Landscape effects on crop pollination services: are there general patterns?

Pollination by bees and other animals increases the size, quality, or stability of harvests for 70% of leading global crops. Because native species pollinate many of these crops effectively, conserving habitats for wild pollinators within agricultural landscapes can help maintain pollination services. Using hierarchical Bayesian techniques, we synthesize the results of 23 studies - representing 16 crops on five continents - to estimate the general relationship between pollination services and distance from natural or semi-natural habitats. We find strong exponential declines in both pollinator richness and native visitation rate. Visitation rate declines more steeply, dropping to half of its maximum at 0.6 km from natural habitat, compared to 1.5 km for richness. Evidence of general decline in fruit and seed set - variables that directly affect yields - is less clear. Visitation rate drops more steeply in tropical compared with temperate regions, and slightly more steeply for social compared with solitary bees. Tropical crops pollinated primarily by social bees may therefore be most susceptible to pollination failure from habitat loss. Quantifying these general relationships can help predict consequences of land use change on pollinator communities and crop productivity, and can inform landscape conservation efforts that balance the needs of native species and people.

Species distribution models for crop pollination: a modelling framework applied to Great Britain

Insect pollination benefits over three quarters of the world's major crops. There is growing concern that observed declines in pollinators may impact on production and revenues from animal pollinated crops. Knowing the distribution of pollinators is therefore crucial for estimating their availability to pollinate crops; however, in general, we have an incomplete knowledge of where these pollinators occur. We propose a method to predict geographical patterns of pollination service to crops, novel in two elements: the use of pollinator records rather than expert knowledge to predict pollinator occurrence, and the inclusion of the managed pollinator supply. We integrated a maximum entropy species distribution model (SDM) with an existing pollination service model (PSM) to derive the availability of pollinators for crop pollination. We used nation-wide records of wild and managed pollinators (honey bees) as well as agricultural data from Great Britain. We first calibrated the SDM on a representative sample of bee and hoverfly crop pollinator species, evaluating the effects of different settings on model performance and on its capacity to identify the most important predictors. The importance of the different predictors was better resolved by SDM derived from simpler functions, with consistent results for bees and hoverflies. We then used the species distributions from the calibrated model to predict pollination service of wild and managed pollinators, using field beans as a test case. The PSM allowed us to spatially characterize the contribution of wild and managed pollinators and also identify areas potentially vulnerable to low pollination service provision, which can help direct local scale interventions. This approach can be extended to investigate geographical mismatches between crop pollination demand and the availability of pollinators, resulting from environmental change or policy scenarios.

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.

Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees

Recent concern over global pollinator declines has led to considerable research on the effects of pesticides on bees1, 2, 3, 4, 5. Although pesticides are typically not encountered at lethal levels in the field, there is growing evidence indicating that exposure to field-realistic levels can have sublethal effects on bees, affecting their foraging behaviour1, 6, 7, homing ability8, 9 and reproductive success2, 5. Bees are essential for the pollination of a wide variety of crops and the majority of wild flowering plants10, 11, 12, but until now research on pesticide effects has been limited to direct effects on bees themselves and not on the pollination services they provide. Here we show the first evidence to our knowledge that pesticide exposure can reduce the pollination services bumblebees deliver to apples, a crop of global economic importance. Bumblebee colonies exposed to a neonicotinoid pesticide provided lower visitation rates to apple trees and collected pollen less often. Most importantly, these pesticide-exposed colonies produced apples containing fewer seeds, demonstrating a reduced delivery of pollination services. Our results also indicate that reduced pollination service delivery is not due to pesticide-induced changes in individual bee behaviour, but most likely due to effects at the colony level. These findings show that pesticide exposure can impair the ability of bees to provide pollination services, with important implications for both the sustained delivery of stable crop yields and the functioning of natural ecosystems.

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.

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.

The identity of crop pollinators helps target conservation for improved ecosystem services

Insect pollinated mass flowering crops are becoming more widespread and there is a need to understand which insects are primarily responsible for the pollination of these crops so conservation measures can be appropriately targeted in the face of pollinator declines. This study used field surveys in conjunction with cage manipulations to identify the relative contributions of different pollinator taxa to the pollination of two widespread flowering crops, field beans and oilseed rape. Flower visiting pollinator communities observed in the field were distinct for each crop; while field beans were visited primarily by a few bumblebee species, multiple pollinator taxa visited oilseed, and the composition of this pollinator community was highly variable spatially and temporally. Neither pollinator community, however, appears to be meeting the demands of crops in our study regions. Cage manipulations showed that multiple taxa can effectively pollinate both oilseed and field beans, but bumblebees are particularly effective bean pollinators. Combining field observations and cage manipulations demonstrated that the pollination demands of these two mass flowering crops are highly contrasting, one would benefit from management to increase the abundance of some key taxa, whilst for the other, boosting overall pollinator abundance and diversity would be more appropriate. Our findings highlight the need for crop specific mitigation strategies that are targeted at conserving specific pollinator taxa (or group of taxa) that are both active and capable of crop pollination in order to reduce pollination deficits and meet the demands of future crop production.

