Search

Bumblebees and other key pollinators are experiencing global declines, a phenomenon driven by multiple environmental stressors, including pesticide exposure. While bumblebee queens spend most of their life hibernating underground, no study to date has examined how exposure to pesticide-contaminated soils might affect bumblebee queens during this solitary phase of their lifecycle. We exposed Bombus impatiens queens (n = 303) to soil treated with field-realistic concentrations of two diamide insecticides (chlorantraniliprole and cyantraniliprole) and two fungicides (boscalid and difenoconazole), alone or combined, during a 30-week hibernation period. We found that exposure to boscalid residues in soil doubled the likelihood of queens surviving through the colony initiation period (after successful hibernation) and laying eggs. Our data also revealed complex interactions between pesticide exposure and queen body mass on aspects of colony founding. Among others, exposure to cyantraniliprole led to lethal and sublethal post-hibernation effects that were dependent on queen size, with larger queens showing higher mortality rates, delayed emergence of their first brood, and producing smaller workers. Our results show that effects of pesticide exposure depend on intrinsic traits of bumblebee queen physiology and challenge our understanding of how bees respond to pesticides under environmentally realistic exposure scenarios., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2024 The Authors. Published by Elsevier B.V. All rights reserved.)

New evidence points to substantial impacts of exposure to pesticide residues in soil for a range of bee taxa that have close regular contact with this substrate. Among others, the risk of exposure is high for bumblebee (Bombus spp.) queens hibernating in agricultural soils. An important question is whether bumblebee queens can detect and avoid pesticide-contaminated soils, or whether they might be attracted to such agrochemical residues. To address this question, we performed a multiple-choice preference experiment in which newly emerged bumblebee (Bombus impatiens) queens were given access to arrays of 36 crates of soil treated with different pesticides in large mesh-covered enclosures. Five of the most commonly encountered pesticides in agricultural soils (boscalid, chlorantraniliprole, clothianidin, cyantraniliprole, difenoconazole) were selected for testing at two contamination levels (lower or higher), based on field-realistic exposure estimates. Bumblebee queens consistently avoided hibernating in pesticide-free soil at both contamination levels, while showing no avoidance for any pesticide-treated soil types. At the lower contamination level, queens selected the pesticide-free soil 1.3 to 2.4-fold less frequently on average than any of the spiked soils, while none of the queens from the higher contamination group selected pesticide-free soil. This apparent preference for pesticide-contaminated soils increases the likelihood of exposure to and potential hazard from pesticide residues in soil for bumblebee queens during hibernation, a critical and highly vulnerable period of their annual life cycle., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2024 The Authors. Published by Elsevier B.V. All rights reserved.)

Agricultural intensification has been identified as one of the key causes of global insect biodiversity losses. These losses have been further linked to the widespread use of agrochemicals associated with modern agricultural practices. Many of these chemicals are known to have negative sublethal effects on commercial pollinators, such as managed honeybees and bumblebees, but less is known about the impacts on wild bees. Laboratory-based studies with commercial pollinators have consistently shown that pesticide exposure can impact bee behavior, with cascading effects on foraging performance, reproductive success, and pollination services. However, these studies typically assess only one chemical, neglecting the complexity of real-world exposure to multiple agrochemicals and other stressors. In the summer of 2020, we collected wild-foraging workers of the common eastern bumblebee, Bombus impatiens, from five squash (Cucurbita) agricultural sites (organic and conventional farms), selected to represent a range of agrochemical, including neonicotinoid insecticide, use. For each bee, we measured two behaviors relevant to foraging success and previously shown to be impacted by pesticide exposure: sucrose responsiveness and locomotor activity. Following behavioral testing, we used liquid chromatography-tandem mass spectrometry (LC-MS/MS) chemical analysis to detect and quantify the presence of 92 agrochemicals in each bumblebee. Bees collected from our sites did not vary in pesticide exposure as expected. While we found a limited occurrence of neonicotinoids, two fungicides (azoxystrobin and difenoconazole) were detected at all sites, and the pesticide synergist piperonyl butoxide (PBO) was present in all 123 bees. We found that bumblebees that contained higher levels of PBO were less active, and this effect was stronger for larger bumblebee workers. While PBO is unlikely to be the direct cause of the reduction in bee activity, it could be an indicator of exposure to pyrethroids and/or other insecticides that we were unable to directly quantify, but which PBO is frequently tank-mixed with during pesticide applications on crops. We did not find a relationship between agrochemical exposure and bumblebee sucrose responsiveness. To our knowledge, this is the first evidence of a sublethal behavioral impact of agrochemical exposure on wild-foraging bees., (© 2024 The Ecological Society of America.)

