Novel indices reveal that pollinator exposure to pesticides varies across biological compartments and crop surroundings.

Declines in insect pollinators have been linked to a range of causative factors such as disease, loss of habitats, the quality and availability of food, and exposure to pesticides. Here, we analysed an extensive dataset generated from pesticide screening of foraging insects, pollen-nectar stores/beebread, pollen and ingested nectar across three species of bees collected at 128 European sites set in two types of crop. In this paper, we aimed to (i) derive a new index to summarise key aspects of complex pesticide exposure data and (ii) understand the links between pesticide exposures depicted by the different matrices, bee species and apple orchards versus oilseed rape crops. We found that summary indices were highly correlated with the number of pesticides detected in the related matrix but not with which pesticides were present. Matrices collected from apple orchards generally contained a higher number of pesticides (7.6 pesticides per site) than matrices from sites collected from oilseed rape crops (3.5 pesticides), with fungicides being highly represented in apple crops. A greater number of pesticides were found in pollen-nectar stores/beebread and pollen matrices compared with nectar and bee body matrices. Our results show that for a complete assessment of pollinator pesticide exposure, it is necessary to consider several different exposure routes and multiple species of bees across different agricultural systems.

A blood test to monitor bee health across a European network of agricultural sites of different land-use by MALDI BeeTyping mass spectrometry.

There are substantial concerns about impaired honey bee health and colony losses due to several poorly understood factors. We used MALDI profiling (MALDI BeeTyping®) analysis to investigate how some environmental and management factors under field conditions across Europe affected the honey bee haemolymph peptidome (all peptides in the circulatory fluid), as a profile of molecular markers representing the immune status of Apis mellifera. Honey bees were exposed to a range of environmental stressors in 128 agricultural sites across eight European countries in four biogeographic zones, with each country contributing eight sites each for two different cropping systems: oilseed rape (OSR) and apple (APP). The full haemolymph peptide profiles, including the presence and levels of three key immunity markers, namely the antimicrobial peptides (AMPs) Apidaecin, Abaecin and Defensin-1, allowed the honey bee responses to environmental variables to be discriminated by country, crop type and site. When considering just the AMPs, it was not possible to distinguish between countries by the prevalence of each AMP in the samples. However, it was possible to discriminate between countries on the amounts of the AMPs, with the Swedish samples in particular expressing high amounts of all AMPs. A machine learning model was developed to discriminate the haemolymphs of bees from APP and OSR sites. The model was 90.6 % accurate in identifying the crop type from the samples used to build the model. Overall, MALDI BeeTyping® of bee haemolymph represents a promising and cost-effective "blood test" for simultaneously monitoring dozens of peptide markers affected by environmental stressors at the landscape scale, thus providing policymakers with new diagnostic and regulatory tools for monitoring bee health.

Distribution of infectious and parasitic agents among three sentinel bee species across European agricultural landscapes.

Infectious and parasitic agents (IPAs) and their associated diseases are major environmental stressors that jeopardize bee health, both alone and in interaction with other stressors. Their impact on pollinator communities can be assessed by studying multiple sentinel bee species. Here, we analysed the field exposure of three sentinel managed bee species (Apis mellifera, Bombus terrestris and Osmia bicornis) to 11 IPAs (six RNA viruses, two bacteria, three microsporidia). The sentinel bees were deployed at 128 sites in eight European countries adjacent to either oilseed rape fields or apple orchards during crop bloom. Adult bees of each species were sampled before their placement and after crop bloom. The IPAs were detected and quantified using a harmonised, high-throughput and semi-automatized qPCR workflow. We describe differences among bee species in IPA profiles (richness, diversity, detection frequencies, loads and their change upon field exposure, and exposure risk), with no clear patterns related to the country or focal crop. Our results suggest that the most frequent IPAs in adult bees are more appropriate for assessing the bees' IPA exposure risk. We also report positive correlations of IPA loads supporting the potential IPA transmission among sentinels, suggesting careful consideration should be taken when introducing managed pollinators in ecologically sensitive environments.

