Martin H. Entling

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.

High effectiveness of tailored flower strips in reducing pests and crop plant damage

Providing key resources to animals may enhance both their biodiversity and the ecosystem services they provide. We examined the performance of annual flower strips targeted at the promotion of natural pest control in winter wheat. Flower strips were experimentally sown along 10 winter wheat fields across a gradient of landscape complexity (i.e. proportion non-crop area within 750 m around focal fields) and compared with 15 fields with wheat control strips. We found strong reductions in cereal leaf beetle (CLB) density (larvae: 40%; adults of the second generation: 53%) and plant damage caused by CLB (61%) in fields with flower strips compared with control fields. Natural enemies of CLB were strongly increased in flower strips and in part also in adjacent wheat fields. Flower strip effects on natural enemies, pests and crop damage were largely independent of landscape complexity (8–75% non-crop area). Our study demonstrates a high effectiveness of annual flower strips in promoting pest control, reducing CLB pest levels below the economic threshold. Hence, the studied flower strip offers a viable alternative to insecticides. This highlights the high potential of tailored agri-environment schemes to contribute to ecological intensification and may encourage more farmers to adopt such schemes.

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.

Tailored flower strips promote natural enemy biodiversity and pest control in potato crops

Sown flower strips are increasingly implemented within agri-environment schemes (AES) to increase functional biodiversity and ecosystem services such as pollination or natural pest control, but their effectiveness in achieving these goals remains poorly studied. We tested the performance of experimentally sown annual flower strips specifically designed to promote natural enemies of aphids and their pest control services (tailored flower strips) in adjacent potato crops (n = 8) compared with control fields (n = 10). Flower strips consisted of 11 plant species providing abundant floral and extra-floral resources. The abundance of key natural enemies of aphids (hoverflies, lacewings and ladybirds) and hoverfly species richness was greatly enhanced in tailored flower strips compared with potato control strips. This resulted in an average increase in the number of eggs deposited by hoverflies and lacewings by 127% and 48%, respectively, and a reduction in the number of aphids by 75% in adjacent potato crops. Synthesis and applications. We conclude that tailored flower strips can be an effective agri-environmental measure to enhance natural enemies and aphid control in nearby crops. Indeed, tailored flower strips may help to reduce insecticide input in potato production as they significantly decrease the probability that action thresholds are reached. Promoting natural enemy abundance and diversity, as observed for hoverflies, may increase the stability of pest control and provide additional benefits to agro-ecosystems in terms of natural enemy conservation. We thus recommend establishing tailored flower strips as a promising management option to reconcile the objectives of ecological intensification and biodiversity conservation.

Review on environmental alterations propagating from aquatic to terrestrial ecosystems.

Terrestrial inputs into freshwater ecosystems are a classical field of environmental science. Resource fluxes (subsidy) from aquatic to terrestrial systems have been less studied, although they are of high ecological relevance particularly for the receiving ecosystem. These fluxes may, however, be impacted by anthropogenically driven alterations modifying structure and functioning of aquatic ecosystems. In this context, we reviewed the peer-reviewed literature for studies addressing the subsidy of terrestrial by aquatic ecosystems with special emphasis on the role that anthropogenic alterations play in this water-land coupling. Our analysis revealed a continuously increasing interest in the coupling of aquatic to terrestrial ecosystems between 1990 and 2014 (total: 661 studies), while the research domains focusing on abiotic (502 studies) and biotic (159 studies) processes are strongly separated. Approximately 35% (abiotic) and 25% (biotic) of the studies focused on the propagation of anthropogenic alterations from the aquatic to the terrestrial system. Among these studies, hydromorphological and hydrological alterations were predominantly assessed, whereas water pollution and invasive species were less frequently investigated. Less than 5% of these studies considered indirect effects in the terrestrial system e.g. via food web responses, as a result of anthropogenic alterations in aquatic ecosystems. Nonetheless, these very few publications indicate far-reaching consequences in the receiving terrestrial ecosystem. For example, bottom-up mediated responses via soil quality can cascade over plant communities up to the level of herbivorous arthropods, while top-down mediated responses via predatory spiders can cascade down to herbivorous arthropods and even plants. Overall, the current state of knowledge calls for an integrated assessment on how these interactions within terrestrial ecosystems are affected by propagation of aquatic ecosystem alterations. To fill these gaps, we propose a scientific framework, which considers abiotic and biotic aspects based on an interdisciplinary approach.

Effects of habitat fragmentation on abundance, larval food and parasitism of a spider-hunting wasp.

Habitat fragmentation strongly affects species distribution and abundance. However, mechanisms underlying fragmentation effects often remain unresolved. Potential mechanisms are (1) reduced dispersal of a species or (2) altered species interactions in fragmented landscapes. We studied if abundance of the spider-hunting and cavity-nesting wasp Trypoxylon figulus Linnaeus (Hymenoptera: Crabronidae) is affected by fragmentation, and then tested for any effect of larval food (bottom up regulation) and parasitism (top down regulation). Trap nests of T. figulus were studied in 30 agricultural landscapes of the Swiss Plateau. The sites varied in the level of isolation from forest (adjacent, in the open landscape but connected, isolated) and in the amount of woody habitat (from 4 % to 74 %). We recorded wasp abundance (number of occupied reed tubes), determined parasitism of brood cells and analysed the diversity and abundance of spiders that were deposited as larval food. Abundances of T. figulus were negatively related to forest cover in the landscape. In addition, T. figulus abundances were highest at forest edges, reduced by 33.1% in connected sites and by 79.4% in isolated sites. The mean number of spiders per brood cell was lowest in isolated sites. Nevertheless, structural equation modelling revealed that this did not directly determine wasp abundance. Parasitism was neither related to the amount of woody habitat nor to isolation and did not change with host density. Therefore, our study showed that the abundance of T. figulus cannot be fully explained by the studied trophic interactions. Further factors, such as dispersal and habitat preference, seem to play a role in the population dynamics of this widespread secondary carnivore in agricultural landscapes.

