Dara A. Stanley

Non-bee insects are important contributors to global crop pollination

Significance Many of the world’s crops are pollinated by insects, and bees are often assumed to be the most important pollinators. To our knowledge, our study is the first quantitative evaluation of the relative contribution of non-bee pollinators to global pollinator-dependent crops. Across 39 studies we show that insects other than bees are efficient pollinators providing 39% of visits to crop flowers. A shift in perspective from a bee-only focus is needed for assessments of crop pollinator biodiversity and the economic value of pollination. These studies should also consider the services provided by other types of insects, such as flies, wasps, beetles, and butterflies—important pollinators that are currently overlooked. 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.

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 bees. 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 behaviour, homing ability and reproductive success. Bees are essential for the pollination of a wide variety of crops and the majority of wild flowering plants, 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.

Relative abundance of an invasive alien plant affects native pollination processes

One major characteristic of invasive alien species is their occurrence at high abundances in their new habitat. Flowering invasive plant species that are visited by native insects and overlap with native plant species in their pollinators may facilitate or disrupt native flower visitation and fertilisation by forming large, dense populations with high numbers of flowers and copious rewards. We investigated the direction of such a proposed effect for the alien invasive Rhododendron ponticum in Irish habitats. Flower visitation, conspecific and alien pollen deposition, fruit and seed set were measured in a self-compatible native focal plant, Digitalis purpurea, and compared between field sites that contained different relative abundances of R. ponticum. Flower visitation was significantly lower at higher alien relative plant abundances than at lower abundances or in the absence of the alien. Native flowers experienced a significant decrease in conspecific pollen deposition with increasing alien abundance. Heterospecific pollen transfer was very low in all field sites but increased significantly with increasing relative R. ponticum abundance. However, lower flower visitation and lower conspecific pollen transfer did not alter reproductive success of D. purpurea. Our study shows that indirect interactions between alien and native plants for pollination can be modified by population characteristics (such as relative abundance) in a similar way as interactions among native plant species. In D. purpurea, only certain aspects of pollination and reproduction were affected by high alien abundances which is probably a result of high resilience due to a self-compatible breeding system. Native species that are more susceptible to pollen limitation are more likely to experience fitness disadvantages in habitats with high relative alien plant abundances.

Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide

Bumblebees are exposed to pesticides applied for crop protection while foraging on treated plants, with increasing evidence suggesting that this sublethal exposure has implications for pollinator declines. The challenges of navigating and learning to manipulate many different flowers underline the critical role learning plays for the foraging success and survival of bees. We assessed the impacts of both acute and chronic exposure to field-realistic levels of a widely applied neonicotinoid insecticide, thiamethoxam, on bumblebee odour learning and memory. Although bees exposed to acute doses showed conditioned responses less frequently than controls, we found no difference in the number of individuals able to learn at field-realistic exposure levels. However, following chronic pesticide exposure, bees exposed to field-realistic levels learnt more slowly and their short-term memory was significantly impaired following exposure to 2.4 ppb pesticide. These results indicate that field-realistic pesticide exposure can have appreciable impacts on learning and memory, with potential implications for essential individual behaviour and colony fitness.

Quantifying the impacts of bioenergy crops on pollinating insect abundance and diversity: a field‐scale evaluation reveals taxon‐specific responses

Summary Global declines in pollinating insects have been linked with agricultural intensification and land-use change. Increased production of novel crops for bioenergy is causing changes in agricultural practice, but the effects on different pollinating taxa have not yet been quantified. However, the major pollinating groups (social bees, solitary bees, hoverflies and butterflies) are likely to respond differently to changes in land use and shifts in crop cultivation patterns. We assessed the impacts of two bioenergy crops, oilseed rape Brassica napus L. and Miscanthus Miscanthus X giganteus on (i) the diversity and abundance of four taxonomic groups of pollinating insects, (ii) insect community composition, (iii) floral resources and (iv) nesting sites for bumblebees, by comparing bioenergy crops with conventional arable and grass crops in a large network of commercial fields. We found that although there were more bumblebees in oilseed rape fields, conventional crops and bioenergy crops did not differ greatly in species richness of most pollinator groups, although more floral resources were found in the bioenergy crops. However, solitary bees were more abundant and species rich in energy crops than conventional wheat, and more trap-nesting bees and wasps were found in Miscanthus than oilseed rape. In addition, novel assemblages of solitary bees were found in the bioenergy crops. All pollinator groups, and flowering plants, were more abundant in field margins than in the centre of crop fields. Although there were no differences among crop types, nest-searching bumblebees were confined to field margins. This highlights the importance of field margins as forage and nesting habitat for pollinators in farmland. Synthesis and applications. Differential responses to field-scale growth of bioenergy crops were displayed by the taxonomic groups studied, suggesting that effects on biodiversity cannot be generalized from studies based on a small suite of taxonomic groups and must include a range of taxa for overarching results. To optimize habitat for pollinators in agricultural areas, our data suggest that a diversity of crop types at small scales may have positive impacts and supports appropriate management and conservation of field margins and hedgerows during conversion to bioenergy production.

