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Short Communication
A SURVEY OF NEONICOTINOID USE AND POTENTIAL EXPOSURE TO NORTHERN
BOBWHITE (COLINUS VIRGINIANUS) AND SCALED QUAIL (CALLIPEPLA SQUAMATA)
IN THE ROLLING PLAINS OF TEXAS AND OKLAHOMA
UDAY TURAGA,ySTEVEN T. PEPER,yNICHOLAS R. DUNHAM,yNAVEEN KUMAR,yWHITNEY KISTLER,ySADIA ALMAS,z
STEVEN M. PRESLEY,zand RONALD J. KENDALL*y
yThe Wildlife Toxicology Laboratory, The Institute of Environmental and Human Health, Texas Tech University, Lubbock, Texas, USA
zZoonoses and Wildlife Diseases Laboratory, The Institute of Environmental and Human Health, Texas Tech University, Lubbock, Texas, USA
(Submitted 24 August 2015; Returned for Revision 19 September 2015; Accepted 30 October 2015)
Abstract: Northern bobwhite (quail) (Colinus virginianus) and scaled quail (Callipepla squamata) populations have declined
dramatically in the Rolling Plains ecoregion of Texas and Oklahoma (USA). There is rising concern about potential toxicity of
neonicotinoids to birds. To investigate this concern, the authors examined crops of 81 northern bobwhite and 17 scaled quail to determine
the presence or absence of seeds treated with 3 neonicotinoids (clothianidin, imidacloprid, and thiamethoxam). No treated seeds were
found in the 98 crops examined. Liver samples from all 98 quail were collected and analyzed for neonicotinoid residues. Analysis
revealed very low concentrations of neonicotinoids within the quail liver samples. The results suggest there is little to no risk of direct
toxicity to quail from neonicotinoids. Environ Toxicol Chem 2016;35:1511–1515. #2015 SETAC
Keywords: Insecticides Neonicotinoids Northern bobwhite Rolling Plains Scaled quail Texas Treated seeds
INTRODUCTION
The Rolling Plains ecoregion of Texas and Oklahoma (USA)
has experienced dramatic population declines of northern
bobwhite (quail) (Colinus virginianus) and scaled quail/blue
quail (Callipepla squamata), particularly since 2010 [1]; the
cause of these declines remains unclear. Possible explanations
for the decline in quail populations across the United States are
parasitic eyeworms [2], semiarid environments linked to
survival and reproductive success of bobwhites [3], lack of
suitable habitat [4], and habitat fragmentation [5]. More
recently, there has been rising concern for the potential toxicity
of neonicotinoids in birds [6].
Developed in the 1980s and first made available in the early
1990s [7], neonicotinoids are among the most popular and
widespread insecticides used today [7,8]. Owing to their plant
systemicity, neonicotinoids applied to seeds translocate to
various plant tissues. This plays a key role in protecting the
plants from root-eating and other sucking insects responsible for
transmission of various plant viruses [8,9]. Neonicotinoids are a
class of polar insecticides that mimic nicotine [10], a naturally
occurring insecticide [11]; they act as agonists by blocking the
nicotinic acetylcholine receptor, ultimately causing death via
neurotoxicity [8,10]. Neonicotinoids are among the most
effective insecticides available today [8], with a low acute
toxicity to vertebrates and invertebrates and a high toxicity to
insects [10].
The use of neonicotinoids is currently a controversial topic, as
the side effects of these insecticides are negatively affecting
nontarget species such as bees [10] and some vertebrates [12,13].
Pesticides and insecticides have often been associated with
declines in bird populations as a result of their direct and indirect
effects [14]. Direct effects include toxicity of pesticides to birds,
and indirect effects include potential interference in the food chain
of birds [14]. Research in The Netherlands has shown a similar
trend, whereby increasing concentrations of neonicotinoids in
the environment were associated with decreased insectivorous
passerine populations [15].