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.

Technologies for biological containment of GM and Non-GM crops

International Perspective The development of GM technology continues to expand into increasing numbers of crops and conferred traits. Inevitably, the focus remains on the major field crops of soybean, maize, cotton, oilseed rape and potato with introduced genes conferring herbicide tolerance and/or pest resistance. Although there are comparatively few GM crops that have been commercialised to date, GM versions of 172 plant species have been grown in field trials in 31 countries. European Crops with Containment Issues Of the 20 main crops in the EU there are four for which GM varieties are commercially available (cotton, maize for animal feed and forage, and oilseed rape). Fourteen have GM varieties in field trials (bread wheat, barley, durum wheat, sunflower, oats, potatoes, sugar beet, grapes, alfalfa, olives, field peas, clover, apples, rice) and two have GM varieties still in development (rye, triticale). Many of these crops have hybridisation potential with wild and weedy relatives in the European flora (bread wheat, barley, oilseed rape, durum wheat, oats, sugar beet and grapes), with escapes (sunflower); and all have potential to cross-pollinate fields non-GM crops. Several fodder crops, forestry trees, grasses and ornamentals have varieties in field trials and these too may hybridise with wild relatives in the European flora (alfalfa, clover, lupin, silver birch, sweet chestnut, Norway spruce, Scots pine, poplar, elm, Agrostis canina, A. stolonifera, Festuca arundinacea, Lolium perenne, L. multiflorum, statice and rose). All these crops will require containment strategies to be in place if it is deemed necessary to prevent transgene movement to wild relatives and non-GM crops. Current Containment Strategies A wide variety of GM containment strategies are currently under development, with a particular focus on crops expressing pharmaceutical products. Physical containment in greenhouses and growth rooms is suitable for some crops (tomatoes, lettuce) and for research purposes. Aquatic bioreactors of some non-crop species (algae, moss, and duckweed) expressing pharmaceutical products have been adopted by some biotechnology companies. There are obvious limitations of the scale of physical containment strategies, addressed in part by the development of large underground facilities in the US and Canada. The additional resources required to grow plants underground incurs high costs that in the long term may negate any advantage of GM for commercial productioNatural genetic containment has been adopted by some companies through the selection of either non-food/feed crops (algae, moss, duckweed) as bio-pharming platforms or organisms with no wild relatives present in the local flora (safflower in the Americas). The expression of pharmaceutical products in leafy crops (tobacco, alfalfa, lettuce, spinach) enables growth and harvesting prior to and in the absence of flowering. Transgenically controlled containment strategies range in their approach and degree of development. Plastid transformation is relatively well developed but is not suited to all traits or crops and does not offer complete containment. Male sterility is well developed across a range of plants but has limitations in its application for fruit/seed bearing crops. It has been adopted in some commercial lines of oilseed rape despite not preventing escape via seed. Conditional lethality can be used to prevent flowering or seed development following the application of a chemical inducer, but requires 100% induction of the trait and sufficient application of the inducer to all plants. Equally, inducible expression of the GM trait requires equally stringent application conditions. Such a method will contain the trait but will allow the escape of a non-functioning transgene. Seed lethality (‘terminator’ technology) is the only strategy at present that prevents transgene movement via seed, but due to public opinion against the concept it has never been trialled in the field and is no longer under commercial development. Methods to control flowering and fruit development such as apomixis and cleistogamy will prevent crop-to-wild and wild-to-crop pollination, but in nature both of these strategies are complex and leaky. None of the genes controlling these traits have as yet been identified or characterised and therefore have not been transgenically introduced into crop species. Neither of these strategies will prevent transgene escape via seed and any feral apomicts that form are arguably more likely to become invasives. Transgene mitigation reduces the fitness of initial hybrids and so prevents stable introgression of transgenes into wild populations. However, it does not prevent initial formation of hybrids or spread to non-GM crops. Such strategies could be detrimental to wild populations and have not yet been demonstrated in the field. Similarly, auxotrophy prevents persistence of escapes and hybrids containing the transgene in an uncontrolled environment, but does not prevent transgene movement from the crop. Recoverable block of function, intein trans-splicing and transgene excision all use recombinases to modify the transgene in planta either to induce expression or to prevent it. All require optimal conditions and 100% accuracy to function and none have been tested under field conditions as yet. All will contain the GM trait but all will allow some non-native DNA to escape to wild populations or to non-GM crops. There are particular issues with GM trees and grasses as both are largely undomesticated, wind pollinated and perennial, thus providing many opportunities for hybridisation. Some species of both trees and grass are also capable of vegetative propagation without sexual reproduction. There are additional concerns regarding the weedy nature of many grass species and the long-term stability of GM traits across the life span of trees. Transgene stability and conferred sterility are difficult to trial in trees as most field trials are only conducted during the juvenile phase of tree growth. Bio-pharming of pharmaceutical and industrial compounds in plants Bio-pharming of pharmaceutical and industrial compounds in plants offers an attractive alternative to mammalian-based pharmaceutical and vaccine production. Several plantbased products are already on the market (Prodigene’s avidin, β-glucuronidase, trypsin generated in GM maize; Ventria’s lactoferrin generated in GM rice). Numerous products are in clinical trials (collagen, antibodies against tooth decay and non-Hodgkin’s lymphoma from tobacco; human gastric lipase, therapeutic enzymes, dietary supplements from maize; Hepatitis B and Norwalk virus vaccines from potato; rabies vaccines from spinach; dietary supplements from Arabidopsis). The initial production platforms for plant-based pharmaceuticals were selected from conventional crops, largely because an established knowledge base already existed. Tobacco and other leafy crops such as alfalfa, lettuce and spinach are widely used as leaves can be harvested and no flowering is required. Many of these crops can be grown in contained greenhouses. Potato is also widely used and can also be grown in contained conditions. The introduction of morphological markers may aid in the recognition and traceability of crops expressing pharmaceutical products. Plant cells or plant parts may be transformed and maintained in culture to produce recombinant products in a contained environment. Plant cells in suspension or in vitro, roots, root cells and guttation fluid from leaves may be engineered to secrete proteins that may be harvested in a continuous, non-destructive manner. Most strategies in this category remain developmental and have not been commercially adopted at present. Transient expression produces GM compounds from non-GM plants via the utilisation of bacterial or viral vectors. These vectors introduce the trait into specific tissues of whole plants or plant parts, but do not insert them into the heritable genome. There are some limitations of scale and the field release of such crops will require the regulation of the vector. However, several companies have several transiently expressed products in clinical and pre-clinical trials from crops raised in physical containment.

