Article

Distributions of neonicotinoid insecticides in the Commonwealth of Massachusetts: A temporal and spatial variation analysis for pollen and honey samples

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Abstract

It is known that honeybees are exposed to a wide variety of pesticides, including systemic neonicotinoids, through different media. Pollen might be a better matrix for assessing exposure to neonicotinoid not only because it is the protein source for bees, but also because pollen collected from foraging bees could help to establish the field-realistic levels of neonicotinoids. In this study, we aimed to assess temporal and spatial variations of neonicotinoids in pollen collected across the Commonwealth of Massachusetts. Monthly pollen samples and a honey sample were collected between April and August 2013 from 62 volunteered hives and analysed for eight neonicotinoids. We utilised the relative potency factor (RPF) method to integrate individual neonicotinoids into a single measurement of imidaclopridRPF. We then analysed the spatial and temporal variations of imidaclopridRPF in pollen using the response profile analysis. Overall, 73% of pollen and 72% of honey samples contained at least one detectable neonicotinoid. We found that 49, 20 and 4% of pollen samples contained one, two and three neonicotinoids respectively. In honey, we detected that 57 and 15% of samples contained one and two neonicotinoids respectively. Neonicotinoids as a group, or imidacloprid, in pollen exhibited no significant temporal or spatial variation, however, we found statistically significant spatialoral interaction differences of imidaclopridRPF concentrations. Considering the ubiquitous of neonicotinoids in the environment and their effects on bees at the sub-lethal levels, it is prudent to identify ways to minimise the uses of neonicotinoids in order to reduce the risk of neonicotinoid exposure to honeybees.

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... Two methods have been used to collect substantial amounts of pollen for analysis of pesticide residue: trapping pollen from foragers as they return with pollen loads to the hive (Chauzat et al. 2006, Chauzat et al. 2011, Stoner and Eitzer 2013, Lu et al. 2015, Niell et al. 2015, David et al. 2016, de Oliveira et al. 2016, Long and Krupke 2016, Alburaki et al. 2017, Colwell et al. 2017, Nai et al. 2017, Smart et al. 2017, Böhme et al. 2018, Drummond et al. 2018, Prado et al. 2018, Tosi et al. 2018) and collecting stored pollen or bee bread inside the hive (Škerl et al. 2009, Bernal et al. 2010, Lawrence et al. 2016, Traynor et al. 2016, McArt et al. 2017. ...
... A previous survey of pesticides from 32 sites in Maine, ranging from unmanaged to managed agricultural and urban landscapes (Drummond et al. 2018), did not detect any nitroguanidine neonicotinoids, and also did not detect acephate or methamidophos, but did find the insecticides phosmet and carbaryl at a few sites. Another survey in Massachusetts, collecting pollen from 62 hives in 10 counties across the state and analyzing only neonicotinoids (Lu et al. 2015), found neonicotinoids more frequently than this study (72% of Massachusetts samples had at least one neonicotinoid, compared with 38% here), likely due in part to having much lower detection limits (0.1 ppb, compared with 2 ppb here). These samples, taken 1 day per month over 5 mo at each site, found some high concentrations of neonicotinoids (e.g., 25.2 ppb of imidacloprid-equivalent as a monthly average for one county). ...
... These samples, taken 1 day per month over 5 mo at each site, found some high concentrations of neonicotinoids (e.g., 25.2 ppb of imidacloprid-equivalent as a monthly average for one county). This mean presumably included substantial variation among sites within the county because the standard deviation was 3.3× the mean (Lu et al. 2015). ...
Article
Full-text available
Worldwide studies have used the technique of pollen trapping, collecting pollen loads from returning honey bee (Apis mellifera L.) (Hymenoptera: Apidae) foragers, to evaluate the exposure of honey bees to pesticides through pollen and as a biomonitoring tool. Typically, these surveys have found frequent contamination of pollen with multiple pesticides, with most of the estimated risk of acute oral toxicity to honey bees coming from insecticides. In our survey of pesticides in trapped pollen from three commercial ornamental plant nurseries in Connecticut, we found most samples within the range of acute toxicity in a previous state pollen survey, but a few samples at one nursery with unusually high acute oral toxicity. Using visual sorting by color of the pollen pellets collected in two samples from this nursery, followed by pesticide analysis of the sorted pollen and palynology to identify the plant sources of the pollen with the greatest acute toxicity of pesticide residues, we were able to associate pollen from the plant genus Spiraea L. (Rosales: Rosaceae) with extraordinarily high concentrations of thiamethoxam and clothianidin, and also with high concentrations of acephate and its metabolite methamidophos. This study is the first to trace highly toxic pollen collected by honey bees to a single plant genus. This method of tracking high toxicity pollen samples back to potential source plants could identify additional high-risk combinations of pesticide application methods and timing, movement into pollen, and attractiveness to bees that would be difficult to identify through modeling each of the contributing factors. This article is open access. You can get it here: https://academic.oup.com/ee/advance-article/doi/10.1093/ee/nvz007/5310146
... This is not surprising due to the low concentrations that are biologically active in honey bees (≤50 ppb, Yang et al. 2008) and also because of their ubiquitous presence in many geographic regions. Lu et al. (2016), in Massachusetts, found at least one neonicotinoid present in 73% of their pollen samples and 57% contained imidacloprid. A study in France revealed that half of all pollen samples tested positive for imidacloprid (Chauzat et al. 2006). ...
... A number of honey bee colony constituents can be and have been tested for pesticides to estimate exposure including the bees themselves, wax, honey, and pollen (Al Naggar et al. 2015). Pollen trapping has been a common route of exposure explored since residues on pollen brought into a hive can be linked directly to what bees are being exposed to while foraging (Chauzat et al. 2006, Stoner and Eitzer 2013, Lu et al. 2016. Pollen is an important food source for bees and therefore pesticide levels in pollen can have a direct negative effect on the bees feeding on it, especially the brood (Brodschneider and Crailsheim 2010). ...
... We found that neonicotinoids were not an exposure risk to honey bees in Maine in 2015 and are probably not a threat most years in most parts of the state, based upon the proportion of land area that is nonforested (<8%, Huff and McWilliams 2016). This was not the case in France, Connecticut, or Massachusetts (Lu et al. 2016). In Massachusetts, 73% of all sampled pollen contained at least one neonicotinoid and the spatio-temporal variation was characterized by peak neonicotinoid detections in April through August, depending upon the geographic sampling site. ...
Article
In 2015, we conducted a statewide assessment of honey bee exposure to pesticides with assistance of volunteer beekeepers. Pollen trapping was conducted at 32 sites in the spring, summer, and early fall. Apiary locations ranged from unmanaged natural landscapes to managed agricultural or urban landscapes. Pollen samples at each site were aggregated over the collection dates and chemical residue analysis was conducted on each pollen sample for 190 pesticides and metabolites using HPLC/MS. Twenty-five different residues were detected for an average of 2.9 detections per site. Detections were dominated by fungicides, but risk, calculated as: ppb residue concentration/LD50, was mostly due to insecticides. Beekeeper perceived land-use in the vicinity of each apiary was associated with significant differences in the number of detections and residue concentrations, agricultural landscapes greater than nonagricultural. However, there was no significant difference in oral or contact risk quotients due to land-use type. The landscape composition surrounding apiaries, derived with GIS, determined pesticide exposure for honey bees when total detections, log pesticide residue concentration, and log contact risk quotients were used as measures. Partial least squares explained 43.9% of the variance in pesticide exposure due to landscape composition. The best predictors describing pesticide exposure were: area (ha) of blueberry, coniferous forest, and urban/developed land cover types. Maine is the most forested state in the United States (as determined by % land area forested, 93%) and a negative exponential decay was observed between land area in conifer forest and the number of pesticide detections per apiary.
... Recent studies emphasized the presence of common pesticide residues in honey bee colonies and bee products , Lu et al. 2016. Pesticides can be brought to beehives from the foraging of flowers that were sprayed with pesticides, or from applications applied by beekeepers to control pest problems inside the hives (Haouar et al. 1990, Chauzat et al. 2006, Bonzini et al. 2011, Ko et al. 2017. ...
... A previous study mentioned that honey bee workers treated with sublethal levels of imidacloprid at the larval stage would exhibit abnormal olfactory associative behaviors (Yang et al. 2012). The effect of pesticide residues on honey bee colonies has become a serious problem without dispute (Rice et al. 2004, Lu et al. 2016, Ko et al. 2017. ...
... The high pesticide stress impact on the development of honey bees in Taiwan must be resolved. Pesticides (e.g., neonicotinoid insecticides, such as imidacloprid and thiamethoxam), organophosphates (e.g., chlorpyrifos), and the mixtures of cyhalothrin and ergosterol inhibiting fungicides were found in pollen and honey in the United States, France, and Spain (Chauzat et al. 2006, Bernal et al. 2010, Stoner and Eitzer 2013, Sanchez-Bayo and Goka 2014, Lu et al. 2016. Pollen and honey can be used as indicators of environmental contamination, so the presence of pesticide residues in the food of bees raises concerns about their health in those countries and in Taiwan. ...
