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 species^1,2, 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 landscapes^4–9 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 impacts^10,11. 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.

Introduction: Heterogeneity in composition and spatial configuration of landscape elements support diversity and abundance of flower-visiting insects, but this is likely dependent on taxonomic group, spatial scale, weather and climatic conditions, and is particularly impacted by agricultural intensification. Here, we analyzed the impacts of both aspects of landscape heterogeneity and the role of climatic and weather conditions on pollinating insect communities in two economically important mass-flowering crops across Europe.Methods: Using a standardized approach, we collected data on the abundance of five insect groups (honey bees, bumble bees, other bees, hover flies and butterflies) in eight oilseed rape and eight apple orchard sites (in crops and adjacent crop margins), across eight European countries (128 sites in total) encompassing four biogeographic regions, and quantified habitat heterogeneity by calculating relevant landscape metrics for composition (proportion and diversity of land-use types) and configuration (the aggregation and isolation of land-use patches).Results: We found that flower-visiting insects responded to landscape and climate parameters in taxon- and crop-specific ways. For example, landscape diversity was positively correlated with honey bee and solitary bee abundance in oilseed rape fields, and hover fly abundance in apple orchards. In apple sites, the total abundance of all pollinators, and particularly bumble bees and solitary bees, decreased with an increasing proportion of orchards in the surrounding landscape. In oilseed rape sites, less-intensively managed habitats (i.e., woodland, grassland, meadows, and hedgerows) positively influenced all pollinators, particularly bumble bees and butterflies. Additionally, our data showed that daily and annual temperature, as well as annual precipitation and precipitation seasonality, affects the abundance of flower-visiting insects, although, again, these impacts appeared to be taxon- or crop-specific.Discussion: Thus, in the context of global change, our findings emphasize the importance of understanding the role of taxon-specific responses to both changes in land use and climate, to ensure continued delivery of pollination services to pollinator-dependent crops.

To provide a complete portrayal of the multiple factors negatively impacting insects in agricultural landscapes it is necessary to assess the concurrent incidence, magnitude, and interactions among multiple stressors over substantial biogeographical scales. Trans-national ecological field investigations with wide-ranging stakeholders typically encounter numerous challenges during the design planning stages, not least that the scientific soundness of a spatially replicated study design must account for the substantial geographic and climatic variation among distant sites. ‘PoshBee’ (Pan-European assessment, monitoring, and mitigation of Stressors on the Health of Bees) is a multi-partner transdisciplinary agroecological project established to investigate the suite of stressors typically encountered by pollinating insects in European agricultural landscapes. To do this, PoshBee established a network of 128 study sites across eight European countries and collected over 50 measurements and samples relating to the nutritional, toxicological, pathogenic, and landscape components of the bees’ environment. This paper describes the development process, rationale, and end-result of each aspect of the of the PoshBee field investigation. We describe the main issues and challenges encountered during the design stages and highlight a number of actions or processes that may benefit other multi-partner research consortia planning similar large-scale studies. It was soon identified that in a multi-component study design process, the development of interaction and communication networks involving all collaborators and stakeholders requires considerable time and resources. It was also necessary at each planning stage to be mindful of the needs and objectives of all stakeholders and partners, and further challenges inevitably arose when practical limitations, such as time restrictions and labour constraints, were superimposed upon prototype study designs. To promote clarity for all stakeholders, for each sub-component of the study, there should be a clear record of the rationale and reasoning that outlines how the final design transpired, what compromises were made, and how the requirements of different stakeholders were accomplished. Ultimately, multi-national agroecological field studies such as PoshBee benefit greatly from the involvement of diverse stakeholders and partners, ranging from field ecologists, project managers, policy legislators, mathematical modelers, and farmer organisations. While the execution of the study highlighted the advantages and benefits of large-scale transdisciplinary projects, the long planning period emphasized the need to formally describe a design framework that could facilitate the design process of future multi-partner collaborations.

Current global change substantially threatens pollinators, which directly impacts the pollination services underpinning the stability, structure and functioning of ecosystems. Amongst these threats, many synergistic drivers, such as habitat destruction and fragmentation, increasing use of agrochemicals, decreasing resource diversity, as well as climate change, are known to affect wild and managed bees. Therefore, reliable indicators for pollinator sensitivity to such threats are needed. Biological traits, such as phenotype (e.g. shape, size and asymmetry) and storage reserves (e.g. fat body size), are important pollinator traits linked to reproductive success, immunity, resilience and foraging efficiency and, therefore, could serve as valuable markers of bee health and pollination service potential. This data paper contains an extensive dataset of wing morphology and fat body content for the European honeybee (Apis mellifera) and the buff-tailed bumblebee (Bombus terrestris) sampled at 128 sites across eight European countries in landscape gradients dominated by two major bee-pollinated crops (apple and oilseed rape), before and after focal crop bloom and potential pesticide exposure. The dataset also includes environmental metrics of each sampling site, namely landscape structure and pesticide use. The data offer the opportunity to test whether variation in the phenotype and fat bodies of bees is structured by environmental factors and drivers of global change. Overall, the dataset provides valuable information to identify which environmental threats predominantly contribute to the modification of these traits.

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.