A novel method for assessing risks to pollinators from plant protection products using honeybees as a model species

Pollination is one of the most important ecosystem services in agroecosystems and supports food production. Pollinators are potentially at risk being exposed to pesticides and the main route of exposure is direct contact, in some cases ingestion, of contaminated materials such as pollen, nectar, flowers and foliage. To date there are no suitable methods for predicting pesticide exposure for pollinators, therefore official procedures to assess pesticide risk are based on a Hazard Quotient. Here we develop a procedure to assess exposure and risk for pollinators based on the foraging behaviour of honeybees (Apis mellifera) and using this species as indicator representative of pollinating insects. The method was applied in 13 European field sites with different climatic, landscape and land use characteristics. The level of risk during the crop growing season was evaluated as a function of the active ingredients used and application regime. Risk levels were primarily determined by the agronomic practices employed (i.e. crop type, pest control method, pesticide use), and there was a clear temporal partitioning of risks through time. Generally the risk was higher in sites cultivated with permanent crops, such as vineyard and olive, than in annual crops, such as cereals and oil seed rape. The greatest level of risk is generally found at the beginning of the growing season for annual crops and later in June–July for permanent crops.

Pollination services in the UK: how important are honeybees?

Pollination services are known to provide substantial benefits to human populations and agriculture in particular. Although many species are known to provide pollination services, honeybees (Apis mellifera) are often assumed to provide the majority of these services to agriculture. Using data from a range of secondary sources, this study assesses the importance of insect pollinated crops at regional and national scales and investigates the capacity of honeybees to provide optimal pollination services to UK agriculture. The findings indicate that insect pollinated crops have become increasingly important in UK crop agriculture and, as of 2007, accounted for 20% of UK cropland and 19% of total farmgate crop value. Analysis of honeybee hive numbers indicates that current UK populations are only capable of supplying 34% of pollination service demands even under favourable assumptions, falling from 70% in 1984. In spite of this decline, insect pollinated crop yields have risen by an average of 54% since 1984, casting doubt on long held beliefs that honeybees provide the majority of pollination services. Future land use and crop production patterns may further increase the role of pollination services to UK agriculture, highlighting the importance of measures aimed at maintaining both wild and managed species.

Diesel exhaust rapidly degrades floral odours used by honeybees

Honeybees utilise floral odours when foraging for flowers; we investigated whether diesel exhaust pollution could interrupt these floral odour stimuli. A synthetic blend of eight floral chemicals, identified from oilseed rape, was exposed to diesel exhaust pollution. Within one minute of exposure the abundances of four of the chemicals were significantly lowered, with two components rendered undetectable. Honeybees were trained to recognise the full synthetic odour mix; altering the blend, by removing the two chemicals rendered undetectable, significantly reduced the ability of the trained honeybees to recognize the altered odour. Furthermore, we found that at environmentally relevant levels the mono-nitrogen oxide (NOx) fraction of the exhaust gases was a key facilitator of this odour degradation. Such changes in recognition may impact upon a honeybee's foraging efficiency and therefore the pollination services that they provide.

Inference on microsatellite mutation processes in the invasive mite, Varroa destructor, using reversible jump Markov chain Monte Carlo

Varroa destructor is a parasitic mite of the Eastern honeybee Apis cerana. Fifty years ago, two distinct evolutionary lineages (Korean and Japanese) invaded the Western honeybee Apis mellifera. This haplo-diploid parasite species reproduces mainly through brother sister matings, a system which largely favors the fixation of new mutations. In a worldwide sample of 225 individuals from 21 locations collected on Western honeybees and analyzed at 19 microsatellite loci, a series of de novo mutations was observed. Using historical data concerning the invasion, this original biological system has been exploited to compare three mutation models with allele size constraints for microsatellite markers: stepwise (SMM) and generalized (GSM) mutation models, and a model with mutation rate increasing exponentially with microsatellite length (ESM). Posterior probabilities of the three models have been estimated for each locus individually using reversible jump Markov Chain Monte Carlo. The relative support of each model varies widely among loci, but the GSM is the only model that always receives at least 9% support, whatever the locus. The analysis also provides robust estimates of mutation parameters for each locus and of the divergence time of the two invasive lineages (67,000 generations with a 90% credibility interval of 35,000-174,000). With an average of 10 generations per year, this divergence time fits with the last post-glacial Korea Japan land separation. (c) 2005 Elsevier Inc. All rights reserved.