Article
Full-text available
Significant pesticide residues are among the most serious problems for sustainable agriculture. In the beekeeping environment, pesticides not only impact a honey bee's survival, but they also contaminate bee products. Taiwan's agricultural environment has suffered from pesticide stress that was higher than that found in Europe and America. This study deciphered problems of pesticide residues in fresh honey bee pollen samples collected from 14 monitoring apiaries in Taiwan, which reflected significant contaminations within the honey bee population. In total, 155 pollen samples were screened for 232 pesticides, and 56 pesticides were detected. Among the residues, fluvalinate and chlorpyrifos showed the highest concentrations, followed by carbendazim, carbaryl, chlorfenapyr, imidacloprid, ethion, and flufenoxuron. The average frequency of pesticide residues detected in pollen samples was ca. 74.8%. The amounts and types of pesticides were higher in winter and in southwestern Taiwan. Moreover, five of these pollen samples were contaminated with 11-15 pesticides, with average levels between 1,560 and 6,390 μg/kg. Compared with the literature, this study emphasized that pollen gathered by honey bee was highly contaminated with more pesticides in Taiwan than in the America, France, and Spain. The ubiquity of pesticides in the pollen samples was likely due to the field applications of common pesticides. Recently, the Taiwanese government began to improve the pesticide policy. According to the resurvey data in 2016, there were reductions in several pesticide contamination parameters in pollen samples from west to southwest Taiwan. A long-term investigation of pollen pesticide residues should be conducted to inspect pesticides usage in Taiwan's agriculture.
... This sp 3 nitrogen, in association with a conjugated electron-withdrawing group, led to the definition for "neonicotinoid" [40], and remains central to the neonicotinoid pharmacophore [41]. Neonicotinoids are found in many commercially available insecticide products, for instance, Advocate, Confidor and Admire (imidacloprid), Actra, Endigo and Durivo (thiamethoxam) and Assil, Intruder and Saurus (acetamiprid) ( Table 1) which are broadly used to control agricultural and domestic insects [42][43][44]. Owing to their presumed low toxicity to mammals compared to other pesticides and high potency against target insects [45], these insecticides are registered in more than 120 nations [28,41]. Neonicotinoids are one of the most effective pesticides available for the control of sucking insect pests, for example, whiteflies, aphids, thrips, a number micro Lepidoptera, leaf-and plant-hoppers and some beetles [41,46]. ...
... Structural-binding analysis has demonstrated the binding of neonicotinoids to acetylcholine binding proteins from two molluscs species, Lymnaea stagnalis and Aplysia californica [55]. Neonicotinoids are found in many commercially available insecticide products, for instance, Advocate, Confidor and Admire (imidacloprid), Actra, Endigo and Durivo (thiamethoxam) and Assil, Intruder and Saurus (acetamiprid) ( Table 1) which are broadly used to control agricultural and domestic insects [42][43][44]. Owing to their presumed low toxicity to mammals compared to other pesticides and high potency against target insects [45], these insecticides are registered in more than 120 nations [28,41]. Neonicotinoids are one of the most effective pesticides available for the control of sucking insect pests, for example, whiteflies, aphids, thrips, a number micro Lepidoptera, leaf-and plant-hoppers and some beetles [41,46]. ...
Article
Full-text available
The broad utilisation of neonicotinoids in agriculture has led to the unplanned contamination of adjacent terrestrial and aquatic systems around the world. Environmental monitoring regularly detects neonicotinoids at concentrations that may cause negative impacts on molluscs. The toxicity of neonicotinoids to some non-target invertebrates has been established; however, information on mollusc species is limited. Molluscs are likely to be exposed to various concentrations of neonicotinoids in the soil, food and water, which could increase their vulnerability to other sources of mortality and cause accidental exposure of other organisms higher in the food chain. This review examines the impacts of various concentrations of neonicotinoids on molluscs, including behavioural, physiological and biochemical responses. The review also identifies knowledge gaps and provides recommendations for future studies, to ensure a more comprehensive understanding of impacts from neonicotinoid exposure to molluscs.
... Neonicotinoids are also frequently found in pollen of seedtreated crops (Bredeson and Lundgren 2015b;Byrne et al. 2014;KniPke et al. 2012). Pollens from untreated wildflowers and conservation strips that are embedded in an agricultural matrix also are frequently contaminated with neonicotinoids (Botiß et al. 2015;Chauzat et al. 2006;David et al. 2016;Lu et al. 2015). Hives placed in conservation suips adjacent to comfields collected pollens that had 10 times the honey bee LD50 for clothianidin (Mogren and Lundgren 2016). ...
... Converting nectar to honey does not necessarily reduce the risk of pesticide contamination (Blasco et al. 2003;Chen et al. 2014;Rissato et al. 2007). In one recent study, 70% of Massachusetts honey samples were contaminated with neonicotinoids, with imidacloprid being particularly prevalent (Lu et al. 2015). In addition to the harm these pesticides and residues pose to the hive itself, these contaminants become problematic when marketing the honey due to food safety regulations. ...
Chapter
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Pesticides are a necessary component of the monoculture-based food production system. The chemical management of pests can affect non-target organisms, including honey bees. Risk assessment is a way to evaluate the cost–benefit of pesticide use to honey bees and involves understanding the exposure routes and hazards posed by each particular pesticide. The effects of insecticides on bees are intuitively recognized, but other types of pesticides can affect honey bees too. Even “inactive” ingredients in a pesticide formulation can pose a risk to bees. Bees encounter pesticides as they forage in the environment through direct exposure to pesticide applications, and through contaminated resources such as pollen, nectar, water, comb, and propolis. Pesticides can affect bees in myriad ways. The toxicity of pesticides is highly context-specific, challenging risk assessments. Mortality is the most commonly measured effect of pesticides on bees but sublethal effects range from developmental problems, reduced reproductive fitness, diminished overwintering capacity, and numerous behavioral issues that may not kill the bee outright, but may kill the hives. The pervasiveness of pesticides in the environment means that bees cannot avoid exposure to numerous chemicals. Selecting for bees that are adapted to agrichemical-intensive landscapes may be a short-term solution, but the dynamic evolution of chemical use may prohibit long-term tolerances. Beekeepers and farmers need to work together to create and promote reduced chemical intensive food production systems. This is the only long-term answer for the survival of honey bees and biodiversity in general.
... Honey bee, Apis mellifera, is a major pollinator in agricultural systems (Kevan, 1999), and produces valuable products such as honey, royal jelly, and bee pollen. However, honey bees are also exposed to various pesticides when they are collecting nectar and pollen (Kevan, 1975;Crane and Walker, 1983;Lu et al., 2015). Honey bees may be influenced by the pesticide-contaminated nectar and pollen, which is brought back to bee hives from foraging on flowers that have been sprayed with pesticides, or from applications aimed to control pest problems inside the colonies by the beekeepers themselves; larvae, drones and queen will be also influenced by these pesticidecontaminated nectar and pollen (Sanchez-Bayo and Goka, 2014). ...
... The honey bee is a social insect, with the colony being maintained by the workers (Seeley, 1982;Calderone and Page, 1992). Honey bees can be easily poisoned by various pesticides when they are collecting nectar and pollen (Kevan, 1975;Crane and Walker, 1983;Chauzat et al., 2006;Lu et al., 2015) and further influence other members in the colony. Pesticide-contaminated nectar and pollen more heavily affect the larvae, drones and queen (Sanchez-Bayo and Goka, 2014). ...
Article
Full-text available
Pyriproxyfen (PPN) is an insect growth regulator (IGR) that interferes with insect metamorphosis. Although the side effects of PPN on honey bee larval/adult stages have been studied, the risk to honey bee larvae from PPN residue in the environment is still unclear. In this study, we evaluated the impact of PPN on larval honey bees in field colonies by using an in vivo feeding assay. Oral toxicity to adult honey bees were determined. Finally, influence on royal jelly production was also examined. For in vivo feeding assay, the highest observed PPN treatment caused 67% mortality during pupal stage and in the remaining bees, 62.3% showed abnormal eclosion. Reductions in hatching rate, capping rate and adult emergence rate and increased abnormal eclosion rate were found in the colonies fed with 10 ppm PPN syrup. Oral toxicity test revealed that adult honey bees were less susceptible to PPN. Moreover, PPN reduced not only queen cell acceptance rate but also yield of royal jelly in queen cells. These results indicate that PPN has negative impacts on both larval and adult honey bees and royal jelly production, especially under high PPN concentrations. Since PPN is harmful to the development of honey bee larvae and pupae in the natural environment, the issue of honey bee colony contamination by PPN should be addressed.
... Recent studies have indicated that neonicotinoids can affect the acetylcholine levels of honey bees, resulting in paralysis, loss of orientation and flight ability, and possibly even death [5,6]. Due to their systemic mode of action, approximately 73% of pollen and honey collected from beehives contained at least one neonicotinoid [7]. Furthermore, neonicotinoids are highly stable in water and soil and cannot be washed off before consumption, potentially endangering human health [3,[8][9][10]. ...
Article
Full-text available
A rapid, effective, and reliable method for the simultaneous detection of 20 neonicotinoids and their metabolites in infant foods has been developed using liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). To improve the accuracy and precision of the method, different extraction solvents, extraction methods, and adsorbents were evaluated to achieve a better recovery and clean-up effect. Under optimized conditions, the samples were extracted with acetic acid acidified acetonitrile/ethyl acetate by ultrasonication, and then were cleaned with reduced graphene oxide@Fe3O4 (rGO@Fe3O4) and primary and secondary amine (PSA) through a QuEChERS step. A matrix-matched calibration method was applied for quantification. Relative standard deviations were all <15% for intraday and interday precision. The values of limit of detection and limit of quantification were ranging from 0.02–0.35 μg·kg−1 and 0.1–1.0 μg·kg−1, respectively. The presented method was applied to the analysis of real samples.
