Pollinator-mediated effects of landscape-scale land use on grassland plant community composition and ecosystem functioning - seven hypotheses.

Environmental change is disrupting mutualisms between organisms worldwide. Reported declines in insect populations and changes in pollinator community compositions in response to land use and other environmental drivers have put the spotlight on the need to conserve pollinators. While this is often motivated by their role in supporting crop yields, the role of pollinators for reproduction and resulting taxonomic and functional assembly in wild plant communities has received less attention. Recent findings suggest that observed and experimental gradients in pollinator availability can affect plant community composition, but we know little about when such shifts are to be expected, or the impact they have on ecosystem functioning. Correlations between plant traits related to pollination and plant traits related to other important ecosystem functions, such as productivity, nitrogen uptake or palatability to herbivores, lead us to expect non-random shifts in ecosystem functioning in response to changes in pollinator communities. At the same time, ecological and evolutionary processes may counteract these effects of pollinator declines, limiting changes in plant community composition, and in ecosystem functioning. Despite calls to investigate community- and ecosystem-level impacts of reduced pollination, the study of pollinator effects on plants has largely been confined to impacts on plant individuals or single-species populations. With this review we aim to break new ground by bringing together aspects of landscape ecology, ecological and evolutionary plant-insect interactions, and biodiversity-ecosystem functioning research, to generate new ideas and hypotheses about the ecosystem-level consequences of pollinator declines in response to land-use change, using grasslands as a focal system. Based on an integrated set of seven hypotheses, we call for more research investigating the putative pollinator-mediated links between landscape-scale land use and ecosystem functioning. In particular, future research should use combinations of experimental and observational approaches to assess the effects of changes in pollinator communities over multiple years and across species on plant communities and on trait distributions both within and among species.

Seed treatment with clothianidin induces changes in plant metabolism and alters pollinator foraging preferences.

Neonicotinoids, systemic insecticides that are distributed into all plant tissues and protect against pests, have become a common part of crop production, but can unintentionally also affect non-target organisms, including pollinators. Such effects can be direct effects from insecticide exposure, but neonicotinoids can affect plant physiology, and effects could therefore also be indirectly mediated by changes in plant phenology, attractiveness and nutritional value. Under controlled greenhouse conditions, we tested if seed treatment with the neonicotinoid clothianidin affected oilseed rape's production of flower resources for bees and the content of the secondary plant products glucosinolates that provide defense against herbivores. Additionally, we tested if seed treatment affected the attractiveness of oilseed rape to flower visiting bumblebees, using outdoor mesocosms. Flowers and leaves of clothianidin-treated plants had different profiles of glucosinolates compared with untreated plants. Bumblebees in mesocosms foraged slightly more on untreated plants. Neither flower timing, flower size nor the production of pollen and nectar differed between treatments, and therefore cannot explain any preference for untreated oilseed rape. We instead propose that this small but significant preference for untreated plants was related to the altered glucosinolate profile caused by clothianidin. Thereby, this study contributes to the understanding of the complex relationships between neonicotinoid-treated crops and pollinator foraging choices, by suggesting a potential mechanistic link by which insecticide treatment can affect insect behavior.

Biodiversity and pollination benefits trade off against profit in an intensive farming system.

Agricultural expansion and intensification have boosted global food production but have come at the cost of environmental degradation and biodiversity loss. Biodiversity-friendly farming that boosts ecosystem services, such as pollination and natural pest control, is widely being advocated to maintain and improve agricultural productivity while safeguarding biodiversity. A vast body of evidence showing the agronomic benefits of enhanced ecosystem service delivery represent important incentives to adopt practices enhancing biodiversity. However, the costs of biodiversity-friendly management are rarely taken into account and may represent a major barrier impeding uptake by farmers. Whether and how biodiversity conservation, ecosystem service delivery, and farm profit can go hand in hand is unknown. Here, we quantify the ecological, agronomic, and net economic benefits of biodiversity-friendly farming in an intensive grassland-sunflower system in Southwest France. We found that reducing land-use intensity on agricultural grasslands drastically enhances flower availability and wild bee diversity, including rare species. Biodiversity-friendly management on grasslands furthermore resulted in an up to 17% higher revenue on neighboring sunflower fields through positive effects on pollination service delivery. However, the opportunity costs of reduced grassland forage yields consistently exceeded the economic benefits of enhanced sunflower pollination. Our results highlight that profitability is often a key constraint hampering adoption of biodiversity-based farming and uptake critically depends on society's willingness to pay for associated delivery of public goods such as biodiversity.