Pesticide use negatively affects bumble bees across European landscapes.

Sustainable agriculture requires balancing crop yields with the effects of pesticides on non-target organisms, such as bees and other crop pollinators. Field studies demonstrated that agricultural use of neonicotinoid insecticides can negatively affect wild bee species1,2, leading to restrictions on these compounds3. However, besides neonicotinoids, field-based evidence of the effects of landscape pesticide exposure on wild bees is lacking. Bees encounter many pesticides in agricultural landscapes4-9 and the effects of this landscape exposure on colony growth and development of any bee species remains unknown. Here we show that the many pesticides found in bumble bee-collected pollen are associated with reduced colony performance during crop bloom, especially in simplified landscapes with intensive agricultural practices. Our results from 316 Bombus terrestris colonies at 106 agricultural sites across eight European countries confirm that the regulatory system fails to sufficiently prevent pesticide-related impacts on non-target organisms, even for a eusocial pollinator species in which colony size may buffer against such impacts10,11. These findings support the need for postapproval monitoring of both pesticide exposure and effects to confirm that the regulatory process is sufficiently protective in limiting the collateral environmental damage of agricultural pesticide use.

Pesticide Exposure and Effects on Non-Apis Bees.

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.

Seed treatment with clothianidin induces changes in plant metabolism and alters pollinator foraging preferences.

Neonicotinoids, systemic insecticides that are distributed into all plant tissues and protect against pests, have become a common part of crop production, but can unintentionally also affect non-target organisms, including pollinators. Such effects can be direct effects from insecticide exposure, but neonicotinoids can affect plant physiology, and effects could therefore also be indirectly mediated by changes in plant phenology, attractiveness and nutritional value. Under controlled greenhouse conditions, we tested if seed treatment with the neonicotinoid clothianidin affected oilseed rape's production of flower resources for bees and the content of the secondary plant products glucosinolates that provide defense against herbivores. Additionally, we tested if seed treatment affected the attractiveness of oilseed rape to flower visiting bumblebees, using outdoor mesocosms. Flowers and leaves of clothianidin-treated plants had different profiles of glucosinolates compared with untreated plants. Bumblebees in mesocosms foraged slightly more on untreated plants. Neither flower timing, flower size nor the production of pollen and nectar differed between treatments, and therefore cannot explain any preference for untreated oilseed rape. We instead propose that this small but significant preference for untreated plants was related to the altered glucosinolate profile caused by clothianidin. Thereby, this study contributes to the understanding of the complex relationships between neonicotinoid-treated crops and pollinator foraging choices, by suggesting a potential mechanistic link by which insecticide treatment can affect insect behavior.

Revised guidance on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees).

The European Commission asked EFSA to revise the risk assessment for honey bees, bumble bees and solitary bees. This guidance document describes how to perform risk assessment for bees from plant protection products, in accordance with Regulation (EU) 1107/2009. It is a review of EFSA's existing guidance document, which was published in 2013. The guidance document outlines a tiered approach for exposure estimation in different scenarios and tiers. It includes hazard characterisation and provides risk assessment methodology covering dietary and contact exposure. The document also provides recommendations for higher tier studies, risk from metabolites and plant protection products as mixture.

Ecological traits interact with landscape context to determine bees' pesticide risk.

Widespread contamination of ecosystems with pesticides threatens non-target organisms. However, the extent to which life-history traits affect pesticide exposure and resulting risk in different landscape contexts remains poorly understood. We address this for bees across an agricultural land-use gradient based on pesticide assays of pollen and nectar collected by Apis mellifera, Bombus terrestris and Osmia bicornis, representing extensive, intermediate and limited foraging traits. We found that extensive foragers (A. mellifera) experienced the highest pesticide risk-additive toxicity-weighted concentrations. However, only intermediate (B. terrestris) and limited foragers (O. bicornis) responded to landscape context-experiencing lower pesticide risk with less agricultural land. Pesticide risk correlated among bee species and between food sources and was greatest in A. mellifera-collected pollen-useful information for future postapproval pesticide monitoring. We provide foraging trait- and landscape-dependent information on the occurrence, concentration and identity of pesticides that bees encounter to estimate pesticide risk, which is necessary for more realistic risk assessment and essential information for tracking policy goals to reduce pesticide risk.

