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Bees and pesticide regulation: Lessons from the neonicotinoid experience
Abstract
Neonicotinoid insecticides have been signaled as an important driver of widespread declines in bee diversity and abundance. Neonicotinoids were registered in the 1990s and by 2010 accounted for one third of the global insecticide market. Following a moratorium in 2013, their use on open-field crops was completely banned in the EU in 2018. Pesticide regulation should be based on solid and updated scientific evidence, whereby products showing unacceptable effects on the environment are not approved. Clearly, pesticide regulation failed to detect the ecological threats posed by neonicotinoids. We argue that at the time neonicotinoids were authorized, risk assessment (RA) protocols were inadequate to detect some of the risks associated with neonicotinoid properties, including high efficacy, long persistence, high systemicity, high mobility, and application versatility. We advocate for the adoption of a more holistic RA approach that should account for: a) temporal and spatial dimensions of pesticide exposure; b) co-exposure to multiple compounds; c) differences among bee species with different life histories in levels of exposure and sensitivity; and d) sublethal effects (mostly ignored in current RA procedures). We also argue that regulatory studies conducted to support pesticide registration should be publicly available, and that pesticide regulation should not be discontinued once a product has been authorized. We should use the knowledge acquired through the neonicotinoid experience as an opportunity to profoundly revise bee RA schemes. These efforts should be initiated promptly; the neonicotinoid story has also taught us that the regulatory system is reluctant to react.
... Although these declines have multiple causes, the use of pesticides is considered one of the major contributing factors Sánchez-Bayo and Wyckhuys, 2019). Prior to their approval for commercial use, pesticides undergo a risk assessment process to ensure their use will not pose a threat to non-target organisms, including bees (Sgolastra et al., 2020). Bee risk assessment follows a tiered approach, progressing from simpler assessments in the laboratory (tier 1), to more realistic assessments in semi-field and field (higher tier) conditions. ...
... Bee risk assessment follows a tiered approach, progressing from simpler assessments in the laboratory (tier 1), to more realistic assessments in semi-field and field (higher tier) conditions. When laboratory tests, conducted under worst-case exposure conditions, indicate a high potential risk, higher tier experiments are conducted (Sgolastra et al., 2020). ...
... Pesticide regulation is an essential component of pollinator protection programs. However, pesticide risk assessment schemes have some limitations and, therefore, are permanently being revised to increase the level of protection (EFSA, 2013;Sgolastra et al., 2020). One of these limitations is an insufficient coverage of chronic exposure. ...
... Despite being vital to life on our planet, compelling evidence from both past and present studies indicates that INPOs are becoming less common in agricultural habitats [3,10]. Apart from a multitude of factors such as exotic invasive species and infections that contribute to their demise or decline [11,12], agrochemicals (Table 1) have also been linked to the decline of INPOs [7,9,13,14]. Increased agrochemical inputs decrease the effectiveness of INPO communities in providing ecological services [10,15,16]. ...
... This is because most, if not all, INPOs are very sensitive to exposure to various agrochemicals [7,13,17]. These agrochemicals cover a broad spectrum of chemical agents meant to improve productivity [6,14,18] (Table 1); nevertheless, they are impairing and threatening the INPOs biodiversity community. ...
... Their potential to induce flower abscission can cause the dwindling of INPOs' food resources. [3,13,14] INPOs such as bees, hoverflies, and butterflies could be threatened by the increasing use of harmful agrochemicals (Table 2), such as neonicotinoid pesticides [3,27], which have an adverse impact on non-target species [7,8,10,28]. They can be exposed to agrochemicals in different ways: through air particles, eating contaminated food (nectar or pollen), and consuming contaminated water [4,10,29]. ...
The extensive application of agrochemicals in agricultural habitats in the Southern Highlands of Tanzania (SHOT) is supposed to negatively impact the biodiversity community of insect–pollinators (INPOs). However, in light of existing knowledge, there are no studies to back up this claim. We carried out field surveys in the SHOT to assess and characterize the INPO biodiversity community in agricultural habitats and compare it with protected habitats. Direct observations, transect counts, sweep netting, and pan trap techniques were used for sampling the INPOs. Overall, the INPOs’ relative abundance (57.14%) and species diversity index in protected habitats were significantly higher compared to agricultural habitats. Similarly, we recorded a higher number of plant–INPO interactions in protected habitats than agricultural habitats. Our results suggest that, in contrast to protected habitats, agrochemicals might have driven out or discouraged INPOs from agricultural habitats, resulting in dwindling species richness, diversity, and abundance. This could be due to agrochemical contamination that impairs the quantity and quality of floral resources (nectar and pollen) required by INPOs. Alternatively, protected habitats seemed healthy and devoid of agrochemical contamination, which attracted many INPOs for foraging and nesting. Thus, in order to maintain healthy agricultural habitats and support INPO biodiversity, conservation agriculture is imperative.
... Cependant, les insectes pollinisateurs des cultures et des plantes sauvages sont menacés à l'échelle mondiale et leur déclin ou perte pourrait avoir des désavantages économiques et environnementaux [3,4,2].Parmi ces menaces figurent les pesticides surtout ceux de la famille chimique des néonicotinoïdes menaçant ainsi la sécurité alimentaire. Effectivement, les insecticides néonicotinoïdes ont été signalés comme un facteur important du déclin généralisé de la diversité et de l'abondance des pollinisateurs (abeilles) [5,6]. Ainsi, leur utilisation sur les cultures de plein champ a été complètement interdite dans l'UE en 2018 [6]. ...
... Effectivement, les insecticides néonicotinoïdes ont été signalés comme un facteur important du déclin généralisé de la diversité et de l'abondance des pollinisateurs (abeilles) [5,6]. Ainsi, leur utilisation sur les cultures de plein champ a été complètement interdite dans l'UE en 2018 [6]. Au niveau algérien, dans l'index phytosanitaire de 2015 [7] figure quatre substances actives (SA) appartenant aux néonicotinoïdes : l'Acétamipride, l'Imidaclopride, le Thiaclopride et le Thiaméthoxame, entrant dans la composition de 50 formulations commerciales insecticides [8]. ...
... Les néonicotinoïdes (chloronicotinyles) sont parmi les insecticides les plus efficaces pour le contrôle des insectes suceurs tels que les pucerons et les aleurodes [13].Dans son étude, Bettiche (2017) [12]a trouvé que pour lutter contre ces derniers ravageurs, quelques agriculteurs procédaient,parfois, à des mélanges d'« Acétamipride/acétamipride » correspondant à 2 différentes formulations commerciales qui sont « Mospilate/Vapcomor ».Selon Goulson, (2013) [14], Les insecticides à base de néonicotinoïdes sont les insecticides les plus vendus dans le monde et représentaient en 2010 un tiers du marché mondial des insecticides [6]. ...
La production agricole assurant la sécurité alimentaire dépend impérativement des pollinisateurs. Cependant, le risque du déclin de ces derniers à cause de l’usage des pesticides menace
la sécurité et la durabilité alimentaire et environnementale. Les néonicotinoïdes, classe chimique
d’insecticides bannies en Europe à cause de leur relation possible à ce déclin sont toujours autorisés
en Algérie. Le présent travail comporte 1) un volet enquête des substances actives (SA) rapportés
d’usage par les agriculteurs au Ziban, 2) l’étude des risques des SA néonicotinoides envers les
abeilles à travers l’usage de la Pesticides Properties DataBase (PPDB). Le thiaméthoxame semble la
SA la plus toxique pour les abeilles, suivi par l’imidaclopride, l’acétamipride et le thiaclopride. Les
néonicotinoïdes doivent donc être retirés de l’homologation algérienne et interdits d’importation.
Aussi, des observatoires, des réseaux et des programmes de recherche doivent être initiés pour
l’étude, le suivi et la préservation des pollinisateurs et de leurs milieux.
... Although neonicotinoids, such as 56 thiamethoxam, are efficient in controlling economically important crop pest populations, there has 57 been global concern about their harmful effects on pollinators due to their widespread use, persistence 58 and high systemicity, meaning that they are absorbed by the treated plant and translocated to all plant 59 organs, reaching nectar and pollen in flowers 24 . To address risks to bees, many countries have national 60 pesticide regulation, which requires studies from laboratory to field scales, using primarily the 61 honeybee Apis mellifera as a surrogate for thousands of bee species 25 . Given the diversity in life 62 history and physiology, growing evidence shows that there is a substantial interspecific variation in 63 pesticide susceptibilities, highlighting the need to (re)assess lethal doses and/or exposure routes of 64 the pesticide products that could have relevant impacts on non-Apis bees 25,26 , such as the tropical 65 social stingless bees 26,27 . ...
... To address risks to bees, many countries have national 60 pesticide regulation, which requires studies from laboratory to field scales, using primarily the 61 honeybee Apis mellifera as a surrogate for thousands of bee species 25 . Given the diversity in life 62 history and physiology, growing evidence shows that there is a substantial interspecific variation in 63 pesticide susceptibilities, highlighting the need to (re)assess lethal doses and/or exposure routes of 64 the pesticide products that could have relevant impacts on non-Apis bees 25,26 , such as the tropical 65 social stingless bees 26,27 . For instance, stingless bees may be threatened by pesticides that are harmless 66 to A. mellifera, as most species rely on symbiont microorganisms and their biomolecules to prevent 67 stored food from spoiling and to improve its nutritional/hormonal quality 28 , or even Melipona species 68 that depend on mud to build their nests 29 . ...
The integration of managed pollinators into agricultural systems represents a practical strategy for boosting crop production, optimising sustainable farming practices, and improving rural livelihoods. However, the use of managed bees to supplement the contribution of wild pollinators still faces challenges, such as over-reliance on pesticides in intensively managed agroecosystems. Here, we placed managed bee colonies on conventional farms to assess their impact on arabica coffee yield, quality and market value, while also to evaluate colony health in coffee fields treated with field rates of thiamethoxam based products. We show that supplementing farms with managed bees increased farmer income by enhancing coffee yield and beverage quality, which is rewarded by specialty coffee markets. Moreover, our field-based study reveals that, even when exposed to field-realistic levels of the neonicotinoid thiamethoxam, managed bee colonies exhibited no significant adverse effects on their health within coffee fields. Our results underline that pollination is a key input on intensively managed coffee farms, and that agricultural production and environmental conservation interact synergically to maximize profitability, which is fundamental to encourage farmers to be good stewards of their croplands by adopting nature-positive practice.
... These results are concerning as flupyradifurone can be used on bee-visited crops while they are in bloom. Our findings add to a growing body of evidence demonstrating that pesticide risk assessments do not sufficiently protect wild bees from the negative consequences of pesticide use (Nicholson et al., 2023;Raine and Rundlöf, 2024;Sgolastra et al., 2020;Siviter, Fisher et al., 2023). ...
... One current criticism of pesticide risk assessments is that sub-lethal effects on non-Apis bee behaviour or fecundity are rarely assessed in any detail due to a dearth of internationally standardized laboratorybased protocols for assessing sub-lethal impacts on bees (Fisher et al., 2023;Sgolastra et al., 2020;Siviter et al., 2023aSiviter et al., , 2023b. Novel insecticides such as flupyradifurone can have significant sub-lethal effects on social bees, influencing learning, foraging success, and flight at field realistic levels (Hesselbach et al., 2020;Siviter and Muth, 2022;Tan et al., 2017;Tong et al., 2019). ...
... Landscape transformation and agriculture intensification expose honey bees to an ever increasing number of pesticides that threaten their survival or affect their performance and consequently pollination (van der Sluijs and Vaage, 2016). For this reason, the evaluation of the effects of pesticides on non-target insect species, particularly those providing important ecosystem services like the honey bee Apis mellifera L., prior to their registration, is essential to avoid the impact of cycles of novel pesticide release and banning (Sgolastra et al., 2020). ...
... Moreover, our work demonstrates how a multifactorial approach to hazard assessment allows to study, in a realistic context, possible lethal effects and reveal unexpected sublethal effects that are worth of further investigation prior to authorization, so as to reduce the environmental risks related to the release and subsequent ban of novel pesticides (Sgolastra et al., 2020;Siviter et al., 2023). We suggest that the concept of inclusive and interactive effect of pesticides that we introduced here should be incorporated into risk assessment procedures of insecticides, further than the already largely used concept of exclusive effect. ...