In a previous study, an experimental oversight led to the accumulation of water filling a container housing diapausing bumblebee queens. Surprisingly, after draining the water, queens were found to be alive. This observation raises a compelling question: can bumblebee queens endure periods of inundation while overwintering underground? To address this question, we conducted an experiment using 143 common eastern bumblebee ( Bombus impatiens ) queens placed in soil-filled tubes and subjected to artificially induced diapause in a refrigerated unit for 7 days. Tap water was then added to the tubes and queens ( n = 21 per treatment) were either maintained underwater using a plunger-like apparatus or left to float naturally on the water's surface for varying durations (8 h, 24 h or 7 days) while remaining in overwintering conditions. Seventeen queens served as controls. After the submersion period, queens were removed from water, transferred to new tubes with soil and kept in cold storage for eight weeks. Overall, queen survival remained consistently high (89.5 ± 6.4%) across all treatments and did not differ among submersion regimes and durations. These results demonstrate the remarkable ability of diapausing B. impatiens queens to withstand submersion under water for up to one week, indicating their adaptations to survive periods of flooding in the wild.

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.

Bees are essential pollinators of many crops and wild plants, and pesticide exposure is one of the key environmental stressors affecting their health in anthropogenically modified landscapes. Until recently, almost all information on routes and impacts of pesticide exposure came from honey bees, at least partially because they were the only model species required for environmental risk assessments (ERAs) for insect pollinators. Recently, there has been a surge in research activity focusing on pesticide exposure and effects for non- Apis bees, including other social bees (bumble bees and stingless bees) and solitary bees. These taxa vary substantially from honey bees and one another in several important ecological traits, including spatial and temporal activity patterns, foraging and nesting requirements, and degree of sociality. In this article, we review the current evidence base about pesticide exposure pathways and the consequences of exposure for non- Apis bees. We find that the insights into non- Apis bee pesticide exposure and resulting impacts across biological organizations, landscapes, mixtures, and multiple stressors are still in their infancy. The good news is that there are many promising approaches that could be used to advance our understanding, with priority given to informing exposure pathways, extrapolating effects, and determining how well our current insights (limited to very few species and mostly neonicotinoid insecticides under unrealistic conditions) can be generalized to the diversity of species and lifestyles in the global bee community. We conclude that future research to expand our knowledge would also be beneficial for ERAs and wider policy decisions concerning pollinator conservation and pesticide regulation.

Habitat loss and fragmentation are major drivers of global pollinator declines, yet even after recent unprecedented periods of anthropogenic land-use intensification the amount of habitat needed to support insect pollinators remains unknown. Here we use comprehensive pan trap bee survey datasets from Ontario, Canada, to determine which habitat types are needed and at what spatial scales to support wild bee communities. Safeguarding wild bee communities in a Canadian landscape requires 11.6-16.7% land-cover from a diverse range of habitats (~ 2.6-3.7 times current policy guidelines) to provide targeted habitat prescriptions for different functional guilds over a variety of spatial scales, irrespective of whether conservation aims are enhancing bee species richness or abundance. Sensitive and declining habitats, like tallgrass woodlands and wetlands, were important predictors of bee biodiversity. Conservation strategies that under-estimate the extent of habitat, spatial scale and specific habitat needs of functional guilds are unlikely to protect bee communities and the essential pollination services they provide to both crops and wild plants., (© 2023. The Author(s).)

Exposure to pesticides is a major threat to bumblebee (Bombus spp.) health. In temperate regions, queens of many bumblebee species hibernate underground for several months, putting them at potentially high risk of exposure to soil contaminants. The extent to which bumblebees are exposed to residues in agricultural soils during hibernation is currently unknown, which limits our understanding of the full pesticide exposome for bumblebees throughout their lifecycle. To generate field exposure estimates for overwintering bumblebee queens to pesticide residues, we sampled soils from areas corresponding to suitable likely hibernation sites at six apple orchards and 13 diversified farms throughout Southern Ontario (Canada) in fall 2019-2020. Detectable levels of pesticides were found in 65 of 66 soil samples analysed for multi-pesticide residues (UPLC-MS/MS). A total of 53 active ingredients (AIs) were detected in soils, including 27 fungicides, 13 insecticides, and 13 herbicides. Overall, the frequency of detection, residue levels (median = 37.82 vs. 2.20 ng/g), and number of pesticides per sample (mean = 12 vs. 4 AIs) were highest for orchard soils compared to soils from diversified farms. Ninety-one percent of samples contained multiple residues (up to 29 different AIs per sample), including mixtures of insecticides and fungicides that might lead to synergistic effects. Our results suggest that when hibernating in agricultural areas, bumblebee queens are very likely to be exposed to a wide range of pesticide residues in soil, including potentially harmful levels of insecticides (e.g., cyantraniliprole up to 148.82 ng/g). Our study indicates the importance of empirically testing the potential effects of pesticide residues in soils for hibernating bumblebee queens, using field exposure data such as those generated here. The differences in potential exposure that we detected between cropping systems can also be used to better inform regulations that govern the use of agricultural pesticides, notably in apple orchards., (Copyright © 2022 The Authors. Published by Elsevier Ltd.. All rights reserved.)

