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Honey bees, neonicotinoids and bee incident reports: The Canadian situation
Abstract
Neonicotinoid insecticides have been the target of much scrutiny as possible causes of recent declines observed in pollinator populations. Although neonicotinoids have been implicated in honey bee pesticide incidents, there has been little examination of incident report data. Here we summarize honey bee incident report data obtained from the Canadian Pest Management Regulatory Agency (PMRA).
In Canada, there were very few honey bee incidents reported 2007-2011 and data were not collected prior to 2007. In 2012, a significant number of incidents were reported in the province of Ontario, where exposure to neonicotinoid dust during planting of corn was suspected to have caused the incident in up to 70% of cases. Most of these incidents were classified as "minor" by PMRA, and only six cases were considered "moderate" or "major". In that same year, there were over three times as many moderate or major incidents due to older non-neonicotinoid pesticides, involving numbers of hives or bees far greater than those suspected to be due to neonicotinoid poisoning.
These data emphasize that, while exposure of honey bees to neonicotinoid-contaminated dust during corn planting needs to be mitigated, other pesticides also pose a risk.
... Cutler et al. [16] reported a significant number of honeybee incidents in Ontario, Canada, where exposure to neonicotinoids dust during corn planting was suspected to have caused 67 cases of a total of 110 honeybee incidents. They explained most of these incidents (61 cases) were classified as "minor" (death or abnormal behavior was observed in ≤ 10% of bees in any one colony) by the Canadian Pest Management Regulatory Agency, and only 6 cases were considered "moderate" (1000-3000 bees from each of five or more colonies, or 10-30% of bees in any one colony die or display abnormal behavioral effects) or "major" (at least 3000 bees from each of five or more colonies, or 30% of the bees in any one colony die or exhibit abnormal behavioral effects). ...
... They explained most of these incidents (61 cases) were classified as "minor" (death or abnormal behavior was observed in ≤ 10% of bees in any one colony) by the Canadian Pest Management Regulatory Agency, and only 6 cases were considered "moderate" (1000-3000 bees from each of five or more colonies, or 10-30% of bees in any one colony die or display abnormal behavioral effects) or "major" (at least 3000 bees from each of five or more colonies, or 30% of the bees in any one colony die or exhibit abnormal behavioral effects). Cutler et al. [16] showed that in the same year, there were over three times as many moderate or major incidents (20 cases) caused by non-neonicotinoid pesticides including carbofuran, chlorpyrifos, coumaphos, diazinon, dimethoate, fluvalinate, formic acid, permethrin, and phosmet, involving numbers of hives or bees that are far greater than those suspected to be caused by neonicotinoid poisoning. They concluded that, while exposure of honeybees to neonicotinoid-contaminated dust during corn planting needs to be mitigated, other pesticides also pose a risk, if not a higher risk. ...
... They argued that by de-registering neonicotinoids for crop protection would force growers to revert to increased use of older broad-spectrum chemistries that neonicotinoids have largely replaced, with increased risks to pollinators. The viewpoints of Cutler et al. [16] on how neonicotinoids could harm pollinators' health appeared to be dramatically different to the Ontario government in which a proposal was announced in November 2014 to reduce the use of neonicotinoids by 80% in order to reverse the declining trend of honeybee colonies by 2017 ...
Purpose of Review
Beekeepers around the world have been reporting the ongoing weakening of honeybee health and subsequently the increasing colony losses since 1990. However, it was not until the abrupt emergence of colony collapse disorder (CCD) in the 2000s that has raised the concern of losing this important perennial pollinator. In this report, we provide a summary of the sub-lethal effects of pesticides, in particular of neonicotinoids, on pollinators’ health from papers published in peer-review journals.
Recent Findings
We have identified peer-review papers that are relevant to examine the effects of sub-lethal pesticide exposures on the health of honeybees (Apis mellifera), bumblebees (Bombus terrestris), and other bees from a literature search on PubMed and Google Scholar using the following combined keywords of “pollinators,” “honeybee,” “bees,” “pesticides,” or “neonicotinoids,” and from a cross-reference check of a report made available by the European Parliament in preparation to fulfill their regulatory mandate on the issue of protecting pollinators among their membership nations.
Summary
The weight-of-evidence of this review clearly demonstrated bees’ susceptibility to insecticides, in particular to neonicotinoids, and the synergistic effects to diseases that are commonly present in bee colonies. One important aspect of assessing and managing the risks posed by neonicotinoids to bees is the chronic effects induced by exposures at the sub-lethal levels. More than 90% of literature published after 2009 directly or indirectly demonstrated the adverse health effects associated with sub-lethal exposure to neonicotinoids, including abnormal foraging activities, impaired brood development, neurological or cognitive effects, and colony collapse disorder.
... Honeybees can be exposed to IDP from the pollen of crops grown from IDP-treated seeds and pollution from the surrounding environment [46]. Thus, approximately 20% of IDP residue may remain in commercial honey products [46]. ...
... Honeybees can be exposed to IDP from the pollen of crops grown from IDP-treated seeds and pollution from the surrounding environment [46]. Thus, approximately 20% of IDP residue may remain in commercial honey products [46]. Therefore, the MIP@CNT/CNC MN sensor was evaluated for its ability to quantify IDP in a honey sample using a standard addition method. ...
A portable, molecularly imprinted polymer (MIP)-based microneedle (MN) sensor for the electrochemical detection of imidacloprid (IDP) has been demonstrated. The MN sensor was fabricated via layer-by-layer (LbL) in-tube coating using a carbon nanotube (CNT)/cellulose nanocrystal (CNC) composite, and an IDP-imprinted polyaniline layer co-polymerized with imidazole-functionalized CNCs (PANI-co-CNC-Im) as the biomimetic receptor film. The sensor, termed MIP@CNT/CNC MN, was analyzed using both cyclic voltammetry (CV) and differential pulse voltammetry (DPV) and showed excellent electrochemical performance for the detection of IDP. The CV detection range for IDP was 2.0–99 µM, with limits of detection (LOD) of 0.35 µM, while the DPV detection range was 0.20–92 µM with an LOD of 0.06 µM. Additionally, the MIP@CNT/CNC MN sensor showed excellent reusability and could be used up to nine times with a 1.4 % relative standard deviation (% RSD) between uses. Lastly, the MIP@CNT/CNC MN sensor successfully demonstrated the quantification of IDP in a honey sample.
... In the past decade, several severe bee poisoning incidents during sowing maize seed treated with neonicotinoids, caused by emission of dust containing insecticides, with confirmed lethal effects on forager and hive bees occurred in Europe, Canada and the US (Pistorius et al., 2009;Forster, 2009;Bortolotti et al., 2009;Ap-eNet, 2009;Krupke et al., 2012;Cutler et al., 2013). While insecticidal seed treatments in maize are generally seen critical, especially for neonicotinoids (Maini et al., 2010), the incidents have highlighted the importance of insecticidal dust drift as a highly important route of exposure to be considered in risk assessment. ...
... In about 4 % of these samples up to 5 µg/kg, in 64 % up to 15 µg/kg and in 25 % more than 15 µg/kg with a maximum of 212 µg/kg were detected (Pistorius et al., 2009). Krupke et al. (2012) reported 4 -13 µg Clothianidin/kg dead bees, Cutler et al. (2013) up to 72 µg/kg Clothianidin and 168 µg/kg Thiamethoxam in single samples. In our trial, a clear dose-dependent treatment related mortality of unacceptable and biologically relevant magnitude of acute mortality was demonstrated which experimentally reconfirms the causality conclusions of reported bee incidents. ...
This study explored the effects of insecticidal dusts on honey bee colonies (Apis mellifera L.) after exposure to a priori defined dose under field conditions. For this purpose two different rates of abraded seed dust, containing active substance Clothianidin, were applied on flowering Phacelia tanacetifolia Bentham during bee-flight with a purpose-built dust applicator. We observed dose-related high acute effects on bee mortality at both application rates, 0.25 and 1.0 g a.s. Clothianidin in dust per ha, resulting in up to 4.3 and 17 fold higher mortality compared to pre-application level and an overall increase of mortality during the 7 days exposure period of 2.0 and 9.8 fold. In dead bees, residues detected between both rates applied were up to 2.6 fold higher in the 1.0 g a.s. Clothianidin dust exposure scenario. On day 7, residues up to 28 μg Clothianidin/kg were detected in bee bread of stored Phacelia pollen. The findings of high effects at chosen rates highlight the need to include specific dust drift field trials for seed treatment products with highly toxic insecticides in risk assessment used in crops with potential dust abrasion and emission from seeds. Further work is required to determine appropriate application rates in further semi-field and field testing that reflect field realistic drift exposure levels.
... The latter means of coyote control is controversial and highly regulated. Registered lethal poisons for coyote control include sodium cyanide gas injection cartridges (Alberta only), sodium fluoroacetate tablets (Alberta and Saskatchewan only), and toxic neck collars [9,10]. Despite the availability and potency of approved pesticides for coyote control, occurrence of illegal coyote poisoning with acetyl cholinesterase inhibitor pesticides remains a regular occurrence [2]. ...
... Due to the rapid hydrolysis of organophosphate and carbamate pesticides at warm ambient temperatures, the proximity of dead eagles (and other wildlife species) to dead coyotes or poisoned livestock carcasses is often useful to identifying secondary toxicity. Proximity of carcasses and evidence of predation on coyotes by bald eagles has been noted previously in Western Canada [1][2][3][4][5][6][7][8][9][10][11]. ...
... • Cutler et al. (2014) placed hives of honey bee in fields of canola treated with clothianidin for the flowering period, then maintained them in apiaries surrounded by untreated crops. Comparison with control hives showed no detectable effects on colony performance or winter survival. ...
... Although the adverse effects of some highly toxic pesticides have been demonstrated on bees in laboratory and field studies, there are some disputes about whether exposures used in these studies reflect normal field exposure scenarios (Carreck & Ratnieks, 2014;Cutler et al., 2014b). Defining realistic pesticide exposure scenarios for environmental risk assessments regarding bees requires considering the magnitude, duration and frequency of exposure, as well as the multiple potential routes of exposure for the wide diversity of bee species (Franklin & Raine, 2019). ...
Fungicides account for more than 35% of the global pesticide market and their use is predicted to increase in the future. While fungicides are commonly applied during bloom when bees are likely foraging on crops, whether real-world exposure to these chemicals – alone or in combination with other stressors – constitutes a threat to the health of bees is still the subject of great uncertainty. The first step in estimating the risks of exposure to fungicides for bees is to understand how and to what extent bees are exposed to these active ingredients. Here we review the current knowledge that exists about exposure to fungicides that bees experience in the field, and link quantitative data on exposure to acute and chronic risk of lethal endpoints for honey bees (Apis mellifera). From the 702 publications we screened, 76 studies contained quantitative data on residue detections in honey bee matrices, and a further 47 provided qualitative information about exposure for a range of bee taxa through various routes. We compiled data for 90 fungicides and metabolites that have been detected in honey, beebread, pollen, beeswax, and the bodies of honey bees. The risks posed to honey bees by fungicide residues was estimated through the EPA Risk Quotient (RQ) approach. Based on residue concentrations detected in honey and pollen/beebread, none of the reported fungicides exceeded the levels of concern (LOC) set by regulatory agencies for acute risk, while 3 and 12 fungicides exceeded the European Food Safety Authority (EFSA) chronic LOC for honey bees and wild bees, respectively. When considering exposure to all bees, fungicides of most concern include many broad-spectrum systemic fungicides, as well as the widely used broad-spectrum contact fungicide chlorothalonil. In addition to providing a detailed overview of the frequency and extent of fungicide residue detections in the bee environment, we identified important research gaps and suggest future directions to move towards a more comprehensive understanding and mitigation of the risks of exposure to fungicides for bees, including synergistic risks of co-exposure to fungicides and other pesticides or pathogens.
... These insecticides are the most often used for insect pest management on vegetable and horticultural crops and they can be apply directly or indirectly to plant canopy [16]. Neonicotinoids causes chronic cholinergic receptor activation, resulted in hyperexcitation and finally lead to mortality [17] as systemic pesticides deposited in pollen and nectar of treated crops during the blooming and flowering time [18] come into the contact of the honey bees for longer periods of time, but there are no harmful impacts reported from the crop grown from treated seeds [19]. Pesticide exposure appears to be a dosedependent affect to foraging response of the bee. ...
