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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

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Northern Bobwhite (Colinus virginianus) and Scaled quail (Callipepla squamata) populations have seen a dramatic decline in the Rolling Plains ecoregion of Texas and Oklahoma, USA. There is a rising concern for the potential toxicity of neonicotinoids in birds. To investigate this concern, we examined crops of 81 Northern Bobwhite and 17 Scaled quail to determine the presence or absence of three neonicotinoid (clothianidin, imidacloprid, and thiamethoxam) treated seeds. We did not find any treated seeds in the 98 crops examined. We collected liver samples from all 98 quail and analyzed them for neonicotinoid residues. Analysis revealed very low concentrations of neonicotinoids within the quail liver samples. Our study suggested there is little to no risk of direct toxicity of neonicotinoids to quail. This article is protected by copyright. All rights reserved.
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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;35:15111515. #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 rst 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 elds, 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 specic 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 chromatographymass 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 (AugustOctober) 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 identied 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]. Briey, 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 nely 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 ltered the extracts through a
0.45-mmnylonlter before loading on to the autosampler.
For quantication of neonicotinoids in quail livers, LC/MS
was performed using an Accela
TM
LC system (Thermo Scientic)
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 ow
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 acidied with 0.1% v/v
formic acid, as the mobile phase with the following gradient
elution prole: 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
Scientic) 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
40.775%) 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 prole 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.
AcknowledgmentFunding for the present study was provided by Park
Cities Quail. We thank all of the universities and state organizations who
assisted with trapping and eld processing and the Central Receiving
Laboratory at The Institute of Environmental and Human Health, Texas
Tech University, for their eld 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 availabilityData, associated metadata, and calculation tools are
available on request by contacting R.J. Kendall (ron.kendall@ttu.edu).
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Bobwhite quail. CGA 293343/0047.
Neonicotinoid use and potential exposure Environ Toxicol Chem 35, 2016 1515
... 3,10−13 On the basis of its median lethal dose, technical-grade IMI is the most potent neonicotinoid seed treatment in birds, being classed as highly toxic to gray partridge (Perdix perdix; LD50 = 13.9 mg/kg BW), Japanese quail (Coturnix japonica; LD50 = 31 mg/kg BW), feral pigeon (Columba livia domestica; LD50 = 25−50 mg/kg BW), house sparrow (Passer domesticus; LD50 = 41 mg/kg BW) and canary (Serinus canaria domestica; LD50 = 25−50 mg/kg BW). 14 Imidacloprid and other neonicotinoids have occasionally been detected in free-ranging birds 15−18 and implicated with varying degrees of certainty in some bird mortality events. 15,16,18,19 Despite evidence that exposure of wild birds to IMI following seed ingestion could result in toxicity, toxicokinetic data (absorption, distribution, metabolism, excretion; ADME) for IMI (or any neonicotinoid) are lacking for avian species. In laboratory rats (Rattus norvegicus), orally administered IMI was found to be extensively (>92%) and rapidly absorbed from the gastrointestinal (GI) tract. ...
... 19,49 In a study of freeranging Northern bobwhite (Colinus virginianus) and scaled quail (Callipepla squamata) in Texas and Oklahoma, no treated seeds were present in the crop of 98 individuals, but residues of IMI, clothianidin, or thiamethoxam were detected in the liver of 17% of the birds (IMI ranged up to 62.3 ng/g ww). 16 It was concluded that neonicotinoid treated seeds posed no imminent danger to quail in this region, 16 although others suggest a negative association between neonicotinoid use and bobwhite abundance for this region. 50 However, in France, which has an established incident monitoring program, 101 poisoning incidents in or near agricultural fields were attributed to use of pesticide-treated seeds between 1995 and 2014. ...
... 19,49 In a study of freeranging Northern bobwhite (Colinus virginianus) and scaled quail (Callipepla squamata) in Texas and Oklahoma, no treated seeds were present in the crop of 98 individuals, but residues of IMI, clothianidin, or thiamethoxam were detected in the liver of 17% of the birds (IMI ranged up to 62.3 ng/g ww). 16 It was concluded that neonicotinoid treated seeds posed no imminent danger to quail in this region, 16 although others suggest a negative association between neonicotinoid use and bobwhite abundance for this region. 50 However, in France, which has an established incident monitoring program, 101 poisoning incidents in or near agricultural fields were attributed to use of pesticide-treated seeds between 1995 and 2014. ...