Investigating the impacts of field‐realistic exposure to a neonicotinoid pesticide on bumblebee foraging, homing ability and colony growth

Summary The ability to forage and return home is essential to the success of bees as both foragers and pollinators. Pesticide exposure may cause behavioural changes that interfere with these processes, with consequences for colony persistence and delivery of pollination services. We investigated the impact of chronic exposure (5–43 days) to field‐realistic levels of a neonicotinoid insecticide (2·4 ppb thiamethoxam) on foraging ability, homing success and colony size using radio frequency identification (RFID) technology in free‐flying bumblebee colonies. Individual foragers from pesticide‐exposed colonies carried out longer foraging bouts than untreated controls (68 vs. 55 min). Pesticide‐exposed bees also brought back pollen less frequently than controls indicating reduced foraging performance. A higher proportion of bees from pesticide‐exposed colonies returned when released 1 km from their nests; this is potentially related to increased orientation experience during longer foraging bouts. We measured no impact of pesticide exposure on homing ability for bees released from 2 km, or when data were analysed overall. Despite a trend for control colonies to produce more new workers earlier, we found no overall impacts of pesticide exposure on whole colony size. Synthesis and applications. This study shows that field‐realistic neonicotinoid exposure can have impacts on both foraging ability and homing success of bumblebees, with implications for the success of bumblebee colonies in agricultural landscapes and their ability to deliver crucial pollination services. Pesticide risk assessments should include bee species other than honeybees and assess a range of behaviours to elucidate the impact of sublethal effects. This has relevance for reviews of neonicotinoid risk assessment and usage policy world‐wide.

Chronic exposure to a neonicotinoid pesticide alters the interactions between bumblebees and wild plants

Summary Insect pollinators are essential for both the production of a large proportion of world crops and the health of natural ecosystems. As important pollinators, bumblebees must learn to forage on flowers to feed both themselves and provision their colonies. Increased use of pesticides has caused concern over sublethal effects on bees, such as impacts on reproduction or learning ability. However, little is known about how sublethal exposure to field‐realistic levels of pesticide might affect the ability of bees to visit and manipulate flowers. We observed the behaviour of individual bumblebees from colonies chronically exposed to a neonicotinoid pesticide (10 ppb thiamethoxam) or control solutions foraging for the first time on an array of morphologically complex wildflowers (Lotus corniculatus and Trifolium repens) in an outdoor flight arena. We found that more bees released from pesticide‐treated colonies became foragers, and that they visited more L. corniculatus flowers than controls. Interestingly, bees exposed to pesticide collected pollen more often than controls, but control bees learnt to handle flowers efficiently after fewer learning visits than bees exposed to pesticide. There were also different initial floral preferences of our treatment groups; control bees visited a higher proportion of T. repens flowers, and bees exposed to pesticide were more likely to choose L. corniculatus on their first visit. Our results suggest that the foraging behaviour of bumblebees on real flowers can be altered by sublethal exposure to field‐realistic levels of pesticide. This has implications for the foraging success and persistence of bumblebee colonies, but perhaps more importantly for the interactions between wild plants and flower‐visiting insects and ability of bees to deliver the crucial pollination services to plants necessary for ecosystem functioning.

Response of farmland biodiversity to the introduction of bioenergy crops: effects of local factors and surrounding landscape context.

