Article

A large-scale survey of house sparrows feathers reveals ubiquitous presence of neonicotinoids in farmlands

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Abstract

The massive use of neonicotinoid insecticides has been repeatedly incriminated for their impacts to avian populations. Some studies have reported contamination of granivorous birds by neonicotinoids but very little is known about exposure to neonicotinoids in other bird species. To fill this lack of knowledge, we trapped house sparrows Passer domesticus, an omnivorous bird whose diet is composed of both grains and insects, and we collected 617 feathers from individuals living on 47 conventional, integrated-production (IP-Suisse) and organic farms distributed all over the Swiss plateau, the country's main agricultural area. We then assessed the concentration of five neonicotinoids in 146 pools of feathers. We found that all feather samples were contaminated by at least one neonicotinoid at measurable concentration (>LOQ), with thiacloprid accounting for most of the prevalence (99%), while clothianidin was found at highest concentrations (with averages ranging from 1.68 to 9.2 ppb). Additionally, house sparrows living on conventional farms showed higher concentrations of neonicotinoids (15.26 ± 3.58 ppb) than individuals living on IP-Suisse (3.38 ± 0.86 ppb), and organic farms (2.59 ± 0.56 ppb). Our large-scale survey highlights how ubiquitous neonicotinoid insecticides have become in agricultural habitats, and reveals generalized exposure of house sparrows, and potentially other species inhabiting farmlands, to neonicotinoids.

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... Only three studies have measured concentrations of NNs in avian plasma: two in raptor species (Byholm et al., 2018;Taliansky-Chamudis et al., 2017), and one in a songbird species (Hao et al., 2018), with 38 out of 76 individuals testing positive for NNs across the three separate datasets. Most recently, a large study in Switzerland measured NN concentrations in the feathers of house sparrows Passer domesticus and found 100% prevalence of NNs (consisting of five compounds) in 146 pooled samples collected from 62 farms across the Swiss plateau (Humann-Guilleminot et al., 2019a). ...
... composition to that in Roy et al. (2019), and 12 of the 30 species observed consuming seeds treated with pesticides in a previous study conducted in Spain (Lopez-Antia et al., 2016). This included multiple sparrow species, such as house sparrow, which have also been reported to be extensively exposed to NNs across the Swiss plateau (Humann-Guilleminot et al., 2019a). Overall exposure was not limited to any specific species ecology or taxonomy, other than that the majority of species exposed are known to have cereal grain in their diet (Table S3) (Cramp, 1985). ...
... The prevalence of CLO residues in plasma samples collected postsowing (~50%) was broadly similar to that reported previously; of the three other studies that have measured NN residue in plasma samples collected from wild birds, positive samples accounted for 3% (n = 30 bird of prey samples), 60% (n = 10 bird of prey samples) and 80% (n = 36 passerine samples) of the total sample size (Byholm et al., 2018;Taliansky-Chamudis et al., 2017;Hao et al., 2018). Comparatively, Humann-Guilleminot et al. reported 100% prevalence of NN residue in 146 pooled house sparrow feather samples (each pool contained one feather from three individuals) (Humann-Guilleminot et al., 2019a). When comparing these data, differences in sample type, time of sampling (in relation to exposure) and the ecology of the species investigated are all likely to explain the observed variation between studies. ...
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Neonicotinoids are the largest group of systemic insecticides worldwide and are most commonly applied as agricultural seed treatments. However, little is known about the extent to which farmland birds are exposed to these compounds during standard agricultural practices. This study uses winter cereal, treated with the neonicotinoid clothianidin, as a test system to examine patterns of exposure in farmland birds during a typical sowing period. The availability of neonicotinoid-treated seed was recorded post-sowing at 39 fields (25 farms), and camera traps were used to monitor seed consumption by wild birds in situ. The concentration of clothianidin in treated seeds and crop seedlings was measured via liquid chromatography-tandem mass spectrometry, and avian blood samples were collected from 11 species of farmland bird from a further six capture sites to quantify the prevalence and level of clothianidin exposure associated with seed treatments. Neonicotinoid-treated seeds were found on the soil surface at all but one of the fields surveyed at an average density of 2.8 seeds/m². The concentration of clothianidin in seeds varied around the target application rate, whilst crop seedlings contained on average 5.9% of the clothianidin measured in seeds. Exposure was confirmed in 32% of bird species observed in treated fields and 50% of individual birds post-sowing; the median concentration recorded in positive samples was 12 ng/mL. Results here provide clear evidence that a variety of farmland birds are subject to neonicotinoid exposure following normal agricultural sowing of neonicotinoid-treated cereal seed. Furthermore, the widespread availability of seeds at the soil surface was identified as a primary source of exposure. Overall, these data are likely to have global implications for bird species and current agricultural policies where neonicotinoids are in use, and may be pertinent to any future risk assessments for systemic insecticide seed treatments.
... Our results revealed that seabirds with different trophic habits are exposed to neonicotinoids and provide further evidence that not only granivorous, nectar-sucking, and insectivorous species may be affected by neonicotinoid contamination. Recent studies evidenced that residues of neonicotinoids may also be detected in not-strictly granivorous birds (Humann-Guilleminot et al., 2019a;Lennon et al., 2020) and birds of prey (Byholm et al., 2018;Humann-Guilleminot et al., 2021). In particular, studies performed in Swiss farmland and non-agricultural areas outlined the occurrence of neonicotinoid residues in feathers of adult house sparrows (Passer domesticus), nestlings of Alpine swifts (Tachymarptis melba), and both adults and nestlings of barn owls (Tyto alba), with peaks of accumulation observed in house sparrows sampled on conventional farms (Humann-Guilleminot et al., 2019a, 2019a. ...
... Recent studies evidenced that residues of neonicotinoids may also be detected in not-strictly granivorous birds (Humann-Guilleminot et al., 2019a;Lennon et al., 2020) and birds of prey (Byholm et al., 2018;Humann-Guilleminot et al., 2021). In particular, studies performed in Swiss farmland and non-agricultural areas outlined the occurrence of neonicotinoid residues in feathers of adult house sparrows (Passer domesticus), nestlings of Alpine swifts (Tachymarptis melba), and both adults and nestlings of barn owls (Tyto alba), with peaks of accumulation observed in house sparrows sampled on conventional farms (Humann-Guilleminot et al., 2019a, 2019a. Compared with MG and ST, the residues observed in house sparrow from conventional farms were one order of magnitude lower for IMI (0.52 ng g − 1 in house sparrow; 5.8 and 8.8 ng g − 1 in ST and MG, respectively) and one order of magnitude higher for TMX (3.5 ng g − 1 in house sparrow; 0.36 and 0.16 ng g − 1 in ST and MG, respectively) (Humann-Guilleminot et al., 2019a). ...
... Recent studies evidenced that residues of neonicotinoids may also be detected in not-strictly granivorous birds (Humann-Guilleminot et al., 2019a;Lennon et al., 2020) and birds of prey (Byholm et al., 2018;Humann-Guilleminot et al., 2021). In particular, studies performed in Swiss farmland and non-agricultural areas outlined the occurrence of neonicotinoid residues in feathers of adult house sparrows (Passer domesticus), nestlings of Alpine swifts (Tachymarptis melba), and both adults and nestlings of barn owls (Tyto alba), with peaks of accumulation observed in house sparrows sampled on conventional farms (Humann-Guilleminot et al., 2019a, 2019a. Compared with MG and ST, the residues observed in house sparrow from conventional farms were one order of magnitude lower for IMI (0.52 ng g − 1 in house sparrow; 5.8 and 8.8 ng g − 1 in ST and MG, respectively) and one order of magnitude higher for TMX (3.5 ng g − 1 in house sparrow; 0.36 and 0.16 ng g − 1 in ST and MG, respectively) (Humann-Guilleminot et al., 2019a). ...
Article
Neonicotinoids are one of the most diffusely used classes of pesticides whose level of danger toward non-target invertebrate and vertebrate species has raised increasing concern in the last decades. Among vertebrates, birds are particularly susceptible to unintentional neonicotinoid poisoning since they can be exposed through different pathways, including ingestion of dressed seeds, sucking of contaminated pollen, ingestion of sprayed insects, predation on contaminated aquatic and terrestrial preys. In the present study, we investigated the possible exposure of seabirds by measuring the residues of five neonicotinoids (acetamiprid, clothianidin, imidacloprid, thiacloprid and thiamethoxam) in samples of pooled feathers collected from fledglings of the strictly piscivorous Sandwich tern (Thalasseus sandvicensis) and the mixotrophic species Mediterranean gull (Ichthyaetus melanocephalus). At least one neonicotinoid was quantified in all the Mediterranean gull samples (n = 11) and 89% of the analysed Sandwich tern samples (n = 36). The active principles with the highest quantification rates were imidacloprid (100% in Mediterranean gulls and 58% in Sandwich terns) and clothianidin (100% in Mediterranean gulls and 61% in Sandwich terns), while thiacloprid was the less frequently detected pesticide (<20% of samples in both species). Mean concentrations ± standard error for imidacloprid, clothianidin and thiamethoxam were 8.8 ± 1.4, 4.5 ± 0.19 and 0.16 ± 0.02 ng g⁻¹ for the Mediterranean gull, and 5.8 ± 0.55, 0.60 ± 0.08 and 0.36 ± 0.03 ng g⁻¹for the Sandwich tern, respectively. Our data evidenced the exposure of seabirds to neonicotinoids and the further need to investigate the extent of neonicotinoid contamination in non-agricultural ecosystems.
... These studies suggest that NNIs are likely to affect a much larger spectrum of species than just granivorous birds. Overall, regardless of their diet, birds living in agricultural environments are the most exposed to a direct contamination by neonicotinoids, sometimes at a large scale (Humann-Guilleminot et al., 2019a). However, we may still underestimate the extent of the contamination to other species that would not be suspected of being in direct contact with NNIs. ...
... We extracted neonicotinoid insecticides following the protocol described in Humann- Guilleminot et al. (2019a). Fifteen mg of feathers were weighed and cut in a 2-mL tube and ground with three 5-mm metal beads using a Retsch mill for 6 min at 26 Hz. ...
... This field study provides additional evidence that birds are exposed to NNIs. Recent research shows that non-strictly granivorous birds can be contaminated by NNIs (Humann-Guilleminot et al., 2019a;Lennon et al., 2020). Yet, data on the presence of neonicotinoid residues in birds higher up in the food web is very scarce. ...
Article
Monitoring the extent to which wildlife is exposed to the broadly used neonicotinoid insecticides (NNIs) is essential to assess their potential negative effects on biodiversity. Birds are good subjects to assess such exposure, because they inhabit various habitats and they feed at different trophic levels. However, so far, most studies have focused on the contamination of granivorous species. In this study, we assess the concentrations of five NNIs (acetamiprid, clothianidin, imidacloprid, thiacloprid, thiamethoxam) in the carnivorous Barn owl (Tyto alba), and the insectivorous Alpine swift (Tachymarptis melba). NNIs were measured in the Barn owl in feathers collected from nestlings in 2012 (n = 49 broods) and adults in 2016 (n = 58 individuals), and in the Alpine swift from feathers collected from 50 pooled nestling samples from 50 nests between 2004 and 2017 (nestlings raised in five different nests over ten years; n = 50 broods), plasma samples from adults in 2018 (n = 15), and food boluses collected from nestling provisioning adults in 2018 (n = 12). We found that 69% and 56.9% of Barn owl feathers from nestlings and adults respectively contained at least one NNI at measurable concentration. Mean ± SE and median concentrations (in ppb) of total NNIs were 0.66 ± 1.13 and 0.42 for nestlings, and 0.17 ± 0.57 and 0.04 for adults. In the Alpine swift, although we detected no NNI in nestling feathers, we found that 75% of food boluses and 20% adult plasma samples contained at least one NNI at measurable concentration. Mean ± SE and median concentrations (in ppb) of total NNIs were 0.24 ± 0.20 and 0.24 in food boluses, and 0.06 ± 0.13 and 0 in plasma. In view of these results, further research is warranted to determine the extent of contamination in non-granivorous birds and their potential effects.
... Given that populations of agricultural and migratory bird species have been declining over the last few years in North America and European countries (Donald et al., 2001;Murphy, 2003) it is important to identify possible causes for this trend since there is evidence that neonicotinoids impair the migratory ability of birds (Eng et al., 2017). Neonicotinoid residues have been detected in the blood of long-distance migratory honey buzzards (Pernis apivorus) in the U.K. (Byholm et al., 2018) as well as in that of Eurasian eagle-owls (Bubo bubo) in Spain (Taliansky-Chamudis et al., 2017), and appear in the feathers of house sparrows (Passer domesticus) in Switzerland (Humann-Guilleminot et al., 2019). Because local farmers use modern agricultural practices and routinely apply pesticides to their crops, we hypothesized that environmental contamination by agricultural pesticides may be increasing to levels potentially incompatible with long-term conservation of biodiversity in nearby protected areas. ...