Characterization Factors to Assess Land Use Impacts on Pollinator Abundance in Life Cycle Assessment.

While wild pollinators play a key role in global food production, their assessment is currently missing from the most commonly used environmental impact assessment method, Life Cycle Assessment (LCA). This is mainly due to constraints in data availability and compatibility with LCA inventories. To target this gap, relative pollinator abundance estimates were obtained with the use of a Delphi assessment, during which 25 experts, covering 16 nationalities and 45 countries of expertise, provided scores for low, typical, and high expected abundance associated with 24 land use categories. Based on these estimates, this study presents a set of globally generic characterization factors (CFs) that allows translating land use into relative impacts to wild pollinator abundance. The associated uncertainty of the CFs is presented along with an illustrative case to demonstrate the applicability in LCA studies. The CFs based on estimates that reached consensus during the Delphi assessment are recommended as readily applicable and allow key differences among land use types to be distinguished. The resulting CFs are proposed as the first step for incorporating pollinator impacts in LCA studies, exemplifying the use of expert elicitation methods as a useful tool to fill data gaps that constrain the characterization of key environmental impacts.

A model of wild bee populations accounting for spatial heterogeneity and climate-induced temporal variability of food resources at the landscape level.

The viability of wild bee populations and the pollination services that they provide are driven by the availability of food resources during their activity period and within the surroundings of their nesting sites. Changes in climate and land use influence the availability of these resources and are major threats to declining bee populations. Because wild bees may be vulnerable to interactions between these threats, spatially explicit models of population dynamics that capture how bee populations jointly respond to land use at a landscape scale and weather are needed. Here, we developed a spatially and temporally explicit theoretical model of wild bee populations aiming for a middle ground between the existing mapping of visitation rates using foraging equations and more refined agent-based modeling. The model is developed for Bombus sp. and captures within-season colony dynamics. The model describes mechanistically foraging at the colony level and temporal population dynamics for an average colony at the landscape level. Stages in population dynamics are temperature-dependent triggered by a theoretical generalized seasonal progression, which can be informed by growing degree days. The purpose of the LandscapePhenoBee model is to evaluate the impact of system changes and within-season variability in resources on bee population sizes and crop visitation rates. In a simulation study, we used the model to evaluate the impact of the shortage of food resources in the landscape arising from extreme drought events in different types of landscapes (ranging from different proportions of semi-natural habitats and early and late flowering crops) on bumblebee populations.

Archetype models upscale understanding of natural pest control response to land-use change.

Control of crop pests by shifting host plant availability and natural enemy activity at landscape scales has great potential to enhance the sustainability of agriculture. However, mainstreaming natural pest control requires improved understanding of how its benefits can be realized across a variety of agroecological contexts. Empirical studies suggest significant but highly variable responses of natural pest control to land-use change. Current ecological models are either too specific to provide insight across agroecosystems or too generic to guide management with actionable predictions. We suggest obtaining the full benefit of available empirical, theoretical, and methodological knowledge by combining trait-mediated understanding from correlative studies with the explicit representation of causal relationships achieved by mechanistic modeling. To link these frameworks, we adapt the concept of archetypes, or context-specific generalizations, from sustainability science. Similar responses of natural pest control to land-use gradients across cases that share key attributes, such as functional traits of focal organisms, indicate general processes that drive system behavior in a context-sensitive manner. Based on such observations of natural pest control, a systematic definition of archetypes can provide the basis for mechanistic models of intermediate generality that cover all major agroecosystems worldwide. Example applications demonstrate the potential for upscaling understanding and improving predictions of natural pest control, based on knowledge transfer and scientific synthesis. A broader application of this mechanistic archetype approach promises to enhance ecology's contribution to natural resource management across diverse regions and social-ecological contexts.

Do improved pollination services outweigh farm-economic disadvantages of working in small-structured agricultural landscapes? - Development and application of a bio-economic model.

