Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success

1. Pollinating insects provide crucial and economically important ecosystem services to crops and wild plants, but pollinators, particularly bees, are globally declining as a result of various driving factors, including the prevalent use of pesticides for crop protection. Sublethal pesticide exposure negatively impacts numerous pollinator lifehistory traits, but its influence on reproductive success remains largely unknown. Such information is pivotal, however, to our understanding of the long-term effects on population dynamics. 2 We investigated the influence of field-realistic trace residues of the routinely used neonicotinoid insecticides thiamethoxam and clothianidin in nectar substitutes on the entire life-time fitness performance of the red mason bee Osmia bicornis. 3 We show that chronic, dietary neonicotinoid exposure has severe detrimental effects on solitary bee reproductive output. Neonicotinoids did not affect adult bee mortality; however, monitoring of fully controlled experimental populations revealed that sublethal exposure resulted in almost 50% reduced total offspring production and a significantly male-biased offspring sex ratio. 4 Our data add to the accumulating evidence indicating that sublethal neonicotinoid effects on non-Apis pollinators are expressed most strongly in a rather complex, fitness-related context. Consequently, to fully mitigate long-term impacts on pollinator population dynamics, present pesticide risk assessments need to be expanded to include whole life-cycle fitness estimates, as demonstrated in the present study using O. bicornis as a model.

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.

Local and landscape effects on bee functional guilds in pigeon pea crops in Kenya

Pollinators face many challenges within agricultural systems due to landscape changes and intensification which can affect resource availability that can impact pollination services. This paper examines pigeon pea pollination and considers how landscape context and agricultural intensification in terms of pesticide use affects the abundance of bees characterized by species guilds on crops. The study was conducted on six paired farms across a gradient of habitat complexity based on the distance of each farm from adjacent semi-natural vegetation in Kibwezi Sub-county, Kenya. The study found that farms which do not use insecticides in farm management, but are in close proximity to natural habitat have greater bee guild abundance, but at further distances, overall abundance is reduced with or without insecticide use. At 1 km landscape radius, the complexity of habitats but not patch size had a positive impact on the abundance of cavity nesting bees and mason bees, which can be attributed to the interspersion of the small-holder farms with semi-natural habitats across the landscapes producing mosaics of heterogeneous habitats. The study revealed the strongest relationships between fruit set and bee abundance to be with the carpenter bee, social bee and solitary bee guilds, which are among the most abundant bees visiting pigeon pea flowers in this system. Our findings provide the foundation for conservation efforts by identifying which bee guilds pollinated pigeon peas. From this study, we suggest managing the floral and nesting resources that would best support the most abundant crop pollinators, and also reducing insecticide application to the crop.

When bookkeepers become beekeepers: why bee accountability

Accounting for biodiversity has received increasing attention from the academic accounting community in recent years. Despite a stream of research investigating the quality and quantity of biodiversity reporting in general, no academic research has focused on reporting related to one specific species. This paper explores the quality and quantity of corporate disclosures relating to bees. Society is becoming increasingly concerned about the accelerating fall in bee populations around the world. Colony Collapse Disorder has been spreading through global bee populations since 2006, decimating commercial hives. Concerns are fuelled by fears that pollinators may become extinct which would have dire consequences for the majority of world food production, leaving human pollination, at immense cost, the only alternative. On the basis of these fears, companies as well as other organisations, have started to establish programmes aimed at rejuvenating global bee populations. In this paper we explore the bee-related disclosures provided by a large selection of UK listed companies. We assess the extent to which companies believe they have a role to play in enhancing and protecting bee populations. Further we consider whether corporate accountability in this area derives solely from a business case or whether there is a deeper societal connection with bees as a species which is encouraging companies to protect their survival. The paper investigates the historical and philosophical connection between bees and human beings, for example the ways industrial production has been likened to honey production. We draw parallels between bees and human industrial organisation as well as between the role and responsibilities of the bookkeeper and the beekeeper.

The effects of diesel exhaust pollution on floral volatiles and the consequences for honey bee olfaction

There is growing evidence of a substantial decline in pollinators within Europe and North America, most likely caused by multiple factors such as diseases, poor nutrition, habitat loss, insecticides, and environmental pollution. Diesel exhaust could be a contributing factor to this decline, since we found that diesel exhaust rapidly degrades floral volatiles, which honey bees require for flower recognition. In this study, we exposed eight of the most common floral volatiles to diesel exhaust in order to investigate whether it can affect volatile mediated plant-pollinator interaction. Exposure to diesel exhaust altered the blend of common flower volatiles significantly: myrcene was considerably reduced, β-ocimene became undetectable, and β-caryophyllene was transformed into its cis-isomer isocaryophyllene. Proboscis extension response (PER) assays showed that the alterations of the blend reduced the ability of honey bees to recognize it. The chemically reactive nitrogen oxides fraction of diesel exhaust gas was identified as capable of causing degradation of floral volatiles.

