Effects of Traditional Orchard Abandonment and Landscape Context on the Beneficial Arthropod Community in a Mediterranean Agroecosystem.

Agricultural abandonment is one of the main land-use changes in Europe, and its consequences on biodiversity are context- and taxa-dependent. While several studies have worked on this topic, few have focused on traditional orchards, especially in different landscapes and under a Mediterranean climate. In this context, we aimed to determine the effects of almond orchard abandonment on the communities of three groups of beneficial arthropods and the role of the landscape context in modulating these effects. Between February and September 2019, four samplings were carried out in twelve almond orchards (three abandoned and three traditional (active orchards under traditional agricultural management) located in simple landscapes as well as three abandoned and three traditional in complex landscapes). Abandoned and traditional almond orchards harbor different arthropod communities and diversity metrics that are strongly conditioned by seasonality. Abandoned orchards can favor pollinators and natural enemies, providing alternative resources in simple landscapes. However, the role that abandoned orchards play in simple landscapes disappears as the percentage of semi-natural habitats in the landscape increases. Our results show that landscape simplification, through the loss of semi-natural habitats, has negative consequences on arthropod biodiversity, even in traditional farming landscapes with small fields and high crop diversity.

A multitaxa assessment of the effectiveness of agri-environmental schemes for biodiversity management.

Agri-environmental schemes (AES) aim to restore biodiversity and biodiversity-mediated ecosystem services in landscapes impoverished by modern agriculture. However, a systematic, empirical evaluation of different AES types across multiple taxa and functional groups is missing. Within one orthogonal design, we studied sown flowering AES types with different temporal continuity, size, and landscape context and used calcareous grasslands as seminatural reference habitat. We measured species richness of 12 taxonomic groups (vascular plants, cicadas, orthopterans, bees, butterflies, moths, hoverflies, flower visiting beetles, parasitoid wasps, carabid beetles, staphylinid beetles, and birds) representing 5 trophic levels. A total of 54,955 specimens were identified using traditional taxonomic methods, and bulk arthropod samples were identified through DNA metabarcoding, resulting in a total of 1,077 and 2,110 taxa, respectively. Species richness of most taxonomic groups, as well as multidiversity and richness of pollinators, increased with temporal continuity of AES types. Some groups responded to size and landscape context, but multidiversity and richness of pollinators and natural enemies were not affected. AES flowering fields supported different species assemblages than calcareous grasslands, but assemblages became more similar to those in seminatural grasslands with increasing temporal continuity. Our results indicate that AES flowering fields and seminatural grasslands function synergistically. Flowering fields support biodiversity even when they are relatively small and in landscapes with few remaining seminatural habitats. We therefore recommend a network of smaller, temporally continuous AES flowering fields of different ages, combined with permanent seminatural grasslands, to maximize benefits for biodiversity conservation and ecosystem service delivery in agricultural landscapes.

A critical analysis of the potential for EU Common Agricultural Policy measures to support wild pollinators on farmland.

Agricultural intensification and associated loss of high-quality habitats are key drivers of insect pollinator declines. With the aim of decreasing the environmental impact of agriculture, the 2014 EU Common Agricultural Policy (CAP) defined a set of habitat and landscape features (Ecological Focus Areas: EFAs) farmers could select from as a requirement to receive basic farm payments. To inform the post-2020 CAP, we performed a European-scale evaluation to determine how different EFA options vary in their potential to support insect pollinators under standard and pollinator-friendly management, as well as the extent of farmer uptake.A structured Delphi elicitation process engaged 22 experts from 18 European countries to evaluate EFAs options. By considering life cycle requirements of key pollinating taxa (i.e. bumble bees, solitary bees and hoverflies), each option was evaluated for its potential to provide forage, bee nesting sites and hoverfly larval resources.EFA options varied substantially in the resources they were perceived to provide and their effectiveness varied geographically and temporally. For example, field margins provide relatively good forage throughout the season in Southern and Eastern Europe but lacked early-season forage in Northern and Western Europe. Under standard management, no single EFA option achieved high scores across resource categories and a scarcity of late season forage was perceived.Experts identified substantial opportunities to improve habitat quality by adopting pollinator-friendly management. Improving management alone was, however, unlikely to ensure that all pollinator resource requirements were met. Our analyses suggest that a combination of poor management, differences in the inherent pollinator habitat quality and uptake bias towards catch crops and nitrogen-fixing crops severely limit the potential of EFAs to support pollinators in European agricultural landscapes. Policy Implications. To conserve pollinators and help protect pollination services, our expert elicitation highlights the need to create a variety of interconnected, well-managed habitats that complement each other in the resources they offer. To achieve this the Common Agricultural Policy post-2020 should take a holistic view to implementation that integrates the different delivery vehicles aimed at protecting biodiversity (e.g. enhanced conditionality, eco-schemes and agri-environment and climate measures). To improve habitat quality we recommend an effective monitoring framework with target-orientated indicators and to facilitate the spatial targeting of options collaboration between land managers should be incentivised.

