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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
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
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
Published online 13 November 2015 in Wiley Online Library
DOI: 10.1002/etc.3305
Environmental Toxicology and Chemistry, Vol. 35, No. 6, pp. 1511–1515, 2016
#2015 SETAC
Printed in the USA
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.
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
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
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
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
LC system (Thermo Scientic)
equipped with an autosampler and a degasser. Chromatographic
separation of neonicotinoids was attained on an Ascentis
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
(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
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.
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
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
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
(clothianidin-based, active ingredient
40.3%) and Gaucho
(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
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.
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 (
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Neonicotinoid use and potential exposure Environ Toxicol Chem 35, 2016 1515
... All these studies, as well as others that have monitored the exposure of wild birds to pesticides used for seed treatments (e. g. Bro et al., 2016;Ertl et al., 2018;MacDonald et al., 2018;Turaga et al., 2016), use invasive methods (e.g. blood collection) or biological samples (e.g. ...
... Because of the sowing asynchrony among fields, treated seeds were continuously available to birds on the field surfaces during the whole period of sample collection. To ensure the collection of freshly excreted faeces, these were collected from birds while roosting at night (Turaga et al., 2016). Birds were located at dusk to identify their roosting sites, which were visited later on the same night. ...
The treatment of seeds with pesticides is an extended practice in current agriculture. There is a high risk of exposure in granivorous birds, such as the red-legged partridge (Alectoris rufa), that can consume those seeds remaining on the surface during sowing. Fungicide exposure could in turn affect bird reproductive capacity. To better understand to what extent triazole fungicides are a threat to granivorous birds, we need an easy and reliable method to quantify field exposure. In this study, we tested a novel non-invasive method to detect the presence of triazole fungicide residues in farmland bird faeces. We experimentally exposed captive red-legged partridges to validate the method, and then applied it in a real scenario to assess exposure of wild partridges. We exposed adult partridges to seeds treated with two formulations containing triazole fungicides as active ingredients: Vincit®Minima (flutriafol 2.5%) and Raxil®Plus (prothioconazole 25% and tebuconazole 15%). We collected two types of faeces (caecal and rectal samples) immediately after exposure and 7 days later and quantified the concentrations of the three triazoles and their common metabolite (1,2,4-triazole). The three active ingredients and 1,2,4-triazole were only detected in faeces collected immediately after exposure. Triazole fungicide detection rates in rectal stool were 28.6%, 73.3% and 80% for flutriafol, prothioconazole and tebuconazole, respectively. In caecal samples, detection rates were 40%, 93.3% and 33.3%, respectively. 1,2,4-triazole was detected in 53% of rectal samples. For an applied use of the method in the field, we collected 43 faecal samples from wild red-legged partridges during autumn cereal seed sowing and found detectable levels of tebuconazole in 18.6% of the analysed wild partridges. Our study shows that faecal analysis can be a useful tool to assess farmland bird exposure to triazole fungicides, when samples are fresh and the method has been validated for the detection of target molecules.
... Vol:. (1234567890) appears to be infrequent (McGee et al., 2018;Turaga et al., 2016), treated seeds do not seem to be avoided, especially during the sowing period of winter cereals (Lennon et al., 2020;Lopez-Antia et al., 2016;Roy & Coy, 2020;Roy et al., 2019). Although the number of seeds consumed by birds represents an overall concentration of active molecules below LD 50 , individuals may ingest doses that are known to produce acute and/or chronic exposure (lowest observed adverse effect level, LOAEL; see Table 4 in Roy & Coy, 2020). ...
... Although the number of seeds consumed by birds represents an overall concentration of active molecules below LD 50 , individuals may ingest doses that are known to produce acute and/or chronic exposure (lowest observed adverse effect level, LOAEL; see Table 4 in Roy & Coy, 2020). Studies finding no 'imminent danger' to wildlife (see Turaga et al., 2016 for an example) should, however, refer to LOAEL rather than to LD 50 , which is not representative of the risk to granivorous bird endangered by treated seed consumption (see section 'Improving ecological risk assessment' for a discussion on these endpoints). ...