... This has led to restrictions on neonicotinoid use in the European Union (Sgolastra et al., 2020). However, these restrictions, along with rising pest resistance to neonicotinoids (Bass et al., 2015), has increased the demand for alternative, novel pesticides for controlling insect pests (Brown et al., 2016). ...
... As such, sub-lethal effects and effects specific to other species are not encompassed by the current regulatory processes. Over the past 5-10 years neonicotinoids have become increasingly restricted (Sgolastra et al., 2020), in part due to the sub-lethal effects that were not captured when they were initially registered for use. Our results suggest that a risk assessment that does not systematically measure these sub-lethal effects is unlikely to appropriately determine the consequences that an insecticide will have on bumblebee populations and the pollination services they provide. ...
Novel insecticides are continuously being developed for application in response to increased legal restriction of previously developed insecticides and resistance in target insects. These novel insecticides, such as flupyradifurone (FPF), remain relatively untested on non‐target organisms, including bumblebees. Further, existing tests on honeybees tend to focus on adult mortality and thus sub‐lethal effects, such as impacts on reproductive output, are neglected, despite their importance for population‐level impacts.
To address if the novel insecticide FPF has sub‐lethal effects on bumblebee reproduction and behaviour, we established microcolonies and chronically exposed them to field‐realistic concentrations over a 14‐day period.
We found that exposure to FPF reduced the bumblebees' reproductive output in terms of the number of larvae produced and the mean mass of each larval instar. FPF‐treated bees also stored less sucrose and constructed fewer honeypots. However, adult bumblebee mortality was similar between control and FPF‐exposed microcolonies.
Our results show that field‐realistic FPF exposure leads to increased larval mortality and/or delayed larval development, as well as reduced nectar storage, without affecting adult mortality.
Policy implications. Insecticides that impair bumblebee reproduction can have long‐term population‐level consequences, even if adult bees do not experience increased mortality. Despite this fact, sub‐lethal effects, such as impacts on reproduction, are not mandatorily assessed within the regulatory process. Our findings highlight the importance of determining sub‐lethal effects of pesticides across developmental stages, as well as using pollinator species other than honeybees within the regulatory process.
... However, non-bee pollinators are poorly represented in current environmental risk assessment. Bee risk assessment schemes rely on a surrogate species, the western honey bee, Apis mellifera L., and are based on the calculation of the dose of pesticide that is lethal to 50% of the population (LD50) following acute exposure [28,29]. This approach does not account for potential sensitivity differences among bee species [30][31][32][33][34][35]. ...
... From the resulting curve, we obtained the 5% (HD5, as the lower limit of the distribution) hazardous dose, and calculated the 95% confidence intervals (CIs, 1000 interactions). Using the approach of Arena and Sgolastra [28], we calculated the sensitivity ratio (R) between A. mellifera and the other pollinator species: ...
Insects play an essential role as pollinators of wild flowers and crops. At the same time, pollinators in agricultural environments are commonly exposed to pesticides, compromising their survival and the provision of pollination services. Although pollinators include a wide range of species from several insect orders, information on pesticide sensitivity is mostly restricted to bees. In addition, the disparity of methodological procedures used for different insect groups hinders the comparison of toxicity data between bees and other pollinators. Dipterans are a highly diverse insect order that includes some important pollinators. Therefore, in this study, we assessed the sensitivity of two hoverflies (Sphaerophoria rueppellii, Eristalinus aeneus) and one tachinid fly (Exorista larvarum) to a neonicotinoid insecticide (Confidor®, imidacloprid) following a comparative approach. We adapted the standardized methodology of acute contact exposure in honey bees to build dose–response curves and calculate median lethal doses (LD50) for the three species. The methodology consisted in applying 1 µL of the test solution on the thorax of each insect. Sphaerophoria rueppelli was the most sensitive species (LD50 = 10.23 ng/insect), and E. aeneus (LD50 = 18,176 ng/insect) the least. We then compared our results with those available in the literature for other pollinator species using species sensitivity distribution (SSD). Based on the SSD curve, the 95th percentile of pollinator species would be protected by a safety factor of 100 times the Apis mellifera endpoint. Overall, dipterans were less sensitive to imidacloprid than most bee species. As opposed to most bee species, oviposition and fecundity of many dipteran species can be reliably assessed in the laboratory. We measured the number of eggs laid following exposure to different insecticide doses and assessed the potential trade-off between oviposition and survival through the sublethal sensitivity index (SSI). Exposure to imidacloprid had a significant effect on fecundity, and SSI values indicated that oviposition is a sensitive endpoint for the three dipteran species tested. Future studies should integrate this information related to population dynamics in simulation models for environmental risk assessment.
... Larvae of wild solitary bees can be exposed to pesticides mainly via the consumption of or contact with contaminated pollen provisions (Eeraerts et al., 2020;Sgolastra et al., 2020) or nesting material (i.e., mud, Fortuin et al., 2021). Risk assessment of pesticides on larval stages of bees is currently restricted to social honeybees and bumblebees, while risk assessment and standard protocols for solitary bee larvae are lacking (Sgolastra et al., 2020), although recommendations for such tests have recently been proposed (Eeraerts et al., 2020). ...
... Larvae of wild solitary bees can be exposed to pesticides mainly via the consumption of or contact with contaminated pollen provisions (Eeraerts et al., 2020;Sgolastra et al., 2020) or nesting material (i.e., mud, Fortuin et al., 2021). Risk assessment of pesticides on larval stages of bees is currently restricted to social honeybees and bumblebees, while risk assessment and standard protocols for solitary bee larvae are lacking (Sgolastra et al., 2020), although recommendations for such tests have recently been proposed (Eeraerts et al., 2020). Yet, solitary bees differ in life history and physiological traits from social bees, which may result in different routes and levels of exposure, as well as different sensitivity associated with distinct levels and pathways of metabolization of compounds and their detoxification (Arena and Sgolastra, 2014;Beadle et al., 2019;Sgolastra et al., 2019). ...
Floral resource loss and pesticide exposure are major threats to bees in intensively managed agroecosystems, but interactions among these drivers remain poorly understood. Altered composition and lowered diversity of pollen nutrition may reinforce negative pesticide impacts on bees. Here we investigated the development and survival of the solitary bee Osmia bicornis provisioned with three different pollen types, as well as a mixture of these types representing a higher pollen diversity. We exposed bees of each nutritional treatment to five pesticides at different concentrations in the laboratory. Two field-realistic concentrations of three nicotinic acetylcholine receptor (nAChR) modulating insecticides (thiacloprid, sulfoxaflor and flupyradifurone), as well as of two fungicides (azoxystrobin and tebuconazole) were examined. We further measured the expression of two detoxification genes (CYP9BU1, CYP9BU2) under exposure to thiacloprid across different nutrition treatments as a potential mechanistic pathway driving pesticide-nutrition interactions. We found that more diverse pollen nutrition reduced development time, enhanced pollen efficacy (cocoon weight divided by consumed pollen weight) and pollen consumption, and increased weight of O. bicornis after larval development (cocoon weight). Contrary to fungicides, high field-realistic concentrations of all three insecticides negatively affected O. bicornis by extending development times. Moreover, sulfoxaflor and flupyradifurone also reduced pollen efficacy and cocoon weight, and sulfoxaflor reduced pollen consumption and increased mortality. The expression of detoxification genes differed across pollen nutrition types, but was not enhanced after exposure to thiacloprid. Our findings highlight that lowered diversity of pollen nutrition and high field-realistic exposure to nAChR modulating insecticides negatively affected the development of O. bicornis, but we found no mitigation of negative pesticide impacts through increased pollen diversity. These results have important implications for risk assessment for bee pollinators, indicating that negative effects of nAChR modulating insecticides to developing solitary bees are currently underestimated.
... In our study, we adopted a holistic approach (Sgolastra et al., 2020), focusing not only on the potential adverse effects of the biopesticide on the individual but also on the social insect colony as a whole. The adoption of a holistic approach is a crucial step to conduct more realistic ecotoxicological studies on non-target beneficial social insects (Chapman, 2002;Sgolastra et al., 2020). ...
... In our study, we adopted a holistic approach (Sgolastra et al., 2020), focusing not only on the potential adverse effects of the biopesticide on the individual but also on the social insect colony as a whole. The adoption of a holistic approach is a crucial step to conduct more realistic ecotoxicological studies on non-target beneficial social insects (Chapman, 2002;Sgolastra et al., 2020). Thus, we used the small colonies of the Polistes dominula, a predatory paper wasp that serves as a natural enemy of agricultural pests (Southon et al., 2019;Brock et al., 2021) easy to maintain and manipulate under laboratory conditions (Starks and Turillazzi, 2006). ...
... However, food security concerns have been raised due to declining bee populations, as it negatively effects the pollination process, which directly affects food production Lu et al., 2023;Mitchell et al., 2017;Reilly et al., 2020). Synthetic chemical insecticides are among the most significant causes of bee population decline, especially the chemical group of neonicotinoids, which are used worldwide on various crops Dai et al., 2019;Leska et al., 2021;Mitchell et al., 2017;Sgolastra et al., 2020;Wueppenhorst et al., 2022). These insecticides are neurotoxic and affect the ability of colonies to survive, develop, behave and reproduce (Carneiro et al., 2022;Colin et al., 2020;Jacob et al., 2019). ...
... In bioassay 1, the LC50 was found to be below the recommended concentration for field use. The release and regulation of synthetic phytosanitary products must be reviewed, taking into account solid and up-to-date scientific evidence, so that products that have negative effects on the environment are not approved or are restricted for commercialization or use (Sgolastra et al., 2020). ...
Apis mellifera L. (Hymenoptera: Apidae) is fundamental in the production chain, ensuring food diversity through the ecosystem service of pollination. The aim of this work was to evaluate the impact of imidacloprid, orally, topically, and by contact, on A. mellifera workers and to verify the presence of this active ingredient in honey. Toxicity levels were verified by bioassays. In bioassay 1, the levels correspond to the percentages of 100, 10, 1, 0.1, and 0.01% of the recommended concentration for field application of the commercial product Nortox® (active ingredient imidacloprid), with which we obtained the mean lethal concentration (LC50) in 48 h for A. mellifera, determining the concentration ranges to be used in the subsequent bioassays. Bioassays 2 and 3 followed the guidelines of the Organization for Economic Cooperation and Development, which specify the LC50 (48 h). In bioassay 4, the LC50 (48 h) and the survival rate of bees for a period of 120 h were determined by contact with a surface contaminated with imidacloprid, and in bioassay 5, the interference of the insecticide with the flight behavior of bees was evaluated. Honey samples were collected in agroecological and conventional georeferenced apiaries and traces of the imidacloprid were detected by means of high-performance liquid chromatography (HPLC-UV) with extraction by SPE C18. Bee survival was directly affected by the concentration and exposure time, as well behavioral performance, demonstrating the residual effect of imidacloprid on A. mellifera workers. Honey samples from a conventional apiary showed detection above the maximum residue limits (MRL) allowed by the European Union (0.05 μg mL-1), but samples from other apiaries showed no traces of this insecticide. Imidacloprid affects the survival rate and behavior of Africanized A. mellifera and honey quality.
... Although neonicotinoids are positioned as a new generation of less dangerous insecticides, a lot of information has been accumulated about their negative effects, which affect both the regulations concerning their use and the requirements with regards to their levels in foods. Neonicotinoids have caused the recent worldwide crisis, with mass deaths of bees [3,4]. In this regard, three intensively produced neonicotinoids, imidacloprid, clothianidin, and thiamethoxam, have been banned in the EU for outdoor uses, though they are continuing to be applied in permanent greenhouses and for other agricultural needs [5]. ...
