The use of neonicotinoid insecticides in agriculture is now recognized for the health risks it poses to non-target wildlife, with associated honey bee mortality especially concerning. Research directed toward the presence and effects of these pesticides on terrestrial vertebrates that consume neonicotinoid-coated seeds, such as wild turkeys (Meleagris gallopavo silvestris), is lacking. This study used liquid chromatography attached to a tandem mass spectrometer to assess the liver from 40 wild turkeys for neonicotinoid and other pesticide residues and compared detected levels of these contaminants across the southern Ontario, Canada. Nine (22.5%) wild turkeys had detectible levels of neonicotinoid residues—clothianidin in eight, and thiamethoxam in three. Two (5.0%) of these turkeys had detectable levels of both clothianidin and thiamethoxam. Fuberidazole was detected in two (5.0%) wild turkeys. The highest level of thiamethoxam detected was 0.16 ppm, while clothianidin was detected at 0.12 ppm, and fuberidazole at 0.0094 ppm. Knowledge of exposure in free-ranging wildlife is critical for better understanding the effects of neonicotinoids on wildlife health; thus, these data help establish baseline data for southern Ontario wild turkeys and provide context for reference values in future analyses. . . . . . . . Keywords Bioaccumulation Birds Insecticides Neonicotinoids Non-targetspecies Pesticides Treated seeds Wild Turkey Introduction used on many large-acreage crops in southern Ontario (e.g., corn, soy, grains, dry beans, and canola), 60% are utilized as Neonicotinoid insecticides (NNIs) have become the most seed coatings (Jeschke et al. 2011;OMNRF 2017). NNIs are widely used insecticides in the world (Schaafsma et al. systemic insecticides, taken up by the plant following appli- 2015). Commonly used in agriculture, they are applied as cation and distributed systemically through plant tissues as it various formulations including as foliage sprays, seed coating, grows. They act by affecting the central nervous system of and soil treatments. Of NNIs used globally, including those insects, causing over-excitation of nerve synapses, followed by paralysis and eventually death (Fishel 2013). Recently, these insecticides have been recognized for the risks they pose Responsible editor: Philippe Garrigues to non-target wildlife, including as a potential factor driving colony collapse disorder in honey bees (Farooqui 2013). However, little attention has been paid to higher trophic biota, * Amanda M. MacDonald email@example.com including terrestrial vertebrates. Wild turkeys (Meleagris gallopavo), and other avian spe- cies such as gray partridges (Perdix perdix) and pigeons Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON NIG 2W1, Canada (Columba palumbus, C. livia, and C. oenas), readily ingest treated corn or soya seeds (Mineau and Palmer 2013;Millot Canadian Wildlife Health Cooperative, Ontario Veterinary College, University of Guelph, Guelph, ON NIG 2W1, Canada et al. 2017); in fact, depending on food availability, these resources comprise a significant portion of the wild turkey’s Environment and Climate Change Canada, Science and Technology Branch, National Wildlife Research Center, Ottawa, ON K1A 0H3, diet (OMNRF 2007). These seeds can contain some of the Canada highest concentrations of NNIs (Gibbons et al. 2015), making Present address: Southeastern Cooperative Wildlife Disease Study, them of particular concern because of their availability to birds University of Georgia, Athens, GA 30602, USA and the potential for repeat or ongoing exposure. A single corn Environ Sci Pollut Res (2018) 25:16254–16260 16255 16256 Environ Sci Pollut Res (2018) 25:16254–16260 Fig. 1 Map depicting the locations and pesticide compounds detected supernatant was cleaned with methanol and 0.1 M ammonium among 40 hunter-harvested wild turkeys collected during the 2015 spring acetate. Sample extracts were analyzed using LC-MS/MS op- hunt (April–May) in Ontario, Canada erated in electrospray ionization mode. kernel is typically treated with approximately 1 mg of active ingredient (Rexrode et al. 2003) and consumption of just one Results imidacloprid-treated corn seed, or a few clothianidin- or thiamethoxam-treated seeds, could be lethally toxic to a bird Of 40 wild turkey livers tested, all were male (due to hunter- the size of a blue jay (Mineau and Palmer 2013). The persis- harvest regulations), 3 were juveniles, and 37 were adults. tence of NNIs in the environment as well as their potential ill- NNI compounds were detected by LC-MS/MS in liver sam- ples from 17 wild turkeys (i.e., 43% of samples analyzed) at effects on non-target