Article
Birds are potentially exposed to neonicotinoid insecticides by ingestion of coated seeds during crop planting. Adult male Japanese quail were orally dosed with wheat seeds coated with an imidacloprid (IMI) formulation at either 0.9 mg/kg body weight (BW) or 2.7 mg/kg BW (~3 and 9% of IMI LD50 for Japanese quail, respectively) for 1 or 10 days. Quail were euthanized between 1 and 24 h post-exposure to assess toxicokinetics. Analysis revealed rapid absorption (1 h) into blood, and distribution to brain, muscle, kidney and liver. Clearance to below detection limits occurred at both dose levels and exposure durations in all tissues within 24 h. Metabolism was extensive, with 5-OH-IMI and IMI-olefin detected at greater concentrations than IMI in tissues and fecal samples. There was no lethality or overt signs of toxicity at either dose level. Furthermore, no evidence of enhanced expression of mRNA genes associated with hepatic xenobiotic metabolism, oxidative DNA damage or alterations in concentrations of corticosterone and thyroid hormones was observed. Application of the toxicokinetic data was used to predict IMI residue levels in liver with reasonable results for some field exposure and avian mortality events. It would appear that some affected species are either consuming larger quantities of seeds or exhibit differences in ADME or sensitivity than predicted by read-across from these data.
... NN residues have been measured in a range of avian samples, but only from a limited number of farmland species. Thus far, NNs have been detected in the liver, crop or eggs of four gamebird and three columbid species (Bro et al., 2016;Millot et al., 2017;Ertl et al., 2018;Turaga et al., 2016). NN poisonings have also been documented in grey partridge Perdix perdix and columbid species, of which N70% (of 101 incidences and 734 mortalities) occurred during the autumn sowing period (Millot et al., 2017). ...
... The species exposed were not restricted to any one taxonomic group: plasma samples tested positive in species of sparrow, bunting, finch and thrush, whilst species of columbid, galliforme, corvid and passerine were observed consuming treated seed at spilt seed clusters. Observations relating to galliformes and columbids are consistent with previous observations of NN poisonings during autumn months and the detection of NN residues in samples of liver and eggs collected from quail, partridge and pigeon (Bro et al., 2016;Millot et al., 2017;Ertl et al., 2018;Turaga et al., 2016). Furthermore, exposure was confirmed here for a similar species Table 5 Summary of the prevalence of clothianidin (CLO) in avian samples collected post sowing and the concentrations of the compound measured in individual plasma samples collected from each species. ...
Article
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Neonicotinoids are the largest group of systemic insecticides worldwide and are most commonly applied as agricultural seed treatments. However, little is known about the extent to which farmland birds are exposed to these compounds during standard agricultural practices. This study uses winter cereal, treated with the neonicotinoid clothianidin, as a test system to examine patterns of exposure in farmland birds during a typical sowing period. The availability of neonicotinoid-treated seed was recorded post-sowing at 39 fields (25 farms), and camera traps were used to monitor seed consumption by wild birds in situ. The concentration of clothianidin in treated seeds and crop seedlings was measured via liquid chromatography-tandem mass spectrometry, and avian blood samples were collected from 11 species of farmland bird from a further six capture sites to quantify the prevalence and level of clothianidin exposure associated with seed treatments. Neonicotinoid-treated seeds were found on the soil surface at all but one of the fields surveyed at an average density of 2.8 seeds/m². The concentration of clothianidin in seeds varied around the target application rate, whilst crop seedlings contained on average 5.9% of the clothianidin measured in seeds. Exposure was confirmed in 32% of bird species observed in treated fields and 50% of individual birds post-sowing; the median concentration recorded in positive samples was 12 ng/mL. Results here provide clear evidence that a variety of farmland birds are subject to neonicotinoid exposure following normal agricultural sowing of neonicotinoid-treated cereal seed. Furthermore, the widespread availability of seeds at the soil surface was identified as a primary source of exposure. Overall, these data are likely to have global implications for bird species and current agricultural policies where neonicotinoids are in use, and may be pertinent to any future risk assessments for systemic insecticide seed treatments.
