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First national-scale reconnaissance of neonicotinoid insecticides in streams across the USA

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To better understand the fate and transport of neonicotinoid insecticides, water samples were collected from streams across the United States. In a nationwide study, at least one neonicotinoid was detected in 53% of the samples collected, with imidacloprid detected most frequently (37 %), followed by clothianidin (24 %), thiamethoxam (21 %), dinotefuran (13 %), acetamiprid (3 %) and thiacloprid (0 %). Clothianidin and thiamethoxam concentrations were positively related to the percentage of the land use in cultivated crop production and imidacloprid concentrations were positively related to the percentage of urban area within the basin. Additional sampling was also conducted in targeted research areas to complement these national-scale results, including determining: (1) neonicotinoid concentrations during elevated flow conditions in an intensely agricultural region; (2) temporal patterns of neonicotinoids in heavily urbanised basins; (3) neonicotinoid concentrations in agricultural basins in a nationally important ecosystem; and (4) in-stream transport of neonicotinoids near a wastewater treatment plant. Across all study areas, at least one neonicotinoid was detected in 63% of the 48 streams sampled.
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First national-scale reconnaissance of neonicotinoid
insecticides in streams across the USA
Michelle L. Hladik
A
,
C
and Dana W. Kolpin
B
A
US Geological Survey, California Water Science Center, 6000 J Street, Placer Hall, Sacramento,
CA 95819, USA.
B
US Geological Survey, Iowa Water Science Center, 400 S. Clinton Street, Iowa City, IA 52240,
USA; dwkolpin@usgs.gov
C
Corresponding author. Email address: mhladik@usgs.gov
Environmental context. Neonicotinoids are under increased scrutiny because they have been implicated in
pollinator declines and, more recently, as potential aquatic toxicants. Nevertheless, there is currently little
information on concentrations of multiple neonicotinoids in surface water. This paper presents a summary of
concentrations of six neonicotinoids in streams from across the United States in both urban and agricultural
areas. These environmental data are important in determining the potential risk of neonicotinoids to non-target
aquatic and terrestrial organisms.
Abstract. To better understand the fate and transport of neonicotinoid insecticides, water samples were collected from
streams across the United States. In a nationwide study, at least one neonicotinoid was detected in 53 % of the samples
collected, with imidacloprid detected most frequently (37 %), followed by clothianidin (24 %), thiamethoxam (21 %),
dinotefuran (13 %), acetamiprid (3 %) and thiacloprid (0 %). Clothianidin and thiamethoxam concentrations were
positively related to the percentage of the land use in cultivated crop production and imidacloprid concentrations were
positively related to the percentage of urban area within the basin. Additional sampling was also conducted in targeted
research areas to complement these national-scale results, including determining: (1) neonicotinoid concentrations during
elevated flow conditions in an intensely agricultural region; (2) temporal patterns of neonicotinoids in heavily urbanised
basins; (3) neonicotinoid concentrations in agricultural basins in a nationally important ecosystem; and (4) in-stream
transport of neonicotinoids near a wastewater treatment plant. Across all study areas, at least one neonicotinoid was
detected in 63 % of the 48 streams sampled.
Received 21 March 2015, accepted 15 April 2015, published online 18 August 2015
Introduction
There is increasing concern about neonicotinoid insecticides
not only to pollinators
[1]
but also to other organisms such as
those residing in aquatic environments.
[2]
Elevated surface-
water concentrations of imidacloprid have been correlated with
direct effects on invertebrates
[3]
and indirect effects on insec-
tivorous birds
[4]
and some fish.
[5]
Recent research has focussed
on not only acute toxicity of neonicotinoids but also chronic
toxicity, especially to aquatic invertebrates that may be exposed
to neonicotinoids by water.
[2]
Neonicotinoid use has continued to increase both in the
United States
[6,7]
and worldwide.
[8,9]
They are applied in
both agricultural (foliar sprays, in-furrow treatments and
seed coatings) and urban (lawn and garden foliar sprays,
granular, tree injections; companion animal flea treatment)
settings. Neonicotinoids are highly water-soluble (octanol–
water partition coefficients, log K
ow
, range from 0.55
to 1.26)
[10]
with fairly long soil degradation half-lives
(DT
50
3 to 545 days),
[10]
making them both mobile and
persistent with the potential for offsite transport to adjacent
water bodies.
