We present a method for calculating the Acute Insecticide Toxicity Loading (AITL) on US agricultural lands and surrounding areas and an assessment of the changes in AITL from 1992 through 2014. The AITL method accounts for the total mass of insecticides used in the US, acute toxicity to insects using honey bee contact and oral LD 50 as reference values for arthropod toxicity, and the environmental persistence of the pesticides. This screening analysis shows that the types of synthetic insecticides applied to agricultural lands have fundamentally shifted over the last two decades from predominantly organophosphorus and N-methyl carbamate pesticides to a mix dominated by neonicotinoids and pyrethroids. The neonicotinoids are generally applied to US agricultural land at lower application rates per acre; however, they are considerably more toxic to insects and generally persist longer in the environment. We found a 48- and 4-fold increase in AITL from 1992 to 2014 for oral and contact toxicity, respectively. Neonicotinoids are primarily responsible for this increase, representing between 61 to nearly 99 percent of the total toxicity loading in 2014. The crops most responsible for the increase in AITL are corn and soybeans, with particularly large increases in relative soybean contributions to AITL between 2010 and 2014. Oral exposures are of potentially greater concern because of the relatively higher toxicity (low LD 50 s) and greater likelihood of exposure from residues in pollen, nectar, guttation water, and other environmental media. Using AITL to assess oral toxicity by class of pesticide, the neonicotinoids accounted for nearly 92 percent of total AITL from 1992 to 2014. Chlorpyrifos, the fifth most widely used insecticide during this time contributed just 1.4 percent of total AITL based on oral LD 50 s. Although we use some simplifying assumptions, our screening analysis demonstrates an increase in pesticide toxicity loading over the past 26 years, which potentially threatens the health of honey bees and other pollinators and may contribute to declines in beneficial insect populations as well as insectivorous birds and other insect consumers.

Competing interests: KK is a staff scientist at Friends of the Earth. MD is the Principal Scientist of Toxicology Research International (TRI), which is a Sole Proprietorship. SK is the Principal Scientist and CEO of Pesticide Research Institute (PRI) and RR is a Staff Scientist at PRI. This does not alter adherence to PLOS ONE policies on sharing data and materials. There are no patents, products in development, or marketed products to declare.

Funding: This study was funded by Friends of the Earth U.S. (FOE). MD, SK, RR, and PM received research fees as contractors to FOE. KK is a staff scientist at FOE. SK and RR are paid employees of the Pesticide Research Institute (PRI). The specific roles of these authors are articulated in the “author contributions.” The funders did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2019 DiBartolomeis et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

Insects form the basis of the food web that sustains life on Earth. They are critical to ecosystem success, providing food for amphibians, fish, birds, reptiles, and mammals. Insects play a role in decomposing animal wastes and dead vegetation, recycling the nutrients in these materials and returning them to the soil. Insects also contribute to the agricultural production of crops that feed humankind, both as the primary pollinators of many plants and as natural controls of pest insects that feed on crops important to human survival. A diverse population of insects benefits agriculture by keeping a balance between predatory and pest insects and providing pollination services [1].

Insecticides targeting crop-damaging pests reduce both the number and diversity of insects in an ecosystem [2]. With conventional farming practices relying primarily on chemical insecticides for pest insect management, ecosystems comprising US agricultural lands are highly impacted through both direct effects on insects and direct and indirect effects on other species [3]. Although many members of the ecosystem may not be exposed to sufficient doses of insecticides to suffer acutely lethal poisonings, sublethal and indirect adverse effects have been demonstrated to occur [4].

Insecticide use patterns in the US The types of synthetic insecticides applied to agricultural lands have fundamentally shifted over the last two decades from predominantly organophosphorus and N-methyl carbamate insecticides to substantially lower amounts of organophosphorus compounds along with a substantial increase in neonicotinoids and a modest increase in pyrethroids (Fig 1). Petroleum derivatives such as mineral oil and inorganics such as kaolin clay, lime-sulfur, cryolite, and borates remain as some of the primary lower-toxicity chemical classes of insecticides in current use, with little change over time. PPT PowerPoint slide

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larger image TIFF original image Download: Fig 1. Change in use of insecticide chemical classes in the US (1992–2014). Data source: US Geological Survey pesticide use estimates for the US [5–7]. https://doi.org/10.1371/journal.pone.0220029.g001 These changes in use patterns reflect the outcome of US Environmental Protection Agency (US EPA) re-registration of pesticides mandated by the Food Quality Protection Act of 1996 and the development of new pesticide chemistries targeting different receptors in insect physiology to combat resistance in pest species [8]. These changes have almost certainly altered the toxicity landscape for insects. In general, systemic pesticides, in particular the neonicotinoids, are now one of the preferred or most readily available and economically efficient class of insecticides used in conventional agriculture practices in rotation with carbamate, pyrethroid, and organophosphorus-containing pesticide products, many of which are still registered for use in the US. The organophosphorus and N-methyl carbamate classes of pesticides are highly toxic to insects but are not especially persistent in the environment, with half-lives ranging from several days to several weeks [9, 10]. Neonicotinoids, like organophosphates and N-methyl carbamates, are neurotoxicants that target the central nervous system by binding to nicotinic acetylcholine receptors leading to overstimulation and paralysis. However, neonicotinoids generally pose lower acute hazards to mammals and greater toxicity to insects due to their differential binding abilities to invertebrate and vertebrate cholinergic receptors (Table 1) [11]. The nitro-substituted neonicotinoids, including imidacloprid, thiamethoxam, and clothianidin (which is also a metabolite of thiamethoxam), are the most frequently used neonicotinoids and tend to have measurably greater persistence than the organophosphorus, carbamate, and pyrethroid insecticides, with half-lives of 39 to 174 days in soils (see S1 Appendix for the source information of these data). In addition, the neonicotinoids exhibit higher water solubility, leading to greater exposure potential for insects consuming pollen, nectar, guttation water, or plant tissue or aquatic insects exposed to runoff containing these pesticides [12]. On the other hand, lipophilic chemicals would tend to accumulate more in the lipid components of pollen and bee bread [13]. PPT PowerPoint slide