species remains unclear. Recently, there has been a great deal of public and political controversy and levels approaching the lower detection limit. In 6 of these samples, levels were higher than the lower detection limit media coverage regarding the use and associated risks of NNIs to honey bee health and mortality. There has also been grow- but still below quantification limits (BAppendix^ Table 2). Nine of 40 (22.5%) adult wild turkeys had detectible levels ing concern among natural resource managers, conservation- ists, and hunters about whether NNI use may be linked to poor of NNI residues, clothianidin in eight, and thiamethoxam in reproductive output of wild turkeys and potential bioaccumu- three. Two (5.0%) of these turkeys had detectable levels of lation of NNIs in wild turkey meat intended for human both clothianidin and thiamethoxam. Fuberidazole (a fungi- consumption. cide used as a seed treatment for cereals) was detected in two The present study was conducted to address knowledge (5.0%) wild turkeys. The highest levels detected for each com- gaps and the concerns described above. Samples originated pound were 0.16 ppm of thiamethoxam, 0.12 ppm of clothianidin, and fuberidazole at 0.0094 ppm (Table 1). from healthy-appearing, hunter-harvested wild turkeys from across southern Ontario. The objectives were to (1) assess wild turkey liver tissues for NNIs and other potential environ- mental contaminants and (2) compare levels of detected con- Discussion taminants across the geographic area of the study site. 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 in- Materials and methods cludes acetamiprid, clothianidin, dinotefuran, imidacloprid, nitenpyram, nithiazine, thiacloprid, and thiamethoxam. During the 2015 Ontario spring hunting season (April–May), Imidacloprid, clothianidin, and thiamethoxam are the most 147 hunter-harvested wild turkey carcasses were collected common NNIs applied for agricultural use in Ontario (Wildlife Scientific Collector’s Authorization from the (Somers and Chung 2014). Wild turkeys in Ontario and other Ontario Ministry of Natural Resources and Forestry, regions live within concentrated areas used for agriculture and #1079555) from across southern Ontario. Carcasses were often rely on croplands for supplemental feeding to survive, stored at − 20 °C and thawed at 4 °C prior to sample collec- particularly in winter months (Porter et al. 1980; Vander tion. Liver samples from each turkey were collected and Haegen et al. 1989). Thus far, NNIs have been best known stored at − 80 °C until testing. Forty samples were selected for the adverse effects they cause in honey bees. Mass die- to represent regions across the collection range (Fig. 1)and offs, and subsequent declines in bee population numbers, have were sent for pesticide residue analysis at Laboratory garnered widespread attention and concern in recent years Services, Agriculture and Food Laboratory, University of because of the importance of bees in providing a vital ecosys- Guelph, Guelph, Ontario. The testing proceeded using liquid tem service, namely, pollination (Whitehorn et al. 2012; chromatography attached to a tandem mass spectrometer (LC- Godfray et al. 2015; Rundlöf et al. 2015). MS/MS). The TOPS-142 screening procedure included the Pesticides, including the NNIs clothianidin and analysis and quantification of 142 different pesticide com- thiamethoxam, were detected in the liver of nearly half of wild pounds, including seven neonicotinoids (Wang and Leung turkeys tested. These turkeys were likely exposed to NNIs by 2009). consuming pesticide-coated seeds during crop sowing that Extraction of pesticides from wet turkey livers was per- spring, as treated seeds were observed in the crops of several formed using the QuEChERS method (Anastassiades et al. birds at the time of necropsy. Although accumulated residues 2003). Briefly, each sample was extracted using 1% acetic were low, evidence is mounting that non-target avian species, acid in acetonitrile and liquid phases were partitioned using such as partridges, pigeons, and quail (Colinus virginianus, sodium acetate and anhydrous magnesium sulfate. The Coturnix japonica), are exposed through the consumption of Environ Sci Pollut Res (2018) 25:16254–16260 16257 Table 1 Summary of detectible Pesticide Main use No. of turkeys (%) MDL (ppm) Range (ppm) levels of pesticide residues in livers of hunter-harvested wild turkeys Clothianidin Insecticide 8 (20.0) 0.001 0.0086–0.1200 (n = 40) in April–May 2015, from Ontario, Canada Thiamethoxam Insecticide 3 (7.5) 0.001 0.0110–0.1600 Fuberidazol Fungicide 2 (5.0) 0.0005 0.0077–0.0094 MDL minimum detection limit