Honey contamination from plant protection products approved for cocoa (Theobroma cacao) cultivation: A systematic review of existing research and methods.

The main component of chocolate, cocoa (Theobroma cacao), is a significant commercial agricultural plant that directly sustains the livelihoods of an estimated forty to fifty million people. The economies of many cocoa producing nations, particularly those in the developing world, are supported by cocoa export revenue. To ensure satisfactory yields, however, the plant is usually intensely treated with pesticides because it is vulnerable to disease and pest attacks. Even though pesticides help protect the cocoa plant, unintended environmental contamination is also likely. Honey, produced from nectar obtained by honeybees from flowers while foraging, can serve as a good indicator for the level of pesticide residues and environmental pesticide build-up in landscapes. Here, we use a systematic literature review to quantify the extent of research on residues of pesticides used in cocoa cultivation in honey. In 81% of the 104 studies examined for this analysis, 169 distinct compounds were detected. Imidacloprid was the most frequently detected pesticide, making neonicotinoids the most frequently found class of pesticides overall. However, in cocoa producing countries, organophosphates, organochlorines, and pyrethroids were the most frequently detected pesticides. Interestingly, only 19% of studies were carried out in cocoa producing countries. We recommend prioritizing more research in the countries that produce cocoa to help to understand the potential impact of pesticide residues linked with cocoa cultivation in honey and the environment more generally to inform better pesticide usage, human health, and environmental policies.

The breeding systems and floral visitors of two widespread African dry forest species of ethnobotanical significance.

Forest products derived from woody trees, such as fruits, seeds, honey, wood and others, are important resources for supporting rural livelihoods. However, little is known about the breeding systems or floral visitors of trees that provide these resources, often due to the difficulty of accessing tree canopies. This study addresses key knowledge gaps from a data poor region, providing information on the breeding systems and contribution of biotic pollination to two trees abundant in south-central Africa, that provide forest product supports for rural livelihoods: Julbernardia paniculata (Benth.) Troupin and Syzygium guineense (Willd.) subsp. barotsense F. White (Fabaceae and Myrtaceae respectively). The breeding systems of these species were assessed by conducting controlled pollination experiments, and then measuring the effects on reproductive success to determine the degree of self-compatibility and pollen limitation. Floral visitors and their behaviour were observed to provide preliminary information on possible pollinator groups. S. guineense appeared to be self-compatible, while J. paniculata showed signs of both self-incompatibility and pollen limitation. Floral visitors of both species were dominated by bees, with native honeybees (Apis mellifera) providing the highest visitation rates. These insights provide the first steps for understanding the reproductive ecology of these key tree species and can help to inform sustained management and conservation aimed at protecting forests and supporting rural livelihoods, as well as broaden the understanding of the floral visitors, and contribution of biotic pollination to forest tree reproductive success.

Weak evidence base for bee protective pesticide mitigation measures.

Pesticides help produce food for humanity's growing population, yet they have negative impacts on the environment. Limiting these impacts, while maintaining food supply, is a crucial challenge for modern agriculture. Mitigation measures are actions taken by pesticide users, which modify the risk of the application to nontarget organisms, such as bees. Through these, the impacts of pesticides can be reduced, with minimal impacts on the efficacy of the pesticide. Here we collate the scientific evidence behind mitigation measures designed to reduce pesticide impacts on bees using a systematic review methodology. We included all publications which tested the effects of any pesticide mitigation measure (using a very loose definition) on bees, at any scale (from individual through to population level), so long as they presented evidence on the efficacy of the measure. We found 34 publications with direct evidence on the topic, covering a range of available mitigation measures. No currently used mitigation measures were thoroughly tested, and some entirely lacked empirical support, showing a weak evidence base for current recommendations and policy. We found mitigation measure research predominantly focuses on managed bees, potentially failing to protect wild bees. We also found that label-recommended mitigation measures, which are the mitigation measures most often applied, specifically are seldom tested empirically. Ultimately, we recommend that more, and stronger, scientific evidence is required to justify existing mitigation measures to help reduce the impacts of pesticides on bees while maintaining crop protection.

Solitary bee behaviour and pollination service delivery is differentially impacted by neonicotinoid and pyrethroid insecticides.