... Aside from palatability, other factors present in a natural environment such as hunger/starvation (Pascual et al. 1999c), predation risk (Avery et al. 1994), food unpredictability and accessibility (Lopez-Antia et al. 2014;Murton and Visozo 1963;Browns 1968), or competition (McKay et al. 1999) are all likely to influence consumption rates of different bird species in real-world situations. Complex though, all of these effects may be field evidence of bird fatality due to imidacloprid-treated and neonicotinoid-treated seed poisoning has been discovered, showing that wild birds do not always avoid eating treated seeds (Berny et al. 1999;Bro et al. 2004Bro et al. , 2010Turaga et al. 2016;Millot et al. 2017;Ertl et al. 2018). ...
Article
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We determine the exposure of wild birds to pesticides via consumption of fludioxonil-treated winter wheat seeds following autumn drilling. We recorded the density of seeds left on the soil surface, bird density, and consumption of pesticide-treated seed by birds using camera traps. We calculated the dose ingested by each bird species in a single feeding bout and if they ate treated seeds exclusively for 1 day. We extrapolated this for an additional 19 pesticides commonly used as seed treatments, assuming equal consumption rates. All three fields contained grains on the soil surface (mean 7.14 seeds/m 2 on sowing day). In total, 1,374 granivorous birds spanning 18 different species were observed in the fields, with 11 species filmed eating the seeds. Fludioxonil appears to pose a low risk to birds, with <1.14% of the LD50 potentially ingested by a bird for a daily maximum amount of seeds. Analysis of the further 19 pesticides commonly used as seed dressings suggests that the neonicotinoid insecticides imidacloprid, clothianidin, and thiamethoxam represent the highest risk for granivorous birds. For example, chaffinch (Fringilla coelebs) could consume 63% of LD50 of imidacloprid in a single feeding bout, and 370% in a day. Further investigation is clearly required to determine whether seeds treated with these other pesticides are consumed as readily as those treated with fludioxonil, as if so this is likely to cause significant harm.
... Ertl et al. (2018) detected imidacloprid, clothianidin or thiamethoxam in 12% of the liver samples of northern bobwhite quails (Colinus virginianus) from Texas (USA). Turaga et al. (2016) detected the same neonicotinoids in 17% of the liver samples of scaled quails (Callipepla squamata) from the Rolling Plains eco-region (USA), although in that study no treated seeds were found in the examined crops. MacDonald et al. (2018) found that 22.5% of analysed wild turkeys (Meleagris gallopavo) from southern Ontario (Canada) had detectable levels of clothianidin and thiamethoxam residues in the liver, and 5% of them had detectable levels of fuberidazole, a triazole fungicide. ...
Article
Sown seeds are a key component of many farmland birds’ diets due to natural food shortages in autumn and winter. Because these seeds are often treated with pesticides, their ingestion by birds can result in toxic effects. For risk assessment, data on treated seed toxicity should be combined with information about exposure risk for wild birds and the factors that modulate it. We characterised the exposure of red-legged partridges to pesticide-treated seeds through the analysis of digestive contents of birds shot by hunters (n = 194) in an agricultural region in central Spain. We measured the contribution of sown seeds to the partridges´ diet and how it related to pesticide exposure. Moreover, we evaluated the influence of landscape composition on the intake of sown seeds and pesticides by partridges. During peak sowing time, seeds constituted half (50.7%) of the fresh biomass ingested by partridges, which consumed mostly winter cereal seeds (42.3% of biomass). Residues of seven fungicides and one insecticide (active ingredients) were detected in 33.0% of birds. The presence of pesticides in digestive contents was linked to the ingestion of cereal sown seeds. Moreover, dietary exposure of birds to pesticides was modulated by landscape characteristics, being lower in areas with heterogeneous landscapes, greater habitat mosaic and more natural vegetation. The estimated dietary intake of pesticides resulting from our field observations, in combination with experimental data on pesticide toxicity, raise concerns about the risks that pesticide-treated cereal seeds pose to granivorous bird populations. Our results highlight the importance of farming landscape composition and diversification, which should be considered as a priority in the agricultural policy to mitigate pesticide risks to farmland birds through the consumption of treated seeds.