[11,12]
The lack of surface-water data is considered an important
knowledge gap for neonicotinoids.
[13]
This information is
needed to accurately assess potential environmental effects from
neonicotinoid exposures from stream concentrations. Current
surface-water data exist primarily for imidacloprid, the mostly
widely use neonicotinoid globally.
[8]
More recent studies, how-
ever, have documented mixtures of neonicotinoids in wet-
lands,
[1416]
groundwater
[12]
and surface water.
[11,1719]
An
example of such research documented that neonicotinoid mix-
tures were prevalent in streams in the Midwestern US, even in
the largest systems (i.e. Missouri and Mississippi Rivers), with
substantial temporal pulses of neonicotinoids in streams follow-
ing rainfall events during crop planting likely attributed to seed
treatment applications.
[11]
The current study provides the first national-scale assess-
ment of neonicotinoids in USA streams that has been con-
ducted to date. In addition, targeted research studies were
conducted to complement these national-scale results to
enhance our understanding of the contributions of both agri-
cultural and urban neonicotinoid use to stream concentrations.
Such national- and regional-scale data sets provide important
geographic and temporal data that can be used to provide
important baseline concentration information for determining
potential environmental effects from exposure to stream neo-
nicotinoid concentrations.
CSIRO PUBLISHING
Environ. Chem.
http://dx.doi.org/10.1071/EN15061
Journal compilation ÓCSIRO 2015 www.publish.csiro.au/journals/envA
Research Paper
Experimental
Sampling
National study
To obtain the first nationwide data set on neonicotinoids, 38
streams across 24 US states and Puerto Rico were sampled one
time for neonicotinoids between November 2012 and June 2014
(Fig. 1; Table S1). These samples were collected as part of larger
project to assess the human and ecological health risks associated
with exposure to complex chemical mixtures.
[20]
Thirty-four of
the streams were specifically selected owing to a wide range of
contaminant sources within their watersheds (e.g. agricultural and
urban sources). In addition, four streams were selected as
biological reference sites because they are considered to have
fish and aquatic macroinvertebrate communities that have been
minimallydisturbed by human development. The sampled water-
sheds range in size from12 to 16 200 km
2
(median ¼170 km
2
).
[20]
All water samples were collected from the centroid of flow.
Additional information on the site characteristics can be found
in Table S1.
Streams during elevated hydrologic conditions:
Iowa, 2014
To determine neonicotinoid concentrations in streams during
elevated hydrologic conditions in an intensely agricultural
region, grab samples from six sites in Iowa (Table 1;Fig. 2a)
Nationwide study site
Targeted research site
0 250
Explanation
Puerto Rico
0 250 500 km
500 miles
Fig. 1. Map showing sample locations for the nationwide study (2012–14) and targeted research studies
(2011–14).
Table 1. Site information, neonicotinoid concentrations and instantaneous loads for samples collected from Iowa stream and rivers after heavy rains
and flooding in 2014
Samples collected in 2013 for these sites are also included
Site USGS
site ID
Drainage
area
(km
2
)
Date Discharge
(m
3
s
1
)
Clothianidin
(ng L
1
)
Imidacloprid
(ng L
1
)
Thiamethoxam
(ng L
1
)
Total
neonicotinoid
load (g s
1
)
Missouri River at Omaha, NE 06610000 836 000 19-Jun-13 1150 18 4.4 11 0.038
18-Jun-14 2080 25 11 18 0.11
North Fork Maquoketa River
near Fulton, IA
05418400 1310 24-Jun-13 28 74 4.8 40 0.003
19-Jun-14 77 98 11 40 0.011
Old Mans Creek near Iowa City,
IA
05455100 521 26-Jun-13 36 84 23 26 0.005
01-Jul-14 157 68 25 20 0.018
Iowa River at Wapello, IA 05465500 32 400 01-Jul-13 1420 62 15 30 0.15
03-Jul-14 3030 53 19 20 0.28
Big Sioux River at Sioux City, IA 06485950 24 400 20-Jun-14 1821 77 20 38 0.25
Turkey River at Garber, IA 05412500 4000 20-Jun-14 708 132 26 73 0.16
M. L. Hladik and D. W. Kolpin
B
were collected from the centroid of flow following heavy
rainfall and after most row crops (corn and soybeans) had been
planted in these watersheds. Four out of the six sites were above
flood stage and all samples were collected near the crest of the
hydrograph. The drainage area for the basins sampled ranged
from 521 to 836 000 km
2
.
