Summary 1. Neonicotinoids are now the most widely used insecticides in the world. They act systemically, travelling through plant tissues and protecting all parts of the crop, and are widely applied as seed dressings. As neurotoxins with high toxicity to most arthropods, they provide effective pest control and have numerous uses in arable farming and horticulture. 2. However, the prophylactic use of broad-spectrum pesticides goes against the long-established principles of integrated pest management (IPM), leading to environmental concerns. 3. It has recently emerged that neonicotinoids can persist and accumulate in soils. They are water soluble and prone to leaching into waterways. Being systemic, they are found in nectar and pollen of treated crops. Reported levels in soils, waterways, field margin plants and floral resources overlap substantially with concentrations that are sufficient to control pests in crops, and commonly exceed the LC50 (the concentration which kills 50% of individuals) for beneficial organisms. Concentrations in nectar and pollen in crops are sufficient to impact substantially on colony reproduction in bumblebees. 4. Although vertebrates are less susceptible than arthropods, consumption of small numbers of dressed seeds offers a route to direct mortality in birds and mammals. 5. Synthesis and applications. Major knowledge gaps remain, but current use of neonicotinoids is likely to be impacting on a broad range of non-target taxa including pollinators and soil and aquatic invertebrates and hence threatens a range of ecosystem services.

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REVIEW: An overview of the environmental risks posed by neonicotinoid insecticides

Since their discovery in the late 1980s, neonicotinoid pesticides have become the most widely used class of insecticides worldwide, with large-scale applications ranging from plant protection (crops, vegetables, fruits), veterinary products, and biocides to invertebrate pest control in fish farming. In this review, we address the phenyl-pyrazole fipronil together with neonicotinoids because of similarities in their toxicity, physicochemical profiles, and presence in the environment. Neonicotinoids and fipronil currently account for approximately one third of the world insecticide market; the annual world production of the archetype neonicotinoid, imidacloprid, was estimated to be ca. 20,000 tonnes active substance in 2010. There were several reasons for the initial success of neonicotinoids and fipronil: (1) there was no known pesticide resistance in target pests, mainly because of their recent development, (2) their physicochemical properties included many advantages over previous generations of insecticides (i.e., organophosphates, carbamates, pyrethroids, etc.), and (3) they shared an assumed reduced operator and consumer risk. Due to their systemic nature, they are taken up by the roots or leaves and translocated to all parts of the plant, which, in turn, makes them effectively toxic to herbivorous insects. The toxicity persists for a variable period of time—depending on the plant, its growth stage, and the amount of pesticide applied. A wide variety of applications are available, including the most common prophylactic non-Good Agricultural Practices (GAP) application by seed coating. As a result of their extensive use and physicochemical properties, these substances can be found in all environmental compartments including soil, water, and air. Neonicotinoids and fipronil operate by disrupting neural transmission in the central nervous system of invertebrates. Neonicotinoids mimic the action of neurotransmitters, while fipronil inhibits neuronal receptors. In doing so, they continuously stimulate neurons leading ultimately to death of target invertebrates. Like virtually all insecticides, they can also have lethal and sublethal impacts on non-target organisms, including insect predators and vertebrates. Furthermore, a range of synergistic effects with other stressors have been documented. Here, we review extensively their metabolic pathways, showing how they form both compound-specific and common metabolites which can themselves be toxic. These may result in prolonged toxicity. Considering their wide commercial expansion, mode of action, the systemic properties in plants, persistence and environmental fate, coupled with limited information about the toxicity profiles of these compounds and their metabolites, neonicotinoids and fipronil may entail significant risks to the environment. A global evaluation of the potential collateral effects of their use is therefore timely. The present paper and subsequent chapters in this review of the global literature explore these risks and show a growing body of evidence that persistent, low concentrations of these insecticides pose serious risks of undesirable environmental impacts.

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Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites

We assessed the state of knowledge regarding the effects of large-scale pollution with neonicotinoid insecticides and fipronil on non-target invertebrate species of terrestrial, freshwater and marine environments. A large section of the assessment is dedicated to the state of knowledge on sublethal effects on honeybees (Apis mellifera) because this important pollinator is the most studied non-target invertebrate species. Lepidoptera (butterflies and moths), Lumbricidae (earthworms), Apoidae sensu lato (bumblebees, solitary bees) and the section “other invertebrates” review available studies on the other terrestrial species. The sections on freshwater and marine species are rather short as little is known so far about the impact of neonicotinoid insecticides and fipronil on the diverse invertebrate fauna of these widely exposed habitats. For terrestrial and aquatic invertebrate species, the known effects of neonicotinoid pesticides and fipronil are described ranging from organismal toxicology and behavioural effects to population-level effects. For earthworms, freshwater and marine species, the relation of findings to regulatory risk assessment is described. Neonicotinoid insecticides exhibit very high toxicity to a wide range of invertebrates, particularly insects, and field-realistic exposure is likely to result in both lethal and a broad range of important sublethal impacts. There is a major knowledge gap regarding impacts on the grand majority of invertebrates, many of which perform essential roles enabling healthy ecosystem functioning. The data on the few non-target species on which field tests have been performed are limited by major flaws in the outdated test protocols. Despite large knowledge gaps and uncertainties, enough knowledge exists to conclude that existing levels of pollution with neonicotinoids and fipronil resulting from presently authorized uses frequently exceed the lowest observed adverse effect concentrations and are thus likely to have large-scale and wide ranging negative biological and ecological impacts on a wide range of non-target invertebrates in terrestrial, aquatic, marine and benthic habitats.