... Besides exposure to mammals, also pesticide residues in birds are of a high interest. Different studies claim declines in bird populations due to neonicotinoid use (Hallmann et al., 2014;Turaga et al., 2016). Rial-Berriel et al. (2020) investigated more than 300 pesticides, rodenticides and pharmaceuticals in blood samples of different raptor species and found persistent compounds like PCB's in one third of all samples. ...
Article
In order to gain a better insight into pesticide and pollutant exposure of small (non-target) wildlife animals, a QuEChERS sample preparation method was first developed for 5 g liver tissues (e.g. hedgehog samples) and then downscaled for the analysis of 100 mg liver tissues (e.g. bat samples). The optimized (micro) QuEChERS methods used 1% acetic acid in acetonitrile as organic solvent for liquid-liquid extraction (LLE) and salting out was performed with anhydrous magnesium sulfate and sodium acetate (4:1). After a freezing-out step, sample clean-up was carried out with anhydrous magnesium sulfate, PSA, C18, and GCB (150:25:20:5). Overall, 209 pesticides and persistent organic pollutants (POPs) can be analysed within each sample with gas chromatography coupled to tandem mass spectrometry (GC-MS/MS). Both methods were validated with representative analytes according to the European Commission guideline SANTE/12682/2019. Limits of quantification were between 1 and 20 μg kg⁻¹, and the methods proved to be linear up to 400 μg kg⁻¹. Additionally, the analytes delivered satisfactory results regarding recovery and precision. As proof of concept, samples of six hedgehog livers were analysed with both methods to prove the accuracy of the micro QuEChERS method. Additionally, six livers of different bat species were analysed with the downscaled method. The newly developed micro QuEChERS method for multiresidue analysis requires only minute amounts of biomaterial and represents a sophisticated novel technique for determining the exposure of small wildlife animals to different contaminants.
... Unfortunately, the aforementioned study is not the only one that has recently reported the presence of NNIs in birds. Additionally to the honey buzzard, NNIs have been found in other birds such as the Eurasian eagle owl (Taliansky-Chamudis et al. 2017), hummingbirds (Bishop et al. 2018) and quail (Turaga et al. 2016). The ingestion of NNIs by birds may result in toxic effects. ...
Chapter
Current rates of economic development are interrelated with an increase in environmental pollution. Among different contamination agents, modern insecticides such as neonicotinoids (NNIs) require precise attention in evaluation of losses and benefits. NNIs is relatively new class of systemic insecticides, being in use for about 20 years and embracing around 25% of global pesticide market. Currently there are several methods to apply NNIs to plants such as foliar sprays, soil drenches and seed treatments, and in recent years there has been a global shift towards seed treatment (seed dressing) rather than aerial spraying. The discovery of NNIs was considered as a milestone in the research on insecticides. Possessing chemical structure similar to nicotine and acting as agonists at insects’ acetylcholine receptors, NNIs demonstrate selective toxicity to invertebrates versus vertebrates. In addition, toxicity of NNIs in mammals is between one to three orders of magnitude lower than the toxicity caused by their predecessors: organophosphates, carbamates and pyrethroids. However, NNIs are mobile contaminants that can be transferred from plants to soils and water and induce diverse array of toxic effects in non-target organisms, even affecting animals not in contact with them directly. Surface- and groundwater may also act as vector for the transport of NNIs to untreated locations. The presence of NNIs in water bodies might facilitate their uptake by non-target plants present in littoral and riparian zones, with the potential threat to herbivorous insects. Leaching of NNIs to groundwater may imply their further distribution to other matrices, potentially leading to undesirable environmental issues. Pollinators and aquatic insects appear to be especially susceptible to these insecticides and chronic sublethal effects tend to be more prevalent than acute toxicity. Although a complete knowledge of the fate of NNIs in the environments is missing, authorities are starting to react to the threat they pose by limiting their use and application. Relevant improvements have been made in the field of the toxicity to non-target organisms. Studies that include factors such as mixture toxicity, field or semi-field exposures can make significant contribution to the further evaluating of costs-benefits of neonicotinoids.