... Preparation and extraction of soil and sediment samples was performed following a protocol adapted from Mitchell et al. (2017) and Humann-Guilleminot et al. (2019). Fresh samples were dried for 2e3 weeks at 40 C in an oven, homogenized, sieved through (0.5 mm mesh) and ground to a fine powder with a mortar and a pestle. ...
Article
Usage of neonicotinoids is common in all agricultural regions of the world but data on environmental contamination in tropical regions is scarce. We conducted a survey of five neonicotinoids in soil, water and sediment samples along gradients from crops fields to protected lowland tropical forest, mangroves and wetlands in northern Belize, a region of high biodiversity value. Neonicotinoid frequency of detection and concentrations were highest in soil (68%) and lowest in water (12%). Imidacloprid was the most common residue reaching a maximum of 17.1 ng/g in soil samples. Concentrations in soils differed among crop types, being highest in melon fields and lowest in banana and sugarcane fields. Residues in soil declined with distance to the planted fields, with clothianidin being detected at 100 m and imidacloprid at more than 10 km from the nearest applied field. About half (47%) of the sediments collected contained residues of at least one compound up to 10 km from the source. Total neonicotinoid concentrations in sediments (range 0.014–0.348 ng/g d. w.) were about 10 times lower than in soils from the fields, with imidacloprid being the highest (0.175 ng/g). A probabilistic risk assessment of the residues in the aquatic environment indicates that 31% of sediment samples pose a risk to invertebrate aquatic and benthic organisms by chronic exposure, whereas less than 5% of sediment samples may incur a risk by acute exposure. Current residue levels in water samples do not appear to pose risks to the aquatic fauna. Fugacity modeling of the four main compounds detected suggest that most of the dissipation from the agricultural fields occurs via runoff and leaching through the porous soils of this region. We call for better monitoring of pesticide contamination and invertebrate inventories and finding alternatives to the use of neonicotinoids in agriculture.
... We aimed at exposing birds to a field realistic amount of acetamiprid and chose a very low dose corresponding to 0.5% of the zebra finch LD 50 (the LD 50 of the house sparrow being unknown) spread over the whole duration (19 days) of the experiment. Based on the available literature, we believe that this dose reflects the concentrations of neonicotinoids, including acetamiprid, to which birds are chronically exposed in the fields (Hao et al., 2018;Humann-Guilleminot et al., 2019). A total of 56 males were dispatched in 14 aviaries and divided in two groups receiving either an oral dose of acetamiprid or the vector (saline solution). ...
... Assessing the actual exposure rate of farmland bird species is difficult, yet the dose we used may well be underestimated compared to what birds may ingest in the field. Birds living in agricultural habitats are particularly exposed to NNIs (Hao et al., 2018;Humann-Guilleminot et al., 2019;MacDonald et al., 2018) through various pathways. First, they may ingest NNIs at high concentrations when they eat treated seeds (MacDonald et al., 2018;Millot et al., 2017). ...
Article
Farmland bird species are particularly exposed to pesticides through various pathways. Among pesticides, neonicotinoids insecticides are commonly used in agriculture, but their influence on bird reproductive capacities is poorly understood. In this study, we experimentally tested the effects of the neonicotinoid acetamiprid on House sparrows' sperm quality and oxidative status following ingestion of a low and field-realistic dose of the compound. To do so, 56 males were captured, held and orally dosed seven times over 19 days of experiment with either a saline solution (control) or an acetamiprid-saline solution, and sperm samples were retrieved before and after the experiment. The overall dose given to the birds corresponded to 0.5% of the LD50 for the Zebra finch (5.7 mg/kg BW) spread into 7 separate doses and administered every three days over the entire duration of the study (ca. 0.07% LD50 per oral dose). Sperm mobility and sperm oxidative status were unaffected by the treatment, but sperm density was. Birds that received oral doses of acetamiprid suffered a significant decline in their sperm density compared to control birds. This result was confirmed by a significant decrease in the activity of the antioxidant enzyme SOD in the sperm of acetamiprid-dosed birds. These results provide the first evidence of sublethal toxicity of acetamiprid in a songbird and suggest that passerine birds’ fertility may be negatively affected by very small doses of neonicotinoids in the wild.
... Prosser (2001) recorded a total of 18 species foraging on seed types that are regularly treated with NNs as part of agricultural practice [26] and Lopez-Antia et al. (2016) observed 30 species consuming NN-treated seeds in recently drilled fields [16]. Furthermore, NN residues have been detected in two wild passerine species [20,27], and in the eggs, crops and livers of wild partridges [28,29]. A detailed review conducted by the American Bird Conservancy calculated that as few as 3.9 and 1.3 imidacloprid-coated wheat seeds could produce lethal and sub-lethal (reproductive) effects, respectively, if ingested by a 15-g bird [11]. ...
... Of these, one was placed in the high exposure group (turtle dove), three belonged to the medium-exposure group (house sparrow, red-legged partridge, skylark), and all except red-legged partridge experienced overall population declines in England between 1995 and 2016. It is possible that the negative estimates for these species may be indicative of a true negative relationship between NN application and population change; indeed, a recent study reported widespread exposure of house sparrow to NNs in the field [27], but the implications of this exposure for fitness and/or survival were not assessed. However, other ecological factors may have also been important drivers. ...
Article
Full-text available
Over the last 20 years, a new group of systemic insecticides – the neonicotinoids - has gained prominence in arable systems, and their application globally has risen year on year. Previous modelling studies using long-term data have suggested that neonicotinoid application has had a detrimental impact on bird populations, but these studies were either limited to a single species or neglected to analyse specific exposure pathways in conjunction with observed population trends. Using bird abundance data, neonicotinoid usage records and cropping data for England at a 5x5 km resolution, generalised linear mixed models were used to test for spatio-temporal associations between neonicotinoid use and changes in the populations of 22 farmland bird species between 1994 and 2014, and to determine whether any associations were explained by dietary preferences. We assigned farmland bird species to three categories of dietary exposure to neonicotinoids based on literature data for species diets and neonicotinoid residues present in dietary items. Significant estimates of neonicotinoid-related population change were obtained for 13 of the 22 species (9 positive effects, 4 negative effects). Model estimates for individual species were not collectively explained by dietary risk categories, so dietary exposure to neonicotinoids via ingestion of treated seeds and seedlings could not be confirmed as a causal factor in farmland bird declines. Although it is not possible to infer any generic effect of dietary exposure to neonicotinoids on farmland bird populations, our analysis identifies three species with significant negative estimates that may warrant further research (house sparrow Passer domesticus, skylark Alauda arvensis and red-legged partridge Alectoris rufa). We conclude that there was either no consistent effect of dietary exposure to neonicotinoids on farmland bird populations in England, or that any over-arching effect was not detectable using our study design. The potential for indirect effects of insecticide use on bird populations via reduced food availability was not considered here and should be a focus for future research.
... They have been detected in wild flowers (Botias et al., 2015), leaf litter (Englert et al., 2016), and water and sediment of wetlands (Main et al., 2014) near to agricultural fields. The recent detections of neonicotinoids in plasma in wild insectivorous songbirds (Hao et al., 2018), diurnal raptors (Byholm et al., 2018), owls (Taliansky-Chamudis et al., 2017), livers of granivorous birds such as wild Turkeys (Meleagris gallopavo) (MacDonald et al., 2018), feathers of house sparrows (Passer domesticus) (Humann-Guilleminot et al., 2019), and in feathers, whole body carcasses and cloacal fluid of hummingbirds (Bishop et al., 2018;Graves et al., 2019) reveal that these compounds are present in terrestrial vertebrates at multiple trophic levels. The pervasive occurrence of these compounds in wildlife tissues raises concerns because environmentally relevant exposure in birds to neonicotinoids insecticides can be lethal and sublethally neurotoxic to birds and are associated with population declines of insectivorous birds (Lopez-Antia et al., 2013;Gibbons et al., 2014;Hallmann et al., 2014;Eng et al., 2017;Botha et al., 2018;Addy-Orduna et al., 2019;Eng et al., 2019;Rogers et al., 2019). ...
... The infiltration of neonicotinoid compounds into ecosystem food webs from their application as seed-treatments on cereal crops is well documented (Botias et al., 2015;Morrissey et al., 2015) and concentrations are higher in birds living near conventionally sprayed cereal crops (Humann-Guilleminot et al., 2019). There is a dearth of information regarding wildlife exposure near other types of agriculture such as fruit growing systems. ...
Article
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To examine the spatial, and temporal variation and potential sources of pesticide concentrations, primarily neonicotinoid insecticides, in hummingbirds in western Canada, we sampled their cloacal fluid from sites in British Columbia and Saskatchewan, Canada in 2017–2018. At a sub-sample of those sites, we also measured pesticides in honey bee (Apis mellifera) nectar, water, and sediment. We collected cloacal fluid from 5 species of hummingbirds (n = 26 sites) in British Columbia (BC) and Saskatchewan, Canada, and nectar from honey bee hives (n = 4 sites), water and sediment (n = 18 sites) in the Fraser Valley, BC. Among those, multiple types of samples were collected at 6 sites. We report the first measurement of flupyradifurone, a relatively new butenolide insecticide, in wildlife which was detected at 4.58 ng/mL in hummingbird cloacal fluid and 2.18 ng/g in honey bee nectar. We also detected three other neonicotinoids (imidacloprid, clothianidian, acetamiprid) and one metabolite desnitro-imidacloprid, and MGK264, a pesticide synergist, in our samples. Among 49 samples of cloacal fluid from rufous (Selasphorus rufus), Anna's (Calypte anna), calliope (Selasphorus calliope) black-chinned (Archilocus alexandri) and ruby-throated hummingbirds (Archilocus colubris), 26.5% (n = 13) contained neonicotinoids. Maximum pesticide concentrations in hummingbirds, water and sediment were found in samples collected in the Fraser Valley, BC within 0.5 km of conventionally sprayed blueberry fields (CSBF) but highest levels in honey bee nectar were detected at a site 1.5 km from a CSBF. Imidacloprid in honey bee nectar at one site exceeded concentrations (>1 ng/g) that can sublethally affect worker bee foraging efficiency. In water, imidacloprid concentrations at another site exceeded Canadian guidelines (230 ng/mL) for the protection of aquatic invertebrates.
... The ensuing debate juxtaposed these presumed (socio-)economic impacts against an increase in primary productivity and farm profitability related to reconstituted pollination and other biodiversity-based ecosystem services (Garibaldi et al. 2014), while scientific information did not report any benefits of neonicotinoids on crop yields (Seltenrich 2017), quality of harvested produce, or farmlevel profitability (LaCanne and Lundgren 2018). Parallel to the accumulating scientific evidence of their deleterious effects on human health (Seltenrich 2017) and biodiversity, including vertebrate and invertebrate wildlife Pisa et al. 2015;Gibbons et al. 2015;Humann-Guilleminot et al. 2019b;Pisa et al. 2017;Sánchez-Bayo et al. 2016;Lundin et al. 2015;Tosi et al. 2017;Taliansky-Chamudis et al. 2017;Pecenka and Lundgren 2015;, there was a disclosure of scientific arguments and field observations (Blacquière et al. 2012;Carreck and Ratnieks 2014;Cresswell et al. 2012). From 2012 onward, the European Food Safety Authority (EFSA) suggested to suspend certain uses of active ingredients, and by March 2017, the European Commission had proposed a ban of all outdoor usage of three neonicotinoid pesticides (i.e., imidacloprid, clothianidin, and thiamethoxam). ...
... Frogs, fish and ducks can consume large numbers of rice pests, including planthoppers (Khatiwada et al. 2016;Zou et al. 2017;Sheng-miao et al. 2004); for WCR and wireworms, birds act as key predators and can suppress field populations (Bollinger and Caslick 1985;Sheng-miao et al. 2004) and rodents possibly engage in larval predation . A phase-out of neonicotinoid use is key to safeguard and fully exploit these vertebrate-mediated pest control services (e.g., (Humann-Guilleminot et al. 2019b). For example, Gurr et al. (2016) have indicated that pest suppression in ecologically engineered rice fields in China was greatest where farmers suspended the use of chemical insecticides. ...
Article
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We present a synthetic review and expert consultation that assesses the actual risks posed by arthropod pests in four major crops, identifies targets for integrated pest management (IPM) in terms of cultivated land needing pest control and gauges the implementation “readiness” of non-chemical alternatives. Our assessment focuses on the world’s primary target pests for neonicotinoid-based management: western corn rootworm (WCR, Diabrotica virgifera virgifera) in maize; wireworms (Agriotes spp.) in maize and winter wheat; bird cherry-oat aphid (Rhopalosiphum padi) in winter wheat; brown planthopper (BPH, Nilaparvata lugens) in rice; cotton aphid (Aphis gossypii) and silver-leaf whitefly (SLW, Bemisia tabaci) in cotton. First, we queried scientific literature databases and consulted experts from different countries in Europe, North America, and Asia about available IPM tools for each crop-pest system. Next, using an online survey, we quantitatively assessed the economic relevance of target pests by compiling country-level records of crop damage, yield impacts, extent of insecticide usage, and “readiness” status of various pest management alternatives (i.e., research, plot-scale validation, grower-uptake). Biological control received considerable scientific attention, while agronomic strategies (e.g., crop rotation), insurance schemes, decision support systems (DSS), and innovative pesticide application modes were listed as key alternatives. Our study identifies opportunities to advance applied research, IPM technology validation, and grower education to halt or drastically reduce our over-reliance on systemic insecticides globally.