A highly sensitive lateral flow immunoassay (LFIA) for imidacloprid, a widely used neonicotinoid insecticide, has been developed. The LFIA realizes the indirect coupling of anti-imidacloprid antibodies and gold nanoparticle (GNP) labels directly in the course of the assay. For this purpose, the common GNPs conjugate with anti-imidacloprid antibodies and are changed into a combination of non-modified, anti-imidacloprid antibodies, and the GNPs conjugate with anti-species antibodies. The given approach provides the possibility of selecting independent concentrations of GNPs and anti-imidacloprid antibodies to obtain the influence of minimal imidacloprid concentrations in the samples on the formation of detected, labeled immune complexes. A comparative study of imidacloprid LFIAs with common and indirect antibody–label coupling was implemented. The second variant reduced the limit of detection (LOD) of imidacloprid 20 times, reaching 0.2 ng/mL and 0.002 ng/mL for visual and instrumental detection, respectively, thus surpassing the existing LFIAs for imidacloprid. The developed highly sensitive LFIA was tested for imidacloprid detection in freshly squeezed fruits and berries without any additional sample preparation. The imidacloprids revealed were in the range of 75–97% for grape, 75–85% for orange, and 86–97% for apple samples. The time of the testing was 15 min.
... Several anthropogenic factors threaten, and are causing the decline of bee populations in different parts of the world (Potts et al., 2010(Potts et al., , 2015Nieto et al., 2014;Goulson et al., 2015;Kopec and Burd, 2017;Lima et al., 2022;Toledo-Hernández et al., 2022), and the extensive use of agrochemicals is one of the most important among them Bernardes et al., 2022). The toxicity and danger of neonicotinoid insecticides to bees has been well-known from various studies conducted from the 1990s to the present (Mayer and Lunden, 1997;Decourtye and Devillers, 2010;Blacquière et al., 2012;Lima et al., 2016;Sgolastra et al., 2020;Paloschi et al., 2023). Knowledge regarding the lethal and sublethal effects of these pesticides on bees has led to several restrictions in Europe, starting with the ban in 2018 of the outdoor use of clothianidin, imidacloprid, and thiamethoxam (EC, 2018a, b, c). ...
... Prior to causing death, the pesticide can also cause sublethal effects, such as food aversion, shaking or aberrant behaviour (e.g. . The lethal versus sublethal distinction is very important, because the regulatory system is largely built upon an understanding of the lethal effects of pesticides (Sgolastra et al., 2020), with sublethal effects only more recently starting to be considered (Straub et al., 2020). Yet, sublethal effects can be equally, if not more important to bees (e.g. ...
Bees and pesticides is a topic which attracts a considerable amount of research and media attention. It is also an applied topic, with experimental results informing policy. Policy decisions have‐real world consequences for food production and need to be made using the best available evidence.
This article aims to be an entry point for the increasing number of researchers now studying the topic, who may not have worked with pesticides beforehand. We have assumed a general knowledge of bee ecology, but no knowledge of pesticides.
We build up the knowledge base throughout the article, introducing concepts one‐by‐one and building on those concepts to tackle the more complex ideas later in the article.
Synthesis and applications. Our article is a starting point for those entering bee and pesticide research, and can help introduce the complex concepts and terminology of the field. We point to some further reading and resources throughout and offer some advice on best practice within the field. We hope this will ultimately help new researchers to quickly design high‐quality experiments, which can better inform pesticide policy and usage.
... However, at this point, bees face a number of threats that could lead to their extinction. The use of pesticides, especially neonicotinoids, is one of the main threats to bees [1]. These chemicals can cause acute poisoning, affect the nervous system of bees, and disrupt their ability to navigate, feed, and reproduce [2]. ...
The man-made load on the environment and the decrease in biodiversity cause a direct negative environmental impact on the existence of honey bees and beekeeping products. The priority directions of the food industry are the use of high-quality environmentally friendly raw materials and the prevention of the ingress and formation of harmful substances in food products, including honey. This implies the need to develop methods for assessing the environmental safety of the studied raw materials and products. The purpose of this study was to implement a mathematical modeling method for studying the environmental safety of honey. Five types of honey were studied: Robinia, rapeseed, linden, buckwheat, and sunflower. Mathematical models were built according to the following parameters: total activity of β-emitting radionuclides; residues of levomycetin (chloramphenicol), nitrofuran (according to AOZ and AMOZ), metronidazole, and pesticides (according to hexachloran); and the content of water-insoluble substances (mechanical impurities) and heavy metals. On the basis of the obtained data and established quality criteria, calculation graphic models were built. Using algebraic methods, they derived new formulas for calculating quality coefficients. Multivariate analysis and programming methods were used to evaluate honey using mathematical modeling. The most and least ecologically dangerous contaminants and their share of influence for different types of honey were determined based on the complex of research on negative factors. The proposed mathematical models can be implemented for practical use in specialized laboratories as a tool for determining the environmental safety of honey of various botanical origins.
... The use of this class of pesticides is usually justified by the excellent results derived from the molecules in controlling pests, which directly or indirectly help protect crops and maintain high productivity [7]. Several factors contributed to the rapid success of NEOs, such as high efficacy and lower application doses, prolonged and systemic protection, facilitating the control of a wide spectrum of pests, and high application versatility [9]. ...
Pesticide use offers disease and pest control in plants assisting in preserving food, leading to enhanced productivity, and ensuring food availability reduced economic losses. Furthermore, pesticides also control vectors that cause human pathogenesis. Among the vast universe of pesticides, neonicotinoids (NEOs) represent 24% of the total insecticide market. Their use is justified by their great efficacy in controlling pests. However, many problems are also related to the extensive use of such substances, such as environmental contamination (water, soil, and air), the presence of residues in food, their persistence in the environment, and the harmful effects caused by their toxicity affecting non-target organisms, among others. Therefore, a literature review was conducted aiming multidisciplinary and contextualized point of view, to compile the most recent and relevant results of their use of NEOs in the agriculture and control of vector-borne diseases in tropical countries and the impacts on environmental and living beings, caused by the large scale use these substances. Our profound literature review evidence these substances have neurotoxic properties and potential bioaccumulation. Moreover, the excessive substances cause resistance in target pests, compromising their efficacy for pest control, and have been linked to the decline of pollinators, such as bees and butterflies. Understanding these problems is crucial for developing sustainable and environmentally friendly pest management practices, ensuring the protection of ecosystems, biodiversity, agricultural productivity, and public health.
... Uses of agrochemicals have been associated with a variety of impacts to beneficial organisms. Some insecticides like neonicotinoids have been found to have sublethal effects on pollinators that may include negatively affect their productivity, reproduction or behaviour (Sgolastra et al., 2020). In many cases, some chemicals have been banned due to their environmental consequences like sublethal effects, synergestic interaction with other chemicals or toxicity to some species (Mancini et al., 2019 ----13010 --------15030 1 0 1 0 Outgrower --------may have lethal effects on bees upon exposure, Nicholsona (2017) and Main et al. (2020) observed that herbicides may enhance the adverse effects on insecticides either additively or synergistically. ...
... Therefore, measures to mitigate pesticide risk for bees may not necessarily be useful for human health, and vice-versa. Our findings emphasize the need to change our approach to environmental toxicology assessment, moving from a traditional farm-centred view of pesticide applications to a landscape-scale view considering both pesticide translocation and persistence, as well as the foraging ranges of non-target-organisms (Focks, 2014;Sgolastra et al., 2020;Topping et al., 2020). To reach this aim, access to pesticide-use data at field scale is an essential policy measure (Mesnage et al., 2021). ...
Agricultural environments, including crop and non-crop areas, often provide important pollen and nectar resources for managed and wild bees. However, these resources may be contaminated with pesticides detrimental to bees and other non-target organisms, including humans. Differences in life-history traits among bee species influence food resource exploitation and pesticide exposure. This study assesses the potential of honey bees (Apis mellifera) and mason bees (Osmia), two bee species with highly contrasting functional traits, as biological indicators of pesticide exposure in 34 Italian agricultural farms. Pollen loads of both species were used to identify pollen species collected and to analyse multi-residue levels of pesticides. Pesticide risk indexes were calculated for honey bees, mason bees and humans. In mason bees, pesticide risk was not influenced by plant diversity. In agreement with their pollen preferences and short foraging ranges, mason bees collected a high proportion of pollen from flowers of the target crop. Conversely, pesticide risk decreased with increasing pollen diversity in honey bees. In agreement with their generalist foraging habits and long foraging ranges honey bees collected a greater diversity of pollen species and a lower proportion of target crop pollen. Although honey bees and mason bees showed similar toxic loads and pesticide composition, at a field scale pesticide risk of one species is not a good indicator of the risk to the other species. Our study confirms that bees in agricultural environments are pervasively exposed to multi-residue pesticide loads. Exposure is conditioned by specific bee traits but is also highly context-dependent.
... Ultimately, this information should be used to develop integrated pest management programs that provide both effective pest control and pollinator protection (Biddinger and Rajotte, 2015;Topping et al., 2021). Our findings also call for a rethinking of pesticide risk assessment, which should target not only single products but also combinations of products likely to co-occur in agricultural environments (Carnesecchi et al., 2019;Sgolastra et al., 2020;Topping et al., 2020). ...
... About 19% (58 samples) of the pollinator-friendly plants analyzed were contaminated with pyrethroids, 18% (55 samples) with neonicotinoids, and 2% (7 samples) with chlorpyrifos. The systemically acting neonicotinoids are particularly problematic, as they have many harmful effects on honeybees and wild bees (Fischer et al. 2014;Rundlöf et al. 2015) and the use of three neonicotinoid AIs (imidacloprid, thiamethoxam, clothianidin) on open-field crops was therefore completely banned in the EU in 2018 (Sgolastra et al. 2020). While the potential hazards of neonicotinoids for honeybees can be severe, wild bee species are expected to be even more at risk from this exposure (Nicholson et al. 2024). ...
The production of conventional ornamental plants is pesticide-intensive. We investigated whether pesticide active ingredients (AIs) are still present in ornamentals at the time of purchase and assessed their potential ecotoxicity to non-target organisms. We purchased 1000 pot plants and 237 cut flowers of different species from garden centers in Austria and Germany between 2011 and 2021 and analyzed them for up to 646 AIs. Ecotoxicological risks of AIs were assessed by calculating toxic loads for honeybees (Apis mellifera), earthworms (Eisenia fetida), birds (Passer domesticus), and mammals (Rattus norvegicus) based on the LD50 values of the detected AIs. Human health risks of AIs were assessed on the basis of the hazard statements of the Globally Harmonized System. Over the years, a total of 202 AIs were detected in pot plants and 128 AIs in cut flowers. Pesticide residues were found in 94% of pot plants and 97% of cut flowers, with cut flowers containing about twice as many AIs (11.0 ± 6.2 AIs) as pot plants (5.8 ± 4.0 AIs). Fungicides and insecticides were found most frequently. The ecotoxicity assessment showed that 47% of the AIs in pot plants and 63% of the AIs in cut flowers were moderately toxic to the considered non-target organisms. AIs found were mainly toxic to honeybees; their toxicity to earthworms, birds, and mammals was about 105 times lower. Remarkably, 39% of the plants labeled as “bee-friendly” contained AIs that were toxic to bees. More than 40% of pot plants and 72% of cut flowers contained AIs classified as harmful to human health. These results suggest that ornamental plants are vectors for potential pesticide exposure of consumers and non-target organisms in home gardens.
Supplementary Information
The online version contains supplementary material available at 10.1007/s11356-024-34363-x.
... Determining impact is more complicated when multiple active ingredients (a.i.) with fungicidal action are used in the same commercial product. These mixtures can lead to synergistic effects, which may not be observed when they are evaluated individually [8][9][10]. ...
The aim of this study was to evaluate whether alterations in food availability compromise the metabolic homeostasis of honey bees exposed to three fungicides alone or together. Ten honey bee colonies were used, with half receiving carbohydrate-protein supplementation for 15 weeks while another five colonies had their protein supply reduced with pollen traps. Subsequently, forager bees were collected and exposed by contact to 1 or 7 μg of bixafen, prothioconazole, or trifloxystrobin, either individually or in combination. After 48 h, bee abdomens without the intestine were used for the analysis of expression of antioxidant genes (SOD-1, CAT, and GPX-1), detoxification genes (GST-1 and CYP306A1), the storage protein gene vitellogenin, and immune system antimicrobial peptide genes (defensin-1, abaecin, hymenoptaecin, and apidaecin), through real-time PCR. All fungicide treatments induced changes in gene expression, with bixafen showing the most prominent upregulation. Exposure to 1 μg of each of the three pesticides resulted in upregulation of genes associated with detoxification and nutrition processes, and downregulation of immune system genes. When the three pesticides were combined at a dose of 7 μg each, there was a pronounced downregulation of all genes. Food availability in the colonies affected the impact of fungicides on the
expression of the studied genes in forager bees.