Identifying key knowledge needs for evidence-based conservation of wild insect pollinators: a collaborative cross-sectoral exercise

In response to evidence of insect pollinator declines, organisations in many sectors, including the food and farming industry, are investing in pollinator conservation. They are keen to ensure that their efforts use the best available science. We convened a group of 32 ‘conservation practitioners’ with an active interest in pollinators and 16 insect pollinator scientists. The conservation practitioners include representatives from UK industry (including retail), environmental non-government organisations and nature conservation agencies. We collaboratively developed a long list of 246 knowledge needs relating to conservation of wild insect pollinators in the UK. We refined and selected the most important knowledge needs, through a three-stage process of voting and scoring, including discussions of each need at a workshop. We present the top 35 knowledge needs as scored by conservation practitioners or scientists. We find general agreement in priorities identified by these two groups. The priority knowledge needs will structure ongoing work to make science accessible to practitioners, and help to guide future science policy and funding. Understanding the economic benefits of crop pollination, basic pollinator ecology and impacts of pesticides on wild pollinators emerge strongly as priorities, as well as a need to monitor floral resources in the landscape.

EDITOR'S CHOICE: REVIEW: Trait matching of flower visitors and crops predicts fruit set better than trait diversity

Understanding the relationships between trait diversity, species diversity and ecosystem functioning is essential for sustainable management. For functions comprising two trophic levels, trait matching between interacting partners should also drive functioning. However, the predictive ability of trait diversity and matching is unclear for most functions, particularly for crop pollination, where interacting partners did not necessarily co-evolve. World-wide, we collected data on traits of flower visitors and crops, visitation rates to crop flowers per insect species and fruit set in 469 fields of 33 crop systems. Through hierarchical mixed-effects models, we tested whether flower visitor trait diversity and/or trait matching between flower visitors and crops improve the prediction of crop fruit set (functioning) beyond flower visitor species diversity and abundance. Flower visitor trait diversity was positively related to fruit set, but surprisingly did not explain more variation than flower visitor species diversity. The best prediction of fruit set was obtained by matching traits of flower visitors (body size and mouthpart length) and crops (nectar accessibility of flowers) in addition to flower visitor abundance, species richness and species evenness. Fruit set increased with species richness, and more so in assemblages with high evenness, indicating that additional species of flower visitors contribute more to crop pollination when species abundances are similar. Synthesis and applications. Despite contrasting floral traits for crops world-wide, only the abundance of a few pollinator species is commonly managed for greater yield. Our results suggest that the identification and enhancement of pollinator species with traits matching those of the focal crop, as well as the enhancement of pollinator richness and evenness, will increase crop yield beyond current practices. Furthermore, we show that field practitioners can predict and manage agroecosystems for pollination services based on knowledge of just a few traits that are known for a wide range of flower visitor species.

