Location and Creation of Nest Sites for Ground-Nesting Bees in Apple Orchards.

Wild ground-nesting bees are key pollinators of apple (Malus domestica). We explored, (1) where they choose to nest, (2) what influences site selection and (3) species richness in orchards. Twenty-three orchards were studied over three years; twelve were treated with additional herbicide to increase bare ground with the remainder as untreated controls. Vegetation cover, soil type, soil compaction, nest number and location, and species were recorded. Fourteen species of ground-nesting solitary/eusocial bee were identified. Most nests were in areas free of vegetation and areas treated with additional herbicide were utilised by ground nesting bees within three years of application. Nests were also evenly distributed along the vegetation-free strips underneath the apple trees. This area was an important ground-nesting bee habitat with mean numbers of nests at peak nest activity of 873 per ha (range 44-5705), and 1153 per ha (range 0-4082) in 2018 and 2019, respectively. Increasing and maintaining areas of bare ground in apple orchards during peak nesting events could improve nesting opportunities for some species of ground-nesting bee and, combined with flowers strips, be part of a more sustainable pollinator management approach. The area under the tree row is an important contributor to the ground-nesting bee habitat and should be kept bare during peak nesting.

Conservation measures or hotspots of disease transmission? Agri-environment schemes can reduce disease prevalence in pollinator communities.

Insects are under pressure from agricultural intensification. To protect pollinators, conservation measures such as the EU agri-environment schemes (AES) promote planting wildflowers along fields. However, this can potentially alter disease ecology by serving as transmission hubs or by diluting infections. We tested this by measuring plant-pollinator interactions and virus infections (DWV-A, DWV-B and ABPV) across pollinator communities in agricultural landscapes over a year. AES had a direct effect on DWV-B, reducing prevalence and load in honeybees, with a tentative general dilution effect on load in early summer. DWV-A prevalence was reduced both under AES and with increasing niche overlap between competent hosts, likely via a dilution effect. By contrast, AES had no impact on ABPV, its prevalence driven by the proportion of bumblebees in the community. Epidemiological differences were also reflected in the virus phylogenies, with DWV-B showing recent rapid expansion, while DWV-A and ABPV showed slower growth rates and geographical population structure. Phylogenies indicate that all three viruses freely circulate across their host populations. Our study illustrates how complex interactions between environmental, ecological and evolutionary factors may influence wildlife disease dynamics. Supporting pollinator nutrition can mitigate the transmission of important bee diseases, providing an unexpected boost to pollinator conservation. This article is part of the theme issue 'Infectious disease ecology and evolution in a changing world'.

Addressing pollination deficits in orchard crops through habitat management for wild pollinators.

There is increasing evidence that farmers in many areas are achieving below maximum yields due to insufficient pollination. Practical and effective approaches are needed to maintain wild pollinator populations within agroecosystems so they can deliver critical pollination services that underpin crop production. We established nesting and wildflower habitat interventions in 24 UK apple orchards and measured effects on flower-visiting insects and the pollination they provide, exploring how this was affected by landscape context. We quantified the extent of pollination deficits and assessed whether the management of wild pollinators can reduce deficits and deliver improved outcomes for growers over 3 years. Wildflower interventions increased solitary bee numbers visiting apple flowers by over 20%, but there was no effect of nesting interventions. Other pollinator groups were influenced by both local and landscape-scale factors, with bumblebees and hoverflies responding to the relative proportion of semi-natural habitat at larger spatial scales (1000 m), while honeybees and other flies responded at 500 m or less. By improving fruit number and quality, pollinators contributed more than £16 k per hectare. However, deficits (where maximum potential was not being reached due to a lack of pollination) were recorded and the extent of these varied across orchards, and from year to year, with a 22% deficit in output in the worst (equivalent to ~£14 k/ha) compared to less than 3% (equivalent to ~£2 k/ha) in the best year. Although no direct effect of our habitat interventions on deficits in gross output was observed, initial fruit set and seed set deficits were reduced by abundant bumblebees, and orchards with a greater abundance of solitary bees saw lower deficits in fruit size. The abundance of pollinators in apple orchards is influenced by different local and landscape factors that interact and vary between years. Consequently, pollination, and the extent of economic output deficits, also vary between orchards and years. We highlight how approaches, including establishing wildflower areas and optimizing the ratio of cropped and non-cropped habitats can increase the abundance of key apple pollinators and improve outcomes for growers.