Honey bees are social insects produce honey and other hive products like propolis, royal jelly, bee venom and bee wax. Besides, their significance as the valued pollinators of many vegetable and horticultural crops they also play a crucial role in preservation of natural biodiversity. Many (diseases, parasites, insects) and environmental stress have an impact on the longevity and efficiency of honey bees. Gasses, heavy metals and air pollutants, in addition to inorganic compounds, have been linked to increased queen replacement and winter mortality in honey bees, as well as reduced brood survival and interference with cellular metabolism. Furthermore, natural poisons in food including toxic polysaccharides, phenolics, cyanogenic glycosides and alkaloids can impair colony performance, influence energy production via mitochondrial ATP synthase inhibition and result in acute mortality. In addition, adult bees ingesting acaricides such as formic acid and oxalic acid may die midgut cells, reducing bee activity, nursing behavior and longevity. Furthermore, biosphere pollution caused by irresponsible pesticide usage causing several issues to honey bee species, the most prominent of which is Apis mellifera L. Although no one chemical has been linked to colony collapse disorder, it is possible that it contributes to decreased honey bee health. Well understanding of pesticide mode of action in targeted pests and honey bees has resulted in a viable technique to prevent pesticide side effects on honey bees. As a result, the purpose of this review is to look into the toxicity of some pesticides used on crops, acaricides used in honey bee colonies and natural plant toxins. Understanding the role of these compounds and their side effects on honey bees is undoubtedly important in preventing colony collapse.
... For instance, the pesticide chlorothalonil was found to lower commensal bacterial sugar metabolism 5 . Similarly, bees live in densely populated colonies with ≥ 50,000 individuals 6 and must contest with greater risk from infectious agents. For example, lethal foulbrood infections are caused by the bacterium Paenibacillus larvae 7 . ...
Honeybees ( Apis Mellifera) perform an essential role in the ecosystem and economy through pollination of insect-pollinated plants, but their population is declining. Many causes of honeybees’ decline are likely to be influenced by the microbiome which is thought to play an important role in bees and is particularly susceptible to infection and pesticides. However, there has been no systematic review or meta-analysis on honeybee microbiome data. Therefore, we conducted the first systematic meta-analysis of 16S-rRNA data to address this gap in the literature. Four studies were in a usable format – accounting for 336 honeybee’s worth of data – the largest such dataset to the best of our knowledge. We analysed these datasets in QIIME2 and visualised the results in R-studio. For the first time, we conducted a multi-study evaluation of the core and rare bee microbiome and confirmed previous compositional microbiome data. We established that Snodgrassella, Lactobacillus, Bifidobacterium, Fructobacillus and Saccaribacter form part of the core microbiome and identify 251 rare bacterial genera. Additional components of the core microbiome were likely obscured by incomplete classification. Future studies should refine and add to our existing dataset to produce a more conclusive and high-resolution portrait of the honeybee microbiome. Furthermore, we emphasise the need for an actively curated dataset and enforcement of data sharing standards.
Abstract Figure
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Graphical abstract
Made by the author in Biorender.com .
... Potential sublethal effects include reduction in the return of foraging bees to hives (Henry et al., 2012), reduction of resistance to parasites and diseases (Alaux et al., 2010;Brandt et al., 2016), and reduction of reproductive success of queens (Williams et al., 2015). In-field experiments for honeybee impacts are challenging and have provided mixed results (Chambers et al., 2019;Cutler et al., 2014;Lu et al., 2020). For wild pollinators, data are more limited, and impacts may vary from species to species and across locations (Rundlöf & Lundin, 2019;Strobl et al., 2020). ...
This is a review of contributions on pollination economics, including economics of beekeeping, pollination service valuation and pesticide regulation.
... A largescale study even found a correlation between the use of imidacloprid and the loss of honey bee colonies (Budge et al. 2015). Moreover, episodes of high honey bee mortality in Quebec and Ontario (Canada) have been linked to neonicotinoid-treated corn or soybean sowings (Cutler et al. 2014a;Health Canada 2017). ...
Water is essential for honey bees (Apis mellifera L.), but contaminated sources of water in agricultural environments represent a risk of exposure to potentially harmful contaminants. Providing clean water to honey bees could be an efficient and cost-effective measure for beekeepers to reduce bee mortality associated with pesticides and improve the health of their colonies. The main goal of this study was to design a waterer prototype to fulfill the water requirements of honey bees and to evaluate the potential of this waterer in improving colonies’ health in agricultural settings, through mitigating the possible impact of an exposure to pesticides from puddle water. We tested the preference of honey bees regarding water composition and waterer prototypes, among which honey bees showed a strong preference for salted water and a poultry-type waterer. Our waterer models were quickly adopted and intensively used through the season in both the context of honey production in field crops and pollination services in cranberry crops. However, in neither context did the use of waterers reduce worker mortality nor increase overall colony weight. Our waterers provided bees with water containing fewer pesticides and were associated with reduced risks of drowning compared to natural sources of water. Our study suggests that the use of waterers fulfills an important requirement for honey bees and represents an interesting and convenient precautionary measure for beekeepers.
... The incidents of bee poisoning by pesticides in the UK were summarized in different years (Fletcher and Barnett, 2003;Barnett et al., 2007). Furthermore, there is an available report of bee poisoning in Germany in spring 2008 from the abrasion of active substances on treated seeds during the sowing of maize (Pistorius et al., 2009) and a study of incidents in Canada in 2007e2012 due to neonicotinoid exposure (Cutler et al., 2014) There is also a report on the largest mass incident in Czechia due to the insecticide Regent containing the active substance fipronil (Modra and Svobodova, 2009). Along with these and other publications, additional information should be found from the governmental organizations in different countries that analyze samples collected by local bee inspectors of the suspected poisonings from beekeepers. ...
Honey bees are major pollinators of crops with high economic value. Thus, bees are considered to be the most important nontarget organisms exposed to adverse effects of plant protection product use. The side effects of pesticides are one of the major factors often linked to colony losses. Fewer studies have researched acute poisoning incidents in comparison to the study of the sublethal effects of pesticides. Here, we compared pesticides in dead/dying bees from suspected poisoning incidents and the suspected crop source according to government protocols. Additionally, we analyzed live bees and bee bread collected from the brood comb to determine recent in-hive contamination. We used sites with no reports of poisoning for reference. Our analysis confirmed that not all of the suspected poisonings correlated with the suspected crop. The most important pesticides related to the poisoning incidents were highly toxic chlorpyrifos, deltamethrin, cypermethrin and imidacloprid and slightly toxic prochloraz and thiacloprid. Importantly, poisoning was associated with pesticide cocktail application. Almost all poisoning incidents were investigated in relation to rapeseed. Some sites were found to be heavily contaminated with several pesticides, including a reference site. However, other sites were moderately contaminated despite agricultural use, including rapeseed cultivation sites, which can influence the extent of pesticide use, including tank mixes and other factors. We suggest that the analysis of pesticides in bee bread and in bees from the brood comb is a useful addition to dead bee and suspected crop analysis in poisoning incidents to inform the extent of recent in-hive contamination.
... Moreover, honeybees approaching the drilling machine during sowing collect particulate matter containing high doses of pesticides and lethal acute effects were observed in the exposed honeybees [44,[49][50][51][52]. In Europe, Canada and the US several cases of colony loss related to corn sowing were observed, where beekeepers have reported huge and rapid mortality in their hives due to emission of dust containing insecticides (see Krupke et al. [51], Pistorius et al. [53], the following reviews [54,55] and references therein). More recently, after the neonicotinoid bans and the introduction of new coatings and sowing technologies aimed to reduce seed abrasion, massive spring colony losses were observed in northeastern Italy. ...
Background
Large amounts of insecticide-containing dusts produced from abrasion of the seed dressing can be released into the atmosphere during sowing operations. Neonicotinoid pesticides, introduced in the 1990s for several crops, are the leading products for seed-coating treatments in many countries. Neonicotinoid containing dusts can be effectively intercepted by bees in flight over the sowing field, inducing lethal acute effects, so that restrictions in the use of the main neonicotinoids have been adopted in the European Union. This led to the consequent introduction of replacement insecticides for seed-coating, i.e. methiocarb and thiacloprid, despite the lack of information on both the toxicity and the exposure scenarios for honeybees.
Results
In this study, a laboratory apparatus was developed in order to quantify the toxicity of the dusts produced from the abrasion of the seed coating. This quantification is based on (i) an airstream transporting coating particles into an exposure chamber; (ii) exposure of bees to reproducible and measurable concentrations of insecticide, and (iii) direct measurement of the exposure dose on single bees. The method allowed us to perform in vivo experiments of honeybee exposure to provide toxicity data in more realistic exposure conditions. In fact, the formulation rather than the active principle alone can be tested, and the exposure is through dusts rather than a solution so that specific absorption behavior can be studied in representative environmental conditions. The method was used to quantify the acute toxicity (LD50) of dusts obtained from the abrasion of corn seeds coated with clothianidin, thiacloprid and methiocarb.
Conclusions
Our results show that, surprisingly, the replacement insecticide methiocarb has a toxicity (LD50 = 421–693 ng/bee) in the same order of magnitude as clothianidin (LD50 = 113–451 ng/bee) through this specific exposure route, while thiacloprid (LD50 = 16.9·10³ ng/bee) has a significantly lower acute toxicity. Moreover, dusts containing methiocarb and clothianidin show a significant increase in toxicity when, after exposure, bees are kept under high humidity conditions. This suggests that the method here presented can be used to obtain complementary toxicity data in the risk assessment procedure for the authorization of new seed-coating insecticides or new formulations.
... Approximately 35% of crops depend directly on pollinators as shown by Klein et al., 1987. While there are many factors that can potentially affect survival of bees, including changes in climate, genetics, changes in nutrition due to changes in cropping patterns from year to year, parasites and viral diseases (Fairbrother et al., 2014), results of some studies have suggested that extensive use of insecticides might be a factor in the increased rates of loss of colonies during the dormant period of winter (Cutler et al., 2014). ...
... Such declines threaten the economic viability of the beekeeping industry and have serious implications to pollination services for both cultivated and wild plants (Clermont et al., 2015). Many factors have been linked to colony declines, such as parasitic mites, pathogens, loss of foraging habitat, and widespread pesticide application (Cutler et al., 2014;Goulson et al., 2015;Sánchez-Bayo et al., 2016;Abbo et al., 2017;O'Neal et al., 2018). Although the causes of honey bee decline may be complex and subjected to disagreement, the large-scale application of pesticides has been indicated as a potential contributing factor (Diao et al., 2018;Tosi et al., 2018). ...
The neonicotinoid insecticide acetamiprid (ACT) and seven pesticides [abamectin (ABA), emamectin benzoate (EMB), dicrotophos (DIC), bifenthrin (BIF), cypermethrin (CYP), lambda-cyhalothrin (LCY) and tetraconazole (TET)] are widely applied agrochemicals worldwide. Since most previous studies on these pesticides are performed merely based on toxicity tests with individual active ingredients, only finite knowledge is available on the mixture toxicities of these formulated compounds to crop pollinators. In this study, we examined their toxicities of binary, ternary, quaternary, quinquenary, senary, septenary and octonary mixtures to honey bee (Apis mellifera L.) with feeding toxicity test. Results showed that EMB and ABA had the highest toxicities to A. mellifera with LC50 values of 0.033 (0.028-0.038) and 0.047 (0.039-0.056) μg a. i. mL-1 after exposure for 7 days, respectively, followed by DIC with an LC50 value of 1.22 (1.01-1.41) μg a. i. mL-1. In contrast, relatively low toxicities were found from pyrethroid insecticides, ACT, and TET with their LC50 values ranged from 44.76 (38.75-50.89) to 251.7 (198.4-297.3) μg a. i. mL-1. Most of pesticide mixtures containing ACT and TET elicited synergistic interactions to honey bees. Besides, four pesticide mixtures of ACT + BIF, ACT + BIF + CYP, ACT + BIF + LCY and ACT + CYP + DIC + EMB also displayed synergistic effects. Among 98 tested binary to octonary mixtures of ACT in combination with seven pesticides, 44.90% of combinations exhibited synergistic effects on honey bees. Considering ACT was permitted to use on flowering crops, more attention should be paid to its application in the fields due to the synergistic effects of ACT in combination with other pesticides on A. mellifera under laboratory conditions.