Fungicides account for more than 35% of the global pesticide market and their use is predicted to increase in the future. While fungicides are commonly applied during bloom when bees are likely foraging on crops, whether real-world exposure to these chemicals - alone or in combination with other stressors - constitutes a threat to the health of bees is still the subject of great uncertainty. The first step in estimating the risks of exposure to fungicides for bees is to understand how and to what extent bees are exposed to these active ingredients. Here we review the current knowledge that exists about exposure to fungicides that bees experience in the field, and link quantitative data on exposure to acute and chronic risk of lethal endpoints for honey bees (Apis mellifera). From the 702 publications we screened, 76 studies contained quantitative data on residue detections in honey bee matrices, and a further 47 provided qualitative information about exposure for a range of bee taxa through various routes. We compiled data for 90 fungicides and metabolites that have been detected in honey, beebread, pollen, beeswax, and the bodies of honey bees. The risks posed to honey bees by fungicide residues was estimated through the EPA Risk Quotient (RQ) approach. Based on residue concentrations detected in honey and pollen/beebread, none of the reported fungicides exceeded the levels of concern (LOC) set by regulatory agencies for acute risk, while 3 and 12 fungicides exceeded the European Food Safety Authority (EFSA) chronic LOC for honey bees and wild bees, respectively. When considering exposure to all bees, fungicides of most concern include many broad-spectrum systemic fungicides, as well as the widely used broad-spectrum contact fungicide chlorothalonil. In addition to providing a detailed overview of the frequency and extent of fungicide residue detections in the bee environment, we identified important research gaps and suggest future directions to move towards a more comprehensive understanding and mitigation of the risks of exposure to fungicides for bees, including synergistic risks of co-exposure to fungicides and other pesticides or pathogens., (Copyright © 2022 The Authors. Published by Elsevier Ltd.. All rights reserved.)

The Common Eastern Bumblebee (Bombus impatiens) is native to North America with an expanding range across Eastern Canada and the USA. This species is commercially produced primarily for greenhouse crop pollination and is a common and abundant component of the wild bumblebee fauna in agricultural, suburban and urban landscapes. However, there is a dearth of pesticide toxicity information about North American bumblebees. The present study determined the acute oral lethal toxicity (48-h LD50) of: the butenolide, flupyradifurone (>1.7 μg/bee); the diamide, cyantraniliprole (>0.54 μg/bee); the neonicotinoid, thiamethoxam (0.0012 μg/bee); and the sulfoximine, sulfoxaflor (0.0177 μg/bee). Compared with published honey bee (Apis mellifera) LD50 values, the present study shows that sulfoxaflor and thiamethoxam are 8.3× and 3.3× more acutely toxic to B. impatiens, whereas flupyradifurone is more acutely toxic to A. mellifera. The current rule of thumb for toxicity extrapolation beyond the honey bee as a model species, termed 10× safety factor, may be sufficient for bumblebee acute oral toxicity. A comparison of five risk assessment equations suggested that the Standard Risk Approach (SRA) and Fixed Dose Risk Approach (FDRA) provide more nuanced levels of risk evaluation compared to the Exposure Toxicity Ratio (ETR), Hazard Quotient (HQ), and Risk Quotient (RQ), primarily because the SRA and FDRA take into account real world variability in pollen and nectar pesticide residues and the chances that bees may be exposed to them., (Copyright © 2022 The Authors. Published by Elsevier Ltd.. All rights reserved.)