... Recent studies have indicated that neonicotinoids can affect the acetylcholine levels of honey bees, resulting in paralysis, loss of orientation and ight ability, and possibly even death 5,6 . Due to their systemic mode of action, approximately 73% of pollen and honey collected from beehives contained at least one neonicotinoid 7 . Furthermore, neonicotinoids are highly stable in water and soil and cannot be washed off before consumption, potentially endangering human health 3,8−10 . ...
Preprint
Full-text available
A rapid, effective, and reliable method for the simultaneous detection of 20 neonicotinoids and their metabolites in infant foods has been developed using liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). To improve the accuracy and precision of the method, different extraction solvents, extraction methods, and adsorbents were evaluated to achieve a better recovery and clean-up effect. Under optimized conditions, the samples were extracted with acetic acid acidified acetonitrile/ethyl acetate by ultrasonication, and then were cleaned with reduced graphene oxide@Fe 3 O 4 (rGO@Fe 3 O 4 ) and primary and secondary amine (PSA) through a QuEChERS step. A matrix-matched calibration method was applied for quantification. In three different food matrixes (vegetable & fruit cookies, grain rice cereals, and vegetable purees), all the target compounds showed good linearity, both with values of r ² > 0.99. The average recovery of all neonicotinoids ranges from 68.0%~106.5% (vegetable & fruit cookies), 70.4%~105.4% (grain rice cereals), and 71.9%~107.4% (vegetable purees). Relative standard deviations were all < 15% for intraday and interday precision. The values of limit of detection and limit of quantification were, respectively, ranging from 0.02–0.35 µg kg − 1 and 0.1-1.0 µg kg − 1 . The presented method was applied to the analysis of real samples.
... IMD used for seed coating (Goulson, 2013) can be deposited in nectar and pollen with average concentrations of 0.9-41.9 ng/g (Bonmatin et al., 2005;Chauzat et al., 2011;Jiang et al., 2018;Lu et al., 2016;Stoner and Eitzer, 2012;Tong et al., 2018;Tosi et al., 2018) and affects the physiology of honey bees foraging on them (Colin et al., 2019;Cook, 2019;Demares et al., 2018;Eiri and Nieh, 2012;Li et al., 2019). A number of studies have reported the hazardous impacts and mechanisms of neonicotinoids on honey bees such as impairments of foraging behavior (Colin et al., 2019), proboscis extension reflex (Thany et al., 2015), immunity (Brandt et al., 2016;Christen and Fent, 2017), energy metabolism (Cook, 2019;Gooley and Gooley, 2020), development (Tome et al., 2020), and motility (Delkash-Roudsari et al., 2020). ...
Article
There have been many investigations on the negative effects of imidacloprid (IMD) on honey bees. IMD is known to disrupt honey bee physiology and colony health at a relatively low concentration compared to other pesticides. In this study, honey bee colonies were chronically exposed to field-realistic concentrations (5, 20, and 100 ppb) of IMD, and the body weight, flight performance, carbohydrate reserve, and lipid contents of forager bees analyzed. Transcriptome analyses followed by quantitative PCR were also conducted for both nurse and forager bees to elucidate any changes in energy metabolism related to phenotypic disorders. The body weights of newly emerged and nurse bees showed decreasing tendencies as the IMD concentration increased. In forager bees, however, IMD induced a biphasic change in body weight: body weight was decreased at the lower concentrations (5 and 20 ppb) but increased at the higher concentration (100 ppb). Nevertheless, the flight capability of forager bees significantly decreased in a concentration-dependent manner. The effects of IMD on target gene transcription in forager bees showed biphasic patterns between low (5 and 20 ppb) and high (100 ppb) concentrations. Nurse bees showed typical features of premature transition to foragers in a concentration-dependent manner. When exposed to low concentrations, forager bees exhibited downregulation of genes involved in carbohydrate and lipid metabolism and in the insulin/insulin-like growth factor signaling pathway, upregulation of transporter activity, and a dose-dependent body weight reduction, which were similar to insulin resistance and diabetic symptoms. However, increased lipid metabolism and decreased energy metabolism with body weight gain were observed at high IMD concentration. Considered together, these results suggest that field-realistic doses of IMD alter honey bee energy metabolism in distinctly different ways at low and high concentrations, both of which negatively affect honey bee colony health.
... Exposure of honey bees (Apis mellifera) to various environmental pesticides when they are collecting nectar and pollen represents a serious problem [1][2][3]. Honey bees can be affected by contaminated nectar and pollen that are brought back to the hive from foraging on flowers that have been sprayed with pesticides. Moreover, they are also affected by applications of medicine aimed at controlling the widespread honey bee parasite varroa mite (Varroa destructor), which has been closely linked to colony losses and the mortality of honey bees [4][5][6]. ...
Article
Full-text available
Fluvalinate is a widely used insecticide for varroa mite control in apiculture. While most beekeepers have ignored the effects of low levels of fluvalinate on bees, this study aims to demonstrate its effects at very low concentrations. We first used fluvalinate doses ranging from 0.4 to 400 ng/larva to monitor the capping, pupation, and emergence rates of larval bees. Second, we used the honey bees’ proboscis extension reflex reaction to test the learning ability of adult bees that were exposed to fluvalinate doses from 0.004 to 4 ng/larva in the larval stage. The brood-capped rate of larvae decreased dramatically when the dose was increased to 40 ng/larva. Although no significant effect was observed on brood-capping, pupation, and eclosion rates with a dose of 4 ng/larva, we found that the olfactory associative behavior of adult bees was impaired when they were treated with sublethal doses from 0.004 to 4 ng/larva in the larval stage. These findings suggest that a sublethal dose of fluvalinate given to larvae affects the subsequent associative ability of adult honey bee workers. Thus, a very low dose may affect the survival conditions of the entire colony.
... While longer exposure durations appear more likely to produce observable effects of pesticides on bee gut microbiotas, they may not always be field-realistic. Pesticides that are applied as seed coatings-such as neonicotinoids and some fungicidesmay be consistently present in agricultural environments over spring and summer months (Krupke et al. 2012;Lu et al. 2016). However, residues of pesticides applied via spray application may show temporal variation. ...
Article
Social bee gut microbiotas play key roles in host health and performance. Worryingly, a growing body of literature shows that pesticide exposure can disturb these microbiotas. Most studies examine changes in taxonomic composition in Western honey bee (Apis mellifera) gut microbiotas caused by insecticide exposure. Core bee gut microbiota taxa shift in abundance after exposure but are rarely eliminated, with declines in Bifidobacteriales and Lactobacillus near melliventris abundance being the most common shifts. Pesticide concentration, exposure duration, season and concurrent stressors all influence whether and how bee gut microbiotas are disturbed. Also, the mechanism of disturbance-i.e. whether a pesticide directly affects microbial growth or indirectly affects the microbiota by altering host health-likely affects disturbance consistency. Despite growing interest in this topic, important questions remain unanswered. Specifically, metabolic shifts in bee gut microbiotas remain largely uninvestigated, as do effects of pesticide-disturbed gut microbiotas on bee host performance. Furthermore, few bee species have been studied other than A. mellifera, and few herbicides and fungicides have been examined. We call for these knowledge gaps to be addressed so that we may obtain a comprehensive picture of how pesticides alter bee gut microbiotas, and of the functional consequences of these changes.
... Neonicotinoids, an emerging class of insecticides, were developed in the early 1980s, and in the 1990s, the first popularly available product in this class of chemicals, imidacloprid (IMI) was released (Jeschke & Nauen, 2008;Goulson, 2013). The active ingredient IMI, is found in a number of products such as Advocate, Confidor, Admire, Gaucho and Spectrum ( Elbert et al., 2008;Lu et al., 2015;Fauser et al., 2017). Owing to its low toxicity to mammals and high potency against target insects (Phugare et al., 2013), IMI insecticides are registered in more than 120 nations, including many Asian countries (Jeschke et al., 2011;Li et al., 2019;Mahai et al., 2019;Wang et al., 2020). ...
Thesis
Neonicotinoids are an emerging class of insecticides, with potential for aquatic toxicity, that have been used within the last decades as agrochemicals. These insecticides have been detected in Australian aquatic systems. Here I investigate the impacts of a neonicotinoid (imidacloprid) on Sydney rock oyster. There was a quick uptake of imidacloprid and a fast elimination when the exposed oysters were placed in clean water. Imidacloprid was found to impact a wide range of behavioural, physiological and biochemical parameters in oysters. The impact of imidacloprid on oysters was not compounded at mild salinity reduction or by other ingredients in a commercial formulation. This confirms that imidacloprid alone can impact oyster health.
... Chen et al. (2014b) showed that 72% of investigated fruits, 45% of vegetables and 50% of honey contained at least two different neonicotinoids in one sample. Similar results were obtained by Lu et al. (2015), showing that 49%, 20% and 4% of pollen samples collected across the Commonwealth of Massachusetts contained one, two and three neonicotinoids, respectively. Furthermore, 57 and 15% of honey samples contained one and two neonicotinoids, respectively. ...