Seed-coating of rapeseed (Brassica napus) with the neonicotinoid clothianidin affects behaviour of red mason bees (Osmia bicornis) and pollination of strawberry flowers (Fragaria × ananassa).

Neonicotinoid insecticides applied to flowering crops can have negative impacts on bees, with implications for crop pollination. To assess if exposure to the neonicotinoid clothianidin via a treated crop (rapeseed) affected bee behaviour, pollination performance (to strawberry), and bee reproduction, we provided each of 12 outdoor cages with rapeseed (autumn-sown plants complemented with a few spring-sown plants to extend the flowering period) grown from either clothianidin-treated or untreated (control) seeds, together with strawberry plants and a small population of red mason bees (Osmia bicornis). We expected clothianidin to reduce bee foraging activity, resulting in impaired strawberry pollination and bee reproduction. During the early stage of the experiment, we observed no difference between treatments in the length of entire foraging trips, or the combined number of rapeseed and strawberry flowers that the bees visited during these trips. During the later stage of the experiment, we instead determined the time a female took to visit 10 rapeseed flowers, as a proxy for foraging performance. We found that they were 10% slower in clothianidin cages. Strawberries weighed less in clothianidin cages, suggesting reduced pollination performance, but we were unable to relate this to reduced foraging activity, because the strawberry flowers received equally many visits in the two treatments. Clothianidin-exposed females sealed their nests less often, but offspring number, sex ratio and weight were similar between treatments. Observed effects on bee behaviour appeared by the end of the experiment, possibly because of accumulated effects of exposure, reduced bee longevity, or higher sensitivity of the protocols we used during the later phase of the experiment. Although the lack of a mechanistic explanation calls for interpreting the results with cautiousness, the lower strawberry weight in clothianidin cages highlights the importance of understanding complex effects of plant protection products, which could have wider consequences than those on directly exposed organisms.

Statement on the active substance flupyradifurone.

Flupyradifurone is a novel butenolide insecticide, first approved as an active substance for use in plant protection products by Commission Implementing Regulation (EU) 2015/2084. Following concerns that this substance may pose high risks to humans and the environment, the French authorities, in November 2020, asked the Commission to restrict its uses under Article 69 of Regulation (EC) No 1107/2009. To support this request, competent Authorities from France cited a series of literature papers investigating its hazards and/or exposure to humans and the environment. In addition, in June 2020, the Dutch Authorities notified the Commission, under Article 56 of Regulation (EC) No 1107/2009, of new information on flupyradifurone on the wild bee species Megachile rotundata. This notification is also referred to in the French notification on flupyradifurone. Consequently, the EFSA PPR Panel was mandated to quantify the likelihood of this body of evidence constituting proof of serious risks to humans or the environment. Therefore, the EFSA PPR Panel evaluated the likelihood of these studies indicating new or higher hazards and exposure to humans and the environment compared to previous EU assessments. A stepwise methodology was designed, including: (i) the initial screening; (ii) data extraction and critical appraisal based on the principles of OHAT/NTP; (iii) weight of evidence, including consideration of the previous EU assessments; (iv) uncertainty analysis, followed, whenever relevant, by an expert knowledge elicitation process. For the human health, only one study was considered relevant for the genotoxic potential of flupyradifurone in vitro. These data did not provide sufficient information to overrule the EU assessment, as in vivo studies already addressed the genotoxic potential of flupyradifurone. Environment: All available data investigated hazards in bee species. For honey bees, the likelihood of the new data indicating higher hazards than the previous EU assessment was considered low or moderate, with some uncertainties. However, among solitary bee species - which were not addressed in the previous EU assessment - there was evidence that Megachile rotundata may be disproportionately sensitive to flupyradifurone. This sensitivity, which may partially be explained by the low bodyweight of this species, was mechanistically linked to inadequate bodily metabolisation processes.