Temporal patterns in urban streams in the Southeast
Two urban-affected streams (Sope Creek, 80 km
2
,39%
urban; Chattahoochee River, 6300 km
2
, 18 % urban) were
frequently sampled (67 total samples) in Georgia to better
understand temporal variations in stream neonicotinoid con-
centrations derived from urban sources (Fig. 2b). All water
samples from these sites were collected through depth and
width-integrated composites.
[19,21]
Samples were collected
from Sope Creek every 2 weeks on a set schedule for 2 years
starting in October 2011 (48 samples collected). Samples were
collected from the Chattahoochee River on an alternating once
or twice per month set schedule (19 samples collected). No
samples from these two sites were collected in relation to any
specific flow conditions.
Streams in a nationally important ecosystem:
Chesapeake Bay
As part of a larger study to determine if chemical exposure is
contributing to fish health issues being observed in the Chesa-
peake Bay watershed,
[2224]
water samples were collected from
three sites in this watershed (Fig. 2c): six samples from Antietam
Creek (725 km
2
, 25 % cultivated crops, 10 % urban); seven
samples from Big Pipe Creek (270 km
2
, 41 % cultivated crops,
2 % urban); and four samples from Chillisquaque Creek,
(290 km
2
, 32 % cultivated crops, 2 % urban). Automatic sam-
plers were used to collect water.
In-stream transport: Fourmile Creek, Iowa
To better understand the contributions of neonicotinoids to
streams from wastewater treatment plant (WWTP) discharge
and their in-stream fate, a 4.8-km reach of Fourmile Creek,
located near Ankeny, Iowa, was investigated (Fig. 2a). The
study reach extends from 1.9 km above the WWTP outfall
(46 10
6
L day
1
; activated sludge treatment) to 2.9 km down-
stream of the WWTP outfall. In addition to a WWTP effluent
sample, stream samples were collected at 1.9, 1.6, 0.08,
0.05, 0.05, 0.33 and 2.9-km distance in relation to WWTP
outfall. Samples were collected in a Lagrangian approach, in
which the same approximate parcel of water was tracked as it
moved downstream, as was conducted previously in this study
reach.
[2527]
All samples were collected at the centroid of flow.
The proportion of stream flow derived from WWTP effluent
below the outfall varies depending on antecedent moisture
conditions. The first sampling of this study reach occurred from
5 to 6 December 2012 during a time of prolonged drought
conditions. Thus, the stream flow below the outfall was
0.17 m
3
s
1
, with 99 % of this flow derived from effluent. The
second sampling occurred on 20 June 2013 during more normal
early-summer flow conditions, with the stream flow below the
outfall at 1.7 m
3
s
1
, with 11 % of this flow derived from
effluent.
Analytical method
All samples were placed in 1-L amber glass bottles and chilled at
48C until extraction. The six neonicotinoids (acetamiprid,
clothianidin, dinotefuran, imidacloprid, thiacloprid and thia-
methoxam) were measured in the water samples using a previ-
ously published method.
[19]
Samples were filtered with a
0.7-mm glass-fibre filter (Whatman, Piscataway, NJ), spiked
with a surrogate (imidacloprid-d
4
; Cambridge Isotope,
Andover, MA), and passed through an Oasis HLB solid-phase
Turkey River
Big Sioux River North Fork Maquoketa River
Fourmile Creek
Missouri River
Sope Creek
Chattahoochee River
Chillisquaque Creek
Antietam Creek
Chesapeake Bay
Big Pipe Creek
Iowa River
Old Mans Creek
Targeted research site
Explanation
km
miles03060
03060
Targeted research site
Explanation
km
miles03060
03060
Targeted research site
Explanation
km
miles03060
03060
Fig. 2. Sites sampled as part of targeted research studies: elevated
hydrologic conditions and in-stream transport in an intense agricultural
region in Iowa (a); urban streams in the south-eastern USA (b); and
Chesapeake Bay (c).
