J. M. Holland

The value of uncropped field margins for foraging bumblebees

The intensification of agriculture has led to declines in species diversity and abundance within groups of certain flora and fauna. Bumblebees (Bombus spp.) are one group where a decline has been documented, and it is thought to be attributable to a decrease in forage resources and potential nest sites. As bumblebees play an important role in the pollination of many entomophilous crops, this decline could impact on agricultural productivity. We examined the role of naturally regenerated field margins in providing forage plants on land where nectar resources are otherwise impoverished. The following question was addressed – Are naturally regenerated unsprayed field margins more attractive to foraging bumblebees and honeybees than cropped field margins managed as conservation headlands? Significantly more bees visited naturally regenerated field margins than cropped field margins. Honeybees (Apis mellifera), Bombus terrestris, and Bombus lapidarius were the most commonly observed bee species. Different wildflower species within the naturally regenerated margins varied greatly in relative number of visits received, and bumblebee species were found to prefer different flower species to honeybees. The potential role that naturally regenerated field margins could play in the conservation of bumblebee species, and the implications for other species of flora and fauna, are discussed.

Intraguild predation in winter wheat: prey choice by a common epigeal carabid consuming spiders

Predators can provide a valuable ecosystem service by suppressing crop pests. However, intraguild predation, where predators compete for the same prey resource whilst consuming each other, may destabilize population dynamics and increase the risk of pest outbreaks. Very little is known about intraguild predation in open fields or the strengths of trophic links between predators which may negatively affect pest control. We tested the null hypothesis that predation by the epigeal predator Pterostichus melanarius (Coleoptera: Carabidae) on different spiders is species-independent (proportional to density). A combination of population monitoring in winter wheat, molecular identification of juvenile spiders, molecular analysis of predator gut contents and a Monte Carlo simulation model were used to analyse prey choice. Pterostichus melanarius were pitfall-trapped over three months, and 622 individuals were screened for the remains of four spider species. Predation rates on spiders were 43·6% in June and 33·3% in August and showed clear evidence of prey choice. Predation on the web-dependent Tenuiphantes tenuis (Linyphiidae) was significantly greater than predicted from a random choice model, while predation on Bathyphantes gracilis (Linyphiidae) was significantly lower. The beetles may be selecting the most abundant species disproportionately (switching) or responding in some cases to spatial niche separation (T. tenuis locate their webs marginally lower than B. gracilis). However, two itinerant hunters, Erigone spp. (Linyphiidae) and Pachygnatha degeeri (Tetragnathidae), were consumed in proportion to their density. Synthesis and applications. High levels of intraguild predation were revealed using molecular diagnostics. The gut analysis approach provided invaluable data that will inform the future design of appropriate pest management and integrated farming strategies that encourage these predators. The data showed strong evidence of prey choice. Managers can, however, probably encourage high densities of all these known aphid predators (spiders and carabids) because disproportionately high rates of predation on the most common spiders at our field sites (T. tenuis) were not sufficient to prevent strong growth in the density of this species between June and August (adults increased × 1·6 and juveniles × 8·6). Such work is essential if we are to reveal the processes behind functional biodiversity in crops.

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.

Botanical diversity of beetle banks: Effects of age and comparison with conventional arable field margins in southern UK

Beetle banks are simple, grass-sown raised strips providing habitat for the invertebrate predators of arable crop pests and other farmland wildlife. To date, research has mainly focussed on such predators. Establishment guidelines for these features, which are considered as inexpensive substitutes for the considerable amount of hedgerows that have been lost in the UK, are available, as is some funding, but long-term management guidance is lacking. The botanical composition and diversity of a range of beetle banks was examined in southern UK over two summers and a winter, and compared with that of typical, adjacent field margins including grassy strips and hedgebanks, with a view to indicating potential management requirements.

Structure, function and management of semi-natural habitats for conservation biological control : A review of European studies

Different semi-natural habitats occur on farmland, and it is the vegetations traits and structure that subsequently determine their ability to support natural enemies and their associated contribution to conservation biocontrol. New habitats can be created and existing ones improved with agri-environment scheme funding in all EU member states. Understanding the contribution of each habitat type can aid the development of conservation control strategies. Here we review the extent to which the predominant habitat types in Europe support natural enemies, whether this results in enhanced natural enemy densities in the adjacent crop and whether this leads to reduced pest densities. Considerable variation exists in the available information for the different habitat types and trophic levels. Natural enemies within each habitat were the most studied, with less information on whether they were enhanced in adjacent fields, while their impact on pests was rarely investigated. Most information was available for woody and herbaceous linear habitats, yet not for woodland which can be the most common semi-natural habitat in many regions. While the management and design of habitats offer potential to stimulate conservation biocontrol, we also identified knowledge gaps. A better understanding of the relationship between resource availability and arthropod communities across habitat types, the spatiotemporal distribution of resources in the landscape and interactions with other factors that play a role in pest regulation could contribute to an informed management of semi-natural habitats for biocontrol.