Pollinator community responses to the spatial population structure of wild plants: A pan-European approach

Land-use changes can alter the spatial population structure of plant species, which may in turn affect the attractiveness of flower aggregations to different groups of pollinators at different spatial scales. To assess how pollinators respond to spatial heterogeneity of plant distributions and whether honeybees affect visitation by other pollinators we used an extensive data set comprising ten plant species and their flower visitors from five European countries. In particular we tested the hypothesis that the composition of the flower visitor community in terms of visitation frequencies by different pollinator groups were affected by the spatial plant population structure, viz. area and density measures, at a within-population (‘patch’) and among-population (‘population’) scale. We found that patch area and population density were the spatial variables that best explained the variation in visitation frequencies within the pollinator community. Honeybees had higher visitation frequencies in larger patches, while bumblebees and hoverflies had higher visitation frequencies in sparser populations. Solitary bees had higher visitation frequencies in sparser populations and smaller patches. We also tested the hypothesis that honeybees affect the composition of the pollinator community by altering the visitation frequencies of other groups of pollinators. There was a positive relationship between visitation frequencies of honeybees and bumblebees, while the relationship with hoverflies and solitary bees varied (positive, negative and no relationship) depending on the plant species under study. The overall conclusion is that the spatial structure of plant populations affects different groups of pollinators in contrasting ways at both the local (‘patch’) and the larger (‘population’) scales and, that honeybees affect the flower visitation by other pollinator groups in various ways, depending on the plant species under study. These contrasting responses emphasize the need to investigate the entire pollinator community when the effects of landscape change on plant–pollinator interactions are studied.

Enhancement of buffer strips can improve provision of multiple ecosystem services

Farmland invertebrates play a pivotal role in the provision of ecosystem services, i.e. services that benefit humans. For example, bumblebees, solitary bees and honeybees, are crucial to the pollination of many of the world's crops and wildflowers, with over 70% of the world's major food crops dependent on the pollination services provided by these insects. The larvae of some butterfly species are considered to be pests; however, together with moth and sawfly larvae, they represent a key dietary component for many farmland birds. Spiders and ground beetles predate on crop pests including aphids, whilst soil macrofauna such as earthworms are vital for soil fertility services and nutrient recycling. Despite their importance, population declines of invertebrates have been observed during the last sixty years in the UK and NW Europe. For example, seven UK bumblebee species are in decline, and in the last 20 years, the species Bombus subterraneus (short-haired bumblebee) has become extinct, whilst there was a 54% decline in honeybee colony numbers in England from 1985 to 2005. Comparable trends have been documented for butterflies with a 23% decline in UK farmland species such as Anthocharis cardamines (orange tip) between 1990 and 2007. These declines have been widely attributed to the modern intensive arable management practices that have been developed to maximise crop yield. For example, loss and fragmentation of foraging and nesting habitats, including species-rich meadows and hedgerows, have been implicated in the decline of bees and butterflies. Increased use of herbicides and fertilisers has caused detrimental effects on many plant species with negative consequences for predatory invertebrates such as spiders and beetles which rely on plants for food and shelter.

Agricultural policies exacerbate honeybee pollination service supply-demand mismatches across Europe

Declines in insect pollinators across Europe have raised concerns about the supply of pollination services to agriculture. Simultaneously, EU agricultural and biofuel policies have encouraged substantial growth in the cultivated area of insect pollinated crops across the continent. Using data from 41 European countries, this study demonstrates that the recommended number of honeybees required to provide crop pollination across Europe has risen 4.9 times as fast as honeybee stocks between 2005 and 2010. Consequently, honeybee stocks were insufficient to supply >90% of demands in 22 countries studied. These findings raise concerns about the capacity of many countries to cope with major losses of wild pollinators and highlight numerous critical gaps in current understanding of pollination service supplies and demands, pointing to a pressing need for further research into this issue.

Contribution of insect pollinators to crop yield and quality varies with agricultural intensification

Background: Up to 75% of crop species benefit at least to some degree from animal pollination for fruit or seed set and yield. However, basic information on the level of pollinator dependence and pollinator contribution to yield is lacking for many crops. Even less is known about how insect pollination affects crop quality. Given that habitat loss and agricultural intensification are known to decrease pollinator richness and abundance, there is a need to assess the consequences for different components of crop production. Methods: We used pollination exclusion on flowers or inflorescences on a whole plant basis to assess the contribution of insect pollination to crop yield and quality in four flowering crops (spring oilseed rape, field bean, strawberry, and buckwheat) located in four regions of Europe. For each crop, we recorded abundance and species richness of flower visiting insects in ten fields located along a gradient fromsimple to heterogeneous landscapes. Results: Insect pollination enhanced average crop yield between 18 and 71% depending on the crop. Yield quality was also enhanced in most crops. For instance, oilseed rape had higher oil and lower chlorophyll contents when adequately pollinated, the proportion of empty seeds decreased in buckwheat, and strawberries’ commercial grade improved; however, we did not find higher nitrogen content in open pollinated field beans. Complex landscapes had a higher overall species richness of wild pollinators across crops, but visitation rates were only higher in complex landscapes for some crops. On the contrary, the overall yield was consistently enhanced by higher visitation rates, but not by higher pollinator richness. Discussion. For the four crops in this study, there is clear benefit delivered by pollinators on yield quantity and/or quality, but it is not maximized under current agricultural intensification. Honeybees, the most abundant pollinator, might partially compensate the loss of wild pollinators in some areas, but our results suggest the need of landscape-scale actions to enhance wild pollinator populations.