Increases in the size of agricultural fields, the loss of permanent green field edges and other semi-natural habitats have accompanied the intensification of agriculture, and are still ongoing. From a farm economic perspective, an increase in field size increases efficiency mainly due to cost savings. However, recent evidence suggests that increases in field size might lead to the loss of ecosystem services provided by farmland biodiversity, but this trade-off is rarely considered. Here, we aim to quantify the economic and ecological effects of these changes by developing a bio-economic simulation-based land-use modelling framework based on spatially explicit data from an agricultural region in Germany. The results show a substantial decrease in flower visitation in oilseed rape when field sizes increase and permanent green edges are lost. This also leads to a decrease in pollination from wild bees and affects yields and farm economics. However, this loss in agricultural gross margin is overcompensated by economic gains of field enlargement. We conclude that further, more comprehensive evaluations are required and suggest that maintaining fine-grained agricultural landscapes with permanent field margins in the long term may require incentives to farmers, as well as innovations that allow to farm small fields at lower costs.

Land-use history impacts functional diversity across multiple trophic groups.

Land-use change is a major driver of biodiversity loss worldwide. Although biodiversity often shows a delayed response to land-use change, previous studies have typically focused on a narrow range of current landscape factors and have largely ignored the role of land-use history in shaping plant and animal communities and their functional characteristics. Here, we used a unique database of 220,000 land-use records to investigate how 20-y of land-use changes have affected functional diversity across multiple trophic groups (primary producers, mutualists, herbivores, invertebrate predators, and vertebrate predators) in 75 grassland fields with a broad range of land-use histories. The effects of land-use history on multitrophic trait diversity were as strong as other drivers known to impact biodiversity, e.g., grassland management and current landscape composition. The diversity of animal mobility and resource-acquisition traits was lower in landscapes where much of the land had been historically converted from grassland to crop. In contrast, functional biodiversity was higher in landscapes containing old permanent grasslands, most likely because they offer a stable and high-quality habitat refuge for species with low mobility and specialized feeding niches. Our study shows that grassland-to-crop conversion has long-lasting impacts on the functional biodiversity of agricultural ecosystems. Accordingly, land-use legacy effects must be considered in conservation programs aiming to protect agricultural biodiversity. In particular, the retention of permanent grassland sanctuaries within intensive landscapes may offset ecological debts.

Field sizes and the future of farmland biodiversity in European landscapes.

Lower diversity of plant and animal farmland species are usually reported where cropland has been aggregated into larger fields, which raises prospects of curbing declines in European farmland biodiversity and associated ecosystem services by halting trends to field size increases associated to agricultural intensification, without having to set aside arable land for conservation. Here, we consider the factors underlying trade-offs between farmer income and biodiversity as mediated by field size at local and landscape scales, and how these trade-offs may be overcome. Field sizes are still increasing, facilitated by increasing farm sizes and land consolidation. Decreases in working time and fuel expenses when fields are larger, uptake of larger machinery and subsidies favoring larger farms provide incentives to manage land in larger units, putting farmland biodiversity further at risk. Yet, field size-mediated ecological-economic trade-offs are largely ignored in policy and research. We recommend internalizing the ecological effects of changes in landscape-scale field size into land consolidation scheme design, ensuring that EU Common Agricultural Policy post-2020 rewards farmers that maintain and recreate fine-grained landscapes where these are essential for farmland biodiversity targets, and reducing economic-ecological trade-offs by stimulating agricultural research and innovation for economically efficient yet biodiversity-friendly farming in fine-grained landscapes.

Communities of oil palm flower-visiting insects: investigating the covariation of Elaeidobius kamerunicus and other dominant species.

Insects visit flowers not only to forage for nectar or pollen but also to search for hosts or prey, and to look for suitable habitats for breeding sites. In oil palm flowers, it has been documented that not all flower-visiting insects are pollinators, but some insects are recognized as predators, parasitoids or saprophages, which may affect the abundance and persistence of the weevil pollinating oil palm, Elaeidobius kamerunicus. We studied the community of oil palm flower-visiting insects and investigated the covariation between the abundance E. kamerunicus and that of other dominant species. Ecological research was conducted in oil palm plantations with different tree ages in Central Borneo. Our results found that tree age and flower type of oil palm did not influence the abundance and species richness of flower-visiting insects, but significantly affected their species composition. There was a significant positive relationship between the abundance of E. kamerunicus and the fly Scaptodrosophila sp, indicating that these species covariate in oil palm flowers. These findings suggest that understanding the covariation between E. kamerunicus and Scaptodrosophila sp may help develop the conservation strategies for E. kamerunicus to support the sustainable production of oil palm.