Article
Neonicotinoid insecticides have been widely used in plant protection against pests worldwide. Generally, more than one neonicotinoids are detected in plants and foods, and such mixtures may show combined toxicity and increase the risk for both insects and higher organisms. In this study, the combined toxicity of imidacloprid (IM), acetamiprid (AC) and thiamethoxam (TH) was investigated using human neuroblastoma cell line (SK-N-SH) and lepidopteran cell line (Sf-9). Results showed that binary and ternary mixtures could enhance the inhibition of growth of both SK-N-SH and Sf-9 cells at low doses. In SK-N-SH cells, based on CompuSyn software analysis, all the mixtures of IM+AC, IM+TH, AC+TH and IM+AC+TH showed synergistic effects at concentrations < 50 mg/L, but IM+AC, IM+TH showed antagonistic effects at higher concentrations. For Sf-9 cells, all mixtures revealed synergistic effects at low concentrations (< 0.1 mg/L) except IM+AC, showing antagonism at higher concentrations (> 0.5 mg/L). The toxicity thresholds of mixtures denoted by BMDL10 values were all lower than those for single pesticides and the combined BMDL10 value of AC+TH was the lowest one. It is concluded that the co-occurrence of several neonicotinoid insecticides may enhance their toxicity and aggravate the health risk for both insects and human.
... The use of chemicals in urban gardens-fertilizers and pesticides often used to promote areas dominated by turf grassescan exceed that of farmland (Robbins and Sharp, 2003). Beehives in Suffolk County, Massachusetts, USA-where Boston is located-had the highest levels of neonicotinoid insecticides in pollen and honey samples collected from beehives across the state (Lu et al., 2016). Manufacturing, power generation, and other industrial activities can also produce high concentrations of heavy metal contaminants that accumulate in both bee's bodies and the honey they produce (Bogdanov, 2006;Skorbiłowicz et al., 2018). ...
... Only two statewide surveys of potential pesticide exposure in NNE (MA, ME) have been conducted (Lu et al. 2016. The results of these surveys of pollen contamination suggest that there is high variation among sites within states and among states. ...
Technical Report
Bees are crucial to pollination in unmanaged ecosystems and some crops, and their roles are increasingly understood in four states in the Northeastern U.S., abbreviated “NNE” in this paper: Maine (ME), Massachusetts (MA), New Hampshire (NH), and Vermont (VT). The four states have in common many native bee and plant species, forest types, and natural communities. They share drought events and risk of wildfire (Irland 2013). They are exposed to many of the same major storms (e.g., hurricanes, Foster 1988), pollution events (Hand et al. 2014), and effects ascribed to climate change (Hayhoe et al. 2008). Beekeeping enterprises (the western honey bee, Apis mellifera, an introduced species) of various sizes exist in each of the states. By including the four states in this review, we hope to better understand wild bee distributions, inspire the expansion of floral resources to support bee populations in a strategic manner, reduce use of pesticides, create pollinator corridors, and protect subtle habitat features such as ground nest sites for solitary bees and patches of native vegetation that are free of invasive plants. Our objective in this review is to synthesize from a conservation standpoint the state of knowledge regarding bees in NNE, including their diversity, and biology especially as it relates to climate change. We review foraging and nutrition, nest ecology, parasites and parasitoids, native vs. managed bees, and interactions with plants. We then turn our focus to bee habitats, and identify 15 habitat types we find useful for recognizing essential bee resources. We discuss habitat aspects including forest succession, invasive plants, land use alterations, and agriculture including impacts of pesticides, and cover economic aspects of crop-related pollination reservoirs in NNE that demonstrate cost-effectiveness at various scales. We present habitat improvement strategies including passive and active approaches, based on the literature and our experiences in NNE, and we suggest plants for pollinator plantings. Wherever pertinent throughout the text, we highlight threats to bees in our region such as pests and pathogens, pesticides, and habitat loss. Finally, we identify gaps in knowledge that could help in prioritizing directions for future research. We hope this review will be useful to anyone seeking to protect bees and their habitats.
... 29 Several suggestions of the possible causes have been made, including extensive monoculture, genetically modified crops and pesticides. 30,31 As a result, the use of three neonicotinoids have been banned for outdoor use in Europe. 32 Fluralaner shows excellent biological activity to many insect pests and may provide an alternative choice in the control of insect pests in an agricultural setting. ...
Article
BACKGROUD Fluralaner, a novel pesticide that targets the γ‐aminobutyric acid (GABA) receptor subunit of resistant to dieldrin (RDL), exhibits strong potential to be an insecticide to control agricultural insect pests. However, the risk and action of fluralaner to economic insects, e.g., honeybee Apis mellifera Linnaeus, remains unclear. RESULTS In this study, both oral and contact toxicity of fluralaner to honeybee were found to be 0.13 μg adult‐1. Abamectin, dieldrin, ethiprole, α‐endosulfan, fipronil and fluralaner strongly inhibited the GABA‐induced current in A. mellifera RDL (AmRDL), expressed in Xenopus laevis oocytes, with median inhibitory concentration (IC50) values of 7.99, 868.1, 27.10, 412.0, 11.21 and 13.59 nM, respectively. The binding free energy and electrophysiological response of AmRDL and insecticides were opposite. The correlation values between toxicity (to A. mellifera) and binding free energy/electrophysiological inhibition (to AmRDL) were at a moderate level. CONCLUSION In conclusion, we report for the first time the notable risk of fluralaner to honeybee in vivo and compared the actions of GABAR‐targeted insecticides on the AmRDL receptor. (Words count: 167) This article is protected by copyright. All rights reserved.
... For total NNIs, we utilized the RPFs for integrating six individual NNIs detected in water sample into a single measurement as IMI eq (IMI-equivalent total NNIs) (Lu et al., 2016) which was calculated using equation (2): ...
... Zero detection of neonicotinoids in PDP honey samples from 1999 to 2015 in our analysis stands in stark contrast with small studies led by others [28,58]. Given the systemic properties of neonicotinoids, these pesticides can penetrate and translocate through the plant including pollen and nectar [14,54,59]. Bees rely on nectar and pollen for energy and use nectar from flowers to make honey. ...
Article
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Background Neonicotinoids are a class of systemic insecticides widely used on food crops globally. These pesticides may be found in “off-target” food items and persist in the environment. Despite the potential for extensive human exposure, there are limited studies regarding the prevalence of neonicotinoid residues in foods sold and consumed in the United States. Methods Residue data for seven neonicotinoid pesticides collected between 1999 and 2015 by the US Department of Agriculture’s Pesticide Data Program (PDP) were collated and summarized by year across various food commodities, including fruit, vegetable, meat, dairy, grain, honey, and baby food, as well as water to qualitatively describe and examine trends in contamination frequency and residue concentrations. Results The highest detection frequencies (DFs) for neonicotinoids by year on all commodities were generally below 20%. Average DFs over the entire study period, 1999–2015, for domestic and imported commodities were similar at 4.5%. For all the samples (both domestic and imported) imidacloprid was the neonicotinoid with the highest overall detection frequency at 12.0%. However, higher DFs were observed for specific food commodity-neonicotinoid combinations such as: cherries (45.9%), apples (29.5%), pears (24.1%) and strawberries (21.3%) for acetamiprid; and cauliflower (57.5%), celery (20.9%), cherries (26.3%), cilantro (30.6%), grapes (28.9%), collard greens (24.9%), kale (31.4%), lettuce (45.6%), potatoes (31.2%) and spinach (38.7%) for imidacloprid. Neonicotinoids were also detected in organic commodities, (DF < 6%). Individual commodities with at least 5% of samples testing positive for two or more neonicotinoids included apples, celery, and cherries. Generally, neonicotinoid residues on food commodities did not exceed US Environmental Protection Agency tolerance levels. Increases in detection trends for both finished and untreated water samples for imidacloprid were observed from 2004 to 2011. Conclusions Analysis of PDP data indicates that low levels of neonicotinoids are present in commonly-consumed fruits and vegetables sold in the US. Trends in detection frequencies suggest an increase in use of acetamiprid, clothianidin and thiamethoxam as replacements for imidacloprid. Given these findings, more extensive surveillance of the food and water supply is warranted, as well as biomonitoring studies and assessment of cumulative daily intake in high risk groups, including pregnant women and infants. Electronic supplementary material The online version of this article (10.1186/s12940-018-0441-7) contains supplementary material, which is available to authorized users.
... In another study, survival was unaffected by oral imidacloprid exposure in honey bees fed pollen-supplemented diets, whereas mortality increased in those simultaneously exposed to dietary imidacloprid and protein-lacking diets [16]. Together, these results suggest that pollen as a dietary constituent is critical for mitigating stress associated with sublethal neonicotinoid exposures, which are found in bee-collected pollen worldwide [North America: Mogren and Lundgren [5], Lu, Chang [29], Codling, Al Naggar [30]; Europe: Botías, David [6], David, Botías [31], Sánchez-Hernández, Hernández-Domínguez [32], Tosi, Costa [33]; Africa: Codling, Al Naggar [34]]. ...