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For decades, we have observed a major biodiversity crisis impacting all taxa. Avian spe- cies have been particularly well monitored over the long term, documenting their declines. In particular, farmland birds are decreasing worldwide, but the contribution of pesticides to their decline remains controversial. Most studies addressing the effects of agrochemicals are limited to their assessment under controlled laboratory conditions, the determination of lethal dose 50 (LD50) values and testing in a few species, most belonging to Galliformes. They often ignore the high interspecies variability in sensitivity, delayed sublethal effects on the physiology, behaviour and life-history traits of individuals and their con- sequences at the population and community levels. Most importantly, they have entirely neglected to test for the multiple exposure pathways to which individu- als are subjected in the field (cocktail effects). The present review aims to provide a comprehensive over- view for ecologists, evolutionary ecologists and con- servationists. We aimed to compile the literature on the effects of pesticides on bird physiology, behaviour and life-history traits, collecting evidence from model and wild species and from field and lab experiments to highlight the gaps that remain to be filled. We show how subtle nonlethal exposure might be pernicious, with major consequences for bird populations and communities. We finally propose several prospec- tive guidelines for future studies that may be consid- ered to meet urgent needs.
... As a result of these chemical advances and despite the lack of a 'smoking gun' indicative of levels causing intoxication such as a biochemical test of impairment, there is now a plethora of studies that show extensive exposure of birds in farmland. Turaga et al. (2015) provided data on bird exposure to treated seed in NW Texas, USA on Bobwhite Quail and Scaled Quail (Callipepla squamata), two species exhibiting declines in that region. They trapped and euthanized individuals of both species (81 BOBW; 17 SCQU) in the late summer of 2013, the time of winter wheat sowing. ...
Technical Report
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A 10 year update of the science behind the need to restrict neonicotinoid insecticides to protect birds and the ecosystems on which they depend. As with the 2013 report, this was produced on behalf of the American Bird Conservancy.
... The next most "popular" are seed dressings with the active substances thiamethoxam and clothianidin (in 2018, 14 and 11 preparations were registered, respectively, see List of pesticides..., 2018) have a much lower level of toxicity for birds -approximately 50-100 times. In particular, LD50 of the first of these is 1552 mg/kg BW for Virginia Quail, Colinus virginianus (Linnaeus, 1758) (Turaga et al., 2016), for clothianidin -more than 2000 mg/kg BW (Gibbons et al., 2015). There are two preparations with the active substance fipronil among the insecticide-treatments registered in Ukraine. ...
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Since the 1980s, a significant decline in the number of breeding populations of the Rook, Corvus frugilegus Linnaeus, 1758, has been observed in many European countries. In Ukraine, this trend has been observed since the late 1990s. In 2021, the conservation status of the Rook in Europe was significantly upgraded — from “LC” (Least Concern) to “VU” (Vulnerable). The analysis of the material of surveys in 1983–1985 and 2021 on the territory of 1850 km² in Kyiv Region showed that during the 35 years, there was a catastrophic decrease in the number of nesting birds, it decreased almost 12 times, from 11,480 pairs in the 1980s to 961 pairs in 2021. In addition, the spatial structure of the distribution of colonies in relation to large arable agricultural land has changed. We suggest that the main reason for these changes is the widespread use of seed treatments with the active ingredient imidacloprid. The use of treated grains for food by birds leads to their death. Since 2018, the countries of the European Union countries have banned the use of insecticides containing imidacloprid on open land.
... The efficiency of sowing is never complete in practice, and the unincorporated treated seeds remaining on the soil surface, although at varying densities, are available to seed-eating birds (de Leeuw et al., 1995;De Snoo & Luttik, 2004;López-Antia et al., 2016;McKay et al., 1999). Most field studies have focused on the risk to birds of winter cereal seeds (mainly wheat and barley) treated with neonicotinoids (Botha et al., 2018;Ertl et al., 2018;Lennon et al., 2020aLennon et al., , 2020bTuraga et al., 2016). Recent studies in Canada and the United States evaluated the risk to birds posed by spring cereal seeds (i.e., maize) and oilseeds (i.e., soybean) treated with neonicotinoids (McGee et al., 2018;Roy & Coy, 2020;Roy et al., 2019), but little is known about the risk posed by seeds and their cotyledons treated with imidacloprid in South American agroecosystems. ...