Increasing flower species richness in agricultural landscapes alters insect pollinator networks: Implications for bee health and competition.

Ecological restoration programs are established to reverse land degradation, mitigate biodiversity loss, and reinstate ecosystem services. Following recent agricultural intensification that led to a decrease in flower diversity and density in rural areas and subsequently to the decline of many insects, conservation measures targeted at pollinators have been established, including sown wildflower strips (WFS) along field margins. Historically successful in establishing a high density of generalist bees and increasing pollinator diversity, the impact of enhanced flower provision on wider ecological interactions and the structure of pollinator networks has been rarely investigated. Here, we tested the effects of increasing flower species richness and flower density in agricultural landscapes on bee-plant interaction networks. We measured plant species richness and flower density and surveyed honeybee and bumblebee visits on flowers across a range of field margins on 10 UK farms that applied different pollinator conservation measures. We found that both flower species richness and flower density significantly increased bee abundance, in early and late summer, respectively. At the network level, we found that higher flower species richness did not significantly alter bee species' generality indices, but significantly reduced network connectance and marginally reduced niche overlap across honeybees and bumblebee species, a proxy for insect competition. While higher connectance and niche overlap is believed to strengthen network robustness and often is the aim for the restoration of pollinator networks, we argue that carefully designed WFS may benefit bees by partitioning their foraging niche, limiting competition for resources and the potential for disease transmission via shared floral use. We also discuss the need to extend WFS and their positive effects into spring when wild bee populations are established.

Establishment and management of wildflower areas for insect pollinators in commercial orchards.

Sown wildflower areas are increasingly recommended as an agri-environmental intervention measure, but evidence for their success is limited to particular insect groups or hampered by the challenges of establishing seed mixes and maintaining flower abundance over time. We conducted a replicated experiment to establish wildflower areas to support insect pollinators in apple orchards. Over three years, and across 23 commercial UK orchards with and without sown wildflowers, we conducted 828 transect surveys across various non-crop habitats. We found that the abundance of flower-visiting solitary bees, bumblebees, honeybees, and beetles was increased in sown wildflower areas, compared with existing non-crop habitats in control orchards, from the second year following floral establishment. Abundance of hoverflies and other non-syrphid flies was increased in wildflower areas from the first year. Beyond the effect of wildflower areas, solitary bee abundance was also positively related to levels of floral cover in other local habitats within orchards, but neither local nor wider landscape-scale context affected abundance of other studied insect taxa within study orchards. There was a change in plant community composition on the sown wildflower areas between years, and in patterns of flowering within and between years, showing a succession from unsown weedy species towards a dominance of sown species over time. We discuss how the successful establishment of sown wildflower areas and delivery of benefits for different insect taxa relies on appropriate and reactive management practices as a key component of any such agri-environment scheme.

occAssess: An R package for assessing potential biases in species occurrence data.

