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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction?

Climate warming will increase the drought exposure of many forests world-wide. It is not well understood how trees adapt their hydraulic architecture to a long-term decrease in water availability. We examined 23 traits characterizing the hydraulic architecture and growth rate of branches and the dependent foliage of mature European beech (Fagus sylvatica) trees along a precipitation gradient (855-594 mm yr(-1) ) on uniform soil. A main goal was to identify traits that are associated with xylem efficiency, safety and growth. Our data demonstrate for the first time a linear increase in embolism resistance with climatic aridity (by 10%) across populations within a species. Simultaneously, vessel diameter declined by 7% and pit membrane thickness (Tm ) increased by 15%. Although specific conductivity did not change, leaf-specific conductivity declined by 40% with decreasing precipitation. Of eight plant traits commonly associated with embolism resistance, only vessel density in combination with pathway redundancy and Tm were related. We did not confirm the widely assumed trade-off between xylem safety and efficiency but obtained evidence in support of a positive relationship between hydraulic efficiency and growth. We conclude that the branch hydraulic system of beech has a distinct adaptive potential to respond to a precipitation reduction as a result of the environmental control of embolism resistance.

Feeding damage to plants increases with plant size across 21 Brassicaceae species.

Plant size is a major predictor of ecological functioning. We tested the hypothesis that feeding damage to plants increases with plant size, as the conspicuousness of large plants makes resource finding and colonisation easier. Further, large plants can be attractive to herbivores, as they offer greater amounts and ranges of resources and niches, but direct evidence from experiments testing size effects on feeding damage and consequently on plant fitness is so far missing. We established a common garden experiment with a plant size gradient (10-130 cm height) using 21 annual Brassicaceae species, and quantified plant size, biomass and number of all aboveground components (flowers, fruits, leaves, stems) and their proportional feeding damage. Plant reproductive fitness was measured using seed number, 1000 seed weight and total seed weight. Feeding damage to the different plant components increased with plant size or component biomass, with mean damage levels being approximately 30 % for flowers, 5 % for fruits and 1 % for leaves and stems. Feeding damage affected plant reproductive fitness depending on feeding damage type, with flower damage having the strongest effect, shown by greatly reduced seed number, 1000 seed weight and total seed weight. Finally, we found an overall negative effect of plant size on 1000 seed weight, but not on seed number and total seed weight. In conclusion, being conspicuous and attractive to herbivores causes greater flower damage leading to higher fitness costs for large plants, which might be partly counterbalanced by benefits such as enhanced competitive/compensatory abilities or more mutualistic pollinator visits.

Density of insect-pollinated grassland plants decreases with increasing surrounding land-use intensity.

Pollinator declines have raised concerns about the persistence of plant species that depend on insect pollination, in particular by bees, for their reproduction. The impact of pollinator declines remains unknown for species-rich plant communities found in temperate seminatural grasslands. We investigated effects of land-use intensity in the surrounding landscape on the distribution of plant traits related to insect pollination in 239 European seminatural grasslands. Increasing arable land use in the surrounding landscape consistently reduced the density of plants depending on bee and insect pollination. Similarly, the relative abundance of bee-pollination-dependent plants increased with higher proportions of non-arable agricultural land (e.g. permanent grassland). This was paralleled by an overall increase in bee abundance and diversity. By isolating the impact of the surrounding landscape from effects of local habitat quality, we show for the first time that grassland plants dependent on insect pollination are particularly susceptible to increasing land-use intensity in the landscape.

Interaction complexity matters: disentangling services and disservices of ant communities driving yield in tropical agroecosystems.

Owing to complex direct and indirect effects, impacts of higher trophic levels on plants is poorly understood. In tropical agroecosystems, ants interact with crop mutualists and antagonists, but little is known about how this integrates into the final ecosystem service, crop yield. We combined ant exclusion and introduction of invasive and native-dominant species in cacao agroecosystems to test whether (i) ant exclusion reduces yield, (ii) dominant species maximize certain intermediate ecosystem services (e.g. control of specific pests) rather than yield, which depends on several, cascading intermediate services and (iii) even, species-rich ant communities result in highest yields. Ants provided services, including reduced leaf herbivory and fruit pest damage and indirect pollination facilitation, but also disservices, such as increased mealybug density, phytopathogen dissemination and indirect pest damage enhancement. Yields were highest with unmanipulated, species-rich, even communities, whereas ant exclusion decreased yield by 27%. Introduction of an invasive-dominant ant decreased species density and evenness and resulted in 34% lower yields, whereas introduction of a non-invasive-dominant species resulted in similar species density and yields as in the unmanipulated control. Species traits and ant community structure affect services and disservices for agriculture in surprisingly complex ways, with species-rich and even communities promoting highest yield.

Bee pollination improves crop quality, shelf life and commercial value.

Pollination improves the yield of most crop species and contributes to one-third of global crop production, but comprehensive benefits including crop quality are still unknown. Hence, pollination is underestimated by international policies, which is particularly alarming in times of agricultural intensification and diminishing pollination services. In this study, exclusion experiments with strawberries showed bee pollination to improve fruit quality, quantity and market value compared with wind and self-pollination. Bee-pollinated fruits were heavier, had less malformations and reached higher commercial grades. They had increased redness and reduced sugar-acid-ratios and were firmer, thus improving the commercially important shelf life. Longer shelf life reduced fruit loss by at least 11%. This is accounting for 0.32 billion US$ of the 1.44 billion US$ provided by bee pollination to the total value of 2.90 billion US$ made with strawberry selling in the European Union 2009. The fruit quality and yield effects are driven by the pollination-mediated production of hormonal growth regulators, which occur in several pollination-dependent crops. Thus, our comprehensive findings should be transferable to a wide range of crops and demonstrate bee pollination to be a hitherto underestimated but vital and economically important determinant of fruit quality.

Combining high biodiversity with high yields in tropical agroforests.

Local and landscape-scale agricultural intensification is a major driver of global biodiversity loss. Controversially discussed solutions include wildlife-friendly farming or combining high-intensity farming with land-sparing for nature. Here, we integrate biodiversity and crop productivity data for smallholder cacao in Indonesia to exemplify for tropical agroforests that there is little relationship between yield and biodiversity under current management, opening substantial opportunities for wildlife-friendly management. Species richness of trees, fungi, invertebrates, and vertebrates did not decrease with yield. Moderate shade, adequate labor, and input level can be combined with a complex habitat structure to provide high biodiversity as well as high yields. Although livelihood impacts are held up as a major obstacle for wildlife-friendly farming in the tropics, our results suggest that in some situations, agroforests can be designed to optimize both biodiversity and crop production benefits without adding pressure to convert natural habitat to farmland.

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.

Bats and birds increase crop yield in tropical agroforestry landscapes.

Human welfare is significantly linked to ecosystem services such as the suppression of pest insects by birds and bats. However, effects of biocontrol services on tropical cash crop yield are still largely unknown. For the first time, we manipulated the access of birds and bats in an exclosure experiment (day, night and full exclosures compared to open controls in Indonesian cacao agroforestry) and quantified the arthropod communities, the fruit development and the final yield over a long time period (15 months). We found that bat and bird exclusion increased insect herbivore abundance, despite the concurrent release of mesopredators such as ants and spiders, and negatively affected fruit development, with final crop yield decreasing by 31% across local (shade cover) and landscape (distance to primary forest) gradients. Our results highlight the tremendous economic impact of common insectivorous birds and bats, which need to become an essential part of sustainable landscape management.