Solitary bees are important pollinators of crops and wild plants, and their decline poses a risk to the sustained provision of the services they provide. Although evidence suggests that exposure to insecticides can affect bees, most pesticide research and risk assessment has focussed on social bees and mortality while solitary species are understudied. The ability to forage is critical for solitary bee reproduction, also in how they deliver pollination services, and we know little about how insecticides can impact these behaviours. We exposed solitary red mason bees (Osmia bicornis) to field realistic levels of two widely used insecticides with differing modes of action (lambda-cyhalothrin (pyrethroid) and acetamiprid (neonicotinoid)), in a semi-field setting over multiple rounds of exposure. We then tested impacts on bee behaviour and pollination in apples, an important global insect-pollinated crop. Pollination by insecticide-treated bees reduced apple production by up to 86 % depending on the compound and the number of exposures, but the underlying mechanism behind this remains unclear and should be investigated further. Other measurements of pollination services including number of seeds per apple and stigma pollen deposition showed no relationship with pesticide treatment. Bee foraging behaviour was also affected by treatment where both insecticides appear to induce an excitatory effect which was constant for acetamiprid and eventually ceased for lambda-cyhalothrin after multiple exposures. This suggests that both neonicotinoid and non­neonicotinoid insecticides can potentially affect behaviour and pollination services of solitary bees depending on how often they are exposed, which is particularly important given the changing usage patterns of these compound classes based on regulations around their use. This highlights the importance of moving insecticide risk assessment towards more field realistic scenarios and including sublethal effects on solitary and social bees, in addition to considering repeated exposures of bees to pesticides as is realistic in the field.

Contrasting effects of fungicide and herbicide active ingredients and their formulations on bumblebee learning and behaviour.

Fungicides and herbicides are two of the most heavily applied pesticide classes in the world, but receive little research attention with regards to their potential impacts on bees. As they are not designed to target insects, the mechanisms behind potential impacts of these pesticides are unclear. It is therefore important to understand their influence at a range of levels, including sublethal impacts on behaviours such as learning. We used the proboscis extension reflex (PER) paradigm to assess how the herbicide glyphosate and the fungicide prothioconazole affect bumblebee olfactory learning. We also assessed responsiveness, and compared the impacts of these active ingredients and their respective commercial formulations (Roundup Biactive and Proline). We found that learning was not impaired by either formulation but, of the bees that displayed evidence of learning, exposure to prothioconazole active ingredient increased learning level in some situations, while exposure to glyphosate active ingredient resulted in bumblebees being less likely to respond to antennal stimulation with sucrose. Our data suggest that fungicides and herbicides may not negatively impact olfactory learning ability when bumblebees are exposed orally to field-realistic doses in a lab setting, but that glyphosate has the potential to cause changes in responsiveness in bees. As we found impacts of active ingredients and not commercial formulations, this suggests that co-formulants may modify impacts of active ingredients in the products tested on olfactory learning without being toxic themselves. More research is needed to understand the mechanisms behind potential impacts of fungicides and herbicides on bees, and to evaluate the implications of behavioural changes caused by glyphosate and prothioconazole for bumblebee fitness.

Self-reported assessment of compliance with pesticide rules.

How pesticides are used is very important in determining the risk they pose to both the user, and the environment. Given they can have toxic properties, if pesticides are misused they could cause serious harm to the users health as well as a range of environmental damage. Despite this, very little research has quantified whether agricultural use of pesticides is compliant with the legally binding obligations and associated guidance surrounding application. In this survey we used an online, fully anonymous, questionnaire to ask Irish farmers about how they use pesticides. We used a self-reporting methodology, directly asking farmers about their compliance levels. We had a total of 76 unique valid respondents. Our respondents covered the broad range of Irish agriculture, and we quantified how this relates to national demographics. Overall compliance regarding pesticide use was high, with the majority of respondents complying the majority of the time. However, we also found a sizable group who report low compliance levels for certain topics. Respondents reported the highest levels of non-compliance with the use of personal protective equipment, with nearly half of all respondents admitting to not wearing certain required protective equipment on a regular basis. In contrast, for some areas like application rate, very high compliance was reported. Moderate levels of non-compliance with bee protective mitigation measures were found, and some reported practices like not emptying or washing out the spray tank between sprays could have serious impacts on pollinators, soil organisms and other non-targets. Additionally, a minority of respondents admitted to actions which could cause serious water course pollution. As the first survey on a range of pesticide compliance topics within a developed nation, the compliance seen is very high compared to levels in developing nations. Our results demonstrate that the assumption that all legal obligations and guidance surrounding pesticide use are followed is unfounded, but that the majority of the respondents are mostly compliant. Education or enforcement should be targeted to certain areas where compliance is weakest to minimise harm from pesticide use. Reducing the non-compliance we report here could benefit both farmer and environmental health, and ensure that pesticides are used in a manner that risk assessment has deemed safe.

Responses in honeybee and bumblebee activity to changes in weather conditions.

