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.

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.

Spatio-temporal shifts in British wild bees in response to changing climate.

Climate plays a major role in determining where species occur, and when they are active throughout the year. In the face of a changing climate, many species are shifting their ranges poleward. Many species are also shifting their emergence phenology. Wild bees in Great Britain are susceptible to changes in climatic conditions but little is known about historic or potential future spatio-temporal trends of many species. This study utilized a sliding window approach to assess the impacts of climate on bee emergence dates, estimating the best temperature window for predicting emergence dates for 88 species of wild bees. Using a 'middle-of-the-road' (RCP 4.5) and 'worst-case' (RCP 8.5) climate scenario for the period 2070-2079, predictions of future emergence dates were made. In general, the best predicting climate window occurred in the 0-3 months preceding emergence. Across the 40 species that showed a shift in emergence dates in response to a climate window, the mean advance was 13.4 days under RCP 4.5 and 24.9 days under RCP 8.5. Species distribution models (SDMs) were used to predict suitable climate envelopes under historic (1980-1989), current (2010-2019) and future (2070-2079 under RCP 4.5 and RCP 8.5 scenarios) climate conditions. These models predict that the climate envelope for 92% of studied species has increased since the 1980s, and for 97% and 93% of species under RCP 4.5 and RCP 8.5 respectively, this is predicted to continue, due to extension of the northern range boundary. While any range changes will be moderated by habitat availability, it highlights that Great Britain will likely experience northward shifts of bee populations in the future. By combining spatial and temporal trends, this work provides an important step towards informing conservation measures suitable for future climates, directing how interventions can be provided in the right place at the right time.

Emerging threats and opportunities to managed bee species in European agricultural systems: a horizon scan.

Managed bee species provide essential pollination services that contribute to food security worldwide. However, managed bees face a diverse array of threats and anticipating these, and potential opportunities to reduce risks, is essential for the sustainable management of pollination services. We conducted a horizon scanning exercise with 20 experts from across Europe to identify emerging threats and opportunities for managed bees in European agricultural systems. An initial 63 issues were identified, and this was shortlisted to 21 issues through the horizon scanning process. These ranged from local landscape-level management to geopolitical issues on a continental and global scale across seven broad themes-Pesticides & pollutants, Technology, Management practices, Predators & parasites, Environmental stressors, Crop modification, and Political & trade influences. While we conducted this horizon scan within a European context, the opportunities and threats identified will likely be relevant to other regions. A renewed research and policy focus, especially on the highest-ranking issues, is required to maximise the value of these opportunities and mitigate threats to maintain sustainable and healthy managed bee pollinators within agricultural systems.

Neither sulfoxaflor, Crithidia bombi, nor their combination impact bumble bee colony development or field bean pollination.

Many pollinators, including bumble bees, are in decline. Such declines are known to be driven by a number of interacting factors. Decreases in bee populations may also negatively impact the key ecosystem service, pollination, that they provide. Pesticides and parasites are often cited as two of the drivers of bee declines, particularly as they have previously been found to interact with one another to the detriment of bee health. Here we test the effects of an insecticide, sulfoxaflor, and a highly prevalent bumble bee parasite, Crithidia bombi, on the bumble bee Bombus terrestris. After exposing colonies to realistic doses of either sulfoxaflor and/or Crithidia bombi in a fully crossed experiment, colonies were allowed to forage on field beans in outdoor exclusion cages. Foraging performance was monitored, and the impacts on fruit set were recorded. We found no effect of either stressor, or their interaction, on the pollination services they provide to field beans, either at an individual level or a whole colony level. Further, there was no impact of any treatment, in any metric, on colony development. Our results contrast with prior findings that similar insecticides (neonicotinoids) impact pollination services, and that sulfoxaflor impacts colony development, potentially suggesting that sulfoxaflor is a less harmful compound to bee health than neonicotinoids insecticides.

Functional and Behavioral Responses of the Natural Enemy Anthocoris nemoralis to Cacopsylla pyri, at Different Temperatures.

Anthocoris nemoralis is the dominant predator of pear sucker (Cacopsylla pyri) in the UK. Anthocoris nemoralis migrates into orchards in spring or is introduced as a biocontrol agent, reaching peak population levels in July-August, contributing to effective control of summer pear sucker populations. However, due to temperature dependent development and metabolism there are concerns that C. pyri populations or feeding rates may increase due to changing climatic conditions. Thus, how A. nemoralis responds to temperature, impacts its ability as a biocontrol agent. Functional response assays, monitoring attack rate and handling time of A. nemoralis and behavioral assays, using Ethovision tracking software occurred, to assess the impact of temperature on predation. Experiments were conducted at current and future July-August mean temperatures, predicted using RCP4.5 and RCP8.5 (medium and high, representative concentration pathway) emissions scenarios, using 2018 UK Climate Projections (UKCP18). All treatments demonstrated a Type II functional response, with female anthocorids demonstrating shorter handling times and higher attack rates than males. Males showed longer prey handling times at 18 °C compared to 23 °C and more time was spent active at lower temperatures for both sexes. Females did not show significant differences in attack rate or handling time in response to temperature. Overall prey consumption was also not significantly affected by temperature for either sex. This study suggests that anthocorids are likely to remain effective natural enemies under future predicted temperatures, due to non-significant differences in prey consumption. Supplementary Information: The online version contains supplementary material available at 10.1007/s10905-023-09836-5.