Article
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Neonicotinoid insecticides have come under scrutiny for their potential role in honey bee declines. Additionally, reduced access to forage in agricultural areas creates the potential for risk interactions with these pesticides in regions critical for honey production. In this study, we sought to determine whether sufficient access to pollen during larval development could mitigate stress associated with oral clothianidin exposure in honey bee adults. An apiary was established where pollen traps deprived half of the colonies of pollen, which was then supplemented to the others. Adults were fed 0, 10, 40, 200, or 400 µg/L clothianidin in the laboratory, and larval and adult lipids and superoxide dismutase (SOD) activities were compared between feeding treatments. Survival at sublethal concentrations of clothianidin was significantly reduced for adult bees reared in pollen deprived colonies. Adult SOD activity was affected by clothianidin dose but not larval feeding treatment, though within the pollen-deprived cohort, SOD was greater in controls than those fed clothianidin. Larval SOD differed between field replicates, with supplemented colonies having slightly higher activity levels during a period of pollen dearth, indicating that supplementation during these periods is particularly important for mitigating oxidative stress within the hive. Larval lipids were significantly higher in supplemented colonies during a substantial pollen flow, though adult lipids were unaffected by feeding treatment. These results suggest that during periods of pollen dearth, oxidative stress and adult worker longevity will be improved by supplementing colonies with locally collected pollen.
... Only two statewide surveys of potential pesticide exposure in NNE (MA, ME) have been conducted (Lu et al. 2016. The results of these surveys of pollen contamination suggest that there is high variation among sites within states and among states. ...
Technical Report
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Four states contain over 401 species of bees, about which little is known except for a few common species. Forests of Maine, Massachusetts, New Hampshire, and Vermont were largely cleared in colonial times, then trees grew back as of the 1870s. Canopy closure, urbanization, and intensive agriculture have led to reduced habitats for bees. Managed and wild bees of the region are found especially in forest openings. Many visit flowers across different plant species, though an estimated 15% visit only one or a few plant taxa. Because bee life histories, population dynamics, and host plant relations are incompletely known, an emphasis on habitat is appropriate because the environment can be manipulated. We list 15 bee habitats with natural and anthropogenic features, and suggest 40 plant taxa that may be effective in plantings for bees. Pollination systems in two native crops, lowbush blueberry (Vaccinium angustifolium) and cranberry (V. macrocarpon), are better-studied than most crops; from these we developed an economic perspective on altering habitat to support bees. Threats to bees include habitat loss, pests and pathogens, pesticides, and climate change. We consider practical aspects for improving pollinator habitats. The adoption of suggested habitat improvements will help meet goals in bee conservation and pollination security, and could aid in protecting pollination of the native flora. We identify gaps in knowledge to help prioritize future research directions.
... Two recent studies using honey bees to sample pollen from landscapes in the Northeast and Northwest U. S. found levels of contamination of about 2 ppb for imidacloprid, and approximately 6 ppb for imidacloprid equivalents, when combining the exposure risk from all neonicotinoid insecticides into imidacloprid toxicity equivalents (Lu et al. 2015;Lawrence et al. 2016). These empirical data indicate that current use practices for neonicotinoids do not generally result in hazardous exposure for honey bees. ...
Article
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Systemic insecticides used for ornamental horticulture crops can protect all portions of a plant with long-lasting effects. However, they may be hazardous to pollinators foraging on contaminated nectar or pollen. Two model plant cultivars were chosen based upon their ability to produce large quantities of pollen or nectar, enabling examination of the level of nectar or pollen contamination (e.g., insecticide “residues”) following insecticide treatments, rather than for the need or advisability to treat these plants in production nurseries or the landscape with systemic insecticides. These plants were sunflower (Helianthus annuus L. ‘Taiyo') for pollen, and swamp milkweed (Asclepius incarnata L. ‘Ice Ballet') for nectar. Plants were treated at labeled nursery rates with imidacloprid, dinotefuran, or thiamethoxam via foliar spray or soil drench at various times before bloom. Insecticide residues from pollen and nectar varied based upon application method, insecticide, and rate. Assuming that residues should be considered hazardous when they exceed 25 parts per billion (ppb) for nectar or 100 ppb for pollen, potentially bee-toxic concentrations of insecticide in sunflower pollen only followed high-rate drench treatments. Toxic concentrations of neonicotinoids were found in milkweed nectar when applied either as a drench or as a foliar spray up to six weeks before bloom. Label directions for nursery and greenhouse plants permit very high application rates relative to agronomic crops. These high rates can create hazardous conditions for pollinators, and should be avoided for ornamental crops that are highly attractive to bees. Index words: sunflower (Helianthus annuus L.); swamp milkweed (Asclepius incarnata L.); dinotefuran; imidacloprid; thiamethoxam; pollinator; systemic insecticides. Chemicals used in this study: dinotefuran (Safari 20 SG); imidacloprid (Xytect 2F); thiamethoxam (Flagship 25 WG). Species used in this study: sunflower (Helianthus annuus L.); swamp milkweed (Asclepius incarnata L.).
... The presence of pesticides in the environment is one of the most serious problems that impacts the life of a honey bee [1][2][3] . Several studies have demonstrated the common presence of pesticide residues in honey bee colonies and bee products. ...
Article
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The presence of pesticides in the beekeeping environment is one of the most serious problems that impacts the life of a honey bee. Pesticides can be brought back to the beehive after the bees have foraged on flowers that have been sprayed with pesticides. Pesticide contaminated food can be exchanged between workers which then feed larvae and therefore can potentially affect the development of honey bees. Thus, residual pesticides in the environment can become a chronic damaging factor to honey bee populations and gradually lead to colony collapse. In the presented protocol, honey bee feeding methods are described and applied to either an individual honey bee or to a colony. Here, the insect growth regulator (IGR) pyriproxyfen (PPN), which is widely used to control pest insects and is harmful to the development of honey bee larvae and pupae, is used as the pesticide. The presenting procedure can be applied to other potentially harmful chemicals or honeybee pathogens for further studies.
... Pollen traps 52 (Rortais et al., 2005;Cutler and Scott-Dupree, 2007;Jiménez et al., 2007;Rose et al., 2007, Chauzat et al., 2009Mullin et al., 2010;Bernal et al., 2011;Chauzat et al., 2011;Wiest et al., 2011;Krupke et al., 2012;Pohorecka et al., 2012;Boily et al., 2013;Degrandi-Hoffman et al., 2013;Johnson and Percel, 2013;Pettis et al., 2013;Pilling et al., 2013;Pohorecka et al., 2013;Stoner and Eitzer, 2013;Byrne et al., 2014;Sandrock et al., 2014;Stewart et al., 2014;Thompson, Levine, et al., 2014;Zhu et al., 2014;Alburaki et al., 2015;Botias et al., 2015;Degrandi-Hoffman et al., 2015;Dively et al., 2015;Frazier et al., 2015;Lu et al., 2015;Williams et al., 2015;David et al., 2016;Thompson et al., 2016) Not specified 14 (Liu et al., 2009;Han et al., 2010a;Chen and Mullin, 2013;2014;Costa et al., 2014;Sanchez-Bayo and Goka, 2014;Chen et al., 2015;Dolezal et al., 2015;Vázquez et al., 2015) Sampling of anthers 13 (Rose et al., 2007;Han et al., 2010b;Mullin et al., 2010;Krupke et al., 2012;Stoner and Eitzer, 2012;Gillespie et al., 2014;Botias et al., 2015;Renzi et al., 2016) Collecting pollen from brood combs 4 ( Bernal et al., 2010;Kasiotis et al., 2014;Muli et al., 2014;Li et al., 2015) Collecting pollen from any combs 3 Krupke et al., 2012;Codling et al., 2016) Collecting pollen in beebread 3 Al-Naggar, Codling, et al., 2015;Pistorius et al., 2015) Using craft bags around the flowers 2 ( Dively and Kamel, 2012;Gillespie et al., 2014) Bees-wax 25 ...
Article
Losses of honey bees have been repeatedly reported from many places worldwide. The widespread use of synthetic pesticides has led to concerns regarding their environmental fate and their effects on pollinators. Based on a standardised review, we report the use of a wide variety of honey bee matrices and sampling methods in the scientific papers studying pesticide exposure. Matrices such as beeswax and beebread were very little analysed despite their capacities for long-term pesticide storage. Moreover, bioavailability and transfer between in-hive matrices were poorly understood and explored. Many pesticides were studied but interactions between molecules or with other stressors were lacking. Sampling methods, targeted matrices and units of measure should have been, to some extent, standardised between publications to ease comparison and cross checking. Data on honey bee exposure to pesticides would have also benefit from the use of commercial formulations in experiments instead of active ingredients, with a special assessment of co-formulants (quantitative exposure and effects). Finally, the air matrix within the colony must be explored in order to complete current knowledge on honey bee pesticide exposure.
