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Farmers, regulators, and researchers rely on pesticide use data to assess the effects of pesticides on crop yield, farm economics, off-target organisms, and human health. The publicly available pesticide use data in the United States do not currently account for pesticides applied as seed treatments. We find that seed treatment use has increased in major field crops over the last several decades but that there is a high degree of uncertainty about the extent of acreage planted with treated seeds, the amount of regional variability, and the use of certain active ingredients. One reason for this uncertainty is that farmers are less likely to know what pesticides are on their seed than they are about what pesticides are applied conventionally to their crops. This lack of information affects the quality and availability of seed treatment data and also farmers’ ability to tailor pesticide use to production and environmental goals.

Each year, millions of kilograms of insecticides are applied to crops in the US. While insecticide use supports food, fuel, and fiber production, it can also threaten non-target organisms, a concern underscored by mounting evidence of widespread decline of pollinator populations. Here, we integrate several public datasets to generate county-level annual estimates of total ‘bee toxic load’ (honey bee lethal doses) for insecticides applied in the US between 1997–2012, calculated separately for oral and contact toxicity. To explore the underlying components of the observed changes, we divide bee toxic load into extent (area treated) and intensity (application rate x potency). We show that while contact-based bee toxic load remained relatively steady, oral-based bee toxic load increased roughly 9-fold, with reductions in application rate outweighed by disproportionate increases in potency (toxicity/kg) and extent. This pattern varied markedly by region, with the greatest increase seen in Heartland (121-fold increase), likely driven by use of neonicotinoid seed treatments in corn and soybean. In this “potency paradox”, farmland in the central US has become more hazardous to bees despite lower volumes of insecticides applied, raising concerns about insect conservation and highlighting the importance of integrative approaches to pesticide use monitoring.

Each year, millions of kilograms of insecticides are applied to crops in the US. While insecticide use supports food, fuel, and fiber production, it can also threaten non-target organisms, a concern underscored by mounting evidence of widespread insect decline. Nevertheless, answers to basic questions about the spatiotemporal patterns of insecticide use remain elusive, due in part to the inherent complexity of insecticide use, and exacerbated by the dispersed nature of the relevant data, divided between several government repositories. Here, we integrate these public datasets to generate county-level annual estimates of total ‘insect toxic load’ (honey bee lethal doses) for insecticides applied in the US between 1997-2012, calculated separately for oral and contact toxicity. To explore the underlying drivers of the observed changes, we divide insect toxic load into the components of extent (area treated) and intensity (application rate x potency). We show that while contact-based insect toxic load remained relatively steady over the period of our analysis, oral-based insect toxic load increased roughly 9-fold, with reductions in application rate outweighed by disproportionate increases in potency (toxicity/kg) and increases in extent. This pattern varied markedly by region, with the greatest increases seen in Heartland and Northern Great Plains regions, likely driven by use of neonicotinoid seed treatments in corn and soybean. In this “potency paradox,” US farmland has become more hazardous to insects despite lower volumes of insecticides applied, raising serious concerns about insect conservation and highlighting the importance of integrative approaches to pesticide use monitoring.Significance statementPrevious analyses disagree about whether US insecticide use is increasing or decreasing, a question of significant importance given the putative role of insecticides in recent insect declines. We integrated information from multiple national databases to estimate ‘insect toxic load’ (represented as honey bee lethal doses) of the agricultural insecticides applied in each US county from 1997 to 2012, and factors responsible for its change. Across the US, insect toxic load – calculated on the basis of oral toxicity – increased 9-fold. This increase was due to increases in the potency (toxicity/kg) of insecticides applied and in the area treated; the volume of insecticides applied declined. Toxic load increased most dramatically in regions where neonicotinoid seed treatments for field crops are commonly used.

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.

Educational materials guiding the use of pesticides are often sponsored or co-created by pesticide manufacturers, raising potential conflicts of interest. For example, early in 2017, two registrant-sponsored webinars from the American Society of Agronomy addressed benefits of neonicotinoid seed coatings, which are routinely applied to seeds of many field crops. While these products can protect yield in certain situations, they also carry significant limitations; unfortunately, these presentations avoided such downsides. Here, we provide an overview of key limitations of neonicotinoid seed treatments (NST). First, we address Integrated Pest Management (IPM) and how current use of NST violates its key principles and ignores lessons learned. Second, we address inconsistent yield responses, resistance concerns, and nontarget effects. Third, we return to IPM to discuss how this proven framework can be used to more effectively guide and steward NST to avoid mounting reports of negative side effects.