Climate-driven phenological shifts in emergence dates of British bees.

Climate change has a diverse range of impacts on wild bees, including their phenology or timing of life history events. Climate-driven phenological shifts can not only impact individuals at species level but also threaten the vital pollination service that wild bees provide to both wild plants and cultivated crops. Despite their involvement in pollination, for most bee species, especially in Great Britain, little is known about phenological shifts. This study makes use of 40 years of presence-only data for 88 species of wild bees to analyse shifts in emergence dates, both over time and in relation to temperature. The analyses reveal widespread advances in emergence dates of British wild bees, at an average rate of 0.40 ± 0.02 days per year since 1980 across all species in the study data set. Temperature is a key driver of this shift, with an average advance of 6.5 ± 0.2 days per 1°C warming. For change in emergence dates both over time and in relation to temperature, there was significant species-specific variation, with 14 species showing significant advances over time and 67 showing significant advances in relation to temperature. Traits did not appear to explain variation in individual species' responses, with overwintering stage, lecty, emergence period and voltinism considered as possible explanatory traits. Pairwise comparisons showed no differences in sensitivity of emergence dates to increasing temperature between trait groups (groups of species which share all four traits) that differed by only one trait. These results highlight not only a direct impact of temperature on the phenology of wild bees themselves but also the species-specific shifts highlight a possible impact on the temporal structure of bee communities and the pollination networks for which the wild bees are so crucial.

Landscape-scale drivers of pollinator communities may depend on land-use configuration.

Research into pollinators in managed landscapes has recently combined approaches of pollination ecology and landscape ecology, because key stressors are likely to interact across wide areas. While laboratory and field experiments are valuable for furthering understanding, studies are required to investigate the interacting drivers of pollinator health and diversity across a broader range of landscapes and a wider array of taxa. Here, we use a network of 96 study landscapes in six topographically diverse regions of Britain, to test the combined importance of honeybee density, insecticide loadings, floral resource availability and habitat diversity to pollinator communities. We also explore the interactions between these drivers and the cover and proximity of semi-natural habitat. We found that among our four drivers, only honeybee density was positively related to wild pollinator abundance and diversity, and the positive association between abundance and floral resources depended on insecticide loadings and habitat diversity. By contrast, our exploratory models including habitat composition metrics revealed a complex suite of interactive effects. These results demonstrate that improving pollinator community composition and health is unlikely to be achieved with general resource enhancements only. Rather, local land-use context should be considered in fine-tuning pollinator management and conservation. This article is part of the theme issue 'Natural processes influencing pollinator health: from chemistry to landscapes'.

Determining the role of climate change in India's past forest loss.

Tropical forests in India have declined at an alarming rate over the past century, with extensive literature focusing on the high contributions of agricultural expansions to deforestation, while the effects of climate change have largely been overlooked. Climate change effects, such as increasing temperatures, drought and flooding, have already occurred, and are projected to worsen. Climate velocity, a metric that accounts for spatial heterogeneity in climate, can help identify contiguous areas under greater climate stress and potential climate refuges in addition to traditional temporal trends. Here, we examined the relative contribution of climate changes to forest loss in India during the period 2001-2018, at two spatial (regional and national) and two temporal (seasonal and annual) scales. This includes, for the first time, a characterization of climate velocity in the country. Our findings show that annual forest loss increased substantially over the 17-year period examined (2001-2018), with the majority of forest loss occurring in the Northeast region. Decreases in temporal trends of temperature and precipitation were most associated with forest losses, but there was large spatial and seasonal variation in the relationship. In every region except the Northeast, forest losses were correlated with faster velocities of at least one climate variable but overlapping areas of high velocities were rare. Our findings indicate that climate changes have played an important role in India's past forest loss, but likely remain secondary to other factors at present. We stress concern for climates velocities recorded in the country, reaching 97 km year-1 , and highlight that understanding the different regional and seasonal relationships between climatic conditions and forest distributions will be key to effective protection of the country's remaining forests as climate change accelerates.

Communicating carabids: Engaging farmers to encourage uptake of integrated pest management.

