Multi-scale availability of neonicotinoid-treated seed for wildlife in an agricultural landscape during spring planting

Highlights

• We quantified neonicotinoid-treated seeds on the soil surface after planting.

• Probability and density of soybean seeds on the soil surface were higher than corn.

• Neonicotinoids decreased rapidly on seeds on the soil surface but persisted 30 days.

• Over a dozen species of birds and mammals consumed seeds at simulated spills.

• Seeds on the soil surface should be considered in pesticide risk assessments.

Abstract

Neonicotinoid pesticides are applied to seeds and are known to cause lethal and sub-lethal effects in birds and mammals. Neonicotinoid-treated seeds could be available to wildlife through spillage or exposed seeds near or at the soil surface due to incomplete or shallow drilling. We quantified seed spills that may occur during loading or refilling the hopper at a landscape-scale using road-based surveys. We also quantified undrilled seeds in 1-m² frames on the soil in the center and corner of fields to obtain estimates at the field scale. We broadcast seeds on the soil surface of a tilled field and left them for 0, 1, 2, 4, 8, 16, and 30 days to quantify the decrease of neonicotinoids under field conditions. Lastly, we documented wildlife at neonicotinoid-treated seed spills with trail cameras. We estimated the number of spills during planting to be 3496 (95% CI: 1855–5138) and 2609 (95% CI: 862–4357) for corn, 11,009 (95% CI: 6950–15,067) and 21,105 (95% CI: 6162–36,048) for soybean, and 830 (95% CI: 160–1500) and 791 (95% CI: 0–1781) for wheat in 2016 and 2017, respectively. Exposed seeds were present at the soil surface in 35% of 71 fields. The probability that seeds were present on the soil surface was higher for soybeans (18.8 and 49.4% in the center and corners, respectively) than for corn (1.6 and 2.7%, respectively), and seed densities were also higher (1.04 vs 0.07 seeds/m², respectively). Neonicotinoids decreased rapidly on seeds on the soil surface but persisted as long as 30 days. Over a dozen species of birds and mammals consumed seeds at simulated spills, with an average time for birds to find spills of 1.3 ± 1.5 days and an average time to consumption of 4.1 ± 3.4 days. Seeds are abundant on the soil surface for wildlife to consume during the spring planting season and should be considered in pesticide risk assessments.

Introduction

Neonicotinoids, including imidacloprid (IMI), clothianidin (CLO), and thiamethoxam (TMX), comprise 25% of the global agricultural insecticide market, making them the most widely used pesticides worldwide, with imidacloprid comprising nearly half of this market (Jeschke et al., 2011; Mineau and Palmer, 2013; Goulson, 2013) until 2012 when thiamethoxam had the largest market share (Bass et al., 2015). Neonicotinoids are systemic pesticides that are commonly applied as seed treatments to important food crops like corn, soybeans, oilseed rape, sunflower, cereals, and beets. About 2–20% of the seed treatment is taken up by the plant as it grows and is distributed among the leaves, flowers, pollen, and nectar, at concentrations sufficient to control invertebrate pests (e.g., 5–10 μg per liter in sap; Sanchez-Bayo, 2014). Invertebrates are impacted at doses (0.82–88 ng active ingredient/insect) that are considered safe for vertebrates, because toxicity in vertebrates requires exposure to doses (14–5000 mg active ingredient/kg body weight) that greatly exceed the levels that produce effects in invertebrates (Goulson, 2013). Neonicotinoids bind very specifically to invertebrate nicotinic acetylcholine receptors, and because they bind less strongly to vertebrate receptors and are not as persistent in the environment as organochlorines, they have been considered much less toxic to vertebrates than pesticide options that predated the early 1990's (Tomizawa and Casida, 2005; Jeschke et al., 2011). This high specificity and systemic nature contributed to their widespread and rapid adoption beginning in 1994 with the registration of imidacloprid in the United States (FIFRA, 1996).

Importantly, demonstrated impacts of neonicotinoids on non-target invertebrates have been documented over the last decade (Krupke et al., 2012; Sanchez-Bayo, 2014; Goulson et al., 2015). Concerns for incidental impacts on pollinators (e.g., through availability in nectar and pollen) led the European Union to ban or place a moratorium on use of IMI, CLO, and TMX on flowering crops in 2013. In May 2018, the moratorium was expanded to include all outdoor use of IMI, CLO, and TMX by the end of 2018, based on the threat that these chemicals pose to pollinators due to their persistence in soil, solubility in water, transport away from the site of application, and uptake by other plants (Krupke et al., 2012; Main et al., 2014; Bonmatin et al., 2015; Morrissey et al., 2015). However, these pesticides are widely used in North America, and elsewhere in the world. Recent studies are now also documenting adverse effects of neonicotinoids that reach beyond pollinators to include vertebrates (see reviews in Mineau and Palmer, 2013; Gibbons et al., 2014). In the United States, neonicotinoids are currently under registration review by the Environmental Protection Agency (EPA), with risks to both pollinators and non-pollinators, including birds and mammals, under consideration.