La intensificación agrícola y la consecuente pérdida de hábitats de alta calidad son desencadenantes clave del declive de los insectos polinizadores. Con el objetivo de disminuir el impacto ambiental de la agricultura, la Política Agrícola Común (PAC) de la UE de 2014 definió un conjunto de medidas para hábitats y paisajes (Áreas de Enfoque Ecológico: EFA por sus siglas en inglés) que los agricultores podían seleccionar como requisito para recibir pagos agrícolas básicos. Para informar la reforma de la PAC a partir a 2020, realizamos una evaluación a escala europea para determinar cómo las diferentes opciones de EFA varían en su potencial para asistir a los insectos polinizadores bajo un manejo estándar y amigable con los polinizadores, así como su aceptación por parte de los agricultores.El proceso estructurado de elicitación Delphi para evaluar las opciones de EFA involucró a 22 expertos de 18 países europeos. Se consideraron los requisitos de los diferentes taxones de polinizadores (es decir, abejorros, abejas solitarias y sírfidos) evaluando cada opción por su potencial para proporcionar forraje, sitios de nidificación y recursos para las larvas.Las opciones de EFA variaron sustancialmente en la cantidad de recursos que se percibía que proporcionan y su efectividad vario geográfica y temporalmente. Por ejemplo, los márgenes de cultivos proporcionan un forraje relativamente bueno durante toda la temporada en el sur y el este de Europa, pero carecen de forraje a principios de temporada en el norte y oeste de Europa. Bajo el manejo estándar, ninguna opción de EFA logró puntuaciones altas en todas las categorías de recursos y en general se percibió una escasez de forraje al final de la temporada.Los expertos identificaron oportunidades sustanciales para mejorar la calidad del hábitat mediante la adopción de un manejo amigable con los polinizadores. Sin embargo, mejorar la gestión por sí solo es poco probable que garantice que se cumplan todos los requisitos necesarios para los polinizadores. Nuestro análisis sugiere que una combinación de manejo inadecuado, diferencias de calidad inherentes a los distintos hábitat y el sesgo de aceptación hacia cultivos de cobertura y cultivos que fijan nitrógeno limitan severamente el potencial de los EFA para apoyar a los polinizadores en los paisajes agrícolas europeos. Implicaciones políticas. Para conservar a los polinizadores y ayudar a proteger los servicios de polinización, nuestro estudio destaca la necesidad de crear una variedad de hábitats interconectados y bien administrados que se complementen entre sí en los recursos que ofrecen. Para lograr esto, la PAC post­2020 debe integrar los diferentes vehículos de implementación destinados a proteger la biodiversidad (por ejemplo, condicionalidad mejorada, esquemas ecológicos y medidas agroambientales y climáticas). Para mejorar la calidad del hábitat, recomendamos un marco de monitoreo efectivo con indicadores orientados a objetivos y incentivar la colaboración entre los administradores de las tierras.