BACKGROUND: Natural enemy pest control is becoming more desirable as restrictions increase on pesticide use. Carabid beetles are proven agents of natural-enemy pest control (NPC), controlling pests and weeds in crop areas. Agro-ecological measures can be effective for boosting carabid abundance and associated NPC, but the benefits of specific interventions to production are seldom communicated to farmers. We explore pathways to improved NPC by engaging farmers and increasing knowledge about farm management practices (FMPs) beneficial to carabids using engagement materials. We used a questionnaire to measure awareness, beliefs and attitudes to carabids and analysed these within a framework of the Theory of Planned Behaviour (TPB), relative to a control group. RESULTS: We found awareness of carabid predation to be associated with beliefs of pest and weed control efficacy. Within the framework of TPB, we found that current implementation of FMPs was higher if farmers perceived them to be both important for carabids and easy to implement. This was also true for future intention to implement, yet the perceived importance was influenced by engagement materials. Field margins/buffer strips and beetle banks (16% and 13% of responses) were the most favoured by farmers as interventions for carabids. CONCLUSION: The TPB is a valuable tool with which to examine internal elements of farmer behaviour. In this study self-selected participants were influenced by online engagement in a single intervention, proving this approach has the potential to change behaviour. Our results are evidence for the effectiveness of raising awareness of NPC to change attitudes and increase uptake of sustainable practices.

Rapid assessment of insect pollination services to inform decision-making.

Pollinator declines have prompted efforts to assess how land-use change affects insect pollinators and pollination services in agricultural landscapes. Yet many tools to measure insect pollination services require substantial landscape-scale data and technical expertise. In expert workshops, 3 straightforward methods (desk-based method, field survey, and empirical manipulation with exclusion experiments) for rapid insect pollination assessment at site scale were developed to provide an adaptable framework that is accessible to nonspecialist with limited resources. These methods were designed for TESSA (Toolkit for Ecosystem Service Site-Based Assessment) and allow comparative assessment of pollination services at a site of conservation interest and in its most plausible alternative state (e.g., converted to agricultural land). We applied the methods at a nature reserve in the United Kingdom to estimate the value of insect pollination services provided by the reserve. The economic value of pollination services provided by the reserve ranged from US$6163 to US$11,546/year. The conversion of the reserve to arable land would provide no insect pollination services and a net annual benefit from insect-pollinated crop production of approximately $1542/year (US$24∙ha-1 ∙year-1 ). The methods had wide applicability and were readily adapted to different insect-pollinated crops: rape (Brassica napus) and beans (Vicia faba) crops. All methods were rapidly employed under a low budget. The relatively less robust methods that required fewer resources yielded higher estimates of annual insect pollination benefit.

Diversidad y Conservación de Gasterópodos Subterráneos de Agua Dulce en los Estados Unidos y en México Resumen Las declinaciones de los polinizadores han impulsado los esfuerzos por evaluar cómo el cambio del uso de suelo afecta a los insectos polinizadores y los servicios de polinización en los paisajes agrícolas. Aun así, muchas de las herramientas para medir los servicios de los insectos polinizadores requieren datos sustanciales a escala de paisaje y el conocimiento de expertos. Desarrollamos tres métodos sencillos (método de gabinete, censo de campo y manipulación empírica con experimentos de exclusión) durante algunos talleres de expertos para la evaluación rápida de la polinización por insectos a escala de sitio con el objetivo de proporcionar un marco de trabajo adaptable y accesible para quienes no son especialistas y cuentan con recursos limitados. Estos métodos fueron diseñados para TESSA (Toolkit for Ecosystem Service Site-Based Assessment, en inglés) y permiten la evaluación comparativa de los servicios de polinización en los sitios de interés para la conservación y su estado alternativo más plausible (p. ej.: convertido a suelo agrícola). Aplicamos los métodos en una reserva natural del Reino Unido para estimar el valor de los servicios de polinización por insectos que proporciona la reserva. El valor económico de los servicios de polinización que proporciona la reserva varió desde US$6,163 a US$11,546 al año-1 . La conversión de la reserva a suelo arable no proporcionaría servicios de polinización por insectos, pero sí un beneficio anual neto a partir de la producción de cultivos polinizados por insectos de aproximadamente $1,542 al año-1 (US$24 ha-1 año-1 ). Los métodos tuvieron una aplicabilidad generalizada y estaban ya adaptados a los diferentes cultivos polinizados por insectos: cultivos de colza (Brassica napus) y habas (Vicia faba). Todos los métodos pudieron usarse con bajo presupuesto. Los métodos relativamente menos robustos que requirieron menos recursos produjeron estimados más elevados del beneficio anual de la polinización por insectos.

Opportunities to reduce pollination deficits and address production shortfalls in an important insect-pollinated crop.