... A survey by Kasiotis et al. (2014) also found neonicotinoid residues in bees and their products. Scientific Review Article Several studies, either field studies or lab studies, have proved that exposure of bees to these chemicals leads them to present affected navigation, foraging, development, lifespan, fecundity and immune system (Gregorc, 2011;Laurino, 2011;Krupke, 2012;Gill, 2012;Schierow, 2012;Schneider , 2012;Wu, 2012;Pettis, 2013;Cutler, 2014;Hallmann , 2014;Kasiotis , 2014;Van der Sluijs, 2015). These are called sublethal effects. ...
Apis mellifera or European honey bee is an insect of great economic and ecologic importance. It is a well-known general pollinator which also helps to improve quantity and quality of crops production. In the last decades European honey bee has experienced a decrease in hives number in some countries and many studies have been and still are carried out to try to find the causes leading to this event. The aim of this paper is to review some of those studies to collect their main findings and their meaning in present situation of honey bees.
... For example, in 2015 in Russia poisoning with such pesticides was a reason of the main causes of death of bees (Klochko and Blinov, 2016). There are cases of poisoning of bee colonies with various insecticides, for example, in Canada (Cutler, 2014). As a rule, the death of bees is noted during the period of mass pesticide treatment of agricultural crops, orchards, forests. ...
... The importance of this source of exposure has been reduced through changes in regulations, the introduction of better coating technology for seeds, better lubricants to reduce abrasion of the coating on the seed, better seeding procedures ( Nuyttens et al. 2013), and equipment such as deflectors, which can reduce the levels of airborne dust by 90-99% ( Vrbka et al. 2014). Many review papers have been devoted to the topic of neonicotinoids and their potential effects in pollinators ( Alkassab and Kirchner 2017;Blacquière et al. 2012;Cresswell 2011;Cresswell et al. 2014;Cutler, Scott-Dupree, and Drexler 2013;Decourtye and Devillers 2010;Fairbrother et al. 2014;Godfray et al. CONTACT Keith R Solomon ksolomon@uoguelph.ca ...
A quantitative weight of evidence (QWoE) methodology was developed and used to assess many higher-tier studies on the effects of three neonicotinoid insecticides: clothianidin (CTD), imidacloprid (IMI), and thiamethoxam (TMX) on honeybees. A general problem formulation, a conceptual model for exposures of honeybees, and an analysis plan were developed. A QWoE methodology was used to characterize the quality of the available studies from the literature and unpublished reports of studies conducted by or for the registrants. These higher-tier studies focused on the exposures of honeybees to neonicotinoids via several matrices as measured in the field as well as the effects in experimentally controlled field studies. Reports provided by Bayer Crop Protection and Syngenta Crop Protection and papers from the open literature were assessed in detail, using predefined criteria for quality and relevance to develop scores (on a relative scale of 0–4) to separate the higher-quality from lower-quality studies and those relevant from less-relevant results. The scores from the QWoEs were summarized graphically to illustrate the overall quality of the studies and their relevance. Through mean and standard errors, this method provided graphical and numerical indications of the quality and relevance of the responses observed in the studies and the uncertainty associated with these two metrics. All analyses were conducted transparently and the derivations of the scores were fully documented. The results of these analyses are presented in three companion papers and the QWoE analyses for each insecticide are presented in detailed supplemental information (SI) in these papers.
... Declines in bee numbers, particularly honeybees, are often attributed to a group of pesticides called neonicotinoids (neonics), considered to be harmful and potentially lethal to bees [74,75]. Growing evidence for their toxic impacts on bee populations range from reduced queen production [73], disorientation [76], reduced immunity [77], and mortality [76,78]. ...
There is increasing recognition in academic circles of the importance of adaptive governance for the sustainability of social-ecological systems, but little examination of specific implications for the 34% of land-use where human activities are pervasive but potentially commensurate with functioning ecosystems: agricultural production systems. In this paper, we argue for the need to view food systems and agro-ecosystems as multi-scalar complex adaptive systems and identify five key challenging characteristics of such systems: multi-causality; cumulative impacts; regime shifts; teleconnections and mismatch of scales. These characteristics are necessary features of multi-scalar adaptive systems, and apply equally to social and natural subsystems. We discuss the implications of these characteristics for agricultural production systems and consider how governance can rise to these challenges. We present five case studies that highlight these issues: pollinator declines; payments for ecosystem services; pest control and pesticide resistance; downstream aquatic systems in Tasman Bay, New Zealand; and riparian buffers in Puget Sound, USA. From these case studies we derive recommendations for managing agricultural systems, both specific and general. Ultimately, adaptive governance of agro-ecosystems will likely hinge upon three paradigm shifts: viewing farmers and ranchers not only as food producers but also as land and water managers; seeking not yield maximization but rather resilient management of food ecosystems; and critically, as it transcends the production-system literature, engaging broad audiences not only as consumers but also citizens.
... Although seeds of many different crops have been treated with neonicotinoids, bee kills at planting have generally been associated with treated corn (3,4,5,6,21). A few studies of treated seeds of other crops have found much less insecticide dust in batches of sugar beet and oil seed rape seeds than in corn (6), although another detailed study found that wheat may have as much risk of dust drift as corn (22). ...
General Principles for Best Management Practices:
1. Do not use seed treated with neonicotinoids unless there is a specific pest problem that can be effectively managed with a neonicotinoid seed treatment.
2. When the use of neonicotinoids is not warranted, purchase seed that is not treated with this group of chemicals (seeds may be treated with fungicides or other pesticides). If seed selection is limited, contact your seed company’s field representative to request increased selection and availability of seed that is not treated with neonicotinoids.
3. Before planting with seeds treated with neonicotinoids, notify any nearby beekeepers, so that they can protect their bees. Also remove flowering plants from the field and field edges by mowing or tillage.
4. Read and follow all instructions on the seed tag including personal protective equipment to be used in handling seed and required buffer zones.
5. Keep the treatment on the seed during storage and handling. Avoid storing seed under extreme temperatures and excessive humidity that may increase the breakdown of the seed treatment.
6. Reduce insecticide dust produced at planting, keeping the treatment on the seed as much as possible. Load treated seed into planter boxes in a manner that will minimize the dust from becoming airborne. Minimize any drift of dust outside the field. Most problems with neonicotinoid-contaminated dust drifting in the air have been with treated corn planted using vacuum planters. There is currently no single solution to this problem. Options, including using deflectors or filters on the planting equipment and changing the lubricant mixed with the seed, are discussed below.
7. Avoid planting on windy days when any dust will blow into the environment, particularly if wind is blowing toward bee hives, flowering trees or standing water sources used by bees.
8. Dispose of any leftover treated seed properly, following directions on the seed tag. Generally it is best to plant it or bury it in an appropriate place away from water bodies.
9. Dispose of any dust left over in seed bags and filters properly, following any instructions on the seed bag or using the hazardous waste collection process in your municipality. (Because this is farm waste rather than household waste, there may be a fee.)
... Vacuum type planters have been shown to dislodge, as a result of abrasion, insecticide seed coatings during planting, and exhaust them to the atmosphere (Greatti et al., 2003(Greatti et al., , 2006Nikolakis et al., 2009;Nuyttens et al., 2013). These abraded particles or contaminated dust, are potentially toxic to exposed honeybees and other pollinators (Krupke et al., 2012;Sgolastra et al., 2012;Girolami et al., 2012;Pistorius et al., 2009Pistorius et al., , 2015Marzaro et al., 2011;Pochi et al., 2012;Tapparo et al., 2012), with some cases of acute mortality by direct contact reported (EFSA, 2013b;Sgolastra et al., 2012;Health Canada, 2012Pistorius et al., 2009;Girolami et al., 2012;Marzaro et al., 2011;Cutler et al., 2014;Sgolastra et al., 2017). Fugitive residues could also contaminate other environmental matrices such as surface water (Anderson et al., 2015;Bonmatin et al., 2015;Morrissey et al., 2015;Schaafsma et al., 2015;Starner and Goh, 2012) or nearby vegetation (Greatti et al., 2003(Greatti et al., , 2006Krupke et al., 2012;Nikolakis et al., 2009). ...
Atmospheric emissions of neonicotinoid seed treatment insecticides as particulate matter in field crops occur mainly for two reasons: 1) due to abraded dust of treated seed generated during planting using vacuum planters, and 2) as a result of disturbances (tillage or wind events) in the surface of parental soils which release wind erodible soil-bound residues. In the present study, concentration and movement of neonicotinoids as particulate matter were quantified under real conditions using passive and active air samplers. Average neonicotinoid concentrations in Total Suspended Particulate (TSP) using passive samplers were 0.48 ng/cm2, trace, trace (LOD 0.80 and 0.04 ng/cm2 for clothianidin and thiamethoxam, respectively), and using active samplers 16.22, 1.91 and 0.61 ng/m3 during planting, tillage and wind events, respectively. There was a difference between events on total neonicotinoid concentration collected in particulate matter using either passive or active sampling. Distance of sampling from the source field during planting of treated seed had an effect on total neonicotinoid air concentration. However, during tillage distance did not present an effect on measured concentrations. Using hypothetical scenarios, values of contact exposure for a honey bee were estimated to be in the range from 1.1% to 36.4% of the reference contact LD50 value of clothianidin of 44 ng/bee.
... The Canadian Pest Management Regulatory Agency (PMRA) classifies bee poisoning incidents as 'minor', 'moderate', or 'major'. The classification is based not only on the number of dead bees but also on the abnormal behavioural effects exhibited by ≤10% of bees in any one colony, 10-30% of bees in any one colony (1000-3000 bees from each of five or more colonies), or at least 30% of bees in any one colony (at least 3000 bees from each of five or more colonies), respectively (Cutler, Scott-Dupree & Drexler, 2014). Typical clinical symptoms of acute insecti-cide poisoning include cramping, disoriented behaviour of bees, and abnormal wing movements. ...
During the 2000s, the problem of pesticide poisoning of honeybees seemed to be almost solved. The number of cases has decreased in comparison to the 1970s. The problem of acute honeybee poisoning, however, has not disappeared, but instead has transformed into a problem of poisoning from 'traditional' pesticides like organophosphorus pesticides or pyrethroids, to poisoning from additional sources of 'modern' systemic neonicotinoids and fipronil. In this article, the biological activity of pesticides was reviewed. The poisoning symptoms, incident definitions, and monitoring systems, as well as the interpretation of the analytical results, were also reviewed. The range of pesticides, and the detected concentrations of pesticides in poisoned honeybee samples, were reviewed. And, for the first time, cases of poisoning related to neonicotinoids were reviewed. The latter especially is of practical importance and could be helpful to analysts and investigators of honeybee poisoning incidents. It is assumed that secondary poisoning induced by plant collected materials contaminated with systemic pesticides occurs. Food stored in a hive and contaminated with systemic pesticides consumed continuously by the same generation of winter bees, may result in sub-lethal intoxication. This leads to abnormal behaviour identified during acute intoxication. The final result is that the bees discontinue their social role in the honeybee colony super organism, and colony collapse disorder (CCD) takes place. The process described above refers primarily to robust and strong colonies that were able to collect plenty of food due to effective plant protection.
... High purity (>97%) native PCB standards (IUPAC congeners #19, 28,43,52,77,81,101,105,114,118,123,126,138,153,156,157,167,169,180,181,189,194) were supplied by Dr Ehrenstorfer (Augsburg, Germany). Native PBDE standards (IUPAC #1, 2, 3,7,8,10,11,12,13,15,17,25,28,30,32,33,35,37,47,49,66,71,75,77,85,99,100,110,116,118,119,126,138,153,154,155,166,181,183,190) were supplied by AccuStandard (New Haven, CT, USA). 13 47,99,100,154,183,209) were supplied by Cambridge Isotope Laboratories (Andover, MA, USA). ...