... Moreover, global declines of invertebrate abundance, caused in large part by agricultural intensification including pesticide use, may impact hummingbirds and other aerial insectivores indirectly by limiting prey availability (Goebel et al., 2024;Spiller & Dettmers, 2019;Wagner et al., 2021). Indeed, the persistence, accumulation, and effects of neonicotinoids and butenolides on wildlife have spurred calls to review environmental risk-assessment strategies broadly Morrissey et al., 2024;Rattner et al., 2024;Sgolastra et al., 2020;Tosi et al., 2021). Our findings are consistent with the need for more field-based environmental and toxicological data to adequately assess the risk of pesticide exposure and effects on wildlife (Morrissey et al., 2024;Siviter & Muth, 2020;Wagner et al., 2021). ...
After regulation of pesticides, determination of their persistence in the environment is an important indicator of effectiveness of these measures. We quantified concentrations of two types of systemic insecticides, neonicotinoids (imidacloprid, acetamiprid, clothianidin, thiacloprid, and thiamethoxam) and butenolides (flupyradifurone), in off‐crop nontarget media of hummingbird cloacal fluid, honey bee ( Apis mellifera ) nectar and honey, and wildflowers before and after regulation of imidacloprid on highbush blueberries in Canada in April 2021. We found that mean total pesticide load increased in hummingbird cloacal fluid, nectar, and flower samples following imidacloprid regulation. On average, we did not find evidence of a decrease in imidacloprid concentrations after regulation. However, there were some decreases, some increases, and other cases with no changes in imidacloprid levels depending on the specific media, time point of sampling, and site type. At the same time, we found an overall increase in flupyradifurone, acetamiprid, thiamethoxam, and thiacloprid but no change in clothianidin concentrations. In particular, flupyradifurone concentrations observed in biota sampled near agricultural areas increased twofold in honey bee nectar, sevenfold in hummingbird cloacal fluid, and eightfold in flowers after the 2021 imidacloprid regulation. The highest residue detected was flupyradifurone at 665 ng/mL (parts per billion [ppb]) in honey bee nectar. Mean total pesticide loads were highest in honey samples (84 ± 10 ppb), followed by nectar (56 ± 7 ppb), then hummingbird cloacal fluid (1.8 ± 0.5 ppb), and least, flowers (0.51 ± 0.06 ppb). Our results highlight that limited regulation of imidacloprid does not immediately reduce residue concentrations, while other systemic insecticides, possibly replacement compounds, concurrently increase in wildlife. Environ Toxicol Chem 2024;00:1–12. © 2024 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.
... Hence, there is a strong interest in studying the sublethal effects of pesticides. Unwanted, sublethal effects of pesticides on honey bees have led to the regulation and banning of certain chemicals (Sgolastra et al., 2020). However, in order to improve pesticide risk assessment, one major challenge is to increase the ecological relevance of toxicity tests by assessing low-dose effects in free-flying bees (Barascou et al., 2021). ...
Automatic monitoring devices placed at the entrances of honey bee hives have facilitated the detection of various sublethal effects related to pesticide exposure, such as homing failure and reduced flight activity. These devices have further demonstrated that different neurotoxic pesticide molecules produce similar sublethal impacts on flight activity. The detection of these effects was conducted a posteriori, following the recording of flight activity data. This study introduces a method using an artificial intelligence model, specifically a recurrent neural network, to detect the sublethal effects of pesticides in real-time based on honey bee flight activity. This model was trained on a flight activity dataset comprising 42,092 flight records from 1107 control and 1689 pesticide-exposed bees. The model was able to classify honey bees as healthy or pesticide-exposed based on the number of flights and minutes spent foraging per day. The model was the least accurate (68.46%) when only five days of records per bee were used for training. However, the highest classification accuracy of 99%, a Cohen Kappa of 0.9766, a precision of 0.99, a recall of 0.99, and an F1-score of 0.99 was achieved with the model trained on 25 days of activity data, signifying near-perfect classification ability. These results underscore the highly predictive performance of AI models for toxicovigilance and highlight the potential of our approach for real-time and cost-effective monitoring of risks due to exposure to neurotoxic pesticide in honey bee populations.
... Determining impact is more complicated when multiple active ingredients (a.i.) with fungicidal action are used in the same commercial product. These mixtures can lead to synergistic effects, which may not be observed when they are evaluated individually (Zubrod et al., 2019;Sgolastra et al., 2020;Schuhmann et al., 2022). ...
The aim of this study was to evaluate whether alterations in food availability compromise the metabolic homeostasis of honey bees exposed to three fungicides alone or together. Ten honey bee colonies were utilized, with half receiving energy-protein supplementation for 15 weeks while another five colonies had their protein supply reduced with pollen traps. Subsequently, forager bees were collected and exposed by contact to 1 or 7 µg of bixafen, prothioconazole, and trifloxystrobin, either individually or in combination. After 48 hours, abdomens without the intestine was used for the analysis of expression of antioxidant genes (SOD-1, CAT, and GPX-1), detoxification genes (GST-1 and CYP306A1), the storage protein gene vitellogenin, and immune system antimicrobial peptide genes (Defensin-1, Abaecin, Hymenoptaecin, and Apidaecin), through real-time PCR. All pesticide treatments induced changes in gene expression, with bixafen showing the most prominent upregulation. Exposure to 1 µg of each of the three pesticides resulted in upregulation of genes associated with detoxification and nutrition processes, and downregulation of immune system genes. When the three pesticides were combined at a dose of 7 µg each, there was a pronounced downregulation of all genes. Dietary supplementation led to a slight reduction in gene expression alterations provoked by the fungicides.
... We examined whether a commercial herbicide formulation was detrimental to predatory social wasps, focusing on the survival, behavior, physiology, and functional morphology of both adult and immature wasps. This holistic approach is recommended for conducting more realistic ecotoxicological studies on non-targeted beneficial insects (Sgolastra et al., 2020). We found that exposure to herbicides can be lethal to P. satan, depending on their concentration. ...
Herbicides have been intensively used for weed control, raising concerns about their potentially adverse effects on non-target organisms. Research on the effects of these common agrochemicals on beneficial insects and the ecosystem services they provide (e.g., predation and pollination) is scarce. Therefore, we tested whether a commercial formulation comprising a mixture of mesotrione and atrazine was detrimental to adult females and larvae of the Neotropical predatory social wasp Polistes satan, which is an effective natural enemy of crop pests. Wasps were individually fed syrups contaminated with different concentrations of the herbicide above and below the maximum label rate (MLR = 12 ml/L). Survival was assessed. The locomotor activity, immune response, and midgut morphology of adults as well as the immune response of the larvae were also studied. Herbicide concentrations far above the MLR (12, 40, and 100 times) caused adult mortality, whereas lower concentrations (0.5, 1, and 6 times) did not. Herbicide exposure at 0.5 to 12 times the MLR increased adult activity. Adult exposure at 0.1 or 0.5 times the MLR did not affect melanotic encapsulation of foreign bodies but led to changes in the morphology of the midgut epithelium and peritrophic matrix. In larvae, the ingestion of herbicide at 0.1 or 0.2 times the MLR (corresponding to 9.6 and 19.2 ng of herbicide per individual) did not cause mortality but decreased their melanization-encapsulation response. Increased locomotor activity in herbicide-exposed adults can affect their foraging activity. The altered midgut morphology of adults coupled with the decreased immune response in larvae caused by herbicide exposure at realistic concentrations can increase the susceptibility of wasps to infections. Therefore, herbicides are toxic to predatory wasps.
... Chemical pollution is a driver of biodiversity loss on a planetary scale and a major contributor to the declining ecological status of surface waters across the globe (1)(2)(3)(4)(5). Several adverse environmental effects have been directly associated with chemical pollution, such as the extreme decline in vultures in India (6,7) and the general decline in bee populations in the Western world (8). Chemical pollution also negatively affects humans, with an estimated cost of disease of €157 billion and $340 billion for the European Union and United States, respectively (9,10). ...
Environmental hazard assessments are reliant on toxicity data that cover multiple organism groups. Generating experimental toxicity data is, however, resource-intensive and time-consuming. Computational methods are fast and cost-efficient alternatives, but the low accuracy and narrow applicability domains have made their adaptation slow. Here, we present a AI-based model for predicting chemical toxicity. The model uses transformers to capture toxicity-specific features directly from the chemical structures and deep neural networks to predict effect concentrations. The model showed high predictive performance for all tested organism groups—algae, aquatic invertebrates and fish—and has, in comparison to commonly used QSAR methods, a larger applicability domain and a considerably lower error. When the model was trained on data with multiple effect concentrations (EC 50 /EC 10 ), the performance was further improved. We conclude that deep learning and transformers have the potential to markedly advance computational prediction of chemical toxicity.
... Economic thresholds may therefore differ from farm-to-farm making the use of blanket application recommendation inefficient in the management of insect pests on cocoa. Blanket application of insecticides using a calendar-based system has several negative consequences on the environment and biodiversity (Arcury et al. 2002;Zhang et al. 2018;Sgolastra et al. 2020). With increasing global concerns on the effect of pesticides on human health and biodiversity, there is a need to shift from calendar-based system approach to insect pest management to need-based systems. ...
... Cross-referencing revealed something of the potential impact of agrochemicals and suggests a study gap that would ideally be closed in Mediterranean regions. The purpose of closing this gap would be to understand the contribution of agrochemicals to a decline in IPAD in the region (individually and in combination), to clarify where the problem mainly lies in the lifecycle of the insects and to establish if some agrochemicals are safer to use than others (Goulson et al., 2015;Potts et al., 2016;Dharampal et al., 2019 andSgolastra et al., 2020;Ali et al., 2021;Keller et al., 2021;Tamburini et al., 2021). ...
There is a concern that Insect pollinator abundance and diversity is declining world-wide, threatening ecosystem function and hence human food security and wellbeing. This decline may be affecting Mediterranean climatic regions, which are sensitive hotspots of biodiversity. Mediterranean river valleys are areas which have been used for agriculture for thousands of years, and are often in a degraded ecological state. These riparian areas may be suffering a decline in pollinator diversity when they could be providing valuable opportunities for restoration and conservation. This thesis comprises two parts. The first part is a semi-structured literature review initiated with three questions: 1) What evidence is there that insect pollinator abundance and diversity is declining in Mediterranean regions? 2) What ecological restoration practices offer the most promise of reversing such declines? 3) What contribution might riparian zones make to reversing any decline? The second part is a case study characterising Hymenopteran and Coleopteran pollinators of the Sorraia river valley in Portugal; an example of a Mediterranean agricultural river valley. Though relatively few studies of pollinator abundance and diversity in Mediterranean regions were found, there is evidence suggesting there is a decline, mostly due to habitat loss, introduced species and climate change. The impact of agrochemicals hardly featured in the articles reviewed here, and represents one of the opportunities for future investigation. The Sorraia valley case study suggests a marginally higher level of pollinator diversity in riparian areas compared to the agricultural matrix. And that there is a complementary effect, with the riparian species increasing richness at the landscape level. Overall, there is strong evidence that riparian areas offer an important opportunity for restoration projects through protected area management, ecologically improved riparian woodland and concerted field margin management, improving pollinator diversity and pollination services in cultivated, Mediterranean river valleys.
