Field-realistic Levels Research Articles

Bumblebee colony development following chronic exposure to field-realistic levels of the neonicotinoid pesticide thiamethoxam under laboratory conditions

Neonicotinoid pesticides are used in agriculture to reduce damage from crop pests. However, beneficial insects such as bees can come into contact with these pesticides when foraging in treated areas, with potential consequences for bee declines and pollination service delivery. Honeybees are typically used as a model organism to investigate insecticide impacts on bees, but relatively little is known about impacts on other taxa such as bumblebees. In this experiment, we chronically exposed whole mature bumblebee (Bombus terrestris) colonies to field-realistic levels of the neonicotinoid thiamethoxam (2.4ppb & 10ppb) over four weeks, and compared colony growth under laboratory conditions. We found no impact of insecticide exposure on colony weight gain, or the number or mass of sexuals produced, although colonies exposed to 2.4ppb produced larger males. As previous studies have reported pesticide effects on bumblebee colony growth, this may suggest that impacts on bumblebee colonies are more pronounced for colonies at an earlier stage in the reproductive cycle. Alternatively, it may also indicate that thiamethoxam differs in toxicity compared to previously tested neonicotinoids in terms of reproductive effects. In either case, assessing bumblebee colony development under field conditions is likely more informative for real world scenarios than tests conducted in laboratory conditions.

Country-specific effects of neonicotinoid pesticides on honey bees and wild bees

Neonicotinoid seed dressings have caused concern world-wide. We use large field experiments to assess the effects of neonicotinoid-treated crops on three bee species across three countries (Hungary, Germany, and the United Kingdom). Winter-sown oilseed rape was grown commercially with either seed coatings containing neonicotinoids (clothianidin or thiamethoxam) or no seed treatment (control). For honey bees, we found both negative (Hungary and United Kingdom) and positive (Germany) effects during crop flowering. In Hungary, negative effects on honey bees (associated with clothianidin) persisted over winter and resulted in smaller colonies in the following spring (24% declines). In wild bees (Bombus terrestris and Osmia bicornis), reproduction was negatively correlated with neonicotinoid residues. These findings point to neonicotinoids causing a reduced capacity of bee species to establish new populations in the year following exposure.

Pesticides and pollinators, an automated platform to assess the effects of neonicotinoid exposure and other environmental stressors on bee colonies: a computational, ethological study

BackgroundAnimal pollinators provide vital ecosystem services that sustain biodiversity and support agricultural yields. Declining pollinator populations threaten to affect human health outcomes by decreasing crop yields and human nutrient intake, and there is a well-recognised need to understand how environmental stressors such as pesticides affect bees, the most important animal pollinators. Neonicotinoid pesticides in particular, the most widely used class of insecticide globally, pose a major threat to bees. While there is now strong evidence that neonicotinoids can affect bee behaviour and colony growth, major knowledge gaps remain in understanding how these pesticides affect pollinator health. First, the specific mechanisms by which neonicotinoid exposure affect bee colonies are not well understood, limiting the ability to predict their effects. Second, it is unclear how pesticide exposure interacts with other environmental stressors, which could either amplify or attenuate the effects of neonicotinoids. MethodsWe describe the development of an automated, robotic system aimed at helping to fill these gaps in knowledge. Specifically, this system harnesses advances in computer vision to track the behaviour of hundreds of individual bees across dozens of colonies simultaneously. Specifically, this system uses a computer-controlled, motorised camera array to collect video data from up to a dozen bumblebee colonies in parallel. We then use computer vision-based techniques to automatically measure key aspects of behaviour (eg, activity level, task performance, and social interactions) for individually tagged bees before and after exposure to neonicotinoid pesticides. FindingsUsing a preliminary version of this system, we have found that exposure to field-realistic levels of a common neonicotinoid pesticide (imidacloprid) affects key aspects of social behaviour in bumblebees (Bombus impatiens). These effects include reduced rates of nursing (27% reduction; p<0·001) and interactions with nestmates (–10·6 unique interactions per h; p<0·001), as well as a reduction in activity level within the nest (27% reduction; p<0·001), suggesting a previously unknown mechanism by which pesticide exposure might lead to impaired growth in bee colonies. InterpretationThis automated, parallel system is ideal for studying the effects of multiple environmental stressors, and we are currently extending it to investigate simultaneous exposure to neonicotinoids, thermal stress, and nutritional deficiency on the behaviour and health of bee colonies. This system can provide efficient screening of agrochemicals at low cost, and could provide an important instrument for policymakers and other shareholders to assess the risk of agrochemicals to the health of both bee and human populations. FundingWinslow Foundation, Rockefeller Foundation.