Species occurrence records from a variety of sources are increasingly aggregated into heterogeneous databases and made available to ecologists for immediate analytical use. However, these data are typically biased, i.e. they are not a probability sample of the target population of interest, meaning that the information they provide may not be an accurate reflection of reality. It is therefore crucial that species occurrence data are properly scrutinised before they are used for research. In this article, we introduce occAssess, an R package that enables straightforward screening of species occurrence data for potential biases. The package contains a number of discrete functions, each of which returns a measure of the potential for bias in one or more of the taxonomic, temporal, spatial, and environmental dimensions. Users can opt to provide a set of time periods into which the data will be split; in this case separate outputs will be provided for each period, making the package particularly useful for assessing the suitability of a dataset for estimating temporal trends in species' distributions. The outputs are provided visually (as ggplot2 objects) and do not include a formal recommendation as to whether data are of sufficient quality for any given inferential use. Instead, they should be used as ancillary information and viewed in the context of the question that is being asked, and the methods that are being used to answer it. We demonstrate the utility of occAssess by applying it to data on two key pollinator taxa in South America: leaf-nosed bats (Phyllostomidae) and hoverflies (Syrphidae). In this worked example, we briefly assess the degree to which various aspects of data coverage appear to have changed over time. We then discuss additional applications of the package, highlight its limitations, and point to future development opportunities.

Opportunities to reduce pollination deficits and address production shortfalls in an important insect-pollinated crop.

Pollinators face multiple pressures and there is evidence of populations in decline. As demand for insect-pollinated crops increases, crop production is threatened by shortfalls in pollination services. Understanding the extent of current yield deficits due to pollination and identifying opportunities to protect or improve crop yield and quality through pollination management is therefore of international importance. To explore the extent of "pollination deficits," where maximum yield is not being achieved due to insufficient pollination, we used an extensive dataset on a globally important crop, apples. We quantified how these deficits vary between orchards and countries and we compared "pollinator dependence" across different apple varieties. We found evidence of pollination deficits and, in some cases, risks of overpollination were even apparent for which fruit quality could be reduced by too much pollination. In almost all regions studied we found some orchards performing significantly better than others in terms of avoiding a pollination deficit and crop yield shortfalls due to suboptimal pollination. This represents an opportunity to improve production through better pollinator and crop management. Our findings also demonstrated that pollinator dependence varies considerably between apple varieties in terms of fruit number and fruit quality. We propose that assessments of pollination service and deficits in crops can be used to quantify supply and demand for pollinators and help to target local management to address deficits although crop variety has a strong influence on the role of pollinators.

Patterns of invertebrate functional diversity highlight the vulnerability of ecosystem services over a 45-year period.

Declines in invertebrate biodiversity1,2 pose a significant threat to key ecosystem services.3-5 Current analyses of biodiversity often focus on taxonomic diversity (e.g., species richness),6,7 which does not account for the functional role of a species. Functional diversity of species' morphological or behavioral traits is likely more relevant to ecosystem service delivery than taxonomic diversity, as functional diversity has been found to be a key driver of a number of ecosystem services including decomposition and pollination.8-12 At present, we lack a good understanding of long-term and large-scale changes in functional diversity, which limits our capacity to determine the vulnerability of key ecosystem services with ongoing biodiversity change. Here we derive trends in functional diversity and taxonomic diversity over a 45-year period across Great Britain for species supporting freshwater aquatic functions, pollination, natural pest control, and agricultural pests (a disservice). Species supporting aquatic functions showed a synchronous collapse and recovery in functional and taxonomic diversity. In contrast, pollinators showed an increase in taxonomic diversity, but a decline and recovery in functional diversity. Pest control agents and pests showed greater stability in functional diversity over the assessment period. We also found that functional diversity could appear stable or show patterns of recovery, despite ongoing changes in the composition of traits among species. Our results suggest that invertebrate assemblages can show considerable variability in their functional structure over time at a national scale, which provides an important step in determining the long-term vulnerability of key ecosystem services with ongoing biodiversity change.

No severe genetic bottleneck in a rapidly range-expanding bumblebee pollinator.