Laboratory studies with insecticides have shown behav-
ioral disturbances in bobwhite quail [16], and recent research
has documented the effects of neonicotinoids on
quail [17,18]. Studies have determined that exposure to
clothianidin (1-[2-chloro-1,3-thiazol-5-ylmethyl]-3-methyl-
2-nitroguanidine) affects reproductive function in quail and
may inhibit/delay embryo development [17]. Exposure to
imidacloprid (N-[1-{(6-chloro-3-pyridyl) methyl}-4,5-dihy-
droimidazol-2-yl] nitramide) has resulted in histopatholog-
ical changes in liver and testes of quail [18]. Furthermore,
studies with insects and plants have demonstrated that
exposure to thiomethoxam (3-[{2-chloro-1,3-thiazol-5-yl}
methyl]-5-methyl-N-nitro-1,3,5-oxadiazinan-4-imine) may
likely act as a precursor to a more potent neonicotinoid,
clothianidin [19]. Neonicotinoids may also interfere with the
food chain of wild birds, such as quail, by decreasing the
availability of their prey [20]. The growing concern about
neonicotinoid toxicity in the environment has led some
countries in the European Union and Asia to tighten
restrictions on the use of these compounds [10,17].
Treating seeds such as cotton, corn, cereals, sugar beets,
oilseed rape, and others with neonicotinoid insecticides has
become a common practice [8] not only in the Rolling Plains
ecoregion but also throughout the agriculture industry. Because
birds such as the northern bobwhite and scaled quail tend to feed
near agricultural fields, they have the potential to ingest seeds
that are treated with insecticides [21]. Of particular concern is
the widespread wheat planting that occurs in August and
September. The relative toxicity of specific neonicotinoids is
moderate to low (Table 1). However, if high quantities of treated
* Address correspondence to ron.kendall@ttu.edu
Published online 13 November 2015 in Wiley Online Library
(wileyonlinelibrary.com).
DOI: 10.1002/etc.3305
Environmental Toxicology and Chemistry, Vol. 35, No. 6, pp. 1511–1515, 2016
#2015 SETAC
Printed in the USA
1511
seeds are consumed, this may constitute a risk [22] depending
on the acute toxic potential of pesticides used for seed
treatments [23]. Goulson [22] has observed that, in some
instances, the amount of seeds consumed in a single visit
exceeds lethal doses [22]. In addition, neonicotinoids cause
sublethal effects in birds, including reduced appetite, eggshell
thinning, and diarrhea [22,24]. In the present study, we looked at
the availability and possible exposure of northern bobwhite and
scaled quail to 3 neonicotinoids (clothianidin, imidacloprid, and
thiomethoxam) throughout the Rolling Plains ecoregion
(Figure 1). Clothianidin and imidacloprid have been associated
with toxic effects in quail [17,18]. Thiamethoxam is a
pro-insecticide, and in vivo metabolism of thiamethoxam to
clothianidin has been documented in the literature [19].
Considering the many direct and indirect effects of these
compounds on quail [14], it is important to monitor the exposure
of quail to neonicotinoids. The objective of the present
study was to evaluate qualitative and quantitative exposure of
quail to neonicotinoids. We evaluated qualitative exposure by
looking for the presence of neonicotinoid-coated seeds in quail
crops, and we used liquid chromatography–mass spectrometry
(LC/MS) to quantify tissue concentrations of neonicotinoids in
quail. In addition, we attempted to understand the extent of use
of neonicotinoids in the Rolling Plains ecoregion. The present
study increases our understanding of how the use of
neonicotinoids is affecting quail populations in the Rolling
Plains ecoregion of Texas and Oklahoma.
MATERIALS AND METHODS
Sampling sites and sample collection
Northern bobwhites and scaled quail were trapped as part of
a multiphase broad-scale project focused on identifying the
leading cause(s) of the quail population decline in the Rolling
Plains. Crops from 81 bobwhites and 17 scaled quail trapped
during the months of August 2013 through October 2013 were
necropsied and examined. The birds were collected from more
than 30 counties in the Rolling Plains ecoregion. All bobwhite
and scaled quail were trapped and handled under Texas Parks
and Wildlife Permit SRP-1098-984, Texas A&M University
Animal Use Protocol 2011-193, and Texas Tech University
Animal Care and Usage Committee protocols 11049-07 and
13027-03. Euthanasia was performed by CO
2
asphyxiation
followed by cervical dislocation per Texas Tech University
Institutional Animal Care and Use Committee approval. All
necropsies were carried out at Texas Tech University Institute of
Environmental and Human Health.