Existe a preocupação de que a abundância e diversidade de polinizadores de insectos esteja a diminuir em todo o mundo, ameaçando o funcionamento do ecossistema e, consequentemente, a segurança alimentar e o bem-estar humano. Este declínio pode estar a afectar as regiões climáticas mediterrânicas, que são focos sensíveis de biodiversidade. Os vales fluviais mediterrânicos são áreas que têm sido utilizadas para a agricultura durante milhares de anos, estando frequentemente num estado ecológico degradado. Estas zonas ribeirinhas podem estar a sofrer um declínio na diversidade de polinizadores quando poderiam estar a proporcionar valiosas oportunidades de restauração e conservação. Esta tese é apresentada em duas partes. Na primeira parte faz-se uma revisão semi-estruturada da literatura iniciada com três questões: 1) Que provas existem de que a abundância e diversidade de polinizadores de insectos está a diminuir nas regiões mediterrânicas? 2) Que práticas de restauração ecológica oferecem a maior oportunidade de reverter tais declínios? 3) Que contribuição podem dar as zonas ribeirinhas para inverter qualquer declínio? A segunda parte é um estudo de caso que caracteriza os polinizadores Hymenoptera e Coleoptera do vale do rio Sorraia em Portugal; um exemplo de um vale de rio agrícola mediterrânico. Embora tenham sido encontrados relativamente poucos estudos sobre a abundância e diversidade de polinizadores nas regiões mediterrânicas, há provas que sugerem que existe um declínio, principalmente devido à perda de habitat, espécies introduzidas e alterações climáticas. O impacto negativo dos agroquímicos foi escassamente mencionado nos artigos aqui analisados, e representa uma das oportunidades para investigações futuras. O estudo de caso do vale do Sorraia sugere um nível marginalmente mais elevado de diversidade de polinizadores em zonas ribeirinhas, em comparação com a matriz agrícola. Este estudo sugere ainda um efeito complementar entre as infraestruturas ripícolas e a matriz agrícola, permitindo aumentar a riqueza a nível da paisagem. Globalmente, há fortes indícios de que as áreas ripícolas oferecem uma importante oportunidade para projetos de restauração através da gestão de áreas protegidas, melhoria das matas ripícolas ecologicamente, gestão de concertada das bordaduras nos campos agrícolas, melhorando a diversidade de polinizadores e o serviço de polinização nos vales mediterrânicos cultivados.
... The suggested use of an assessment or bridging factor of 10, to allow toxicological data from A. mellifera to be used in other species, as recommended by the European Chemical Agency in 2020, would also not reduce the risks to species such as M. rotundata to a safe level for certain insecticides (Ansell et al., 2021;Arena & Sgolastra, 2014;ECHA, 2020;Hayward et al., 2019;Pamminger, 2021). The suggestion that either B. terrestris or O. bicornis (or both) should be added as extra model species to the toxicity trials would also not give at risk Megachilidae taxa the protection they need (EFSA, 2013;Sgolastra et al., 2019Sgolastra et al., , 2020Uhl et al., 2019). ...
Recent work has demonstrated that many bee species have specific cytochrome P450 enzymes (P450s) that can efficiently detoxify certain insecticides. The presence of these P450s, belonging or closely related to the CYP9Q subfamily (CYP9Q‐related), is generally well conserved across the diversity of bees. However, the alfalfa leafcutter bee, Megachile rotundata, lacks CYP9Q‐related P450s and is 170–2500 times more sensitive to certain insecticides than bee pollinators with these P450s. The extent to which these findings apply to other Megachilidae bee species remains uncertain. To address this knowledge gap, we sequenced the transcriptomes of four Megachile species and leveraged the data obtained, in combination with publicly available genomic data, to investigate the evolution and function of P450s in the Megachilidae. Our analyses reveal that several Megachilidae species, belonging to the Lithurgini, Megachilini and Anthidini tribes, including all species of the Megachile genus investigated, lack CYP9Q‐related genes. In place of these genes Megachile species have evolved phylogenetically distinct CYP9 genes, the CYP9DM lineage. Functional expression of these P450s from M. rotundata reveal they lack the capacity to metabolize the neonicotinoid insecticides thiacloprid and imidacloprid. In contrast, species from the Osmiini and Dioxyini tribes of Megachilidae have CYP9Q‐related P450s belonging to the CYP9BU subfamily that are able to detoxify thiacloprid. These findings provide new insight into the evolution of P450s that act as key determinants of insecticide sensitivity in bees and have important applied implications for pesticide risk assessment.
... Finally, challenges in estimating the persistence of pesticides in the environment have caused insufficient estimations of exposure (Traynor et al. 2021 ). As a prime example, exposure to wind-blown dust from seeds coated with neonicotinoids was not predicted to be a major route of exposure when these pesticides were approved (Sgolastra et al. 2020, Greatti et al. 2003 ). ...
Over decades, pesticide regulations have cycled between approval and implementation, followed by the discovery of negative effects on nontarget organisms that result in new regulations, pesticides, and harmful effects. This relentless pattern undermines the capacity to protect the environment from pesticide hazards and frustrates end users that need pest management tools. Wild pollinating insects are in decline, and managed pollinators such as honey bees are experiencing excessive losses, which threatens sustainable food security and ecosystem function. An increasing number of studies demonstrate the negative effects of field-realistic exposure to pesticides on pollinator health and fitness, which contribute to pollinator declines. Current pesticide approval processes, although they are superior to past practices, clearly continue to fail to protect pollinator health. In the present article, we provide a conceptual framework to reform cyclical pesticide approval processes and better protect pollinators.
... Extrapolating from our results requires caution. Bee species have frequently been shown to differ in sensitivity to pesticides [82][83][84][85] , and consequently in experiencing sub-lethal effects 47 . For example, Boff et al. 85 found that Osmia bicornis exposed to field-realistic doses of sulfoxaflor showed changes in foraging behaviour, including the number of flower visits and flight performance, suggesting that impacts of this agrochemical on pollination services supplied by different bee species may vary. ...
Many pollinators, including bumble bees, are in decline. Such declines are known to be driven by a number of interacting factors. Decreases in bee populations may also negatively impact the key ecosystem service, pollination, that they provide. Pesticides and parasites are often cited as two of the drivers of bee declines, particularly as they have previously been found to interact with one another to the detriment of bee health. Here we test the effects of an insecticide, sulfoxaflor, and a highly prevalent bumble bee parasite, Crithidia bombi, on the bumble bee Bombus terrestris. After exposing colonies to realistic doses of either sulfoxaflor and/or Crithidia bombi in a fully crossed experiment, colonies were allowed to forage on field beans in outdoor exclusion cages. Foraging performance was monitored, and the impacts on fruit set were recorded. We found no effect of either stressor, or their interaction, on the pollination services they provide to field beans, either at an individual level or a whole colony level. Further, there was no impact of any treatment, in any metric, on colony development. Our results contrast with prior findings that similar insecticides (neonicotinoids) impact pollination services, and that sulfoxaflor impacts colony development, potentially suggesting that sulfoxaflor is a less harmful compound to bee health than neonicotinoids insecticides.
... In contrast, the EU operates under the precautionary principle, whereby the regulatory environment assumes that pesticides could have uncertain or undesirable externalities and proactively regulates their usage (Ollinger et al., 1998;Suryanarayanan, 2015;Donley, 2019;Kudsk and Mathiassen, 2020). Consequently, pesticide regulations in Europe, especially for neonicotinoids, are more stringent, with most of their uses being banned within the EU (EC, 2009a(EC, , 2013(EC, , 2020Dewar, 2019;Sgolastra et al., 2020;Demortain, 2021). In addition, the EU has undertaken centrally-coordinated research to determine the implications of neonicotinoid insecticide use on pollinators, whereas in the US, collaborations among agencies remain limited and fragmented. ...
The alarming decline of pollinator populations has raised significant concerns worldwide and prompted the need for effective pesticide risk assessment within the Integrated Pest and Pollinator Management (IPPM) framework. This paper examines the diverse approaches to pollinator protection within the pesticide regulatory environments of the United States (US), the European Union (EU), and selected Asian countries. The US adopts a reactive approach, regulating pesticides only after evidence of harm emerges, while the EU embraces a proactive stance under the precautionary principle. The EU has implemented stringent regulations, including neonicotinoid bans, and conducts coordinated research on pesticide impacts. In contrast, some Asian countries face challenges with inadequate regulations, leading to adverse health and environmental consequences. This article highlights the need for comprehensive pesticide regulations across different regions to safeguard pollinators and mitigate the non-target risks associated with pesticide use.
... The use of insecticides has also severely harmed insect assemblages. For example, some of the most widely used insecticides are compounds of the neonicotinoid group (Sgolastra et al., 2020), which interfere with the nervous system of insects. In many cases, these pesticides are applied directly to seeds (i.e., seed coating), making not only them but the entire plant toxic to insects and even persisting and affecting other insects of the food chain (Calvo-Agudo et al., 2019;Rundlöf et al., 2015. ...
Globalization is accelerating the intentional and unintentional introductions of species beyond their natural biogeographic boundaries. Of all introduced species, only a small proportion become invasive, causing a wide variety of negative impacts. Some of them have detrimental consequences for native insects. In this chapter, which serves as an introduction to this book, we discuss the role of biological invasions as a driver of the current global decline in insect diversity, as well as the importance of considering biological invasions when planning insect conservation actions.
... From the recognized gaps, differences in pesticide sensitivities, exposure levels (e.g., nectar and pollen consumption), and exposure routes among bee species have been reported as some of the most important limitations on the current risk assessment of pesticides to pollinators in the world (Assis et al., 2022;Sgolastra et al., 2020;Topping et al., 2021). In the present study, we calculated the LC50 (medium lethal concentration) and LD50 values of dimethoate for males and females of the Neotropical solitary bee Centris analis (Fabricius, 1804) as the first step to gather more information regarding pesticide effects on solitary bees, hence helping to improve risk assessment conducted in tropical countries. ...
Currently, only Apis mellifera species is used in environmental regulation to evaluate the hazard of pesticides to pollinators. The low representativeness of pollinators and bee diversity in this approach may result in insufficient protection for the wild species. This scenario is intensified in tropical environments, where little is known about the effects of pesticides on solitary bees. Here, we aimed to calculate the medium lethal dose (LD50 ) and medium lethal concentration (LC50 ) of the insecticide dimethoate in the Neotropical solitary bee Centris analis, a cavity-nesting oil-collecting bee distributed from Brazil to Mexico. Males and females of C. analis were exposed orally to dimethoate for 48 hours under laboratory conditions. The lethality was assessed every 24 hours until 144 hours after the beginning of the test. After the LD50 calculation, we compared the value with available LD50 in the literature of other bee species using the species sensitivity distribution curve. In 48 hours of exposure, the males showed an LD50 value 1.33 times lower than females (32.78 and 43.84 ng a.i./bee, respectively). C. analis was more sensitive to dimethoate than the model species A. mellifera and the solitary bee from temperate zones, Osmia lignaria. However, on a body weight basis, C. analis and A. mellifera had similar LD50 values. This is the first study that calculated an LD50 for a Neotropical solitary bee. Besides, the results presented here are of crucial importance for a better understanding of the effects of pesticides on the tropical bee fauna and will help to improve the risk assessment of pesticides to bees under tropical conditions, giving attention to wild species, which is commonly neglected.
... More studies are necessary if a global assessment of the effects of pesticides on sexual communication and reproduction is to be obtained for bees. The inclusion of reproductive aspects, including mating behavior and chemical communication, is required as a further step (Sgolastra et al., 2020) during pesticide risk assessment in (wild) bees. ...
The aboveground oligolectic bee, Heriades truncorum, is a particularly good model for studying the impact of pesticides on sexual communication, since some aspects of its mating behavior have previously been described. We have tested (1) the interference of the pesticide flupyradifurone on male precopulatory behavior and male mating partner preferences, (2) the way that the pesticide interferes in male quality assessment by the female , and (3) the effects of the pesticide on the chemical compounds in the female cuticle. We exposed bees of both sexes to a sublethal concentration of flupyradifurone. Various behaviors were registered in a mating arena with two females (one unexposed and one exposed) and one male (either unexposed or exposed). Unexposed males were quicker to attempt to mate. Treatment also impacted precopulatory behavior and male quality assessment by females. Males approached unexposed females more quickly than insecticide-exposed ones. Females exposed to insecticide produced lower amounts of some cuticular hydrocarbons (sex pheromone candidates) and appeared less choosy than unexposed females. Our findings suggest that insecticide exposure affects sexual communication, playing a role both in male preference and in male quality assessment by the female.
... Toxics 2023, 11, x FOR PEER REVIEW 3 of 17 In recent years, there has been increasing concerns over extensive environmental threats of NEO insecticides [17]. These substances were discovered in the 1980s, and in the early 1990s, the first commercial compound, imidacloprid, was made available. ...
