Metabarcoding of trap nests reveals differential impact of urbanization on cavity-nesting bee and wasp communities.

Urbanization is affecting arthropod communities worldwide, for example by changing the availability of food resources. However, the strength and direction of a community's response is species-specific and depends on species' trophic level. Here, we investigated interacting species at different trophic levels in nests of cavity-nesting bees and wasps along two urbanization gradients in four German cities using trap nests. We analysed bee and wasp diversity and their trophic interaction partners by metabarcoding the DNA of bee pollen and preyed arthropods found in wasp nests. We found that the pollen richness increased with increasing distance from city centres and at sites characterized by a high percentage of impervious and developed surface, while the richness of pollinators was unaffected by urbanization. In contrast, species richness of wasps, but not their arthropod prey, was highest at sites with low levels of urbanization. However, the community structure of wasp prey changed with urbanization at both local and regional scales. Throughout the study area, the community of wasps consisted of specialists, while bee species were generalists. Our results suggest that Hymenoptera and their food resources are negatively affected by increasing urbanization. However, to understand distribution patterns of both, wasps and bees in urban settings other factors besides food availability should be considered.

Microhabitat conditions remedy heat stress effects on insect activity.

Anthropogenic global warming has major implications for mobile terrestrial insects, including long-term effects from constant warming, for example, on species distribution patterns, and short-term effects from heat extremes that induce immediate physiological responses. To cope with heat extremes, they either have to reduce their activity or move to preferable microhabitats. The availability of favorable microhabitat conditions is strongly promoted by the spatial heterogeneity of habitats, which is often reduced by anthropogenic land transformation. Thus, it is decisive to understand the combined effects of these global change drivers on insect activity. Here, we assessed the movement activity of six insect species (from three orders) in response to heat stress using a unique tracking approach via radio frequency identification. We tracked 465 individuals at the iDiv Ecotron across a temperature gradient up to 38.7°C. In addition, we varied microhabitat conditions by adding leaf litter from four different tree species to the experimental units, either spatially separated or well mixed. Our results show opposing effects of heat extremes on insect activity depending on the microhabitat conditions. The insect community significantly decreased its activity in the mixed litter scenario, while we found a strong positive effect on activity in the separated litter scenario. We hypothesize that the simultaneous availability of thermal refugia as well as resources provided by the mixed litter scenario allows animals to reduce their activity and save energy in response to heat stress. Contrary, the spatial separation of beneficial microclimatic conditions and resources forces animals to increase their activity to fulfill their energetic needs. Thus, our study highlights the importance of habitat heterogeneity on smaller scales, because it may buffer the consequences of extreme temperatures of insect performance and survival under global change.

Species-habitat networks elucidate landscape effects on habitat specialisation of natural enemies and pollinators.

Measuring habitat specialisation is pivotal for predicting species extinctions and for understanding consequences on ecosystem functioning. Here, we sampled pollinator and natural enemy communities in all major habitat types occurring across multiple agricultural landscapes and used species-habitat networks to determine how habitat specialisation changed along gradients in landscape composition and configuration. Although it is well known that landscape simplification often causes the replacement of specialists with generalists, our study provided evidence for intraspecific variation in habitat specialisation, highlighting how a large number of arthropod species adapted their way of selecting habitat resources depending on the landscape structure. Groups with higher diet specialisation and limited foraging flexibility appeared to have a reduced ability to respond to landscape changes, indicating that some arthropod taxa are better able than others to adapt to an increasingly broad set of resources and persist in highly impacted landscapes.

Winners and losers of national and global efforts to reconcile agricultural intensification and biodiversity conservation.