The highest potential for quail in the Rolling Plains
ecoregion to consume treated seeds is during the agricultural
planting of wheat, which occurs during the months of August
and September. Despite the small sample size, these birds were
collected at a critical time (August–October) and in more than
30 counties in the Rolling Plains ecoregion to identify evidence
of consumption of treated seeds. Also, a brief questionnaire
survey was performed to identify the extent of use of
neonicotinoids in the Rolling Plains ecoregion.
We dissected 98 birds and removed the crops, which we then
examined for the presence of neonicotinoid-treated seeds.
Treated seeds are easily identified through the purple, pink, or
greenish dye that is mixed with the chemical prior to application
to seeds. We then completely removed the contents of each crop
from the 98 birds and placed them in a Petri dish to determine the
presence of any treated seeds, cracked or whole.
Extraction and analysis of neonicotinoids in livers of quail
We collected liver samples from all 98 birds for analysis of
neonicotinoid residues. We extracted liver tissues using a
dispersive solid phase extraction (dSPE) technique, more
commonly referred to as the QuEChERS (Quick, Easy, Cheap,
Effective, Rugged, and Safe) method [25]. Briefly, 10 mL
of acetonit rile an d internal standard (100 mLof1mg/mL
tris[1-chloro-2-propyl] phosphate [TCPP], mixture of isomers)
were added to finely chopped liver samples in a 50-mL centrifuge
tube. After vortexing for 1 min, a citrate/sodium bicarbonate
mixture (55237-U Supel
TM
QuE; Sigma-Aldrich) was added to
the centrifuge tube followed by centrifugation at 1200 gfor 5 min.
The extract was refrigerated (4 8C) for 1 h to separate the lipid
components. We then performed a clean-up by adding the
contents of a primary secondary amine tube (55228-U Supel
TM
QuE; Sigma-Aldrich)to the extract. We thenvortexed the mixture
for 1 min, followed by centrifugation for 5 min at 1200 g.We
collectedthe supernatant and usedit for analysis of neonicotinoids
without any sample concentration. We added 20 mLof5%formic
acid to the extracts and then filtered the extracts through a
0.45-mmnylonfilter before loading on to the autosampler.
For quantification of neonicotinoids in quail livers, LC/MS
was performed using an Accela
TM
LC system (Thermo Scientific)
equipped with an autosampler and a degasser. Chromatographic
separation of neonicotinoids was attained on an Ascentis
1
C18
column (3-mm particle size, 15 cm length 2.1 mm inner
diameter) at 25 8C. We used an injection volume and a flow
rate of 5 mL and 100 mL/min, respectively. We employed a
Table 1. Common neonicotinoids and their LD50 values for northern
bobwhite (Colinus virginianus)
Active ingredient Measurement
Amount
(mg/kg body wt) Reference
Acetamiprid LD50 180 [34]
Clothianidin LD50 >2000 [13]
Thiacloprid LD50 2716 [35]
Thiamethoxam LD50 1552 [36]
Imidacloprid LD50 152 [13]
LD50 ¼median lethal dose.
Figure 1. Counties surveyed in the Rolling Plains ecoregion of Texas and
Oklahoma (USA) for neonicotinoid availability and usage.
1512 Environ Toxicol Chem 35, 2016 U. Turaga et al.
mixture of water and acetonitrile, both acidified with 0.1% v/v
formic acid, as the mobile phase with the following gradient
elution profile: 0 min to 3 min,100% to 30% water;3 min to 6 min,
30% to 15% water; 6 min to 12 min, 15% to 50% water; 12min to
14 min, return to 100% water; and 14 min to 15 min, equilibration
of the LC system.