Seventy five percent of the world's food crops benefit from insect pollination. Hence, there has been increased interest in how global change drivers impact this critical ecosystem service. Because standardized data on crop pollination are rarely available, we are limited in our capacity to understand the variation in pollination benefits to crop yield, as well as to anticipate changes in this service, develop predictions, and inform management actions. Here, we present CropPol, a dynamic, open, and global database on crop pollination. It contains measurements recorded from 202 crop studies, covering 3,394 field observations, 2,552 yield measurements (i.e., berry mass, number of fruits, and fruit density [kg/ha], among others), and 47,752 insect records from 48 commercial crops distributed around the globe. CropPol comprises 32 of the 87 leading global crops and commodities that are pollinator dependent. Malus domestica is the most represented crop (32 studies), followed by Brassica napus (22 studies), Vaccinium corymbosum (13 studies), and Citrullus lanatus (12 studies). The most abundant pollinator guilds recorded are honey bees (34.22% counts), bumblebees (19.19%), flies other than Syrphidae and Bombyliidae (13.18%), other wild bees (13.13%), beetles (10.97%), Syrphidae (4.87%), and Bombyliidae (0.05%). Locations comprise 34 countries distributed among Europe (76 studies), North America (60), Latin America and the Caribbean (29), Asia (20), Oceania (10), and Africa (7). Sampling spans three decades and is concentrated on 2001-2005 (21 studies), 2006-2010 (40), 2011-2015 (88), and 2016-2020 (50). This is the most comprehensive open global data set on measurements of crop flower visitors, crop pollinators and pollination to date, and we encourage researchers to add more datasets to this database in the future. This data set is released for non-commercial use only. Credits should be given to this paper (i.e., proper citation), and the products generated with this database should be shared under the same license terms (CC BY-NC-SA)., (© 2021 The Ecological Society of America.)

The phenology of crop flowering and pollinator reproduction can become asynchronous at the edge of their respective ranges. At a northern site in Peterborough County, Ontario, we evaluated offspring emergence of Cucurbita pollen specialist hoary squash bees ( Eucera pruinosa ) from nests in enclosures to determine their phenological synchrony with a squash crop ( Cucurbita pepo ). For the crop, we evaluated the percentage of bees that emerged in time to provide pollination services during the crop pollination window. For the bees, we compared the period when both male and females were present and could mate to the whole crop flowering period. We found that fewer than half the bees had emerged by the time the crop pollination window closed and only 34.1% of the flowering period of the crop could support the reproductive activities of the bees, suggesting that phenological synchrony was imperfect from the perspective of both the crop and the pollinator at this northern site., Competing Interests: The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (© 2021 The Author(s).)

The increasing demand for insect-pollinated crops highlights the need for crop pollination paradigms that include all available pollinators. In North America, Cucurbita crops (pumpkin, squash) depend on both wild (solitary and Bombus spp.: Hymenoptera: Apidae) and managed honey bees (Apis mellifera L. 1758: Hymenoptera: Apidae) for pollination. Temporal and spatial differences in abundance may determine which bee taxa are the most important pollinators of Cucurbita crops. We surveyed bees visiting Cucurbita crop flowers on 19 farms over four years (2015-2018) during the crop flowering period (July 1-August 30 from 06:00-12:00). All the farms surveyed had hoary squash bees (Eucera pruinosa (Say, 1867), and most also had some combination of honey bees, bumble bees (Bombus spp.), or other wild bees present on their Cucurbita crop flowers. All four bee taxa were present on about two-thirds of farms. Spatially and temporally, wild bees were more abundant on Cucurbita crop flowers than managed honey bees. Hoary squash bees were the most abundant wild bees, maintaining their abundance relative to other wild bee taxa year-over-year. Male hoary squash bees were both more frequently and consistently seen visiting crop flowers than females in all years. Peak activity of hoary squash bees and bumble bees coincided with the daily crop pollination window, whereas peak activity of honey bees and other wild bees occurred after that window. In addition to elucidating the ecological interactions among wild and managed pollinators on Cucurbita crops, our work provides a novel practical way to evaluate pollinator abundance using a crop-centered benchmark framework., (© The Author(s) 2021. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Eastern North American migratory monarch butterflies ( Danaus plexippus ) have faced sharp declines over the past two decades. Captive rearing of monarch butterflies is a popular and widely used approach for both public education and conservation. However, recent evidence suggests that captive-reared monarchs may lose their capacity to orient southward during fall migration to their Mexican overwintering sites, raising questions about the value and ethics of this activity undertaken by tens of thousands of North American citizens, educators, volunteers and conservationists each year. We raised offspring of wild-caught monarchs on swamp milkweed ( Asclepias incarnata ) indoors at 29°C during the day and 23°C at night (~77% RH, 18L:6D), and after eclosion, individuals were either tested in a flight simulator or radio tracked in the wild using an array of automated telemetry towers. While 26% (10/39) of monarchs tested in the flight simulator showed a weakly concentrated southward orientation, 97% (28/29) of the radio-tracked individuals that could be reliably detected by automated towers flew in a south to southeast direction from the release site and were detected at distances of up to 200 km away. Our results suggest that, although captive rearing of monarch butterflies may cause temporary disorientation, proper orientation is likely established after exposure to natural skylight cues., (© The Author(s) 2021. Published by Oxford University Press and the Society for Experimental Biology.)

