Jeroen Scheper

Does conservation on farmland contribute to halting the biodiversity decline

Biodiversity continues to decline, despite the implementation of international conservation conventions and measures. To counteract biodiversity loss, it is pivotal to know how conservation actions affect biodiversity trends. Focussing on European farmland species, we review what is known about the impact of conservation initiatives on biodiversity. We argue that the effects of conservation are a function of conservation-induced ecological contrast, agricultural land-use intensity and landscape context. We find that, to date, only a few studies have linked local conservation effects to national biodiversity trends. It is therefore unknown how the extensive European agri-environmental budget for conservation on farmland contributes to the policy objectives to halt biodiversity decline. Based on this review, we identify new research directions addressing this important knowledge gap.

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.

Environmental factors driving the effectiveness of European agri‐environmental measures in mitigating pollinator loss – a meta‐analysis

In Europe, agri-environmental schemes (AES) have been introduced in response to concerns about farmland biodiversity declines. Yet, as AES have delivered variable results, a better understanding of what determines their success or failure is urgently needed. Focusing on pollinating insects, we quantitatively reviewed how environmental factors affect the effectiveness of AES. Our results suggest that the ecological contrast in floral resources created by schemes drives the response of pollinators to AES but that this response is moderated by landscape context and farmland type, with more positive responses in croplands (vs. grasslands) located in simple (vs. cleared or complex) landscapes. These findings inform us how to promote pollinators and associated pollination services in species-poor landscapes. They do not, however, present viable strategies to mitigate loss of threatened or endangered species. This indicates that the objectives and design of AES should distinguish more clearly between biodiversity conservation and delivery of ecosystem services.

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.

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.

Museum specimens reveal loss of pollen host plants as key factor driving wild bee decline in The Netherlands

Significance Growing concern about bee declines and associated loss of pollination services has increased the urgency to identify the underlying causes. So far, the identification of the key drivers of decline of bee populations has largely been based on speculation. We assessed the relative importance of a range of proposed factors responsible for wild bee decline and show that loss of preferred host plant species is one of the main factors associated with the decline of bee populations in The Netherlands. Interestingly, species foraging on crop plant families have stable or increasing populations. These results indicate that mitigation strategies for loss of wild bees will only be effective if they target the specific host plants of declining bee species. Evidence for declining populations of both wild and managed bees has raised concern about a potential global pollination crisis. Strategies to mitigate bee loss generally aim to enhance floral resources. However, we do not really know whether loss of preferred floral resources is the key driver of bee decline because accurate assessment of host plant preferences is difficult, particularly for species that have become rare. Here we examine whether population trends of wild bees in The Netherlands can be explained by trends in host plants, and how this relates to other factors such as climate change. We determined host plant preference of bee species using pollen loads on specimens in entomological collections that were collected before the onset of their decline, and used atlas data to quantify population trends of bee species and their host plants. We show that decline of preferred host plant species was one of two main factors associated with bee decline. Bee body size, the other main factor, was negatively related to population trend, which, because larger bee species have larger pollen requirements than smaller species, may also point toward food limitation as a key factor driving wild bee loss. Diet breadth and other potential factors such as length of flight period or climate change sensitivity were not important in explaining twentieth century bee population trends. These results highlight the species-specific nature of wild bee decline and indicate that mitigation strategies will only be effective if they target the specific host plants of declining species.

Local and landscape‐level floral resources explain effects of wildflower strips on wild bees across four European countries

Growing evidence for declines in wild bees calls for the development and implementation of effective mitigation measures. Enhancing floral resources is a widely accepted measure for promoting bees in agricultural landscapes, but effectiveness varies considerably between landscapes and regions. We hypothesize that this variation is mainly driven by a combination of the direct effects of measures on local floral resources and the availability of floral resources in the surrounding landscape. To test this, we established wildflower strips in four European countries, using the same seed mixture of forage plants specifically targeted at bees. We used a before-after control-impact approach to analyse the impacts of wildflower strips on bumblebees, solitary bees and Red List species and examined to what extent effects were affected by local and landscape-wide floral resource availability, land-use intensity and landscape complexity. Wildflower strips generally enhanced local bee abundance and richness, including Red-listed species. Effectiveness of the wildflower strips increased with the local contrast in flower richness created by the strips and furthermore depended on the availability of floral resources in the surrounding landscape, with different patterns for solitary bees and bumblebees. Effects on solitary bees appeared to decrease with increasing amount of late-season alternative floralresources in the landscape, whereas effects on bumblebees increased with increasing early-season landscape-wide floral resource availability.Synthesis and applications. Our study shows that the effects of wildflower strips on bees are largely driven by the extent to which local flower richness is increased. The effectiveness of this measure could therefore be enhanced by maximizing the number of bee forage species in seed mixtures, and by management regimes that effectively maintain flower richness in the strips through the years. In addition, for bumblebees specifically, our study highlights the importance of a continuous supply of food resources throughout the season. Measures that enhance early-season landscape-wide floral resource availability, such as the cultivation of oilseed rape, can benefit bumblebees by providing the essential resources for colony establishment and growth in spring. Further research is required to determine whether, and under what conditions, wildflower strips result in actual population-level effects. Our study shows that the effects of wildflower strips on bees are largely driven by the extent to which local flower richness is increased. The effectiveness of this measure could therefore be enhanced by maximizing the number of bee forage species in seed mixtures, and by management regimes that effectively maintain flower richness in the strips through the years. In addition, for bumblebees specifically, our study highlights the importance of a continuous supply of food resources throughout the season. Measures that enhance early-season landscape-wide floral resource availability, such as the cultivation of oilseed rape, can benefit bumblebees by providing the essential resources for colony establishment and growth in spring. Further research is required to determine whether, and under what conditions, wildflower strips result in actual population-level effects. (Less)