... Notwithstanding their negative effects, neonicotinoid use in wild bird habitat is extremely widespread, and exposure is ubiquitous in agricultural habitats across many bird taxa. A recent study found that every collected sample of House Sparrow feathers contained at least one neonicotinoid compound, and samples from conventional farms had significantly higher concentrations than samples from organic farms (Humann-Guilleminot et al. 2019a). Another recent investigation found that 69% of Barn Owl (Tyto alba) nestling feathers and 57% of Barn Owl adult feathers contained at least one neonicotinoid compound (Humann-Guilleminot et al. 2021). ...
Article
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There is increasing awareness of the negative ecological and environmental effects of widespread use of pesticides on the landscape. Spillover or drift of pesticides from agricultural areas has been shown to impact species health, reproduction, and trophic dynamics through both direct and indirect mechanisms. Neonicotinoid insecticides are associated with observed declines of insectivorous and grassland birds, and these environmental pollutants are a significant conservation concern for many species that have experienced past or current population declines. Due to the high efficacy of these modern insecticides in depressing local insect populations, insectivorous birds can be negatively impacted by a pesticide-mediated reduction in food supply. Neonicotinoids may act synergistically with other stressors, such as habitat loss, to exacerbate threats to species or population viability. The Tricolored Blackbird is an insectivorous grassland bird of conservation concern in California, USA. Due to the high association of this species with agricultural habitats, we sought to quantify the amount of neonicotinoid residues in Tricolored Blackbird carcasses as a first step in assessing how this species may be impacted by pesticides. Out of 85 salvaged carcasses sampled ( N = 24 adults, N = 3 fledglings, and N = 58 nestlings), only two contained detectable levels of target compounds. These were an adult and one nestling that contained clothianidin residue (40 ppb and 7 ppb, respectively); both of these birds were salvaged from breeding colonies associated with dairy farms in Kern County, California. We suggest that further work is needed to assess neonicotinoid exposure of Tricolored Blackbirds in dairy-associated breeding colonies.
... However, the extent of contamination of agri-environment schemes (AESs) by neonicotinoid insecticides remains largely unknown. World-wide and nation-wide studies exist, which have examined honey and bird feathers contamination by neonicotinoids (Humann-Guilleminot, Clément et al., 2019;Mitchell et al., 2017;Woodcock et al., 2018), but they do not provide information about contamination of soils and plants from agri-environment schemes, because the exact foraging sites of honeybees and birds are either unknown or likely situated within a cultivated field. Hence, data on the presence of neonicotinoids in organic soils and crops and in non-cultivated vegetation at a scale covering a whole country are lacking, and this prevents any accurate evaluation of the European policies for a sustainable agriculture management. ...
Article
1.Neonicotinoids are the most widely used class of insecticides globally. However, the link between farming practices and the extent of contamination of soils and crops by neonicotinoid insecticides, as well as and the extent of such contamination in organic fields and ecological focus areas (EFAs) are currently unclear. 2.We measured the concentrations of five neonicotinoid insecticides (imidacloprid, clothianidin, thiamethoxam, thiacloprid, acetamiprid) in 702 soil and plant samples in 169 cultivated fields and EFAs from 62 conventional, integrated production and organic farms distributed over the entire lowland of Switzerland. 3.We detected neonicotinoids in 93% of organic soils and crops, and more than 80% of EFA soils and plants – two types of arable land supposedly free of insecticides. We also tested 16 samples of organic seeds, of which 14 were positive for neonicotinoids. 4.Finally, we calculated hazard quotients (HQs) and potentially affected fractions for 72 beneficial and 12 pest species. Under a field‐realistic scenario, we found that between 5.3 and 8.6% of above‐ground invertebrate species may be exposed to lethal concentrations of clothianidin, and 31.6 to 41.2% to sublethal concentrations, in “integrated production” and conventional fields. We also found that 1.3 to 6.8% (up to 12.5% based on HQs) of the beneficial invertebrate species may be exposed to sublethal concentrations of neonicotinoids in EFAs and organic fields. In contrast, no pest species would be exposed to lethal concentrations, even under a worst‐case scenario. 5.Synthesis and applications. Our study suggests that diffuse contamination by neonicotinoids may harm a significant fraction of non‐target beneficial species. The Use of neonicotinoids on crops may threaten biodiversity in refuge areas, while also potentially jeopardizing the practice of organic farming by impeding the biological control of pests. Based on our results, we call for a reduction in the dispersion and overuse of neonicotinoid insecticides in order to prevent any detrimental effects on biodiversity and ecosystem services associated with agroecosystems. This article is protected by copyright. All rights reserved.
... The US Department of Agriculture reported that neonics are detected in almost all fruits and vegetables and 90% of honey samples, and many samples contain multiple residues of neonics (Chen et al., 2014). Neonic residues have been also found in milk, tea, drinking water, river, soil, bees, and feathers (Bonmatin et al., 2019;Dankyi et al., 2014;Humann-Guileminot et al., 2019;Ikenaka et al., 2018;Lachat and Glauser, 2018;Nicholls et al., 2018;Tong et al., 2018;Xiong et al., 2019;Zhou et al., 2018), apart from in vegetables and fruits , and honey growing evidence suggests that the widespread use of neonics could negatively affect nontarget organisms, such as bees (Baron et al., 2017;der Sluijs et al., 2013;Woodcock et al., 2016), shrimps (Butcherine et al., 2019), birds (Eng et al., 2017;Hallmann et al., 2014) and other species (Morrissey et al., 2015). In response to these studies, the European Union banned three main neonics, namely, clothianidin (CLO), imidacloprid (IMI), and thiamethoxam (THI), except in greenhouses, in 2018 (Butler, 2018). ...
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Neonicotinoid insecticides are ubiquitous in food and the environment due to their wide use. Growing evidence suggests the adverse effects of neonicotinoids in many species, including mammals. Some studies have reported the urinary concentrations of neonicotinoids in human biological monitoring, but the potential risks of neonicotinoids on human health based on long-term chronic exposure studies in any general population have been rarely tackled. In this study, the dietary exposure to neonicotinoids of the Chinese adult population was studied on the basis of composite dietary samples collected from the 5th (2009-2012) and 6th (2015-2018) Chinese total diet studies (TDS). Residue levels of ten neonicotinoids were determined in 528 composite dietary samples from 24 provinces in China. Most of the samples (53.3% and 70.5% in the 5th and 6th TDS, respectively) that we analyzed contained the multi-residue of neonicotinoids. Imidacloprid and acetamiprid were the most frequently detected neonicotinoids, and thiamethoxam and clothianidin were increasingly used and found in the 6th TDS. The estimated daily intake (EDI) for total neonicotinoids was calculated to evaluate health risk of the Chinese adult population based on a relative potency factor assessment method. The mean EDIs of total neonicotinoids in the 5th and 6th TDS respectively reached 598.95 and 710.38 ng/kg bw per day. Although the mean EDIs of total neonics in 6th TDS was relatively higher than that in 5th TDS, no statistical difference was observed (p > 0.05). Vegetables were the main source of dietary exposure, but exposure via cereals and beverages and water must also be addressed in China. Although the average exposure for total neonicotinoids was much lower than the current chronic reference dose (57 μg/kg bw per day), the dietary exposure risks of a general population for total neonicotinoids should not be overlooked due to the ubiquity of neonicotinoids in food and the environment.
... However, linking changes in these parameters to neonicotinoid exposure is difficult in wild animals. Making the exposure-to-effect linkage in the field requires, at a minimum, a method to detect recent exposure (Hao et al. 2018;Humann-Guilleminot et al. 2019); even so, drawing conclusions is complicated by other variables that can influence these parameters in the absence of neonicotinoid exposure. Currently, specific biomarkers are not available to indirectly indicate exposure. ...
Article
We used domestic chickens (Gallus gallus domesticus) as a model for granivorous birds to identify methods to detect recent imidacloprid (IMI) exposure in wild birds. We conducted dosing experiments of 1%, 5%, 10%, and 20% of a reported LD50 for domestic chickens using repeated daily exposures over 7 d, at dosages equating to 1.04, 5.2, 10.4, and 20.8 mg/kg/d. We examined parent compound and metabolites in serial collections of feces and blood during exposures and for 15 d after exposures. We also collected liver, kidney, brain, muscle, and spleen at the experiment end. Mean concentrations of parent compound 15 d post‐exposure were highest in the feces and brain, then liver, muscle, spleen, and kidney, but mean concentrations of metabolites 5‐OH‐IMI and IMI‐olefin were highest in feces, then liver, spleen, muscle, kidney, then brain. Imidacloprid was rapidly cleared from blood, with only one individual in any dose group having detectable concentrations after 48 h. In contrast, fecal pellets had the highest frequency of IMI detection after 15 d. Concentrations of metabolites were higher than parent compound at all sampling times examined, but provided no information about time since exposure. Feces may provide a reliable non‐lethal method for detection of recent IMI exposure in wild birds. Additional work is needed to disentangle exposure dose concentration and time since exposure in field‐collected samples. This article is protected by copyright. All rights reserved.
... The risk of indirect exposure through food webs is also unknown, but birds are among top consumers of arthropods from all trophic levels. Ingestion and accumulation of neonicotinoids by birds appears to be widespread, with one study finding 100% of sparrows with neonicotinoids in their feathers (19). Just as concerning, birds and other vertebrates with higher trophic positions in food webs may be suffering from arthropod depletion and/or contamination by neonicotinoids, as suggested by some declining bird populations (20). ...
... Feather samples, which are grown over an extended period and may reflect longer periods of exposure than blood, can also be useful to detect neonicotinoid exposure; 146 pooled house sparrow feather samples had detectable concentrations (above 0.013-0.127 ppb) of more than one neonicotinoid, with higher concentrations in birds living on conventional farms than organic and integrated production farms in Switzerland (Humann-Guilleminot et al., 2019). More recently, fecal pellets have been shown to provide a non-invasive sampling option to test for neonicotinoids and their metabolites in birds . ...
Article
The most likely route of exposure to high concentrations of neonicotinoids capable of producing lethal or sublethal effects in birds and mammals is consumption of treated seeds. We placed trail cameras at simulated seed spills to document wildlife consuming treated seeds during the spring planting season. We simulated 4 types of spills, corn treated with 2 concentrations of clothiandin (0.5 or 0.25 mg/seed), corn treated with thiamethoxam (0.25 mg/seed), and soybean treated with imidacloprid (0.15 mg/seed). We documented 16 species of birds and 14 species of mammals eating neonicotinoid-treated seeds at spills. Of these, we quantified consumption of treated seeds by 12 species of birds and 13 species of mammals. Birds and mammals did not consume enough seeds to exceed published LD50s in related taxa, but most species did consume enough seeds to reach or exceed thresholds for sublethal effects based on currently available studies. Birds and mammals did not increase the amount of seeds consumed over time, as would be expected if responsive to the concentration of neonicotinoids on seeds, but more birds and mammals consumed seeds over time, as a proportion of the number at spills each day. More birds also consumed seeds after a soaking rain event, which likely reduced the amount of treatment on the seeds. Importantly, wildlife are consuming seeds while neonicotinoids are still concentrated on seeds. Our findings indicate that previously held assumptions about the safety of neonicotinoid seed treatments for vertebrate wildlife need to be revisited.
... In 2018, the European Commission banned the outdoor use of clothianidin (Commission Implementing Regulation (EU), 2018a), imidacloprid (IMC) (Commission Implementing Regulation (EU), 2018b), and thiamethoxam (Commission Implementing Regulation (EU), 2018c) but no regulation have been established for the others yet. Although many studies have reported neonicotinoid bioaccumulation in birds from Europe (Addy-Orduna et al., 2019;Humann-Guilleminot et al., 2019;Lennon et al., 2019), little is known about the accumulation of these contaminants in raptors. In fact, no studies on analysis of neonicotinoids in these species were found beyond Europe. ...
Article
Raptors (birds of prey and owls) have been widely used as suitable bioindicators of environmental pollution. They occupy the highest trophic positions in their food chains and are documented to bioaccumulate high concentrations of persistent pollutants such as toxic metals and legacy persistent organic pollutants (POPs).Whereas raptors played a critical role in developing awareness of and policy for chemical pollution, they have thus far played a much smaller role in current research on contaminants of emerging concern (CECs). Given the critical knowledge obtained from monitoring 'legacy contaminants' in raptors, more information on the levels and effects of CECs on raptors is urgently needed. This study critically reviews studies on raptors from Europe reporting the occurrence of CECs with focus on the investigated species, the sampled matrices, and the bioanalytical methods applied. Based on this, we aimed to identify future needs for monitoring CECs in Europe. Perfluoroalkyl substances (PFASs), novel flame retardants (NFRs), and to a lesser extent UV-filters, neonicotinoids, chlorinated paraffins, parabens and bisphenols have been reported in European raptors. White-tailed Eagle (Haliaeetus albicilla), Peregrine falcon (Falco peregrinus) and Northern goshawk (Accipiter gentilis) were the most frequently studied raptor species. Among matrices, eggs, feathers and plasma were the most widely employed, although the potential role of the preen gland as an excretory organ for CECs has recently been proposed. This review highlights the following research priorities for pollution research on raptors in Europe: 1) studies covering all the main classes of CECs; 2) research in other European regions (mainly East Europe); 3) identification of the most suitable matrices and species for the analysis of different CECs; and 4) the application of alternative sample treatment strategies (e.g. QuEChERS or pressurized liquid extraction) is still limited and conventional solvent-extraction is the preferred choice.