Increasing crop heterogeneity enhances multitrophic diversity across agricultural regions.

Agricultural landscape homogenization has detrimental effects on biodiversity and key ecosystem services. Increasing agricultural landscape heterogeneity by increasing seminatural cover can help to mitigate biodiversity loss. However, the amount of seminatural cover is generally low and difficult to increase in many intensively managed agricultural landscapes. We hypothesized that increasing the heterogeneity of the crop mosaic itself (hereafter "crop heterogeneity") can also have positive effects on biodiversity. In 8 contrasting regions of Europe and North America, we selected 435 landscapes along independent gradients of crop diversity and mean field size. Within each landscape, we selected 3 sampling sites in 1, 2, or 3 crop types. We sampled 7 taxa (plants, bees, butterflies, hoverflies, carabids, spiders, and birds) and calculated a synthetic index of multitrophic diversity at the landscape level. Increasing crop heterogeneity was more beneficial for multitrophic diversity than increasing seminatural cover. For instance, the effect of decreasing mean field size from 5 to 2.8 ha was as strong as the effect of increasing seminatural cover from 0.5 to 11%. Decreasing mean field size benefited multitrophic diversity even in the absence of seminatural vegetation between fields. Increasing the number of crop types sampled had a positive effect on landscape-level multitrophic diversity. However, the effect of increasing crop diversity in the landscape surrounding fields sampled depended on the amount of seminatural cover. Our study provides large-scale, multitrophic, cross-regional evidence that increasing crop heterogeneity can be an effective way to increase biodiversity in agricultural landscapes without taking land out of agricultural production.

The interplay of landscape composition and configuration: new pathways to manage functional biodiversity and agroecosystem services across Europe.

Managing agricultural landscapes to support biodiversity and ecosystem services is a key aim of a sustainable agriculture. However, how the spatial arrangement of crop fields and other habitats in landscapes impacts arthropods and their functions is poorly known. Synthesising data from 49 studies (1515 landscapes) across Europe, we examined effects of landscape composition (% habitats) and configuration (edge density) on arthropods in fields and their margins, pest control, pollination and yields. Configuration effects interacted with the proportions of crop and non-crop habitats, and species' dietary, dispersal and overwintering traits led to contrasting responses to landscape variables. Overall, however, in landscapes with high edge density, 70% of pollinator and 44% of natural enemy species reached highest abundances and pollination and pest control improved 1.7- and 1.4-fold respectively. Arable-dominated landscapes with high edge densities achieved high yields. This suggests that enhancing edge density in European agroecosystems can promote functional biodiversity and yield-enhancing ecosystem services.

Landscape configurational heterogeneity by small-scale agriculture, not crop diversity, maintains pollinators and plant reproduction in western Europe.

Agricultural intensification is one of the main causes for the current biodiversity crisis. While reversing habitat loss on agricultural land is challenging, increasing the farmland configurational heterogeneity (higher field border density) and farmland compositional heterogeneity (higher crop diversity) has been proposed to counteract some habitat loss. Here, we tested whether increased farmland configurational and compositional heterogeneity promote wild pollinators and plant reproduction in 229 landscapes located in four major western European agricultural regions. High-field border density consistently increased wild bee abundance and seed set of radish (Raphanus sativus), probably through enhanced connectivity. In particular, we demonstrate the importance of crop-crop borders for pollinator movement as an additional experiment showed higher transfer of a pollen analogue along crop-crop borders than across fields or along semi-natural crop borders. By contrast, high crop diversity reduced bee abundance, probably due to an increase of crop types with particularly intensive management. This highlights the importance of crop identity when higher crop diversity is promoted. Our results show that small-scale agricultural systems can boost pollinators and plant reproduction. Agri-environmental policies should therefore aim to halt and reverse the current trend of increasing field sizes and to reduce the amount of crop types with particularly intensive management.

Direct and cascading impacts of tropical land-use change on multi-trophic biodiversity.