Testing projected wild bee distributions in agricultural habitats: predictive power depends on species traits and habitat type

Species distribution models (SDM) are increasingly used to understand the factors that regulate variation in biodiversity patterns and to help plan conservation strategies. However, these models are rarely validated with independently collected data and it is unclear whether SDM performance is maintained across distinct habitats and for species with different functional traits. Highly mobile species, such as bees, can be particularly challenging to model. Here, we use independent sets of occurrence data collected systematically in several agricultural habitats to test how the predictive performance of SDMs for wild bee species depends on species traits, habitat type, and sampling technique. We used a species distribution modeling approach parametrized for the Netherlands, with presence records from 1990 to 2010 for 193 Dutch wild bees. For each species, we built a Maxent model based on 13 climate and landscape variables. We tested the predictive performance of the SDMs with independent datasets collected from orchards and arable fields across the Netherlands from 2010 to 2013, using transect surveys or pan traps. Model predictive performance depended on species traits and habitat type. Occurrence of bee species specialized in habitat and diet was better predicted than generalist bees. Predictions of habitat suitability were also more precise for habitats that are temporally more stable (orchards) than for habitats that suffer regular alterations (arable), particularly for small, solitary bees. As a conservation tool, SDMs are best suited to modeling rarer, specialist species than more generalist and will work best in long-term stable habitats. The variability of complex, short-term habitats is difficult to capture in such models and historical land use generally has low thematic resolution. To improve SDMs’ usefulness, models require explanatory variables and collection data that include detailed landscape characteristics, for example, variability of crops and flower availability. Additionally, testing SDMs with field surveys should involve multiple collection techniques.

Diversity in a honey bee pathogen: first report of a third master variant of the Deformed Wing Virus quasispecies

Treatment of emerging RNA viruses is hampered by the high mutation and replication rates that enable these viruses to operate as a quasispecies. Declining honey bee populations have been attributed to the ectoparasitic mite Varroa destructor and its affiliation with Deformed Wing Virus (DWV). In the current study we use next-generation sequencing to investigate the DWV quasispecies in an apiary known to suffer from overwintering colony losses. We show that the DWV species complex is made up of three master variants. Our results indicate that a new DWV Type C variant is distinct from the previously described types A and B, but together they form a distinct clade compared with other members of the Iflaviridae. The molecular clock estimation predicts that Type C diverged from the other variants ~319 years ago. The discovery of a new master variant of DWV has important implications for the positive identification of the true pathogen within global honey bee populations.

Non-bee insects are important contributors to global crop pollination

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

High-throughput monitoring of wild bee diversity and abundance via mitogenomics

1. Bee populations and other pollinators face multiple, synergistically acting threats, which have led to population declines, loss of local species richness and pollination services, and extinctions. However, our understanding of the degree, distribution and causes of declines is patchy, in part due to inadequate monitoring systems, with the challenge of taxonomic identification posing a major logistical barrier. Pollinator conservation would benefit from a high-throughput identification pipeline. 2. We show that the metagenomic mining and resequencing of mitochondrial genomes (mitogenomics) can be applied successfully to bulk samples of wild bees. We assembled the mitogenomes of 48 UK bee species and then shotgun-sequenced total DNA extracted from 204 whole bees that had been collected in 10 pan-trap samples from farms in England and been identified morphologically to 33 species. Each sample data set was mapped against the 48 reference mitogenomes. 3. The morphological and mitogenomic data sets were highly congruent. Out of 63 total species detections in the morphological data set, the mitogenomic data set made 59 correct detections (93�7% detection rate) and detected six more species (putative false positives). Direct inspection and an analysis with species-specific primers suggested that these putative false positives were most likely due to incorrect morphological IDs. Read frequency significantly predicted species biomass frequency (R2 = 24�9%). Species lists, biomass frequencies, extrapolated species richness and community structure were recovered with less error than in a metabarcoding pipeline. 4. Mitogenomics automates the onerous task of taxonomic identification, even for cryptic species, allowing the tracking of changes in species richness and istributions. A mitogenomic pipeline should thus be able to contain costs, maintain consistently high-quality data over long time series, incorporate retrospective taxonomic revisions and provide an auditable evidence trail. Mitogenomic data sets also provide estimates of species counts within samples and thus have potential for tracking population trajectories.

Dispersal capacity and diet breadth modify the response of wild bees to habitat loss

Habitat loss poses a major threat to biodiversity, and species-specific extinction risks are inextricably linked to life-history characteristics. This relationship is still poorly documented for many functionally important taxa, and at larger continental scales. With data from five replicated field studies from three countries, we examined how species richness of wild bees varies with habitat patch size. We hypothesized that the form of this relationship is affected by body size, degree of host plant specialization and sociality. Across all species, we found a positive species–area slope (z ¼ 0.19), and species traits modified this relationship. Large-bodied generalists had a lower z value than small generalists. Contrary to predictions, small specialists had similar or slightly lower z value compared with large specialists, and small generalists also tended to be more strongly affected by habitat loss as compared with small specialists. Social bees were negatively affected by habitat loss (z ¼ 0.11) irrespective of body size. We conclude that habitat loss leads to clear shifts in the species composition of wild bee communities.