The detection system consisted of a triple quadrupole mass
spectrophotometer (TSQ Quantum
TM
Access MAX; Thermo
Scientific) equipped with an electrospray ionization (ESI)
interface. We operated the device in an ESI (positive ion) mode
using a vaporizer temperature of 290 8C and capillary
temperature of 370 8C. We achieved collision-induced dissoci-
ation by using nitrogen as the collision gas. Mass spectrometric
detection was performed in a dynamic multiple reaction
monitoring mode, and the optimized MS/MS parameters are
summarized in Table 2.
RESULTS AND DISCUSSION
We found no treated seeds, cracked or whole, in the 98 crops.
For a variety of reasons, however, this qualitative observation
cannot be used to determine whether quail in the Rolling Plains
ecoregion are consuming neonicotinoid-treated seeds. Studies
have suggested that birds avoid ingesting lethal doses by ceasing
to feed, a phenomenon known as avoidance [26]. In addition,
birds often tend to regurgitate toxic food products [27].
Regurgitation of treated seeds prevents the internal concen-
trations of pesticide from reaching a lethal dose. This may
eventually aid in mitigating the effects of acute pesticide
poisoning [26]. Furthermore, laboratory studies with imidaclo-
prid-treated seeds have suggested that the seeds have a repellent
effect on birds and other small mammals. If neonicotinoids,
being the active ingredient in treated seeds, result in sublethal
effects on quail because of their acute toxicity, there is every
possibility that quail tend to avoid feeding on them [28].
Another phenomenon that prevents birds from ingesting
pesticide-coated seeds is dehusking [21]. The process of
dehusking makes it easier for the bird to sense the surface
seed treatment, thereby assisting in the phenomenon of
avoidance of those seeds [23]. More importantly, the studies
of Edwards et al. have suggested that birds that dehusk seeds are
at a lower risk of pesticide-induced toxic effects, because 80%
to 95% of spray residue is present on the husk [29]. However,
dehusking is often associated with the size of birds, and birds
weighing more than 50 g have not been observed to dehusk
seeds [29]. To the best of our knowledge, there is no reported
evidence that quail dehusk seeds. Nevertheless, an understand-
ing of the extent of the use of treated seeds is crucial to evaluate
exposure of quail to these seeds [8].
A comprehensive survey of the use of neonicotinoids in the
Rolling Plains ecoregion is beyond the scope of the present
study. Nevertheless, a brief questionnaire survey of stores
within 12 counties (Figure 1) of the Rolling Plains ecoregion
indicated that 10 of the 13 stores sold neonicotinoid-treated
seeds. Six of the stores sold a form of neonicotinoids other than
treated seeds, such as neonicotinoid sprays, albeit in small
Table 2. Optimized mass spectrometry conditions for analysis of neonicotinoids
Compound Precursor ions (m/z) Product ion (m/z) Collision energy (eV) Tube lens offset (V)
Thiamethoxam 291.99 211.07 15 60
132.04 25 60
Imidacloprid 255.950 208.98 20 75
175.24 23 75
Clothianidin 249.99 168.97 15 60
132.00 20 60
TCPP 326.96 99.00 25 50
CPP ¼tris(1-chloro-2-propyl) phosphate.