Closing yield gaps within existing croplands, and thereby avoiding further habitat conversions, is a prominently and controversially discussed strategy to meet the rising demand for agricultural products, while minimizing biodiversity impacts. The agricultural intensification associated with such a strategy poses additional threats to biodiversity within agricultural landscapes. The uneven spatial distribution of both yield gaps and biodiversity provides opportunities for reconciling agricultural intensification and biodiversity conservation through spatially optimized intensification. Here, we integrate distribution and habitat information for almost 20,000 vertebrate species with land-cover and land-use datasets. We estimate that projected agricultural intensification between 2000 and 2040 would reduce the global biodiversity value of agricultural lands by 11%, relative to 2000. Contrasting these projections with spatial land-use optimization scenarios reveals that 88% of projected biodiversity loss could be avoided through globally coordinated land-use planning, implying huge efficiency gains through international cooperation. However, global-scale optimization also implies a highly uneven distribution of costs and benefits, resulting in distinct "winners and losers" in terms of national economic development, food security, food sovereignty or conservation. Given conflicting national interests and lacking effective governance mechanisms to guarantee equitable compensation of losers, multinational land-use optimization seems politically unlikely. In turn, 61% of projected biodiversity loss could be avoided through nationally focused optimization, and 33% through optimization within just 10 countries. Targeted efforts to improve the capacity for integrated land-use planning for sustainable intensification especially in these countries, including the strengthening of institutions that can arbitrate subnational land-use conflicts, may offer an effective, yet politically feasible, avenue to better reconcile future trade-offs between agriculture and conservation. The efficiency gains of optimization remained robust when assuming that yields could only be increased to 80% of their potential. Our results highlight the need to better integrate real-world governance, political and economic challenges into sustainable development and global change mitigation research.

Interannual variation in land-use intensity enhances grassland multidiversity.

Although temporal heterogeneity is a well-accepted driver of biodiversity, effects of interannual variation in land-use intensity (LUI) have not been addressed yet. Additionally, responses to land use can differ greatly among different organisms; therefore, overall effects of land-use on total local biodiversity are hardly known. To test for effects of LUI (quantified as the combined intensity of fertilization, grazing, and mowing) and interannual variation in LUI (SD in LUI across time), we introduce a unique measure of whole-ecosystem biodiversity, multidiversity. This synthesizes individual diversity measures across up to 49 taxonomic groups of plants, animals, fungi, and bacteria from 150 grasslands. Multidiversity declined with increasing LUI among grasslands, particularly for rarer species and aboveground organisms, whereas common species and belowground groups were less sensitive. However, a high level of interannual variation in LUI increased overall multidiversity at low LUI and was even more beneficial for rarer species because it slowed the rate at which the multidiversity of rare species declined with increasing LUI. In more intensively managed grasslands, the diversity of rarer species was, on average, 18% of the maximum diversity across all grasslands when LUI was static over time but increased to 31% of the maximum when LUI changed maximally over time. In addition to decreasing overall LUI, we suggest varying LUI across years as a complementary strategy to promote biodiversity conservation.

Corridors restore animal-mediated pollination in fragmented tropical forest landscapes.

Tropical biodiversity and associated ecosystem functions have become heavily eroded through habitat loss. Animal-mediated pollination is required in more than 94% of higher tropical plant species and 75% of the world's leading food crops, but it remains unclear if corridors avert deforestation-driven pollination breakdown in fragmented tropical landscapes. Here, we used manipulative resource experiments and field observations to show that corridors functionally connect neotropical forest fragments for forest-associated hummingbirds and increase pollen transfer. Further, corridors boosted forest-associated pollinator availability in fragments by 14.3 times compared with unconnected equivalents, increasing overall pollination success. Plants in patches without corridors showed pollination rates equal to bagged control flowers, indicating pollination failure in isolated fragments. This indicates, for the first time, that corridors benefit tropical forest ecosystems beyond boosting local species richness, by functionally connecting mutualistic network partners. We conclude that small-scale adjustments to landscape configuration safeguard native pollinators and associated pollination services in tropical forest landscapes.

Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment.