Impacts of a pesticide on pollinator species richness at different spatial scales

Pesticides are an important potential cause of biodiversity and pollinator decline. Little is known about the impacts of pesticides on wild pollinators in the field. Insect pollinators were sampled in an agricultural system in Italy with the aim of detecting the impacts of pesticide use. The insecticide fenitrothion was over 150 times greater in toxicity than other pesticides used in the area, so sampling was set up around its application. Species richness of wild bees, bumblebees and butterflies were sampled at three spatial scales to assess responses to pesticide application: (i) the ‘field’ scale along pesticide drift gradients; (ii) the ‘landscape’ scale sampling in different crops within the area and (iii) the ‘regional’ scale comparing two river basins with contrasting agricultural intensity. At the field scale, the interaction between the application regime of the insecticide and the point in the season was important for species richness. Wild bee species richness appeared to be unaffected by one insecticide application, but declined after two and three applications. At the landscape scale, the species richness of wild bees declined in vine fields where the insecticide was applied, but did not decline in maize or uncultivated fields. At the regional scale, lower bumblebee and butterfly species richness was found in the more intensively farmed basin with higher pesticide loads. Our results suggest that wild bees are an insect pollinator group at particular risk from pesticide use. Further investigation is needed on how the type, quantity and timing of pesticide application impacts pollinators.

Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands

Despite widespread concern about declines in pollination services, little is known about the patterns of change in most pollinator assemblages. By studying bee and hoverfly assemblages in Britain and the Netherlands, we found evidence of declines (pre- versus post-1980) in local bee diversity in both countries; however, divergent trends were observed in hoverflies. Depending on the assemblage and location, pollinator declines were most frequent in habitat and flower specialists, in univoltine species, and/or in nonmigrants. In conjunction with this evidence, outcrossing plant species that are reliant on the declining pollinators have themselves declined relative to other plant species. Taken together, these findings strongly suggest a causal connection between local extinctions of functionally linked plant and pollinator species.

Conservation ecology of bees: populations, species and communities

Recent concerns regarding the decline of plant and pollinator species, and the impact on ecosystem functioning, has focused attention on the local and global threats to bee diversity. As evidence for bee declines is now accumulating from over broad taxonomic and geographic scales, we review the role of ecology in bee conservation at the levels of species, populations and communities. Bee populations and communities are typified by considerable spatiotemporal variation; whereby autecological traits, population size and growth rate, and plant-pollinator network architecture all play a role in their vulnerability to extinction. As contemporary insect conservation management is broadly based on species- and habitat-targeted approaches, ecological data will be central to integrating management strategies into a broader, landscape scale of dynamic, interconnected habitats capable of delivering bee conservation in the context of global environmental change.

Plant-pollinator biodiversity and pollination services in a complex Mediterranean landscape

Mediterranean landscapes comprise a complex mosaic of different habitats that vary in the diversity of their floral communities, pollinator communities and pollination services. Using the Greek Island of Lesvos as a model system, we assess the biodiversity value of six common habitats and measure ecosystemic 'health' using pollen grain deposition in three core flowering plants as a measure of pollination services. Three fire-driven habitats were assessed: freshly burnt areas, fully regenerated pine forests and intermediate age scrub; in addition we examined oak woodlands, actively managed olive groves and groves that had been abandoned from agriculture. Oak woodlands, pine forests and managed olive groves had the highest diversity of bees. The habitat characteristics responsible for structuring bee communities were: floral diversity, floral abundance, nectar energy availability and the variety of nectar resources present. Pollination services in two of our plant species, which were pollinated by a limited sub-set of the pollinator community, indicated that pollination levels were highest in the burnt and mature pine habitats. The third species, which was open to all flower visitors, indicated that oak woodlands had the highest levels of pollination from generalist species. Pollination was always more effective in managed olive groves than in abandoned groves. However, the two most common species of bee, the honeybee and a bumblebee, were not the primary pollinators within these habitats. We conclude that the three habitats of greatest overall value for plant-pollinator communities and provision of the healthiest pollination services are pine forests, oak woodland and managed olive groves. We indicate how the highest value habitats may be maintained in a complex landscape to safeguard and enhance pollination function within these habitats and potentially in adjoining agricultural areas. (c) 2005 Elsevier Ltd. All rights reserved.

Declines of managed honey bees and beekeepers in Europe

Growing evidence indicates that European managed honey bees are in decline, but information for Europe remains patchy and localized. Here we compile data from 18 European countries to assess trends in the number of honey bee colonies and beekeepers between 1965 and 2005. We found consistent declines in colony numbers in central European countries and some increases in Mediterranean countries. Beekeeper numbers have declined in all of the European countries examined. Our data support the view that honey bees are in decline at least in some regions, which is probably closely linked to the decreasing number of beekeepers. Our data on colony numbers and beekeepers must, however, be interpreted with caution due to different approaches and socioeconomic factors in the various countries, thereby limiting their comparability. We therefore make specific recommendations for standardized methodologies to be adopted at the national and global level to assist in the future monitoring of honey bees.