The conversion of tropical rainforest to agricultural systems such as oil palm alters biodiversity across a large range of interacting taxa and trophic levels. Yet, it remains unclear how direct and cascading effects of land-use change simultaneously drive ecological shifts. Combining data from a multi-taxon research initiative in Sumatra, Indonesia, we show that direct and cascading land-use effects alter biomass and species richness of taxa across trophic levels ranging from microorganisms to birds. Tropical land use resulted in increases in biomass and species richness via bottom-up cascading effects, but reductions via direct effects. When considering direct and cascading effects together, land use was found to reduce biomass and species richness, with increasing magnitude at higher trophic levels. Our analyses disentangle the multifaceted effects of land-use change on tropical ecosystems, revealing that biotic interactions on broad taxonomic scales influence the ecological outcome of anthropogenic perturbations to natural ecosystems.

Similar alpha and beta diversity changes in tropical ant communities, comparing savannas and rainforests in Brazil and Indonesia.

Local biodiversity can be expected to be similar worldwide if environmental conditions are similar. Here, we hypothesize that tropical ant communities with different types of regional species pools but at similar habitat types in Brazil and Indonesia show similar diversity patterns at multiple spatial scales, when comparing (1) the relative contribution of alpha and beta diversity to gamma diversity; (2) the number of distinct communities (community differentiation); and (3) the drivers of ß-diversity (species replacement or species loss/gain) at each spatial scale. In both countries, rainforests and savannas (biome scale) were represented by three landscapes (landscape scale), each with four transects (site scale) and each transect with 10 pitfall traps (local scale). At the local scale, α-diversity was higher and ß-diversity lower than expected from null models. Hence, we observed a high coexistence of species across biomes. The replacement of species seemed the most important factor for ß-diversity among sites and among landscapes across biomes. Species sorting, landscape-moderated species distribution and neutral drift are potential mechanisms for the high ß-diversity among sites within landscapes. At the biome scale, different evolutionary histories produced great differences in ant community composition, so the replacement of species is, at this scale, the most important driver of beta diversity. According to these key findings, we conclude that distinct regional ant species pools from similar tropical habitat types are similarly constrained across several spatial scales, regardless of the continent considered.

A global synthesis of the effects of diversified farming systems on arthropod diversity within fields and across agricultural landscapes.

Agricultural intensification is a leading cause of global biodiversity loss, which can reduce the provisioning of ecosystem services in managed ecosystems. Organic farming and plant diversification are farm management schemes that may mitigate potential ecological harm by increasing species richness and boosting related ecosystem services to agroecosystems. What remains unclear is the extent to which farm management schemes affect biodiversity components other than species richness, and whether impacts differ across spatial scales and landscape contexts. Using a global metadataset, we quantified the effects of organic farming and plant diversification on abundance, local diversity (communities within fields), and regional diversity (communities across fields) of arthropod pollinators, predators, herbivores, and detritivores. Both organic farming and higher in-field plant diversity enhanced arthropod abundance, particularly for rare taxa. This resulted in increased richness but decreased evenness. While these responses were stronger at local relative to regional scales, richness and abundance increased at both scales, and richness on farms embedded in complex relative to simple landscapes. Overall, both organic farming and in-field plant diversification exerted the strongest effects on pollinators and predators, suggesting these management schemes can facilitate ecosystem service providers without augmenting herbivore (pest) populations. Our results suggest that organic farming and plant diversification promote diverse arthropod metacommunities that may provide temporal and spatial stability of ecosystem service provisioning. Conserving diverse plant and arthropod communities in farming systems therefore requires sustainable practices that operate both within fields and across landscapes.

The role of ants, birds and bats for ecosystem functions and yield in oil palm plantations.

One of the world's most important and rapidly expanding crops, oil palm, is associated with low levels of biodiversity. Changes in predator communities might alter ecosystem services and subsequently sustainable management but these links have received little attention to date. Here, for the first time, we manipulated ant and flying vertebrate (birds and bats) access to oil palms in six smallholder plantations in Sumatra (Indonesia) and measured effects on arthropod communities, related ecosystem functions (herbivory, predation, decomposition and pollination) and crop yield. Arthropod predators increased in response to reductions in ant and bird access, but the overall effect of experimental manipulations on ecosystem functions was minimal. Similarly, effects on yield were not significant. We conclude that ecosystem functions and productivity in oil palm are, under current levels of low pest pressure and large pollinator populations, robust to large reductions of major predators.