Insect pollination, and in particular pollination by bees, is a highly valued ecosystem service that ensures plant reproduction and the production of high-quality crops. Bee activity is known to be influenced by the weather, and as the global climate continues to change, the flying frequency and foraging behaviour of bees may also change. To maximise the benefits of pollination in a changing world, we must first understand how current weather conditions influence the activity of different bee species. This is of particular interest in a country such as Ireland where inclement weather conditions are nominally sub-optimal for foraging. We observed honeybee (Apis mellifera) and buff-tailed bumblebee (Bombus terrestris) activity across a variety of weather conditions at seven apple orchards to determine how four weather variables (temperature, relative humidity, solar radiation, wind) influenced the flight activity of each species. Each orchard contained three honeybee and three bumblebee colonies, and so we were able to observe a colony of each species concurrently in the same weather conditions. Overall, honeybees were more sensitive to changes in weather than bumblebees and could be more predisposed to future changes in within-day weather conditions. Our results indicate bumblebees could compensate for low honeybee activity in inclement conditions, which supports the theory that pollinator diversity provides resilience. This may be particularly important in management of pollinators in crops that flower in the spring when weather is more variable, and to allow varied responses to global climate change.

Investigating the effects of glyphosate on the bumblebee proteome and microbiota.

Glyphosate is one of the most widely used herbicides globally. It acts by inhibiting an enzyme in an aromatic amino acid synthesis pathway specific to plants and microbes, leading to the view that it poses no risk to other organisms. However, there is growing concern that glyphosate is associated with health effects in humans and an ever-increasing body of evidence that suggests potential deleterious effects on other animals including pollinating insects such as bees. Although pesticides have long been considered a factor in the decline of wild bee populations, most research on bees has focussed on demonstrating and understanding the effects of insecticides. To assess whether glyphosate poses a risk to bees, we characterised changes in survival, behaviour, sucrose solution consumption, the digestive tract proteome, and the microbiota in the bumblebee Bombus terrestris after chronic exposure to field relevant doses of technical grade glyphosate or the glyphosate-based formulation, RoundUp Optima+®. Regardless of source, there were changes in response to glyphosate exposure in important cellular and physiological processes in the digestive tract of B. terrestris, with proteins associated with oxidative stress regulation, metabolism, cellular adhesion, the extracellular matrix, and various signalling pathways altered. Interestingly, proteins associated with endocytosis, oxidative phosphorylation, the TCA cycle, and carbohydrate, lipid, and amino acid metabolism were differentially altered depending on whether the exposure source was glyphosate alone or RoundUp Optima+®. In addition, there were alterations to the digestive tract microbiota of bees depending on the glyphosate source No impacts on survival, behaviour, or food consumption were observed. Our research provides insights into the potential mode of action and consequences of glyphosate exposure at the molecular, cellular and organismal level in bumblebees and highlights issues with the current honeybee-centric risk assessment of pesticides and their formulations, where the impact of co-formulants on non-target organisms are generally overlooked.

Conserving diversity in Irish plant-pollinator networks.

Beneficial insects provide valuable services upon which we rely, including pollination. Pollinator conservation is a global priority, and a significant concern in Ireland, where over half of extant bee species have declined significantly in recent decades. As flower-visiting insects rely on flowering plants, one way to conserve and promote pollinator populations is to protect high-quality habitat. We analyzed the structure of insect-flower interactions from multiple habitat categories in a large database of interactions from Ireland. Our primary goals were to compare spatial and temporal variation in Irish network structures, compare Irish networks to published networks from other countries, and provide evidence-based recommendations for pollinator conservation in Ireland by identifying well-visited plant species that may promote high pollinator diversity, abundance, and functional complementarity. Habitat types within Ireland differed substantially: seminatural grasslands had the highest pollinator species richness and largest number of unique pollinator species, while intensively managed habitats exhibited negative asymmetry (more plant than pollinator species). This negative asymmetry is notable because most plant-pollinator networks exhibit a positive asymmetry. Within intensively managed habitats, agricultural and urban habitats differed. Urban habitats had the highest number of non-native plant species while agricultural habitats had the lowest pollinator species richness. We also found Irish networks varied across the growing season, where July had the highest plant and insect species richness. When comparing Irish networks to published networks from other countries, we found Irish networks had a higher ratio of plant species to pollinator species, and that this difference was most evident in agricultural habitats. This ratio means the typical network asymmetry (more pollinator than plant species) was flipped (more plant than pollinator species) in the Irish network. We conclude that conserving seminatural grasslands in Ireland will be an essential component of pollinator conservation and identify thirty-five plant species important for restoring seminatural habitats.