Table 3. Concentrations (ng/g wet wt) of select neonicotinoids in liver samples of quail sampled throughout the Rolling Plains (USA) ecoregion from August
through October 2013
a
Sample ID Species Clothianidin (ng/g) Imidacloprid (ng/g) Thiamethoxam (ng/g)
130251 BOB BQL 12.89 BQL
130275 BOB BQL 3.65 4.75
130287 BOB 40.93 BQL BQL
130307 BOB BQL 14.80 BQL
130329 BOB BQL 13.33 BQL
130347 BOB BQL 62.29 BQL
130371 BOB BQL 59.05 BQL
130503 BOB BQL BQL 24.78
130515 BOB BQL 10.37 BQL
130755 BOB BQL 14.73 BQL
130794 BOB 5.76 3.72 BQL
131320 BOB BQL 24.85 BQL
131416 BLUE BQL 4.17 BQL
131461 BOB BQL 7.85 BQL
131496 BOB BQL BQL 16.13
131541 BOB BQL 8.47 BQL
131986 BOB BQL 7.37 BQL
a
Quantitation limits for clothianidin, imidacloprid, and thiamethoxam are 3.61 ng/g, 3.49 ng/g, and 3.42 ng/g, respectively. Recovery (n¼5): 100.2% to 106.2%
for clothianidin, 90% to 98.2% for imidacloprid, and 104.3% to 113.8% for thiamethoxam.
BOB ¼northern bobwhite quail; BLUE ¼scaled quail; BQL ¼below quantitation limit.
Neonicotinoid use and potential exposure Environ Toxicol Chem 35, 2016 1513
quantities. It was also inferred that 2 brands of neonicotinoid
products, Poncho
1
(clothianidin-based, active ingredient
40.3%) and Gaucho
1
(imidacloprid-based, active ingredient
40.7–75%) are predominantly used throughout the Rolling
Plains ecoregion. Despite the absence of treated seeds in the
crops of quail, it can be inferred based on the questionnaire
surveys that there is a potential for quail in the Rolling Plains
ecoregion to become exposed to neonicotinoids. Liver samples
of quail were analyzed to quantitate exposure of quail to
neonicotinoids.
Analysis of liver samples
Quantitation of crop and gizzard concentrations of neon-
icotinoids may not provide a reliable estimate of exposure [27],
possibly because of dehusking [21], avoidance [26], regurgita-
tion [27], repellent effect [28], modes of neonicotinoid
application other than seed treatment [30], and additional
reasons. More importantly, the ecotoxicological profile of
imidacloprid suggested that liver and kidney concentrations
provide the most reliable estimates of exposure [28]. Analyses
of liver samples has revealed very low concentrations of
clothianidin, imidacloprid, and thiamethoxam in the Rolling
Plains ecoregion (Table 3). We detected neonicotinoids above
the quantitation limits in 17% (17/98) of the samples analyzed.
We found quantitation limits for clothianidin, imidacloprid,
and thiamethoxam of 3.61 ng/g, 3.49 ng/g, and 3.42 ng/g,
respectively. In addition to the limited use of neonicotinoid-
treated seeds in the selected ecoregion, the poor lipophilic
nature of neonicotinoids explains the low concentrations of
these insecticides in liver samples. Log P values of imidaclo-
prid, thiametoxam, and clothianidin were found to be 0.57,
–0.13, and 0.7, respectively [31,32]. The low bioaccumulation
potential of neonicotinoids (owing to poor lipophilicity),
coupled with their broad-spectrum insecticidal activity, has
played a key role in facilitating widespread use of these
compounds in agriculture [33]. It can be inferred that quail
in the Rolling Plains ecoregion are exposed to and are
accumulating neonicotinoids, albeit at low levels.
CONCLUSIONS
The present study suggests there is no imminent danger to
quail as a result of seeds treated with neonicotinoids in the
Rolling Plains ecoregion. The limited use of neonicotinoid-
treated seeds in the Rolling Plains ecoregion and the low
concentrations of neonicotinoids found in livers of quail
suggest that neonicotinoids are not directly involved in the
decline of quail populations in this ecoregion. However,
further research is needed to fully determine both sublethal
and chronic effects of neonicotinoid exposure. In addition,
the potential for indirect effects of neonicotinoids on quail,
such as possible interferences with the food chain, need to
be investigated. Finally, understanding the metabolism of
neonicotinoids in quail and screening for neonicotinoid
metabolites would help in determining whether neonicotinoid
use has a role in the decline of quail populations in the Rolling
Plains ecoregion.