Genetic bottlenecks can limit the success of populations colonizing new ranges. However, successful colonizations can occur despite bottlenecks, a phenomenon known as the genetic paradox of invasion. Eusocial Hymenoptera such as bumblebees (Bombus spp.) should be particularly vulnerable to genetic bottlenecks, since homozygosity at the sex-determining locus leads to costly diploid male production (DMP). The Tree Bumblebee (Bombus hypnorum) has rapidly colonized the UK since 2001 and has been highlighted as exemplifying the genetic paradox of invasion. Using microsatellite genotyping, combined with the first genetic estimates of DMP in UK B. hypnorum, we tested two alternative genetic hypotheses ('bottleneck' and 'gene flow' hypotheses) for B. hypnorum's colonization of the UK. We found that the UK population has not undergone a recent severe genetic bottleneck and exhibits levels of genetic diversity falling between those of widespread and range-restricted Bombus species. Diploid males occurred in 15.4% of reared colonies, leading to an estimate of 21.5 alleles at the sex-determining locus. Overall, the findings show that this population is not bottlenecked, instead suggesting that it is experiencing continued gene flow from the continental European source population with only moderate loss of genetic diversity, and does not exemplify the genetic paradox of invasion.

A validated workflow for rapid taxonomic assignment and monitoring of a national fauna of bees (Apiformes) using high throughput DNA barcoding.

Improved taxonomic methods are needed to quantify declining populations of insect pollinators. This study devises a high-throughput DNA barcoding protocol for a regional fauna (United Kingdom) of bees (Apiformes), consisting of reference library construction, a proof-of-concept monitoring scheme, and the deep barcoding of individuals to assess potential artefacts and organismal associations. A reference database of cytochrome oxidase c subunit 1 (cox1) sequences including 92.4% of 278 bee species known from the UK showed high congruence with morphological taxon concepts, but molecular species delimitations resulted in numerous split and (fewer) lumped entities within the Linnaean species. Double tagging permitted deep Illumina sequencing of 762 separate individuals of bees from a UK-wide survey. Extracting the target barcode from the amplicon mix required a new protocol employing read abundance and phylogenetic position, which revealed 180 molecular entities of Apiformes identifiable to species. An additional 72 entities were ascribed to nuclear pseudogenes based on patterns of read abundance and phylogenetic relatedness to the reference set. Clustering of reads revealed a range of secondary operational taxonomic units (OTUs) in almost all samples, resulting from traces of insect species caught in the same traps, organisms associated with the insects including a known mite parasite of bees, and the common detection of human DNA, besides evidence for low-level cross-contamination in pan traps and laboratory procedures. Custom scripts were generated to conduct critical steps of the bioinformatics protocol. The resources built here will greatly aid DNA-based monitoring to inform management and conservation policies for the protection of pollinators.

Widespread losses of pollinating insects in Britain.

Pollination is a critical ecosystem service underpinning the productivity of agricultural systems across the world. Wild insect populations provide a substantial contribution to the productivity of many crops and seed set of wild flowers. However, large-scale evidence on species-specific trends among wild pollinators are lacking. Here we show substantial inter-specific variation in pollinator trends, based on occupancy models for 353 wild bee and hoverfly species in Great Britain between 1980 and 2013. Furthermore, we estimate a net loss of over 2.7 million occupied 1 km2 grid cells across all species. Declines in pollinator evenness suggest that losses were concentrated in rare species. In addition, losses linked to specific habitats were identified, with a 55% decline among species associated with uplands. This contrasts with dominant crop pollinators, which increased by 12%, potentially in response agri-environment measures. The general declines highlight a fundamental deterioration in both wider biodiversity and non-crop pollination services.

Spatial ecology of a range-expanding bumble bee pollinator.