Bumblebees can be Exposed to the Herbicide Glyphosate when Foraging.

Herbicides are the most widely used pesticides globally. Although used to control weeds, they may also pose a risk to bee health. A key knowledge gap is how bees could be exposed to herbicides in the environment, including whether they may forage on treated plants before they die. We used a choice test to determine if bumblebees would forage on plants treated with glyphosate at two time periods after treatment. We also determined whether glyphosate and its degradation product aminomethylphosphonic acid were present as residues in the pollen collected by the bees while foraging. Finally, we explored if floral resources (nectar and pollen) remained present in plants after herbicide treatment. In general bees indiscriminately foraged on both plants treated with glyphosate and controls, showing no avoidance of treated plants. Although the time spent on individual flowers was slightly lower on glyphosate treated plants, this did not affect the bees' choice overall. We found that floral resources remained present in plants for at least 5 days after lethal treatment with glyphosate and that glyphosate residues were present in pollen for at least 70 h posttreatment. Our results suggest that bees could be exposed to herbicide in the environment, both topically and orally, by foraging on plants in the period between herbicide treatment and death. Identifying this route of exposure is a first step in understanding the risks of herbicides to bees. The effects of herbicides on bees themselves are uncertain and warrant further investigation to allow full risk assessment of these compounds to pollinating insects. Environ Toxicol Chem 2022;41:2603-2612. © 2022 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Assessing availability of European plant protection product data: an example evaluating basic area treated.

Besides the benefits of plant protection products (PPPs) for agricultural production, there is an increasing acknowledgement of the associated potential environmental risks. Here, we examine the feasibility of summarizing the extent of PPP usage at the country level, using Ireland as a case study, as well as at the European level. We used the area over which PPPs are applied (basic area) as an example variable that is relevant to initially assess the geographic extent of environmental risk. In Irish agricultural systems, which are primarily grass-based, herbicides fluroxypyr and glyphosate are the most widely applied active substances (ASs) in terms of basic area, followed by the fungicides chlorothalonil and prothioconazole that are closely associated with arable crops. Although all EU countries are subject to Regulation (EC) No 1185/2009, which sets the obligation of PPP usage data reporting at the national level, we only found usable data that met our criteria for Estonia, Germany, Finland, and Spain (4 of 30 countries reviewed). Overall, the most widely applied fungicide and herbicide in terms of basic area were prothioconazole (20%, 7% and 5% of national cultivated areas of Germany, Estonia and Ireland) and glyphosate (11%, 8% and 5% of national cultivated areas of Spain, Estonia and Ireland) respectively, although evaluations using application frequency may result in the observation of different trends. Several recommendations are proposed to tackle current data gaps and deficiencies in accessibility and usability of pesticide usage data across the EU in order to better inform environmental risk assessment and promote evidence-based policymaking.

Fungicides, herbicides and bees: A systematic review of existing research and methods.

Bees and the pollination services they deliver are beneficial to both food crop production, and for reproduction of many wild plant species. Bee decline has stimulated widespread interest in assessing hazards and risks to bees from the environment in which they live. While there is increasing knowledge on how the use of broad-spectrum insecticides in agricultural systems may impact bees, little is known about effects of other pesticides (or plant protection products; PPPs) such as herbicides and fungicides, which are used more widely than insecticides at a global scale. We adopted a systematic approach to review existing research on the potential impacts of fungicides and herbicides on bees, with the aim of identifying research approaches and determining knowledge gaps. While acknowledging that herbicide use can affect forage availability for bees, this review focussed on the potential impacts these compounds could have directly on bees themselves. We found that most studies have been carried out in Europe and the USA, and investigated effects on honeybees. Furthermore, certain effects, such as those on mortality, are well represented in the literature in comparison to others, such as sub-lethal effects. More studies have been carried out in the lab than in the field, and the impacts of oral exposure to herbicides and fungicides have been investigated more frequently than contact exposure. We suggest a number of areas for further research to improve the knowledge base on potential effects. This will allow better assessment of risks to bees from herbicides and fungicides, which is important to inform future management decisions around the sustainable use of PPPs.

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.

The long and the short of it: a global analysis of hawkmoth pollination niches and interaction networks.