Targeted agri-environment schemes significantly improve the population size of common farmland bumblebee species

Changes in agricultural practice across Europe and North America have been associated with range contractions and local extinction of bumblebees (Bombus spp.). A number of agri‐environment schemes have been implemented to halt and reverse these declines, predominantly revolving around the provision of additional forage plants. Although it has been demonstrated that these schemes can attract substantial numbers of foraging bumblebees, it remains unclear to what extent they actually increase bumblebee populations. We used standardized transect walks and molecular techniques to compare the size of bumblebee populations between Higher Level Stewardship (HLS) farms implementing pollinator‐friendly schemes and Entry Level Stewardship (ELS) control farms. Bumblebee abundance on the transect walks was significantly higher on HLS farms than ELS farms. Molecular analysis suggested maximum foraging ranges of 566 m for Bombus hortorum, 714 m for B. lapidarius, 363 m for B. pascuorum and 799 m for B. terrestris. Substantial differences in maximum foraging range were found within bumblebee species between farm types. Accounting for foraging range differences, B. hortorum (47 vs 13 nests/km2) and B. lapidarius (45 vs 22 nests/km2) were found to nest at significantly greater densities on HLS farms than ELS farms. There were no significant differences between farm type for B. terrestris (88 vs 38 nests/km2) and B. pascuorum (32 vs 39 nests/km2). Across all bumblebee species, HLS management had a significantly positive effect on bumblebee nest density. These results show that targeted agri‐environment schemes that increase the availability of suitable forage can significantly increase the size of wild bumblebee populations.

Using functional traits to quantify the value of plant communities to invertebrate ecosystem service providers in arable landscapes

1. The loss of farmland biodiversity threatens the sustainability of ecosystem services delivered within agricultural landscapes. The functional trait approach has been successfully used in grassland systems to quantify trade-offs and synergies between services delivered directly by plant communities. Many of the services delivered by arable landscapes, however, depend on invertebrate consumers, and the application of the trait-based approach to these systems depends on quantifying functional relationships between trophic levels. 2. Two data sets of plant and invertebrate communities from a range of annual crops and uncropped land habitats were analysed. The community-weighted means of plant functional traits were calculated for the vegetation samples and used as the explanatory variables in a multivariate analysis of plant species composition across habitats. The constrained axes scores were used in statistical models to explain the variance in associated total invertebrate abundance, phytophagous invertebrates and invertebrate numbers weighted by importance in the diet of farmland bird chicks. 3. The multivariate analysis discriminated between plant communities characterized by ruderal traits (high specific leaf area and early flowering) and those with more competitive traits. More ruderal communities also supported proportionally more invertebrates. The suite of traits included in the analysis explained a greater proportion of the variance in invertebrate abundance between uncropped habitats, as opposed to between annual crops. 4. The overlap between the plant traits that respond to disturbance (functional response traits) and those that affect the abundance of phytophagous invertebrates (functional effect traits) and the diet of farmland birds demonstrates the potential for using common functional metrics to integrate the assessment of an ecosystem service across different habitats particularly on uncropped land where intensity of disturbance is the main environmental driver. 5. Synthesis. The quantification of functional linkages between arable plants and the abundance of their associated invertebrate consumer communities is the first step in extending the trait-based approach to quantify trade-offs and synergies between ecosystem services developed in grassland systems to landscapes dominated by arable crops. However, applying the functional approach to in-crop weed communities and other service providers such as pollinators will require the incorporation of additional response and effect traits.