Statement on the active substance acetamiprid.

Acetamiprid is a pesticide active substance with insecticidal action currently under the third renewal (AIR3) of the Commission implementing regulation (EU) No 844/2012. Following concerns that this substance may pose high risks to humans and the environment, the French authorities asked the Commission to restrict its uses under Article 69 of Regulation (EC) No 1107/2009. To support this request, competent Authorities from France cited a series of literature papers investigating its hazards and/or exposure to humans and the environment. Consequently, the EFSA PPR Panel was mandated to advise on the likelihood that body of evidence would constitute proof of serious risks to humans or the environment. Therefore, the EFSA PPR Panel evaluated the likelihood of these studies indicating new or higher hazards and exposure to humans and the environment compared to previous EU assessments.A stepwise methodology was designed, including: (i) the initial screening; (ii) the data extraction and critical appraisal based on the principles of OHAT/NTP; (iii) the weight of evidence, including consideration of the previous EU assessments; (iv) the uncertainty analysis, followed, whenever relevant, by an expert knowledge elicitation process. For human health, no conclusive evidence of higher hazards compared to previous assessment was found for genotoxicity, developmental toxicity, neurotoxicity including developmental neurotoxicity and immunotoxicity. However, due to the lack of adequate assessment of the current data set, the PPR Panel recommends conducting an assessment of endocrine disrupting properties for acetamiprid in line with EFSA/ECHA guidance document for the identification of endocrine disruptors. For environment, no conclusive, robust evidence of higher hazards compared to the previous assessment was found for birds, aquatic organisms, bees and soil organisms. However, the potential of high inter-species sensitivity of birds and bees towards acetamiprid requires further consideration.

Early resources lead to persistent benefits for bumble bee colony dynamics.

Conditions experienced early in development can affect the future performance of individuals and populations. Demographic theories predict persistent population impacts of past resources, but few studies have experimentally tested such carry-over effects across generations or cohorts. We used bumble bees to test whether resource timing had persistent effects on within-colony dynamics over sequential cohorts of workers. We simulated a resource pulse for field colonies either early or late in their development and estimated colony growth rates during pulse- and non-pulse periods. During periods when resources were not supplemented, early-pulse colonies grew faster than late-pulse colonies; early-pulse colonies grew larger as a result. These results revealed persistent effects of past resources on current growth and support the importance of transient dynamics in natural ecological systems. Early-pulse colonies also produced more queen offspring, highlighting the critical nature of resource timing for the population, as well as colony, dynamics of a key pollinator.

CropPol: A dynamic, open and global database on crop pollination.

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).

Wild insect diversity increases inter-annual stability in global crop pollinator communities.

While an increasing number of studies indicate that the range, diversity and abundance of many wild pollinators has declined, the global area of pollinator-dependent crops has significantly increased over the last few decades. Crop pollination studies to date have mainly focused on either identifying different guilds pollinating various crops, or on factors driving spatial changes and turnover observed in these communities. The mechanisms driving temporal stability for ecosystem functioning and services, however, remain poorly understood. Our study quantifies temporal variability observed in crop pollinators in 21 different crops across multiple years at a global scale. Using data from 43 studies from six continents, we show that (i) higher pollinator diversity confers greater inter-annual stability in pollinator communities, (ii) temporal variation observed in pollinator abundance is primarily driven by the three-most dominant species, and (iii) crops in tropical regions demonstrate higher inter-annual variability in pollinator species richness than crops in temperate regions. We highlight the importance of recognizing wild pollinator diversity in agricultural landscapes to stabilize pollinator persistence across years to protect both biodiversity and crop pollination services. Short-term agricultural management practices aimed at dominant species for stabilizing pollination services need to be considered alongside longer term conservation goals focussed on maintaining and facilitating biodiversity to confer ecological stability.

The effectiveness of flower strips and hedgerows on pest control, pollination services and crop yield: a quantitative synthesis.