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larger image TIFF original image Download: Table 1. Top ten most acutely toxic insecticides to honey bees by the oral route. https://doi.org/10.1371/journal.pone.0220029.t001 Although the neonicotinoids are highly toxic to insects, their effects are not confined to insects. For example, recent analyses indicate that insectivorous bird declines observed in the Netherlands and France appear to be associated with the use of neonicotinoid insecticides in the field or as seed treatments [14, 15]. Another review of the direct and indirect ecosystem effects of insecticides linked impaired growth in fish to reductions in invertebrate prey due to imidacloprid and fipronil use and linked reductions in lizard species to the effects of fipronil on termite prey [3]. Surface waters in agricultural areas have been shown to contain concentrations of neonicotinoids that exceed acute and chronic “invertebrate aquatic life benchmarks” and toxicity thresholds (e.g., no observed effect concentrations or NOEC) for aquatic life [16, 17]. Long-term pest control often suffers from pesticide application since beneficial predatory insects that consume pest insects are susceptible to insecticide exposure and often not as quick to rebound [18–20]. Prophylactic use of neonicotinoids as seed treatments in corn, soy, and other crops has risen in recent years; research has shown that this use has potentially damaged predatory beneficial insect populations and disrupted integrated pest management (IPM) programs [21].

Honey bees as an indicator species of ecotoxicity Honey bees are the most well studied indicator of insect health in US agricultural lands and surrounding areas. Because they are economically important for crop pollination, honey production, and wild plant pollination, the National Agricultural Statistics Service (NASS) tracks colony counts and honey production in the US [22]. The honey bee (Apis mellifera) is generally considered to be relatively sensitive to pesticides when compared to other bee species [23] and has historically been used as an indicator for ecotoxicological testing. However, there has also been some concern that the honey bee is not a good indicator for other bees or other beneficial insects because of species differences in autecology and sensitivity [24]. Information is being developed on the toxicity of insecticides to pollinators other than honey bees, notably bumble bees (Bombus species) and several solitary bee species. However, to date, data are only available for a small proportion of active ingredients, and tests have not been standardized. Heard et al. developed a “standardized” toxicity test system to compare the relative sensitivity between bee species in terms of a pesticide’s toxic potency and the time needed for the onset of toxicity [24]. Although there were significant inter-species differences that varied through time, overall, the magnitude of these differences was generally within an acceptable two-fold range. A recent meta-analysis of paired toxicity data from the same sources demonstrated a high variability of sensitivity among bee species (Max/Min ratio from 0.001 to 2085.7) [23]. However, an extrapolation factor of 10 applied to honey bee toxicity endpoints was sufficiently protective in 95 percent of cases, and the honey bee tended (as shown by a median value of ratios) to be slightly more sensitive than the paired test species. Sanchez-Bayo and Goka regressed Bombus LD 50 values against Apis LD 50 values and concluded that the susceptibility of both genera was similar when exposed by the oral route [25]. However, the honey bee was found to be more sensitive than bumble bees by the contact route even after correcting for weight. It is clear that the susceptibility of any one insect species could be substantially different from another. In our work, we use honey bee toxicity as an indicator for other bees and beneficial insects in US agricultural land because the available data appear to demonstrate that the honey bee is sensitive to the toxicity of chemical pesticides and has the most comprehensive data set available for insects. Until more data on other insects become available, the use of the honey bee as an indicator for other species is a reasonable approach to show how insecticide toxicity loadings have changed over time. The toxicity database on honey bees is compiled from test results submitted by pesticide manufacturers (“registrants”), academic researchers, and other independent research institutes. In order to register (license) a pesticide product in the US, applicants for registration must satisfy several criteria specified in the Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA) including but not limited to the product’s toxicity in a variety of biological systems, its fate and impact on the environment, and for certain pesticide products, proof of its performance (efficacy) [26]. Acute lethality (LD 50 ) testing in honey bees is required under FIFRA, however, field tests are only required on a rarely invoked case-by-case basis. Despite these limitations and data gaps, the acute toxicity data base (LD 50 s) for honey bees is sufficient to allow for a comparative screening analysis of acute insecticide toxicity loading in the environment.