Insect pollinators are threatened by multiple environmental stressors, including pesticide exposure. Despite being important pollinators, solitary ground-nesting bees are inadequately represented by pesticide risk assessments reliant almost exclusively on honeybee ecotoxicology. Here we evaluate the effects of realistic exposure via squash crops treated with systemic insecticides (Admire-imidacloprid soil application, FarMore FI400-thiamethoxam seed-coating, or Coragen-chlorantraniliprole foliar spray) for a ground-nesting bee species (Hoary squash bee, Eucera pruinosa) in a 3-year semi-field experiment. Hoary squash bees provide essential pollination services to pumpkin and squash crops and commonly nest within cropping areas increasing their risk of pesticide exposure from soil, nectar, and pollen. When exposed to a crop treated at planting with soil-applied imidacloprid, these bees initiated 85% fewer nests, left 5.3 times more pollen unharvested, and produced 89% fewer offspring than untreated controls. No measurable impacts on bees from exposure to squash treated with thiamethoxam as a seed-coating or foliage sprayed with chlorantraniliprole were found. Our results demonstrate important sublethal effects of field-realistic exposure to a soil-applied neonicotinoid (imidacloprid) on bee behaviour and reproductive success. Soil must be considered a potential route of pesticide exposure in risk assessments, and restrictions on soil-applied insecticides may be justified, to mitigate impacts on ground-nesting solitary bee populations and the crop pollination services they provide.

Migratory insects use a variety of innate mechanisms to determine their orientation and maintain correct bearing. For long-distance migrants, such as the monarch butterfly ( Danaus plexippus ), these journeys could be affected by exposure to environmental contaminants. Neonicotinoids are synthetic insecticides that work by affecting the nervous system of insects, resulting in impairment of their mobility, cognitive performance, and other physiological and behavioural functions. To examine how neonicotinoids might affect the ability of monarch butterflies to maintain a proper directional orientation on their ∼4000 km migration, we grew swamp milkweed ( Asclepias incarnata ) in soil that was either untreated (0 ng g -1 : control) or mixed with low (15 ng g -1 of soil) or high (25 ng g -1 of soil) levels of the neonicotinoid clothianidin. Monarch caterpillars were raised on control or clothianidin-treated milkweed and, after pupation, either tested for orientation in a static flight simulator or radio-tracked in the wild during the autumn migration period. Despite clothianidin being detectable in milkweed tissue consumed by caterpillars, there was no evidence that clothianidin influenced the orientation, vector strength (i.e. concentration of direction data around the mean) or rate of travel of adult butterflies, nor was there evidence that morphological traits (i.e. mass and forewing length), testing time, wind speed or temperature impacted directionality. Although sample sizes for both flight simulator and radio-tracking tests were limited, our preliminary results suggest that clothianidin exposure during early caterpillar development does not affect the directed flight of adult migratory monarch butterflies or influence their orientation at the beginning of migration., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2021. Published by The Company of Biologists Ltd.)

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 (LC 50 s) 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 LC 50 s for all residues evaluated but exceeded 5% for clothianidin and imidacloprid using a solitary bee LC 50 . 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.