... As environmental contamination affects the people that live in a region, we also collected hair samples from people in addition to a survey of soils and water. Similarly to feathers, which can be used to monitor residues of chemical contaminants in birds (Dauwe et al., 2005;Humann-Guilleminot et al., 2019b), hair can be used as a matrix for the monitoring of pesticide residues in humans and animals (Smith-Baker and Saleh, 2011), providing a useful tool to explore the mid-to long-term occurrence of pesticides in the general population of a country (Yusa et al., 2015). ...
Article
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Synthetic pesticides such as neonicotinoids are commonly used to treat crops in tropical regions, where data on environmental and human contamination are patchy and make it difficult to assess to what extent pesticides may harm human health, especially in less developed countries. To assess the degree of environmental and human contamination with neonicotinoids we collected soil, water and people's hair in three agricultural regions of the Philippines and analysed them by ultra-high performance liquid chromatography coupled to tandem mass spectrometry (UHPLC-MS-MS). Five neonicotinoids, namely acetamiprid, clothianidin, imidacloprid, thiacloprid and thiamethoxam were targeted. Residues of neonicotinoids were found in 78% of 67 soil samples from the three provinces. Total neonicotinoid loads ranged on average between 0.017 and 0.89 μg/kg in soils of rice, banana and vegetable crops, and were 130 times higher (113.5 μg/kg) in soils of a citrus grove. Imidacloprid was the most prevalent compound at an average of 0.56 μg/kg in soil while thiacloprid was below the limit of detection. Half of the eight water samples from a rice field and nearby creek contained residues of imidacloprid (mean 1.29 ng/L) and one contained thiamethoxam (0.15 ng/L). Residues of neonicotinoids were found in 81% of 99 samples of people's hair from the surveyed regions (average total concentrations 0.14 to 1.18 ng/g, maximum 350 ng/g). Hair residue levels correlated well with the concentrations of thiamethoxam and total residues in soils from the same locality (r=0.98). The presence of thiacloprid in 15% of the hair samples but not in soil samples suggests an additional route of exposure among people, which is most likely to be through ingestion of agricultural food and drinks available in the market.
... Lots of evidence J o u r n a l P r e -p r o o f evaluation of the risk to consumers eating boar meat, neonicotinoid insecticides were found in more than 83% of pork samples, with the highest mean concentration of THI (6.2 ng/g) (Kaczyński et al., 2021). Some studies reported that 99% of feather samples from wild house sparrows (Passer domesticus) in Swiss lowland agricultural areas contained THI (Humann-Guilleminot et al., 2019). The unregulated use of THI poses a risk to animal and even human health as migration and transformation allow them to enter the food chain (Lu et al., 2020;Zhao et al., 2022). ...
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Neonicotinoid insecticides (NNIs) are the most widely used class of pesticides globally. However, NNIs may cause adverse health effects, including chronic liver disease, and perturbation of the gut microbiota. Thiacloprid (THI) is one of the NNIs widely used in agriculture. Therefore, it is essential to elucidate effects of THI on the microbiota–gut–liver axis to assess the risk of chronic liver disease following exposure to NNIs. This study aimed at investigating whether THI exposure promoted liver injury by altering the gut microbiota and related metabolites. In this study, healthy male quails were exposed to 2 or 4 mg/kg THI or 0.75% (w/v) saline once daily for 6 weeks, respectivey. Metabolomics, 16 S rRNA sequencing, and transcriptomic methods were performed to analyze the toxic mechanisms of THI in Japanese quails. We found that THI evoked damage and disruption to intestinal barrier function, leading to increased harmful substances such as lipopolysaccharide (LPS) and phenylacetic acid entering the liver. Besides, our results showed significantly altered hepatic bile acid and cholesterol metabolism in THI-exposed quails, with abnormal liver lipid metabolism, showing severe liver injury, fibrosis, and steatosis compared with the control quails. In conclusion, THI exposure aggravates liver injury via microbiota–gut–liver axis.
... By providing the first data on wild rodents and shrews, our results provide additional evidence of the exposure to and accumulation of neonicotinoids in many trophic groups worldwide, as shown in birds including nectarivores 74 , granivores and omnivores 50,75 , insectivores and birds of prey 66,76 . Some recent studies evidenced, as here, the detection of various CUPs in wildlife. ...
Article
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Knowledge gaps regarding the potential role of pesticides in the loss of agricultural biodiversity worldwide and mixture-related issues hamper proper risk assessment of unintentional impacts of pesticides, rendering essential the monitoring of wildlife exposure to these compounds. Free-ranging mammal exposure to legacy (Banned and Restricted: BRPs) and currently used (CUPs) pesticides was investigated, testing the hypotheses of: (1) a background bioaccumulation for BRPs whereas a “hot-spot” pattern for CUPs, (2) different contamination profiles between carnivores and granivores/omnivores, and (3) the role of non-treated areas as refuges towards exposure to CUPs. Apodemus mice (omnivore) and Crocidura shrews (insectivore) were sampled over two French agricultural landscapes (n = 93). The concentrations of 140 parent chemicals and metabolites were screened in hair samples. A total of 112 compounds were detected, showing small mammal exposure to fungicides, herbicides and insecticides with 32 to 65 residues detected per individual (13–26 BRPs and 18–41 CUPs). Detection frequencies exceeded 75% of individuals for 13 BRPs and 25 CUPs. Concentrations above 10 ng/g were quantified for 7 BRPs and 29 CUPs (in 46% and 72% of individuals, respectively), and above 100 ng/g for 10 CUPs (in 22% of individuals). Contamination (number of compounds or concentrations) was overall higher in shrews than rodents and higher in animals captured in hedgerows and cereal crops than in grasslands, but did not differ significantly between conventional and organic farming. A general, ubiquitous contamination by legacy and current pesticides was shown, raising issues about exposure pathways and impacts on ecosystems. We propose a concept referred to as “biowidening”, depicting an increase of compound diversity at higher trophic levels. This work suggests that wildlife exposure to pesticide mixtures is a rule rather than an exception, highlighting the need for consideration of the exposome concept and questioning appropriateness of current risk assessment and mitigation processes.
... Luzardo et al., 2014;Botha et al., 2015;Abbasi et al., 2016; see a recent review from India, which is the current major user of DDT, Malik et al., 2018), as well as molecules such as neonics that are partially banned (or on the way to being banned) (e.g. Byholm et al., 2018;Humann-Guilleminot et al., 2019a, 2021Millot et al., 2017). In Brazil, OCs were mostly banned in 1985, with some exceptions until 2007; nonetheless, some molecules, such as heptachlor, were still found in raptor feathers in 2015 (Aver et al., 2020). ...
Article
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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.
... The positive side of presenting low hydrophobicity and a 292 high solubility in water is that their accumulation in biological sytems is 293 relatively low. Neonicotinoids have been found in water [61], soil [62], plants [63], insects [64], 302 birds [65], aquatic organisms [66], mammals [67,68] and food [69][70][71]. An inter-303 esting case that illustrates the entrance of neonicotinoids to the food web was the ...
Chapter
Pollinators are vital for ecosystems, agriculture and the economy. Their population has been declining over several decades and the current situation is serious and of great concern. Multiple stressors are likely to have contributed to this, and exposure to neonicotinoid pesticides is one possible causative factor. Pollinators, including bees, can encounter neonicotinoids when foraging contaminated flowers, and although they were not the target organism for such pesticides, neonicotinoids can be fatal for them (lethal dose that will reduce the insect population by 50% is ~2 mg/kg). The specific application of these pesticides plays an important role in their dispersion into the environment and application to the seed coating itself provides a more targeted way to release the pesticide with a reduced risk. Neonicotinoids can disperse via aerosols (when sprayed), bound to soil dust and dust abrasion from the seed coating, via the degradation of contaminated plants or run-off from crops treated with the pesticide. They have high solubility in water (e.g. 39.8 g dinotefuran/L, 4.1 g thiamethoxam/L) and this favours their spread, however natural factors such as sunlight, warm weather and microorganisms can degrade them and reduce their persistence. The time required for the concentration of neonicotinoids in soil to reach half of their initial concentration is varied (e.g. 3.4–7,000 days). Soils that are poor in organic matter will poorly retain neonicotinoids and as a result they will be very mobile in them and potentially pollute water systems. In contrast, soils rich in organic matter will have greater retention of neonicotinoids and once saturated, neonicotinoids will leach in a sustained manner. The benefits given by neonicotinoids explain why they are widely used across the globe. Their potential impact in the fields on bees and pollinators in general thus calls for a globally responsible and restricted use of neonicotinoids as well as innovation to reduce their ecotoxicity.
... The intensive use of neonics has led to a dramatic decline of non-target organisms such as bees (Rundlof et al., 2015), especially bumblebee (Whitehorn et al., 2012) colonies, worldwide. Presence of thia, a neonicotinoid, had been identified in 75% of the honey samples from Europe (Mitchell et al., 2017) as well as in the feathers of house sparrows (Humann-Guilleminot et al., 2019) indicating their widespread prevalence in the environment. Although neonics were originally thought to be safe, recent studies show that they cause developmental alterations in chicken embryos (Gallus gallus domesticus) (Salvaggio et al., 2018), affect common carp (Cyprinus carpio) growth rates (Velisek and Stara, 2018), and illicit abnormal foraging behavior in carpenter ants (Camponotus japonicus) (Jung et al., 2018). ...
Article
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Background Neonicotinoids, a widely used class of insecticide, have attracted much attention because of their widespread use that has resulted in the decline of the bee population. Accumulating evidence suggests potential animal and human exposure to neonicotinoids, which is a cause of public concern. Objectives In this study, we examined the effects of a neonicotinoid, thiacloprid (thia) , on the male reproductive system. Methods The pregnant outbred Swiss female mice were exposed to thia at embryonic days E6.5 to E15.5 using “0,” “0.06,” “0.6,” and “6” mg/kg/day doses. Adult male progeny was analyzed for morphological and cytological defects in the testes using hematoxylin and eosin (H&E) staining. We also used immunofluorescence, Western blotting, RT-qPCR and RNA-seq techniques for the analyses of the effects of thia on testis. Results We found that exposure to thia causes a decrease in spermatozoa at doses “0.6” and “6” and leads to telomere defects at all tested doses. At doses “0.6” and “6,” thia exposure leads to an increase in meiotic pachytene cells and a decrease in lumen size, these changes were accompanied by increased testis-to-body weight ratios at high dose. By using RNA-seq approach we found that genes encoding translation, ATP production, ATP-dependent proteins and chromatin-modifying enzymes were deregulated in testes. In addition, we found that exposure to thia results in a decrease in H3K9me3 levels in spermatocytes. The changes in H3K9me3 were associated with a dramatic increase in activity of retroelements. Conclusion Our study suggests that gestational exposure to thia affects epigenetic mechanisms controlling meiosis which could lead to deleterious effects on male spermatogenesis.
... Among pesticides, neonicotinoids (NN), which are selectively neurotoxic and bind to nicotinic acetycholine receptors (nAChRs), are of special concern for their impacts on the environment and human health since they are the most widely used class of insecticides worldwide [6] and are ubiquitously found in the environment [7], wildlife [8], and various foods [9,10]. NN use has been restricted in some part of the world due to their significant toxicity to non-target insects such as bees [11]. ...
Article
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Background Neonicotinoids (NN) are selective neurotoxic pesticides that bind to insect but also mammal nicotinic acetycholine receptors (nAChRs). As the most widely used class of insecticides worldwide, they are ubiquitously found in the environment, wildlife, and foods, and thus of special concern for their impacts on the environment and human health. nAChRs are vital to proper brain organization during the prenatal period and play important roles in various motor, emotional, and cognitive functions. Little is known on children’s contamination by NN. In a pilot study we tested the hypothesis that children’s cerebro-spinal fluid (CSF) can be contaminated by NN. Methods NN were analysed in leftover CSF, blood, and urine samples from children treated for leukaemias and lymphomas and undergoing therapeutic lumbar punctions. We monitored all neonicotinoids approved on the global market and some of their most common metabolites by ultra-high performance liquid chromatography-tandem mass spectrometry. Results From August to December 2020, 14 children were consecutively included in the study. Median age was 8 years (range 3–18). All CSF and plasma samples were positive for at least one NN. Nine (64%) CSF samples and 13 (93%) plasma samples contained more than one NN. Thirteen (93%) CSF samples had N-desmethyl-acetamiprid (median concentration 0.0123, range 0.0024–0.1068 ng/mL), the major metabolite of acetamiprid. All but one urine samples were positive for ≥ one NN. A statistically significant linear relationship was found between plasma/urine and CSF N-desmethyl-acetamiprid concentrations. Conclusions We have developed a reliable analytical method that revealed multiple NN and/or their metabolites in children’s CSF, plasma, and urine. Our data suggest that contamination by multiple NN is not only an environmental hazard for non-target insects such as bees but also potentially for children.