Acknowledgment—Funding for the present study was provided by Park
Cities Quail. We thank all of the universities and state organizations who
assisted with trapping and field processing and the Central Receiving
Laboratory at The Institute of Environmental and Human Health, Texas
Tech University, for their field and laboratory assistance. In addition, we
thank all the landowners who graciously provided access to the study ranch
and housed our trapping teams. We also thank the reviewers for their time
and their valuable input into this manuscript.
Data availability—Data, associated metadata, and calculation tools are
available on request by contacting R.J. Kendall (ron.kendall@ttu.edu).
REFERENCES
1. Texas Parks and Wildlife Department. 2014. Bobwhite and scaled
quail in the Rolling Plains. [cited 2014 July]. Available from: http://
www.twpd.state.tx.us/huntwild/hunt/planning/quail_forcast/forecast/
rolling_plains/.
2. Dunham NR, Soliz LA, Fedynich AM, Rollins D, Kendall RJ. 2014.
Evidence of an Oxyspirura petrowi epizootic in northern bobwhites
(Colinus virginianus). J Wildl Dis 50:552–558.
3. Guthrey FS, Koerth NE, Smith DS. 1988. Reproduction of
Northern Bobwhites in semiarid environments. J Wildl Manage
52:144–149.
4. Blank PJ. 2013. Northern Bobwhite response to conservation
reserve program habitat and landscape attributes. J Wildl Manage
77:68–74.
5. Duren KR, Buler JJ, Jones W, Williams CK. 2011. An improved multi-
scale approach to modeling habitat occupancy of Northern Bobwhite.
J Wildl Manage 75:1700–1709.
6. Mineau P, Palmer C. 2013. The impact of the nation’s most widely
used insecticides on birds. American Bird Conservancy, The Plains,
VA, USA.
7. Millar NS, Denholm I. 2007. Nicotinic acetylcholine receptors: Targets
for commercially important insecticides. Invert Neurosci 7:53–66.
8. Douglas MR, Tooker, JF. 2015. Large-scale deployment of seed
treatments has driven rapid increase in use of neonicotinoid insecticides
and preemptive pest management in U.S. field crops. Environ Sci
Technol 49:5088–5097.
9. Tapparo A, Giorio C, Marzaro M, Marton D, Solda L, Girolami V.
2011. Rapid analysis of neonicotinoid insecticides in guttation drops of
corn seedlings obtained from coated seeds. J Environ Monit 13:
1564–1568.
10. Stockstad E. 2013. Pesticides under fire for risks to pollinators. Science
340:674–676.
11. Soloway SB. 1976. Naturally occurring insecticides. Environ Health
Perspect 14:109–117.
12. Mason R, Tennekes H, Sanchez-Bayo F, Uhd Jepsen P. 2013. Immune
suppression by neonicotinoid insecticides at the root of global wildlife
declines. J Environ Immunol Toxicol 1:3–12.
13. Gibbons D, Morrissey C, Mineau P. 2014. A review of the direct and
indirect effects of neonicotinoids and fipronil on vertebrate wildlife.
Environ Sci Pollut Res 22:103–118.
14. Gill HK, Garg H. 2014. Pesticides: Environmental impacts and
management strategies. In Soloneski S, ed, Pesticides—Toxic Aspects.
[cited 2015 October 1]. Available from: http://www.intechopen.com/
books/pesticides-toxic-aspects/pesticides-environmental-impacts-and-
management-strategies
15. Hallmann CA, Foppen RPB, van Turnhout CAM, de Kroon H,
Jongejans E. 2014. Declines in insectivorous birds are associated with
high neonicotinoid concentrations. Nature 511:341–343.
16. Peakall DB. 1985. Behavioural responses of birds to pesticides and
other contaminants. Residue Rev 96:45–77.
17. Tokumoto J, Danjo M, Kobayashi Y, Kinoshita K, Omotehara T,
Tatsumi A, Hashiguchi M, Sekijima T, Kamisoyama H, Yokoyama
T, Kitagawa H, Hoshi N. 2013. Effects of exposure to clothianidin
on the reproductive system of male quail. J Vet Med Sci 75:
755–760.
