invasive O. ypsilongriseus (HE  = 0.211; FST  = 0.038, P = 0.013). Nonetheless, only the former exhibited significant correlation between genetic and geographic distances (r = 0.48, P = 0.013). CONCLUSION: Despite the pointed peculiarities, the obtained results indicate overlap in both species' occurrence and similar genetic structure allowing for a compound problem to be dealt with as the complex requires managing without, as yet, a prevailing species or a niche specialization. © 2022 Society of Chemical Industry.

Plant-pest interactions under the microscope of chemical hormesis.

Low doses of contaminants and toxins can stimulate pests feeding on contaminated tissues of host plants and enhance herbivore activity and plant damage. These effects are opposite to those of high toxic doses, have largely been missed so far, and could compromise crop production. Thus, they deserve further consideration and study.

The effects of thiamethoxam on coffee seedling morphophysiology and Neotropical leaf miner (Leucoptera coffeella) infestations.

BACKGROUND: Coffee (Coffea arabica L.) is one of the main commodities produced in Brazil. Insecticides like the (systemic) neonicotinoid thiamethoxam are widely used to suppress pest populations during coffee production, in particular the Neotropical leaf miner (Leucoptera coffeella Guérin-Mèneville & Perrottet, 1842) (Lepidoptera: Lyonetiidae). In addition to its efficacy against this pest species, thiamethoxam is also thought to be a bioactivator of plant metabolism, but has not yet been tested for such activity. Thus, the objectives of the present study were (1) to assess the concentration-response effects of thiamethoxam on the vegetative vigor of coffee seedlings (C. arabica 'Catuaí 144' cultivar) at different concentrations [2, 20, 40, 80 and 200 mg active ingredient (a.i.) kg-1 ] applied via soil drenching and (2) to evaluate if the plant response interferes with the effectiveness of thiamethoxam in controlling leaf miner populations. The morphophysiological traits of the coffee seedlings were evaluated 20, 40, 60 and 80 days after application, and leaf miner infestations were recorded starting 20 days after the insecticide application with the releasing of adults, and every 20 days afterwards. RESULTS: The results indicated that thiamethoxam has a deleterious effect on the morphophysiological traits of the plants compromising their development with increase in concentrations. However, leaf area exhibited a different pattern with a peak at 50 mg a.i. kg-1 consistent with thiamethoxam-induced hormesis (i.e. biphasic response with stimulatory effect at sublethal range of a toxic substance at the higher concentration). Nonetheless, such bioactivator effect did not affect thiamethoxan effectiveness against the leaf miner even at the lowest concentration tested. CONCLUSION: Thiamethoxan exhibited bioactivation effect on leaf at low concentration, but without compromising efficacy against leaf miner populations. Therefore, its proposed metabolism-boosting properties may encourage the unnecessary use of this insecticide, potentially leading to higher selection for insecticide resistance and an eventual decline in its effectiveness against the Neotropical leaf miner. © 2022 Society of Chemical Industry.

The Genome of Rhyzopertha dominica (Fab.) (Coleoptera: Bostrichidae): Adaptation for Success.

The lesser grain borer, Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae), is a major global pest of cereal grains. Infestations are difficult to control as larvae feed inside grain kernels, and many populations are resistant to both contact insecticides and fumigants. We sequenced the genome of R. dominica to identify genes responsible for important biological functions and develop more targeted and efficacious management strategies. The genome was assembled from long read sequencing and long-range scaffolding technologies. The genome assembly is 479.1 Mb, close to the predicted genome size of 480.4 Mb by flow cytometry. This assembly is among the most contiguous beetle assemblies published to date, with 139 scaffolds, an N50 of 53.6 Mb, and L50 of 4, indicating chromosome-scale scaffolds. Predicted genes from biologically relevant groups were manually annotated using transcriptome data from adults and different larval tissues to guide annotation. The expansion of carbohydrase and serine peptidase genes suggest that they combine to enable efficient digestion of cereal proteins. A reduction in the copy number of several detoxification gene families relative to other coleopterans may reflect the low selective pressure on these genes in an insect that spends most of its life feeding internally. Chemoreceptor genes contain elevated numbers of pseudogenes for odorant receptors that also may be related to the recent ontogenetic shift of R. dominica to a diet consisting primarily of stored grains. Analysis of repetitive sequences will further define the evolution of bostrichid beetles compared to other species. The data overall contribute significantly to coleopteran genetic research.

Hormesis and insects: Effects and interactions in agroecosystems.

Insects in agroecosystems contend with many stressors - e.g., chemicals, heat, nutrient deprivation - that are often encountered at low levels. Exposure to mild stress is now well known to induce hormetic (stimulatory) effects in insects, with implications for insect management, and ecological structure and function in agroecosystems. In this review, we examine the major ecological niches insects occupy or guilds to which they belong in agroecosystems and how hormesis can manifest within and across these groups. The mechanistic underpinnings of hormesis in insects are starting to become established, explaining the many phenotypic hormetic responses observed in insect reproduction, development, and behavior. Whereas potential effects on insect populations are well supported in laboratory experiments, field-based hypothesis-driven research on hormesis is greatly lacking. Furthermore, because most ecological paradigms are founded within the context of communities, entomological agroecologists interested in hormesis need to 'level up' and test hypotheses that explore effects on species interactions, and community structure and functioning. Embedded in this charge is to continue experimentation on herbivorous pest species while shifting more focus towards insect natural enemies, pollinators, and detritivores - guilds that play crucial roles in highly functioning agroecosystems that have been understudied in hormesis research. Important areas for future insect agroecology research on hormesis are discussed.

Does refuge spillover affect arthropod food webs associated with Bt maize?