Article
The aim was to determine, for the first time, concentrations of 7 neonicotinoids (NEOs) and 5 metabolites in Sus scrofa from hunting areas in north-eastern Poland and assess the risk to consumers eating boar meat. 42 wild boar muscle samples were collected over a one-year period. The concentrations of 12 NEOs were determined by a fully validated LC-ESI-MS/MS protocol based on ultrasonic, freezing and cleanup EMR–lipid sample preparation. NEOs were present in over 83% of samples, 17% had no residue, and one pesticide was present in 36% of samples. Most often found were: clothianidin (35%), acetamiprid and imidacloprid (33%), thiacloprid (31%), thiamethoxam (9%), and the average concentrations were (ng g⁻¹): thiacloprid 6.2 > imidacloprid 5.7 > acetamiprid 4.6 > clothianidin 2.2 > thiacloprid 1.6 > thiamethoxam 1.0. Multi-residue samples were found, one with 7 and one with 5 NEOs. Two NEOs were present in 24%; 3 in 39% and 4 in 10% of samples. In the metabolic degradation of acetamiprid, imidacloprid and thiacloprid, it was observed that metabolites account for no more than 8.5% of the measured parent substance. Acetamiprid-n-desmethyl was noted most often (21%). Due to the detection of NEOs in a large proportion of samples, chronic and acute risk assessment were performed. The estimated chronic and acute risk for consumers from NEOs neonicotinoids through the consumption of wild boar was very low and amounted to respectively 0.02% of ADI and 0.86% of ARfD.
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Birds are bioindicators for research on the relationship between environmental heavy metal concentration levels and accumulation levels in bird tissues. We use roadkill samples, collected by citizen science participants, to investigate the accumulation levels and associations of seven heavy metals in internal organs (heart, liver, and kidney), feathers (primary and breast), and bone (sternum and femur) of two focal species, Amaurornis phoenicurus and Gallinula chloropus. We found that heavy metal accumulation varied by target body part, and that variables are associated with bird species and heavy metal type. Although Zn and Cu were highest by concentration among both species, Cu was mostly accumulated in internal organs, As in feathers, and Pb in bone. Concentrations of As, Ni, and Pb in feathers of both focal species were lower than those reported in literature, whereas Cd and Cr were above toxic levels. The results also showed that spatial correlation for heavy metal concentration among bird body parts were poorer than non-spatial correlation, suggesting low spatial autocorrelations and variability. In addition, multiple regression analysis revealed significant correlation for Cr, As, and Pb estimations in A. phoenicurus heart, sternum, and kidney, respectively; and potentially Cr in G. chloropus femur by using feathers. These results support the feasibility of using feathers as indicators of As, Cr, and Pb heavy metal contamination to enhance our understanding of heavy metal accumulation in birds, especially at spatial scale, although caution is required for feather-based estimations of Cd, Cu, and Ni concentration.
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Due to increasing amounts of hazardous chemicals released into the environment, there is a high demand for developing easy and non-destructive biomonitoring tools. In a recent paper published in Trends in Analytical Chemistry, Rutkowska et al. (2018) concluded that feathers are a good matrix for biomonitoring of environmental pollutants in birds. In this commentary, we discuss the general conclusion of this paper. We provide several examples for which this statement is not correct, and we emphasize that only for legacy persistent organic pollutants (POPs) and mercury there is currently enough scientific evidence to use feathers as a reliable biomonitor, given that appropriate sampling designs and QA/QC protocols are taken into account. Furthermore, we discuss different pretreatment (e.g. feather washing) and analytical protocols along with specific QA/QC to be considered. In summary, this commentary provides an overview of the prospects and pitfalls when using feathers as a biomonitor for environmental pollutants.
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Hazardous delays Neonicotinoids are a widely used group of pesticides that have been shown to have negative impacts on an increasing number of species, most notably pollinators. Eng et al. tested how exposure to these compounds influenced the behavior of a migrating songbird. Ingestion of field-realistic levels of neonicotinoid insecticides reduced feeding and accumulation of body mass and fat stores, which led to delayed departure from stopover sites. Such delays can lead to reduced migration survival and decreased reproductive success and therefore have the potential to impose population-level impacts. Science , this issue p. 1177
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Neonicotinoid insecticides (NENIs) have become increasingly common in recent decades in the control of crop pests and other plant pathogens. It is undeniable that the practice improves crop yield and economic productivity in agriculture in general. However, the ongoing use of these chemicals in modern agriculture, as well as their widespread occurrence in the environment, poses a significant threat to food quality as well as safety, potentially posing a health risk to the public. This paper presents a comprehensive review of the latest explorations of NENIs based on extensive scientific collections to illustrate their distribution in soil, surface waters, and groundwater; discuss their exposure risk and potential toxic effects on the environment. It also highlights the connections between NENIs usage and their footprint on natural resources and the major food chains involving plants, animals, and humans. Web of Science, Google Scholar, PubMed, Science Direct, and other web sources were searched for scientific literature on NENIs distribution, properties, usage, cycling, and intrusion in the environment and food chain covering the last 14 years (2008 – 2022). A significant portion of available literature indicates an exponential increase in the use of NENIs within the last decade, and the large body of data shows that these group of insecticides pose substantial risks to the environment, humans, and other non-target living species. Here, the current state of knowledge, sources, environmental distribution, and the health effects of NENIs for soil organisms, plants, birds, animals, humans, and other non-target organisms are discussed. However, a great deal of information is still lacking, including NENIs threshold levels in soil, aquatic, terrestrial resources, and living organisms. Thus, a global multidisciplinary research effort is necessary to fill the existing knowledge gap, particularly related to NENIs toxic effects on the ecosystem. The review article will interest a wide range of stakeholders, from soil and water scientists to conservationists to academics and researchers.
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Neonicotinoids are among the most widely used insecticides worldwide, and as such, have garnered increasing attention from the scientific community in regards to their potentially negative environmental impacts. Recently, the degradability of neonicotinoid in soil has gained more attentions. However, what role soil microbes play in this degradation remains vastly underexplored. In this study, we compared the capacity of soil microbes sampled from different geographic regions and fields to degrade the neonicotinoid insecticide imidacloprid. Additionally, the composition of microbiota having low, middle, and high degradation activity was analyzed via high throughput sequencing. Correlations between microbiota composition and degradation activities were analyzed and reconfirmed. The results showed that the composition of soil microbiota and their degradation activity (ranged from zero to 96.25%) varied significantly between soil samples from different geographic locations. Correlation analysis showed that Paracoccus and Achromobacter bacteria were positively correlated with high degradation activity. Imidacloprid degradation experiments using these bacteria showed that Achromobacter sp. alone exhibited degradation activity reaching and sustaining 100% by day 20 while Paracoccus sp. did not. However, combining these bacteria resulted in increased degradation activity which reached 100% at day 15 relative to that achieved by Achromobacter sp. alone. This study demonstrated the capacity of soil microbes to degrade imidacloprid, and identified two promising bacterial candidates that could be potentially used in future to reduce imidacloprid accumulation in soils.
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Pestizide werden primär in der Landwirtschaft, aber auch im Siedlungsraum und in weiteren Bereichen eingesetzt. Als Pflanzenschutzmittel vermindern sie Ertrags- oder Qualitätseinbussen durch Schadorganismen. Der heutige Pestizideinsatz belastet aber die Umwelt und insbesondere die Biodiversität beträchtlich. Trotz Wissenslücken sind die unerwünschten Auswirkungen gut dokumentiert. Das Faktenblatt nimmt spezifisch die Auswirkungen von Pestiziden auf Umwelt, Biodiversität und Ökosystemleistungen in den Blick und zeigt mögliche Handlungsansätze für Politik und Gesellschaft zur Reduktion der unerwünschten Nebenwirkungen des Pestizideinsatzes auf. Nicht thematisiert werden im Faktenblatt etwa die Bedeutung von Pestiziden für die landwirtschaftliche Produktion oder die Auswirkungen auf die menschliche Gesundheit.
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Despite a generalist life history and a widespread distribution, the Common Grackle (Quiscalus quiscula) has declined by more than 58% since 1970. In Illinois, where this study was conducted, the current rate of decline is 7.03% annually. We hypothesized that low reproductive success in intensely agricultural areas is driving population decline. To test this, we quantified the nesting success and post-fledging survival of Common Grackles in central Illinois. Over a 2-year period, we monitored 188 nests and tracked the survival of 53 fledglings. Our estimate for nesting success of 0.622 (95% CI: 0.549-0.695) was much higher than the literature average of 0.267. Similarly, although post-fledging survival had not been estimated previously for Common Grackles, our estimate of 0.617 (95% CI: 0.471-0.764) was relatively high compared to that of other songbirds (range: 0.23-0.87). The most important factor influencing these estimates was ordinal date, which had a negative relationship with both nesting success and post-fledging survival. These results suggest that reproductive success is not the primary driver of population decline in Illinois. To expand upon the field portion of our study, we constructed a demographic model and used it to conduct a global sensitivity analysis. In our model, adult survival was the most influential demographic parameter in the context of population change. This study serves as an initial step in understanding the mechanism(s) of decline in the Common Grackle. We recommend additional research on the survival of Common Grackles, particularly in relation to persecution on the wintering grounds and exposure to agricultural chemicals.
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Since neonicotinoid insecticides were introduced to the agricultural market, evidence of the negative impacts of these systemic compounds on non-target species has accumulated. Birds are one of the largest groups of species to inhabit farmland, but the extent of neonicotinoid exposure in avian communities is poorly understood and very little is known about how any exposure may affect wild birds. Here, free-living gamebirds were used as a model group to measure the extent of avian exposure to the neonicotinoid clothianidin via seed treatment. During a typical sowing period of winter cereals treated with clothianidin, blood and liver samples were collected simultaneously from individual hunted gamebird carcasses, both pre- (n = 18) and post-sowing (n = 57) and were analysed for clothianidin via LC/MS-MS. Body weight, fat score and faecal parasite load were also quantified in the birds to ascertain whether any of these health parameters were associated with clothianidin exposure under field conditions. Clothianidin was detected in 6% of individuals sampled pre-sowing and 89% of individuals sampled post-sowing. The frequency of clothianidin detection in plasma samples and the concentration of clothianidin in liver and plasma samples decreased significantly between the first week and 2–4 weeks post-sowing. Faecal parasite load was positively associated with concentrations of clothianidin in the liver (but not plasma) of partridge species, but there was no association between clothianidin concentration and fat score or body weight, for either sample type. This study provides clear evidence that treated seed is a source of pesticide exposure for gamebirds following autumn sowing. These findings have implications for gamebirds worldwide where seed treatments are in use, and will aid the design of any future avian biomonitoring studies for agrochemical compounds.
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Geochemical approaches are popular for evaluations based on heavy metal concentrations in sediments or soils for eco-risk assessment. This study proposes a systematic geochemical approach (SymGeo) to explore six heavy metals in topsoils and bird tissues and organs of the target birds. We assume that the proposed approach based on field-collected heavy metals in topsoils and feathers can predict the areas with the potential risk of the heavy metals in birds. Finite mixture distribution modeling (FMDM) was used to identify background values of the heavy metal concentrations in topsoil. A spatial enrichment factor (EF), potential contamination index (PCI), contamination degree (Cod), and potential ecological risk index (PRI) based on FMDM results for topsoil, and a potential risk index (PRIbird) of heavy metals in the birds, were utilized for systematic prioritization of high eco-risk areas. Using multiple EF, PRI, and Cod results and multiple PRI-based maps of the heavy metals in feathers, we systematically prioritized risk areas where there is a high potential for heavy metal contamination in the birds. Our results indicate that heavy metal concentrations in the feather, liver, and kidney are not spatially cross-autocorrelated but are statistically significantly correlated with some heavy metals in topsoil due to external and internal depositions. Further, multiple EF, Cod, and RI distributions for topsoil, along with the PRI of the feather, showed that adequate coverages for potential risk for birds were greater than 71.05% in the top 30% and 84.69% in the top 20% potential eco-risk priority area of heavy metals in bird liver and kidney. Hence, our proposed approach suggests that assessments of heavy metals in bird feathers and topsoils without bird organs can be utilized to identify spatially high-risk areas. The proposed approach could be improved by incorporating water and sediment samples to enhance the crowdsourcing and the species-specific data.