Summary 1. Neonicotinoids are the most widely used insecticides world-wide, but their fate in the environment remains unclear, as does their potential to influence non-target species and the roles they play in agroecosystems. 2. We investigated in laboratory and field studies the influence of the neonicotinoid thiamethoxam, applied as a coating to soya bean seeds, on interactions among soya beans, nontarget molluscan herbivores and their insect predators. 3. In the laboratory, the pest slug Deroceras reticulatum was unaffected by thiamethoxam, but transmitted the toxin to predaceous beetles (Chlaenius tricolor), impairing or killing >60%. 4. In the field, thiamethoxam-based seed treatments depressed activity–density of arthropod predators, thereby relaxing predation of slugs and reducing soya bean densities by 19% and yield by 5%. 5. Neonicotinoid residue analyses revealed that insecticide concentrations declined through the food chain, but levels in field-collected slugs (up to 500 ng g 1 ) were still high enough to harm insect predators. 6. Synthesis and applications. Our findings reveal a previously unconsidered ecological pathway through which neonicotinoid use can unintentionally reduce biological control and crop yield. Trophic transfer of neonicotinoids challenges the notion that seed-applied toxins precisely target herbivorous pests and highlights the need to consider predatory arthropods and soil communities in neonicotinoid risk assessment and stewardship.

BackgroundSeed-applied neonicotinoids are widely used in agriculture, yet their effects on non-target species remain incompletely understood. One important group of non-target species is arthropod natural enemies (predators and parasitoids), which contribute considerably to suppression of crop pests. We hypothesized that seed-applied neonicotinoids reduce natural-enemy abundance, but not as strongly as alternative insecticide options such as soil- and foliar-applied pyrethroids. Furthermore we hypothesized that seed-applied neonicotinoids affect natural enemies through a combination of toxin exposure and prey scarcity.MethodsTo test our hypotheses, we compiled datasets comprising observations from randomized field studies in North America and Europe that compared natural-enemy abundance in plots that were planted with seed-applied neonicotinoids to control plots that were either (1) managed without insecticides (20 studies, 56 site-years, 607 observations) or (2) managed with pyrethroid insecticides (eight studies, 15 site-years, 384 observations). Using the effect size Hedge’sdas the response variable, we used meta-regression to estimate the overall effect of seed-applied neonicotinoids on natural-enemy abundance and to test the influence of potential moderating factors.ResultsSeed-applied neonicotinoids reduced the abundance of arthropod natural enemies compared to untreated controls (d= −0.30 ± 0.10 [95% confidence interval]), and as predicted under toxin exposure this effect was stronger for insect than for non-insect taxa (QM= 8.70, df = 1,P= 0.003). Moreover, seed-applied neonicotinoids affected the abundance of arthropod natural enemies similarly to soil- or foliar-applied pyrethroids (d= 0.16 ± 0.42 or −0.02 ± 0.12; with or without one outlying study). Effect sizes were surprisingly consistent across both datasets (I2 = 2.7% for no-insecticide controls;I2 = 0% for pyrethroid controls), suggesting little moderating influence of crop species, neonicotinoid active ingredients, or methodological choices.DiscussionOur meta-analysis of nearly 1,000 observations from North American and European field studies revealed that seed-applied neonicotinoids reduced the abundance of arthropod natural enemies similarly to broadcast applications of pyrethroid insecticides. These findings suggest that substituting pyrethroids for seed-applied neonicotinoids, or vice versa, will have little net affect on natural enemy abundance. Consistent with previous lab work, our results also suggest that seed-applied neonicotinoids are less toxic to spiders and mites, which can contribute substantially to biological control in many agricultural systems. Finally, our ability to interpret the negative effect of neonicotinoids on natural enemies is constrained by difficulty relating natural-enemy abundance to biological control function; this is an important area for future study.