The combined effects of a monotonous diet and exposure to thiamethoxam on the performance of bumblebee micro-colonies

There is a pressing need to better understand the factors contributing to declines of wild pollinators such as bumblebees. Many different contributors have been postulated including: loss of flower-rich habitats and nesting sites; monotonous diets; impacts of invasive pathogens; exposure to pesticides such as neonicotinoids. Past research has tended to investigate the impacts of these stressors in isolation, despite the increasing recognition that bees are simultaneously exposed to a combination of stressors, with potentially additive or synergistic effects. No studies to date have investigated the combined effects of a monotonous diet and exposure to pesticides. Using queenless micro-colonies of Bombus terrestris audax, we examined this interaction by providing bees with monofloral or polyfloral pollen that was either contaminated with field-realistic levels of thiamethoxam, a commonly used neonicotinoid, or not contaminated. Both treatments were found to have a significant effect on various parameters relating to micro-colony performance. Specifically, both pesticide-treated micro-colonies and those fed monofloral pollen grew more slowly than those given polyfloral pollen or pollen without pesticides. The two factors appeared to act additively. Micro-colonies given monofloral pollens also exhibited lower reproductive efforts and produced smaller drones. Although further research is needed to examine whether similar effects are found in whole colonies, these findings increase our understanding of the likely effects of multiple stressors associated with agricultural intensification on bee declines.

Chronic oral lethal and sub‐lethal toxicities of different binary mixtures of pesticides and contaminants in bees (Apis mellifera, Osmia bicornis and Bombus terrestris)

Chronic oral lethal and sub‐lethal toxicities of different binary mixtures of pesticides and contaminants in bees (Apis mellifera, Osmia bicornis and Bombus terrestris)

Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees.

Learning and memory are crucial functions which enable insect pollinators to efficiently locate and extract floral rewards. Exposure to pesticides or infection by parasites may cause subtle but ecologically important changes in cognitive functions of pollinators. The potential interactive effects of these stressors on learning and memory have not yet been explored. Furthermore, sensitivity to stressors may differ between species, but few studies have compared responses in different species. Here, we show that chronic exposure to field-realistic levels of the neonicotinoid clothianidin impaired olfactory learning acquisition in honeybees, leading to potential impacts on colony fitness, but not in bumblebees. Infection by the microsporidian parasite Nosema ceranae slightly impaired learning in honeybees, but no interactive effects were observed. Nosema did not infect bumblebees (3% infection success). Nevertheless, Nosema-treated bumblebees had a slightly lower rate of learning than controls, but faster learning in combination with neonicotinoid exposure. This highlights the potential for complex interactive effects of stressors on learning. Our results underline that one cannot readily extrapolate findings from one bee species to others. This has important implications for regulatory risk assessments which generally use honeybees as a model for all bees.

Chronic exposure to a neonicotinoid pesticide alters the interactions between bumblebees and wild plants.

Summary Insect pollinators are essential for both the production of a large proportion of world crops and the health of natural ecosystems. As important pollinators, bumblebees must learn to forage on flowers to feed both themselves and provision their colonies.Increased use of pesticides has caused concern over sublethal effects on bees, such as impacts on reproduction or learning ability. However, little is known about how sublethal exposure to field‐realistic levels of pesticide might affect the ability of bees to visit and manipulate flowers.We observed the behaviour of individual bumblebees from colonies chronically exposed to a neonicotinoid pesticide (10 ppb thiamethoxam) or control solutions foraging for the first time on an array of morphologically complex wildflowers (Lotus corniculatus and Trifolium repens) in an outdoor flight arena.We found that more bees released from pesticide‐treated colonies became foragers, and that they visited more L. corniculatus flowers than controls. Interestingly, bees exposed to pesticide collected pollen more often than controls, but control bees learnt to handle flowers efficiently after fewer learning visits than bees exposed to pesticide. There were also different initial floral preferences of our treatment groups; control bees visited a higher proportion of T. repens flowers, and bees exposed to pesticide were more likely to choose L. corniculatus on their first visit.Our results suggest that the foraging behaviour of bumblebees on real flowers can be altered by sublethal exposure to field‐realistic levels of pesticide. This has implications for the foraging success and persistence of bumblebee colonies, but perhaps more importantly for the interactions between wild plants and flower‐visiting insects and ability of bees to deliver the crucial pollination services to plants necessary for ecosystem functioning.