these coated seeds (Mineau and Palmer 2013; Millot et al. consuming approximately 4 imidacloprid-treated canola 2017). Recently, concentrations up to 0.067 mg/kg of seeds, or just 0.2 treated corn seeds (i.e., dosage of 4.1 μg thiamethoxam/clothianidin were reported in failed eggs of imidacloprid/g bw/day, equivalent to 10% of the LD of gray partridge known to frequent pesticide-treated cereal house sparrows; Eng et al. 2017). fields in north-central France (Bro et al. 2016). Very little Additional research is required to determine the chronic published information is available on fuberidazole in non- health and reproductive effects on wild turkeys and other target species; however, it was suspected to have played a role wildlife that may occur with repeated exposure and ingestion in the morbidity observed in pheasants feeding on treated of NNI-coated seeds. For example, knowledge gaps exist on wheat within a game farm in the UK (Laing 2001). the timing and duration of exposure, the rate at which these Most experimental pesticide toxicity studies are limited to chemicals are metabolized in birds, and what proportion of the observations of acute toxicity in laboratory rats, even though ingested material reaches the liver. Such information will re- birds are often more susceptible than rats to pesticide toxicity. quire both field studies to understand wildlife feeding habits These laboratory assessments often target single compounds, and behavior and experimental studies to delineate toxic levels when in reality, non-target wildlife species are exposed to com- and associated clinical effects. It should be noted that studies plex mixtures of pesticides/contaminants with synergistic and/ such as ours also carry inherent sampling biases. First, we or inhibitory effects. Such laboratory studies also neglect to relied on sampling of hunter-harvested wild turkeys, which consider species-specific sensitivities to single compounds, or tend to be skewed toward larger, healthy-appearing male complex mixtures that could ultimately impair whole popula- birds. Also, wild turkeys that may be suffering from morbidity tions. For example, clothianidin, which was detected in 20% of or mortality associated with NNI ingestion are less likely to be wild turkeys in the present study, is considered far less toxic to recovered and tested, as they may hide in vegetation prior to rats (LD > 5000 mg/kg) compared to Japanese quail (423 mg/ death or be killed and consumed by predators. kg) and northern bobwhite quail (> 2000 mg/kg). The LD of Little is known about NNI persistence and impacts on non- imidacloprid in rats ranges from 379 to 648 mg/kg (or ppm), target avian species in agricultural landscapes. As of July 1, but this dose is much lower for birds: 14 mg/kg for gray par- 2015, new regulatory requirements came into effect for the tridge, 31 mg/kg for Japanese quail, and 152 mg/kg for north- sale and use of NNI-treated seeds in Ontario. These require- ern bobwhite quail (SERA 2005; Anon 2012; Rose 2012; ments support reducing the use of imidacloprid, Mineau and Palmer 2013). Currently available toxicity data thiamethoxam, and clothianidin on specific crops (corn and often disregard the chronic effects of exposure, which may soybean) planted with NNI-treated seeds by 80% by 2017; occur at lower concentrations and over longer periods of time however, only an estimated 25% reduction has been reported in free-ranging wildlife or other animals. For example, a dose based on 2014 baseline data (MOECC 2015). Knowledge of equivalent to 0.10% of a neonicotinoid-coated corn seed chronic and acute bird exposure, particularly in farmland ingested daily during the egg-laying season can adversely af- birds, should be a first step in understanding the effects of fect reproduction in birds (Mineau and Palmer 2013). NNIs on the health of birds and other wildlife. These data Although not detected in the present study, imidacloprid is are important to serve as baseline data for southern Ontario considered the most toxic NNI in birds (EPA 2016), although wild turkeys and to provide context for reference values in toxicity varies across species. For example, a study involving future analyses. pigeons and partridges found dead in a barn following expo- Acknowledgements We would like to thank Pud Hunter for valuable sure to coated seeds showed hepatic toxicity levels of advice and logistical support, in addition to Dave Snook, Aylmer imidacloprid ranging from 1.0–1.6 μg/g (ppm) in partridges District Stakeholders Committee, Kathy Moore, Brian Moore, Tony and up to 3.1 μg/g in pigeons (Berney et al. 1999). Recent Jackson, Felix Barbetti and the hunters