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Agricultural chemicals have compromised the climate, human and animal health, groundwater aquifers, and recreational potential of water bodies. Digestate is a possible agent to attenuate external costs imposed on the biosphere by chemical fertilizers. However, nutrient speciation of digestate derived from anaerobic digestion (AD) of cassava peeling residue (CPR) as sole feedstock is not found in published literature. Also unknown is to what extent CPR digestate could substitute inorganic fertilizers in cassava root production. In this study, external costs of agricultural production technologies are thoroughly highlighted. AD experiments were conducted to quantify macronutrients composition of liquid fraction digestate of CPR as sole feedstock. Capability of liquid fraction digestate of CPR to supplant chemical fertilizers in cassava root production was also evaluated. Results indicate that total kjeldahl nitrogen, total phosphorus, and total potassium content are, respectively, 573 mg/L, 31 mg/L, and 1066 mg/L. Also, likely up to 28% nitrogen, 11% phosphorus, and 38% potassium sourced from chemical fertilizers for cassava root production could be replaced with liquid fraction CPR digestate. The results could be used to influence contribution of CPR to the outcome of AD operations when co-digested with other feedstocks; thereby empowering process optimization. The results may also enable typology criteria for quality assurance and regulatory standards for liquid fraction CPR digestate. This paper is potentially the first to report nutrients value of liquid fraction of mono feedstock CPR digestate; and the first to quantify the nutrients capability to supplant inorganic fertilizers in cassava root production. Graphical abstract Schematic visualization of the objectives and summary of this paper
Article
Organofosfatlı ve karbamatlı insektisitlere alternatif olarak geliştirilen neonikotinoidler, günümüzde dünya çapında en yaygın kullanılan insektisit sınıfı olup polen ve nektar dâhil bitkilerin tüm kısımlarına geçerek bu bitkiler tarafından üretilen ürünlere ve hatta arı ürünlerine aktarılabilmektedir. Bu sistemik özellikleriyle neonikotinoidler, bal arıları ve yabani arılar gibi canlıların yanı sıra, insanlar dahil diğer omurgalılar üzerinde de olumsuz etkilere yol açmaktadır. Bu nedenle hangi türevlerinin ne oranda etki oluşturduğuna ilişkin araştırmalar son yıllarda hızla artmakta ve bu çalışma sonuçlarına göre farklı ülkelerde neonikotinoid kullanımlarına yasaklar ve kısıtlamalar getirilmektedir. Bu çalışmanın amacı Türkiye’de üretilen ballarda neonikotinoid varlığının ve dolayısıyla çevredeki kirlilik seviyesinin ölçülmesidir. Bu amaçla, hasat sonrası Türkiye’nin farklı illerindeki arı yetiştiricilerinden direkt temin edilen 44 bal örneği materyal olarak kullanılmıştır. Örneklerde acetamiprid, clothianidin, dinotefuran, imidacloprid, nitenpyram, thiacloripid ve thiamethoxam varlığı Sıvı Kromatografi Kuadrupol Uçuş Zamanlı Kütle Spektrometresi (LC-MS Q-TOF) kullanılarak araştırılmıştır. Analiz edilen örneklerin hiçbirinde neonikotinoid grubu insektisitlere rastlanmamıştır. Analiz edilen örneklerde neonikotinoidlere rastlanmaması Türkiye açısından umut verici bir bulgudur. Neonikotinoidlerin kullanım şekilleri ve canlı organizmalara etkileri üzerine artan araştırmalar yanında, çevresel varlığının da düzenli olarak takip edilmesi ve limitlerin belirlenmesinin, halk sağlığının korunması açısından önemli olduğu düşünülmektedir.
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Neonicotinoids, a group of widely used systemic insecticides worldwide, have been shown as one of the risk factors to honeybee colony collapse disorder (CCD). Although the exact underlying mechanisms of honeybee (Apis mellifera) colony collapse disorder (CCD) have yet been confirmed, we postulated that mitochondrial DNA (mtDNA) damage in honeybees resulting from sub-lethal neonicointoids (neonics) exposure could be a plausible cause leading to malfunctioned thermoregulation. In this study, we demonstrated using relative mitochondrial DNA copy number (RmtDNAcn) as an early biomarker to elucidate the association between chronic sub-lethal neonicotinoid exposure and mtDNA damage in honeybees. We collected adult worker bees collected from hives that were exposed to either sub-lethal level of imidacloprid, clothianidin, or control in three different brood generations coincided with before, during, and after treatments. Although there were no apparent adverse health effects in individual bees or the whole colony during and after neonics administration, the cumulative mtDNA damage in winter bees might have negatively impacted their hives’ survival over winter due to the perturbation of energy metabolism. Those results shall contribute to the explanation of potential mechanism of CCD.
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Neonicotinoids (Neonics) have become the most widely used insecticides around the world in recent years. Due to the hydrophilic character, neonics are emerging contaminants in drinking water. In this study, we aimed to characterize and quantify the fate and transport of neonics in the drinking water treatment system and their contributions to the overall dietary risks. Seven neonics in 97 surface and drinking water samples in the city of Hangzhou, China were analyzed. The relative potency factor method was adopted in order to calculate the total neonics concentrations. We then used the Monte Carlo simulation to calculate the chronic daily intake (CDI) of total neonics from water consumption. All 16 surface water samples collected from two rivers contained at least two neonics, and more than 93% of those contained 3 or more neonics. Imidacloprid was detected in all 16 surface water samples, followed by clothianidin and acetamiprid with average concentrations of 11.9, 7.6, 17.6 ng L-1, respectively. The drinking water treatment plants removed approximately 50% of neonics from surface water. However, 68 out of 71 tap water samples that we collected from the household faucets contained at least one neonic, with the highest average concentrations of 5.8 ng L-1 for acetamiprid. The maximum of CDIs of total neonics from water consumption for adult and children were 10.2 and 12.4 ng kg-1 d-1, respectively, which are significantly lower than the acceptable daily intake (ADI). The results presented here shown drinking water consumption only represented an insignificant portion of dietary risks of total neonics, mainly due to the modern drinking water treatment technologies that are capable of removing significant amount of neonics from drinking water. However, the ubiquity of neonics in the drinking water sources to kitchen faucets, should be a concern for public health.
Article
Recent studies have shown that neonicotinoids in pollen and honey (collected by honeybees)are likely to pose risks to honeybees. However, data on the integrated residue and spatial-temporal variation of neonicotinoids from noncrop plants, the principle sources of pollen for honey bees, are very limited, especially in China. In this study, we employed a novel assessment method based on the relative potency factor to calculate the integrated residue of seven neonicotinoids in pollen and honey samples collected from noncrop plants in 12 stations of Zhejiang province in three consecutive months. The integrated concentration of neonicotinoids (IMI RPF )ranged from no detected (ND)to 34.93 ng/g in pollen and ND to 8.51 ng/g in honey. Acetamiprid showed the highest detection frequency of 41.7%, followed by clothianidin (33.3%)and dinotefuran (22.2%). The highest IMI RPF occurred in April for stations in the fringe areas of Zhejiang province, whereas for stations in the central areas of Zhejiang province, the IMI RPF in May was relatively higher than the other two months. In terms of spatial change, the pollution variation of pollen samples in Lin'an—Tonglu—Pujiang was relative highly polluted—lightly polluted—highly polluted. For honey samples, spatial variation showed a single trend, and peak values were found in Wenzhou, which may be attributed to the local climate and farming practices. This fundamental information will be helpful to understand the effects of neonicotinoids on honeybees foraging habits.
Article
Although neonicotinoids have been the most commonly used insecticides globally, very limited data related to their dietary intake and health risks are available. In this study, we used the relative potency factor approach to aggregate individual neonicotinoids into a single metric (IMIRPF) representing the intakes of total neonicotinoids in relation to imidacloprid for each food item. We then estimated the average daily intake (ADI) of neonicotinoids using residue data collected from US Congressional Cafeteria study (USCC) and USDA/PDP, and food consumption data from NHANES 2011–2012. Among the USCC and USDA/PDP samples, squash (427.2 ng/g) and spinach (569.2 ng/g), had the highest average IMIRPF, respectively. The estimated ADIs were below the current chronic reference dose (cRfD) for imidacloprid. However, due to their wide use, it is logical to expect the ubiquity of neonicotinoids in foods. Therefore, the importance of conducting routine dietary intake assessment for neonicotinoids should not be ignored.
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Neonicotinoids have become the most widely used insecticides in the world since introduced in the mid-1990s, and yet the extent of human exposure and health impacts is not fully understood. In this study, the residues of seven neonicotinoids in fruit and vegetable samples collected from two cross-sectional studies, the U.S. Congressional Cafeteria study (USCS) and the Hangzhou China (HZC) study, were analyzed. We then employed a relative potency factor method to integrate all neonicotinoids in each food sample using the respective reference dose values as the basis for summation. The findings were compared with data published by the U.S. Department of Agriculture Pesticide Data Program (USDA/PDP). Imidacloprid and thiamethoxam were the most commonly detected neonicotinoids in fruits and vegetables with 68% and 51% detection in the HZC study, and 59% and 56% detection in the USCC study, respectively. The overall frequency of detection for neonicotinoids in the USDA/PDP samples was much lower than those reported here for the USCS or HZC studies, with imidacloprid the most frequently detected neonicotinoid at 7.3%. The high frequencies of neonicotinoid detection in fruits and vegetables in the USCC and HZC studies give us a snapshot of the ubiquity of neonicotinoid use in global agriculture and make it clear that neonicotinoids have become part of the dietary staple, with possible health implications for individuals as well.
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Concern is growing over the effects of neonicotinoid pesticides, which can impair honey bee cognition. We provide the first demonstration that sublethal concentrations of imidacloprid can harm honey bee decision-making about danger by significantly increasing the probability of a bee visiting a dangerous food source. Apis cerana is a native bee that is an important pollinator of agricultural crops and native plants in Asia. When foraging on nectar containing 40 µg/L (34 ppb) imidacloprid, honey bees (Apis cerana) showed no aversion to a feeder with a hornet predator, and 1.8 fold more bees chose the dangerous feeder as compared to control bees. Control bees exhibited significant predator avoidance. We also give the first evidence that foraging by A. cerana workers can be inhibited by sublethal concentrations of the pesticide, imidacloprid, which is widely used in Asia. Compared to bees collecting uncontaminated nectar, 23% fewer foragers returned to collect the nectar with 40 µg/L imidacloprid. Bees that did return respectively collected 46% and 63% less nectar containing 20 µg/L and 40 µg/L imidacloprid. These results suggest that the effects of neonicotinoids on honey bee decision-making and other advanced cognitive functions should be explored. Moreover, research should extend beyond the classic model, the European honey bee (A. mellifera), to other important bee species.