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Effects of neonicotinoids and fipronil on non-target invertebrates

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 escala...

Large-Scale Deployment of Seed Treatments Has Driven Rapid Increase in Use of Neonicotinoid Insecticides and Preemptive Pest Management in U.S. Field Crops

Fungicides are indispensable to global food security and their use is forecasted to intensify. Fungicides can reach aquatic ecosystems and occur in surface water bodies in agricultural catchments throughout the entire growing season due to their frequent, prophylactic application. However, in comparison to herbicides and insecticides, the exposure to and effects of fungicides have received less attention. We provide an overview of the risk of fungicides to aquatic ecosystems covering fungicide exposure (i.e., environmental fate, exposure modeling, and mitigation measures) as well as direct and indirect effects of fungicides on microorganisms, macrophytes, invertebrates, and vertebrates. We show that fungicides occur widely in aquatic systems, that the accuracy of predicted environmental concentrations is debatable, and that fungicide exposure can be effectively mitigated. We additionally demonstrate that fungicides can be highly toxic to a broad range of organisms and can pose a risk to aquatic biota. Finally, we outline central research gaps that currently challenge our ability to predict fungicide exposure and effects, promising research avenues, and shortcomings of the current environmental risk assessment for fungicides.

Fungicides: An overlooked pesticide class?

Insecticidal seed treatments are increasingly being applied to soybeans in North America, and several recent studies question what they add to current pest management. Here, we examine the effects of two neonicotinoid insecticidal seed treatments on insect populations (pest and natural enemies) in SD soybeans over 2 years. Moreover, we conducted laboratory experiments to determine the duration that seed treatments remained effective against the soybean aphid (Aphis glycines, Hemiptera: Aphididae) and how thiamethoxam affected survival of one of the aphid’s predators, Orius insidiosus (Hemiptera: Anthocoridae) on soybean. Soybean aphids, thrips, and grasshopper populations were unaffected by the insecticidal seed treatments in the field. The laboratory trial revealed that all bioactivity of the seed treatments against soybean aphids was gone within 46 days after planting, prior to aphid populations damaging the crop. Bean leaf beetles, a sporadic pest in our area, were reduced by the seed treatments. But, there were no yield benefits of insecticidal seed treatments over the 2 years of the study at this location. Natural enemy communities were significantly reduced by thiamethoxam seed treatments relative to the untreated control, particularly populations of Nabis americoferus (Hemiptera: Nabidae). Chrysoperla (Neuroptera: Chrysopidae) adults were reduced in the imidacloprid-treated plots. In the laboratory, rearing O. insidiosus on soybean plants treated with thiamethoxam resulted in higher mortality for both the nymphs and the adult stage. Offering the predator insect prey on the thiamethoxam-treated plants improved survival of the adult stage, but not the nymphal stage. This work confirms that insecticidal seed treatments offer little benefit to soybean producers of the Northern Great Plains and adds to the discussion by suggesting that generalist predators are adversely affected by the insecticides.

Effects of neonicitinoid seed treatments on soybean aphid and its natural enemies

Lady beetle oviposition behavior in response to the trophic environment

Sucrose was applied weekly throughout the growing season at three US locations (South Dakota [SD], Maryland [MD], and Kentucky [KY]), and coccinellids and aphids (Aphis glycines Matsumura [Hemiptera: Aphididae]) were sampled 24 h later. Total coccinellid densities were 50–77% greater in sugar-sprayed soybean than in untreated plots. Coccinella septempuncata L., Hippodamia convergens Guerin-Meneville, and Harmonia axyridis Pallas were more abundant where sugar was applied. Coleomegilla maculata (DeGeer) was found in equally low numbers in all treatments. Aphid densities were similar in both treatments, and only reached economically threatening levels in SD. Coccinellids digested sugar meals within 1 h of consumption (measured using the cold anthrone test). Despite this narrow window of detection, field-collected coccinellids frequently tested positive for fructose. Under natural conditions, sugar is commonly ingested by coccinellids and sugar sprays increase coccinellid densities and their consumption of sugar. Sugar sprays did not enhance biological control of aphids in this experiment.

Sugar feeding by coccinellids under field conditions: the effects of sugar sprays in soybean

https://pubag.nal.usda.gov/download/48980/pdf

Oviposition response by Orius insidiosus (Hemiptera: Anthocoridae) to plant quality and prey availability

We hypothesize that herbivory by predators is affected by the complexity of their diet. Coleomegilla maculata larvae fed prey – Acyrthosiphon pisum or Ostrinia nubilalis eggs – consumed two to three times more plant tissue (pinto beans) than those fed a mixed diet (containing pollen substitute and prey-based components). Simple, prey-only diets appear to lack plant-based nutrients important to this predator.

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Michael P. Seagraves

Papers

Effects of neonicitinoid seed treatments on soybean aphid and its natural enemies

Lady beetle oviposition behavior in response to the trophic environment

Sugar feeding by coccinellids under field conditions: the effects of sugar sprays in soybean

Oviposition response by Orius insidiosus (Hemiptera: Anthocoridae) to plant quality and prey availability

The effects of diet on herbivory by a predaceous lady beetle