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.

Diversity for resilience : multi-scale application of agro-ecology

The integration of ecological principles into agricultural systems presents major opportunities for spreading risk at the crop and farm scale. This paper presents mechanisms by which diversity at several scales within the farming system can increase the stability of production. Diversity of above- and below-ground biota, but also genetic and phenotypic diversity within crops, has an essential role in safeguarding farm production. Novel mixtures of legume-grass leys have been shown to potentially provide significant benefits for pollinator and decomposer ecosystem services but to realise the greatest improvements carefully tailored farm management is needed such as mowing or grazing time, and the type and depth of cutivation. Complex farmland landscapes such as agroforestry systems have the potential to support pollinator abundance and diversity and spread risk across production enterprises. At the crop level, early results indicate that the vulnerability of pollen development, flowering and early grain set to abiotic stress can be ameliorated by managing flowering time through genotypic selection, and through the buffering effects of pollinators. Finally, the risk of sub-optimal quality in cereals can be mitigated through integration of near isogenic lines selected to escape specific abiotic stress events. We conclude that genotypic, phenotypic and community diversity can all be increased at multiple scales to enhance resilience in agricultural systems.

Molecular species delimitation of a symbiotic fig-pollinating wasp species complex reveals extreme deviation from reciprocal partner specificity

Background: Symbiotic relationships have contributed to major evolutionary innovations, the maintenance of fundamental ecosystem functions, and the generation and maintenance of biodiversity. However, the exact nature of host/symbiont associations, which has important consequences for their dynamics, is often poorly known due to limited understanding of symbiont taxonomy and species diversity. Among classical symbioses, figs and their pollinating wasps constitute a highly diverse keystone resource in tropical forest and savannah environments. Historically, they were considered to exemplify extreme reciprocal partner specificity (one-to-one host-symbiont species relationships), but recent work has revealed several more complex cases. However, there is a striking lack of studies with the specific aims of assessing symbiont diversity and how this varies across the geographic range of the host. Results: Here, we use molecular methods to investigate cryptic diversity in the pollinating wasps of a widespread Australian fig species. Standard barcoding genes and methods were not conclusive, but incorporation of phylogenetic analyses and a recently developed nuclear barcoding gene (ITS2), gave strong support for five pollinator species. Each pollinator species was most common in a different geographic region, emphasising the importance of wide geographic sampling to uncover diversity, and the scope for divergence in coevolutionary trajectories across the host plant range. In addition, most regions had multiple coexisting pollinators, raising the question of how they coexist in apparently similar or identical resource niches. Conclusion: Our study offers a striking example of extreme deviation from reciprocal partner specificity over the full geographical range of a fig-wasp system. It also suggests that superficially identical species may be able to co-exist in a mutualistic setting albeit at different frequencies in relation to their fig host’s range. We show that comprehensive sampling and molecular taxonomic techniques may be required to uncover the true structure of cryptic biodiversity underpinning intimate ecological interactions.

An evidence-based review on the likely economic and environmental impact of genetically modified cereals and oilseeds for UK agriculture