Impact of chronic neonicotinoid exposure on honeybee colony performance and queen supersedure

BACKGROUND: Honeybees provide economically and ecologically vital pollination services to crops and wild plants. During the last decade elevated colony losses have been documented in Europe and North America. Despite growing consensus on the involvement of multiple causal factors, the underlying interactions impacting on honeybee health and colony failure are not fully resolved. Parasites and pathogens are among the main candidates, but sublethal exposure to widespread agricultural pesticides may also affect bees. METHODOLOGY/PRINCIPAL FINDINGS: To investigate effects of sublethal dietary neonicotinoid exposure on honeybee colony performance, a fully crossed experimental design was implemented using 24 colonies, including sister-queens from two different strains, and experimental in-hive pollen feeding with or without environmentally relevant concentrations of thiamethoxam and clothianidin. Honeybee colonies chronically exposed to both neonicotinoids over two brood cycles exhibited decreased performance in the short-term resulting in declining numbers of adult bees (-28%) and brood (-13%), as well as a reduction in honey production (-29%) and pollen collections (-19%), but colonies recovered in the medium-term and overwintered successfully. However, significantly decelerated growth of neonicotinoid-exposed colonies during the following spring was associated with queen failure, revealing previously undocumented long-term impacts of neonicotinoids: queen supersedure was observed for 60% of the neonicotinoid-exposed colonies within a one year period, but not for control colonies. Linked to this, neonicotinoid exposure was significantly associated with a reduced propensity to swarm during the next spring. Both short-term and long-term effects of neonicotinoids on colony performance were significantly influenced by the honeybees' genetic background. CONCLUSIONS/SIGNIFICANCE: Sublethal neonicotinoid exposure did not provoke increased winter losses. Yet, significant detrimental short and long-term impacts on colony performance and queen fate suggest that neonicotinoids may contribute to colony weakening in a complex manner. Further, we highlight the importance of the genetic basis of neonicotinoid susceptibility in honeybees which can vary substantially.

Ecological and social drivers of coffee pollination in Santander, Colombia

Bees and other insects provide pollination services that are key to determining the fruit set on coffee plantations. These pollination services are influenced by local ecology as well as human factors, both social and economic. To better understand these different factors, we assessed their effect on pollinators and coffee pollination services in Santander, Colombia. We quantified the effect of key ecological drivers on pollinator community composition, such as the method of farm management (either conventional or organic) and the surrounding landscape composition, specifically the proximity to forest. We found that ambient levels of pollination services provided by the local pollinator fauna (open pollination) accounted for a 10.5 ± 2.0% increase in final coffee fruit set, and that the various pollinators are affected differently by the differing factors. For example, our findings indicate that conventional farm management, using synthetic inputs, can promote pollinators, especially if they are in close proximity to natural forest fragments. This is particularly true for stingless bees. Honeybee visitation to coffee is also positively influenced by the conventional management of farms. Factors associated with greater numbers of stingless bees on farms include greater shade cover, lower tree densities, smaller numbers and types of trees in bloom, and younger coffee plantations. A forested landscape close to farms appears to enhance these factors, giving increased stability and resilience to the pollinating bees and insects. However we found that organic farms also support diverse pollinator communities, even if distant from forest fragments. The contribution of honeybees to pollination value (US$129.6/ha of coffee) is greater than that of stingless bees (US$16.5/ha of coffee). Since the method of farm management has a major impact on the numbers and types of pollinators attracted to farms, we have analysed the statistically significant social factors that influence farmers’ decisions on whether to adopt organic or conventional practices. These include the availability of technology, the type of landowner (whether married couples or individual owners), the number of years of farmers’ formal education, the role of institutions, membership of community organizations, farm size, coffee productivity and the number of coffee plots per farm. It is hoped that the use of our holistic approach, which combines investigation of the social as well as the ecological drivers of pollination, will help provide evidence to underpin the development of best practices for integrating the management of pollination into sustainable agricultural practices.

Apple pollination: demand depends on variety and supply depends on pollinator identity

Insect pollination underpins apple production but the extent to which different pollinator guilds supply this service, particularly across different apple varieties, is unknown. Such information is essential if appropriate orchard management practices are to be targeted and proportional to the potential benefits pollinator species may provide. Here we use a novel combination of pollinator effectiveness assays (floral visit effectiveness), orchard field surveys (flower visitation rate) and pollinator dependence manipulations (pollinator exclusion experiments) to quantify the supply of pollination services provided by four different pollinator guilds to the production of four commercial varieties of apple. We show that not all pollinators are equally effective at pollinating apples, with hoverflies being less effective than solitary bees and bumblebees, and the relative abundance of different pollinator guilds visiting apple flowers of different varieties varies significantly. Based on this, the taxa specific economic benefits to UK apple production have been established. The contribution of insect pollinators to the economic output in all varieties was estimated to be £92.1M across the UK, with contributions varying widely across taxa: solitary bees (£51.4M), honeybees (£21.4M), bumblebees (£18.6M) and hoverflies (£0.7M). This research highlights the differences in the economic benefits of four insect pollinator guilds to four major apple varieties in the UK. This information is essential to underpin appropriate investment in pollination services management and provides a model that can be used in other entomolophilous crops to improve our understanding of crop pollination ecology.