18. Eissa OS. 2004. Protective effect of vitamin C and glutathione against
the histopathological changes induced by imidacloprid in the liver and
testis of Japanese quail. Egypt J Hosp Med 16:39–54.
19. Nauen R, Ebbinghaus-Kintscher U, Salgado VL, Kaussmann M. 2003.
Thiamethoxam is a neonicotinoid precursor converted to clothianidin in
insects and plants. Pest Biochem Physiol 76:55–69.
20. Goulson D. 2014. Ecology: Pesticides linked to bird declines. Nature
511:295–296.
21. Avrey ML, Fischer DL, Primus TM. 1997. Assessing the hazard of
granivorous birds feeding on chemically treated seeds. Pest Sci
49:362–366.
22. Goulson D. 2013. Review: An overview of the environmental risks
posed by neonicotinoids insecticides. J Appl Ecol 50:977–987.
23. Prosser P, Hart AD. 2005. Assessing potential exposure of birds to
pesticide-treated seeds. Ecotoxicology 14:679–691.
24. Lopez-Antia A, Ortiz-Santaliestra ME, Mougeot F, Mateo R. 2013.
Experimental exposure of red-legged partridges (Alectoris rufa)toseeds
coated with imidacloprid, thiram and difenoconazole. Ecotoxicology
22:125–138.
1514 Environ Toxicol Chem 35, 2016 U. Turaga et al.
25. Anastassiades M, Lehotay, SJ. 2003. Fast and easy multiresidue method
employing acetonitrile extraction/partitioning and dispersive solid
phase extraction for the determination of pesticide residues in produce.
J AOAC Int 86:412–431.
26. Pascual JA, Hart ADM, Fryday SL. 1999. Incidence of lethal bird
poisoning reduced by regurgitation of pesticide-treated food. Environ
Toxicol Chem 18:247–253.
27. Berny PJ, Buronfosse F, Videmann B, Buronfosse T. 1999. Evaluation
of the toxicity of imidacloprid in birds. A new high performance thin
layer chromatography (HPTLC) method for the analysis of liver and
crop samples in suspected poisoning cases. J Liq Chromatogr Relat
Technol 22:1547–1559.
28. Pfluger W, Schmuck R. 1991. Ecotoxicological profile of imidacloprid.
Pflanzenschutz-Nachrichten Bayer 44:145–158.
29. Edwards PJ, Bembridge J, Jackson D, Earl M, Anderson L. 1998.
Estimation of pesticide residues on weed seeds for wildlife risk
assessment. Proceedings, 8th Annual Meeting of SETAC-Europe,
April 14–18, 1998, Bordeaux, France.
30. Elbert A, Haas M, Springer B, Thielert W, Nauen R. 2008. Applied
aspects of neonicotinoid uses in crop protection. Pest Manag Sci
64:1099–1105.
31. Jeschke P, Nauen R. 2008. Neonicitinoids—From zero to hero in
insecticide chemistry. Pest Manag Sci 64:1084–1098.
32. Cloyd RA, Bethke JA. 2011. Impact of neonicotinoid insecticides on
natural enemies in greenhouse and interiorscape environments. Pest
Manag Sci 67:3–9.
33. Liu L, Feng T, Wang C, Wu Q, Wang Z. 2014. Enrichment of
neonicotinoid insecticides from lemon juice sample with magnetic
three-dimensional grapheme as the adsorbent followed by determination
with high-performance liquid chromatography. J Sep Sci 37:1276–1282.
34. European Commission. 2004. Acetamiprid. SANCO/1392/2001-Final.
Brussels, Belgium.
35. Grau R. 1995. YRC 2894 techn. Acute oral toxicity to Bobwhite quail.
Bayer AG Report No. VB-036. 39 pp.
36. Johnson AJ. 1996. CGA 293343 Subacute dietary toxicity (LC50) to the
Bobwhite quail. CGA 293343/0047.
Neonicotinoid use and potential exposure Environ Toxicol Chem 35, 2016 1515