for providing samples. experimental research on the migratory white-crowned spar- row (Zonotrichia leucophrys) in Saskatchewan, Canada, Funding information This research was funded by the Ontario Ministry of Agriculture, Food, and Rural Affairs–University of Guelph Partnership showed that delays in and impaired orientation during migra- (No. 2013-1530) and was further supported by the Ontario Federation of tion, loss of body mass, decreased reproduction efforts, and Anglers and Hunters, Zone J, and its members. potentially increased mortality are possible outcomes after 16258 Environ Sci Pollut Res (2018) 25:16254–16260 Appendix Table 2 Pesticide residue testing results from livers of 40 hunter-harvested wild turkeys in April–May 2015, from Ontario, Canada Neonicotinoid (ppm) Other (ppm) Sample Acetamiprid Clothianidin Dinotefuran Imidacloprid Nitenpyram Thiabendazole Thiacloprid Thiamethoxam Fuberidazol Mandipropamid MDL (ppm) 0.001 0.001 0.002 0.001 0.001 0.0005 0.001 0.001 0.0005 0.0005 1 N.D. N.D. N.D. N.D. N.D. < MDL N.D. N.D. N.D. N.D. 2 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 3 N.D. N.D. N.D. N.D. N.D. < MDL N.D. N.D. N.D. N.D. 4 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 5 N.D. 0.11 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 6 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. < MDL N.D. 7 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 8 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 9 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 10 N.D. 0.0091 N.D. N.D. N.D. N.D. N.D. < MDL N.D. N.D. 11 N.D. < MDL N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 12 N.D. < MDL N.D. N.D. N.D. N.D. N.D. 0.011 < MQL N.D. 13 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 14 N.D. < MDL N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 15 N.D. 0.069 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 16 N.D. < MDL N.D. N.D. N.D. < MDL N.D. N.D. N.D. N.D. 17 N.D. < MQL N.D. N.D. N.D. N.D. N.D. < MQL N.D. N.D. 18 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. < MDL 19 N.D. < MDL N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 20 N.D. < MQL N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 21 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 22 N.D. < MDL N.D. N.D. N.D. N.D. N.D. N.D. < MDL N.D. 23 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 24 N.D. 0.0089 N.D. N.D. N.D. < MDL N.D. < MQL N.D. N.D. 25 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 26 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 27 N.D. 0.026 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 28 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 29 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 30 N.D. 0.023 N.D. N.D. N.D. N.D. N.D. 0.16 N.D. < MDL 31 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. Environ Sci Pollut Res (2018) 25:16254–16260 16259 Table 2 (continued) Neonicotinoid (ppm) Other (ppm) Sample Acetamiprid Clothianidin Dinotefuran Imidacloprid Nitenpyram Thiabendazole Thiacloprid Thiamethoxam Fuberidazol Mandipropamid MDL (ppm) 0.001 0.001 0.002 0.001 0.001 0.0005 0.001 0.001 0.0005 0.0005 32 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 33 N.D. 0.0086 N.D. N.D. N.D. N.D. N.D. 0.016 N.D. N.D. 34 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 35 N.D. < MDL N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 36 N.D. 0.12 N.D. N.D. N.D. < MDL N.D. N.D. N.D. N.D. 37 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 0.0094 N.D. 38 N.D. N.D. N.D. N.D. N.D. < MQL N.D. N.D. 0.0077 N.D. 39 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 40 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. not detected, <MDL less than minimum detection limits, <MQL less than minimum quantification limits 16260 Environ Sci Pollut Res (2018) 25:16254–16260 Open Access This article is distributed under the terms of the Creative Millot F, Decors A, Mastain O, Quintaine T, Berny P, Vey D, Lasseur R, Commons Attribution 4.0 International License (http:// Bro E (2017) Field evidence of bird poisonings by imidacloprid- creativecommons.org/licenses/by/4.0/), which permits unrestricted use, treated seeds: a review of incidents reported by the French SAGIR distribution, and reproduction in any medium, provided you give network from 1995 to 2014. Environ Sci Pollut Res 24:5469–5485 appropriate credit to the original author(s) and the source, provide a link Mineau P, Palmer C (2013) The impact of the Nation's most widely used to the Creative Commons license, and indicate if changes were made. insecticides on birds: neonicotinoid insecticides and birds. 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