Vertebrate toxicity is expected to occur at doses that exceed the levels available in crop plants consumed by humans and livestock (FIFRA 1996). Wild birds and mammals are most likely to be exposed to large doses of neonicotinoids through ingestion of treated seeds (Goulson, 2013; Gibbons et al., 2014), although numerous other exposure mechanisms exist (e.g., soil, trophic transfer; SERA, 2005; Douglas et al., 2015). The Minnesota Department of Agriculture (2014) stated that, “Although neonicotinoids are less toxic to vertebrates than to arthropods, direct consumption of neonicotinoid treated seeds may expose birds and other taxa to acute or chronic doses.” Ingestion of a small number of neonicotinoid-treated seeds can be lethal to birds; for example, ingestion of a single treated corn kernel is lethal to a blue-jay sized (~85 g) bird (see reviews in Mineau and Palmer, 2013; Gibbons et al., 2014). However, toxicity varies by chemical and species, given differences in genetic and physiological factors including size, absorption, distribution, metabolic, and excretion processes (Bean et al., 2019). Differences among species in seed handling behavior could affect the ingested amount of chemical (Avery et al., 1997).

Sub-lethal effects in birds in the lab include hyporeactivity, lack of coordination, wing drop, immobility, disruption of migratory coordination, eggshell thinning, reduced egg hatching rate, impaired testicular function, and low weight in chicks (Cox, 2001; Lopez-Antia et al., 2013, Lopez-Antia et al., 2014, Lopez-Antia et al., 2015; Tokumoto et al., 2013; Mineau and Palmer, 2013; Eng et al., 2017). Sub-lethal impacts in mammals include delayed sexual maturation, sperm deformities, premature deliveries, stillbirths, and offspring deformities (Rexrode et al., 2003; Anon, 2007). Yet, studies of neonicotinoid effects on vertebrates are overwhelmingly laboratory-based (91% of studies), which limits our ability to interpret the significance of findings in more natural settings (Gibbons et al., 2014).

Neonicotinoid-treated seeds could be available to wildlife through spillage during transport, reloading and refilling of the hopper or through seeds near or at the soil surface after planting (de Leeuw et al., 1995; Pascual et al., 1999; Lopez-Antia et al., 2016). The U.S. EPA estimated that ~1% of seeds remain accessible to granivores after planting (as reported by Goulson, 2013; Lopez-Antia et al., 2015). Higher densities of exposed seeds generally result in greater attraction of birds to fields (Murton et al., 1963; Feare et al., 1974). In Spain, 30 bird species were observed picking up treated seeds from cereal fields, and 3.1% of red-legged partridge (Alectoris rufa) gut contents collected by hunters tested positive for imidacloprid after planting of winter cereal crops despite insecticides not normally being used on winter cereal crops in the study area (Lopez-Antia et al., 2016). More recently in Texas, USA, 7 of 57 northern bobwhite (Colinus virginianus) livers had detectable concentrations of neonicotinoids (Ertl et al., 2018).

Given the toxicity to birds and mammals at the concentrations of neonicotinoids applied to treated seeds, consumption of treated seeds would be expected to produce lethal or sub-lethal effects in granivorous wildlife, yet poisoning incidents are infrequently reported. Dead and poisoned partridges have been found in agricultural fields in France following use of imidacloprid-treated seed (Berny et al., 1999; Mineau and Palmer, 2013; Millot et al., 2017). A few other pesticide poisoning incidents have been detected (Greig-Smith, 1987; Fletcher et al., 1995; de Snoo et al., 1999), but carcasses can be scavenged quickly (Ponce et al., 2010), may not be localized or may be inconspicuous if effects are not immediate (de Snoo et al., 1999), and may not raise suspicion of pesticides as the cause of death (Millot et al., 2017). Thus, seed consumption or sub-lethal exposure may be easier to detect in field settings than mortalities.

Field studies conducted in Spain have focused on availability and consumption of winter cereals (wheat, oats, barley, and triticale seeds) planted in the fall (Lopez-Antia et al., 2016). We therefore conducted a study to estimate availability and document wildlife consumption of neonicotinoid-treated seeds during the spring planting season in the Midwestern USA. Birds are initiating nests, laying eggs, and incubating nests during the spring, and mammals give birth and raise young, so sub-lethal reproductive effects related to consumption of treated seeds during the breeding season might be particularly long-lasting. Furthermore, we examined an agricultural landscape dominated by corn, soybeans, and wheat, which provided 3 sizes of seeds that may be ingested by birds with varied beak sizes and bill types, as well as mammals that consume beans and grains. Almost all corn planted in the Midwestern USA has been treated with these pesticides (Stokstad, 2013); most soybean, wheat, and sunflower seeds are treated also; and neonicotinoids are applied as a foliar spray for several other crop types.

The overarching objective of our research was to determine whether wildlife may be exposed to potentially lethal or sub-lethal doses of neonicotinoids through treated seeds during the spring planting season. Specifically, we aimed to:

• Quantify the rate of large seed spills during planting season at a landscape scale.

• Quantify the availability of seeds on the soil surface in fields after planting.

• Quantify the decrease of neonicotinoids (IMI, TMX, and CLO) on treated seeds left on the soil surface for up to 30 days.

• Quantify the time for wildlife to find neonicotinoid-treated seed spills and determine whether wildlife consume treated seeds at simulated spills.