Consumption of the neonicotinoid thiamethoxam during the larval stage affects the survival and development of the stingless bee, Scaptotrigona aff. depilis

In Brazil, where the use of neonicotinoids is allowed in bee-attracting flowering crops, we investigated whether thiamethoxam intake during the larval stage of the native bee species Scaptotrigona aff. depilis affects the survival and development by exposing larvae to contaminated food. Our results indicated that the larvae exposed to the dose at a field-realistic level and to the doses ranging around it had their survival rates significantly impaired. At the highest doses, we observed larvae and pupae with shorter and longer development times, respectively, and the formation of smaller and asymmetric specimens. Evidently, we need to consider that thiamethoxam reaches the pollen and nectar at residual levels, and that they are processed by nurse bees before destined for offspring. Nevertheless, our findings suggest a warning, since the individuals had their biological parameters affected by thiamethoxam, when exposed to doses at field-realistic levels.

Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops

There is considerable and ongoing debate as to the harm inflicted on bees by exposure to agricultural pesticides. In part, the lack of consensus reflects a shortage of information on field-realistic levels of exposure. Here, we quantify concentrations of neonicotinoid insecticides and fungicides in the pollen of oilseed rape, and in pollen of wildflowers growing near arable fields. We then compare this to concentrations of these pesticides found in pollen collected by honey bees and in pollen and adult bees sampled from bumble bee colonies placed on arable farms. We also compared this with levels found in bumble bee colonies placed in urban areas. Pollen of oilseed rape was heavily contaminated with a broad range of pesticides, as was the pollen of wildflowers growing nearby. Consequently, pollen collected by both bee species also contained a wide range of pesticides, notably including the fungicides carbendazim, boscalid, flusilazole, metconazole, tebuconazole and trifloxystrobin and the neonicotinoids thiamethoxam, thiacloprid and imidacloprid. In bumble bees, the fungicides carbendazim, boscalid, tebuconazole, flusilazole and metconazole were present at concentrations up to 73nanogram/gram (ng/g). It is notable that pollen collected by bumble bees in rural areas contained high levels of the neonicotinoids thiamethoxam (mean 18ng/g) and thiacloprid (mean 2.9ng/g), along with a range of fungicides, some of which are known to act synergistically with neonicotinoids. Pesticide exposure of bumble bee colonies in urban areas was much lower than in rural areas. Understanding the effects of simultaneous exposure of bees to complex mixtures of pesticides remains a major challenge.

Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees.

Recent concern over global pollinator declines has led to considerable research on the effects of pesticides on bees1-5. Although pesticides are typically not encountered at lethal levels in the field, there is growing evidence indicating that exposure to field-realistic levels can have sub-lethal effects on bees affecting their foraging behaviour1,6,7, homing ability8,9 and reproductive success2,5. Bees are essential for the pollination of a wide variety of crops and the majority of wild flowering plants10-12, but until now research on pesticide impacts has been limited to direct effects on bees themselves and not on the pollination services they provide. Here we show the first evidence that pesticide exposure can reduce the pollination services bumblebees deliver to apples, a crop of global economic importance. Colonies exposed to a neonicotinoid pesticide provided lower visitation rates to apple trees and collected pollen less often. Most importantly these pesticide exposed colonies produced apples containing fewer seeds demonstrating a reduced delivery of pollination services. Our results also suggest reduced pollination service delivery is not due to pesticide-induced changes in individual bee behaviour but most likely due to impacts at the colony level. These findings show that pesticide exposure can impair the ability of bees to provide pollination services, with important implications for both the sustained delivery of stable crop yields and the function of natural ecosystems.

Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide

Bumblebees are exposed to pesticides applied for crop protection while foraging on treated plants, with increasing evidence suggesting that this sublethal exposure has implications for pollinator declines. The challenges of navigating and learning to manipulate many different flowers underline the critical role learning plays for the foraging success and survival of bees. We assessed the impacts of both acute and chronic exposure to field-realistic levels of a widely applied neonicotinoid insecticide, thiamethoxam, on bumblebee odour learning and memory. Although bees exposed to acute doses showed conditioned responses less frequently than controls, we found no difference in the number of individuals able to learn at field-realistic exposure levels. However, following chronic pesticide exposure, bees exposed to field-realistic levels learnt more slowly and their short-term memory was significantly impaired following exposure to 2.4 ppb pesticide. These results indicate that field-realistic pesticide exposure can have appreciable impacts on learning and memory, with potential implications for essential individual behaviour and colony fitness.