Recently, neonicotinoids have become the fastest-growing class of insecticides in conventional crop protection, with extensive usage against a wide range of sucking and chewing pests. Neonicotinoids are widely used due to their high toxicity to invertebrates, simplicity, flexibility with which they may be applied, and lengthy persistence, and their systemic nature ensures that they spread to all sections of the target crop. However, these properties raise the risk of environmental contaminations and potential toxicity to non-target organisms. Acetamiprid is a new generation insecticide, which is a safer alternative for controlling insect pests because of its low toxicity to honeybees. Acetamiprid is intended to target nicotinic acetylcholine receptors in insects, but its widespread usage has resulted in negative impacts on non-target animals such as mammals. This review summarizes in vivo and in vitro animal studies that investigated the toxicity of specific neonicotinoids. With summarized data, it can be presumed that certain concentrations of neonicotinoids in the reproductive system cause oxidative stress in the testis; spermatogenesis disruption; spermatozoa degradation; interruptions to endocrine function and Sertoli and Leydig cell function. In the female reproductive system, acetamiprid evokes pathomorphological alterations in follicles, along with metabolic changes in the ovaries.
Neonicotinoids were synthesized as a safer substitute for conventional pesticides, namely organophosphorus and carbamate in the 1990s. However, concerns about their environmental effects soon emerged due to their high toxicity, persistence, and mobility. In addition, their harmful effects on non-target organisms, such as pollinators, aquatic insects, and birds were also identified. Due to their systemic nature, they were found to impact tissues of plants like pollen and nectar on which non-target organisms feed. Their extended half-lives, high solubility, and lack of volatility have impacted the environment. Neonicotinoids were also found to affect birds, insects, and humans, causing disorders like Alzheimer’s, Parkinson’s, schizophrenia, and depression. Neonicotinoids which are effective against sucking insects, are authorized in over 120 countries, with 90% used as seed treatments. However, research indicates that seed coatings are not essential or cost-effective, and their widespread use is driven by the limited availability of uncoated seed. These insecticides have been found to cause a decline in bee population and affect immune function in honeybees, leading to calls for tighter controls. Some countries such as the USA, EU nations, and Canada have imposed bans or tightened regulations on neonicotinoids. To mitigate risks, regulatory authorities have implemented measures like imposing residue limits, bans, and altered application protocols. However, such tighter regulations are lacking among developing countries such as India, South Africa, Thailand, Zimbabwe, Paraguay, Israel, France, El Salvador, and Ecuador. Ecological farming principles and applying them only when necessary can reduce insecticide use, making seed coatings not essential. Alternative strategies like physical inhibition, crop rotation, and biological control can reduce dependency on neonicotinoids. Current studies on environmental dangers, long-term tracking, and education initiatives can help make informed decisions and promote sustainable pesticide usage. Integrated Pest Management programs, research, community outreach, and coordination among stakeholders are much needed to reduce their widespread consumption. Hence, the balance between agricultural yields and ecological responsibility is crucial for long-term sustainability. In this chapter, the history, mode of action, toxicity issues pertaining to non-target organisms, and current regulatory status of neonicotinoids in the world have been discussed.
The study conducted in the state of Colima, western Mexico, aimed to assess the 1) occurrence, 2) temporal variability, 3) spatial variability, and 4) potential risk for honeybees and human consumption of pesticide-contaminated honey. For that purpose, 48 pesticides were determined in bees and their honey during both dry and wet seasons. The research considered two variables: land use categorization (irrigated agriculture, rainfed agriculture, grassland, and forest area) and location (coastal, valley, and mountain). Bee and honey samples were collected, pre-treated using solid-phase extraction (SPE), and analyzed using LC-MS/MS and GC–MS techniques. Occurrence: of the total number of pesticides, 17 were detected in the bee samples and 12 in the honey samples. The pesticides with the highest concentrations in the bee samples were glufosinate ammonium, picloram, and permethrin, while in the honey samples, picloram, permethrin, and atrazine were the most prevalent. Temporal variability: analyses revealed significant differences between dry and wet seasons for glufosinate ammonium and DEET in bee samples and only for glufosinate ammonium in honey samples. Spatial variability: analyses showed a trend in the number of detected pesticides, with irrigated agriculture areas having the highest detection and grassland areas having the least. The human potential risk assessment of contaminated honey consumption indicated no risk. The bee’s potential risk for consumption of pesticides contaminated honey revealed chronic effects due to permethrin in a general scenario, and carbofuran, diazinon and permethrin in the worst scenario, and potential risk of acute effects by permethrin. The findings of this study contribute to understanding the contamination levels of pesticides in bees and their honey, emphasizing the importance of monitoring and mitigating the adverse effects of pesticide exposure on bee populations and environmental health.
Wild bees are important pollinators of crops and wildflowers but are exposed to a myriad of different anthropogenic stressors, such as pesticides and poor nutrition, as a consequence of intensive agriculture. These stressors do not act in isolation, but interact, and may exacerbate one another. Here, we assessed whether a field-realistic concentration of flupyradifurone, a novel pesticide that has been labelled as ‘bee safe’ by regulators, influenced bumblebee sucrose responsiveness and long-term memory. In a fully crossed experimental design, we exposed individual bumblebees (Bombus impatiens) to flupyradifurone at high (50% (w/w)) or low (15% (w/w)) sucrose concentrations, replicating diets that are either carbohydrate rich or poor, respectively. We found that flupyradifurone impaired sucrose responsiveness and long-term memory at both sucrose concentrations, indicating that better nutrition did not buffer the negative impact of flupyradifurone. We found no individual impact of sugar deficiency on bee behaviour and no significant interactions between pesticide exposure and poor nutrition. Our results add to a growing body of evidence demonstrating that flupyradifurone has significant negative impacts on pollinators, indicating that this pesticide is not ‘bee safe’. This suggests that agrochemical risk assessments are not protecting pollinators from the unintended consequences of pesticide use.
Mounting evidence supporting the negative impacts of exposure to neonicotinoids on bees has prompted the registration of novel ‘bee-friendly’ insecticides for agricultural use. Flupyradifurone (FPF) is a butenolide insecticide that shares the same mode of action as neonicotinoids and has been assessed to be ‘practically non-toxic to adult honeybees' using current risk assessment procedures. However, these assessments overlook some routes of exposure specific to wild bees, such as contact with residues in soil for ground-nesters. Co-exposure with other pesticides may also lead to detrimental synergistic effects. In a fully crossed experiment, we assessed the possible lethal and sublethal effects of chronic exposure to two pesticides used on Cucurbita crops, the insecticide Sivanto Prime (FPF) and the fungicide Quadris Top (azoxystrobin and difenoconazole), alone or combined, on solitary ground-nesting squash bees (Xenoglossa pruinosa). Squash bees exposed to Quadris Top collected less pollen per flower visit, while Sivanto-exposed bees produced larger offspring. Pesticide co-exposure induced hyperactivity in female squash bees relative to both the control and single pesticide exposure, and reduced the number of emerging offspring per nest compared to individual pesticide treatments. This study demonstrates that ‘low-toxicity’ pesticides can adversely affect squash bees under field-realistic exposure, alone or in combination.
Pesticide use is one of the main causes of pollinator declines in agricultural ecosystems. Traditionally, most laboratory studies on bee ecotoxicology test acute exposure to single compounds. However, under field conditions, bees are often chronically exposed to a variety of chemicals, with potential synergistic effects. We studied the effects of field-realistic concentrations of three pesticides measured in pollen and nectar of commercial melon fields on the solitary bee Osmia bicornis L. We orally exposed females of this species throughout their life span to 8 treatments combining two neonicotinoid insecticides (acetamiprid, imidacloprid) and a triazole fungicide (myclobutanil) via pollen and sugar syrup. We measured pollen and syrup consumption, longevity, ovary maturation and thermogenesis. Pesticide intake was three orders of magnitude higher via syrup than pollen. At the tested concentrations, no synergistic effects emerged, and we found no effects on longevity and ovary maturation. However, all treatments containing imidacloprid resulted in suppressed syrup consumption and drastic decreases in thoracic temperature and bee activity. Our results have important implications for pesticide regulation. If we had measured only lethal effects we would have wrongly concluded that the pesticide combinations containing imidacloprid were safe to O. bicornis. The incorporation of tests specifically intended to detect sublethal effects in bee risk assessment schemes should be an urgent priority. In this way, the effects of pesticide exposure on the dynamics of bee populations in agroecosystems will be better assessed. Bees, both wild and managed, play an essential role in crop pollination and food production stability 1-3. Yet, especially in intensively farmed areas, bee populations often face adverse environmental conditions, including destruction of nesting habitats, scarcity of floral resources and intensive pesticide presence 4-7 .
Using the hoary squash bee (Peponapis pruinosa) as a model, we provide the first probabilistic risk assessment of exposure to systemic insecticides in soil for ground-nesting bees. To assess risk in acute and chronic exposure scenarios in Cucurbita and field crops, concentrations of clothianidin, thiamethoxam and imidacloprid (neonicotinoids) and chlorantraniliprole (anthranilic diamide) in cropped soil were plotted to produce an environmental exposure distribution for each insecticide. The probability of exceedance of several exposure endpoints (LC50s) was compared to an acceptable risk threshold (5%). In Cucurbita crops, under acute exposure, risk to hoary squash bees was below 5% for honey bee LC50s for all residues evaluated but exceeded 5% for clothianidin and imidacloprid using a solitary bee LC50. For Cucurbita crops in the chronic exposure scenario, exposure risks for clothianidin and imidacloprid exceeded 5% for all endpoints, and exposure risk for chlorantraniliprole was below 5% for all endpoints. In field crops, risk to ground-nesting bees was high from clothianidin in all exposure scenarios and high for thiamethoxam and imidacloprid under chronic exposure scenarios. Risk assessments for ground-nesting bees should include exposure impacts from pesticides in soil and could use the hoary squash bee as an ecotoxicology model.
The honeybee (Apis mellifera L.) is an important pollinator and a model for pesticide effects on insect pollinators. The effects of agricultural pesticides on honeybee health have therefore raised concern. Bees can be exposed to multiple pesticides that may interact synergistically, amplifying their side effects. Attention has focused on neonicotinoid pesticides, but flupyradifurone (FPF) is a novel butenolide insecticide that is also systemic and a nicotinic acetylcholine receptor (nAChR) agonist. We therefore tested the
lethal and sublethal toxic effects of FPF over different seasons and worker types, and the interaction of FPF with a common SBI fungicide, propiconazole. We provide the first demonstration of adverse synergistic effects on bee survival and behaviour (poor coordination, hyperactivity, apathy) even at FPF field-realistic doses (worst-case scenarios). Pesticide effects were significantly influenced by worker type and season. Foragers were consistently more susceptible to the pesticides (4-fold greater effect) than in-hive bees, and both worker types were more strongly affected by FPF in summer as compared with spring. Because risk assessment (RA) requires relatively limited tests that only marginally address bee behaviour and do not consider
the influence of bee age and season, our results raise concerns about the safety of approved pesticides, including FPF. We suggest that pesticide RA also test for common chemical mixture synergies on behaviour and survival.
The relationship between pesticides and pollinators, while attracting no shortage of attention from scientists, regulators, and the public, has proven resistant to scientific synthesis and fractious in matters of policy and public opinion. This is in part because the issue has been approached in a compartmentalized and intradisciplinary way, such that evaluations of organismal pesticide effects remain largely disjoint from their upstream drivers and downstream consequences. Here, we present a socioecological framework designed to synthesize the pesticide-pollinator system and inform future scholarship and action. Our framework consists of three interlocking domains-pesticide use, pesticide exposure, and pesticide effects–each consisting of causally linked patterns, processes, and states. We elaborate each of these domains and their linkages, reviewing relevant literature and providing empirical case studies. We then propose guidelines for future pesticide-pollinator scholarship and action agenda aimed at strengthening knowledge in neglected domains and integrating knowledge across domains to provide decision support for stakeholders and policymakers. Specifically, we emphasize (1) stakeholder engagement, (2) mechanistic study of pesticide exposure, (3) understanding the propagation of pesticide effects across levels of organization, and (4) full-cost accounting of the externalities of pesticide use and regulation. Addressing these items will require transdisciplinary collaborations within and beyond the scientific community, including the expertise of farmers, agrochemical developers, and policymakers in an extended peer community.