Neonicotinoids in US surface water
C
extraction (SPE) cartridge (6 mL, 500 mg; Waters Corporation,
Milford, MA). The cartridge was eluted with 10 mL of 50 : 50
dichloromethane : acetone, reduced under nitrogen and an
internal standard,
13
C
3
-caffeine, was then added. Extracts were
analysed on an Agilent 1260 bio-inert liquid chromatograph
(LC) coupled to an Agilent 6430 tandem mass spectrometer
(MS-MS) (Santa Clara, CA). The theoretical level of detection
(LOD) was 2 ng L
1
and the method detection limits (MDL)
ranged from 3.6 to 6.2 ng L
1
.
[19]
Neonicotinoid concentrations were validated against a set of
quality control parameters including: field blanks (9), replicate
samples (17), matrix spikes (8) and surrogate recovery. No
compounds were detected in any of the blanks, field replicates
had relative percentage differences (RPD) between the regular
and replicate sample of ,25 %. Matrix spike recoveries ranged
from 70 to 102 %. Recovery of the surrogate (imidacloprid-d
4
)
ranged from 70 to 120 % for all samples; data presented here
were not recovery-corrected.
Results and discussion
A total of 149 stream samples were collected and analysed for
six neonicotinoids in one national-scale and four complemen-
tary research studies. A summary of the results of these efforts
follows.
National study
Five of the six neonicotinoids measured were detected in this
first ever national-scale study (Table S1). Although these sam-
ples represent only a single snapshot in time for the 38 sites
sampled, they do represent spatial variations in stream neoni-
cotinoid concentrations across the USA (Fig. 1). At least one
neonicotinoid was detected in 53 % of the 38 sites sampled.
Imidacloprid was the most frequently detected neonicotinoid
(37 %, maximum concentration 140 ng L
1
), followed by clo-
thianidin (24 %, 66 ng L
1
), thiamethoxam (21 %, 190 ng L
1
),
dinotefuran (13 %, 130 ng L
1
) and acetamiprid (3 %, 40 ng L
1
)
(Fig. 3, Table S1). Thiacloprid was not detected in any of the
samples collected. Of the 37 detectable concentrations of indi-
vidual neonicotinoids, 92 % were ,100 ng L
1
with the median
detected concentration of 19 ng L
1
. When summed, the highest
total neonicotinoid concentration for a given sample was 450 ng
L
1
(Fig. 4). Mixtures of multiple neonicotinoids in a single
sample were common; two or more were detected in 26 % of the
samples, three or more were detected in 11 % of the samples, and
one sample (3 %) had five neonicotinoids detected (Table S1).
To provide a better understanding of neonicotinoid sources,
an examination of the relationship between concentration and
land-use (Table S1) was conducted (Table S2). This analysis
determined a significant, positive relation (using Spearman’s
rank correlation) to cultivated crops for clothianidin (r¼0.465,
P¼0.003) and thiamethoxam (r¼0.472, P¼0.003) and a
positive relation to urban land-use for imidacloprid (r¼0.474,
P¼0.003). These were expected relations to land-use based on
the primary use of these neonicotinoids. In addition, a signifi-
cant positive relation was observed between the two principal
agriculturally used neonicotinoids, clothianidin and thia-
methoxam (r¼0.668, P,0.001). Their co-occurrence can at
least partially be explained by the fact that both neonicotinoids
Imidacloprid
37 %
Clothianidin
24 %
Thiamethoxam
21 %
Dinotefuran
13 %
Acetamiprid
3 %
0
50
100
150
200
Concentration (ng L1)
1
10
100
Sum of
Neonicotinoids
Fig. 3. Box plot of total neonicotinoids detected at 38 sites in a nationwide study from 2012 to 2014. Scatterplots show the
range of individual neonicotinoid concentrations for the five compounds detected (out of six measured); overall detection
frequency is listed underneath the compound names.
Site
5101520253035
Total neonicotinoid concentration (ng L1)
0
100
200
300
400 Imidacloprid
Clothianidin
Thiamethoxam
Dinotefuran
Acetamiprid
Fig. 4. Concentrations of neonicotinoid insecticides at 38 individual sites
collected as part nationwide study from 2012 to 2014. The site number
corresponds to the full names given in Table S1.
M. L. Hladik and D. W. Kolpin
D
are primarily used on cultivated crops and that clothianidin is
also a transformation product of thiamethoxam.
[7,28]
There were
no significant relations among the other neonicotinoids under
investigation (Table S2).