... Unfortunately, the aforementioned study is not the only one that has recently reported the presence of NNIs in birds. Additionally to the honey buzzard, NNIs have been found in other birds such as the Eurasian eagle owl (Taliansky-Chamudis et al. 2017), hummingbirds (Bishop et al. 2018) and quail (Turaga et al. 2016). The ingestion of NNIs by birds may result in toxic effects. ...
Chapter
Alzheimer’s disease (AD) is the most common irreversible, progressive brain disorder which causes problems with memory, thinking and behavior with the age. Alzheimer's is the sixth leading cause of death in the United States. Combination of genetic, environmental factors like; chemical radiations, toxicants and mutagens are the main causes for neurodegeneration. Including with these factors some other events can produce early stages of AD, known as early stage AD, and lead to the same eventual distinctive final pathways in the late stages. Such stages could be characterized by neuroinflammation, oxidative stress and neurodegeneration. Furthermore, advanced glycation end products (AGEs) exacerbate amyloid beta (Aβ) has shown enhanced neurotoxicity. Considering these factors, we reinvestigated the role of AGE–RAGE interaction in AD pathology. Accumulation of AGEs is a normal feature of aging, but it becomes impaied in AD. AGEs are prominent in amyloid plaques and neurofibrillary tangles. Several lines of evidences demonstrate that AGE-RAGE interactions are critical for disease pathogenesis and it is at least partially responsible for extensive oxidative stress, inflammation, and neurodegeneration. Therefore many in vitro, in vivo and clinical studies have been focused on AGE–RAGE inhibitors, although their undesirable side effects and solubility issues may limits the usage. Therefore, it is needed to develop a potential, effective and multi-targeted inhibitors in order to prevent AGE induced neurological disorder.
... Unfortunately, the aforementioned study is not the only one that has recently reported the presence of NNIs in birds. Additionally to the honey buzzard, NNIs have been found in other birds such as the Eurasian eagle owl (Taliansky-Chamudis et al. 2017), hummingbirds (Bishop et al. 2018) and quail (Turaga et al. 2016). The ingestion of NNIs by birds may result in toxic effects. ...
Chapter
Nanotechnology, a science dealing with particles at nano scale, is currently used in many fields including environmental management and medicine for welfare of human being. The economic development and quality of life have been improved through nanotechnology. The Polycyclic aromatic hydrocarbons (PAHs) and other toxicants have higher affinity to scaveng by nanopartilces. The structural properties and surface chemistry of nanoparticles are the players, further, extremely high surface area to volume ratio results in multiple enhancement of many beneficial properties. Hence, we have followed a methodology to compare the binding efficiency of nanoparticles and cigarette smoke carcinogens with selected enzymes involved in DNA repair pathways. The molecular interactions have been accomplished using PatchDock server and interestingly got significant interacting results for our hypothesis. PatchDock results showed nanoparticles could be able to trap cigarette smoke carcinogens efficiently in the cellular system. The highest obtained binding efficiency between 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) versus Single wall carbon nanotube (SWcNT) is 2632 score in contrast with NNK versus Human MDC1 BRCT T2067D in complex (PDB ID: 3K05) shows 2454 score, which means NNK could interact with SWcNT more efficiently than 3K05. Another part of the study shows that the highest binding efficiency 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL) versus SWcNT = 2746 score and NNAL versus Titanium dioxide (TiO2) Rutile = 2110 score in contract with NNAL versus Human Thymine DNA Glycosylase(PDB ID: 2RBA) shows 1696 score. It is also signified that NNAL interact with SWcNT and TiO2 rutile more efficiently than 2RBA. The results clearly signifying that SWcNT/TiO2 are binding with NNK/NNAL more efficiently than biomolecules.