An evidence-based review of the potential impact that the introduction of genetically-modified (GM) cereal and oilseed crops could have for the UK was carried out. The inter-disciplinary research project addressed the key research questions using scenarios for the uptake, or not, of GM technologies. This was followed by an extensive literature review, stakeholder consultation and financial modelling. The world area of canola, oilseed rape (OSR) low in both erucic acid in the oil and glucosinolates in the meal, was 34M ha in 2012 of which 27% was GM; Canada is the lead producer but it is also grown in the USA, Australia and Chile. Farm level effects of adopting GM OSR include: lower production costs; higher yields and profits; and ease of farm management. Growing GM OSR instead of conventional OSR reduces both herbicide usage and environmental impact. Some 170M ha of maize was grown in the world in 2011 of which 28% was GM; the main producers are the USA, China and Brazil. Spain is the main EU producer of GM maize although it is also grown widely in Portugal. Insect resistant (IR) and herbicide tolerant (HT) are the GM maize traits currently available commercially. Farm level benefits of adopting GM maize are lower costs of production through reduced use of pesticides and higher profits. GM maize adoption results in less pesticide usage than on conventional counterpart crops leading to less residues in food and animal feed and allowing increasing diversity of bees and other pollinators. In the EU, well-tried coexistence measures for growing GM crops in the proximity of conventional crops have avoided gene flow issues. Scientific evidence so far seems to indicate that there has been no environmental damage from growing GM crops. They may possibly even be beneficial to the environment as they result in less pesticides and herbicides being applied and improved carbon sequestration from less tillage. A review of work on GM cereals relevant for the UK found input trait work on: herbicide and pathogen tolerance; abiotic stress such as from drought or salinity; and yield traits under different field conditions. For output traits, work has mainly focussed on modifying the nutritional components of cereals and in connection with various enzymes, diagnostics and vaccines. Scrutiny of applications submitted for field trial testing of GM cereals found around 9000 applications in the USA, 15 in Australia and 10 in the EU since 1996. There have also been many patent applications and granted patents for GM cereals in the USA for both input and output traits;an indication of the scale of such work is the fact that in a 6 week period in the spring of 2013, 12 patents were granted relating to GM cereals. A dynamic financial model has enabled us to better understand and examine the likely performance of Bt maize and HT OSR for the south of the UK, if cultivation is permitted in the future. It was found that for continuous growing of Bt maize and HT OSR, unless there was pest pressure for the former and weed pressure for the latter, the seed premia and likely coexistence costs for a buffer zone between other crops would reduce the financial returns for the GM crops compared with their conventional counterparts. When modelling HT OSR in a four crop rotation, it was found that gross margins increased significantly at the higher levels of such pest or weed pressure, particularly for farm businesses with larger fields where coexistence costs would be scaled down. The impact of the supply of UK-produced GM crops on the wider supply chain was examined through an extensive literature review and widespread stakeholder consultation with the feed supply chain. The animal feed sector would benefit from cheaper supplies of raw materials if GM crops were grown and, in the future, they might also benefit from crops with enhanced nutritional profile (such as having higher protein levels) becoming available. This would also be beneficial to livestock producers enabling lower production costs and higher margins. Whilst coexistence measures would result in increased costs, it is unlikely that these would cause substantial changes in the feed chain structure. Retailers were not concerned about a future increase in the amount of animal feed coming from GM crops. To conclude, we (the project team) feel that the adoption of currently available and appropriate GM crops in the UK in the years ahead would benefit farmers, consumers and the feed chain without causing environmental damage. Furthermore, unless British farmers are allowed to grow GM crops in the future, the competitiveness of farming in the UK is likely to decline relative to that globally.

A stated preference valuation of the non-market benefits of pollination services in the UK

Using a choice experiment survey this study examines the UK public's willingness to pay to conserve insect pollinators in relation to the levels of two pollination service benefits: maintaining local produce supplies and the aesthetic benefits of diverse wildflower assemblages. Willingness to pay was estimated using a Bayesian mixed logit with two contrasting controls for attribute non-attendance, exclusion and shrinkage. The results suggest that the UK public have an extremely strong preference to avoid a status quo scenario where pollinator populations and pollination services decline. Total willingness to pay was high and did not significantly vary between the two pollination service outputs, producing a conservative total of £379M over a sample of the tax-paying population of the UK, equivalent to £13.4 per UK taxpayer. Using a basic production function approach, the marginal value of pollination services to these attributes is also extrapolated. The study discusses the implications of these findings and directions for related future research into the non-market value of pollination and other ecosystem services.

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.

Where is the UK's pollinator biodiversity? The importance of urban areas for flower-visiting insects

Insect pollinators provide a crucial ecosystem service, but are under threat. Urban areas could be important for pollinators, though their value relative to other habitats is poorly known. We compared pollinator communities using quantified flower-visitation networks in 36 sites (each 1 km2) in three landscapes: urban, farmland and nature reserves. Overall, flower-visitor abundance and species richness did not differ significantly between the three landscape types. Bee abundance did not differ between landscapes, but bee species richness was higher in urban areas than farmland. Hoverfly abundance was higher in farmland and nature reserves than urban sites, but species richness did not differ significantly. While urban pollinator assemblages were more homogeneous across space than those in farmland or nature reserves, there was no significant difference in the numbers of rarer species between the three landscapes. Network-level specialization was higher in farmland than urban sites. Relative to other habitats, urban visitors foraged from a greater number of plant species (higher generality) but also visited a lower proportion of available plant species (higher specialization), both possibly driven by higher urban plant richness. Urban areas are growing, and improving their value for pollinators should be part of any national strategy to conserve and restore pollinators.