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Neonicotinoid insecticides (NIIs) are extensively used worldwide and frequently detected in the environment. The human and ecological risks associated with the occurrence of NIIs in agricultural zones are of high importance. The present study highlights the regional occurrence and human exposure risks of NIIs in agricultural soil within the Pearl River Delta (PRD), South China. Six neonicotinoids, i.e., imidacloprid, clothianidin, acetamiprid, imidaclothiz, dinotefuran, and flonicamid, were measured in 351 soil samples from Zengcheng, a typical agricultural zone. The soil samples were categorized into three groups based on cultivated plants: vegetables, rice, and fruits. At least one of these neonicotinoid insecticides was detected in 95% of the soil samples. The levels of ∑6NII (range (median)) were 0.26−390 (23), 0.26−280 (6.1), and 0.26−120 (5.0) ng g⁻¹ dry weight in soil samples from vegetable farms, rice paddies, and fruit farms, respectively. Neonicotinoids were detected more frequently and at statistically higher concentrations in vegetable farms than in both rice paddies and fruit farms. This is likely ascribed to higher application frequencies of NIIs in vegetable farms due to higher planting frequencies. The hazard index values for human exposure to NIIs in the agricultural soils were all below 1, suggesting negligible non-cancer risks. The current residual levels of NIIs in the soils could however pose sub-lethal or acute effects to non-target terrestrial organisms such as earthworms. The present study suggests that more information is needed regarding NIIs contamination in soils from agricultural regions of South China to ensure that human and ecological risk from exposure to these compounds can be fully addressed.
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The present work is the first extensive study of large-scale pesticides research in wild animals. The investigation covered three game species: wild boar (n=42), roe deer (n=79) and deer (n=15) collected from north-eastern Poland. To characterize the 480 pesticides in muscle samples, LC-GC-MS/MS techniques were used. A total of 28 compounds were detected: 5 neonicotinoids, 6 organochlorine and 5 other insecticides, 9 fungicides and 4 herbicides, in the range of 0.1-85.3 ng g⁻¹. Over four hundred detections were done. The highest mean concentrations were as follows: anthraquinone (85.3 ng g⁻¹)>DDT-p,p’ (4.6 ng g⁻¹)>imidacloprid (4.3 ng g⁻¹)>permethrin (3.6 ng g⁻¹)>thiacloprid (2.8 ng g⁻¹). DDT and metabolites were the most frequently detected, followed by acetamiprid, tebuconazole, clothianidin and imidacloprid. Overall, 92% samples with residues were recorded, including 100% of wild boar, 88% of roe deer and 86% of deer. More than one pesticide (up to 9) was found in over 73% of the tested samples. The estimated chronic and acute risk to consumers of venison were very low (below 1% ADI and ARfD). This interdisciplinary study may be helpful for estimating ecological risk to wild animals and risk to consumers of wild animal products, and also as a source of biomonitoring data.
Chapter
Pesticide impacts on the environment and humans are manifold. Due to the enormous variety of active ingredients with different mode of actions, no general patterns for the different pesticide classes can be identified. This chapter describes experiences from our own experiments and other studies testing pesticide effects on a variety of nontarget organisms, including soil biota, amphibians, insects, birds, and bats. If pesticides are applied at recommended doses, they are rarely acutely toxic to nontarget organisms. However, there are many indirect effects of pesticides on the activity, fitness, neurology, and reproduction of organisms. When a herbicide kills plants, this affects not only the diversity of the vegetation; the removal of nectar, pollen, food, and shelter for many insect pollinators, herbivores, birds, bats, and other mammals impairs overall biodiversity. A major problem is that environmental risk assessments of pesticides are only conducted for single active substances on a few surrogate species, thereby ignoring the agricultural practice with applications of many different pesticides during the cropping season, biodiversity, and ecological interactions in the agroecosystem. Side effects of pesticides on humans are worrying and include acute poisonings, and serious chronic diseases affecting the nerve system, the hormone system, interfering fertility, and reproduction, and can cause tumors. Morbus Parkinson is in some countries an occupational disease for winegrowers. Examples are mentioned where scientists who critically challenge the current use of pesticides were given a hard time.
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Neonicotinoids are the most widely used insecticides globally, but their rapid metabolism in vertebrates makes diagnosing wildlife exposure challenging. More detailed information on the pattern of imidacloprid metabolites over time could be used to better approximate the timing and level of exposure. Here, we applied recently developed sensitive analytical methods to measure imidacloprid (IMI) parent compound along with an expanded suite of metabolites (5-OH-IMI, IMI-olefin, desnitro-IMI, IMI-urea, 6-chloronicotinic acid, 5-AMCP, 6-OH nicotinic acid) and six other neonicotinoids in adult red-winged blackbirds (Agelaius phoeniceus) that were experimentally exposed to one of two field-realistic concentrations of imidacloprid (0.8 or 6.9 mg/kg bw). We measured concentrations in small (25 μL) plasma samples collected pre-exposure and at 1-, 6-, 24- and 48-h post-exposure. Imidacloprid was rapidly absorbed and metabolized within 48 h at both doses, with the largest decrease within 6 h post-exposure. The average proportion of parent IMI decreased from 68% of total detectable residues at 1-h to 34% at 6-h post-exposure. Two primary metabolites in blood were 5-OH-IMI and IMI-olefin, and 5-OH-IMI was the most persistent marker of exposure at 48-h. Desnitro-IMI was consistently detected following very recent (≤ 1-h) IMI exposure, and a higher ratio of parent IMI to metabolites also indicated recent exposure. Other metabolites were only detected in the higher dose group, and could be used as indicators of exposure to higher IMI concentrations. This sensitive analytical method and the observed metabolite patterns could be used to inform a growing body of field studies linking neonicotinoid exposure and effects in free-living birds.
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The evidence of negative impacts of agricultural pesticides on non-target organisms is constantly growing. One of the most widely used group of pesticides are neonicotinoids, used in treatments of various plants, e.g. oilseed crops, corn and apples, to prevent crop damage by agricultural insect pests. Treatment effects have been found to spill over to non-target insects, such as bees, and more recently also to other animal groups, among them passerine birds. Very little is known, however, on the presence of neonicotinoids in other wild species at higher trophic levels. We present results on the presence of neonicotinoid residues in blood samples of a long-distant migratory food-specialist raptor, the European honey buzzard. Further, we investigate the spatial relationship between neonicotinoid residue prevalence in honey buzzards with that of crop fields where neonicotinoids are typically used. A majority of all blood samples contained neonicotinoids, thiacloprid accounting for most of the prevalence. While neonicotinoid residues were detected in both adults and nestlings, the methodological limit of quantification was exceeded only in nestlings. Neonicotinoids were present in all sampled nests. Neonicotinoid presence in honey buzzard nestlings’ blood matched spatially with the presence of oilseed plant fields. These are the first observations of neonicotinoids in a diurnal raptor. For better understanding the potential negative sub-lethal of neonicotinoids in wild vertebrates, new (experimental) studies are needed.
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The use of neonicotinoid insecticides in agriculture is now recognized for the health risks it poses to non-target wildlife, with associated honey bee mortality especially concerning. Research directed toward the presence and effects of these pesticides on terrestrial vertebrates that consume neonicotinoid-coated seeds, such as wild turkeys (Meleagris gallopavo silvestris), is lacking. This study used liquid chromatography attached to a tandem mass spectrometer to assess the liver from 40 wild turkeys for neonicotinoid and other pesticide residues and compared detected levels of these contaminants across the southern Ontario, Canada. Nine (22.5%) wild turkeys had detectible levels of neonicotinoid residues—clothianidin in eight, and thiamethoxam in three. Two (5.0%) of these turkeys had detectable levels of both clothianidin and thiamethoxam. Fuberidazole was detected in two (5.0%) wild turkeys. The highest level of thiamethoxam detected was 0.16 ppm, while clothianidin was detected at 0.12 ppm, and fuberidazole at 0.0094 ppm. Knowledge of exposure in free-ranging wildlife is critical for better understanding the effects of neonicotinoids on wildlife health; thus, these data help establish baseline data for southern Ontario wild turkeys and provide context for reference values in future analyses.
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Global declines in insects have sparked wide interest among scientists, politicians, and the general public. Loss of insect diversity and abundance is expected to provoke cascading effects on food webs and to jeopardize ecosystem services. Our understanding of the extent and underlying causes of this decline is based on the abundance of single species or taxo-nomic groups only, rather than changes in insect biomass which is more relevant for ecological functioning. Here, we used a standardized protocol to measure total insect biomass using Malaise traps, deployed over 27 years in 63 nature protection areas in Germany (96 unique location-year combinations) to infer on the status and trend of local entomofauna. Our analysis estimates a seasonal decline of 76%, and midsummer decline of 82% in flying insect biomass over the 27 years of study. We show that this decline is apparent regardless of habitat type, while changes in weather, land use, and habitat characteristics cannot explain this overall decline. This yet unrecognized loss of insect biomass must be taken into account in evaluating declines in abundance of species depending on insects as a food source, and ecosystem functioning in the European landscape.
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Growing evidence for global pollinator decline is causing concern for biodiversity conservation and ecosystem services maintenance. Neonicotinoid pesticides have been identified or suspected as a key factor responsible for this decline. We assessed the global exposure of pollinators to neonicotinoids by analyzing 198 honey samples from across the world. We found at least one of five tested compounds (acetamiprid, clothianidin, imidacloprid, thiacloprid, and thiamethoxam) in 75% of all samples, 45% of samples contained two or more of these compounds, and 10% contained four or five. Our results confirm the exposure of bees to neonicotinoids in their food throughout the world. The coexistence of neonicotinoids and other pesticides may increase harm to pollinators. However, the concentrations detected are below the maximum residue level authorized for human consumption (average ± standard error for positive samples: 1.8 ± 0.56 nanograms per gram).
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The large-scale use of neonicotinoid insecticides has raised growing concerns about their potential adverse effects on farmland birds, and more generally on biodiversity. Imidacloprid, the first neonicotinoid commercialized, has been identified as posing a risk for seed-eating birds when it is used as seed treatment of some crops since the consumption of a few dressed seeds could cause mortality. But evidence of direct effects in the field is lacking. Here, we reviewed the 103 wildlife mortality incidents reported by the French SAGIR Network from 1995 to 2014, for which toxicological analyses detected imidacloprid residues. One hundred and one incidents totalling at least 734 dead animals were consistent with an agricultural use as seed treatment. Grey partridges (Perdix perdix) and ?pigeons? (Columba palumbus, Columbalivia and Columba oenas) were the main species found. More than 70% of incidents occurred during autumn cereal sowings. Furthermore, since there is no biomarker for diagnosing neonicotinoid poisonings, we developed a diagnostic approach to estimate the degree of certainty that these mortalities were due to imidacloprid poisoning. By this way, the probability that mortality was due to poisoning by imidacloprid-treated seeds was ranked as at least ?likely? in 70% of incidents. As a result, this work provides clear evidence to risk managers that lethal effects due to the consumption by birds of imidacloprid-treated seeds regularly occur in the field. This in turn raises the question of the effectiveness of the two main factors (seed burying and imidacloprid-treated seeds avoidance) that are supposed to make the risk to birds negligible. Risk factors and the relevance of mitigation measures are discussed. Electronic supplementary material The online version of this article (doi:10.1007/s11356-016-8272-y) contains supplementary material, which is available to authorized users.
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One of the frequent questions by users of the mixed model function lmer of the lme4 package has been: How can I get p values for the F and t tests for objects returned by lmer? The lmerTest package extends the 'lmerMod' class of the lme4 package, by overloading the anova and summary functions by providing p values for tests for fixed effects. We have implemented the Satterthwaite's method for approximating degrees of freedom for the t and F tests. We have also implemented the construction of Type I - III ANOVA tables. Furthermore, one may also obtain the summary as well as the anova table using the Kenward-Roger approximation for denominator degrees of freedom (based on the KRmodcomp function from the pbkrtest package). Some other convenient mixed model analysis tools such as a step method, that performs backward elimination of nonsignificant effects - both random and fixed, calculation of population means and multiple comparison tests together with plot facilities are provided by the package as well.
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Least-squares means are predictions from a linear model, or averages thereof. They are useful in the analysis of experimental data for summarizing the effects of factors, and for testing linear contrasts among predictions. The lsmeans package (Lenth 2016) provides a simple way of obtaining least-squares means and contrasts thereof. It supports many models fitted by R (R Core Team 2015) core packages (as well as a few key contributed ones) that fit linear or mixed models, and provides a simple way of extending it to cover more model classes.
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The following species of sedentary birds with widespread and common occurrence are the most convenient as bioindicators: Magpie Pica pica, Feral Pigeon Columba livia f. domestica, House Sparrow Passer domesticus or Tree Sparrow Passer montanus, Blackbird Turdus merula, Goshawk Accipiter gentilis (feathers) and nestlings of various species. The non-destructive method of feather analysis is suitable mainly for assessment of Pb, Cd, As, Sb, Ge, Tl, and Hg. It cannot be applied for Mn, Ni, Sr, Rb, Mo and Fe that are cumulated in feathers at similar levels in polluted and unpolluted areas. Hg, Zn, Cu, Cr, As and Se have stronger affinity to keratin than others. The method requires strict standardisation, particularly in the way samples are to be collected and prepared for mineralisation. None of feather cleaning procedures removes all contaminants from vane surfaces. With respect to many elements, analysing 'concentration in feathers' is a measurement of external deposition therefore metal levels found in feathers correspond more strongly to the data on immission than to the element pool available in food. Mercury is an exception here. In cases of toxic elements as Pb, Cd or Tl it is possible to predict their concentrations in internal tissues on the basis of feather analysis.