Background: Individual bees exhibit complex movement patterns to efficiently exploit small areas within larger plant populations. How such individual spatial behaviours scale up to the collective level, when several foragers visit a common area, has remained challenging to investigate, both because of the low resolution of field movement data and the limited power of the statistical descriptors to analyse them. To tackle these issues we video recorded all flower visits ( N  = 6205), and every interaction on flowers ( N  = 628), involving foragers from a bumblebee ( Bombus terrestris ) colony in a large outdoor flight cage (880 m 2 ), containing ten artificial flowers, collected on five consecutive days, and analysed bee movements using networks statistics., Results: Bee-flower visitation networks were significantly more modular than expected by chance, indicating that foragers minimized overlaps in their patterns of flower visits. Resource partitioning emerged from differences in foraging experience among bees, and from outcomes of their interactions on flowers. Less experienced foragers showed lower activity and were more faithful to some flowers, whereas more experienced foragers explored the flower array more extensively. Furthermore, bees avoided returning to flowers from which they had recently been displaced by a nestmate, suggesting that bees integrate memories of past interactions into their foraging decisions., Conclusion: Our observations, under high levels of competition in a flight cage, suggest that the continuous turnover of foragers observed in colonies can led to efficient resource partitioning among bees in natural conditions., Competing Interests: Not applicable.Not applicable.The authors declare that they have no competing interests.Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Current pesticide risk assessment practices use the honey bee, Apis mellifera L., as a surrogate to characterize the likelihood of chemical exposure of a candidate pesticide for all bee species. Bees make up a diverse insect group that provides critical pollination services to both managed and wild ecosystems. Accordingly, they display a diversity of behaviors and vary greatly in their lifestyles and phenologies, such as their timing of emergence, degree of sociality, and foraging and nesting behaviors. Some of these factors may lead to disparate or variable routes of exposure when compared to honey bees. For those that possess life histories that are distinct from A. mellifera, further risk assessments may be warranted. In January 2017, 40 bee researchers, representative of regulatory agencies, academia, and agrochemical industries, gathered to discuss the current state of science on pesticide exposure to non-Apis bees and to determine how well honey bee exposure estimates, implemented by different regulatory agencies, may be protective for non-Apis bees. Workshop participants determined that although current risk assessment procedures for honey bees are largely conservative, several routes of exposure are unique to non-Apis bees and warranted further investigation. In this forum article, we discuss these key routes of exposure relevant to non-Apis bees and identify important research gaps that can help inform future bee risk assessment decisions.

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.

Sustainably feeding the next generation is often described as one of the most pressing "grand challenges" facing the 21st century. Generally, scholars propose addressing this problem by increasing agricultural production, investing in technology to boost yields, changing diets, or reducing food waste. In this paper, we explore whether global food production is nutritionally balanced by comparing the diet that nutritionists recommend versus global agricultural production statistics. Results show that the global agricultural system currently overproduces grains, fats, and sugars while production of fruits and vegetables and protein is not sufficient to meet the nutritional needs of the current population. Correcting this imbalance could reduce the amount of arable land used by agriculture by 51 million ha globally but would increase total land used for agriculture by 407 million ha and increase greenhouse gas emissions. For a growing population, our calculations suggest that the only way to eat a nutritionally balanced diet, save land and reduce greenhouse gas emissions is to consume and produce more fruits and vegetables as well as transition to diets higher in plant-based protein. Such a move will help protect habitats and help meet the Sustainable Development Goals., Competing Interests: The authors have declared that no competing interests exist.

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.

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.

Bumblebees are essential pollinators of crops and wild plants, but are in decline across the globe. Neonicotinoid pesticides have been implicated as a potential driver of these declines, but most of our evidence base comes from studies of a single species. There is an urgent need to understand whether such results can be generalized across a range of species. Here, we present results of a laboratory experiment testing the impacts of field-relevant doses (1.87-5.32 ppb) of the neonicotinoid thiamethoxam on spring-caught wild queens of four bumblebee species: Bombus terrestris , B. lucorum , B. pratorum and B. pascuorum. Two weeks of exposure to the higher concentration of thiamethoxam caused a reduction in feeding in two out of four species, suggesting species-specific anti-feedant, repellency or toxicity effects. The higher level of thiamethoxam exposure resulted in a reduction in the average length of terminal oocytes in queens of all four species. In addition to providing the first evidence for general effects of neonicotinoids on ovary development in multiple species of wild bumblebee queens, the discovery of species-specific effects on feeding has significant implications for current practices and policy for pesticide risk assessment and use., (© 2017 The Authors.)

Despite widespread interest in the potential adaptive value of individual differences in cognition, few studies have attempted to address the question of how variation in learning and memory impacts their performance in natural environments. Using a novel split-colony experimental design we evaluated visual learning performance of foraging naïve bumble bees (Bombus terrestris) in an ecologically relevant associative learning task under controlled laboratory conditions, before monitoring the lifetime foraging performance of the same individual bees in the field. We found appreciable variation among the 85 workers tested in both their learning and foraging performance, which was not predicted by colony membership. However, rather than finding that foragers benefited from enhanced learning performance, we found that fast and slow learners collected food at comparable rates and completed a similar number of foraging bouts per day in the field. Furthermore, bees with better learning abilities foraged for fewer days; suggesting a cost of enhanced learning performance in the wild. As a result, slower learning individuals collected more resources for their colony over the course of their foraging career. These results demonstrate that enhanced cognitive traits are not necessarily beneficial to the foraging performance of individuals or colonies in all environments.

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.

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.