Organic farming in isolated landscapes does not benefit flower-visiting insects and pollination

Organic farming has often been found to provide benefits for biodiversity, but the benefits can depend on the species considered and characteristics of the surrounding landscape. In an intensively farmed area of Northeast Italy we investigated whether isolated organic farms, in a conventionally farmed landscape, provided local benefits for insect pollinators and pollination services. We quantified the relative effects of local management (i.e. the farm system), landscape management (proportion of surrounding uncultivated land) and interactions between them. We compared six organic and six conventional vine fields. The proportion of surrounding uncultivated land was calculated for each site at radii of 200, 500, 1000 and 2000 m. The organic fields did not differ from the conventional in their floral resources or proportion of surrounding uncultivated land. Data were collected on pollinator abundance and species richness, visitation rates to, and pollination of experimental potted plants. None of these factors were significantly affected by the farming system. The abundance of visits to the potted plants in the conventional fields tended to be negatively affected by the proportion of surrounding uncultivated land. The proportion fruit set, weight of seeds per plant and seed weight in conventional and organic fields were all negatively affected by the proportion of surrounding uncultivated land. In vine fields the impact of the surrounding landscape was stronger than the local management. Enhancement of biodiversity through organic farming should not be assumed to be ubiquitous, as potential benefits may be offset by the crop type, organicmanagement practices and the specific habitat requirements in the surrounding landscape.

Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change

Many ecosystem services are delivered by organisms that depend on habitats that are segregated spatially or temporally from the location where services are provided. Management of mobile organisms contributing to ecosystem services requires consideration not only of the local scale where services are delivered, but also the distribution of resources at the landscape scale, and the foraging ranges and dispersal movements of the mobile agents. We develop a conceptual model for exploring how one such mobile-agent-based ecosystem service (MABES), pollination, is affected by land-use change, and then generalize the model to other MABES. The model includes interactions and feedbacks among policies affecting land use, market forces and the biology of the organisms involved. Animal-mediated pollination contributes to the production of goods of value to humans such as crops; it also bolsters reproduction of wild plants on which other services or service-providing organisms depend. About one-third of crop production depends on animal pollinators, while 60-90% of plant species require an animal pollinator. The sensitivity of mobile organisms to ecological factors that operate across spatial scales makes the services provided by a given community of mobile agents highly contextual. Services vary, depending on the spatial and temporal distribution of resources surrounding the site, and on biotic interactions occurring locally, such as competition among pollinators for resources, and among plants for pollinators. The value of the resulting goods or services may feed back via market-based forces to influence land-use policies, which in turn influence land management practices that alter local habitat conditions and landscape structure. Developing conceptual models for MABES aids in identifying knowledge gaps, determining research priorities, and targeting interventions that can be applied in an adaptive management context.

Asynchronous flowering and within-plant flowering diversity in wheat and the implications for crop resilience to heat

Self-pollination dominates in wheat , with a small level of out-crossing due to flowering asynchrony and male sterility. However, the timing and synchrony of male and female flowering in wheat is a crucial determinant of seed set and may be an important factor affecting gene flow and resilience to climate change. Here, a methodology is presented for assessing the timing and synchrony of flowering in wheat. From the onset of flowering until the end of anthesis, the anther and stigma activity of each floret was assessed on the first five developing ears in potted plants grown under ambient conditions and originating from cv Paragon or cvs Spark-Rialto backgrounds. At harvest maturity, seed presence, size and weight was recorded for each floret scored. The synchrony between pollen dehiscence and stigma collapse within a flower was dependent on its relative position in a spike and within a floret. Determined on the basis of synchrony within each flower, the level of pollination by pollen originating from other flowers reached approximately 30% and did not change throughout the duration of flowering. A modelling exercise parameterised by flowering observations indicated that the temporal and spatial variability of anther activity within and between spikes may influence the relative resilience of wheat to sudden, extreme climatic events which has direct relevance to predicted future climate scenarios in the UK.