Biodiversity is rapidly declining, and this may negatively affect ecosystem processes, including economically important ecosystem services. Previous studies have shown that biodiversity has positive effects on organisms and processes across trophic levels. However, only a few studies have so far incorporated an explicit food-web perspective. In an eight-year biodiversity experiment, we studied an unprecedented range of above- and below-ground organisms and multitrophic interactions. A multitrophic data set originating from a single long-term experiment allows mechanistic insights that would not be gained from meta-analysis of different experiments. Here we show that plant diversity effects dampen with increasing trophic level and degree of omnivory. This was true both for abundance and species richness of organisms. Furthermore, we present comprehensive above-ground/below-ground biodiversity food webs. Both above ground and below ground, herbivores responded more strongly to changes in plant diversity than did carnivores or omnivores. Density and richness of carnivorous taxa was independent of vegetation structure. Below-ground responses to plant diversity were consistently weaker than above-ground responses. Responses to increasing plant diversity were generally positive, but were negative for biological invasion, pathogen infestation and hyperparasitism. Our results suggest that plant diversity has strong bottom-up effects on multitrophic interaction networks, with particularly strong effects on lower trophic levels. Effects on higher trophic levels are indirectly mediated through bottom-up trophic cascades.

Functional trait diversity across trophic levels determines herbivore impact on plant community biomass.

Understanding the consequences of trophic interactions for ecosystem functioning is challenging, as contrasting effects of species and functional diversity can be expected across trophic levels. We experimentally manipulated functional identity and diversity of grassland insect herbivores and tested their impact on plant community biomass. Herbivore resource acquisition traits, i.e. mandible strength and the diversity of mandibular traits, had more important effects on plant biomass than body size. Higher herbivore functional diversity increased overall impact on plant biomass due to feeding niche complementarity. Higher plant functional diversity limited biomass pre-emption by herbivores. The functional diversity within and across trophic levels therefore regulates the impact of functionally contrasting consumers on primary producers. By experimentally manipulating the functional diversity across trophic levels, our study illustrates how trait-based approaches constitute a promising way to tackle existing links between trophic interactions and ecosystem functioning.

Biodiversity conservation across taxa and landscapes requires many small as well as single large habitat fragments.

Agricultural intensification has been shown to reduce biodiversity through processes such as habitat degradation and fragmentation. We tested whether several small or single large habitat fragments (re-visiting the 'single large or several small' debate) support more species across a wide range of taxonomic groups (plants, leafhoppers, true bugs, snails). Our study comprised 14 small (<1 ha) and 14 large (1.5-8 ha) fragments of calcareous grassland in Central Germany along orthogonal gradients of landscape complexity and habitat connectivity. Each taxon was sampled on six plots per fragment. Across taxa, species richness did not differ between large and small fragments, whereas species-area accumulation curves showed that both overall and specialist species richness was much higher on several small fragments of calcareous grassland than on few large fragments. On average, 85% of the overall species richness was recorded on all small fragments taken together (4.6 ha), whereas the two largest ones (15.1 ha) only accounted for 37% of the species. This could be due to the greater geographic extent covered by many small fragments. However, community composition differed strongly between large and small fragments, and some of the rarest specialist species appeared to be confined to large fragments. The surrounding landscape did not show any consistent effects on species richness and community composition. Our results show that both single large and many small fragments are needed to promote landscape-wide biodiversity across taxa. We therefore question the focus on large fragments only and call for a new diversified habitat fragmentation strategy for biodiversity conservation.

Effects of tree and herb biodiversity on Diptera, a hyperdiverse insect order.