Global declines of bumble bees and other pollinator populations are of concern because of their critical role for crop production and maintenance of wild plant biodiversity. Although the consensus among scientists is that the interaction of many factors, including habitat loss, forage scarcity, diseases, parasites, and pesticides, potentially plays a role in causing these declines, pesticides have received considerable attention and scrutiny. In response, regulatory agencies have introduced more stringent pollinator testing requirements for registration and reregistration of pesticides, to ensure that the risks to pollinators are minimized. In this context, guidelines for testing bumble bees (Bombus spp.) in regulatory studies are not yet available, and a pressing need exists to develop suitable protocols for routine higher-tier studies with these non-Apis sp., social bees. To meet this need, Bayer CropScience LP, Syngenta Crop Protection LLC US, and Valent USA. Corporation organized a workshop bringing together a group of global experts on bumble bee behavior, ecology, and ecotoxicology to discuss and develop draft protocols for both semi-field (Tier II) and field (Tier III) studies. The workshop was held May 8-9, 2014, at the Bayer Bee Care Center, North Carolina, USA. The participants represented academic, consulting, and industry scientists from Europe, Canada, the United States, and Brazil. The workshop identified a clear protection goal and generated proposals for basic experimental designs, relevant measurements, and endpoints for both semifield (tunnel) and field tests. These initial recommendations are intended to form the basis of discussions to help advance the development of appropriate protocol guidelines., (© 2015 The Authors. Integrated Environmental Assessment and Management Published by SETAC.)

Pollinators, such as bees, often develop multi-location routes (traplines) to exploit subsets of flower patches within larger plant populations. How individuals establish such foraging areas in the presence of other foragers is poorly explored. Here we investigated the foraging patterns of pairs of bumble bees (Bombus terrestris) released sequentially into an 880m2 outdoor flight cage containing 10 feeding stations (artificial flowers). Using motion-sensitive video cameras mounted on flowers, we mapped the flower visitation networks of both foragers, quantified their interactions and compared their foraging success over an entire day. Overall, bees that were released first (residents) travelled 37% faster and collected 77% more nectar, thereby reaching a net energy intake rate 64% higher than bees released second (newcomers). However, this prior-experience advantage decreased as newcomers became familiar with the spatial configuration of the flower array. When both bees visited the same flower simultaneously, the most frequent outcome was for the resident to evict the newcomer. On the rare occasions when newcomers evicted residents, the two bees increased their frequency of return visits to that flower. These competitive interactions led to a significant (if only partial) spatial overlap between the foraging patterns of pairs of bees. While newcomers may initially use social cues (such as olfactory footprints) to exploit flowers used by residents, either because such cues indicate higher rewards and/or safety from predation, residents may attempt to preserve their monopoly over familiar resources through exploitation and interference. We discuss how these interactions may favour spatial partitioning, thereby maximising the foraging efficiency of individuals and colonies.

The capacity to explore soft tissue structures in detail is important in understanding animal physiology and how this determines features such as movement, behaviour and the impact of trauma on regular function. Here we use advances in micro-computed tomography (micro-CT) technology to explore the brain of an important insect pollinator and model organism, the bumblebee (Bombus terrestris). Here we present a method for accurate imaging and exploration of insect brains that keeps brain tissue free from trauma and in its natural stereo-geometry, and showcase our 3D reconstructions and analyses of 19 individual brains at high resolution. Development of this protocol allows relatively rapid and cost effective brain reconstructions, making it an accessible methodology to the wider scientific community. The protocol describes the necessary steps for sample preparation, tissue staining, micro-CT scanning and 3D reconstruction, followed by a method for image analysis using the freeware SPIERS. These image analysis methods describe how to virtually extract key composite structures from the insect brain, and we demonstrate the application and precision of this method by calculating structural volumes and investigating the allometric relationships between bumblebee brain structures.

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.

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.

A summary is provided of recent advances in the natural science evidence base concerning the effects of neonicotinoid insecticides on insect pollinators in a format (a 'restatement') intended to be accessible to informed but not expert policymakers and stakeholders. Important new studies have been published since our recent review of this field (Godfray et al. 2014 Proc. R. Soc. B 281, 20140558. (doi:10.1098/rspb.2014.0558)) and the subject continues to be an area of very active research and high policy relevance., (© 2015 The Authors.)

There is evidence that in Europe and North America many species of pollinators are in decline, both in abundance and distribution. Although there is a long list of potential causes of this decline, there is concern that neonicotinoid insecticides, in particular through their use as seed treatments are, at least in part, responsible. This paper describes a project that set out to summarize the natural science evidence base relevant to neonicotinoid insecticides and insect pollinators in as policy-neutral terms as possible. A series of evidence statements are listed and categorized according to the nature of the underlying information. The evidence summary forms the appendix to this paper and an annotated bibliography is provided in the electronic supplementary material.