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Variation in the relative abundance and biomass of arthropods has important potential consequences for insectivores. We studied the influence of temporal variation and habitat management (i.e., burning and strip-disking) on the availability of potential arthropod prey for brooding northern bobwhites (Colinus virginianus) in the mixed-grass prairie of western Oklahoma. Burning changed the composition of the arthropod community by biomass, but disking did not result in any community-level changes. Burning also increased the total abundance and biomass of arthropods collected compared with the control, but disking did not affect total abundance or biomass. Temporal variation exerted a broader influence on arthropods, and total abundance and biomass increased throughout the duration of the sampling period (May-July) at paired burn/control and paired disked/control sites. Ants, which had the highest abundance and biomass of any taxa, appeared to drive these patterns. The response of individual orders to management and temporal variation varied in size and direction, though we observed more and stronger effects of temporal variation than burning or disking. These results support the idea that burning provides benefits to foraging bobwhite broods through increased total availability of arthropod prey, as well as favorable habitat characteristics (i.e., bare ground, structural heterogeneity). Large temporal variation in total arthropod abundance and biomass, as well as that of individual orders, likely also influences the relative importance of individual prey items in the bobwhite diet based on the timing of nest initiation and hatching. A better understanding of how these temporal and management-induced shifts in arthropod availability influence potential nutrient gains and limitations for bobwhites will require data on macronutrient content and digestibility (i.e., exoskeleton) of prey taxa.
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Neonicotinoid insecticides are among the latest class of insecticides that can have harmful effects on birds. Approximately 30,000 kg of neonicotinoid insecticides are applied annually to 429,100 ha of row‐crop fields within the South Texas Plains Ecoregion. Various studies have shown that treated seeds can be highly toxic to northern bobwhites, with the consumption of only 20 corn seeds causing a fatality. Similarly, other studies have indicated that neonicotinoid insecticides can reduce arthropod populations—a substantial prey base for northern bobwhites, especially during the breeding season— by approximately 60%. Our objective was to conduct an ecological risk assessment of neonicotinoid insecticides' impact on northern bobwhite (Colinus virginianus) populations in the South Texas Plains Ecoregion. We estimated that juvenile and adult northern bobwhites could intake from 7.32 to 27.0 mg/kg/day and from 10.0 to 37.5 mg/kg/day of neonicotinoid insecticides, respectively, which can cause adverse effects on growth, reproductive output, and long‐term survival. Our study determined that the application of 30,000 kg of neonicotinoid insecticides annually in the South Texas Plains Ecoregion harms the region's northern bobwhite that are exposed to neonicotinoids. This article is protected by copyright. All rights reserved.
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Regurgitation by birds feeding on pesticide-treated seed was quantified in two experiments, and its role in reducing the risk of acute poisoning from an organophosphorus pesticide was assessed. Captive feral pigeons (Columba livia) were offered fonofos-treated seed ad libitum on a test day after a 6-d period in which one group was given free access to untreated seed and another group was given no food in one experiment or 15% of normal intake in the other. Avoidance of treated seed reduced intake substantially, preventing the ingestion of lethal doses for all birds fed ad libitum and some but not all of the food-restricted birds. Some of the latter regurgitated most of the seed taken in (>60%), reducing by similar to 50% the dose of pesticide assimilated and lowering the dose from above to below lethal levels. Regurgitation was the most likely explanation for the survival of at least 12 and 50% of the food-restricted birds in these experiments. Regurgitation reduced but did not prevent mortality, because some birds died without regurgitating and others despite doing so. This study provides the first clear evidence that regurgitation can directly reduce mortality of birds exposed to pesticides in their food. Implications for the risk of poisoning wild birds and avian toxicity testing are discussed.
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Neonicotinoids are the most widely used class of insecticides worldwide, but patterns of their use in the U.S. are surprisingly poorly documented, constraining attempts to understand their role in pest management and potential non-target effects. We synthesized publicly available data to estimate and interpret trends in neonicotinoid use since their introduction in 1994, with a special focus on seed treatments, a major use not captured by the national pesticide-use survey. Neonicotinoid use increased rapidly between 2003 and 2011, as seed-applied products were introduced in field crops, marking an unprecedented shift toward large-scale, preemptive insecticide use: 34-44% of soybeans and 79-100% of corn hectares were treated in 2011. This finding contradicts recent analyses, which concluded that insecticides are used today on fewer corn hectares than a decade or two ago. If current trends continue, neonicotinoid use will increase further through application to more hectares of soybean and other crop species and escalation of per-seed rates. Alternatively, our results, and other recent analyses, suggest that carefully targeted efforts could considerably reduce neonicotinoid use in field crops without yield declines or economic harm to farmers, reducing the potential for pest resistance, non-target pest outbreaks, environmental contamination, and harm to wildlife, including pollinator species.