Treated seeds and their cotyledons can present a toxicological risk to seed-eating birds. To assess whether avoidance behavior limits exposure and consequently the risk to birds, three fields were sown with soybeans. Half of the surface of each field was sown with seeds treated with 42 g /100 kg seed of insecticide imidacloprid (T plot, treated) and the other half with seeds without imidacloprid (C plot, control). Unburied seeds were surveyed in C and T plots at 12 h and 48 h post-sowing. Damaged seedlings was surveyed in C and T plots at 12 days post-sowing. Abundance and richness of birds was surveyed at the field level (without distinguishing between C and T plots) before, during, and after sowing, and 12 days post-sowing. Seed density was higher in the headlands of the T plots than in the C plots, but did not differ between 12 and 48 h. The damage on cotyledons of seedlings was 15.4% higher in C plots than in T plots. The abundance and richness per hectare of birds that eat seeds and cotyledons were lower after sowing, indicating a deterrent effect of sowing imidacloprid-treated seeds on birds. Although the variation in seed density over time does not allow solid conclusions to be drawn about the avoidance of seeds treated by birds, the seedling results suggest an aversive effect of imidacloprid-treated soybeans on birds. The dominant species was the eared dove (Zenaida auriculata), whose risk of acute poisoning by imidacloprid in soybean seeds and cotyledons was low, according to its toxicity exposure ratio (TER), its foraged area of concern, and its foraged time of concern. This article is protected by copyright. All rights reserved. Environ Toxicol Chem 2023;00:0-0. © 2023 SETAC.
... Exposure of birds to pesticide-treated seeds is furthermore demonstrated by mounting evidence that wild birds are exposed to neonicotinoids and fungicides used for seed coating, [108][109][110][111][112][113][114][115][116] as well as reports of mortality linked to ingestion of pesticide-coated seeds. [54][55][56][57][117][118][119][120] The dose ingested by birds in a single feeding bout on treated seeds can be sufficient to cause lethal and sublethal effects. ...
With the expansion of human settlements and the environmental changes brought on by human activity and pollutants, toxicology and risk assessment of bird and reptile species is becoming increasingly of interest to toxicologists involved in environmental research. This book focuses specifically on environmental risk assessment in non-conventional bird and reptile species. Bird and Reptile Species in Environmental Risk Assessment Strategies will be an ideal companion to toxicologists and ecologists interested in risk assessment in the environments of birds and reptiles, particularly those with an interest in the impact introduced by human activity. The book will also be of interest to those working in conservation biology, biological invasion, biocontrol and habitat management.
... This method is used in the gardens for flowers and vegetables and in agriculture on soft fruits and greenhouse crops. Low lipophilicity, indicated by octanol/water partition coefficient value (log Pow), suggest they do not bio-accumulate in the adipose tissues of animals (Turaga et al. 2016). However, moderate water solubility combined with low lipophilicity means they may have a potential to accumulate in water. ...
An ability of insecticides to selectively target pests without affecting non-target species is a key determinant of success of compounds used in agriculture. Neonicotinoids which encompass seven different types of chemical representing three distinct chemical classes, namely the cyanoamidines, nitroguanidines and nitromethylenes, are a major class of insecticides. They effectively control a wide range of insect pests and have low toxicity against mammals, however they can also negatively impact on non-target species of bees, threatening food safety. Neonicotinoids act by targeting insect nicotinic acetylcholine receptors (nAChRs), which are major excitatory receptors in the insect central nervous system. Difficulties in heterologous expression of these proteins hinders their pharmacological characterisation and identification of the molecular determinants of neonicotinoid-toxicity. This thesis describes efforts into developing Caenorhabditis elegans (C. elegans) as a platform in which the mode of action