Neonicotinoids are insecticides used worldwide in agriculture as seed treatments on crops such as corn and soya (Garthwaite et al. 2003; Jeschke et al. 2011). This class of pesticide includes acetamiprid, clothianidin, dinotefuran, imidacloprid, nitenpyram, nithiazine, thiacloprid, and thiamethoxam. Imidacloprid, clothianidin, and thiamethoxam are the most common NNIs applied for agricultural use in Ontario (Somers and Chung 2014). Wild turkeys in Ontario and other regions live within concentrated areas used for agriculture and often rely on croplands for supplemental feeding to survive, particularly in winter months (Porter et al. 1980; Vander Haegen et al. 1989). Thus far, NNIs have been best known for the adverse effects they cause in honey bees. Mass die-offs, and subsequent declines in bee population numbers, have garnered widespread attention and concern in recent years because of the importance of bees in providing a vital ecosystem service, namely, pollination (Whitehorn et al. 2012; Godfray et al. 2015; Rundlöf et al. 2015).
Pesticides, including the NNIs clothianidin and thiamethoxam, were detected in the liver of nearly half of wild turkeys tested. These turkeys were likely exposed to NNIs by consuming pesticide-coated seeds during crop sowing that spring, as treated seeds were observed in the crops of several birds at the time of necropsy. Although accumulated residues were low, evidence is mounting that non-target avian species, such as partridges, pigeons, and quail (Colinus virginianus, Coturnix japonica), are exposed through the consumption of these coated seeds (Mineau and Palmer 2013; Millot et al. 2017). Recently, concentrations up to 0.067 mg/kg of thiamethoxam/clothianidin were reported in failed eggs of gray partridge known to frequent pesticide-treated cereal fields in north-central France (Bro et al. 2016). Very little published information is available on fuberidazole in non-target species; however, it was suspected to have played a role in the morbidity observed in pheasants feeding on treated wheat within a game farm in the UK (Laing 2001).
Most experimental pesticide toxicity studies are limited to observations of acute toxicity in laboratory rats, even though birds are often more susceptible than rats to pesticide toxicity. These laboratory assessments often target single compounds, when in reality, non-target wildlife species are exposed to complex mixtures of pesticides/contaminants with synergistic and/or inhibitory effects. Such laboratory studies also neglect to consider species-specific sensitivities to single compounds, or complex mixtures that could ultimately impair whole populations. For example, clothianidin, which was detected in 20% of wild turkeys in the present study, is considered far less toxic to rats (LD50 > 5000 mg/kg) compared to Japanese quail (423 mg/kg) and northern bobwhite quail (> 2000 mg/kg). The LD50 of imidacloprid in rats ranges from 379 to 648 mg/kg (or ppm), but this dose is much lower for birds: 14 mg/kg for gray partridge, 31 mg/kg for Japanese quail, and 152 mg/kg for northern bobwhite quail (SERA 2005; Anon 2012; Rose 2012; Mineau and Palmer 2013). Currently available toxicity data often disregard the chronic effects of exposure, which may occur at lower concentrations and over longer periods of time in free-ranging wildlife or other animals. For example, a dose equivalent to 0.10% of a neonicotinoid-coated corn seed ingested daily during the egg-laying season can adversely affect reproduction in birds (Mineau and Palmer 2013).
Although not detected in the present study, imidacloprid is considered the most toxic NNI in birds (EPA 2016), although toxicity varies across species. For example, a study involving pigeons and partridges found dead in a barn following exposure to coated seeds showed hepatic toxicity levels of imidacloprid ranging from 1.0–1.6 μg/g (ppm) in partridges and up to 3.1 μg/g in pigeons (Berney et al. 1999). Recent experimental research on the migratory white-crowned sparrow (Zonotrichia leucophrys) in Saskatchewan, Canada, showed that delays in and impaired orientation during migration, loss of body mass, decreased reproduction efforts, and potentially increased mortality are possible outcomes after consuming approximately 4 imidacloprid-treated canola seeds, or just 0.2 treated corn seeds (i.e., dosage of 4.1 μg imidacloprid/g bw/day, equivalent to 10% of the LD50 of house sparrows; Eng et al. 2017).
Additional research is required to determine the chronic health and reproductive effects on wild turkeys and other wildlife that may occur with repeated exposure and ingestion of NNI-coated seeds. For example, knowledge gaps exist on the timing and duration of exposure, the rate at which these chemicals are metabolized in birds, and what proportion of the ingested material reaches the liver. Such information will require both field studies to understand wildlife feeding habits and behavior and experimental studies to delineate toxic levels and associated clinical effects. It should be noted that studies such as ours also carry inherent sampling biases. First, we relied on sampling of hunter-harvested wild turkeys, which tend to be skewed toward larger, healthy-appearing male birds. Also, wild turkeys that may be suffering from morbidity or mortality associated with NNI ingestion are less likely to be recovered and tested, as they may hide in vegetation prior to death or be killed and consumed by predators.
Little is known about NNI persistence and impacts on non-target avian species in agricultural landscapes. As of July 1, 2015, new regulatory requirements came into effect for the sale and use of NNI-treated seeds in Ontario. These requirements support reducing the use of imidacloprid, thiamethoxam, and clothianidin on specific crops (corn and soybean) planted with NNI-treated seeds by 80% by 2017; however, only an estimated 25% reduction has been reported based on 2014 baseline data (MOECC 2015). Knowledge of chronic and acute bird exposure, particularly in farmland birds, should be a first step in understanding the effects of NNIs on the health of birds and other wildlife. These data are important to serve as baseline data for southern Ontario wild turkeys and to provide context for reference values in future analyses.