Biodiversity experiments have shown that plant diversity has largely positive effects on insect diversity and abundance. However, such relationships have rarely been studied in undisturbed and more complex ecosystems such as forests. Flies (Diptera) are among the most dominant taxa in temperate ecosystems, influencing many ecosystem processes. As it is unknown how Diptera respond to changes in forest biodiversity, we examined how community characteristics of Diptera respond to varying levels of tree and herb diversity and vegetation structure. The study was conducted in the Hainich National Park (Central Germany) on 84 plots along a gradient of tree (from two to nine species) and herb (from two to 28 species) diversity. We found that herb and canopy cover as well as spatial effects were the best predictors of Diptera community composition, consisting of 62 families, including 99 Empidoidea and 78 Phoridae species. Abundance of Empidoidea was positively influenced by herb diversity, indicating bottom-up control. A complex causal pathway influenced Dipteran species richness: species-rich forest stands, with low beech cover, had lower canopy cover, resulting in higher Dipteran species richness. In addition, Diptera benefited from a more dense and diverse herb community. Individual species responded differentially to herb layer diversity, indicating that effects of plant diversity on higher trophic levels depend on species identity. We conclude that tree and herb canopy cover as well as herb diversity predominately shape Dipteran communities in temperate deciduous forests, which is in contrast to expectations from grassland studies exhibiting much closer relationships between plant and insect diversity.

Disentangling direct and indirect effects of experimental grassland management and plant functional-group manipulation on plant and leafhopper diversity.

BACKGROUND: Plant biodiversity can affect trophic interactions in many ways, including direct bottom-up effects on insects, but is negatively affected by agricultural intensification. Grassland intensification promotes plant productivity, resulting in changes in plant community composition, and impacts on higher trophic levels. Here, we use a novel grassland management experiment combining manipulations of cutting and fertilization with experimental changes in plant functional group composition (independent of management effects) to disentangle the direct and indirect effects of agricultural management on insect herbivore diversity and abundance. We used leafhoppers as model organisms as they are a key insect taxon in grasslands and react rapidly to management changes. Leafhoppers were sampled between May and September 2010 using standardized sweep netting and pan traps. RESULTS: Plant diversity, functional group composition and management regime in grasslands affected leafhopper species richness and abundance. Higher cutting frequencies directly led to decreasing leafhopper species richness, presumably due to the higher disturbance frequency and the reduction in food-resource heterogeneity. In contrast, fertilizer application had only a small indirect negative effect via enhanced aboveground plant biomass, reduced plant diversity and changes in functional group composition. The manipulated increase in grass cover had contrasting direct and indirect effects on leafhopper species richness: grass cover directly increased leafhopper species richness, but negatively affected plant diversity, which in turn was positively related to leafhopper species richness. In conclusion, insect diversity is driven in complex direct and indirect ways by grassland management, including changes in functional group composition. CONCLUSIONS: The availability of preferred food sources and the frequency of disturbance are important direct and indirect drivers of leafhopper species richness, interacting in complex ways with plant diversity and food resource heterogeneity.

Joint environmental and social benefits from diversified agriculture.

Agricultural simplification continues to expand at the expense of more diverse forms of agriculture. This simplification, for example, in the form of intensively managed monocultures, poses a risk to keeping the world within safe and just Earth system boundaries. Here, we estimated how agricultural diversification simultaneously affects social and environmental outcomes. Drawing from 24 studies in 11 countries across 2655 farms, we show how five diversification strategies focusing on livestock, crops, soils, noncrop plantings, and water conservation benefit social (e.g., human well-being, yields, and food security) and environmental (e.g., biodiversity, ecosystem services, and reduced environmental externalities) outcomes. We found that applying multiple diversification strategies creates more positive outcomes than individual management strategies alone. To realize these benefits, well-designed policies are needed to incentivize the adoption of multiple diversification strategies in unison.

Functionally and phylogenetically diverse plant communities key to soil biota.

Recent studies assessing the role of biological diversity for ecosystem functioning indicate that the diversity of functional traits and the evolutionary history of species in a community, not the number of taxonomic units, ultimately drives the biodiversity--ecosystem-function relationship. Here, we simultaneously assessed the importance of plant functional trait and phylogenetic diversity as predictors of major trophic groups of soil biota (abundance and diversity), six years from the onset of a grassland biodiversity experiment. Plant functional and phylogenetic diversity were generally better predictors of soil biota than the traditionally used species or functional group richness. Functional diversity was a reliable predictor for most biota, with the exception of soil microorganisms, which were better predicted by phylogenetic diversity. These results provide empirical support for the idea that the diversity of plant functional traits and the diversity of evolutionary lineages in a community are important for maintaining higher abundances and diversity of soil communities.