Disentangling multiple drivers of pollination in a landscape-scale experiment

Animal pollination is essential for the reproductive success of many wild and crop plants. Loss and isolation of (semi-)natural habitats in agricultural landscapes can cause declines of plants and pollinators and endanger pollination services. We investigated the independent effects of these drivers on pollination of young cherry trees in a landscape-scale experiment. We included (i) isolation of study trees from other cherry trees (up to 350 m), (ii) the amount of cherry trees in the landscape, (iii) the isolation from other woody habitats (up to 200 m) and (iv) the amount of woody habitats providing nesting and floral resources for pollinators. At the local scale, we considered effects of (v) cherry flower density and (vi) heterospecific flower density. Pollinators visited flowers more often in landscapes with high amount of woody habitat and at sites with lower isolation from the next cherry tree. Fruit set was reduced by isolation from the next cherry tree and by a high local density of heterospecific flowers but did not directly depend on pollinator visitation. These results reveal the importance of considering the plants need for conspecific pollen and its pollen competition with co-flowering species rather than focusing only on pollinators’ habitat requirements and flower visitation. It proved to be important to disentangle habitat isolation from habitat loss, local from landscape-scale effects, and direct effects of pollen availability on fruit set from indirect effects via pollinator visitation to understand the delivery of an agriculturally important ecosystem service.

Large variation of suction sampling efficiency depending on arthropod groups, species traits, and habitat properties.

Suction sampling is widely used to estimate arthropod abundance and diversity. To test the reliability of abundance data derived from suction sampling, we examined sampling efficiency across a wide range of arthropod groups and tested for effects of species traits, vegetation density, and differences between sites. Suction sampling efficiency was quantified by vacuuming an enclosed meadow area and subsequent removal of the turf, which was treated with heat extraction to collect the remaining arthropods. We obtained 250 pairs of suction and turf samples from seven grasslands with variable vegetation density. High suction sampling efficiencies between 49 and 86% were obtained for Auchenorrhyncha, Heteroptera, Araneida, Curculionoidea, Hymenoptera, and Diptera. In contrast, efficiencies were below 30% for Aphidae, Thysanoptera, Staphylinidae and other Coleoptera, and for soil arthropods such as Collembola, Isopoda, Diplopoda, and Formicidae. Efficiency varied significantly among habitats (sites) for most groups, often more than two‐fold. Surprisingly, sampling efficiency for Hymenoptera, Diplopoda, and Collembola increased with vegetation density, probably because aboveground activity of these taxa was higher in dense vegetation. Suction sampling was nearly twice as efficient for spiders living in the vegetation than for spiders living near the soil surface, and cursorial and large‐bodied spider species were more efficiently sampled than web‐builders and small species. Depending on the sampling effort, suction sampling missed between 49% (one sample) and 31% (250 samples) of the spider species present. Suction sampling efficiency varied more strongly among sites and among arthropod groups than previously recognized. Abundance data derived from suction sampling are strongly underestimated, especially for arthropods living near the soil surface. Thus, comparisons of abundance and diversity between sites should be restricted to vegetation‐dwelling species of the most efficiently sampled groups. The positive relationship of sampling efficiency with vegetation density demonstrates that variation in efficiency is mediated by arthropod behaviour.

High bee and wasp diversity in a heterogeneous tropical farming system compared to protected forest.

It is a globally important challenge to meet increasing demands for resources and, at the same time, protect biodiversity and ecosystem services. Farming is usually regarded as a major threat to biodiversity due to its expansion into natural areas. We compared biodiversity of bees and wasps between heterogeneous small-scale farming areas and protected forest in northern coastal Belize, Central America. Malaise traps operated for three months during the transition from wet to dry season. Farming areas consisted of a mosaic of mixed crop types, open habitat, secondary forest, and agroforestry. Mean species richness per site (alpha diversity), as well as spatial and temporal community variation (beta diversity) of bees and wasps were equal or higher in farming areas compared to protected forest. The higher species richness and community variation in farmland was due to additional species that did not occur in the forest, whereas most species trapped in forest were also found in farming areas. The overall regional species richness (gamma diversity) increased by 70% with the inclusion of farming areas. Our results suggest that small-scale farming systems adjacent to protected forest may not only conserve, but even favour, biodiversity of some taxonomic groups. We can, however, not exclude possible declines of bee and wasp diversity in more intensified farmland or in landscapes completely covered by heterogeneous farming systems.

Arthropod Colonisation of Trees in Fragmented Landscapes Depends on Species Traits

Effects of habitat fragmentation vary greatly between organisms. Traits such as dispersal mode and habitat preference may explain these differences. We predict that organisms with low dispersal abilities respond mainly to habitat isolation whereas aerial colonisers respond to the amount of suitable habitats at the landscape scale. To test these predictions 30 sites were chosen that varied independently in the level of isolation from woody habitats and in the percentage of woody habitats in 500 m circumference. At each site seven cherry trees were established. Overwintering arthropods were sampled using cardboard hides. Glue rings were attached around tree stems to distinguish between walking and aerial colonisers. As predicted for walking dispersers, earwig abundance was strongly affected by habitat isolation. In contrast, three species of ballooning spiders responded neither to glue rings nor to habitat isolation. Instead they were affected by habitat amount in accordance with their preferred habitats. These results strongly encourage the use of species traits to predict effects of landscape fragmentation on organisms. However, additional factors such as interactions between species groups need also to be taken into account.