Mass-flowering crops dilute pollinator abundance in agricultural landscapes across Europe

Abstract Mass‐flowering crops (MFCs) are increasingly cultivated and might influence pollinator communities in MFC fields and nearby semi‐natural habitats (SNHs). Across six European regions and 2 years, we assessed how landscape‐scale cover of MFCs affected pollinator densities in 408 MFC fields and adjacent SNHs. In MFC fields, densities of bumblebees, solitary bees, managed honeybees and hoverflies were negatively related to the cover of MFCs in the landscape. In SNHs, densities of bumblebees declined with increasing cover of MFCs but densities of honeybees increased. The densities of all pollinators were generally unrelated to the cover of SNHs in the landscape. Although MFC fields apparently attracted pollinators from SNHs, in landscapes with large areas of MFCs they became diluted. The resulting lower densities might negatively affect yields of pollinator‐dependent crops and the reproductive success of wild plants. An expansion of MFCs needs to be accompanied by pollinator‐supporting practices in agricultural landscapes.

Size and sex-dependent shrinkage of Dutch bees during one-and-a-half centuries of land-use change

Land-use change and global warming are important factors driving bee decline, but it is largely unknown whether these drivers have resulted in changes in the life-history traits of bees. Recent studies have shown a stronger population decline of large- than small-bodied bee species, suggesting there may have been selective pressure on large, but not on small species to become smaller. Here we test this hypothesis by analyzing trends in bee body size of 18 Dutch species over a 147-year period using specimens from entomological collections. Large-bodied female bees shrank significantly faster than small-bodied female bees (6.5% and 0.5% respectively between 1900 and 2010). Changes in temperature during the flight period of bees did not influence the size-dependent shrinkage of female bees. Male bees did not shrink significantly over the same time period. Our results could imply that under conditions of declining habitat quantity and quality it is advantageous for individuals to be smaller. The size and sex-dependent responses of bees point towards an evolutionary response but genetic studies are required to confirm this. The declining body size of the large bee species that currently dominate flower visitation of both wild plants and insect-pollinated crops may have negative consequences for pollination service delivery.

Managing trap‐nesting bees as crop pollinators: Spatiotemporal effects of floral resources and antagonists

Summary 1.The decline of managed honeybees and the rapid expansion of mass-flowering crops increase the risk of pollination limitation in crops and raise questions about novel management approaches for wild pollinators in agroecosystems. Adding artificial nesting sites, such as trap nests, can promote cavity-nesting bees in agroecosystems, but effectiveness could be limited by the availability of floral resources in the surrounding landscape and by natural antagonists. 2.In two European regions, we exposed artificial trap nests in paired field boundaries adjacent to oilseed rape (OSR) fields or non-flowering crops for two years within 32 landscapes covering two independent gradients of OSR cover and semi-natural habitat (SNH) cover in the landscape. We analysed the effects of local and landscape-wide floral resource availability, land-use intensity, landscape complexity and natural antagonists on community composition and population dynamics of trap-nesting bees. 3.Number of brood cells showed a strong, three-fold increase in response to the additional nesting sites. Species richness and abundance of cavity-nesting bees that were active during OSR flowering increased significantly with increasing amount of early-season landscape-wide floral resource availability, such as the cultivation of OSR. Later foraging species benefited instead from the availability of late-season alternative flower resources or SNH cover once the mass-flowering had ceased. Density-dependent parasitism increased following mass-flowering, while no density-dependent effect was found during mass-flowering. 4.Structural equation modelling revealed that the influence of floral resource availability on community growth rate was mediated by community size. Community size showed a strong negative effect on community growth rate. Despite positive density-dependent parasitism, antagonists had only weak regulating effects on community growth rate. 5.Synthesis and applications. Trap-nesting bee populations grow markedly with the increasing availability of food resources in the landscape and effectiveness of trap nests is only marginally limited by natural antagonists. Thus, trap nests could be a simple pollinator-supporting strategy to accompany the current expansion of mass-flowering crops, and to ensure pollination services for insect-pollinated crops. Trap nests benefit not only early season active generalist bees during oilseed rape flowering but also species with later phenology if accompanied by other pollinator-supporting practices. This article is protected by copyright. All rights reserved.