Delivery of crop pollination services is an insufficient argument for wild pollinator conservation

There is compelling evidence that more diverse ecosystems deliver greater benefits to people, and these ecosystem services have become a key argument for biodiversity conservation. However, it is unclear how much biodiversity is needed to deliver ecosystem services in a cost-effective way. Here we show that, while the contribution of wild bees to crop production is significant, service delivery is restricted to a limited subset of all known bee species. Across crops, years and biogeographical regions, crop-visiting wild bee communities are dominated by a small number of common species, and threatened species are rarely observed on crops. Dominant crop pollinators persist under agricultural expansion and many are easily enhanced by simple conservation measures, suggesting that cost-effective management strategies to promote crop pollination should target a different set of species than management strategies to promote threatened bees. Conserving the biological diversity of bees therefore requires more than just ecosystem-service-based arguments.

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.

Insect pollination reduces yield loss following heat stress in faba bean (Vicia faba L.)

Global food security, particularly crop fertilization and yield production, is threatened by heat waves that are projected to increase in frequency and magnitude with climate change. Effects of heat stress on the fertilization of insect-pollinated plants are not well understood, but experiments conducted primarily in self-pollinated crops, such as wheat, show that transfer of fertile pollen may recover yield following stress. We hypothesized that in the partially pollinator-dependent crop, faba bean (Vicia faba L.), insect pollination would elicit similar yield recovery following heat stress. We exposed potted faba bean plants to heat stress for 5 days during floral development and anthesis. Temperature treatments were representative of heat waves projected in the UK for the period 2021-2050 and onwards. Following temperature treatments, plants were distributed in flight cages and either pollinated by domesticated Bombus terrestris colonies or received no insect pollination. Yield loss due to heat stress at 30°C was greater in plants excluded from pollinators (15%) compared to those with bumblebee pollination (2.5%). Thus, the pollinator dependency of faba bean yield was 16% at control temperatures (18 to 26°C) and extreme stress (34°C), but was 53% following intermediate heat stress at 30°C. These findings provide the first evidence that the pollinator dependency of crops can be modified by heat stress, and suggest that insect pollination may become more important in crop production as the probability of heat waves increases.

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.

A multi level analysis on pollination-related policies

The paper explores pollination from a multi level policy perspective and analyses the institutional fit and inter play of multi-faceted pollination-related policies. First, it asks what the major policies are that frame pollination at the EU level. Second, it explores the relationship between the EU policies and localised ways of understanding pollination. Addressed third is how the concept of ecosystem services can aid in under- standing the various ways of framing and governing the situation. The results show that the policy systems affecting pollination are abundant and that these systems create different kinds of pressure on stakeholders, at several levels of society. The local-level concerns are more about the loss of pollination services than about loss of pollinators. This points to the problem of fit between local activity driven by economic reasoning and biodiversity-driven EU policies. Here we see the concept of ecosystem services having some potential, since its operationalisation can combine economic and environmental considerations. Further- more, the analysis shows how, instead of formal institutions, it seems that social norms, habits, and motivation are the key to understanding and developing effective and attractive governance measures.

Measuring the economic value of pollination services: principles, evidence and knowledge gaps

An increasing degree of attention is being given to the ecosystem services which insect pollinators supply, and the economic value of these services. Recent research suggests that a range of factors are contributing to a global decline in pollination services, which are often used as a “headline” ecosystem service in terms of communicating the concept of ecosystem services, and how this ties peoples׳ well-being to the condition of ecosystems and the biodiversity found therein. Our paper offers a conceptual framework for measuring the economic value of changes in insect pollinator populations, and then reviews what evidence exists on the empirical magnitude of these values (both market and non-market). This allows us to highlight where the largest gaps in knowledge are, where the greatest conceptual and empirical challenges remain, and where research is most needed.