A comparison of the strength of biodiversity effects across multiple functions.

In order to predict which ecosystem functions are most at risk from biodiversity loss, meta-analyses have generalised results from biodiversity experiments over different sites and ecosystem types. In contrast, comparing the strength of biodiversity effects across a large number of ecosystem processes measured in a single experiment permits more direct comparisons. Here, we present an analysis of 418 separate measures of 38 ecosystem processes. Overall, 45 % of processes were significantly affected by plant species richness, suggesting that, while diversity affects a large number of processes not all respond to biodiversity. We therefore compared the strength of plant diversity effects between different categories of ecosystem processes, grouping processes according to the year of measurement, their biogeochemical cycle, trophic level and compartment (above- or belowground) and according to whether they were measures of biodiversity or other ecosystem processes, biotic or abiotic and static or dynamic. Overall, and for several individual processes, we found that biodiversity effects became stronger over time. Measures of the carbon cycle were also affected more strongly by plant species richness than were the measures associated with the nitrogen cycle. Further, we found greater plant species richness effects on measures of biodiversity than on other processes. The differential effects of plant diversity on the various types of ecosystem processes indicate that future research and political effort should shift from a general debate about whether biodiversity loss impairs ecosystem functions to focussing on the specific functions of interest and ways to preserve them individually or in combination.

taxalogue: a toolkit to create comprehensive CO1 reference databases.

Background: Taxonomic identification through DNA barcodes gained considerable traction through the invention of next-generation sequencing and DNA metabarcoding. Metabarcoding allows for the simultaneous identification of thousands of organisms from bulk samples with high taxonomic resolution. However, reliable identifications can only be achieved with comprehensive and curated reference databases. Therefore, custom reference databases are often created to meet the needs of specific research questions. Due to taxonomic inconsistencies, formatting issues, and technical difficulties, building a custom reference database requires tremendous effort. Here, we present taxalogue, an easy-to-use software for creating comprehensive and customized reference databases that provide clean and taxonomically harmonized records. In combination with extensive geographical filtering options, taxalogue opens up new possibilities for generating and testing evolutionary hypotheses. Methods: taxalogue collects DNA sequences from several online sources and combines them into a reference database. Taxonomic incongruencies between the different data sources can be harmonized according to available taxonomies. Dereplication and various filtering options are available regarding sequence quality or metadata information. taxalogue is implemented in the open-source Ruby programming language, and the source code is available at https://github.com/nwnoll/taxalogue. We benchmark four reference databases by sequence identity against eight queries from different localities and trapping devices. Subsamples from each reference database were used to compare how well another one is covered. Results: taxalogue produces reference databases with the best coverage at high identities for most tested queries, enabling more accurate, reliable predictions with higher certainty than the other benchmarked reference databases. Additionally, the performance of taxalogue is more consistent while providing good coverage for a variety of habitats, regions, and sampling methods. taxalogue simplifies the creation of reference databases and makes the process reproducible and transparent. Multiple available output formats for commonly used downstream applications facilitate the easy adoption of taxalogue in many different software pipelines. The resulting reference databases improve the taxonomic classification accuracy through high coverage of the query sequences at high identities.

Agricultural intensification and cereal aphid-parasitoid-hyperparasitoid food webs: network complexity, temporal variability and parasitism rates.