Ancestral history matters
Biodiversity is sometimes quantified purely by the number of species within a system that allow it to function to produce ecosystem services. Grab et al. show that simple species counting is too simplistic. They combined remotely sensed land-cover analyses and crop production records with an extensive 10-year pollinator community survey and a complete species-level phylogeny generated using genome-wide phylogenomic methods. They found that the equivalent of millions of years of pollinator evolution were lost in highly altered agricultural environments, which decreased pollination services above and beyond what would be expected from a simple numerical species count.
Science , this issue p. 282
Current pesticide risk assessment for bees relies on a single (social) species, the western honey bee, Apis mellifera L. (Hymenoptera: Apidae). However, most of the >20,000 bee species worldwide are solitary. Differences in life history traits between solitary bees (SB) and honey bees (HB) are likely to determine differences in routes and levels of pesticide exposure. The objectives of this review are to: 1) compare SB and HB life history traits relevant for risk assessment; 2) summarize current knowledge about levels of pesticide exposure for SB and HB; 3) identify knowledge gaps and research needs; 4) evaluate whether current HB risk assessment schemes cover routes and levels of exposure of SB; and 5) identify potential SB model species for risk assessment. Most SB exposure routes seem well covered by current HB risk assessment schemes. Exceptions to this are exposure routes related to nesting substrates and nesting materials used by SB. Exposure via soil is of particular concern because most SB species nest underground. Six SB species (Hymenoptera: Megachilidae-Osmia bicornis L., O. cornifrons Radoszkowski, O. cornuta Latreille, O. lignaria Say, Megachile rotundata F., and Halictidae-Nomia melanderi Cockerell) are commercially available and could be used in risk assessment. Of these, only N. melanderi nests underground, and the rest are cavity-nesters. However, the three Osmia species collect soil to build their nests. Life history traits of cavity-nesting species make them particularly suitable for semifield and, to a lesser extent, field tests. Future studies should address basic biology, rearing methods and levels of exposure of ground-nesting SB species.
To date, regulatory pesticide risk assessments have relied on the honey bee (Apis mellifera L.) (Hymenoptera: Apidae) as a surrogate test species for estimating the risk of pesticide exposure to all bee species. However, honey bees and non-Apis bees may differ in their susceptibility and exposure to pesticides. In 2017, a workshop ('Pesticide Exposure Assessment Paradigm for Non-Apis Bees') was held to assess if honey bee risk assessment frameworks are reflective of non-Apis bee pesticide exposure. In this article, we summarize the workshop discussions on bumble bees (Bombus spp.). We review the life history and foraging behavior of bumble bees and honey bees and discuss how these traits may influence routes and levels of exposure for both taxa. Overall, the major pesticide exposure routes for bumble bees and honey bees are similar; however, bumble bees face additional exposure routes (direct exposure of foraging queens and exposure of larvae and adults to soil residues). Furthermore, bumble bees may receive comparatively higher pesticide doses via contact or oral exposure. We conclude that honey bee pesticide risk assessments may not always be protective of bumble bees, especially queens, in terms of exposure. Data needed to reliably quantify pesticide exposure for bumble bees (e.g., food consumption rates, soil residue levels) are lacking. Addressing these knowledge gaps will be crucial before bumble bee exposure can be incorporated into the pesticide risk assessment process. Because bumble bees exhibit appreciable interspecific variation in colony and behavioral characteristics, data relevant to pesticide exposure should be generated for multiple species.
Pollinators in agroecosystems are often exposed to pesticide mixtures. Even at low concentrations, the effects of these mixtures on bee populations are difficult to predict due to potential synergistic interactions. In this paper, we orally exposed newly emerged females of the solitary beeOsmia bicornis to environmentally realistic levels of clothianidin (neonicotinoid insecticide) and propiconazole (fungicide), singly and in combination. The amount of feeding solution consumed was highest in bees exposed to the neonicotinoid, and lowest in bees exposed to the pesticide mixture. Ovary maturation and longevity of bees of the neonicotinoid and the fungicide treatments did not differ from those of control bees. By contrast, bees exposed to the pesticide mixture showed slow ovary maturation and decreased longevity. We found a synergistic interaction between the neonicotinoid and the fungicide on survival probability. We also found an interaction between treatment and emergence time (an indicator of physiological condition) on longevity. Longevity was negatively correlated to physiological condition only in the fungicide and the mixture treatments. Delayed ovary maturation and premature death imply a shortened nesting period (highly correlated to fecundity in Osmia). Our findings provide a mechanism to explain the observed dynamics of solitary bee populations exposed to multiple chemical residues in agricultural environments.
Intensive agriculture currently relies on pesticides to maximize crop yield1,2. Neonicotinoids are the most widely used insecticides globally³, but increasing evidence of negative impacts on important pollinators4–9 and other non-target organisms¹⁰ has led to legislative reassessment and created demand for the development of alternative products. Sulfoximine-based insecticides are the most likely successor¹¹, and are either licensed for use or under consideration for licensing in several worldwide markets³, including within the European Union¹², where certain neonicotinoids (imidacloprid, clothianidin and thiamethoxam) are now banned from agricultural use outside of permanent greenhouse structures. There is an urgent need to pre-emptively evaluate the potential sub-lethal effects of sulfoximine-based pesticides on pollinators¹¹, because such effects are rarely detected by standard ecotoxicological assessments, but can have major impacts at larger ecological scales13–15. Here we show that chronic exposure to the sulfoximine-based insecticide sulfoxaflor, at dosages consistent with potential post-spray field exposure, has severe sub-lethal effects on bumblebee (Bombus terrestris) colonies. Field-based colonies that were exposed to sulfoxaflor during the early growth phase produced significantly fewer workers than unexposed controls, and ultimately produced fewer reproductive offspring. Differences between the life-history trajectories of treated and control colonies first became apparent when individuals exposed as larvae began to emerge, suggesting that direct or indirect effects on a small cohort may have cumulative long-term consequences for colony fitness. Our results caution against the use of sulfoximines as a direct replacement for neonicotinoids. To avoid continuing cycles of novel pesticide release and removal, with concomitant impacts on the environment, a broad evidence base needs to be assessed prior to the development of policy and regulation.
Synthetic fungicides are pesticides widely used in agriculture to control phytopathogenic fungi. The systemicity, persistency and intense application of some of these fungicides, such as boscalid, leads to long periods of exposure for honeybees via contaminated water, pollen and nectar. We exposed adult honeybees in the lab to food contaminated with boscalid for 33 days instead of the standard 10-day test. Most of the toxic effects were observed after 10 days. The median time to death (LT50) ranged from 24.9 days (lowest concentration) to 7.1 days (highest concentration) and was significantly shorter in all cases than with the control (32.0 days). The concentration and dietary doses of boscalid inducing 50% mortality (LC50 and LDD50, respectively) decreased strongly with the time of exposure: LC50 = 14,729 and 1,174 mg/l and LDD50 = 0.318 and 0.0301 mg bee-1 day-1 at days 8 and 25, respectively. We found evidence of reinforced toxicity when exposure is prolonged, but with an unusual pattern: no cumulative toxicity is observed until 17-18 days, when a point of inflexion appears that suggests a reduced capacity of bees to deal with the toxicant. Our results show the importance of time-to-death experiments rather than fixed-duration studies for evaluating chronic toxicity.
The major pesticides of the world are glyphosate-based herbicides (GBH), and their toxicity is highly debated. To understand their mode of action, the comparative herbicidal and toxicological effects of glyphosate (G) alone and 14 of its formulations were studied in this work, as a model for pesticides. GBH are mixtures of water, with commonly 36–48% G claimed as the active principle. As with other pesticides, 10–20% of GBH consist of chemical formulants. We previously identified these by mass spectrometry and found them to be mainly families of petroleum-based oxidized molecules, such as POEA, and other contaminants. We exposed plants and human cells to the components of formulations, both mixed and separately, and measured toxicity and human cellular endocrine disruption below the direct toxicity experimentally measured threshold. G was only slightly toxic on plants at the recommended dilutions in agriculture, in contrast with the general belief. In the short term, the strong herbicidal and toxic properties of its formulations were exerted by the POEA formulant family alone. The toxic effects and endocrine disrupting properties of the formulations were mostly due to the formulants and not to G. In this work, we also identified by mass spectrometry the heavy metals arsenic, chromium, cobalt, lead and nickel, which are known to be toxic and endocrine disruptors, as contaminants in 22 pesticides, including 11 G-based ones. This could also explain some of the adverse effects of the pesticides. In in vivo chronic regulatory experiments that are used to establish the acceptable daily intakes of pesticides, G or other declared active ingredients in pesticides are assessed alone, without the formulants. Considering these new data, this assessment method appears insufficient to ensure safety. These results, taken together, shed a new light on the toxicity of these major herbicides and of pesticides in general.
The widespread contamination of a significant proportion of the planet’s land and water with
pesticides is undeniable. While this takes place, innumerable species of animals associated with
agricultural landscapes are declining at rates that may put them on the brink to extinction in
the span of a lifetime. It is evident, therefore, that our current risk assessment of agrochemicals
has failed to protect the environment. A new framework is proposed here that combines the
mandatory introduction of new toxicity endpoints with a more logical assessment of risks within
the existing tiered approach. Chronic toxicity tests designed to detect time-cumulative effects
should be a requirement for assessing delayed mortality as well as population endpoints that are
crucial for the recovery and survival of species, such as fecundity. Exposure assessments should
ensure that field monitoring data integrate both the highest and average levels of residues, as the
former levels determine the main ecological impacts. The first tier of the risk assessment should
comprise an evaluation of short-term mortality (as currently done by a hazard quotient on acute
toxicity) and of the lethality after chronic exposure to sublethal levels. Chemicals that pass this
tier should be assessed in a second tier whereby the crucial population endpoints are evaluated.
Unless there is evidence of recovery with no negative effects on reproduction of the species tested,
a chemical should not be registered. Further tiers of assessment, including sublethal effects,
community effects tested in model ecosystems (i.e. microcosms, mesocoms) and field trials can
still be used as supporting evidence, as it is currently done.
Pollinators are in global decline and agricultural pesticides are a potential driver of this. Recent studies have suggested that pesticides may significantly impact bumblebee colonies—an important and declining group of pollinators. Here, we show that colony-founding queens, a critical yet vulnerable stage of the bumblebee lifecycle, are less likely to initiate a colony after exposure to thiamethoxam, a neonicotinoid insecticide. Bombus terrestris queens were exposed to field-relevant levels of thiamethoxam and two natural stressors: the parasite Crithidia bombi and varying hibernation durations. Exposure to thiamethoxam caused a 26% reduction in the proportion of queens that laid eggs, and advanced the timing of colony initiation, although we did not detect impacts of any experimental treatment on the ability of queens to produce adult offspring during the 14-week experimental period. As expected from previous studies, the hibernation duration also had an impact on egg laying, but there was no significant interaction with insecticide treatment. Modelling the impacts of a 26% reduction in colony founding on population dynamics dramatically increased the likelihood of population extinction. This shows that neonicotinoids can affect this critical stage in the bumblebee lifecycle and may have significant impacts on population dynamics.
Damage confirmed
Early studies of the impacts of neonicotinoid insecticides on insect pollinators indicated considerable harm. However, lingering criticism was that the studies did not represent field-realistic levels of the chemicals or prevailing environmental conditions. Two studies, conducted on different crops and on two continents, now substantiate that neonicotinoids diminish bee health (see the Perspective by Kerr). Tsvetkov et al. find that bees near corn crops are exposed to neonicotinoids for 3 to 4 months via nontarget pollen, resulting in decreased survival and immune responses, especially when coexposed to a commonly used agrochemical fungicide. Woodcock et al. , in a multicounty experiment on rapeseed in Europe, find that neonicotinoid exposure from several nontarget sources reduces overwintering success and colony reproduction in both honeybees and wild bees. These field results confirm that neonicotinoids negatively affect pollinator health under realistic agricultural conditions.