Chemical plant protection is a commonly discussed factor potentially responsible for decline in pollinators and other beneficial insect populations. Various groups of chemicals including persistent organic pollutants could impact a bee colony’s welfare and are reported to be present in bee tissue and apiary products. The aim of this work was to evaluate the presence of selected persistent organic pollutant and pesticide residues in bee pollen originating from different geographical regions of Poland. Pesticide residues were identified in 60% of tested bee pollen samples. The compounds identified were mainly active ingredients of fungicide preparations. Insecticide active ingredients were up to 30% of the identified residues. The triazole fungicide tebuconazole and the neonicotinoid insecticide thiacloprid were the most frequently found pesticides in pollen. The highest pesticide concentration was determined for prothioconazole (356 μg kg⁻¹). Mean concentrations of chlorinated biphenyls–EC6 and EC12 were 194 pg g⁻¹ and 74 pg g⁻¹, respectively. CB # 28 has the greatest share in the EC6 profile (mean 61 pg g⁻¹, 31% contribution). Relatively high contributions were also observed for CBs # 101 (35 pg g⁻¹, 18%), # 138 (36 pg g⁻¹, 19%) and # 153 (33 pg g⁻¹, 17%). CB # 114 and 118 have the highest share in the dioxin-like biphenyls fraction with mean concentrations of 17.6 and 37.6 pg g⁻¹ (respectively 23 and 50%). Mean calculated concentrations of 39 polybrominated diphenyl ether congeners (Σ39 BDE) were 20 ± 27.7 pg g⁻¹. High variability was observed between maximal and minimal determined concentration values. Individual BDEs were found at different frequencies and varying concentration levels. BDEs # 47, 75 and 99 dominated the profile with average concentrations of 3 pg g⁻¹, 3.1 pg g⁻¹, and 2.9 pg g⁻¹, respectively.
... In Canada, data obtained from the Canadian Pest Management Regulatory Agency (PMRA) was reviewed by Cutler et al. (2014a). Since 2007, 110 honey bee-pesticide incident reports were received by the PMRA but there were very few incidents (six) reported up to 2011. ...
The nitro-substituted neonicotinoid insecticides, which include imidacloprid, thiamethoxam and clothianidin, are widely used to control a range of important agricultural pests both by foliar applications and also as seed dressings and by soil application. Since they exhibit systemic properties, exposure of bees may occur as a result of residues present in the nectar and/or pollen of seed- or soil-treated crop plants and so they have been the subject of much debate about whether they cause adverse effects in pollinating insects under field conditions. Due to these perceived concerns, the use of the three neonicotinoids imidacloprid, clothianidin and thiamethoxam has been temporarily suspended in the European Union for seed treatment, soil application and foliar treatment in crops attractive to bees. Monitoring data from a number of countries are available to assess the presence of neonicotinoid residues in honey bee samples and possible impacts at the colony level and these are reviewed here together with a number of field studies which have looked at the impact of clothiandin on honey bees in relation to specific crop use and in particular with oilseed rape. Currently there is considerable uncertainty with regards to the regulatory testing requirements for field studies. Accordingly, a testing protocol was developed to address any acute and chronic risks from oilseed rape seeds containing a coating with 10 g clothianidin and 2 g beta-cyfluthrin per kg seeds (Elado®) for managed honey bee (Apis mellifera) colonies, commercially bred bumble bee (Bombus terrestris) colonies and red mason bees (Osmia bicornis) as a representative solitary bee species. This is described here together with a summary of the results obtained as an introduction to the study details given in the following papers in this issue.
... If dust particles are abraded from the seed dressing due to friction, they are emitted along with the exhaust air from the fan into the environment. This has caused serious pollinator poisoning incidents in the past [10][11][12] . ...
Drilling of treated seeds with vacuum-based precision drills can cause emissions of pesticide-laden dust, which have been linked with declines of pollinator populations. Predicting the drift pattern of this type of dust is challenging because the particles are very irregular in terms of size, shape, density, internal porosity and chemical composition. In this work, a 3D Computational Fluid Dynamics (CFD) model of seed treatment dust drift was developed and validated with wind tunnel data. In the wind tunnel experiment, dust abraded from pesticide-treated seed was separated in three size fractions and released from a point source at a height of 0.7 m at three air velocities. Dust deposition was measured at six distances on the wind tunnel floor. The physicochemical properties of the dust samples were measured and implemented in the CFD model. Lagrangian tracking was used to calculate the dust particle trajectories. The simulated dust deposition patterns agreed with those observed in the wind tunnel trials. It was demonstrated that an accurate, particle size-dependent description of the shape, chemical content and internal porosity of the dust particles was necessary to achieve good validation results. The CFD model can be used as a basis for the simulation of dust drift in the field during sowing.
... The fungicides shown here, and possibly most others applied as foliar sprays, pose low or negligible risks to bees by direct contact with spray droplets. This evaluation is in agreement with the reported incidents of pesticides on bees in the United Kingdom [63] and Canada [64]. Obviously, the most toxic insecticides are the most dangerous to bees. ...
This chapter focuses on the detrimental effects that pesticides have on managed honey bee colonies and their productivity. We examine first the routes of exposure of bees to agrochemicals used for crop protection and their application to crops, fate and contami‐ nation of water and plants around the fields. Most of the time, the exposure of bees to pesticides is through ingestion of residues found in the pollen and nectar of plants and in water. Honey bees are also exposed to pesticides used for the treatment of Varroa and other parasites. The basic concepts about the toxicity of the different kinds of pesticides are explained next. Various degrees of toxicity are found among agrochemicals, and emphasis is given to the classic tenet of toxicology, " the dose makes the poison, " and its modern version " the dose and the time of exposure makes the poison. " These two factors, dose and time, help us understand the severity of the impacts that pesticides may have on bees and their risk, which are analysed in the third section. Sublethal effects are also considered. The final section is devoted to some practical advice for avoiding adverse impacts of pesticides in beekeeping.
... Reports from Canada show that neonicotinoids account now for 72% of current bee incidents in that country, whereas other pesticides such as organophosphates are implicated only in 18% of the cases. Nevertheless, incidents that caused greater than 10% bee losses in the colony involved neonics 26% of the time, while 74% involved other pesticides (Cutler, Scott-Dupree, & Drexler, 2014). Wherever agriculture has switched from the old to the new insecticides, similar trends may be expected. ...
... While there are many factors that can potentially affect survival of bees, including changes in climate, genetics, changes in nutrition due to changes in cropping patterns from year to year, parasites and viral diseases (Fairbrother et al., 2014), results of some studies have suggested that extensive use of insecticides might be a factor in the increased rates of loss of colonies during the dormant period of winter (Cutler et al., 2014a(Cutler et al., ,b, 2007Al Naggar et al., 2015a,b). Some bees might be particularly susceptible to pesticides because the European honey bee is deficient in some genes encoding for detoxification enzymes (Claudianos et al., 2006). ...
... While there are many factors that can potentially affect survival of bees, including changes in climate, genetics, changes in nutrition due to changes in cropping patterns from year to year, parasites and viral diseases (Fairbrother et al., 2014), results of some studies have suggested that extensive use of insecticides might be a factor in the increased rates of loss of colonies during the dormant period of winter (Cutler et al., 2014a(Cutler et al., ,b, 2007Al Naggar et al., 2015a,b). Some bees might be particularly susceptible to pesticides because the European honey bee is deficient in some genes encoding for detoxification enzymes (Claudianos et al., 2006). ...
... Up to 75% of crop species used for food depend on insect pollination to some degrees [1]. Honeybees are the major pollinators of crop plants; the decline in honeybee population has caused great concerns in recent years [2][3][4]. Neonicotinoid insecticides have been investigated as the possible causes of recent declines in pollinator population [5]. Except the partially suspended use of neonicotinoid insecticides, the potential harm of sublethal doses of neonicotinoid insecticides has caused more concerns [6,7] because of its subtle influence on bee behavior including the effect on normal functions [8], the changing foraging, and the decrease in avoiding predatory behavior [9], particularly referring to the impairment of the olfactory associative behavior of adult honeybees [10]. ...
... For this reason, recent Canadian and international attention has targeted the use of neonicotinoids as a potential explanation for a decline in honey bee and other pollinator populations. [6][7][8] The following write-up has been prepared to respond to a request regarding current information on regulatory decisions surrounding neonicotinoids in Canada and abroad, and to provide information on the use of neonicotinoids and the potential impacts on food security. ...
The Environmental and Occupational Health team responds to specific requests for scientific and technical advice and support from the health care system, the Government of Ontario, and most commonly from Ontario’s local public health units. Based on requests received, we have identified questions, issues and topics that may be of relevance to a broader audience. Therefore, we have created the Case Study series to better share information on the diverse environmental health issues we have encountered, and encourage dialogue in these areas.
This response was originally produced in July 2014. The specifics about the location and requestor involved have been removed. The following was selected as a case study because of the widespread use of neonicotinoids in Ontario.
Original available from: http://www.publichealthontario.ca/en/eRepository/Case_Study_Neonicotinoids_2015.pdf
... Those wintering bees may be Fortunately, as highlighted in a recent study on such issues in Canada, these incidents are relatively few. 84 Accordingly, chemicals need to be used strategically and carefully for both farming and pest control in hives. In both cases, the products yield important benefits in disease reduction and food production, which is why risk management rather than product elimination offers the best course of action. ...
... The much-debated association between honeybee colony decline and neonicotinoid insecticide use is still going on among academics, politicians, regulators, beekeepers, non-governmental organisations (NGOs) and the general public in a myriad of venues from scientific journal articles, to regulations and guidelines, media article pieces and even popular fiction (Rollins, 2009;Schacker, 2009;Blacquière et al., 2012;Kleinman & Suryanarayanan, 2012;Gross, 2013;Tirado et al., 2013;Chauzat et al., 2014;Godfray et al., 2014;Roubik, 2014). Such heated exchange seems to be providing some points of congruence, including the recognition of honeybee decline in different areas and countries, the multifactorial nature of the phenomenon, and the absence of evidence for a direct association between honeybee decline and neonicotinoid use (Kluser et al., 2010;Neumman & Carreck, 2010;Potts et al., 2010;Creswell, 2011;Blacquière et al., 2012;Creswell et al., 2012;Vanbergen et al., 2013;Cutler et al., 2014;Fairbrother et al., 2014;Staveley et al., 2014). Insecticides, and particularly neonicotinoids, are most likely important components in such a scenario, potentiating colony decline in a period of increasing demand for pollination services (Johnson et al., 2013;Breeze et al., 2014;Chauzat et al., 2014;Godfray et al., 2014;Zhu et al., 2014). ...
As honeybees are the main pollinator subject to an intense research regarding effects of pesticides, other ecologically important native bee pollinators have received little attention in ecotoxicology and risk assessment of pesticides in general, and insecticides in particular, some of which are perceived as reduced-risk compounds. Here, the impact of three reduced-risk insecticides – azadirachtin, spinosad and chlorantraniliprole – was assessed in two species of stingless bees, Partamona helleri and Scaptotrigona xanthotrica, which are important native pollinators in Neotropical America. The neonicotinoid imi-dacloprid was used as a positive control. Spinosad exhibited high oral and contact toxicities in adult workers of both species at the recommended label rates, with median survival times (LT 50 s) ranging from 1 to 4 h, whereas these estimates were below 15 min for imidacloprid. Azadirachtin and chlorantranilip-role exhibited low toxicity at the recommended label rates, with negligible mortality that did not allow LT 50 estimation. Sublethal behavioural assessments of these two insecticides indicated that neither one of them affected the overall group activity of workers of the two species. However, both azadirachtin and chlorantraniliprole impaired individual flight takeoff of P. helleri and S. xanthotrica worker bees, which may compromise foraging activity, potentially leading to reduced colony survival. These findings challenge the common perception of non-target safety of reduced-risk insecticides and bioinsecticides, particularly regarding native pollinator species.
... • Cutler et al. (2014) placed hives of honey bee in fields of canola treated with clothianidin for the flowering period, then maintained them in apiaries surrounded by untreated crops. Comparison with control hives showed no detectable effects on colony performance or winter survival. ...
This report can be found at www.easac.eu EASAC EASAC – the European Academies' Science Advisory Council – is formed by the national science academies of the EU Member States to enable them to collaborate with each other in giving advice to European policy-makers. It thus provides a means for the collective voice of European science to be heard. EASAC was founded in 2001 at the Royal Swedish Academy of Sciences. Its mission reflects the view of academies that science is central to many aspects of modern life and that an appreciation of the scientific dimension is a prerequisite to wise policy-making. This view already underpins the work of many academies at national level. With the growing importance of the European Union as an arena for policy, academies recognise that the scope of their advisory functions needs to extend beyond the national to cover also the European level. Here it is often the case that a trans-European grouping can be more effective than a body from a single country. The academies of Europe have therefore formed EASAC so that they can speak with a common voice with the goal of building science into policy at EU level. Through EASAC, the academies work together to provide independent, expert, evidence-based advice about the scientific aspects of public policy to those who make or influence policy within the European institutions. Drawing on the memberships and networks of the academies, EASAC accesses the best of European science in carrying out its work. Its views are vigorously independent of commercial or political bias, and it is open and transparent in its processes. EASAC aims to deliver advice that is comprehensible, relevant and timely.