Providing foraging resources for solitary bees on farmland: current schemes for pollinators benefit a limited suite of species

1. Changes in agricultural practice across Europe and North America have been associated with range contractions and a decline in the abundance of wild bees. Concerns at these declines has led to the development of flower-rich agri-environment schemes as a way to enhance bee diversity and abundance. Whilst the effect of these schemes on bumblebee species (Bombus spp.) has been well studied, their impact on the wider bee community is poorly understood. 2. We used direct observations of foraging bees and pollen load analysis to quantify the relative contribution that sown flowers (i.e. those included in agri-environment scheme seed mixes) make to the pollen diets of wild solitary bees on Higher Level Stewardship farms (HLS) implementing pollinator-focused schemes and on Entry Level Stewardship farms (ELS) without such schemes in southern England, UK. 3. HLS management significantly increased floral abundance, and as the abundance of sown flowers increased these sown plants were utilised for pollen by a greater proportion of the solitary bee species present. However, the overall proportion of pollen collected from sown plants was low for both direct observations (27.0%) and pollen load analysis (23.3%). 4. At most only 25 of the 72 observed species of solitary bee (34.7%) were recorded utilising sown plants to a meaningful degree. The majority of solitary bee species did not collect pollen from flower species sown for pollinators. 5. Total bee species richness was significantly associated with plant species richness, but there was no difference in the total species richness of either bee or flowering plant species between HLS and ELS farms. 6. Synthesis and applications. These results show that the majority of solitary bee species present on farmland in the south-east of England collect the majority of their pollen from plants that persist unaided in the wider environment, not from those included in agri-environment schemes focused on pollinators. If diverse bee communities are to be maintained on farmland, existing schemes should contain an increased number of flowering plant species and additional schemes that increase the diversity of flowering plants in complementary habitats should be studied and trialled.

Monoclonal antibodies reveal changes in predator efficiency with prey spatial pattern

Spatially explicit predator–prey interactions can alter the predatory potential of natural enemies augmented through conservation biological control. To test hypotheses regarding such interactions and predatory efficiency, we used a combination of molecular techniques and mark–release–recapture to study the foraging behaviour of a generalist carabid predator, Poecilus cupreus, in response to spatial patterns of its cereal aphid prey (Metapolophium dirhodum and Sitobion avenae). Beetle and aphid numbers were measured across two grids of sampling locations, within which aphid spatial pattern had been manipulated to generate patchy and more homogenous distributions. Aphid consumption was measured by enzyme‐linked immunosorbent assays (ELISA) of beetle gut contents, using an aphid‐specific monoclonal antibody. Movement and distribution patterns suggest that P. cupreus does not aggregate at, nor instigate prey‐taxis within, aphid patches. However, more than two‐thirds of the 2169 P. cupreus tested by ELISA had consumed aphids and the proportion of beetles containing aphid proteins was positively related to aphid density. Against expectation, the proportion of predators feeding on aphids was greatest where prey were homogenously distributed, and this was attributed to the loss of partial refuges for prey in aphid patches. The functional value of this type of uniform foraging strategy is ideally suited to early colonization of the crop habitat, when aphid numbers are low, before populations build up and form strong spatial patterns.

Semi-natural habitats support biological control, pollination and soil conservation in Europe. A review

Semi-natural habitats are integral to most agricultural areas and have the potential to support ecosystem services, especially biological control and pollination by supplying resources for the invertebrates providing these services and for soil conservation by preventing erosion and run-off. Some habitats are supported through agri-environment scheme funding in the European Union, but their value for ecosystem service delivery has been questioned. An improved understanding of previous research approaches and outcomes will contribute to the development of more sustainable farming systems, improve experimental designs and highlight knowledge gaps especially for funders and researchers. Here we compiled a systematic map to allow for the first time a review of the quantity of evidence collected in Europe that semi-natural habitats support biological control, pollination and soil conservation. A literature search selected 2252 publications, and, following review, 270 met the inclusion criteria and were entered into the database. Most publications were of pest control (143 publications) with less on pollination (78 publications) or soil-related aspects (31). For pest control and pollination, most publications reported a positive effect of semi-natural habitats. There were weaknesses in the evidence base though because of bias in study location and the crops, whilst metrics (e.g. yield) valued by end users were seldom measured. Hedgerows, woodland and grassland were the most heavily investigated semi-natural habitats, and the wider landscape composition was often considered. Study designs varied considerably yet only 24% included controls or involved manipulation of semi-natural habitats. Service providers were commonly measured and used as a surrogate for ecosystem service delivery. Key messages for policymakers and funders are that they should encourage research that includes more metrics required by end users, be prepared to fund longer-term studies (61% were of only 1-year duration) and investigate the role of soils within semi-natural habitats in delivering ecosystem services.