Streams during elevated flow conditions: Iowa, 2014
Because of the generally wet conditions across much of Iowa
during the spring and early summer of 2014, a set of water
samples from six sites were collected (Fig. 2a) to determine the
effect such elevated flow conditions would have on stream
neonicotinoid concentrations in an intensely agricultural region.
Neonicotinoids were present in all six samples collected
(Table 1). These 2014 results were similar to those collected
during this same general time period in 2013
[11]
; median indi-
vidual neonicotinoid concentration was 23 ng L
1
in 2014 and
25 ng L
1
in 2013 for sites with samples collected during both
years. Although stream concentrations were similar between
2013 and 2014, the wet conditions in 2014 did cause substan-
tially higher stream flows compared with 2013, which translated
to higher instantaneous neonicotinoid loads (Table 1); thus,
neonicotinoid loads were two to four times higher in 2014 than
in 2013. These results confirm that precipitation is an important
driver of neonicotinoid transport to streams following periods of
use; even when such precipitation is heavy enough to cause
substantial stream flooding, the neonicotinoid concentrations
were not reduced.
Temporal patterns in urban streams in the Southeast
For this research component, stream samples were collected
from two urban-affected streams (Fig. 2b): Sope Creek and the
Chattahoochee River on a fixed sampling schedule. Not sur-
prisingly, imidacloprid was the dominant neonicotinoid present
Chattahoochee River near Whitesburg, GA
2011
Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct
Total neonicotinoid concentration (ng L1)
0
20
40
60
80
100
120
140
Dischar
g
e (m3 s1)
1
10
100
1000
Imidacloprid
Dinotefuran
Acetamiprid
2012
Sope Creek near Marietta, GA
2012
Oct Jan Apr Jul Oct Jan Apr Jul Oct
imidacloprid concentration (ng L1)
0
20
40
60
80
100
(a)
(b)
0.01
0.1
1
10
100
Imidacloprid
2013 2011
Fig. 5. Concentrations of imidacloprid and the corresponding stream discharge from October 2011 to
October 2013 for Sope Creek (a). Concentrations of imidacloprid, dinotefuran and acetamiprid along with
the corresponding stream discharge from September 2011 to September 2012 for Chattahoochee River (b).
Black bars represent samples where no neonicotinoids were detected.
Neonicotinoids in US surface water
E
in these urban-affected streams, being detected in 87 % of 67
samples collected. Dinotefuran (10 %) and acetamiprid (7 %)
were detected sporadically and were found along with imida-
cloprid (Table S3).
Imidacloprid was present in almost every sample (90 %)
collected from the heavily urbanised Sope Creek (39 % urban)
(Fig. 5a). Unlike what has been observed in agricultural streams
in the Midwest,
[11]
there was no significant relation between
imidacloprid concentrations and stream flow (r¼0.21,
P¼0.17). This may have been at least partially due to the lack
of a distinct use period for imidacloprid in such an urban-
affected basin and the lack of a distinct growing season in the
warmer climate of the south-eastern United States. In addition,
the frequent events (e.g. frequent flushing of the system)
observed in Sope Creek (Fig. 5a) and the warmer climate
(possibly leading to increased degradation rates) may also have
contributed to differences when comparing these urban-affected
results with agricultural areas of the Midwest.
For the Chattahoochee River, which includes the Sope Creek
drainage, one or more neonicotinoids were detected in 79 % of
samples, two or more in 37 %, and three or more in 16 % of the
samples collected. Imidacloprid was the most frequently
detected neonicotinoid (79 %), followed by dinotefuran (32 %)
and acetamiprid (5 %; Table S3). The more varied neonicotinoid
detections in the Chattahoochee River compared with Sope
Creek were likely a reflection of the more diverse land-use
because the larger Chattahoochee watershed is 18 % urban and
includes 9 % pasture (no cultivated crops, however). As with
Sope Creek, there were frequent runoff events (Fig. 5b), with no
significant relation between imidacloprid concentrations and
stream flow (r¼0.05, P,0.87).
Streams in a nationally important ecosystem:
Chesapeake Bay
For this research component, stream samples were collected
from three agriculturally affected streams (Fig. 2c): Antietam
Creek, Big Pipe Creek and Chillisquaque Creek, with a specific
emphasis on collection of runoff samples during the planting
season of cultivated crops. Overall, neonicotinoids were
detected in 59 % of the stream samples. Clothianidin was the
most frequently detected neonicotinoid (59 %), followed by
thiamethoxam (29 %), and imidacloprid (6 %) (Table S4,
Fig. 6). The thiamethoxam and imidacloprid detections were all
found in the presence of clothianidin.