... For example, for foliar applications of compounds in the nitroguanidine class of neonicotinoids (imidacloprid, thiamethoxam, clothianidin, and dinotefuran), there are warnings on product labels in North America not to apply or allow them to drift on to flowering crops or weeds if bees are foraging in the treated area. To minimize exposure to contaminated dust generated during the planting of neonicotinoid treated seeds, which can result in bee-kill incidents (Cutler, Scott-Dupree & Drexler, 2014), efforts are being made to improve the seed treatment process, modify planting equipment, and encourage best management practices among growers and beekeepers to reduce pollinator risk from exposure to neonicotinoid contaminated dust from treated seed (Nuyttens et al., 2013; Health Canada Pest Management Regulatory Agency, 2013). There is perhaps more debate regarding potential risks to bees through feeding on nectar or pollen from plants grown from seed treated with neonicotinoids. ...
In summer 2012, we initiated a large-scale field experiment in southern Ontario, Canada, to determine whether exposure to clothianidin seed-treated canola (oil seed rape) has any adverse impacts on honey bees. Colonies were placed in clothianidin seed-treated or control canola fields during bloom, and thereafter were moved to an apiary with no surrounding crops grown from seeds treated with neonicotinoids. Colony weight gain, honey production, pest incidence, bee mortality, number of adults, and amount of sealed brood were assessed in each colony throughout summer and autumn. Samples of honey, beeswax, pollen, and nectar were regularly collected, and samples were analyzed for clothianidin residues. Several of these endpoints were also measured in spring 2013. Overall, colonies were vigorous during and after the exposure period, and we found no effects of exposure to clothianidin seed-treated canola on any endpoint measures. Bees foraged heavily on the test fields during peak bloom and residue analysis indicated that honey bees were exposed to low levels (0.5-2 ppb) of clothianidin in pollen. Low levels of clothianidin were detected in a few pollen samples collected toward the end of the bloom from control hives, illustrating the difficulty of conducting a perfectly controlled field study with free-ranging honey bees in agricultural landscapes. Overwintering success did not differ significantly between treatment and control hives, and was similar to overwintering colony loss rates reported for the winter of 2012-2013 for beekeepers in Ontario and Canada. Our results suggest that exposure to canola grown from seed treated with clothianidin poses low risk to honey bees.
... For example, for foliar applications of compounds in the nitroguanidine class of neonicotinoids (imidacloprid, thiamethoxam, clothianidin, and dinotefuran), there are warnings on product labels in North America not to apply or allow them to drift on to flowering crops or weeds if bees are foraging in the treated area. To minimize exposure to contaminated dust generated during the planting of neonicotinoid treated seeds, which can result in bee-kill incidents (Cutler, Scott-Dupree & Drexler, 2014), efforts are being made to improve the seed treatment process, modify planting equipment, and encourage best management practices among growers and beekeepers to reduce pollinator risk from exposure to neonicotinoid contaminated dust from treated seed (Nuyttens et al., 2013; Health Canada Pest Management Regulatory Agency, 2013). There is perhaps more debate regarding potential risks to bees through feeding on nectar or pollen from plants grown from seed treated with neonicotinoids. ...
... Monitoring studies by Blacquiere et al. [11] and others conclude that residue concentrations in crops following application of neonicotinoids at recommended rates are too low to cause significant sublethal effects to honeybees. Cutler et al. [35] reviewed the Incident Reporting Program of the Canadian Pest Management Regulatory Agency and reported 110 incidents involving field mortality of bees in Canada since 2007, only 6 of which occurred prior to 2012. Although the neonicotinoids were suspected in a majority of incidents, including a large number in Ontario and Quebec in 2012, more than 90% of these were classified as "minor," meaning that less than 10% of honeybees in the colony were affected; most of the "major" incidents were attributable to other insecticide classes. ...
The European honeybee, Apis mellifera, is an important pollinator of agricultural crops. Since 2006, when unexpectedly high colony losses were first reported, articles have proliferated in the popular press suggesting a range of possible causes and raising alarm over the general decline of bees. Suggested causes include pesticides, genetically modified crops, habitat fragmentation, and introduced diseases and parasites. Scientists have concluded that multiple factors in various combinations-including mites, fungi, viruses, and pesticides, as well as other factors such as reduction in forage, poor nutrition, and queen failure-are the most probable cause of elevated colony loss rates. Investigators and regulators continue to focus on the possible role that insecticides, particularly the neonicotinoids, may play in honeybee health. Neonicotinoid insecticides are insect neurotoxicants with desirable features such as broad-spectrum activity, low application rates, low mammalian toxicity, upward systemic movement in plants, and versatile application methods. Their distribution throughout the plant, including pollen, nectar, and guttation fluids, poses particular concern for exposure to pollinators. The authors describe how neonicotinoids interact with the nervous system of honeybees and affect individual honeybees in laboratory situations. Because honeybees are social insects, colony effects in semifield and field studies are discussed. The authors conclude with a review of current and proposed guidance in the United States and Europe for assessing the risks of pesticides to honeybees. Environ Toxicol Chem 2014;33:719-731. © 2014 The Authors. Environmental Toxicology and Chemistry Published by Wiley Periodicals, Inc., on behalf of SEATC. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution, and reproduction in any medium, provided the original work is properly cited.
Neonicotinoid insecticides have been implicated in honey bee declines, with many studies showing that sublethal exposure impacts bee behaviors such as foraging, learning, and memory. Despite the large number of ecotoxicological studies carried out to date, most focus on a handful of worker phenotypes leading to a “streetlight effect” where the a priori choice of phenotypes to measure may influence the results and conclusions arising from the studies. This bias can be overcome with the use of toxicological transcriptomics, where changes in gene expression can provide a more objective view of how pesticides alter animal traits. Here, we used RNA sequencing to examine the changes in neurogenomic states of nurse and forager honey bees that were naturally exposed to neonicotinoids in the field and artificially exposed to neonicotinoids in a controlled experiment. We found that neonicotinoid exposure influenced the neurogenomic state of foragers and nurses in different ways; foragers experienced shifts in expression of genes involved in cognition and development, while nurses experienced shifts in expression of genes involved in metabolism. Our study suggests that neonicotinoids influence nurse and forager bees in a different manner. We also found no to minimal overlap in the differentially expressed genes in our study and in previously published studies, which might help reconcile the seemingly contradictory results often reported in the neonicotinoid literature.
The decline in populations of insect pollinators is a global concern. While multiple factors are implicated, there is uncertainty surrounding the contribution of certain groups of pesticides to losses in wild and managed bees. Nanotechnology-based pesticides (NBPs) are formulations based on multiple particle sizes and types. By packaging active ingredients in engineered particles, NBPs offer many benefits and novel functions, but may also exhibit different properties in the environment when compared with older pesticide formulations. These new properties raise questions about the environmental disposition and fate of NBPs and their exposure to pollinators. Pollinators such as honey bees have evolved structural adaptations to collect pollen, but also inadvertently gather other types of environmental particles which may accumulate in hive materials. Knowledge of the interaction between pollinators, NBPs, and other types of particles is needed to better understand their exposure to pesticides, and essential for characterizing risk from diverse environmental contaminants. The present review discusses the properties, benefits and types of nanotechnology-based pesticides, the propensity of bees to collect such particles and potential impacts on bee pollinators.
The decline in populations of insect pollinators is a global concern. While multiple factors are implicated, there is uncertainty surrounding the contribution of certain groups of pesticides to losses in wild and managed bees. Nanotechnology-based pesticides (NBPs) are formulations based on multiple particle sizes and types. By packaging active ingredients in engineered particles, NBPs offer many benefits and novel functions, but may also exhibit different properties in the environment when compared with older pesticide formulations. These new properties raise questions about the environmental disposition and fate of NBPs and their exposure to pollinators. Pollinators such as honey bees have evolved structural adaptations to collect pollen, but also inadvertently gather other types of environmental particles which may accumulate in hive materials. Knowledge of the interaction between pollinators, NBPs, and other types of particles is needed to better understand their exposure to pesticides, and essential for characterizing risk from diverse environmental contaminants. The present review discusses the properties, benefits and types of nanotechnology-based pesticides, the propensity of bees to collect such particles and potential impacts on bee pollinators.
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.
Recent research has demonstrated colony-level sublethal effects of imidacloprid on bumble bees affecting foraging and food consumption, and thus colony growth and reproduction, at lower pesticide concentrations than for honey bee colonies. However, these studies may not reflect the full effects of neonicotinoids on bumble bees because bumble bee life cycles are different from those of honey bees. Unlike honey bees, bumble bees live in colonies for only a few months each year. Assessing the sublethal effects of systemic insecticides only on the colony level is appropriate for honey bees, but for bumble bees, this approach addresses just part of their annual life cycle. Queens are solitary from the time they leave their home colonies in fall until they produce their first workers the following year. Queens forage for pollen and nectar, and are thus exposed to more risk of direct pesticide exposure than honey bee queens. Almost no research has been done on pesticide exposure to and effects on bumble bee queens. Additional research should focus on critical periods in a bumble bee queen's life which have the greatest nutritional demands, foraging requirements, and potential for exposure to pesticides, particularly the period during and after nest establishment in the spring when the queen must forage for the nutritional needs of her brood and for her own needs while she maintains an elevated body temperature in order to incubate the brood.
Tools are provided to assess the health status of managed honeybee colonies by facilitating further harmonisation of data collection and reporting, design of field surveys across the European Union (EU) and analysis of data on bee health. The toolbox is based on characteristics of a healthy managed honeybee colony: an adequate size, demographic structure and behaviour; an adequate production of bee products (both in relation to the annual life cycle of the colony and the geographical location); and provision of pollination services. The attributes 'queen presence and performance', 'demography of the colony', 'in-hive products' and 'disease, infection and infestation' could be directly measured in field conditions across the EU, whereas 'behaviour and physiology' is mainly assessed through experimental studies. Analysing the resource providing unit, in particular land cover/use, of a honeybee colony is very important when assessing its health status, but tools are currently lacking that could be used at apiary level in field surveys across the EU. Data on 'beekeeping management practices' and 'environmental drivers' can be collected via questionnaires and available databases, respectively. The capacity to provide pollination services is regarded as an indication of a healthy colony, but it is assessed only in relation to the provision of honey because technical limitations hamper the assessment of pollination as regulating service (e.g. to pollinate wild plants) in field surveys across the EU. Integrating multiple attributes of honeybee health, for instance, via a Health Status Index, is required to support a holistic assessment. Examples are provided on how the toolbox could be used by different stakeholders. Continued interaction between the Member State organisations, the EU Reference Laboratory and EFSA is required to further validate methods and facilitate the efficient use of precise and accurate bee health data that are collected by many initiatives throughout the EU.
Crop seeds are often treated with pesticides before planting. Pesticide-laden dust particles can be abraded from the seed coating during planting and expelled into the environment, damaging non-target organisms. Drift of these dust particles depends on their size, shape and density. In this work, we used X-ray micro-CT to examine the size, shape (sphericity) and porosity of dust particles from treated seeds of various crops. The dust properties quantified in this work were very variable in different crops. This variability may be a result of seed morphology, seed batch, treatment composition, treatment technology, seed cleaning or an interaction of these factors. The intra-particle porosity of seed treatment dust particles varied from 0.02 to 0.51 according to the crop and generally increased with particle size. Calculated settling velocities demonstrated that accounting for particle shape and porosity is important in drift studies. For example, the settling velocity of dust particles with an equivalent diameter of 200 µm may vary between 0.1 and 1.2 m s-1, depending on their shape and density. Our analysis shows that in a wind velocity of 5 m s-1, such particles ejected at 1 m height may travel between 4 and 50 m from the source before settling. While micro-CT is a valuable tool to characterize dust particles, the current image processing methodology limits the number of particles that can be analyzed.