Science , this issue p. 1395 , p. 1393 ; see also p. 1331
Neonicotinoid pesticides were first introduced in the mid-1990s, and since then, their use has grown rapidly. They are now the most widely used class of insecticides in the world, with the majority of applications coming from seed dressings. Neonicotinoids are water-soluble, and so can be taken up by a developing plant and can be found inside vascular tissues and foliage, providing protection against herbivorous insects. However, only approximately 5% of the neonicotinoid active ingredient is taken up by crop plants and most instead disperses into the wider environment. Since the mid-2000s, several studies raised concerns that neonicotinoids may be having a negative effect on non-target organisms, in particular on honeybees and bumblebees. In response to these studies, the European Food Safety Authority (EFSA) was commissioned to produce risk assessments for the use of clothianidin, imidacloprid and thiamethoxam and their impact on bees. These risk assessments concluded that the use of these compounds on certain flowering crops poses a high risk to bees. On the basis of these findings, the European Union adopted a partial ban on these substances in May 2013. The purpose of the present paper is to collate and summarise scientific evidence published since 2013 that investigates the impact of neonicotinoids on non-target organisms. Whilst much of the recent work has focused on the impact of neonicotinoids on bees, a growing body of evidence demonstrates that persistent, low levels of neonicotinoids can have negative impacts on a wide range of free-living organisms.
Imidacloprid is the most widely used insecticide in the world. In this study, we used spraying methods to simulate field exposures of bees to formulated imidacloprid (Advise® 2FL) alone and binary mixtures with seven pesticides from different classes. Synergistic toxicity was detected from mixtures of Advise (58.6 mg a.i./L imidacloprid)+Domark (512.5 mg a.i. /L tetraconazole), Advise+Transform (58.5 mg a.i./L sulfoxaflor), and Advise+Vydate (68 mg a.i./L oxamyl), and mortality was significantly increased by 20%, 15%, and 26% respectively. The mixtures of Advise+Bracket (88.3 mg a.i./L acephate) and Advise+Karate (62.2 mg a.i./L L-cyhalothrin) showed additive interaction, while Advise+Belay (9.4 mg a.i./L clothianidin) and Advise+Roundup (1217.5 mg a.i./L glyphosate) had no additive/synergistic interaction. Spraying bees with the mixture of all eight pesticides increased mortality to 100%, significantly higher than all other treatments. Except Bracket which significantly suppressed esterase and acetylcholinesterase (AChE) activities, other treatments of Advise-only and mixtures with other pesticides did not suppress enzyme activities significantly, including invertase, glutathione S-transferase (GST), and esterase and AChE. Immunity-related phenoloxidase (PO) activities in survivors tended to be more variable among treatments, but mostly still statistically similar to the control. By using specific enzyme inhibitors, we demonstrated that honey bees mainly rely on cytochrome P450 monooxygenases (P450s) for detoxifying Advise, while esterases and GSTs play substantially less roles in the detoxification. This study provided valuable information for guiding pesticide selection in premixing and tank mixing in order to alleviate toxicity risk to honey bees. Our findings indicated mixtures of Advise with detoxification-enzyme-inducing pesticides may help bees to detoxify Advise, while toxicity synergists may pose further risk to bees, such as the Bracket which not only suppressed esterase and AChE activities, but also increased toxicity to bees.
Abstract: Up to now, no official guideline for standardised semi-field trials exists to assess effects of pesticides on bumble bees. Open questions are: What are relevant endpoints for bumble bees? How can these endpoints be assessed in a reliable, reproducible way? To answer these questions, tests have been performed from 2014 to 2016 based on the recommendations of the ICPPR Non-Apis workgroup of 2015 and 2016. Experiences were gained regarding different crops, season and size of colonies. Following endpoints were assessed: brood development, mortality, flight and foraging activity, colony mass and reproduction (young queens and drones). Selected results will be shown and advantages/shortcomings of different designs and endpoints discussed.
In the early 2000s, Italian beekeepers began to report bee mortality events linked to maize sowing. Evidence pointed to three neonicotinoids (imidacloprid, clothianidin, thiamethoxam) and a phenylpyrazole (fipronil) used for seed dressing that were dispersed in the environment during sowing. Following these events and based on the precautionary principle, in September 2008, the Ital-ian Ministry of Health suspended these four active ingredients as maize seed dressing. Here we show that in Italy after the precautionary suspension, the number of bee mortality events linked to maize sowing drastically declined. At the same time, the average annual maize production per hectare remained unchanged. This finding is indicative of the possibility to maintain stable maize productions without affecting honey bee health status. The implementation of Integrated Pest Management for maize production is discussed.
Current approaches to risk assessment in bees do not take into account co-exposures from multiple stressors. The European Food Safety Authority (EFSA) is deploying resources and efforts to move towards a holistic risk assessment approach of multiple stressors in bees. This paper describes the general principles of pesticide risk assessment in bees, including recent developments at EFSA dealing with risk assessment of single and multiple pesticide residues and biological hazards. The EFSA Guidance Document on the risk assessment of plant protection products in bees highlights the need for the inclusion of an uncertainty analysis, other routes of exposures and multiple stressors such as chemical mixtures and biological agents. The EFSA risk assessment on the survival, spread and establishment of the small hive beetle, Aethina tumida, an invasive alien species, is provided with potential insights for other bee pests such as the Asian hornet, Vespa velutina. Furthermore, data gaps are identified at each step of the risk assessment, and recommendations are made for future research that could be supported under the framework of Horizon 2020. Finally, the recent work conducted at EFSA is presented, under the overarching MUST-B project (“EU efforts towards the development of a holistic approach for the risk assessment on MUltiple STressors in Bees”) comprising a toolbox for harmonised data collection under field conditions and a mechanistic model to assess effects from pesticides and other stressors such as biological agents and beekeeping management practices, at the colony level and in a spatially complex landscape. Future perspectives at EFSA include the development of a data model to collate high quality data to calibrate and validate the model to be used as a regulatory tool. Finally, the evidence collected within the framework of MUST-B will support EFSA's activities on the development of a holistic approach to the risk assessment of multiple stressors in bees. In conclusion, EFSA calls for collaborative action at the EU level to establish a common and open access database to serve multiple purposes and different stakeholders.
Background
We assess the analysis of the data resulting from a field experiment conducted by Pilling et al. (PLoS ONE. doi: 10.1371/journal.pone.0077193, 5) on the potential effects of thiamethoxam on honeybees. The experiment had low levels of replication, so Pilling et al. concluded that formal statistical analysis would be misleading. This would be true if such an analysis merely comprised tests of statistical significance and if the investigators concluded that lack of significance meant little or no effect. However, an analysis that includes estimation of the size of any effects—with confidence limits—allows one to reach conclusions that are not misleading and that produce useful insights.
Main body
For the data of Pilling et al., we use straightforward statistical analysis to show that the confidence limits are generally so wide that any effects of thiamethoxam could have been large without being statistically significant. Instead of formal analysis, Pilling et al. simply inspected the data and concluded that they provided no evidence of detrimental effects and from this that thiamethoxam poses a “low risk” to bees.
Conclusions
Conclusions derived from the inspection of the data were not just misleading in this case but also are unacceptable in principle, for if data are inadequate for a formal analysis (or only good enough to provide estimates with wide confidence intervals), then they are bound to be inadequate as a basis for reaching any sound conclusions. Given that the data in this case are largely uninformative with respect to the treatment effect, any conclusions reached from such informal approaches can do little more than reflect the prior beliefs of those involved.
Electronic supplementary material
The online version of this article (doi:10.1186/s12302-016-0103-8) contains supplementary material, which is available to authorized users.
The aim of this study was to investigate the effects of Elado® (10 g clothianidin & 2 g beta-cyfluthrin/kg seed)-dressed oilseed rape on the development and reproduction of mason bees (Osmia bicornis) as part of a large-scale monitoring field study in Northern Germany, where oilseed rape is usually cultivated at 25–33 % of the arable land. Both reference and test sites comprised 65 km2 in which no other crops attractive to pollinating insects were present. Six study locations were selected per site and three nesting shelters were placed at each location. Of these locations, three locations were directly adjacent to oilseed rape fields, while the other three locations were situated 100 m distant from the nearest oilseed rape field. At each location, 1500 cocoons of O. bicornis were placed into the central nesting shelter. During the exposure phase, nest building activities and foraging behaviour were assessed repeatedly. Cocoons were harvested in autumn to assess parasitization and reproduction including larval development. The following spring, the emergence of the next generation of adults from cocoons was monitored. High reproductive output and low parasitization rates indicated that Elado®-dressed oilseed rape did not cause any detrimental effects on the development or reproduction of mason bees.
Background:
Neonicotinoid insecticides have been identified as an important factor contributing to bee diversity declines. Nonetheless, uncertainties remain about their impact under field conditions. Most studies have been conducted on Apis mellifera and tested single compounds. However, in agricultural environments, bees are often exposed to multiple pesticides. We explore synergistic mortality between a neonicotinoid (clothianidin) and an ergosterol-biosynthesis-inhibitor fungicide (propiconazole) in three bee species (A. mellifera, Bombus terrestris, Osmia bicornis) following oral exposure in the laboratory.
Results:
We developed a new approach based on the binomial proportion test to analyze synergistic interactions. We estimated uptake of clothianidin per foraging bout in honey bees foraging on seed-coated rapeseed fields. We found significant synergistic mortality in all three bee species exposed to non-lethal doses of propiconazole and their respective LD10 of clothianidin. Significant synergism was only found in the first assessment times in A. mellifera (4 and 24 h) and B. terrestris (4 h), but persisted throughout the experiment (96 h) in O. bicornis. Osmia bicornis was also the most sensitive species to clothianidin.
Conclusion:
Our results underscore the importance to test pesticide combinations likely to occur in agricultural environments, and to include several bee species in environmental risk assessment schemes.
Monitoring studies at the landscape level are complex, expensive and difficult to conduct. Many aspects have to be considered to avoid confounding effects which is probably the reason why they are not regularly performed in the context of risk assessments of plant protection products to pollinating insects. However, if conducted appropriately their contribution is most valuable. In this paper we identify the requirements of a large-scale monitoring study for the assessment of side-effects of clothianidin seed-treated winter oilseed rape on three species of pollinating insects (Apis mellifera, Bombus terrestris and Osmia bicornis) and present how these requirements were implemented. Two circular study sites were delineated next to each other in northeast Germany and comprised almost 65 km2 each. At the reference site, study fields were drilled with clothianidin-free OSR seeds while at the test site the oilseed rape seeds contained a coating with 10 g clothianidin and 2 g beta-cyfluthrin per kg seeds (Elado®). The comparison of environmental conditions at the study sites indicated that they are as similar as possible in terms of climate, soil, land use, history and current practice of agriculture as well as in availability of oilseed rape and non-crop bee forage. Accordingly, local environmental conditions were considered not to have had any confounding effect on the results of the monitoring of the bee species. Furthermore, the study area was found to be representative for other oilseed rape cultivation regions in Europe.
The objective of this study was to evaluate the effects of chronical exposure of honeybee drones to environmental (5 ppb) and non-environmental concentration (200 ppb) of imidacloprid (IMD) on sperm concentration, motility, viability, and mitochondrial membrane potential measured in semen obtained from 180 drones originating from 18 colonies. The results demonstrate that IMD exposure did not affect sperm concentration; however, there were significant differences in concentration within colonies. IMD exposure was associated with reductions in sperm motility, which also varied within colonies. Statistically significant interactions between IMD exposure and colony were found for active mitochondria and sperm viability. Our results strongly suggest that neonicotinoids can negatively affect honeybee drone sperm quality. It is important to emphasize that IMD actions can be strongly modulated according to the colony.
Many factors can negatively affect honey bee (Apis mellifera L.) health including the pervasive use of systemic neonicotinoid insecticides. Through direct consumption of contaminated nectar and pollen from treated plants, neonicotinoids can affect foraging, learning, and memory in worker bees. Less well studied are the potential effects of neonicotinoids on queen bees, which may be exposed indirectly through trophallaxis, or food-sharing. To assess effects on queen productivity, small colonies of different sizes (1500, 3000, and 7000 bees) were fed imidacloprid (0, 10, 20, 50, and 100 ppb) in syrup for three weeks. We found adverse effects of imidacloprid on queens (egg-laying and locomotor activity), worker bees (foraging and hygienic activities), and colony development (brood production and pollen stores) in all treated colonies. Some effects were less evident as colony size increased, suggesting that larger colony populations may act as a buffer to pesticide exposure. This study is the first to show adverse effects of imidacloprid on queen bee fecundity and behavior and improves our understanding of how neonicotinoids may impair short-term colony functioning. These data indicate that risk-mitigation efforts should focus on reducing neonicotinoid exposure in the early spring when colonies are smallest and queens are most vulnerable to exposure.