Similar to previous research on agricultural streams in the
Midwestern USA,
[11]
an increase in neonicotinoid concentra-
tions was observed in these streams during runoff conditions
associated with the planting season of cultivated crops (Fig. 6).
Although there were not enough samples to test statistically, the
concentrations of clothianidin and thiamethoxam (the two
neonicotinoids primarily used for agricultural purposes) gener-
ally increased as the amount of land used in cultivated crops
increased. The highest concentrations for each site occurred on
16 May 2014 and sites ranked the same with respect to percent-
age cultivated crops and clothianidin plus thiamethoxam con-
centration: Big Pipe Creek (41 %; 93 ng L
1
).Chillisquaque
Creek (32 %; 64 ng L
1
).Antietam Creek (21 %; 11 ng L
1
).
The measurement of neonicotinoids is one component in deter-
mining if chemical exposures are contributing to fish health
issues being observed in the Chesapeake Bay watershed. Future
work will seek to determine the relative effects from various
chemicals (e.g. neonicotinoids) and additive or synergistic
effects from chemical mixtures (e.g. pesticides, hormones,
pharmaceuticals) on fish health.
In-stream transport: Fourmile Creek, Iowa
The two different sampling events of the 4.8-km study reach for
this research component captured two vastly different WWTP-
derived flow scenarios (99.5 and 11.0 % flow-derived effluent
below the WWTP). The December 2012 sampling occurred
during a time of prolonged drought conditions and months after
any agricultural use of neonicotinoids had taken place. Thus, the
flow of Fourmile Creek below the WWTP outfall was 99 %
effluent at this time. Only imidacloprid and clothianidin were
detected during this December sampling (Table S5). During this
time, the input of WWTP effluent into Fourmile Creek caused an
increase in stream concentration for imidacloprid and a decrease
Antietam Creek near Sharpsburg, MD
Apr May Jun
0
5
10
15
20
25
1
10
100
Clothianidin
Thiamethoxam
(a)
(b)
(c)
Big Pipe Creek at Bruceville, MD
Apr May Jun
Total neonicotinoid concentration (ng L1)
0
50
100
150
Dischar
g
e (m3 s1)
0.1
1
10
100
Clothianidin
Thiamethoxam
Chillisquaque Creek at Chillisquaque, PA
2014
Apr May Jun
0
50
100
150
200
0.1
1
10
100
Clothianidin
Imidacloprid
Thiamethoxam
Fig. 6. Concentrations of clothianidin, imidacloprid and thiamethoxam
and the corresponding stream discharge at three sites in the Chesapeake Bay
area sampled in 2014. Black bars represent samples where no neonicotinoids
were detected.
M. L. Hladik and D. W. Kolpin
F
in stream concentration for clothianidin (Fig. 7). This trend was
not unexpected owing to the primary uses for these neonicoti-
noids (i.e. agricultural use for clothianidin and urban use for
imidacloprid). These neonicotinoids appear to be transported
conservatively through this study reach because similar con-
centrations were found from the uppermost sampling point to
just above the WWTP outfall and from just below the WWTP
outfall to the lowermost sampling point (Fig. 7).
The June 2013 sampling occurred during a time of normal,
early-summer flow conditions (i.e. median flow) and soon after
the primary period of the agricultural use of neonicotinoids had
taken place in the headwaters. Correspondingly, the flow of
Fourmile Creek below the WWTP outfall was 11 % effluent at
this time. During this sampling, clothianidin, imidacloprid and
thiamethoxam were detected (Table S5). Given the strong
agricultural use for clothianidin and thiamethoxam, the higher
stream concentrations in the upper portion of the reach, derived
from row-crop production in the headwaters, compared with that
observed during the December 2012 sampling were expected.
As was observed previously, only clothianidin and imidacloprid
were detected in the WWTP effluent, with clothianidin being
present at lower concentrations than imidacloprid. In addition,
the input of WWTP effluent into Fourmile Creek again caused
an increase in stream concentrations for imidacloprid and a
slight decrease in stream concentrations for clothianidin (Fig. 7).