Although invertebrates generally have a low public profile, the honey bee, Apis mellifera L., is a flagship species whose popularity likely derives from the products it provides and its perceived ecological services. Therefore, the raging debate regarding honey bee decline has surpassed the realm of beekeepers, academia, industry and regulatory agencies and now also encompasses non-governmental agencies, media, fiction writers and the general public. The early interest and concern about honey bee colony collapse disorder (CCD) soon shifted to the bigger issue of pollinator decline, with a focus on the potential involvement of pesticides in such a phenomenon. Pesticides were previously recognized as the potential culprits of the reported declines, particularly the neonicotinoid insecticides due to their widespread and peculiar use in agriculture. However, the evidence for the potential pivotal role of these neonicotinoids in the honey bee decline remains a matter of debate, with an increased recognition of the multifactorial nature of the problem and the lack of a direct association between the noted decline and neonicotinoid use. The focus on the decline of honey bee populations subsequently spread to other species, and bumble bees became another matter of concern, particularly in Europe and the US. Other bee species, ones that are particularly important in other regions of the world, remain the object of little concern (unjustifiably so). Furthermore, the continuous focus on neonicotinoids is also in need of revision, as the current evidence suggests that a broad spectrum of compounds deserve attention. Here we address both shortcomings.
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An overview of hybrid seed canola pollination through the use of managed colonies of honey bees in southern Alberta.
Clay, H. 2009 Pollinating hybrid canola- the southern Alberta experience. Hivelights 22(3):14-16
In Northern Italy from 2000 to 2008, many spring bee mortalities were clearly linked to sowing of maize seeds dressed with insecticides. In the present study, we investigated the effects on honey bees of clothianidinderived from maize seed-dressing
(Poncho®) in laboratory (test by indirect contact) and in semi-field conditions. Despite the reduction of dust dispersion due to the
application of the best available sowing techniques (pneumatic seeder equipped with deflector,improvement of seed-dressing
quality) our results showed negative effects on honey bees at individual level. In semi-field study, no effect was observed at the
colony level despite the high bee mortality rate for 2-3 days after dust application. However, we can expect a colony decline and
low honey production if this high forager mortality rate lasts for longer than 10 days. Such a situation is possible if the sowing
period lasts several days as in the Po Valley, where the landscape is characterized by extended maize cultivation.
Specific methodologies to assess the effects of dust have never been included in the official guidelines for the evaluation of
side-effects of plant protection products on honey bees. For this reason, suitable and standardized methods for testing in laboratory and in semi-field conditions the effects on honey bees ofcontaminated dust dispersed during sowing were evaluated
The risk exposure of bee colonies to the toxicity of systemic neonicotinoid insecticides was assessed. Various methods of chemical prevention of commercial winter and spring oilseed rape crops in field-realistic conditions were taken into account in the assessment. Pesticides were applied in accordance with the actual agricultural practice. Commercial crop protection products with thiamethoxam, clothianidin or imidacloprid were used as seed treatment. Formulations containing acetamiprid or thiacloprid were used for spraying. Fifteen healthy bee colonies were placed in close proximity to each of the oilseed rape fields throughout the blooming period. During florescence, the samples of nectar (directly from flowers and nectar flow from combs) and pollen loads were collected repeatedly. Samples of honey, bee bread and adult bees were taken one week after the end of plants flowering. To ensure high specificity and sensitivity of analysed pestcicides modified QuEChERS extraction method and liquid chromatography coupled with tandem mass spectrometry (LC-MS/MS) was used. The five of neonicotinoid insecticides (imidacloprid, clothianidin, thiametoxam, acetamiprid and thiacloprid) were analyzed in multi-residue method with 0.1 - 10 ng/g limits of detection. Palynological analysis was done to determine the botanical origin of the nectar, honey and pollen. Development of bee colonies (brood area, worker biomass, colony health) was assessed every 3 weeks until the end of the beekeeping season. The amount of pollen collected by bees per hive, bee bread area and rape honey yield was also measured. The long-term effects of insecticides on bees were estimated using the same methods in April of the following year.
This paper reviews the available data on the risk potential posed by imidacloprid seed dressings to honey bees. Key studies are briefly described and their results are discussed; of particular interest for this topic are the numerous field and semifield trials which were carried out by different scientists from various institutions. From the reviewed studies a field-relevant NOAEC of 20 ppb is concluded for honey bees. Analytical studies on nectar and pollen samples of sunflower, rape and corn plants have shown that residue levels of imidacloprid and toxicologically relevant imidacloprid metabolites are typically well below 5 ppb. When comparing the NOAEC with the reported residue data, it becomes evident that imidacloprid seed-dressings will pose only a negli- gible risk to honey bees. This conclusion is supported by the findings of more than 30 semifield and field studies conducted in various regions of the world. Finally, the symptoms of the bee incidents in France, which were suspected to be related to imida- cloprid seed-dressings, are described and factors potentially linked to these incidents are discussed.
Dressing seeds with pesticides to control pests is a widespread practice with important advantages. Recent incidents of bee losses, however, have directed attention to the emission of abraded pesticide-coated seed particles to the environment during sowing. This phenomenon of drift of pesticide dust can lead to pesticide contamination of air, water and other natural resources in crop-growing areas. This review article presents the state of the art of the phenomenon of dust emission and drift from pesticide seed dressing during sowing and its consequences. Firstly, pesticide seed treatment is defined and its pros and cons are set out, with the focus on dust, dust emission and dust drift from pesticide-coated seed. The factors affecting emission of pesticide dust (e.g. seed treatment quality, seed drilling technology and environmental conditions) are considered, along with its possible effects. The measuring techniques and protocols and models currently in use for calculating the behaviour of dust are reviewed, together with their features and limitations. Finally, possible mitigation measures are discussed, such as improving the seed quality and the use of modified seed drilling technology, and an overview of regulations and stewardship activities is given. © 2013 Society of Chemical Industry.
Reported widespread declines of wild and managed insect pollinators have serious consequences for global ecosystem services and agricultural production. Bees contribute approximately 80% of insect pollination, so it is important to understand and mitigate the causes of current declines in bee populations . Recent studies have implicated the role of pesticides in these declines, as exposure to these chemicals has been associated with changes in bee behaviour and reductions in colony queen production. However, the key link between changes in individual behaviour and the consequent impact at the colony level has not been shown. Social bee colonies depend on the collective performance of many individual workers. Thus, although field-level pesticide concentrations can have subtle or sublethal effects at the individual level, it is not known whether bee societies can buffer such effects or whether it results in a severe cumulative effect at the colony level. Furthermore, widespread agricultural intensification means that bees are exposed to numerous pesticides when foraging, yet the possible combinatorial effects of pesticide exposure have rarely been investigated. Here we show that chronic exposure of bumblebees to two pesticides (neonicotinoid and pyrethroid) at concentrations that could approximate field-level exposure impairs natural foraging behaviour and increases worker mortality leading to significant reductions in brood development and colony success. We found that worker foraging performance, particularly pollen collecting efficiency, was significantly reduced with observed knock-on effects for forager recruitment, worker losses and overall worker productivity. Moreover, we provide evidence that combinatorial exposure to pesticides increases the propensity of colonies to fail.
Henry et al. (Reports, 20 April, p. 348) used a model to predict that colony collapse in honey bees could be precipitated by pesticide-induced
intoxication that disrupts navigation. Here, we show that collapse disappears when the model is recalculated with parameter
values appropriate to the season when most pesticide-treated flowering crops bloom.
This paper assessed the potential exposure of bees (Apis mellifera L.) to pesticides during maize (Zea mays L.) sowing with pneumatic drills. Data were derived from tests carried out in field tests, comparing two configurations of a pneumatic precision drill: conventional drill; drill with air deflectors. In addition, static tests simulating the sowing under controlled conditions, were performed on the drill equipped with an innovative system developed at CRA-ING. During the field tests, the concentrations in the air of the active ingredients of four insecticides used in maize seed dressing (imidacloprid, clothianidin, thiamethoxam and fipronil) were recorded. The concentrations of active ingredients in the air were used for assessing the quantities of active ingredients that a bee might intercept as it flies in a sort of virtual tunnel, the dimensions of which were dependent upon the bee body cross-section and the length of flight. The results of the field tests show that the air deflectors were not completely effective in reducing the amount of active ingredients dispersed in the air. The results of the static tests with drill equipped with the prototype indicated reductions of the active ingredient air concentrations ranging from 72 % up to 95 %, with reference to the conventional drill. Such ratios were applied to the amounts of active ingredients intercepted by the bees in the virtual tunnel contributing to a consistent reduction of the probability that sub-lethal effects can occur.
Bad News for Bees
Neonicotinoid insecticides were introduced in the early 1990s and have become one of the most widely used crop pesticides in the world. These compounds act on the insect central nervous system, and they have been shown to be persistent in the environment and in plant tissues. Recently, there have been controversial connections made between neonicotinoids and pollinator deaths, but the mechanisms underlying these potential deaths have remained unknown. Whitehorn et al. (p. 351 , published online 29 March) exposed developing colonies of bumble bees to low levels of the neonicotinoid imidacloprid and then released them to forage under natural conditions. Treated colonies displayed reduced colony growth and less reproductive success, and they produced significantly fewer queens to found subsequent generations. Henry et al. (p. 348 , published online 29 March) documented the effects of low-dose, nonlethal intoxication of another widely used neonicotinoid, thiamethoxam, on wild foraging honey bees. Radio-frequency identification tags were used to determine navigation success of treated foragers, which suggested that their homing success was much reduced relative to untreated foragers.
Neonicotinoid insecticides are successfully applied to control pests in a variety of agricultural crops; however, they may not only affect pest insects but also non-target organisms such as pollinators. This review summarizes, for the first time, 15 years of research on the hazards of neonicotinoids to bees including honey bees, bumble bees and solitary bees. The focus of the paper is on three different key aspects determining the risks of neonicotinoid field concentrations for bee populations: (1) the environmental neonicotinoid residue levels in plants, bees and bee products in relation to pesticide application, (2) the reported side-effects with special attention for sublethal effects, and (3) the usefulness for the evaluation of neonicotinoids of an already existing risk assessment scheme for systemic compounds. Although environmental residue levels of neonicotinoids were found to be lower than acute/chronic toxicity levels, there is still a lack of reliable data as most analyses were conducted near the detection limit and for only few crops. Many laboratory studies described lethal and sublethal effects of neonicotinoids on the foraging behavior, and learning and memory abilities of bees, while no effects were observed in field studies at field-realistic dosages. The proposed risk assessment scheme for systemic compounds was shown to be applicable to assess the risk for side-effects of neonicotinoids as it considers the effect on different life stages and different levels of biological organization (organism versus colony). Future research studies should be conducted with field-realistic concentrations, relevant exposure and evaluation durations. Molecular markers may be used to improve risk assessment by a better understanding of the mode of action (interaction with receptors) of neonicotinoids in bees leading to the identification of environmentally safer compounds.
The development of insecticides requires valid risk assessment procedures to avoid causing harm to beneficial insects and especially to pollinators such as the honeybee Apis mellifera. In addition to testing according to current guidelines designed to detect bee mortality, tests are needed to determine possible sublethal effects interfering with the animal's vitality and behavioral performance. Several methods have been used to detect sublethal effects of different insecticides under laboratory conditions using olfactory conditioning. Furthermore, studies have been conducted on the influence insecticides have on foraging activity and homing ability which require time-consuming visual observation. We tested an experimental design using the radiofrequency identification (RFID) method to monitor the influence of sublethal doses of insecticides on individual honeybee foragers on an automated basis. With electronic readers positioned at the hive entrance and at an artificial food source, we obtained quantifiable data on honeybee foraging behavior. This enabled us to efficiently retrieve detailed information on flight parameters. We compared several groups of bees, fed simultaneously with different dosages of a tested substance. With this experimental approach we monitored the acute effects of sublethal doses of the neonicotinoids imidacloprid (0.15-6 ng/bee) and clothianidin (0.05-2 ng/bee) under field-like circumstances. At field-relevant doses for nectar and pollen no adverse effects were observed for either substance. Both substances led to a significant reduction of foraging activity and to longer foraging flights at doses of ≥0.5 ng/bee (clothianidin) and ≥1.5 ng/bee (imidacloprid) during the first three hours after treatment. This study demonstrates that the RFID-method is an effective way to record short-term alterations in foraging activity after insecticides have been administered once, orally, to individual bees. We contribute further information on the understanding of how honeybees are affected by sublethal doses of insecticides.
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.
Recent declines in honey bees for crop pollination threaten fruit, nut, vegetable and seed production in the United States. A broad survey of pesticide residues was conducted on samples from migratory and other beekeepers across 23 states, one Canadian province and several agricultural cropping systems during the 2007-08 growing seasons.
