Quantifying the value of ecosystem services: a case study of honeybee pollination in the UK

There is concern that insect pollinators, such as honey bees, are currently declining in abundance, and are under serious threat from environmental changes such as habitat loss and climate change; the use of pesticides in intensive agriculture, and emerging diseases. This paper aims to evaluate how much public support there would be in preventing further decline to maintain the current number of bee colonies in the UK. The contingent valuation method (CVM) was used to obtain the willingness to pay (WTP) for a theoretical pollinator protection policy. Respondents were asked whether they would be WTP to support such a policy and how much would they pay? Results show that the mean WTP to support the bee protection policy was £1.37/week/household. Based on there being 24.9 million households in the UK, this is equivalent to £1.77 billion per year. This total value can show the importance of maintaining the overall pollination service to policy makers. We compare this total with estimates obtained using a simple market valuation of pollination for the UK.

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.

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.

Convergent evolution: floral guides, stingless bee nest entrances, and insectivorous pitchers

Several recent hypotheses, including sensory drive and sensory exploitation, suggest that receiver biases may drive selection of biological signals in the context of sexual selection. Here we suggest that a similar mechanism may have led to convergence of patterns in flowers, stingless bee nest entrances, and pitchers of insectivorous plants. A survey of these non-related visual stimuli shows that they share features such as stripes, dark centre, and peripheral dots. Next, we experimentally show that in stingless bees the close-up approach to a flower is guided by dark centre preference. Moreover, in the approach towards their nest entrance, they have a spontaneous preference for entrance patterns containing a dark centre and disrupted ornamentation. Together with existing empirical evidence on the honeybee's and other insects' orientation to flowers, this suggests that the signal receivers of the natural patterns we examined, mainly Hymenoptera, have spontaneous preferences for radiating stripes, dark centres, and peripheral dots. These receiver biases may have evolved in other behavioural contexts in the ancestors of Hymenoptera, but our findings suggest that they have triggered the convergent evolution of visual stimuli in floral guides, stingless bee nest entrances, and insectivorous pitchers.

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.

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.

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.

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.

Assembly of Recombinant Israeli Acute Paralysis virus capsids

The dicistrovirus Israeli Acute Paralysis Virus (IAPV) has been implicated in the worldwide decline of honey bees. Studies of IAPV and many other bee viruses in pure culture are restricted by available isolates and permissive cell culture. Here we show that coupling the IAPV major structural precursor protein ORF2 to its cognate 3C-like processing enzyme results in processing of the precursor to the individual structural proteins in a number of insect cell lines following expression by a recombinant baculovirus. The efficiency of expression is influenced by the level of IAPV 3C protein and moderation of its activity is required for optimal expression. The mature IAPV structural proteins assembled into empty capsids that migrated as particles on sucrose velocity gradients and showed typical dicistrovirus like morphology when examined by electron microscopy. Monoclonal antibodies raised to recombinant capsids were configured into a diagnostic test specific for the presence of IAPV. Recombinant capsids for each of the many bee viruses within the picornavirus family may provide virus specific reagents for the on-going investigation of the causes of honeybee loss.

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.

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.