1. Proboscis length has been proposed as a key dimension of plant pollination niches, but this niche space has not previously been explored at regional and global scales for any pollination system. Hawkmoths are ideal organisms for exploring pollinator niches as they are important pollinators in most of the biodiverse regions of the earth and vary greatly in proboscis length, with some species having the longest proboscides of all insects. 2. Using datasets for nine biogeographical regions spanning the Old and New World, we ask whether it is possible to identify distinct hawkmoth pollination niches based on the frequency distribution of proboscis length, and whether these niches are reflected in the depths of flowers that are pollinated by hawkmoths. We also investigate the levels of specialization in hawkmoth pollination systems at the regional and community level using data from interaction network studies. 3. We found that most regional hawkmoth assemblages have bimodal or multimodal distributions of proboscis length, and that these are matched by similar distributions of floral tube lengths. Hawkmoths, particularly those with longer proboscides, are polyphagous and at the network level show foraging specialization equivalent to or less than that of bees and hummingbirds. In the case of plants, shorter-tubed flowers are usually visited by numerous hawkmoth species, while those that are longer-tubed tend to exclude shorter-proboscid hawkmoths and thus become ecologically specialized on longer-proboscid hawkmoth species. Longer-tubed flowers tend to have greater nectar rewards and this promotes short-term constancy by long-proboscid hawkmoths. 4. Our results show that pollinator proboscis length is a key niche axis for plants and can account for patterns of evolution in functional traits such as floral tube length and nectar volume. We also highlight a paradoxical trend for nectar resource niche breadth to increase according to proboscis length of pollinators, while pollinator niche breadth decreases according to the tube length of flowers.

Investigating the impacts of field-realistic exposure to a neonicotinoid pesticide on bumblebee foraging, homing ability and colony growth.

The ability to forage and return home is essential to the success of bees as both foragers and pollinators. Pesticide exposure may cause behavioural changes that interfere with these processes, with consequences for colony persistence and delivery of pollination services.We investigated the impact of chronic exposure (5-43 days) to field-realistic levels of a neonicotinoid insecticide (2·4 ppb thiamethoxam) on foraging ability, homing success and colony size using radio frequency identification (RFID) technology in free-flying bumblebee colonies.Individual foragers from pesticide-exposed colonies carried out longer foraging bouts than untreated controls (68 vs. 55 min). Pesticide-exposed bees also brought back pollen less frequently than controls indicating reduced foraging performance.A higher proportion of bees from pesticide-exposed colonies returned when released 1 km from their nests; this is potentially related to increased orientation experience during longer foraging bouts. We measured no impact of pesticide exposure on homing ability for bees released from 2 km, or when data were analysed overall.Despite a trend for control colonies to produce more new workers earlier, we found no overall impacts of pesticide exposure on whole colony size. Synthesis and applications. This study shows that field-realistic neonicotinoid exposure can have impacts on both foraging ability and homing success of bumblebees, with implications for the success of bumblebee colonies in agricultural landscapes and their ability to deliver crucial pollination services. Pesticide risk assessments should include bee species other than honeybees and assess a range of behaviours to elucidate the impact of sublethal effects. This has relevance for reviews of neonicotinoid risk assessment and usage policy world-wide.

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

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.

Non-bee insects are important contributors to global crop pollination.

Wild and managed bees are well documented as effective pollinators of global crops of economic importance. However, the contributions by pollinators other than bees have been little explored despite their potential to contribute to crop production and stability in the face of environmental change. Non-bee pollinators include flies, beetles, moths, butterflies, wasps, ants, birds, and bats, among others. Here we focus on non-bee insects and synthesize 39 field studies from five continents that directly measured the crop pollination services provided by non-bees, honey bees, and other bees to compare the relative contributions of these taxa. Non-bees performed 25-50% of the total number of flower visits. Although non-bees were less effective pollinators than bees per flower visit, they made more visits; thus these two factors compensated for each other, resulting in pollination services rendered by non-bees that were similar to those provided by bees. In the subset of studies that measured fruit set, fruit set increased with non-bee insect visits independently of bee visitation rates, indicating that non-bee insects provide a unique benefit that is not provided by bees. We also show that non-bee insects are not as reliant as bees on the presence of remnant natural or seminatural habitat in the surrounding landscape. These results strongly suggest that non-bee insect pollinators play a significant role in global crop production and respond differently than bees to landscape structure, probably making their crop pollination services more robust to changes in land use. Non-bee insects provide a valuable service and provide potential insurance against bee population declines.

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 bees. 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 sublethal effects on bees, affecting their foraging behaviour, homing ability and reproductive success. Bees are essential for the pollination of a wide variety of crops and the majority of wild flowering plants, but until now research on pesticide effects has been limited to direct effects on bees themselves and not on the pollination services they provide. Here we show the first evidence to our knowledge that pesticide exposure can reduce the pollination services bumblebees deliver to apples, a crop of global economic importance. Bumblebee 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 indicate that reduced pollination service delivery is not due to pesticide-induced changes in individual bee behaviour, but most likely due to effects 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 functioning 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.