We have used LC/MS-MS and GC/MS to analyze bees and hive matrices for pesticide residues utilizing a modified QuEChERS method. We have found 121 different pesticides and metabolites within 887 wax, pollen, bee and associated hive samples. Almost 60% of the 259 wax and 350 pollen samples contained at least one systemic pesticide, and over 47% had both in-hive acaricides fluvalinate and coumaphos, and chlorothalonil, a widely-used fungicide. In bee pollen were found chlorothalonil at levels up to 99 ppm and the insecticides aldicarb, carbaryl, chlorpyrifos and imidacloprid, fungicides boscalid, captan and myclobutanil, and herbicide pendimethalin at 1 ppm levels. Almost all comb and foundation wax samples (98%) were contaminated with up to 204 and 94 ppm, respectively, of fluvalinate and coumaphos, and lower amounts of amitraz degradates and chlorothalonil, with an average of 6 pesticide detections per sample and a high of 39. There were fewer pesticides found in adults and brood except for those linked with bee kills by permethrin (20 ppm) and fipronil (3.1 ppm).
The 98 pesticides and metabolites detected in mixtures up to 214 ppm in bee pollen alone represents a remarkably high level for toxicants in the brood and adult food of this primary pollinator. This represents over half of the maximum individual pesticide incidences ever reported for apiaries. While exposure to many of these neurotoxicants elicits acute and sublethal reductions in honey bee fitness, the effects of these materials in combinations and their direct association with CCD or declining bee health remains to be determined.
Beekeepers suspected maize, Zea mays L., treated with imidacloprid to result in substantial loss of honey bee (Hymenoptera: Apidae) colonies in Belgium. The objective of this study was to investigate the potential impact of maize grown from imidacloprid-treated seeds on honey bee mortality. A survey of 16 apiaries was carried out, and all maize fields treated or not with imidacloprid were located within a radius of 3,000 m around the observed apiaries. Samples of honey, beeswax, and bees were collected in three colonies per apiary and analyzed for pesticide contain by liquid chromatography-tandem mass spectrometry and gas chromatography-tandem mass spectrometry. We first found a significant correlation between the number of colonies per apiary and the mortality rates in an apiary. In addition, this mortality rate was inversely correlated with the surface of maize fields treated and not with imidacloprid, suggesting that this pesticide do not interact with bees' fitness. Moreover, a very large number of our samples contained acaricides either prohibited or ineffective against Varroa destructor (Anderson & Trueman) (Acari: Varroidae), suggesting that the treatment methods used by the beekeepers to be inadequate for mite control. Our results support the hypothesis that imidacloprid seed-treated maize has no negative impact on honey bees.
Laboratory bioassays were conducted to evaluate the effects on honeybee behavior of sublethal doses of insecticides chronically administered orally or by contact. Emergent honeybees received a daily dose of insecticide ranging from one-fifth to one-five-hundredth of the median lethal dose (LD50) during 11 d. After exposure to fipronil (0.1 and 0.01 ng/bee), acetamiprid (1 and 0.1 microg/bee), or thiamethoxam (1 and 0.1 ng/bee), behavioral functions of honeybees were tested on day 12. Fipronil, used at the dose of 0.1 ng/bee, induced mortality of all honeybees after one week of treatment. As a result of contact treatment at 0.01 ng/bee, honeybees spent significantly more time immobile in an open-field apparatus and ingested significantly more water. In the olfactory conditioning paradigm, fipronil-treated honeybees failed to discriminate between a known and an unknown odorant. Thiamethoxam by contact induced either a significant decrease of olfactory memory 24 h after learning at 0.1 ng/bee or a significant impairment of learning performance with no effect on memory at 1 ng/bee. Responsiveness to antennal sucrose stimulation was significantly decreased for high sucrose concentrations in honeybees treated orally with thiamethoxam (1 ng/bee). The only significant effect of acetamiprid (administered orally, 0.1 microg/bee) was an increase in responsiveness to water. The neonicotinoids acetamiprid and thiamethoxam tested at the highest dose (one-tenth and one-fifth of their oral LD50, respectively) and fipronil at one-five-hundredth of LD50 have limited effects on the motor, sensory, and cognitive functions of the honeybee. Our data on the intrinsic toxicity of the compounds after chronic exposure have to be taken into account for evaluation of risk to honeybees in field conditions.
Insecticides used on turf are sometimes applied to areas with flowering weeds that attract honey bees and native pollinators. We tested residual effects of such treatments on colony vitality and behavior of the bumble bees Bombus impatiens Cresson foraging on turf containingwhite clover, Trifolium repens L. Imidacloprid, a syst emic chloronicotinyl used for preventive control of root-feeding grubs, was applied as granules, followed by irrigation, or sprayed as a wettable powder, with or without irrigation. Hives were confined on the plots in large field cages after residues had dried and colony vitality (i.e., numbers of brood, workers, and honey pots, and weights of queens, workers, and whole colonies with hives) was evaluated after 28-30 d. Workers' foraging activity and defensive response to an aggressive stimulus also were evaluated. In another test, weedy turf was sprayed with chlorpyrifos, carbaryl, or cyfluthrin at labeled rates for surface-feeding pests. Bee colonies were confined on the plots after residues had dried, with effects on colony vitality evaluated after 14 d. Finally, foraging activity of wild bumble bees was monitored on open plots to determine if insecticide-treated areas were avoided. Imidacloprid granules, and imidacloprid sprays applied with posttreatment irrigation, had no effect on colony vitality or workers' behavior, suggesting that such treatments pose little systemic or residual hazard to bumble bees. In contrast, exposure to dry nonirrigated residues of all of the aforementioned insecticides had severe impact on colony vitality. Foraging workers did not avoid insecticide-treated areas. Means by which turf managers can reduce hazards of insecticide applications to pollinators are discussed.
We conducted laboratory experiments to investigate the lethal and sublethal effects of clothianidin on bumble bee, Bombus impatiens Cresson, colony health and foraging ability. Bumble bee colonies were exposed to 6 ppb clothianidin, representing the highest residue levels found in field studies on pollen, and a higher dose of 36 ppb clothianidin in pollen. Clothianidin did not effect pollen consumption, newly emerged worker weights, amount of brood or the number of workers, males, and queens at either dose. The foraging ability of worker bees tested on an artificial array of complex flowers also did not differ among treatments. These results suggest that clothianidin residues found in seed-treated canola and possibly other crops will not adversely affect the health of bumble bee colonies or the foraging ability of workers.
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.
The issue of declining bee health has been in the public eye for some time and it still remains unsolved. The cause of the decline is complex and there is no evidence pointing to a single cause. There are some organisations which push the concept that the decline in bee populations is due to pesticides, the main focus of which is currently the class of insecticides known as the neonicotinoids. There have been recent reviews of this class of insecticides by European Food Safety Agency (EFSA), which has resulted in a call for a European wide restriction of these pesticides by the European Commission (EC). This article is an analysis of these EFSA neonicotinoid reviews and the recent published EFSA scientific opinion and draft guidance for assessing effects of pesticides on bees, which were used as a basis for these reviews. As a result of some highly publicized laboratory studies in 2012, the EC urgently commissioned EFSA to review the risk to bees from the neonicotinoids. EFSA were given a narrow mandate and the time available to complete the reviews was extremely limited. Indeed, by the time the mandate was finalized EFSA had just a few months to complete the reviews in order to meet the EC deadline. Consequently, EFSA were pushed into taking an extremely critical and highly conservative approach in their review, identifying a long list of potential data gaps and risks to bees. However, several important flaws can be identified in some of the specific risk assessments carried out (e.g. for dust and guttation), in the general methodology used (e.g. virtually discounting all field studies and weight of evidence) and the fact that the science based approach used is not yet agreed or adopted within EU, and indeed is considered very controversial by the scientific and regulatory community. As a result the EC has proposed a severe EU wide restriction on the use of the neonicotinoids as seed treatments, soil applications and foliar treatments, even though the foliar uses have not yet been reviewed by EFSA or the MSs. These restrictions must also be considered in light of the recent Humboldt Forum study which concluded that neonicotinoid pesticides make anenormous socio-economic and environmental contribution to European agriculture and the wider economy. Neonicotinoid seed treatments are the most advanced crop protection solutions available for the targeted control of extraordinarily damaging pests. Neonicotinoids are applied with dose rates typically 10–20 times lower than the best available alternatives and prevent crop losses resulting in up to 40% reduction in yield. Without these products an additional 3 million hectares of land outside Europe will need to be brought into production adding an environmental burden of 600 million tons of CO2. It is clear that we need healthy and thriving bee populations. The sustainability of agriculture depends on this. But we also need safe, modern, and innovative pesticides like the neonicotinoids if we are to produce the food we need. Rather than focusing on potential theoretical risks to bees under worst case unrealistic conditions from pesticides, we need to develop regulatory risk assessment guidance that enables in-use field realistic assessment approaches. In this way products and practices can be developed that allow bees and pesticides to co-exist together in a sustainable agricultural production system.
Beekeepers suspected maize, Zea mays L., treated with imidacloprid to result in substantial loss of honey bee (Hymenoptera: Apidae) colonies in Belgium. The objective of this study was to investigate the potential impact of maize grown from imidacloprid-treated seeds on honey bee mortality. A survey of 16 apiaries was carried out, and all maize fields treated or not with imidacloprid were located within a radius of 3,000 m around the observed apiaries. Samples of honey, beeswax, and bees were collected in three colonies per apiary and analyzed for pesticide contain by liquid chromatography-tandem mass spectrometry and gas chromatography-tandem mass spectrometry. We first found a significant correlation between the number of colonies per apiary and the mortality rates in an apiary. In addition, this mortality rate was inversely correlated with the surface of maize fields treated and not with imidacloprid, suggesting that this pesticide do not interact with bees' fitness. Moreover, a very large number of our samples contained acaricides either prohibited or ineffective against Varroa destructor (Anderson & Trueman) (Acari: Varroidae), suggesting that the treatment methods used by the beekeepers to be inadequate for mite control. Our results support the hypothesis that imidacloprid seed-treated maize has no negative impact on honey bees.
Losses of honeybees have been reported in Italy concurrent with the sowing of corn coated with neonicotinoids using a pneumatic drilling machine. Being unconvinced that solid particles containing systemic insecticide, falling on the vegetation surrounding the sown area, could poison bees foraging on contaminated nectar and pollen, the effect of direct aerial powdering was tested on foragers in free flight near the drilling machine. Bees were conditioned to visit a dispenser of sugar solution whilst a drilling machine was sowing corn along the flight path. Samples of bees were captured on the dispenser, caged and held in the laboratory. Chemical analysis showed some hundred nanograms of insecticide per bee. Nevertheless, caged bees, previously contaminated in flight, died only if kept in conditions of high humidity. After the sowing, an increase in bee mortality in front of the hives was also observed. Spring bee losses, which corresponded with the sowing of corn-coated seed, seemed to be related to the casual encountering of drilling machine during foraging flight across the ploughed fields.
Bad News for Bees
Neonicotinoid insecticides were introduced in the early 1990s and have become one of the most widely used crop pesticides in the world. These compounds act on the insect central nervous system, and they have been shown to be persistent in the environment and in plant tissues. Recently, there have been controversial connections made between neonicotinoids and pollinator deaths, but the mechanisms underlying these potential deaths have remained unknown. Whitehorn et al. (p. 351 , published online 29 March) exposed developing colonies of bumble bees to low levels of the neonicotinoid imidacloprid and then released them to forage under natural conditions. Treated colonies displayed reduced colony growth and less reproductive success, and they produced significantly fewer queens to found subsequent generations. Henry et al. (p. 348 , published online 29 March) documented the effects of low-dose, nonlethal intoxication of another widely used neonicotinoid, thiamethoxam, on wild foraging honey bees. Radio-frequency identification tags were used to determine navigation success of treated foragers, which suggested that their homing success was much reduced relative to untreated foragers.
Honey bees are important pollinators of both crops and wild plants. Pesticide regimes that threaten their sustainability should therefore be assessed. As an example, evidence that the agricultural use of neonicotinoid pesticides is a cause of the recently observed declines in honey bees is examined. The aim is to define exacting demographic conditions for a detrimental factor to precipitate a population decline, and Hill's epidemiological 'causality criteria' are employed as a structured process for making an expert judgement about the proposition that trace dietary neonicotinoids in nectar and pollen cause population declines in honey bees.
In spite of the absence of decisive experimental results, the analysis shows that, while the proposition is a substantially justified conjecture in the context of current knowledge, it is also substantially contraindicated by a wide variety of circumstantial epidemiological evidence.