Floral plantings are promoted to foster ecological intensification of agriculture through provisioning of ecosystem services. However, a comprehensive assessment of the effectiveness of different floral plantings, their characteristics and consequences for crop yield is lacking. Here we quantified the impacts of flower strips and hedgerows on pest control (18 studies) and pollination services (17 studies) in adjacent crops in North America, Europe and New Zealand. Flower strips, but not hedgerows, enhanced pest control services in adjacent fields by 16% on average. However, effects on crop pollination and yield were more variable. Our synthesis identifies several important drivers of variability in effectiveness of plantings: pollination services declined exponentially with distance from plantings, and perennial and older flower strips with higher flowering plant diversity enhanced pollination more effectively. These findings provide promising pathways to optimise floral plantings to more effectively contribute to ecosystem service delivery and ecological intensification of agriculture in the future.

A critical analysis of the potential for EU Common Agricultural Policy measures to support wild pollinators on farmland.

Agricultural intensification and associated loss of high-quality habitats are key drivers of insect pollinator declines. With the aim of decreasing the environmental impact of agriculture, the 2014 EU Common Agricultural Policy (CAP) defined a set of habitat and landscape features (Ecological Focus Areas: EFAs) farmers could select from as a requirement to receive basic farm payments. To inform the post-2020 CAP, we performed a European-scale evaluation to determine how different EFA options vary in their potential to support insect pollinators under standard and pollinator-friendly management, as well as the extent of farmer uptake.A structured Delphi elicitation process engaged 22 experts from 18 European countries to evaluate EFAs options. By considering life cycle requirements of key pollinating taxa (i.e. bumble bees, solitary bees and hoverflies), each option was evaluated for its potential to provide forage, bee nesting sites and hoverfly larval resources.EFA options varied substantially in the resources they were perceived to provide and their effectiveness varied geographically and temporally. For example, field margins provide relatively good forage throughout the season in Southern and Eastern Europe but lacked early-season forage in Northern and Western Europe. Under standard management, no single EFA option achieved high scores across resource categories and a scarcity of late season forage was perceived.Experts identified substantial opportunities to improve habitat quality by adopting pollinator-friendly management. Improving management alone was, however, unlikely to ensure that all pollinator resource requirements were met. Our analyses suggest that a combination of poor management, differences in the inherent pollinator habitat quality and uptake bias towards catch crops and nitrogen-fixing crops severely limit the potential of EFAs to support pollinators in European agricultural landscapes. Policy Implications. To conserve pollinators and help protect pollination services, our expert elicitation highlights the need to create a variety of interconnected, well-managed habitats that complement each other in the resources they offer. To achieve this the Common Agricultural Policy post-2020 should take a holistic view to implementation that integrates the different delivery vehicles aimed at protecting biodiversity (e.g. enhanced conditionality, eco-schemes and agri-environment and climate measures). To improve habitat quality we recommend an effective monitoring framework with target-orientated indicators and to facilitate the spatial targeting of options collaboration between land managers should be incentivised.