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Systemic pesticides such as neonicotinoids are commonly used on flowering crops visited by pollinators, and their use has been implicated in the decline of insect pollinator populations in Europe and North America. Several studies show that neonicotinoids affect navigation and learning in bees but few studies have examined whether these substances influence their basic motor function. Here, we investigated how prolonged exposure to sublethal doses of four neonicotinoid pesticides (imidacloprid, thiamethoxam, clothianidin, dinotefuran) and the plant toxin, nicotine, affect basic motor function and postural control in foraging-age worker honeybees. We used doses of 10 nM for each neonicotinoid: field-relevant doses that we determined to be sublethal and willingly consumed by bees. The neonicotinoids were placed in food solutions given to bees for 24 h. After the exposure period, bees were more likely to lose postural control during the motor function assay and fail to right themselves if exposed to imidacloprid, thiamethoxam, clothianidin. Bees exposed to thiamethoxam and nicotine also spent more time grooming. Other behaviours (walking, sitting and flying) were not significantly affected. Expression of changes in motor function after exposure to imidacloprid was dose-dependent and affected all measured behaviours. Our data illustrate that 24 h exposure to sublethal doses of neonicotinoid pesticides has a subtle influence on bee behaviour that is likely to affect normal function in a field setting.
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Imidacloprid, one of the most commonly used insecticides, is highly toxic to bees and other beneficial insects. The regulatory challenge to determine safe levels of residual pesticides can benefit from information about the time-dependent toxicity of this chemical. Using published toxicity data for imidacloprid for several insect species, we construct time-to-lethal-effect toxicity plots and fit temporal power-law scaling curves to the data. The level of toxic exposure that results in 50% mortality after time t is found to scale as t1.7 for ants, from t1.6 to t5 for honeybees, and from t1.46 to t2.9 for termites. We present a simple toxicological model that can explain t2 scaling. Extrapolating the toxicity scaling for honeybees to the lifespan of winter bees suggests that imidacloprid in honey at 0.25 mg/kg would be lethal to a large proportion of bees nearing the end of their life.
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Microbial pathogens are thought to have a profound impact on insect populations. Honey bees are suffering from elevated colony losses in the northern hemisphere possibly because of a variety of emergent microbial pathogens, with which pesticides may interact to exacerbate their impacts. To reveal such potential interactions, we administered at sublethal and field realistic doses one neonicotinoid pesticide (thiacloprid) and two common microbial pathogens, the invasive microsporidian Nosema ceranae and black queen cell virus (BQCV), individually to larval and adult honey bees in the laboratory. Through fully crossed experiments in which treatments were administered singly or in combination, we found an additive interaction between BQCV and thiacloprid on host larval survival likely because the pesticide significantly elevated viral loads. In adult bees, two synergistic interactions increased individual mortality: between N. ceranae and BQCV, and between N. ceranae and thiacloprid. The combination of two pathogens had a more profound effect on elevating adult mortality than N. ceranae plus thiacloprid. Common microbial pathogens appear to be major threats to honey bees, while sublethal doses of pesticide may enhance their deleterious effects on honey bee larvae and adults. It remains an open question as to whether these interactions can affect colony survival.
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Three neonicotinoids, imidacloprid, clothianidin and thiacloprid, agonists of the nicotinic acetylcholine receptor in the central brain of insects, were applied at non-lethal doses in order to test their effects on honeybee navigation. A catch-and-release experimental design was applied in which feeder trained bees were caught when arriving at the feeder, treated with one of the neonicotinoids, and released 1.5 hours later at a remote site. The flight paths of individual bees were tracked with harmonic radar. The initial flight phase controlled by the recently acquired navigation memory (vector memory) was less compromised than the second phase that leads the animal back to the hive (homing flight). The rate of successful return was significantly lower in treated bees, the probability of a correct turn at a salient landscape structure was reduced, and less directed flights during homing flights were performed. Since the homing phase in catch-and-release experiments documents the ability of a foraging honeybee to activate a remote memory acquired during its exploratory orientation flights, we conclude that non-lethal doses of the three neonicotinoids tested either block the retrieval of exploratory navigation memory or alter this form of navigation memory. These findings are discussed in the context of the application of neonicotinoids in plant protection.
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Populations of honey bees and other pollinators have declined worldwide in recent years. A variety of stressors have been implicated as potential causes, including agricultural pesticides. Neonicotinoid insecticides, which are widely used and highly toxic to honey bees, have been found in previous analyses of honey bee pollen and comb material. However, the routes of exposure have remained largely undefined. We used LC/MS-MS to analyze samples of honey bees, pollen stored in the hive and several potential exposure routes associated with plantings of neonicotinoid treated maize. Our results demonstrate that bees are exposed to these compounds and several other agricultural pesticides in several ways throughout the foraging period. During spring, extremely high levels of clothianidin and thiamethoxam were found in planter exhaust material produced during the planting of treated maize seed. We also found neonicotinoids in the soil of each field we sampled, including unplanted fields. Plants visited by foraging bees (dandelions) growing near these fields were found to contain neonicotinoids as well. This indicates deposition of neonicotinoids on the flowers, uptake by the root system, or both. Dead bees collected near hive entrances during the spring sampling period were found to contain clothianidin as well, although whether exposure was oral (consuming pollen) or by contact (soil/planter dust) is unclear. We also detected the insecticide clothianidin in pollen collected by bees and stored in the hive. When maize plants in our field reached anthesis, maize pollen from treated seed was found to contain clothianidin and other pesticides; and honey bees in our study readily collected maize pollen. These findings clarify some of the mechanisms by which honey bees may be exposed to agricultural pesticides throughout the growing season. These results have implications for a wide range of large-scale annual cropping systems that utilize neonicotinoid seed treatments.
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Global pollinators, like honeybees, are declining in abundance and diversity, which can adversely affect natural ecosystems and agriculture. Therefore, we tested the current hypotheses describing honeybee losses as a multifactorial syndrome, by investigating integrative effects of an infectious organism and an insecticide on honeybee health. We demonstrated that the interaction between the microsporidia Nosema and a neonicotinoid (imidacloprid) significantly weakened honeybees. In the short term, the combination of both agents caused the highest individual mortality rates and energetic stress. By quantifying the strength of immunity at both the individual and social levels, we showed that neither the haemocyte number nor the phenoloxidase activity of individuals was affected by the different treatments. However, the activity of glucose oxidase, enabling bees to sterilize colony and brood food, was significantly decreased only by the combination of both factors compared with control, Nosema or imidacloprid groups, suggesting a synergistic interaction and in the long term a higher susceptibility of the colony to pathogens. This provides the first evidences that interaction between an infectious organism and a chemical can also threaten pollinators, interactions that are widely used to eliminate insect pests in integrative pest management.
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The death of honey bees, Apis mellifera L., and the consequent colony collapse disorder causes major losses in agriculture and plant pollination worldwide. The phenomenon showed increasing rates in the past years, although its causes are still awaiting a clear answer. Although neonicotinoid systemic insecticides used for seed coating of agricultural crops were suspected as possible reason, studies so far have not shown the existence of unquestionable sources capable of delivering directly intoxicating doses in the fields. Guttation is a natural plant phenomenon causing the excretion of xylem fluid at leaf margins. Here, we show that leaf guttation drops of all the corn plants germinated from neonicotinoid-coated seeds contained amounts of insecticide constantly higher than 10 mg/l, with maxima up to 100 mg/l for thiamethoxam and clothianidin, and up to 200 mg/l for imidacloprid. The concentration of neonicotinoids in guttation drops can be near those of active ingredients commonly applied in field sprays for pest control, or even higher. When bees consume guttation drops, collected from plants grown from neonicotinoid-coated seeds, they encounter death within few minutes.
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Although sublethal dosages of insecticide to nontarget insects have never been an important issue, they are attracting more and more attention lately. It has been demonstrated that low dosages of the neonicotinoid insecticide imidacloprid may affect honey bee, Apis mellifera L., behavior. In this article, the foraging behavior of the honey bee workers was investigated to show the effects of imidacloprid. By measuring the time interval between two visits at the same feeding site, we found that the normal foraging interval of honey bee workers was within 300 s. However, these honey bee workers delayed their return visit for > 300 s when they were treated orally with sugar water containing imidacloprid. This time delay in their return visit is concentration-dependent, and the lowest effective concentration was found to be 50 microg/liter. When bees were treated with an imidacloprid concentration higher than 1,200 microg/liter, they showed abnormalities in revisiting the feeding site. Some of them went missing, and some were present again at the feeding site the next day. Returning bees also showed delay in their return trips. Our results demonstrated that sublethal dosages of imidacloprid were able to affect foraging behavior of honey bees.