This trend, however, was dampened by the much lower influ-
ence of the WWTP on stream flow below the outfall (11 %
effluent-derived stream flow) compared with the December
Clothianidin
Imidacloprid
December 2012 June 2013
Fig. 7. Concentrations (ng L
1
) of clothianidin and imidacloprid collected along Fourmile Creek near
Ankeny, Iowa, at two sampling times, December 2012 and June 2013. The concentrations in red are those
found at the outfall of the wastewater treatment plant (WWTP).
Neonicotinoids in US surface water
G
2012 sampling (99 % effluent-derived stream flow). As with the
December sampling, conservative transport of neonicotinoids
was observed, with similar concentrations from the uppermost
sampling point to just above the WWTP outfall and from just
below the WWTP outfall to the lowermost sampling point
(Fig. 7).
Summary
In this first wide-scale investigation of neonicotinoids, they were
frequently detected in streams across the USA, with 63 % of the
48 streams samples having a detection of at least one neonicoti-
noid. Both urban and agricultural uses contributed to stream
neonicotinoid concentrations, with imidacloprid occurrence
significantly related to the amount of urban land-use and clo-
thianidin and thiamethoxam significantly related to the amount of
cultivated crops. Similarly to previous research, transport to
streams in agriculturally affected basins is driven by use and
precipitation. The present study,however, has documented this to
be true even when precipitation is heavy enough to cause sub-
stantial flooding. Research within a 4.8-km study reach of
Fourmile Creek found that the input of WWTP effluent into the
system caused stream concentrations of imidacloprid to increase
and clothianidin to decrease. Both neonicotinoids, however,
were found to be transported conservatively throughout the
study reach. Although the present research provides important
baseline data on neonicotinoid concentrations in streams and
helps expand our understanding of their sources and environ-
mental fate, more research is needed to understand the potential
direct effects to aquatic organisms and indirect effects to both
aquatic and terrestrial organisms from these stream neonicoti-
noid concentrations.
Acknowledgements
We thank Dan Calhoun and Pat Phillips for providing samples and site
information for Georgia and Chesapeake Bay respectively; Jim Orlando for
generating maps and the land-use data; Megan McWayne and Corey Sanders
for sample processing; and all of the field crews from across the United
States who collected the various stream samples. Funding or support was
provided by the US Geological Survey (USGS) Toxic Substances Hydrology
Program, USGS Priority Ecosystems Science, USGS National Water
Quality Assessment Program and the Georgia Department of Agriculture.
Any use of trade, firm or product names is for descriptive purposes only and
does not imply endorsement by the US Government.
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Neonicotinoids in US surface water
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Since their discovery in the late 1980s, neonicotinoid pesticides have become the most widely used class of insecticides worldwide, with large-scale applications ranging from plant protection (crops, vegetables, fruits), veterinary products, and biocides to invertebrate pest control in fish farming. In this review, we address the phenyl-pyrazole fipronil together with neonicotinoids because of similarities in their toxicity, physicochemical profiles, and presence in the environment. Neonicotinoids and fipronil currently account for approximately one third of the world insecticide market; the annual world production of the archetype neonicotinoid, imidacloprid, was estimated to be ca. 20,000 tonnes active substance in 2010. There were several reasons for the initial success of neonicotinoids and fipronil: (1) there was no known pesticide resistance in target pests, mainly because of their recent development, (2) their physicochemical properties included many advantages over previous generations of insecticides (i.e., organophosphates, carbamates, pyrethroids, etc.), and (3) they shared an assumed reduced operator and consumer risk. Due to their systemic nature, they are taken up by the roots or leaves and translocated to all parts of the plant, which, in turn, makes them effectively toxic to herbivorous insects. The toxicity persists for a variable period of time — depending on the plant, its growth stage, and the amount of pesticide applied. Awide variety of applications are available, including the most common prophylactic non-Good Agricultural Practices (GAP) application by seed coating. As a result of their extensive use and physicochemical properties, these substances can be found in all environmental compartments including soil, water, and air. Neonicotinoids and fipronil operate by disrupting neural transmission in the central nervous system of invertebrates. Neonicotinoids mimic the action of neurotransmitters, while fipronil inhibits neuronal receptors. In doing so, they continuously stimulate neurons leading ultimately to death of target invertebrates. Like virtually all insecticides, they can also have lethal and sublethal impacts on non-target organisms, including insect predators and vertebrates. Furthermore, a range of synergistic effects with other stressors have been documented. Here, we review extensively their metabolic pathways, showing how they form both compound-specific and common metabolites which can themselves be toxic. These may result in prolonged toxicity. Considering their wide commercial expansion, mode of action, the systemic properties in plants, persistence and environmental fate, coupled with limited information about the toxicity profiles of these compounds and their metabolites, neonicotinoids and fipronil may entail significant risks to the environment. A global evaluation of the potential collateral effects of their use is therefore timely. The present paper and subsequent chapters in this review of the global literature explore these risks and show a growing body of evidence that persistent, low concentrations of these insecticides pose serious risks of undesirable environmental impacts.