La intensificación agrícola y la consecuente pérdida de hábitats de alta calidad son desencadenantes clave del declive de los insectos polinizadores. Con el objetivo de disminuir el impacto ambiental de la agricultura, la Política Agrícola Común (PAC) de la UE de 2014 definió un conjunto de medidas para hábitats y paisajes (Áreas de Enfoque Ecológico: EFA por sus siglas en inglés) que los agricultores podían seleccionar como requisito para recibir pagos agrícolas básicos. Para informar la reforma de la PAC a partir a 2020, realizamos una evaluación a escala europea para determinar cómo las diferentes opciones de EFA varían en su potencial para asistir a los insectos polinizadores bajo un manejo estándar y amigable con los polinizadores, así como su aceptación por parte de los agricultores.El proceso estructurado de elicitación Delphi para evaluar las opciones de EFA involucró a 22 expertos de 18 países europeos. Se consideraron los requisitos de los diferentes taxones de polinizadores (es decir, abejorros, abejas solitarias y sírfidos) evaluando cada opción por su potencial para proporcionar forraje, sitios de nidificación y recursos para las larvas.Las opciones de EFA variaron sustancialmente en la cantidad de recursos que se percibía que proporcionan y su efectividad vario geográfica y temporalmente. Por ejemplo, los márgenes de cultivos proporcionan un forraje relativamente bueno durante toda la temporada en el sur y el este de Europa, pero carecen de forraje a principios de temporada en el norte y oeste de Europa. Bajo el manejo estándar, ninguna opción de EFA logró puntuaciones altas en todas las categorías de recursos y en general se percibió una escasez de forraje al final de la temporada.Los expertos identificaron oportunidades sustanciales para mejorar la calidad del hábitat mediante la adopción de un manejo amigable con los polinizadores. Sin embargo, mejorar la gestión por sí solo es poco probable que garantice que se cumplan todos los requisitos necesarios para los polinizadores. Nuestro análisis sugiere que una combinación de manejo inadecuado, diferencias de calidad inherentes a los distintos hábitat y el sesgo de aceptación hacia cultivos de cobertura y cultivos que fijan nitrógeno limitan severamente el potencial de los EFA para apoyar a los polinizadores en los paisajes agrícolas europeos. Implicaciones políticas. Para conservar a los polinizadores y ayudar a proteger los servicios de polinización, nuestro estudio destaca la necesidad de crear una variedad de hábitats interconectados y bien administrados que se complementen entre sí en los recursos que ofrecen. Para lograr esto, la PAC post­2020 debe integrar los diferentes vehículos de implementación destinados a proteger la biodiversidad (por ejemplo, condicionalidad mejorada, esquemas ecológicos y medidas agroambientales y climáticas). Para mejorar la calidad del hábitat, recomendamos un marco de monitoreo efectivo con indicadores orientados a objetivos y incentivar la colaboración entre los administradores de las tierras.

L'intensification agricole et la perte associée d'habitats semi­naturels sont les principaux moteurs du déclin des insectes pollinisateurs. Dans l'intention de réduire l'impact environnemental de l'agriculture, la politique agricole commune (PAC) de l'UE de 2014 a défini un ensemble d'habitats et d'éléments paysagers (surfaces d'intérêt écologique: SIE) dans la mise en place ou le respect desquels les agriculteurs pouvaient s'engager comme condition pour bénéficier d'aides économiques européennes (droit au paiement de base). Pour éclairer la PAC post­2020, nous avons évalué à l'échelle européenne et à dire d'expert, d'une part les potentialités des diverses SIE à favoriser les insectes pollinisateurs, via une gestion standard et via une gestion optimisée, et d'autre part l'étendue de l'adoption de ces mesures par les agriculteurs.Un processus structuré d'élaboration et d'agrégation des opinions (méthode Delphi) a fait appel à 22 experts de 18 pays européens pour évaluer les potentialités des diverses SIE. Considérant les traits bioécologiques des principaux taxons pollinisateurs (i.e. bourdons, abeilles solitaires et syrphes), chaque SIE a été évaluée pour son potentiel à fournir des ressources trophiques et des sites de reproduction (sites de nidification pour les bourdons et abeilles, sites de ponte et développement larvaire pour les syrphes).Les SIE différaient considérablement les unes des autres sur les ressources qu'elles étaient censées offrir et leur efficacité variait géographiquement et temporellement. Par exemple, les bords de champ peuvent fournir des ressources trophiques tout au long de l'année en Europe du Sud et de l'Est mais pas en début de saison en Europe du Nord et de l'Ouest. En cas de gestion standard, aucun type de SIE n'atteint de score élevé pour aucun type de ressource, et une période de disette alimentaire survient en fin de saison.Les experts ont mis en évidence de possibles et substantielles améliorations des SIE par le biais de leur gestion optimisée. Cependant, cette seule amélioration ne garantit pas la fourniture de ressources suffisantes aux pollinisateurs des paysages agricoles européens. Pour cela, des habitats spécifiques doivent être favorisés, dont la mise en place ne doit pas être entravée par un choix massif de SIE à base de cultures intermédiaires pièges à nitrates ou fixatrices d'azote. Implications politiques. Pour préserver les pollinisateurs et le service de pollinisation des plantes entomophiles, notre étude souligne la nécessité de créer une diversité d'habitats interconnectés, gérés de façon optimale, qui se complètent mutuellement dans les ressources qu'ils offrent. Pour atteindre cet objectif, la PAC post­2020 doit adopter une vision holistique de la mise en œuvre des différents leviers de protection de la biodiversité (e.g. éco­conditionnalité renforcée, programmes verts ou 'eco­schemes', mesures agro­environnementales et climatiques). Pour réellement améliorer la qualité des habitats, nous recommandons des suivis efficaces de la biodiversité à l'aide d'indicateurs pertinents. Enfin, pour optimiser la disposition spatiale des SIE et leur connectivité, la collaboration entre les différents gestionnaires des espaces agricoles doit être encouragée.