Molecular methods have greatly increased our understanding of the previously cryptic spatial ecology of bumble bees (Bombus spp.), with knowledge of the spatial ecology of these bees being central to conserving their essential pollination services. Bombus hypnorum, the Tree Bumble Bee, is unusual in that it has recently rapidly expanded its range, having colonized much of the UK mainland since 2001. However, the spatial ecology of B. hypnorum has not previously been investigated. To address this issue, and to investigate whether specific features of the spatial ecology of B. hypnorum are associated with its rapid range expansion, we used 14 microsatellite markers to estimate worker foraging distance, nest density, between-year lineage survival rate and isolation by distance in a representative UK B. hypnorum population. After assigning workers to colonies based on full or half sibship, we estimated the mean colony-specific worker foraging distance as 103.6 m, considerably less than values reported from most other bumble bee populations. Estimated nest density was notably high (2.56 and 0.72 colonies ha-1 in 2014 and 2015, respectively), estimated between-year lineage survival rate was 0.07, and there was no evidence of fine-scale isolation by distance. In addition, genotyping stored sperm dissected from sampled queens confirmed polyandry in this population (mean minimum mating frequency of 1.7 males per queen). Overall, our findings establish critical spatial ecological parameters and the mating system of this unusual bumble bee population and suggest that short worker foraging distances and high nest densities are associated with its rapid range expansion.

Bumblebee family lineage survival is enhanced in high-quality landscapes.

Insect pollinators such as bumblebees (Bombus spp.) are in global decline. A major cause of this decline is habitat loss due to agricultural intensification. A range of global and national initiatives aimed at restoring pollinator habitats and populations have been developed. However, the success of these initiatives depends critically upon understanding how landscape change affects key population-level parameters, such as survival between lifecycle stages, in target species. This knowledge is lacking for bumblebees, because of the difficulty of systematically finding and monitoring colonies in the wild. We used a combination of habitat manipulation, land-use and habitat surveys, molecular genetics and demographic and spatial modelling to analyse between-year survival of family lineages in field populations of three bumblebee species. Here we show that the survival of family lineages from the summer worker to the spring queen stage in the following year increases significantly with the proportion of high-value foraging habitat, including spring floral resources, within 250-1,000 m of the natal colony. This provides evidence for a positive impact of habitat quality on survival and persistence between successive colony cycle stages in bumblebee populations. These findings also support the idea that conservation interventions that increase floral resources at a landscape scale and throughout the season have positive effects on wild pollinators in agricultural landscapes.

Effects of habitat composition and landscape structure on worker foraging distances of five bumble bee species.

Bumble bees (Bombus spp.) are important pollinators of both crops and wildflowers. Their contribution to this essential ecosystem service has been threatened over recent decades by changes in land use, which have led to declines in their populations. In order to design effective conservation measures, it is important to understand the effects of variation in landscape composition and structure on the foraging activities of worker bumble bees. This is because the viability of individual colonies is likely to be affected by the trade-off between the energetic costs of foraging over greater distances and the potential gains from access to additional resources. We used field surveys, molecular genetics, and fine resolution remote sensing to estimate the locations of wild bumble bee nests and to infer foraging distances across a 20-km² agricultural landscape in southern England, UK. We investigated five species, including the rare B. ruderatus and ecologically similar but widespread B. hortorum. We compared worker foraging distances between species and examined how variation in landscape composition and structure affected foraging distances at the colony level. Mean worker foraging distances differed significantly between species. Bombus terrestris, B. lapidarius, and B. ruderatus exhibited significantly greater mean foraging distances (551, 536, and 501 m, respectively) than B. hortorum and B. pascuorum (336 and 272 m, respectively). There was wide variation in worker foraging distances between colonies of the same species, which was in turn strongly influenced by the amount and spatial configuration of available foraging habitats. Shorter foraging distances were found for colonies where the local landscape had high coverage and low fragmentation of semi-natural vegetation, including managed agri-environmental field margins. The strength of relationships between different landscape variables and foraging distance varied between species, for example the strongest relationship for B. ruderatus being with floral cover of preferred forage plants. Our findings suggest that management of landscape composition and configuration has the potential to reduce foraging distances across a range of bumble bee species. There is thus potential for improvements in the design and implementation of landscape management options, such as agri-environment schemes, aimed at providing foraging habitat for bumble bees and enhancing crop pollination services.