Agricultural intensification (AI) is currently a major driver of biodiversity loss and related ecosystem functioning decline. However, spatio-temporal changes in community structure induced by AI, and their relation to ecosystem functioning, remain largely unexplored. Here, we analysed 16 quantitative cereal aphid-parasitoid and parasitoid-hyperparasitoid food webs, replicated four times during the season, under contrasting AI regimes (organic farming in complex landscapes vs. conventional farming in simple landscapes). High AI increased food web complexity but also temporal variability in aphid-parasitoid food webs and in the dominant parasitoid species identity. Enhanced complexity and variability appeared to be controlled bottom-up by changes in aphid dominance structure and evenness. Contrary to the common expectations of positive biodiversity-ecosystem functioning relationships, community complexity (food-web complexity, species richness and evenness) was negatively related to primary parasitism rates. However, this relationship was positive for secondary parasitoids. Despite differences in community structures among different trophic levels, ecosystem services (parasitism rates) and disservices (aphid abundances and hyperparasitism rates) were always higher in fields with low AI. Hence, community structure and ecosystem functioning appear to be differently influenced by AI, and change differently over time and among trophic levels. In conclusion, intensified agriculture can support diverse albeit highly variable parasitoid-host communities, but ecosystem functioning might not be easy to predict from observed changes in community structure and composition.

The lipidome of an omnivorous insect responds to diet composition and social environment.

Lipids are biomolecules with essential roles in metabolic processes, signaling, and cellular architecture. In this study, we investigated changes in the lipidome of the house cricket Acheta domesticus subjected to diets of different nutritional composition (i.e., protein to carbohydrate ratio) and two distinct social environments (i.e., solitary or in groups). We measured relative abundances of 811 lipid species in whole-body cricket samples using flow injection analysis coupled to tandem mass spectrometry. We assessed differences in the relative abundances of lipid species induced by diet composition and social environment in female and male A. domesticus. Additionally, we performed a functional analysis of the lipids with significant differences using a recently developed database. We found that most differences in the relative abundances of lipid species were explained by sex alone. Furthermore, the lipidome of female A. domesticus was responsive to diet composition. Females fed with the balanced diet had an even higher abundance of lipids involved in lipid storage than their counterparts fed with a protein-rich diet. Interestingly, the male cricket lipidome was not responsive to diet composition. In addition, the social environment did not induce significant changes in the lipid profile neither in female nor in male crickets.

Plant genetic diversity affects multiple trophic levels and trophic interactions.

Intraspecific genetic diversity is an important component of biodiversity. A substantial body of evidence has demonstrated positive effects of plant genetic diversity on plant performance. However, it has remained unclear whether plant genetic diversity generally increases plant performance by reducing the pressure of plant antagonists across trophic levels for different plant life forms, ecosystems and climatic zones. Here, we analyse 4702 effect sizes reported in 413 studies that consider effects of plant genetic diversity on trophic groups and their interactions. We found that that increasing plant genetic diversity decreased the performance of plant antagonists including invertebrate herbivores, weeds, plant-feeding nematodes and plant diseases, while increasing the performance of plants and natural enemies of herbivores. Structural equation modelling indicated that plant genetic diversity increased plant performance partly by reducing plant antagonist pressure. These results reveal that plant genetic diversity often influences multiple trophic levels in ways that enhance natural pest control in managed ecosystems and consumer control of plants in natural ecosystems for sustainable plant production.

The relationship between agricultural intensification and biological control: experimental tests across Europe.

Agricultural intensification can affect biodiversity and related ecosystem services such as biological control, but large-scale experimental evidence is missing. We examined aphid pest populations in cereal fields under experimentally reduced densities of (1) ground-dwelling predators (-G), (2) vegetation-dwelling predators and parasitoids (-V), (3) a combination of (1) and (2) (-G-V), compared with open-fields (control), in contrasting landscapes with low vs. high levels of agricultural intensification (AI), and in five European regions. Aphid populations were 28%, 97%, and 199% higher in -G, -V, and -G-V treatments, respectively, compared to the open fields, indicating synergistic effects of both natural-enemy groups. Enhanced parasitoid: host and predator: prey ratios were related to reduced aphid population density and population growth. The relative importance of parasitoids and vegetation-dwelling predators greatly differed among European regions, and agricultural intensification affected biological control and aphid density only in some regions. This shows a changing role of species group identity in diverse enemy communities and a need to consider region-specific landscape management.