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We assessed the state of knowledge regarding the effects of large-scale pollution with neonicotinoid insecticides and fipronil on non-target invertebrate species of terrestrial, freshwater and marine environments. A large section of the assessment is dedicated to the state of knowledge on sublethal effects on honeybees (Apis mellifera) because this important pollinator is the most studied non-target invertebrate species. Lepidoptera (butterflies and moths), Lumbricidae (earth-worms), Apoidae sensu lato (bumblebees, solitary bees) and the section "other invertebrates" review available studies on the other terrestrial species. The sections on freshwater and marine species are rather short as little is known so far about the impact of neonicotinoid insecticides and fipronil on the diverse invertebrate fauna of these widely exposed habitats. For terrestrial and aquatic invertebrate species, the known effects of neonicotinoid pesticides and fipronil are described ranging from organismal toxicology and behavioural effects to population-level effects. For earthworms, freshwater and marine species, the relation of findings to regulatory risk assessment is described. Neonicotinoid insecticides exhibit very high toxicity to a wide range of invertebrates, particularly insects, and field-realistic exposure is likely to result in both lethal and a broad range of important sublethal impacts. There is a major knowledge gap regarding impacts on the grand majority of invertebrates, many of which perform essential roles enabling healthy ecosystem functioning. The data on the few non-target species on which field tests have been performed are limited by major flaws in the outdated test protocols. Despite large knowledge gaps and uncertainties, enough knowledge exists to conclude that existing levels of pollution with neonicotinoids and fipronil resulting from presently authorized uses frequently exceed the lowest observed adverse effect concentrations and are thus likely to have large-scale and wide ranging negative biological and ecological impacts on a wide range of non-target invertebrates in terrestrial, aquatic, marine and benthic habitats.
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Developed to replace organophosphate and carbamate insecticides, neonicotinoids are structurally similar to nicotine. The three main neonicotinoid insecticides, imidacloprid, clothianidin, and thiamethoxam, are being re-evaluated by Health Canada's Pest Management Regulatory Agency (PMRA). An important aspect of the re-evaluation is the potential for effects in non-target organisms, including aquatic organisms. Leaching into surface waters is one of the major concerns surrounding extensive use of neonicotinoids, especially in close proximity to water bodies. The PMRA has classified IMI as ‘persistent’ with a ‘high’ leaching potential. Globally, neonicotinoids have been detected in a variety of water bodies, typically at concentrations in the low μg/L range. While IMI has been included in some monitoring exercises, there are currently very few published data for the presence of CLO and THM in Canadian water bodies. The majority of neonicotinoid toxicity studies have been conducted with IMI due to its longer presence on the market and high prevalence of use. Aquatic insects are particularly vulnerable to neonicotinoids and chronic toxicity has been observed at concentrations of IMI below 1 μg/L. Acute toxicity has been reported at concentrations below 20 μg/L for the most sensitive species, including Hyalella azteca, ostracods, and Chironomus riparius. Fish, algae, amphibians, and molluscs are relatively insensitive to IMI. However, the biological effects of THM and CLO have not been as well explored. The Canadian interim water quality guideline for IMI is 0.23 μg/L, but there is currently insufficient use, fate, and toxicological information available to establish guidelines for CLO and THM. Based on concentrations of neonicotinoids reported in surface waters in Canada and globally, there is potential for aquatic invertebrates to be negatively impacted by neonicotinoids. Therefore, it is necessary to address knowledge gaps to inform decisions around guidelines and registration status for neonicotinoid insecticides in Canada to protect our aquatic ecosystems.
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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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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.