A intensificação agrícola e a perda associada de habitats de elevada qualidade são os principais factores que impulsionam o declínio dos insetos polinizadores. A fim de mitigar o impacto ambiental da agricultura, a Política Agrícola Comum (PAC) da UE, de 2014, definiu um conjunto de atributos ou estruturas do habitat e da paisagem, designadas de Áreas Foco Ecológico (AFEs) que devem ser mantidas pelos agricultores como requisito para obter as ajudas económicas previstas nas medidas agroambientais. No presente trabalho realizamos uma avaliação à escala europeia das diferentes opções destas estruturas, a fim de munir a PAC pós­2020, com informação sobre a importância das AFEs. Estas variam muito quanto ao seu potencial no apoio às populações de polinizadores, de acordo com a extensão da sua aceitação pelos agricultores e das práticas adoptadas por estes na sua gestão, que podem consistir em práticas padrão ou práticas mais amigáveis para os polinizadores.Um processo estruturado, com base na técnica de elicitação de Delphi foi desenvolvido, envolvendo 22 especialistas de 18 países europeus, com o objectivo de avaliar as opções de AFEs previstas na PAC. Esta avaliação levou em consideração os requisitos do ciclo de vida dos taxa dos principais polinizadores, ou seja, as abelhas, as abelhas solitárias e os sirfídeos ou moscas­das­flores. Cada AFE foi avaliada quanto ao seu potencial para fornecer alimento, locais de nidificação, e recursos para as larvas dos sirfídeos.A percepção quanto à eficácia das AFEs como fonte de recursos (alimento) para os polinizadores variou substancialmente, do ponto de vista quer geográfico, quer temporal (época do ano). Por exemplo, a AFE, faixas verdes nas margens do campo são consideradas uma boa fonte de alimento, no sul e leste da Europa, durante todo ano, mas ineficazes, no norte e oeste da Europa, no início do ano. Nenhuma EFA alcançou pontuações elevadas na categoria de recursos (fonte de alimento), quando submetida ao maneio padrão, sendo consideradas ineficientes, na segunda metade do ano.Os especialistas envolvidos identificaram oportunidades de melhoria substancial na qualidade do habitat, através da adopção de práticas de maneio das EFAs mais "amigáveis" para com os polinizadores. No entanto, a melhoria das práticas de maneio das EFAs por si só, dificilmente garantirá todos os requisitos necessários para a manutenção das populações de polinizadores. A nossa avaliação sugere que a combinação de práticas de má gestão (maneio), diferenças inerentes à qualidade do habitat dos polinizadores e o aumento do bias que resulta da utilização de espécies de crescimento rápido ou fixadoras de azoto limitam severamente o papel e potencial destas estruturas na manutenção das populações de polinizadores nas paisagens agrícolas europeias. Implicações políticas. A conservação dos polinizadores ajuda a proteger os serviços de polinização providenciados por estes. O nosso estudo destaca a necessidade de criar uma variedade de habitats interconectados e geridos de forma que se complementem na oferta de recursos (alimento, locais de nidificação e recursos para as larvas) aos polinizadores. Para atingir este objectivo, a PAC pós­2020 deve adoptar uma visão holística na implementação das EFAs, que integre os diferentes programas destinados a protecção da biodiversidade (por exemplo, maior condicionalidade, esquemas ecológicos, e medidas agroambientais e de adaptação climática). Para melhorar a qualidade do habitat, recomendamos uma estrutura de monitorização eficaz suportada por indicadores quantitativos e qualitativos orientados para metas, que permitam facilitar a tomada de decisões direcionadas especificamente para as EFAs, e que a colaboração entre os gestores da terra (agricultores) seja incentivada.