If the cognitive performance of animals reflects their particular ecological requirements, how can we explain appreciable variation in learning ability amongst closely related individuals (e.g. foraging workers within a bumble bee colony)? One possibility is that apparent 'errors' in a learning task actually represent an alternative foraging strategy. In this study we investigate the potential relationship between foraging 'errors' and foraging success among bumble bee (Bombus terrestris) workers. Individual foragers were trained to choose yellow, rewarded flowers and ignore blue, unrewarded flowers. We recorded the number of errors (visits to unrewarded flowers) each bee made during training, then tested them to determine how quickly they discovered a more profitable food source (either familiar blue flowers, or novel green flowers). We found that error prone bees discovered the novel food source significantly faster than accurate bees. Furthermore, we demonstrate that the time taken to discover the novel, more profitable, food source is positively correlated with foraging success. These results suggest that foraging errors are part of an 'exploration' foraging strategy, which could be advantageous in changeable foraging environments. This could explain the observed variation in learning performance amongst foragers within social insect colonies.

Organisation in eusocial insect colonies emerges from the decisions and actions of its individual members. In turn, these decisions and actions are influenced by the individual's behaviour (or temperament). Although there is variation in the behaviour of individuals within a colony, we know surprisingly little about how (or indeed if) the types of behaviour present in a colony change over time. Here, for the first time, we assessed potential changes in the behavioural type of foragers during colony development. Using an ecologically relevant foraging task, we measured the decision speed and learning ability of bumble bees (Bombus terrestris) at different stages of colony development. We determined whether individuals that forage early in the colony life cycle (the queen and early emerging workers) behaved differently from workers that emerge and forage at the end of colony development. Whilst we found no overall change in the foraging behaviour of workers with colony development, there were strong differences in foraging behaviour between queens and their workers. Queens appeared to forage more cautiously than their workers and were also quicker to learn. These behaviours could allow queens to maximise their nectar collecting efficiency whilst avoiding predation. Because the foundress queen is crucial to the survival and success of a bumble bee colony, more efficient foraging behaviour in queens may have strong adaptive value.

Animal personalities or behavioural syndromes are consistent and/or correlated behaviours across two or more situations within a population. Social insect biologists have measured consistent individual variation in behaviour within and across colonies for decades. The goal of this review is to illustrate the ways in which both the study of social insects and of behavioural syndromes has overlapped, and to highlight ways in which both fields can move forward through the synergy of knowledge from each. Here we, (i) review work to date on behavioural syndromes (though not always referred to as such) in social insects, and discuss mechanisms and fitness effects of maintaining individual behavioural variation within and between colonies; (ii) summarise approaches and principles from studies of behavioural syndromes, such as trade-offs, feedback, and statistical methods developed specifically to study behavioural consistencies and correlations, and discuss how they might be applied specifically to the study of social insects; (iii) discuss how the study of social insects can enhance our understanding of behavioural syndromes-research in behavioural syndromes is beginning to explore the role of sociality in maintaining or developing behavioural types, and work on social insects can provide new insights in this area; and (iv) suggest future directions for study, with an emphasis on examining behavioural types at multiple levels of organisation (genes, individuals, colonies, or groups of individuals)., (© 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society.)

Nosema ceranae is spreading into areas where Nosema apis already exists. N. ceranae has been reported to cause an asymptomatic infection that may lead, ultimately, to colony collapse. It is thought that there may be a temperature barrier to its infiltration into countries in colder climates. In this study, 71 colonies from Scottish Beekeeper's Association members have been screened for the presence of N. apis and N. ceranae across Scotland. We find that only 11 of the 71 colonies tested positive for spores by microscopy. However, 70.4 % of colonies screened by PCR revealed the presence of both N. ceranae and N. apis, with only 4.2 or 7 % having either strain alone and 18.3 % being Nosema free. A range of geographically separated colonies testing positive for N. ceranae were sequenced to confirm their identity. All nine sequences confirmed the presence of N. ceranae and indicated the presence of a single new variant. Furthermore, two of the spore-containing colonies had only N. ceranae present, and these exhibited the presence of smaller spores that could be distinguished from N. apis by the analysis of average spore size. Differential quantification of the PCR product revealed N. ceranae to be the dominant species in all seven samples tested. In conclusion, N. ceranae is widespread in Scotland where it exists in combination with the endemic N. apis. A single variant, identical to that found in France (DQ374655) except for the addition of a single nucleotide polymorphism, is present in Scotland.