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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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Systemic insecticides are applied to plants using a wide variety of methods, ranging from foliar sprays to seed treatments and soil drenches. Neonicotinoids and fipronil are among the most widely used pesticides in the world. Their popularity is largely due to their high toxicity to invertebrates, the ease and flexibility with which they can be applied, their long persistence, and their systemic nature, which ensures that they spread to all parts of the target crop. However, these properties also increase the probability of environmental contamination and exposure of nontarget organisms. Environmental contamination occurs via a number of routes including dust generated during drilling of dressed seeds, contamination and accumulation in arable soils and soil water, runoff into waterways, and uptake of pesticides by nontarget plants via their roots or dust deposition on leaves. Persistence in soils, waterways, and nontarget plants is variable but can be prolonged; for example, the half-lives of neonicotinoids in soils can exceed 1,000 days, so they can accumulate when used repeatedly. Similarly, they can persist in woody plants for periods exceeding 1 year. Breakdown results in toxic metabolites, though concentrations of these in the environment are rarely measured. Overall, there is strong evidence that soils, waterways, and plants in agricultural environments and neighboring areas are contaminated with variable levels of neonicotinoids or fipronil mixtures and their metabolites (soil, parts per billion (ppb)-parts per million (ppm) range; water, parts per trillion (ppt)-ppb range; and plants, ppb-ppm range). This provides multiple routes for chronic (and acute in some cases) exposure of nontarget animals. For example, pollinators are exposed through direct contact with dust during drilling; consumption of pollen, nectar, or guttation drops from seed-treated crops, water, and consumption of contaminated pollen and nectar from wild flowers and trees growing near-treated crops. Studies of food stores in honeybee colonies from across the globe demonstrate that colonies are routinely and chronically exposed to neonicotinoids, fipronil, and their metabolites (generally in the 1-100 ppb range), mixed with other pesticides some of which are known to act synergistically with neonicotinoids. Other nontarget organisms, particularly those inhabiting soils, aquatic habitats, or herbivorous insects feeding on noncrop plants in farmland, will also inevitably receive exposure, although data are generally lacking for these groups. We summarize the current state of knowledge regarding the environmental fate of these compounds by outlining what is known about the chemical properties of these compounds, and placing these properties in the context of modern agricultural practices.
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Maximum likelihood or restricted maximum likelihood (REML) estimates of the parameters in linear mixed-effects models can be determined using the lmer function in the lme4 package for R. As for most model-fitting functions in R, the model is described in an lmer call by a formula, in this case including both fixed- and random-effects terms. The formula and data together determine a numerical representation of the model from which the profiled deviance or the profiled REML criterion can be evaluated as a function of some of the model parameters. The appropriate criterion is optimized, using one of the constrained optimization functions in R, to provide the parameter estimates. We describe the structure of the model, the steps in evaluating the profiled deviance or REML criterion, and the structure of classes or types that represents such a model. Sufficient detail is included to allow specialization of these structures by users who wish to write functions to fit specialized linear mixed models, such as models incorporating pedigrees or smoothing splines, that are not easily expressible in the formula language used by lmer.
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Concerns over the role of pesticides affecting vertebrate wildlife populations have recently focussed on systemic products which exert broad-spectrum toxicity. Given that the neonicotinoids have become the fastest-growing class of insecticides globally, we review here 150 studies of their direct (toxic) and indirect (e.g. food chain) effects on vertebrate wildlife-mammals, birds, fish, amphibians and reptiles. We focus on two neonicotinoids, imidacloprid and clothianidin, and a third insecticide, fipronil, which also acts in the same systemic manner. Imidacloprid and fipronil were found to be toxic to many birds and most fish, respectively. All three insecticides exert sub-lethal effects, ranging from genotoxic and cytotoxic effects, and impaired immune function, to reduced growth and reproductive success, often at concentrations well below those associated with mortality. Use of imidacloprid and clothianidin as seed treatments on some crops poses risks to small birds, and ingestion of even a few treated seeds could cause mortality or reproductive impairment to sensitive bird species. In contrast, environmental concentrations of imidacloprid and clothianidin appear to be at levels below those which will cause mortality to freshwater vertebrates, although sub-lethal effects may occur. Some recorded environmental concentrations of fipronil, however, may be sufficiently high to harm fish. Indirect effects are rarely considered in risk assessment processes and there is a paucity of data, despite the potential to exert population-level effects. Our research revealed two field case studies of indirect effects. In one, reductions in invertebrate prey from both imidacloprid and fipronil uses led to impaired growth in a fish species, and in another, reductions in populations in two lizard species were linked to effects of fipronil on termite prey. Evidence presented here suggests that the systemic insecticides, neonicotinoids and fipronil, are capable of exerting direct and indirect effects on terrestrial and aquatic vertebrate wildlife, thus warranting further review of their environmental safety.
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EXECUTIVE SUMMARY The neonicotinoids represent a relatively new group of insecticides. They were introduced in the early 1990s to counter widespread resistance in insect pests and increasing health and safety objections to the organophosphorous insecticides. Although of lower acute toxicity to vertebrates than the latter, the neonicotinoids’ longer persistence, high water solubility, runoff and leaching potential as well as their very high toxicity to pollinators are placing them under increasing public and political scrutiny, especially now that they have become the most widely used pesticides in the world. Their toxicity to pollinators has brought them the most attention so far and has dominated the recent concerns of regulatory institutions worldwide. The intent of this report is to review the risk that neonicotinoids pose to birds. Birds have borne more than their fair share of impacts from pesticides – from the early issues of eggshell thinning with DDT to the extensive mortality caused by the organophosphorous and carbamate insecticides that followed. Some researchers have suggested that birds may already be affected by neonicotinoids and that, at least in Europe, bird population declines can be blamed on these popular insecticides. The main products reviewed here are acetamiprid, imidacloprid, thiacloprid, clothianidin and thiamethoxam. Minor compounds include dinotefuran, nitenpyram and nithiazine. For the sake of comparison, this report will discuss, where appropriate, a number of older insecticides that the neonicotinoids have replaced. This includes the organophosphorous insecticides diazinon, chlorpyrifos, malathion, terbufos and methamidophos, the carbamate insecticides carbofuran, methomyl, the pyrethroids tefluthrin and deltamethrin as well as the seed treatment insecticide carbathiin. The report will emphasize US regulatory history although it will make reference to Canadian and EU regulatory reviews where relevant. For ease of consultation, summary points made here are detailed in the body of the report under the same section heading: 1. The history of neonicotinoid registrations highlights many of the critical failings of our current pesticide registration system. Regulatory agencies in both the US and Canada (and to some extent in Europe as well) exhibited a conflicted approach to the neonicotinoid class of compounds – on the one hand expressing serious concerns about the persistence, mobility and toxicity of the products – on the other hand, granting registrations in an ever-widening range of crops and non-agricultural use sites. There is evidence the neonicotinoids got a very ‘soft ride’ through registration. Based on the existing record, registration decisions concerning the neonicotinoid insecticides were overwhelmingly positive despite a consistent record of cautionary warnings from the scientists involved in the assessment process. Increased concerns in the scientific and popular literature over imidacloprid, clothianidin and other neonicotinoid insecticides did not deter pesticide manufacturers, who appeared to be in a race to register as many uses as possible. It looks as if the USEPA and other regulatory agencies consistently approved registrations despite their own scientists’ repeated and ever-growing concerns. It is relevant to ask why we conduct scientific evaluations of products if those evaluations have little or no bearing on the registration decisions that are made, and when staff scientists warning of ‘major risk concerns’ appear to be ignored. Even though several early reviews of the first neonicotinoid, imidacloprid, correctly identified Neonicotinoid Insecticides and Birds 6 issues of bird and mammal toxicity, persistence, runoff/leaching and aquatic toxicity, regulators failed to apply some of the lessons learned in the 1990s with imidacloprid to more recently developed compounds such as clothianidin and thiamethoxam. They also failed (and continue to fail) to consider the impact of combined neonicotinoid residues in the environment. Regulators have tended to place inordinate faith in precautionary labelling to mitigate very serious terrestrial and aquatic risks. 2. The acute toxicity of neonicotinoids to birds is lower than the acute toxicity of many of the insecticides they have replaced, notably the organophosphorous and carbamate insecticides. However, EPA and other regulatory agencies worldwide have underestimated the toxicity of these compounds to birds. This undervaluation is partly because the risk assessment methods fail to account sufficiently for interspecies variation in toxicity. Depending on the specific insecticide, we have found that EPA underestimates toxicity by 1.5 - 10 fold if the intent of the exercise is to protect most potentially exposed bird species, and not merely mallards and bobwhites, the two test species. In addition, there is some evidence that the neonicotinoid insecticides will debilitate birds at a much reduced fraction of a lethal dose compared to other pesticides and this debilitation will be longer-lasting. Small non-lethal doses are likely to cause partial paralysis and other sub-lethal effects in birds. These effects slip under the radar screen in regulatory assessments based entirely on lethal levels. 3. The chronic/reproductive toxicity of neonicotinoids to birds is high. This was recognised very early on in the regulatory reviews of the various active ingredients. Yet high reproductive toxicity in birds is typically ignored in the pesticide review process – whether for neonicotinoids or for other pesticides. Many pesticides fail the current reproduction screen, and many uncertainties exist surrounding the extrapolation of laboratory data to actual field conditions. These problems are not new but regulatory agencies have failed to address the situation. Because the neonicotinoids are systemic and persistent in soils, and because several are used as seed treatment chemicals, they are available to birds in a chronic fashion, making their potential to affect reproduction an even greater concern. The standard tests carried out by manufacturers place reproductive effects at dosing levels ranging from 2 to 13 mg/kg/day depending on the product. This level of exposure is easily achieved with seed treatment chemicals. However, very recent toxicological information from Japan suggests that testicular function in male birds as well as embryonic development in the offspring of exposed males is affected at levels much lower than indicated from these standard reproduction tests. 4. Of particular concern to birds are those compounds that are used as seed treatments, primarily imidacloprid, clothianidin, thiamethoxam and acetamiprid. Regardless of the exact label directions and requirements, seed-treatment chemicals are widely available to birds. Seeds are never fully covered with soil, making them easy to find by foraging birds. Spills are commonplace with current machinery. And many species have the ability to scrape and dig for planted seed. Seed treatments, by definition, will result in a high exposure situation for birds (as well as for small mammal species not discussed in this report). Both the EPA in the US and Pest Neonicotinoid Insecticides and Birds 7 Management Regulatory Agency (PMRA) in Canada have failed at times to consider this high exposure potential in their assessments. 5. The amount of insecticide adhering to the average corn (maize) seed can result in acute intoxications in birds with all three registered products – imidacloprid, clothianidin and thiamethoxam. With imidacloprid, a single seed may prove lethal for an average-sized bird (e.g. blue jay-sized) likely to be picking up whole corn seed from seeded fields. A few seeds only are required in the case of clothianidin or thiamethoxam. Indeed, we believe that imidacloprid is too acutely toxic to be used as a seed treatment insecticide on any seed type based on our assessment of its use in cereals and oilseeds. Acute intoxications in wheat or canola are less likely with clothianidin or thiamethoxam because these neonicotinoids are less acutely toxic to birds. The birds would need to ingest a greater number of the treated seeds to receive a lethal dose. However, based on chronic/reproduction endpoints, all seed treatments are predicted to cause effects given the very small number of seeds (as low as 1/10 of a seed per day during egg laying season) needing to be ingested to push birds into a ‘critical range’ where reproductive effects are expected. The main uncertainty here is how long the seeds will be available to birds and how long dosing is necessary before the type of effects seen in the laboratory will be seen in the wild. There are huge uncertainties – for instance what types of effects might be seen in altricial species (those in which the newly-hatched young are born relatively helpless, such as most passerines, or perching birds) and how this differs from effects seen in precocial species (in which the newly hatched young are relatively mature, such as ducks and geese, grouse and pheasants). Based on our current understanding and risk assessment procedures in place, the neonicotinoids as a group have a high potential to affect avian reproduction. This is due in large part to the very high exposure potential that seed treatment chemicals represent and the persistent nature of the neonicotinoids. A publication currently in press advances the hypothesis that the neonicotinoids are a contributory factor to many wildlife diseases through immune suppression. The authors make this claim on the basis of geographic and temporal associations. The sheer scale and seriousness of the issue demands that this hypothesis be investigated more fully. Despite industry claims, the neonicotinoids are not repellant to birds. Any demonstrated avoidance can be explained by hesitation before a new food source or post-ingestion intoxication and illness. Neither is sufficient to spare birds from either acute or chronic effects. There are parallels with the cholinesterase-inhibiting insecticides where repellency was similarly thought to reduce in-field risks. For example, the organophosphorous insecticide diazinon is extremely well avoided in the laboratory. Yet, thousands of geese and other species have grazed their way to an early death on diazinon-treated turf. 6. The link between impacts on the insect food of birds and declines of bird species is difficult to establish unequivocally, save for the evidence linking the grey partridge to pesticide use in the UK. A review of the existing literature suggests that it is difficult to predict the relative importance of food supply during the breeding season (i.e. when an insect food base is critical) compared to other risks such as habitat loss, food supply during migration and during winter, predation or Neonicotinoid Insecticides and Birds 8 even direct losses from poisoning or disturbances such as mowing or tillage. Each species responds to a different set of stressors and it is likely that many of the declines have multiple causes. Nevertheless, it would be foolhardy to argue that dramatic losses of insect biomass from ecosystems is not going to have potential consequences on the integrity of those ecosystems and on the species that depend to varying degrees on the spring-summer flush of insect food. The impacts on terrestrial food chains from neonicotinoid (and other systemic) insecticides may be much longer-lived and pernicious than those we have seen with non-systemic products. Generally speaking, an over-efficient removal of insects in crop fields is seldom seen as a matter of serious concern by regulators – especially in North America. The indirect impacts of pesticides are not considered in registration reviews – whether in the US or anywhere else in the world. In his book, Dutch toxicologist Henk Tennekes (2010) makes the case that the contamination of surface water by neonicotinoids is so widespread in the Netherlands (and possibly elsewhere in Europe), that loss of insect biomass on a continental scale is behind many of the widespread declines that are being seen, be they of marsh birds, heath or meadow birds or even coastal species. This suggests that we should be looking at possible links between neonicotinoid insecticides and birds, not on a farm scale, but in the context of whole watersheds and regions. Impacts from the neonicotinoids may very well be further afield than the arable area on which they are used, and many of those impacts may be mediated through the aquatic environment. Because aquatic impacts are considered during product registration reviews, it is reasonable to ask whether the potential impact of neonicotinoids to aquatic life has been assessed correctly. 