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Acetamiprid and thiamethoxam are insecticides introduced for pest control, but they can also affect non-target insects such as honeybees. In insects, these neonicotinoid insecticides are known to act on acetylcholine nicotinic receptors but the behavioral effects of low doses are not yet fully understood. The effects of acetamiprid and thiamethoxam were studied after acute sublethal treatment on the behavior of the honeybee (Apis mellifera) under controlled laboratory conditions. The drugs were either administered orally or applied topically on the thorax. After oral consumption acetamiprid increased sensitivity to antennal stimulation by sucrose solutions at doses of 1 microg/bee and impaired long-term retention of olfactory learning at the dose of 0.1 microg/bee. Acetamiprid thoracic application induced no effect in these behavioral assays but increased locomotor activity (0.1 and 0.5 microg/bee) and water-induced proboscis extension reflex (0.1, 0.5, and 1 microg/bee). Unlike acetamiprid, thiamethoxam had no effect on bees' behavior under the conditions used. Our results suggest a particular vulnerability of honeybee behavior to sublethal doses of acetamiprid.
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In this study, we quantitatively measured neonicotinoids in various foods that are common to human consumption. All fruit and vegetable samples (except nectarine and tomato) and 90% of honey samples were detected positive for at least one neonicotinoid; 72% of fruits, 45% of vegetables and 50% of honey samples contained at least two different neonicotinoids in one sample, with imidacloprid having the highest detection rate among all samples. All pollen samples from New Zealand contained multiple neonicotinoids and 5 out of 7 pollen from Massachusetts detected positive for imidacloprid. These results show the prevalent presence of low level neonicotinoid residues in fruits, vegetables and honey that are readily available in the market for human consumption and in the environment where honeybees forage. In light of the new reports of toxicological effects in mammals, our results strengthen the importance to assess dietary neonicotinoid intakes and the potential human health effects.
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Pollinating insects provide crucial and economically important ecosystem services to crops and wild plants, but pollinators, particularly bees, are globally declining as a result of various driving factors, including the prevalent use of pesticides for crop protection. Sublethal pesticide exposure negatively impacts numerous pollinator life-history traits, but its influence on reproductive success remains largely unknown. Such information is pivotal, however, to our understanding of the long-term effects on population dynamics.We investigated the influence of field-realistic trace residues of the routinely used neonicotinoid insecticides thiamethoxam and clothianidin in nectar substitutes on the entire life-time fitness performance of the red mason bee Osmia bicornis.We show that chronic, dietary neonicotinoid exposure has severe detrimental effects on solitary bee reproductive output. Neonicotinoids did not affect adult bee mortality; however, monitoring of fully controlled experimental populations revealed that sublethal exposure resulted in almost 50% reduced total offspring production and a significantly male-biased offspring sex ratio.Our data add to the accumulating evidence indicating that sublethal neonicotinoid effects on non-Apis pollinators are expressed most strongly in a rather complex, fitness-related context. Consequently, to fully mitigate long-term impacts on pollinator population dynamics, present pesticide risk assessments need to be expanded to include whole life-cycle fitness estimates, as demonstrated in the present study using O. bicornis as a model.
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Pesticides are important agricultural tools often used in combination to avoid resistance in target pest species, but there is growing concern that their widespread use contributes to the decline of pollinator populations. Pollinators perform sophisticated behaviours while foraging that require them to learn and remember floral traits associated with food, but we know relatively little about the way that combined exposure to multiple pesticides affects neural function and behaviour. The experiments reported here show that prolonged exposure to field-realistic concentrations of the neonicotinoid, imidacloprid, and the organophosphate acetylcholinesterase inhibitor, coumaphos, and their combination impairs olfactory learning and memory formation in the honeybee. Using a method for classical conditioning of proboscis extension, honeybees were trained in either a massed or spaced conditioning protocol to examine how these pesticides affected performance during learning and short- and long-term memory tasks. We found that bees exposed to imidacloprid, coumaphos, or a combination of these compounds, were less likely to express conditioned proboscis extension towards an odor associated with reward. Bees exposed to imidacloprid were less likely to form a long-term memory, whereas bees exposed to coumaphos were only less likely to respond during the short-term memory test after massed conditioning. Both imidacloprid, coumaphos and a combination of the two compounds impaired the bees' ability to differentiate the conditioned odour from a novel odour during the memory test. Our results demonstrate that exposure to sublethal doses of combined cholinergic pesticides significantly impairs important behaviors involved in foraging, implying that pollinator population decline could be the result of a failure of neural function of bees exposed to pesticides in agricultural landscapes.
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Concern about the role of pesticides in honey bee decline has highlighted the need to examine the effects of sublethal exposure on bee behaviors. The video-tracking system EthoVisionXT (Noldus Information Technologies) was used to measure the effects of sublethal exposure to tau-fluvalinate and imidacloprid on honey bee locomotion, interactions, and time spent near a food source over a 24-h observation period. Bees were either treated topically with 0.3, 1.5, and 3 µg tau-fluvalinate or exposed to 0.05, 0.5, 5.0, 50, and 500 ppb imidacloprid in a sugar agar cube. Tau-fluvalinate caused a significant reduction in distance moved at all dose levels (p < 0.05), as did 50 and 500 ppb imidacloprid (p < 0.001). Bees exposed to 50 and 500 ppb spent significantly more time near the food source than control bees (p < 0.05). Interaction time decreased as time in the food zone increased for both chemicals. This study documents that video-tracking of bee behavior can enhance current protocols for measuring the effects of pesticides on honey bees at sublethal levels. It may provide a means of identifying problematic compounds for further testing.
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The loss of biodiversity is a trend that is garnering much concern. As organisms have evolved mutualistic and synergistic relationships, the loss of one or a few species can have a much wider environmental impact. Since much pollination is facilitated by bees, the reported colony collapse disorder has many worried of widespread agricultural fallout and thus deleterious impact on human foodstocks. In this Feature, Spivak et al. review what is known of the present state of bee populations and provide information on how to mitigate and reverse the trend.
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We have compared the sublethal effects of two insecticides in the honeybee (imidacloprid and deltamethrin) in both semi-field and laboratory conditions. A sugar solution containing 24 microg kg(-1) of imidacloprid or 500 microg kg(-1) of deltamethrin was offered to a colony set in an outdoor flight cage. In contrast to imidacloprid, deltamethrin had lethal effect on workers bees. The contamination of syrup with imidacloprid or deltamethrin induced a decrease in both the foraging activity on the food source and activity at the hive entrance. Negative effects of imidacloprid were also observed in an olfactory learnt discrimination task. Free-flying foragers were taken from the contaminated feeder and subjected to a conditioned proboscis extension response (PER) assay under laboratory conditions. As with free-flying bees, no impact of deltamethrin was found on the learning performances of restrained individuals in the PER procedure, whilst significant effects were found with imidacloprid in both semi-field and laboratory conditions.
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The relative potency of polycyclic aromatic compounds as aryl hydrocarbon receptor (AhR) agonists in fish was determined using data on CYP1A induction or AhR binding for 74 polycyclic aromatic hydrocarbons (PAHs) and heterocycles in teleost, avian, or mammalian systems from 18 published papers. Each PAH was assigned a fish potency factor relative to the potency of 2,3,7,8-tetrachlorodibenzo-p-dioxin as an AhR agonist. Two and three ring unsubstituted PAHs were generally inactive in fish, avian, and mammalian systems. Benzo[k]fluoranthene and indeno[1,2,3-cd]pyrene were consistently the most potent PAHs, with fish potency factors of 0.001-0.002. Common structural features associated with higher potency PAHs included 4-6 rings containing fluoranthene or phenanthrene structures with an exposed bay region. These results show that PAHs can have similar potency as many dioxin-like PCBs, and AhR mediated toxicity should be considered in assessing the risks of PAHs in fish.
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Fipronil is a phenylpyrazole insecticide introduced for pest control, but it can also affect non-target insects such as honeybees. In insects, fipronil is known to block GABA receptors and to inhibit ionotropic glutamate-gated chloride channels, but the behavioral effects of low doses are not yet fully understood. We have studied the effect of sublethal doses of fipronil on the behavior of the honeybee (Apis mellifera) under controlled laboratory conditions. The drug was either administered orally or applied topically on the thorax. A significant reduction of sucrose sensitivity was observed for the dose of 1 ng/bee 1 h after a thoracic application. No significant effect on sucrose sensitivity was obtained with acute oral treatment. A lower dose of fipronil (0.5 ng/bee applied topically) impaired the olfactory learning of the honeybees. By contrast, locomotor activity was not affected. Our results suggest a particular vulnerability of the olfactory memory processes and sucrose perception to sublethal doses of fipronil in the honeybee.
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The option of an evaluation and assessment of possible sublethal effects of pesticides on bees has been a subject of discussion by scientists and regulatory authorities. Effects considered included learning behaviour and orientation capacity. This discussion was enhanced by the French bee issue and allegations against systemic insecticides that were linked to the hypothesis that sublethal intoxication might even have led to reported colony losses. This paper considers whether and, if so, how sublethal effects should be incorporated into risk assessment, by addressing a number of questions: What is meant by a sublethal effect? Which sublethal effects should be measured, when and how? How are sublethal effects to be included in risk assessments? The authors conclude that sublethal studies may be helpful as an optional test to address particular, compound-specific concerns, as a lower-tier alternative to semi-field or field testing, if the effects are shown to be ecologically relevant. However, available higher-tier data (semi-field, field tests) should make any additional sublethal testing unnecessary, and higher-tier data should always override data of lower-tier trials on sublethal effects.
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