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

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

Environmental stochasticity promotes copper bioaccumulation and bioenergetic response in tilapia

Environmental change not only undergoes in mean environmental conditions but also in their degree of stochasticity. Changes in waterborne metal variability are often associated with altered disturbance regimes and temporal patterns of source availability. Here copper (Cu) was used as an example because Cu sulfate (CuSO4) has been extensively used as a chemical tool to exterminate phytoplankton for controlling skin lesions and gill disease of fish in aquatic ecosystems. This study showed that increased variability of waterborne Cu concentrations strongly promotes a key process of biokinetics, bioaccumulation. In experimental tilapia populations, the mean growth cost coefficient in pulsed Cu exposures was 7 % lower than the control group. On the other hand, the double-pulse, constant low, and single-pulse scenarios had similar effect on biomass change (2.2–2.4 %). The greatest biomass change (~10 %) occurred where Cu concentrations were gradually increasing over time or at a constant high rate. Most importantly, this study demonstrated that chronic exposure of tilapia to a low Cu concentration rate that approximated a single large pulse of field-realistic levels damaged bioenergetic mechanisms and increased energy acquisition. This study also showed that interactions across multiple pulsed or fluctuating Cu exposures were involved in accumulation changes that could also be achieved by controlling pulse timing and duration. It can be concluded that increased metal variability can promote biokinetic and bioenergetic responses in fish; and that changes in environmental variability may interact with other global change processes and thereby substantially accelerate change in aquatic ecosystems.

Effects of the neonicotinoid pesticide thiamethoxam at field-realistic levels on microcolonies of Bombus terrestris worker bumble bees

Neonicotinoid pesticides are currently implicated in the decline of wild bee populations. Bumble bees, Bombus spp., are important wild pollinators that are detrimentally affected by ingestion of neonicotinoid residues. To date, imidacloprid has been the major focus of study into the effects of neonicotinoids on bumble bee health, but wild populations are increasingly exposed to alternative neonicotinoids such as thiamethoxam. To investigate whether environmentally realistic levels of thiamethoxam affect bumble bee performance over a realistic exposure period, we exposed queenless microcolonies of Bombus terrestris L. workers to a wide range of dosages up to 98μgkg−1 in dietary syrup for 17 days. Results showed that bumble bee workers survived fewer days when presented with syrup dosed at 98μg thiamethoxamkg−1, while production of brood (eggs and larvae) and consumption of syrup and pollen in microcolonies were significantly reduced by thiamethoxam only at the two highest concentrations (39, 98μgkg−1). In contrast, we found no detectable effect of thiamethoxam at levels typically found in the nectars of treated crops (between 1 and 11μgkg−1). By comparison with published data, we demonstrate that during an exposure to field-realistic concentrations lasting approximately two weeks, brood production in worker bumble bees is more sensitive to imidacloprid than thiamethoxam. We speculate that differential sensitivity arises because imidacloprid produces a stronger repression of feeding in bumble bees than thiamethoxam, which imposes a greater nutrient limitation on production of brood.

A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees

Honey bees provide important pollination services to crops and wild plants. The agricultural use of systemic insecticides, such as neonicotinoids, may harm bees through their presence in pollen and nectar, which bees consume. Many studies have tested the effects on honey bees of imidacloprid, a neonicotinoid, but a clear picture of the risk it poses to bees has not previously emerged, because investigations are methodologically varied and inconsistent in outcome. In a meta-analysis of fourteen published studies of the effects of imidacloprid on honey bees under laboratory and semi-field conditions that comprised measurements on 7073 adult individuals and 36 colonies, fitted dose-response relationships estimate that trace dietary imidacloprid at field-realistic levels in nectar will have no lethal effects, but will reduce expected performance in honey bees by between 6 and 20%. Statistical power analysis showed that published field trials that have reported no effects on honey bees from neonicotinoids were incapable of detecting these predicted sublethal effects with conventionally accepted levels of certainty. These findings raise renewed concern about the impact on honey bees of dietary imidacloprid, but because questions remain over the environmental relevance of predominantly laboratory-based results, I identify targets for research and provide procedural recommendations for future studies.