7. Unfortunately, North American regulators have greatly underestimated the toxicity of imidacloprid and other neonicotinoids to aquatic invertebrates. Reference doses are set using outdated methodology which has more to do with a game of chance than with a rigorous scientific process. A complete disregard for the peer-reviewed literature is a constant factor throughout the history of neonicotinoid assessments. For imidacloprid, we believe that a scientifically defensible reference level (a water concentration at which undesirable effects are likely to be seen in reasonably sensitive species) for acute invertebrate effects (following short term exposure) is approximately 0.2 ug/l. European regulators acknowledge that acute effects are likely at levels exceeding 0.5 ug/l. In contrast, the EPA’s regulatory and non-regulatory reference levels are set at 35 ug/l. Similarly, a reasonable reference level for effects following chronic exposure is at least an order of magnitude lower, or between 0.01 and 0.03 ug/l rather than the 0.5 ug/l used in the U.S.. EPA’s approach to the assessment of aquatic risk is scientifically unsound and places aquatic environments at risk. In addition, there is evidence that risk managers at EPA have ignored aquatic risk ratios that exceeded the usual level of concern, notwithstanding the fact that those risk ratios were grossly underestimated in the first place. Based on the relative sensitivity of aquatic insects tested with several of the neonicotinoid insecticides, we suggest that these reference levels should also apply to the other neonicotinoid insecticides, notably acetamiprid, thiacloprid, clothianidin and thiamethoxam. In fact, because of their similarity in mode of action, the above reference levels should apply to the sum of all residues for all parent neonicotinoid compounds as well as some of the degradates. Neonicotinoid Insecticides and Birds 9 Neonicotinoid insecticides may be totally unprecedented in the history of pesticide registration in that measured groundwater contamination levels have been high enough to cause aquatic impacts. Data on surface water contamination from surveys to date, notably from California and from the Canadian Prairies, indicate that concentrations of several of the neonicotinoid insecticides are high enough to be causing impacts in aquatic food chains. Data from other jurisdictions (e.g. the Netherlands) show even higher levels of contamination. It is clear that neonicotinoids have often replaced other insecticides of higher short-term toxicity to aquatic life – especially fish. However, the mode of action of neonicotinoids, which entails a cumulative irreversible action and delayed effects in invertebrates, as well as their persistence in the environment, makes them particularly worrisome. It is clear that we are witnessing contamination of the aquatic environment at levels that will affect aquatic food chains. This has a potential to affect consumers of those aquatic resources, be they birds, fish or amphibians. In conclusion, policymakers and the public should be very concerned about the impact of neonicotinoid insecticides on birds and on the broader environment. Specifically, we should be concerned that:  regulatory procedures are scientifically deficient and prone to the vagaries of chance  risk managers appear to place minimal weight on concerns raised by environmental scientists who carry out the scientific evaluations of the products  despite all the red flags, regulators are adding to the list of permissible uses  neonicotinoids – the most heavily used insecticides in the world – are systemic products that are extremely persistent and very much prone to runoff and groundwater infiltration  some neonicotinoids are capable of causing lethal intoxications and all are predicted to cause reproductive dysfunction in birds  where we have looked, we have found broad-scale aquatic contamination at levels expected to cause impacts on aquatic food chains.  any future re-evaluation of these products appears to focus solely on pollinator toxicity. The seriousness of pollinator losses should not be underestimated, but there is much more at stake. A moratorium on any further use expansion is currently being discussed in the EU and Member States. Some countries have moved forward on limited cancellations. The North American regulatory system needs to act rather than continue to ignore evidence of widespread environmental damage. There is evidence that US regulators waited far too long to impose needed restrictions on the toxic insecticides responsible for millions of bird deaths per year (Mineau 2004) and that this is one of the more plausible reasons for the decline of grassland/farmland birds in North America (Mineau and Whiteside, 2013). The neonicotinoids have largely replaced that older generation of chemicals. We are urging regulators to take seriously the red flags raised by this persistent, cumulative, irreversibly-acting new class of pesticides.
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During the last 50 years, agricultural intensification has caused many wild plant and animal species to go extinct regionally or nationally and has profoundly changed the functioning of agro-ecosystems. Agricultural intensification has many components, such as loss of landscape elements, enlarged farm and field sizes and larger inputs of fertilizer and pesticides. However, very little is known about the relative contribution of these variables to the large-scale negative effects on biodiversity. In this study, we disentangled the impacts of various components of agricultural intensification on species diversity of wild plants, carabids and ground-nesting farmland birds and on the biological control of aphids.
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During the last 50 years, agricultural intensification has caused many wild plant and animal species to go extinct regionally or nationally and has profoundly changed the functioning of agro-ecosystems. Agricultural intensification has many components, such as loss of landscape elements, enlarged farm and field sizes and larger inputs of fertilizer and pesticides. However, very little is known about the relative contribution of these variables to the large-scale negative effects on biodiversity. In this study, we disentangled the impacts of various components of agricultural intensification on species diversity of wild plants, carabids and ground-nesting farmland birds and on the biological control of aphids. In a Europe-wide study in eight West and East European countries, we found important negative effects of agricultural intensification on wild plant, carabid and bird species diversity and on the potential for biological pest control, as estimated from the number of aphids taken by predators. Of the 13 components of intensification we measured, use of insecticides and fungicides had consistent negative effects on biodiversity. Insecticides also reduced the biological control potential. Organic farming and other agri-environment schemes aiming to mitigate the negative effects of intensive farming on biodiversity did increase the diversity of wild plant and carabid species, but – contrary to our expectations – not the diversity of breeding birds. We conclude that despite decades of European policy to ban harmful pesticides, the negative effects of pesticides on wild plant and animal species persist, at the same time reducing the opportunities for biological pest control. If biodiversity is to be restored in Europe and opportunities are to be created for crop production utilizing biodiversity-based ecosystem services such as biological pest control, there must be a Europe-wide shift towards farming with minimal use of pesticides over large areas.
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Neonicotinoids are the most widely used class of insecticides in the world, and there are increasing concerns about their effects on non-target organisms. Analytical methods to diagnose exposure to neonicotinoids in wildlife are still very limited, particularly for small animals such as songbirds. Blood can be used as a non-lethal sampling matrix, but the sample volume is limited by body size. Neonicotinoids have a low bioaccumulation potential and are rapidly metabolized, therefore, sensitive assays are critically needed to reliably detect their residues in blood samples. We developed an efficient LC-MS/MS method at a part-per-trillion (pg/ml) level to measure eight neonicotinoid related insecticides (acetamiprid, clothianidin, dinotefuran, flonicamid, imidacloprid, nitenpyram, thiacloprid and thiamethoxam) plus one metabolite (6-chloronicotinic acid) in small volumes (50 μL) of avian plasma. The average recovery of target compounds ranged from 95.7 to 101.3%, and relative standard deviations were between 0.82 and 2.13%. We applied the method to screen blood samples from 36 seed-eating songbirds (white-crowned sparrows; Zonotrichia leucophrys) at capture, and detected imidacloprid in 78% (28 of 36), thiamethoxam in 22% (8 of 36), thiacloprid in 11% (4 of 36), and acetamiprid in 11% (4 of 36) of wild-caught sparrows. 6 h after capture, birds were orally dosed with 0 (control), 1.2 or 3.9 mg of imidacloprid/kg bw, test results using this method indicated that plasma imidacloprid was significantly elevated (low 26-times, high 316-times) in exposed groups. This is the first study to confirm neonicotinoid exposure in small free-living songbirds through non-lethal blood sampling, and to demonstrate that environmentally realistic doses significantly elevate circulating imidacloprid concentrations. This sensitive method could be applied to characterize exposure to neonicotinoids in free-living wildlife and in toxicological studies.
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Neonicotinoid use has increased rapidly in recent years, with a global shift towards insecticide applications as seed coatings rather than aerial spraying. While the use of seed coatings can lessen the amount of overspray and drift, the near universal and prophylactic use of neonicotinoid seed coatings on major agricultural crops has led to widespread detections in the environment (pollen, soil, water, honey). Pollinators and aquatic insects appear to be especially susceptible to the effects of neonicotinoids with current research suggesting that chronic sub-lethal effects are more prevalent than acute toxicity. Meanwhile, evidence of clear and consistent yield benefits from the use of neonicotinoids remains elusive for most crops. Future decisions on neonicotinoid use will benefit from weighing crop yield benefits versus environmental impacts to non-target organisms and considering whether there are more environmentally benign alternatives.
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"An important, controversial account ... of the way in which man's use of poisons to control insect pests and unwanted vegetation is changing the balance of nature." Booklist.
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The populations of farmland birds in Europe declined markedly during the last quarter of the 20th century, representing a severe threat to biodiversity. Here, we assess whether declines in the populations and ranges of farmland birds across Europe reflect differences in agricultural intensity, which arise largely through differences in political history. Population and range changes were modelled in terms of a number of indices of agricultural intensity. Population declines and range contractions were significantly greater in countries with more intensive agriculture, and significantly higher in the European Union (EU) than in former communist countries. Cereal yield alone explained over 30% of the variation in population trends. The results suggest that recent trends in agriculture have had deleterious and measurable effects on bird populations on a continental scale. We predict that the introduction of EU agricultural policies into former communist countries hoping to accede to the EU in the near future will result in significant declines in the important bird populations there.
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Biodiversity is undergoing unprecedented global decline. Efforts to slow this rate have focused foremost on rarer species, which are at most risk of extinction. Less interest has been paid to more common species, despite their greater importance in terms of ecosystem function and service provision. How rates of decline are partitioned between common and less abundant species remains unclear. Using a 30-year data set of 144 bird species, we examined Europe-wide trends in avian abundance and biomass. Overall, avian abundance and biomass are both declining with most of this decline being attributed to more common species, while less abundant species showed an overall increase in both abundance and biomass. If overall avian declines are mainly due to reductions in a small number of common species, conservation efforts targeted at rarer species must be better matched with efforts to increase overall bird numbers, if ecological impacts of birds are to be maintained.
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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.
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The drive to squeeze ever more food from the land has sent Europe's farmland wildlife into a precipitous decline. How can agricultural policy be reformed so that we have fewer grain mountains and more skylarks?
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Clothianidin (CTD) is a neonicotinoid developed in the 1990s as an insecticide having selective toxicity, but it was later found to cause reproductive abnormalities in rats through oxidative stress. There is an attempt to preserve endangered animals, including the Japanese crested ibis, in Japan. However, there is a concern that neonicotinoid affects the reproduction of this bird, since it is used in its habitat. CTD toxicity in the birds is poorly understood, so we investigated whether or not the daily oral administration of CTD has any deleterious effects on the reproductive functions of mature male quails as experimental animals. The animals were randomly divided into four groups of 6 or 7 quails each, treated orally with 0, 0.02, 1 or 50 mg CTD/kg body weight (control, CTD0.02, CTD1 and CTD50). After that the males bred with untreated females to estimate the egg weights, and rates of fertilization and normal development, the testes, liver and spleen were examined histologically. Vacuolization and the number of germ cells having fragmented DNA in seminiferous tubules, and the number and size of vacuoles in hepatocytes increased dose-dependently. There were no significant differences in egg weights and fertilization rates between the groups, but some eggs of the CTD1 and CTD50 groups failed to develop, and embryonic length decreased dose-dependently. Thus, it was found that CTD affected the reproduction of the male quail through the fragmentation of germ cells and the inhibition or delay of embryonic development.