It is concluded that dietary neonicotinoids cannot be implicated in honey bee declines, but this position is provisional because important gaps remain in current knowledge. Avenues for further investigations to resolve this longstanding uncertainty are therefore identified.
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.
Laboratory bioassays were conducted to determine the contact honey bee toxicity of commercial and candidate neonicotinoid insecticides. The nitro-substituted compounds were the most toxic to the honey bee in our laboratory studies with LD50 values of 18 ng/bee for imidacloprid, 22 ng for clothianidin, 30 ng for thiamethoxam, 75 ng for dinotefuran and 138 ng for nitenpyram. The cyano-substituted neonicotinoids exhibited a much lower toxicity with LD50 values for acetamiprid and thiacloprid of 7.1 and 14.6 μg/bee, respectively. Piperonyl butoxide, triflumizole and propiconazole increased honey bee toxicity of acetamiprid 6.0-, 244- and 105-fold and thiacloprid 154-, 1,141- and 559-fold, respectively, but had a minimal effect on imidacloprid (1.70, 1.85 and 1.52-fold, respectively). The acetamiprid metabolites, N-demethyl acetamiprid, 6-chloro-3-pyridylmethanol and 6-chloro-nicotinic acid when applied topically, produced no mortality at 50 μg/bee. These results suggest that P450s are an important mechanism for acetamiprid and thiacloprid detoxification and their low toxicity to honey bees. When honey bees were placed in cages in forced contact with alfalfa treated with acetamiprid and the synergist, triflumizole, in combination at their maximum recommended application rates, no mortality was detected above that of the control.
The frequency of occurrence and relative concentration of 44 pesticides in apicultural (Apis mellifera) matrices collected from five French locations (24 apiaries) were assessed from 2002 to 2005. The number and nature of the pesticides investigated varied with the matrices examined-living honeybees, pollen loads, honey, and beeswax. Pollen loads and beeswax had the highest frequency of pesticide occurrence among the apiary matrices examined in the present study, whereas honey samples had the lowest. The imidacloprid group and the fipronil group were detected in sufficient amounts in all matrices to allow statistical comparisons. Some seasonal variation was shown when residues were identified in pollen loads. Given the results (highest frequency of presence) and practical aspects (easy to collect; matrix with no turnover, unlike with bees that are naturally renewed), pollen loads were the best matrix for assessing the presence of pesticide residues in the environment in our given conditions.
Assays were conducted to compare direct and residual contact and oral toxicities to honey bees of sweet corn insecticides and of Bt-sweet corn. Direct contact assays focusing on LC50 determined that technical grade clothianidin was most toxic, > carbofuran, > imidacloprid = spinosad, > lambda-cyhalothrin, > Bacillus thuringiensis. In residual contact assays, forager age bees were exposed to treated non-transgenic sweet corn tassels. Carbofuran treated tassels caused significant mortality up to 2 and 3 days after treatment (DAT) in 2002 and 2003, respectively. Lambda-cyhalothrin treated tassels had no impact on honey bees in 2002; in 2003, their toxicity was significantly higher than the untreated control tassels for 1 DAT. In both years, spinosad, imidacloprid and clothianidin or Bt-sweet corn tassels had no impact on honey bee mortality. Pollen collected from insecticide field treated corn and fed to honey bees had no impact on mortality.
Bombus terrestris bumblebees are important pollinators of wild flowers, and in modern agriculture they are used to guarantee pollination of vegetables and fruits. In the field it is likely that worker bees are exposed to pesticides during foraging. To date, several tests exist to assess lethal and sublethal side-effects of pesticides on bee survival, growth/development and reproduction. Within the context of ecotoxicology and insect physiology, we report the development of a new bioassay to assess the impact of sublethal concentrations on the bumblebee foraging behavior under laboratory conditions. In brief, the experimental setup of this behavior test consists of two artificial nests connected with a tube of about 20 cm and use of queenless micro-colonies of 5 workers. In one nest the worker bees constructed brood, and in the other food (sugar and pollen) was provided. Before exposure, the worker bees were allowed a training to forage for untreated food; afterwards this was replaced by treated food. Using this setup we investigated the effects of sublethal concentrations of the neonicotinoid insecticide imidacloprid, known to negatively affect the foraging behavior of bees. For comparison within the family of neonicotinoid insecticides, we also tested different concentrations of two other neonicotinoids: thiamethoxam and thiacloprid, in the laboratory with the new bioassay. Finally to evaluate the new bioassay, we also tested sublethal concentrations of imidacloprid in the greenhouse with use of queenright colonies of B. terrestris, and here worker bees needed to forage/fly for food that was placed at a distance of 3 m from their hives. In general, the experiments showed that concentrations that may be considered safe for bumblebees can have a negative influence on their foraging behavior. Therefore it is recommended that behavior tests should be included in risk assessment tests for highly toxic pesticides because impairment of the foraging behavior can result in a decreased pollination, lower reproduction and finally in colony mortality due to a lack of food.
Pest management practices may be contributing to a decline in wild bee populations in or near canola (Brassica napus L.) agroecosystems. The objective of this study was to investigate the direct contact toxicity of five technical grade insecticides--imidacloprid, clothianidin, deltamethrin, spinosad, and novaluron--currently used, or with potential for use in canola integrated pest management on bees that may forage in canola: common eastern bumble bees [Bombus impatiens (Cresson); hereafter bumble bees], alfalfa leafcutting bees [Megachile rotundata (F.)], and Osmia lignaria Cresson. Clothianidin and to a lesser extent imidacloprid were highly toxic to all three species, deltamethrin and spinosad were intermediate in toxicity, and novaluron was nontoxic. Bumble bees were generally more tolerant to the direct contact applications > O. lignaria > leafcutting bees. However, differences in relative toxicities between the three species were not consistent, e.g., whereas clothianidin was only 4.9 and 1.3x more toxic, deltamethrin was 53 and 68x more toxic to leafcutting bees than to bumble bees and O. lignaria, respectively. Laboratory assessment of direct contact toxicity, although useful, is only one measure of potential impact, and mortality under field conditions may differ greatly depending on management practices. Research conducted using only honey bees as the indicator species may not adequately reflect the risk posed by insecticides to wild bees because of their unique biology and differential susceptibility. Research programs focused on determining nontarget impact on pollinators should be expanded to include not only the honey bee but also wild bee species representative of the agricultural system under investigation.
Seed coating treatments of sunflower by the systemic insecticide imidacloprid was suspected of affecting honey bees and bumblebees. The hypothesis raised was whether imidacloprid could migrate into nectar and pollen, then modify flower attractiveness, homing behavior, and colony development. Our greenhouse and field experiments with Bombus terrestris L. were aimed at the following: the behavior of workers foraging on treated and control plants blooming in a greenhouse, the homing rate of colonies placed for 9 d in a treated field compared with colonies in a control field, and the development of these 20 colonies under laboratory conditions when removed from the fields. In the greenhouse, workers visited blooming heads of treated and control plants at the same rate and the mean duration of their visits was similar. In field colonies, analysis of pollen in hairs and pellets of workers showed that in both fields 98% of nectar foragers visited exclusively sunflowers, whereas only 25% of pollen gatherers collected sunflower pollen. After 9 d, in the control and treated field, 23 and 33% of the marked foragers, respectively, did not return to hives. In both fields, workers significantly drifted from the center to the sides of colony rows. During the 26-d period under field and laboratory conditions, the population increase rate of the 20 colonies was 3.3 and 3.0 workers/d in hives of the control and treated field, respectively. This difference was not significant. New queens were produced in eight colonies in either field. The mean number of new queens per hive was 17 and 24 in the control and treated field, respectively. Their mating rate was the same. It was concluded that applying imidacloprid at the registered dose, as a seed coating of sunflowers cultivated in greenhouse or in field, did not significantly affect the foraging and homing behavior of B. terestris and its colony development.
In a greenhouse metabolism study, sunflowers were seed-treated with radiolabelled imidacloprid in a 700 g kg−1 WS formulation (Gaucho® WS 70) at 0.7 mg AI per seed, and the nature of the resulting residues in nectar and pollen was determined. Only the parent compound and no metabolites were detected in nectar and pollen of these seed-treated sunflower plants (limit of detection <0.001 mg kg−1). In standard LD50 laboratory tests, imidacloprid showed high oral toxicity to honeybees (Apis mellifera), with LD50 values between 3.7 and 40.9 ng per bee, corresponding to a lethal food concentration between 0.14 and 1.57 mg kg−1. The residue level of imidacloprid in nectar and pollen of seed-treated sunflower plants in the field was negligible. Under field-growing conditions no residues were detected (limit of detection: 0.0015 mg kg−1) in either nectar or pollen. There were also no detectable residues in nectar and pollen of sunflowers planted as a succeeding crop in soils which previously had been cropped with imidacloprid seed-treated plants.
Chronic feeding experiments with sunflower honey fortified with 0.002, 0.005, 0.010 and 0.020 mg kg−1 imidacloprid were conducted to assess potential long-term adverse effects on honeybee colonies. Testing end-points in this 39-day feeding study were mortality, feeding activity, wax/comb production, breeding performance and colony vitality. Even at the highest test concentration, imidacloprid showed no adverse effects on the development of the exposed bee colonies. This no-adverse-effect concentration of 0.020 mg kg−1 compares with a field residue level of less than 0.0015 mg kg−1 ( = limit of detection in the field residue studies) which clearly shows that a sunflower seed dressing with imidacloprid poses no risk to honeybees. This conclusion is confirmed by observations made in more than 10 field studies and several tunnel tests.
Two groups of eight honey bee colonies were fed with two different concentrations of imidacloprid in saccharose syrup during summer (each colony was given 1 litre of saccharose syrup containing 0.5 microg litre(-1) or 5 microg litre(-1) of imidacloprid on 13 occasions). Their development and survival were followed in parallel with control hives (unfed or fed with saccharose syrup) until the end of the following winter. The parameters followed were: adult bee activity (number of bee entering the hive and pollen carrying activity), adult bee population level, capped brood area, frequency of parasitic and other diseases, mortality, number of frames with brood after wintering and a global score of colonies after wintering. The only parameters linked to feeding with imidacloprid-supplemented saccharose syrup when compared with feeding with non-supplemented syrup were: a statistically non-significant higher activity index of adult bees, a significantly higher frequency of pollen carrying during the feeding period and a larger number of capped brood cells. When imidacloprid was no longer applied, activity and pollen carrying were re-established at a similar level for all groups. Repeated feeding with syrup supplemented with imidacloprid did not provoke any immediate or any delayed mortality before, during or following the next winter, whereas such severe effects are described by several French bee keepers as a consequence of imidacloprid use for seed dressing in neighbouring cultures. In any case, during the whole study, mortality was very low in all groups, with no difference between imidacloprid-fed and control colonies. Further research should now address several hypotheses: the troubles described by bee keepers have causes other than imidacloprid; if such troubles are really due to this insecticide, they may only be observed either when bees consume contaminated pollen, when no other sources of food are available, in the presence of synergic factors (that still need to be identified), with some particular races of bees or when colonies are not strong and healthy.
We conducted a long-term investigation to ascertain effects on honey bee, Apis mellifera L., colonies during and after exposure to flowering canola, Brassica napus variety Hyola 420, grown from clothianidin-treated seed. Colonies were placed in the middle of 1-ha clothianidin seed-treated or control canola fields for 3 wk during bloom, and thereafter they were moved to a fall apiary. There were four treated and four control fields, and four colonies per field, giving 32 colonies total. Bee mortality, worker longevity, and brood development were regularly assessed in each colony for 130 d from initial exposure to canola. Samples of honey, beeswax, pollen, and nectar were regularly collected for 130 d, and the samples were analyzed for clothianidin residues by using high-performance liquid chromatography with tandem mass spectrometry detection. Overall, no differences in bee mortality, worker longevity, or brood development occurred between control and treatment groups throughout the study. Weight gains of and honey yields from colonies in treated fields were not significantly different from those in control fields. Although clothianidin residues were detected in honey, nectar, and pollen from colonies in clothianidin-treated fields, maximum concentrations detected were 8- to 22-fold below the reported no observable adverse effects concentration. Clothianidin residues were not detected in any beeswax sample. Assessment of overwintered colonies in spring found no differences in those originally exposed to treated or control canola. The results show that honey bee colonies will, in the long-term, be unaffected by exposure to clothianidin seed-treated canola.
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