Pollinator population size and pollination ecosystem service responses to enhancing floral and nesting resources.

Modeling pollination ecosystem services requires a spatially explicit, process-based approach because they depend on both the behavioral responses of pollinators to the amount and spatial arrangement of habitat and on the within- and between-season dynamics of pollinator populations in response to land use. We describe a novel pollinator model predicting flower visitation rates by wild central-place foragers (e.g., nesting bees) in spatially explicit landscapes. The model goes beyond existing approaches by: (1) integrating preferential use of more rewarding floral and nesting resources; (2) considering population growth over time; (3) allowing different dispersal distances for workers and reproductives; (4) providing visitation rates for use in crop pollination models. We use the model to estimate the effect of establishing grassy field margins offering nesting resources and a low quantity of flower resources, and/or late-flowering flower strips offering no nesting resources but abundant flowers, on bumble bee populations and visitation rates to flowers in landscapes that differ in amounts of linear seminatural habitats and early mass-flowering crops. Flower strips were three times more effective in increasing pollinator populations and visitation rates than field margins, and this effect increased over time. Late-blooming flower strips increased early-season visitation rates, but decreased visitation rates in other late-season flowers. Increases in population size over time in response to flower strips and amounts of linear seminatural habitats reduced this apparent competition for pollinators. Our spatially explicit, process-based model generates emergent patterns reflecting empirical observations, such that adding flower resources may have contrasting short- and long-term effects due to apparent competition for pollinators and pollinator population size increase. It allows exploring these effects and comparing effect sizes in ways not possible with other existing models. Future applications include species comparisons, analysis of the sensitivity of predictions to life-history traits, as well as large-scale management intervention and policy assessment.

Experimental Biodiversity Enrichment in Oil-Palm-Dominated Landscapes in Indonesia.

Tropical biodiversity is threatened by the expansion of oil-palm plantations. Reduced-impact farming systems such as agroforests, have been proposed to increase biodiversity and ecosystem functioning. In regions where oil-palm plantations already dominate the landscape, this increase can only be achieved through systematic ecological restoration. However, our knowledge about the underlying ecological and socio-economic processes, constraints, and trade-offs of ecological restoration in oil-palm landscapes is very limited. To bridge this gap, we established a long-term biodiversity enrichment experiment. We established experimental tree islands in a conventional oil-palm plantation and systematically varied plot size, tree diversity, and tree species composition. Here, we describe the rationale and the design of the experiment, the ecosystem variables (soil, topography, canopy openness) and biotic characteristics (associated vegetation, invertebrates, birds) of the experimental site prior to the establishment of the experiment, and initial experimental effects on the fauna. Already one year after establishment of the experiment, tree plantings had an overall positive effect on the bird and invertebrate communities at the plantation scale. The diversity and abundance of invertebrates was positively affected by the size of the tree islands. Based on these results, we expect a further increase of biodiversity and associated ecological functions in the future. The long-term interdisciplinary monitoring of ecosystem variables, flora, fauna, and socio-economic aspects will allow us to evaluate the suitability of tree islands as a restoration measure. Thereof, guidelines for ecologically improved and socio-economically viable restoration and management concepts could be developed.

Land-use choices follow profitability at the expense of ecological functions in Indonesian smallholder landscapes.

Smallholder-dominated agricultural mosaic landscapes are highlighted as model production systems that deliver both economic and ecological goods in tropical agricultural landscapes, but trade-offs underlying current land-use dynamics are poorly known. Here, using the most comprehensive quantification of land-use change and associated bundles of ecosystem functions, services and economic benefits to date, we show that Indonesian smallholders predominantly choose farm portfolios with high economic productivity but low ecological value. The more profitable oil palm and rubber monocultures replace forests and agroforests critical for maintaining above- and below-ground ecological functions and the diversity of most taxa. Between the monocultures, the higher economic performance of oil palm over rubber comes with the reliance on fertilizer inputs and with increased nutrient leaching losses. Strategies to achieve an ecological-economic balance and a sustainable management of tropical smallholder landscapes must be prioritized to avoid further environmental degradation.