Can Costs of Pesticide Exposure for Bumblebees Be Balanced by Benefits from a Mass-Flowering Crop?

Mass-flowering crops provide forage for bees but also contain pesticides. Such pesticide exposure can harm bees, but our understanding of how this cost is balanced by forage benefits is limited. To provide insights into benefits and costs, we placed bumblebee colonies in 18 landscapes with conventional red clover fields treated with the neonicotinoid thiacloprid (flowers + pesticide), untreated organic red clover fields (flowers), or landscapes lacking clover fields (controls). Colonies grew heavier near thiacloprid-treated clover compared to controls lacking clover, while colonies near untreated clover did not differ from colonies in neither of the other landscape types. Thiacloprid treatment effectively controlled pests and increased bumblebee crop visitation. However, colony production of queens and males did not differ among landscape types. In conclusion, thiacloprid application in clover appears to be of low risk for bumblebees. More generally, neonicotinoids may not be equally harmful when used in flowering crops and effective low-risk pest control in such crops could potentially benefit bumblebees and crop pollination.

Substantial Heritable Variation in Recombination Rate on Multiple Scales in Honeybees and Bumblebees.

Meiotic recombination shuffles genetic variation and promotes correct segregation of chromosomes. Rates of recombination vary on several scales, both within genomes and between individuals, and this variation is affected by both genetic and environmental factors. Social insects have extremely high rates of recombination, although the evolutionary causes of this are not known. Here, we estimate rates of crossovers and gene conversions in 22 colonies of the honeybee, Apis mellifera, and 9 colonies of the bumblebee, Bombus terrestris, using direct sequencing of 299 haploid drone offspring. We confirm that both species have extremely elevated crossover rates, with higher rates measured in the highly eusocial honeybee than the primitively social bumblebee. There are also significant differences in recombination rate between subspecies of honeybee. There is substantial variation in genome-wide recombination rate between individuals of both A. mellifera and B. terrestris and the distribution of these rates overlap between species. A large proportion of interindividual variation in recombination rate is heritable, which indicates the presence of variation in trans-acting factors that influence recombination genome-wide. We infer that levels of crossover interference are significantly lower in honeybees compared to bumblebees, which may be one mechanism that contributes to higher recombination rates in honeybees. We also find a significant increase in recombination rate with distance from the centromere, mirrored by methylation differences. We detect a strong transmission bias due to GC-biased gene conversion associated with noncrossover gene conversions. Our results shed light on the mechanistic causes of extreme rates of recombination in social insects and the genetic architecture of recombination rate variation.

The interplay of landscape composition and configuration: new pathways to manage functional biodiversity and agroecosystem services across Europe.

Managing agricultural landscapes to support biodiversity and ecosystem services is a key aim of a sustainable agriculture. However, how the spatial arrangement of crop fields and other habitats in landscapes impacts arthropods and their functions is poorly known. Synthesising data from 49 studies (1515 landscapes) across Europe, we examined effects of landscape composition (% habitats) and configuration (edge density) on arthropods in fields and their margins, pest control, pollination and yields. Configuration effects interacted with the proportions of crop and non-crop habitats, and species' dietary, dispersal and overwintering traits led to contrasting responses to landscape variables. Overall, however, in landscapes with high edge density, 70% of pollinator and 44% of natural enemy species reached highest abundances and pollination and pest control improved 1.7- and 1.4-fold respectively. Arable-dominated landscapes with high edge densities achieved high yields. This suggests that enhancing edge density in European agroecosystems can promote functional biodiversity and yield-enhancing ecosystem services.