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We studied adult northern bobwhites (Colinus virginianus) in 2 semiarid environments (x̄ annu. net evaporation = 140 and 90 cm) during 1981-83 to determine climatic effects on phenology and intensity of reproduction. In the drier environment, gonadal recrudescence began 1-2 weeks earlier and the effective breeding season ended about 2 months earlier. A smaller percentage of females entered laying condition in the drier environment (P < 0.005), but >95% of males had testes large enough to contain motile sperm in both environments during peaks of reproduction (Apr-Jun). A substantial decline in laying in July-August in the drier environment probably reflected an adaptive response to harsh late-summer habitat conditions as well as a physiological response to high ambient temperatures and dietary moisture stress.
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Pesticides are double wedged weapons. They are considered to be the heavy cost of civilization. They are widely used in our daily life. Recently their effects on male fertility have attracted attention. One of these pesticides is imidacloprid. This work was designed to investigate the histological changes in liver and testis of Japanese quail treated with imidacloprid for different periods as well as the reversibility of such changes after arrest of the treatment for recovery period. The effect of vitamin C and glutathione as a protective agent against the action of imidacloprid on liver and testis was also determined.
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Neonicotinoids are now the most widely used insecticides in the world. They act systemically, travelling through plant tissues and protecting all parts of the crop, and are widely applied as seed dressings. As neurotoxins with high toxicity to most arthropods, they provide effective pest control and have numerous uses in arable farming and horticulture.However, the prophylactic use of broad-spectrum pesticides goes against the long-established principles of integrated pest management (IPM), leading to environmental concerns.It has recently emerged that neonicotinoids can persist and accumulate in soils. They are water soluble and prone to leaching into waterways. Being systemic, they are found in nectar and pollen of treated crops. Reported levels in soils, waterways, field margin plants and floral resources overlap substantially with concentrations that are sufficient to control pests in crops, and commonly exceed the LC50 (the concentration which kills 50% of individuals) for beneficial organisms. Concentrations in nectar and pollen in crops are sufficient to impact substantially on colony reproduction in bumblebees.Although vertebrates are less susceptible than arthropods, consumption of small numbers of dressed seeds offers a route to direct mortality in birds and mammals.Synthesis and applications. Major knowledge gaps remain, but current use of neonicotinoids is likely to be impacting on a broad range of non-target taxa including pollinators and soil and aquatic invertebrates and hence threatens a range of ecosystem services.
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Decreases in bird numbers are most rapid in areas that are most heavily polluted with neonicotinoids, suggesting that the environmental damage inflicted by these insecticides may be much broader than previously thought. See Letter p.341
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Recent studies have shown that neonicotinoid insecticides have adverse effects on non-target invertebrate species. Invertebrates constitute a substantial part of the diet of many bird species during the breeding season and are indispensable for raising offspring. We investigated the hypothesis that the most widely used neonicotinoid insecticide, imidacloprid, has a negative impact on insectivorous bird populations. Here we show that, in the Netherlands, local population trends were significantly more negative in areas with higher surface-water concentrations of imidacloprid. At imidacloprid concentrations of more than 20 nanograms per litre, bird populations tended to decline by 3.5 per cent on average annually. Additional analyses revealed that this spatial pattern of decline appeared only after the introduction of imidacloprid to the Netherlands, in the mid-1990s. We further show that the recent negative relationship remains after correcting for spatial differences in land-use changes that are known to affect bird populations in farmland. Our results suggest that the impact of neonicotinoids on the natural environment is even more substantial than has recently been reported and is reminiscent of the effects of persistent insecticides in the past. Future legislation should take into account the potential cascading effects of neonicotinoids on ecosystems.