BACKGROUND: A high dose/refuge combination is the main tactic recommended for mitigating resistance selection of target herbivore species in crops expressing insecticidal proteins of the bacterium Bacillus thuringiensis (i.e. Bt proteins). The tactic consists of the simultaneous use of Bt crops expressing high levels of the Bt protein associated with neighboring areas of refuge of the same non-Bt crop species. Nonetheless, the approach faces controversy regarding its effectiveness and scale of adoption, at least in some regions. One concern focuses on its potential impact on the arthropod community, including its short-term and spatially dependent impact considering the likely biota spillover effect between Bt and non-Bt neighboring areas. Thus, the eventual spillover of Bt maize targeted and non-targeted arthropods was surveyed along transects extending from the refuge border to the center of the Bt maize area. RESULTS: Arthropods were collected throughout the maize vegetative and reproductive stages. A total of 85 arthropod species were collected, but their richness and abundance did not vary with distance from the refuge. By contrast, cultivation season played a significant role in distinguishing the arthropod communities. Refuge distance from the sampling point within Bt-fields did not significantly affect the food web metrics, unlike season, which affected the number of nodes integrating each food web. Winter maize cultivation exhibited higher arthropod diversity and combined values of species numeric abundance and biomass at each trophic level. CONCLUSIONS: No arthropod spillover was evident between the refuge edge and Bt maize, adding further controversy to the tactic currently subjected to lower usage in the region with a disputed cost-benefit relationship, because not even the target and its interdependent species were affected. © 2021 Society of Chemical Industry.

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.

Synergism and unintended effects of the association between imidacloprid and sodium chloride (NaCl) on the management of Euschistus heros.

BACKGROUND: The use of insecticidal solutions containing sodium chloride (NaCl) has been proposed as a more environmentally friendly alternative to managing stink bug infestations of Neotropical soybean fields. The potential sublethal and undesirable effects of this practice have, however, been overlooked, especially with novel insecticides. Here, we have evaluated experimentally whether the addition of NaCl (0.5% w/v) to imidacloprid-containing solutions could alter insecticide toxicity and modify the reproductive responses of the Neotropical brown stink bug Euschistus heros. RESULTS: Adding NaCl to imidacloprid solutions significantly increased imidacloprid toxicity against E. heros. The exposure to E. heros to sublethal concentrations of imidacloprid affected the insect's mating abilities in a concentration-dependent manner. The addition of NaCl to solutions containing imidacloprid at concentrations as low as 0.126 µg a.i. cm-2 (i.e. the equivalent to 3% of field rate recommendation) also impacted the sexual behavior of E. heros, reducing mating duration. NaCl-exposed stink bugs, however, exhibited higher fecundity and fertility rates than those insects that were unexposed to NaCl or those that were exposed to sublethal levels of imidacloprid only. CONCLUSIONS: The addition of low amounts of NaCl resulted in a higher toxicity of imidacloprid. This practice, however, can also lead to undesirable effects as increasing reproductive output of E. heros that can potentially compromise the management of these insect pests.

AC-DC electropenetrography: fundamentals, controversies, and perspectives for arthropod pest management.

Studying the intimate association of arthropods with their physical substrate is both important and challenging. It is important because substrate is a key determinant for organism fitness; challenging because the intricacies of this association are dynamic, and difficult to record and resolve. The advent of electropenetrography (EPG) and subsequent developments allowed researchers to overcome this challenge. Nonetheless, EPG research has been historically restricted to piercing-sucking hemipteran plant pests. Recently, its potential use has been greatly broadened for additional pests with instrument advances. Thus, blood-feeding arthropods and chewing feeders, as well as non-feeding behaviors like oviposition by both pests and parasitoids, are novel new targets for EPG research, with critical consequences for integrated pest management. EPG can explain mechanisms of crop damage, plant or animal pathogen transmission, and the effects of insecticides, antifeedants, repellents, or transgenic plants and animals, on specific behaviors of damage or transmission. This review broadly covers the principles and development of EPG technology, emphasizing controversies and challenges remaining with suggested research to overcome them. In addition, it summarizes 60+ years of basic and applied EPG research, and previews future directions for pest management. The goal is to stimulate new applications for this unique enabling technology. Published 2020. This article is a U.S. Government work and is in the public domain in the USA.

Low temperature shock and chill-coma consequences for the red flour beetle (Tribolium castaneum) and the rice weevil (Sitophilus oryzae).

Insects face several (environmental) abiotic stressors, including low temperature, which cause the failure of neuromuscular function. Such exposure leads insects toa reversible comatose state termed chill-coma, but the consequences of this state for the organism biology were little explored. Here, the consequences of the chill-coma phase were investigated in two of the main stored product pest species - the red flour beetle Tribolium castaneum (larvae and adults) and the rice weevil Sitophilus oryzae (adults). For this purpose, a series of low-temperature shocks were used to estimate the chill-coma recovery time (CCRT), survival, nutrition and weight gain/growth of T. castaneum (larvae and adults) and S. oryzae, as well as the development of T. castaneum life stages. The relatively long CCRT was characteristic of beetle larvae, at different low-temperature shocks, and CCRT increased with decreasing temperatures and increasing exposure intervals for both pest species. The survival was little affected by the low-temperature shocks applied, but such shocks affected insect feeding and growth. Tribolium castaneum larvae was more sensitive than adults of both insect species. Moreover, the relative consumption and weight gain of S. oryzae adults were lower than those of T. castaneum adults and mainly larvae, while feeding deterrence was not affected by low temperature shocks, unlike food conversion efficiency. Low-temperature shocks, even under short duration at some temperatures, significantly delayed development. The lower the temperature and the higher the exposure period, the more delayed the development. Thus, the physiological costs of chill-coma are translated into life-history consequences, with potential implications for the management of this insect pest species in stored products and even more so on red flour beetles and rice weevils.