Pollinators face multiple pressures and there is evidence of populations in decline. As demand for insect-pollinated crops increases, crop production is threatened by shortfalls in pollination services. Understanding the extent of current yield deficits due to pollination and identifying opportunities to protect or improve crop yield and quality through pollination management is therefore of international importance. To explore the extent of "pollination deficits," where maximum yield is not being achieved due to insufficient pollination, we used an extensive dataset on a globally important crop, apples. We quantified how these deficits vary between orchards and countries and we compared "pollinator dependence" across different apple varieties. We found evidence of pollination deficits and, in some cases, risks of overpollination were even apparent for which fruit quality could be reduced by too much pollination. In almost all regions studied we found some orchards performing significantly better than others in terms of avoiding a pollination deficit and crop yield shortfalls due to suboptimal pollination. This represents an opportunity to improve production through better pollinator and crop management. Our findings also demonstrated that pollinator dependence varies considerably between apple varieties in terms of fruit number and fruit quality. We propose that assessments of pollination service and deficits in crops can be used to quantify supply and demand for pollinators and help to target local management to address deficits although crop variety has a strong influence on the role of pollinators.

A global-scale expert assessment of drivers and risks associated with pollinator decline.

Pollinator decline has attracted global attention and substantial efforts are underway to respond through national pollinator strategies and action plans. These policy responses require clarity on what is driving pollinator decline and what risks it generates for society in different parts of the world. Using a formal expert elicitation process, we evaluated the relative regional and global importance of eight drivers of pollinator decline and ten consequent risks to human well-being. Our results indicate that global policy responses should focus on reducing pressure from changes in land cover and configuration, land management and pesticides, as these were considered very important drivers in most regions. We quantify how the importance of drivers and risks from pollinator decline, differ among regions. For example, losing access to managed pollinators was considered a serious risk only for people in North America, whereas yield instability in pollinator-dependent crops was classed as a serious or high risk in four regions but only a moderate risk in Europe and North America. Overall, perceived risks were substantially higher in the Global South. Despite extensive research on pollinator decline, our analysis reveals considerable scientific uncertainty about what this means for human society.

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.

Combined effects of agrochemicals and ecosystem services on crop yield across Europe.

Simultaneously enhancing ecosystem services provided by biodiversity below and above ground is recommended to reduce dependence on chemical pesticides and mineral fertilisers in agriculture. However, consequences for crop yield have been poorly evaluated. Above ground, increased landscape complexity is assumed to enhance biological pest control, whereas below ground, soil organic carbon is a proxy for several yield-supporting services. In a field experiment replicated in 114 fields across Europe, we found that fertilisation had the strongest positive effect on yield, but hindered simultaneous harnessing of below- and above-ground ecosystem services. We furthermore show that enhancing natural enemies and pest control through increasing landscape complexity can prove disappointing in fields with low soil services or in intensively cropped regions. Thus, understanding ecological interdependences between land use, ecosystem services and yield is necessary to promote more environmentally friendly farming by identifying situations where ecosystem services are maximised and agrochemical inputs can be reduced.

The impact of over 80 years of land cover changes on bee and wasp pollinator communities in England.

Change in land cover is thought to be one of the key drivers of pollinator declines, and yet there is a dearth of studies exploring the relationships between historical changes in land cover and shifts in pollinator communities. Here, we explore, for the first time, land cover changes in England over more than 80 years, and relate them to concurrent shifts in bee and wasp species richness and community composition. Using historical data from 14 sites across four counties, we quantify the key land cover changes within and around these sites and estimate the changes in richness and composition of pollinators. Land cover changes within sites, as well as changes within a 1 km radius outside the sites, have significant effects on richness and composition of bee and wasp species, with changes in edge habitats between major land classes also having a key influence. Our results highlight not just the land cover changes that may be detrimental to pollinator communities, but also provide an insight into how increases in habitat diversity may benefit species diversity, and could thus help inform policy and practice for future land management.

Climate change and the risks associated with delayed breeding in a tropical wild bird population.

There is growing evidence of changes in the timing of important ecological events, such as flowering in plants and reproduction in animals, in response to climate change, with implications for population decline and biodiversity loss. Recent work has shown that the timing of breeding in wild birds is changing in response to climate change partly because individuals are remarkably flexible in their timing of breeding. Despite this work, our understanding of these processes in wild populations remains very limited and biased towards species from temperate regions. Here, we report the response to changing climate in a tropical wild bird population using a long-term dataset on a formerly critically endangered island endemic, the Mauritius kestrel. We show that the frequency of spring rainfall affects the timing of breeding, with birds breeding later in wetter springs. Delays in breeding have consequences in terms of reduced reproductive success as birds get exposed to risks associated with adverse climatic conditions later on in the breeding season, which reduce nesting success. These results, combined with the fact that frequency of spring rainfall has increased by about 60 per cent in our study area since 1962, imply that climate change is exposing birds to the stochastic risks of late reproduction by causing them to start breeding relatively late in the season.