The recent growth in bioenergy crop cultivation, stimulated by the need to implement measures to reduce net CO2 emissions, is driving major land‐use changes with consequences for biodiversity and ecosystem service provision. Although the type of bioenergy crop and its associated management is likely to affect biodiversity at the local (field) scale, landscape context and its interaction with crop type may also influence biodiversity on farms. In this study, we assessed the impact of replacing conventional agricultural crops with two model bioenergy crops (either oilseed rape Brassica napus or Miscanthus × giganteus) on vascular plant, bumblebee, solitary bee, hoverfly and carabid beetle richness, diversity and abundance in 50 sites in Ireland. We assessed whether within‐field biodiversity was also related to surrounding landscape structure. We found that local‐ and landscape‐scale variables correlated with biodiversity in these agricultural landscapes. Overall, the differences between the bioenergy crops and the conventional crops on farmland biodiversity were mostly positive (e.g. higher vascular plant richness in Miscanthus planted on former conventional tillage, higher solitary bee abundance and richness in Miscanthus and oilseed rape compared with conventional crops) or neutral (e.g. no differences between crop types for hoverflies and bumblebees). We showed that these crop type effects were independent of (i.e. no interactions with) the surrounding landscape composition and configuration. However, surrounding landscape context did relate to biodiversity in these farms, negatively for carabid beetles and positively for hoverflies. Although we conclude that the bioenergy crops compared favourably with conventional crops in terms of biodiversity of the taxa studied at the field scale, the effects of large‐scale planting in these landscapes could result in very different impacts. Maintaining ecosystem functioning and the delivery of ecosystem services will require a greater understanding of impacts at the landscape scale to ensure the sustainable development of climate change mitigation measures.

Pollinator sharing between mass-flowering oilseed rape and co-flowering wild plants: implications for wild plant pollination

Pollinating insects are not only important in wild plant pollination, but also in the production of a large number of crops. Oilseed rape production is increasing globally due to demands for biofuels which may have impacts on pollinating insects which visit the crop and on the pollination services delivered to co-flowering wild plants. In this study, we tested (1) the degree of pollinator sharing between oilseed rape and native wild plants in field margins and hedgerows and (2) the effects of oilseed rape on the quality of pollination service delivered to these wild plants. We found large overlap between flower visitors of wild plants and oilseed rape, but the composition of species overlap differed with respect to each wild plant species. Nearly all individual visitors caught on both the crop and foraging on wild species carried crop pollen, but more than half the insects also carried pollen from wild plants. However, very little oilseed rape pollen was deposited on wild plant stigmas. This shows that (1) oilseed rape overlaps in pollinator niche with most co-flowering wild plants, and (2) crop pollen deposition on wild plant stigmas is low which may indicate that it is unlikely to cause reductions in seed set of wild plants, although this was not measured here. Furthermore, wild plants in field margins and hedgerows are important sources of alternative forage for pollinating insects even when a crop is mass flowering, and we suggest maintenance and augmentation of field margins and hedgerows to provide alternative forage for pollinator conservation to continue provision of pollination services to both crops and wild plants.

Ecological Variation in Response to Mass-Flowering Oilseed Rape and Surrounding Landscape Composition by Members of a Cryptic Bumblebee Complex

The Bombus sensu stricto species complex is a widespread group of cryptic bumblebee species which are important pollinators of many crops and wild plants. These cryptic species have, until now, largely been grouped together in ecological studies, and so little is known about their individual colony densities, foraging ranges or habitat requirements, which can be influenced by land use at a landscape scale. We used mass-flowering oilseed rape fields as locations to sample bees of this complex, as well as the second most common visitor to oilseed rape B. lapidarius, and molecular RFLP methods to distinguish between the cryptic species. We then used microsatellite genotyping to identify sisters and estimate colony densities, and related both proportions of cryptic species and their colony densities to the composition of the landscape surrounding the fields. We found B. lucorum was the most common member of the complex present in oilseed rape followed by B. terrestris. B. cryptarum was also present in all but one site, with higher proportions found in the east of the study area. High numbers of bumblebee colonies were estimated to be using oilseed rape fields as a forage resource, with B. terrestris colony numbers higher than previous estimates from non-mass-flowering fields. We also found that the cryptic species responded differently to surrounding landscape composition: both relative proportions of B. cryptarum in samples and colony densities of B. lucorum were negatively associated with the amount of arable land in the landscape, while proportions and colony densities of other species did not respond to landscape variables at the scale measured. This suggests that the cryptic species have different ecological requirements (which may be scale-dependent) and that oilseed rape can be an important forage resource for many colonies of bumblebees. Given this, we recommend sustainable management of this crop to benefit bumblebees.