How much flower-rich habitat is enough for wild pollinators? Answering a key policy question with incomplete knowledge.

In 2013, an opportunity arose in England to develop an agri-environment package for wild pollinators, as part of the new Countryside Stewardship scheme launched in 2015. It can be understood as a 'policy window', a rare and time-limited opportunity to change policy, supported by a narrative about pollinator decline and widely supported mitigating actions. An agri-environment package is a bundle of management options that together supply sufficient resources to support a target group of species. This paper documents information that was available at the time to develop such a package for wild pollinators. Four questions needed answering: (1) Which pollinator species should be targeted? (2) Which resources limit these species in farmland? (3) Which management options provide these resources? (4) What area of each option is needed to support populations of the target species? Focussing on wild bees, we provide tentative answers that were used to inform development of the package. There is strong evidence that floral resources can limit wild bee populations, and several sources of evidence identify a set of agri-environment options that provide flowers and other resources for pollinators. The final question could only be answered for floral resources, with a wide range of uncertainty. We show that the areas of some floral resource options in the basic Wild Pollinator and Farmland Wildlife Package (2% flower-rich habitat and 1 km flowering hedgerow), are sufficient to supply a set of six common pollinator species with enough pollen to feed their larvae at lowest estimates, using minimum values for estimated parameters where a range was available. We identify key sources of uncertainty, and stress the importance of keeping the Package flexible, so it can be revised as new evidence emerges about how to achieve the policy aim of supporting pollinators on farmland.

Fine-scale spatial genetic structure of common and declining bumble bees across an agricultural landscape.

Land-use changes have threatened populations of many insect pollinators, including bumble bees. Patterns of dispersal and gene flow are key determinants of species' ability to respond to land-use change, but have been little investigated at a fine scale (<10 km) in bumble bees. Using microsatellite markers, we determined the fine-scale spatial genetic structure of populations of four common Bombus species (B. terrestris, B. lapidarius, B. pascuorum and B. hortorum) and one declining species (B. ruderatus) in an agricultural landscape in Southern England, UK. The study landscape contained sown flower patches representing agri-environment options for pollinators. We found that, as expected, the B. ruderatus population was characterized by relatively low heterozygosity, number of alleles and colony density. Across all species, inbreeding was absent or present but weak (FIS  = 0.01-0.02). Using queen genotypes reconstructed from worker sibships and colony locations estimated from the positions of workers within these sibships, we found that significant isolation by distance was absent in B. lapidarius, B. hortorum and B. ruderatus. In B. terrestris and B. pascuorum, it was present but weak; for example, in these two species, expected relatedness of queens founding colonies 1 m apart was 0.02. These results show that bumble bee populations exhibit low levels of spatial genetic structure at fine spatial scales, most likely because of ongoing gene flow via widespread queen dispersal. In addition, the results demonstrate the potential for agri-environment scheme conservation measures to facilitate fine-scale gene flow by creating a more even distribution of suitable habitats across landscapes.

The potential impact of global warming on the efficacy of field margins sown for the conservation of bumble-bees.

Climate change is expected to drive species extinct by reducing their survival, reproduction and habitat. Less well appreciated is the possibility that climate change could cause extinction by changing the ecological interactions between species. If ecologists, land managers and policy makers are to manage farmland biodiversity sustainably under global climate change, they need to understand the ways in which species interact with each other as this will affect the way they respond to climate change. Here, we consider the ability of nectar flower mixtures used in field margins to provide sufficient forage for bumble-bees under future climate change. We simulated the effect of global warming on the network of plant-pollinator interactions in two types of field margin: a four-species pollen and nectar mix and a six-species wildflower mix. While periods without flowering resources and periods with no food were rare, curtailment of the field season was very common for the bumble-bees in both mixtures. The effect of this, however, could be ameliorated by adding extra species at the start and end of the flowering season. The plant species that could be used to future-proof margins against global warming are discussed.