and selective toxicity of neonicotinoid-insecticides can be studied. We determined the effects of neonicotinoids on C. elegans behaviours governed by the cholinergic neurotransmission. The cyanoamidine represented by clothianidin, the nitroguanidine represented by thiacloprid and the nitromethylene represented by nitenpyram showed low efficacy on locomotion, pharyngeal pumping, egg-laying and egg-hatching of young adult wild-type C. elegans. Exposure of mutant worm with enhanced cuticular permeability showed increased susceptibility of worms to all three neonicotinoids tested, suggesting an adult cuticle limits drug access. The role of the cuticle in neonicotinoids susceptibility was investigated in C. elegans cut-head preparation, in which the cuticle is removed and the effects of compounds on pharyngeal pumping are scored. Out of the three neonicotinoids applied, clothianidin showed the greatest efficacy. It stimulated pharyngeal pumping at ≥ 75 µM (18.75 ppm). Generally, the concentrations effective against the function of the pharynx are an order or magnitude lower than the residual, average concentration of neonicotinoids in the soil, suggesting C. elegans is not impacted in the field, and at least several fold lower than lethal doses in insect-pests. The difference in neonicotinoid-susceptibility between adult C. elegans and insects precludes the use of C. elegans pharynx as a platform for the mode of action studies, but highlights its potential as a suitable background for the heterologous expression of insect nAChRs. Further experiments showed that C. elegans eat-2 nAChR mutant is a suitable genetic background, in which the expression of heterologous nAChRs can be Expression of the exogenous receptor, human α7 in the pharynx of eat-2 mutant led to a cell-surface expression, as shown by staining with labeled α-bungarotoxin (α-bgtx). However the feeding and pharmacological phenotypes of the mutant were not rescued. C. elegans strain in which human α7 is expressed in the wild-type genetic background was also generated to determine whether the pharmacology of the human receptor can be imposed on the C. elegans pharynx. No difference in the pharyngeal response to nAChR agonists cytisine, nicotine or acetylcholine were noted. The lack of apparent functionality of α7 receptor could be due to the incorrect cellular localisation of this protein. α-bgtx staining showed that α7 receptor is expressed in the specific cells of the pharyngeal muscle, however this localisation does not overlap with the localisation of native EAT-2 receptors. A transgenic strain in which exogenous proteins are expressed using EAT-2 native promoter should be made. scored. Expression of C. elegans nAChR EAT-2 in the pharyngeal muscle rescued the blunted feeding phenotype and 5-HT insensitivity of the eat-2 mutant.
... However, this model species does not seem as suitable as Red-legged Partridge for specific ecotoxicological assessment of treated seeds. A recent study found a complete absence of treated seed in the crop contents of Northern Bobwhite captured from the Rolling Plains in Texas and Oklahoma (Turaga et al. 2016). By contrast, Lopez-Antia et al. (2016) observed Red-legged Partridges feeding on cereal fields that had recently been sown with treated seeds. ...
... The results of this work suggest that prescribed burning positively impacted arthropod prey abundance and biomass for bobwhites and that time also exerted a strong influence on arthropod community composition, abundance, and biomass. While we framed these results in terms of bobwhite foraging ecology, they may apply to other taxa that feed on similarly sized arthropods in this system ( Campbell-Kissock et al. 1985 ;Doxon and Carroll 2007 ;Doxon and Carroll 2010 ;Turaga et al., 2015 ) and other systems (Blackshear and 1990;Sikes et al. 1990 ;Kaspari and Joern 1993 ;Boatman et al. 2004 ;Hellgren et al. 2010 ;Morrow et al. 2015 ;Heuring et al. 2019 ;Feijó et al. 2020 ). ...
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.
Contents Chapter 1 General Aspects – Current and Further Perspectives 1 Marcelo L. Larramendy and Guillermo Eli Liwszyc Chapter 2 Development of Aquatic Bird Indicators of Sub-lethal Mercury Exposure and Risk in Wild Populations of Water Birds in the Everglades (Florida, United States of America) 6 J. Zabala and P. Frederick 2.1 Background and Study Area Description 6 2.1.1 Mercury: Local Emissions, Worldwide Contamination 6 2.1.2 The Everglades 7 2.1.3 Mercury Contamination in the Everglades 11 2.1.4 Development of a Field Sampling Protocol 12 2.1.5 Development of Mercury Exposure Indicators – Tissues 13 2.2 Results 15 2.2.1 Sub-lethal Effects: Results from Experimental Studies 15 2.2.2 Evidence of Mercury Effects in Field Conditions 16 2.3 General Discussion, Lessons Learnt and Pros and Cons of Our and Alternative Approaches 18 2.3.1 Evidence and Estimation of Hg Effects in Natural Populations 18 2.3.2 Indicator Tissues: Comparative Advantages, Limitations and Uncertainty 19 Issues in Toxicology No. 45 Bird and Reptile Species in Environmental Risk Assessment Strategies Edited by Guillermo Eli Liwszyc and Marcelo L. Larramendy r The Royal Society of Chemistry 2023 Published by the Royal Society of Chemistry, ix 2.4 Conclusion and Advice for Similar Cases or Final Remarks 24 Acknowledgements 24 References 24 Chapter 3 The Importance of Ecological Traits in Assessing Seabird Vulnerability to Environmental Risks 33 Can Zhou, Joan A. Browder and Yan Jiao 3.1 Introduction 33 3.2 Failings of the Standard Approach 34 3.3 Vulnerability to Anthropogenic and Natural Risks 34 3.4 Challenges for an Observational Study 35 3.5 A Trait-based Approach 37 3.5.1 An Ecological Dimension Reduction Technique 37 3.5.2 Useful Traits for Ecological Risk Evaluation 39 3.5.3 Trait-based Prediction 41 3.6 Other Challenges 43 3.6.1 Correlation vs. Causation 43 3.6.2 The Default of No Risk 43 3.6.3 Ecological Regulation 44 3.6.4 Climate Change and Variability 44 3.6.5 Other Approaches 47 Disclaimer 47 Acknowledgements 47 References 47 Chapter 4 A Review of the Levels and Distribution Patterns of Organochlorine Pesticides in the Eggs of Wild Birds in India 54 Dhananjayan Venugopal, Jayakumar Samidurai, Jayanthi Palaniyappan, Jayakumar Rajamani and Muralidharan Subramanian 4.1 Introduction 54 4.1.1 Organochlorine Pesticides 54 4.1.2 Organochlorine Pesticides – Marketing and Consumption 56 4.2 Pesticides – Indian Scenario 56 4.3 Impact of Pesticides in Eggs of Wild Birds in India 57 4.3.1 OCP Residues in Birds’ Eggs 57 x Contents 4.3.2 Variation in Residue Levels Based on Species and Food Habits 64 4.3.3 Eggshell Thinning and Reproductive Impairment 66 4.4 Conclusions and Further Recommendations 66 References 67 Chapter 5 Impacts of Agricultural Intensification on Farmland Birds and Risk Assessment of Pesticide Seed Treatments 73 Julie Ce´line Brodeur and Maria Bele´n Poliserpi 5.1 The Intensification of Agriculture 73 5.2 Agricultural Intensification and Bird Declines 74 5.3 Impact of Pesticides on Birds: Direct vs. Indirect Effects 77 5.3.1 Direct Effects 77 5.3.2 Indirect Effects 78 5.4 Seed Treatment With Pesticides: Impacts on Birds 79 5.4.1 Agricultural Intensification Through Seed Treatment 79 5.4.2 Bird Exposure to Pesticide-treated Seeds 80 5.5 Assessment of Risks of Pesticide-treated Seeds to Birds 81 5.5.1 Regulatory Environmental Toxicity Testing 81 5.5.2 Tier I Risk Assessment 83 5.5.3 Refinements and Weight-of-evidence Risk Assessment 83 5.5.4 Future Directions 85 References 85 Chapter 6 Teratological Effects of Pesticides in Reptiles – A Review 97 A. Garceˆs and I. Pires 6.1 Introduction 97 6.2 Reptiles as Sentinel Species 99 6.3 Teratological Effects of Pesticides on Reptiles 99 6.3.1 Order Testudinata 99 6.3.2 Order Rhynchocephalia 102 6.3.3 Order Crocodilia 102 6.3.4 Order Squamata 103 6.4 Final Remarks 104 6.5 Conclusion 105 Acknowledgements 105 References 105 Contents xi Chapter 7 Combined Impact of Pesticides and Other Environmental Stressors on Reptile Diversity in Irrigation Ponds Compared to Other Animal Taxa 110 Hiroshi C. Ito and Noriko Takamura 7.1 Introduction 110 7.2 Biological Communities in Irrigation Ponds 112 7.2.1 Biological Communities 112 7.2.2 Reptiles 112 7.3 Combined Impact of Multiple Stressors on Reptile Diversity Compared to Other Animal Taxa 114 7.4 Impact of Each Stressor on Reptile Diversity Compared to Other Animal Taxa 116 7.4.1 Concrete Bank Protection, Water Depth Reduction and Macrophyte Decline 116 7.4.2 Eutrophication and Pesticide Pollution 119 7.4.3 Invasive Alien Species 120 7.5 Perspective: Usefulness of Turtles as Bioindicators 121 7.6 Conclusion 123 Acknowledgements 123 References 123 Chapter 8 Current Progress in Developing Standardized Methods for Reptilian Toxicity Testing to Inform Ecological Risk Assessment 130 Scott M. Weir, Monica R. Youssif, Taylor Anderson and Christopher J. Salice 8.1 Background on Reptile Toxicity Testing 130 8.1.1 Lack of Reptile Toxicity Data in the Literature 130 8.1.2 Lack of Standardized Methods 131 8.2 Progress in Standardized Methods for Reptile Ecotoxicology/Ecological Risk Assessment 131 8.2.1 Early Efforts in Reptile Toxicology 131 8.2.2 Oral Dosing Methods Using Gelatin Capsules to Accommodate Small Reptiles 133 8.2.3 Standardization of Methods and Developing Breeding Assay Using Anolis Species in Reptile Ecotoxicology 137 8.2.4 Moving Beyond Oral Exposure Dosing: The Potential Importance of Dermal Exposure and Toxicity 144 xii Contents 8.3 Conclusions 144 Acknowledgements 145 References 146 Chapter 9 Morphological and Molecular Evidence of Active Principle Glyphosate Toxicity on the Liver of the Field Lizard Podarcis siculus 151 Mariailaria Verderame, Teresa Chianese and Rosaria Scudiero 9.1 Introduction 151 9.2 Lizards in Contaminated Environments 152 9.3 Effects of Pure GLY on the Liver of P. siculus Specimens 154 9.4 GLY-induced Changes in P. siculus Liver Histology 155 9.5 GLY-induced Changes in the Expression and Synthesis of Proteins in the P. siculus Liver 158 9.6 Conclusion 161 Acknowledgements 162 References 162 Chapter 10 What Is Caiman latirostris Teaching Us About Endocrine Disruptors? 169 M. Durando, G. H. Galoppo, Y. E. Tavalieri, M. V. Zanardi and M. Mun˜oz-de-Toro 10.1 Ecophysiological Characteristics of the Broadsnouted Caiman (Caiman latirostris) 169 10.1.1 Sex Determination 170 10.1.2 Reproduction 170 10.1.3 Hatchling Growth and Development 171 10.1.4 Feeding Habits, Social Behavior and Longevity 171 10.1.5 Sexual Dimorphism 171 10.2 Endocrine-disrupting Chemicals 172 10.2.1 Mechanism of Action of EDCs 173 10.2.2 Types of EDCs 173 10.3 Caiman latirostris as a Sentinel of Environmental Pollution 174 10.4 EDCs and Their Effects on Reproductive Features 175 10.4.1 Natural Exposure 175 10.4.2 Experimental Exposure 177 10.5 EDCs and Their Effects on the Thyroid Histofunctional Characteristics 182 Contents xiii 10.6 Conclusions 183 Acknowledgements 183 References 184 Chapter 11 The Broad-snouted Caiman (Caiman latirostris): A Model Species for Environmental Pesticide Contamination Assessment Through Molecular Markers 196 L. M. Odetti, M. F. Simoniello, P. A. Siroski and G. L. Poletta 11.1 Caiman latirostris: Life History Characteristics and Population Situation in Argentina 197 11.1.1 Geographical Distribution and Sustainable Use Programs 197 11.1.2 Environmental Problems Associated With Agricultural Expansion and the Use of Pesticides 198 11.2 Why Use C. latirostris as a Sentinel of Pesticide Contamination? 200 11.2.1 Evidence of Pesticide Effects on the Broad-snouted Caiman 200 11.2.2 Identification and Development of Gene Expression Markers 202 11.3 Future Perspectives 209 Acknowledgements 209 References 209 Chapter 12 Epilogue and Final Remarks 217 Guillermo Eli Liwszyc and Marcelo L. Larramendy Reference 226 Subject Index 227
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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.
At a symposium, which has been considered as a landmark in environmental concerns, held at the Institute for Terrestrial Ecology in 1965 the following statements on behavioral toxicology were made (Warner et al. 1966): (1) “The behavior (or activities) of an organism represents the final integrated result of a diversity of biochemical and physiological processes. Thus, a single behavioral parameter is generally more comprehensive than a physiological or biochemical parameter. (2) Behavioral patterns are known to be highly sensitive to changes in the steady state of an organism. This sensitivity is one of the key values for its use in exploring sublethal toxicity. (3) Behavioral measurements can usually be made without direct physical harm to the organism. With aquatic animals especially, implantation of detectors introduces problems of considerable complexity. Behavioral measurements can avoid this difficulty.”
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.
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.
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 LC 50 (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.
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
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.