L'intensification agricole et la perte associée d'habitats semi­naturels sont les principaux moteurs du déclin des insectes pollinisateurs. Dans l'intention de réduire l'impact environnemental de l'agriculture, la politique agricole commune (PAC) de l'UE de 2014 a défini un ensemble d'habitats et d'éléments paysagers (surfaces d'intérêt écologique: SIE) dans la mise en place ou le respect desquels les agriculteurs pouvaient s'engager comme condition pour bénéficier d'aides économiques européennes (droit au paiement de base). Pour éclairer la PAC post­2020, nous avons évalué à l'échelle européenne et à dire d'expert, d'une part les potentialités des diverses SIE à favoriser les insectes pollinisateurs, via une gestion standard et via une gestion optimisée, et d'autre part l'étendue de l'adoption de ces mesures par les agriculteurs.Un processus structuré d'élaboration et d'agrégation des opinions (méthode Delphi) a fait appel à 22 experts de 18 pays européens pour évaluer les potentialités des diverses SIE. Considérant les traits bioécologiques des principaux taxons pollinisateurs (i.e. bourdons, abeilles solitaires et syrphes), chaque SIE a été évaluée pour son potentiel à fournir des ressources trophiques et des sites de reproduction (sites de nidification pour les bourdons et abeilles, sites de ponte et développement larvaire pour les syrphes).Les SIE différaient considérablement les unes des autres sur les ressources qu'elles étaient censées offrir et leur efficacité variait géographiquement et temporellement. Par exemple, les bords de champ peuvent fournir des ressources trophiques tout au long de l'année en Europe du Sud et de l'Est mais pas en début de saison en Europe du Nord et de l'Ouest. En cas de gestion standard, aucun type de SIE n'atteint de score élevé pour aucun type de ressource, et une période de disette alimentaire survient en fin de saison.Les experts ont mis en évidence de possibles et substantielles améliorations des SIE par le biais de leur gestion optimisée. Cependant, cette seule amélioration ne garantit pas la fourniture de ressources suffisantes aux pollinisateurs des paysages agricoles européens. Pour cela, des habitats spécifiques doivent être favorisés, dont la mise en place ne doit pas être entravée par un choix massif de SIE à base de cultures intermédiaires pièges à nitrates ou fixatrices d'azote. Implications politiques. Pour préserver les pollinisateurs et le service de pollinisation des plantes entomophiles, notre étude souligne la nécessité de créer une diversité d'habitats interconnectés, gérés de façon optimale, qui se complètent mutuellement dans les ressources qu'ils offrent. Pour atteindre cet objectif, la PAC post­2020 doit adopter une vision holistique de la mise en œuvre des différents leviers de protection de la biodiversité (e.g. éco­conditionnalité renforcée, programmes verts ou 'eco­schemes', mesures agro­environnementales et climatiques). Pour réellement améliorer la qualité des habitats, nous recommandons des suivis efficaces de la biodiversité à l'aide d'indicateurs pertinents. Enfin, pour optimiser la disposition spatiale des SIE et leur connectivité, la collaboration entre les différents gestionnaires des espaces agricoles doit être encouragée.

A intensificação agrícola e a perda associada de habitats de elevada qualidade são os principais factores que impulsionam o declínio dos insetos polinizadores. A fim de mitigar o impacto ambiental da agricultura, a Política Agrícola Comum (PAC) da UE, de 2014, definiu um conjunto de atributos ou estruturas do habitat e da paisagem, designadas de Áreas Foco Ecológico (AFEs) que devem ser mantidas pelos agricultores como requisito para obter as ajudas económicas previstas nas medidas agroambientais. No presente trabalho realizamos uma avaliação à escala europeia das diferentes opções destas estruturas, a fim de munir a PAC pós­2020, com informação sobre a importância das AFEs. Estas variam muito quanto ao seu potencial no apoio às populações de polinizadores, de acordo com a extensão da sua aceitação pelos agricultores e das práticas adoptadas por estes na sua gestão, que podem consistir em práticas padrão ou práticas mais amigáveis para os polinizadores.Um processo estruturado, com base na técnica de elicitação de Delphi foi desenvolvido, envolvendo 22 especialistas de 18 países europeus, com o objectivo de avaliar as opções de AFEs previstas na PAC. Esta avaliação levou em consideração os requisitos do ciclo de vida dos taxa dos principais polinizadores, ou seja, as abelhas, as abelhas solitárias e os sirfídeos ou moscas­das­flores. Cada AFE foi avaliada quanto ao seu potencial para fornecer alimento, locais de nidificação, e recursos para as larvas dos sirfídeos.A percepção quanto à eficácia das AFEs como fonte de recursos (alimento) para os polinizadores variou substancialmente, do ponto de vista quer geográfico, quer temporal (época do ano). Por exemplo, a AFE, faixas verdes nas margens do campo são consideradas uma boa fonte de alimento, no sul e leste da Europa, durante todo ano, mas ineficazes, no norte e oeste da Europa, no início do ano. Nenhuma EFA alcançou pontuações elevadas na categoria de recursos (fonte de alimento), quando submetida ao maneio padrão, sendo consideradas ineficientes, na segunda metade do ano.Os especialistas envolvidos identificaram oportunidades de melhoria substancial na qualidade do habitat, através da adopção de práticas de maneio das EFAs mais "amigáveis" para com os polinizadores. No entanto, a melhoria das práticas de maneio das EFAs por si só, dificilmente garantirá todos os requisitos necessários para a manutenção das populações de polinizadores. A nossa avaliação sugere que a combinação de práticas de má gestão (maneio), diferenças inerentes à qualidade do habitat dos polinizadores e o aumento do bias que resulta da utilização de espécies de crescimento rápido ou fixadoras de azoto limitam severamente o papel e potencial destas estruturas na manutenção das populações de polinizadores nas paisagens agrícolas europeias. Implicações políticas. A conservação dos polinizadores ajuda a proteger os serviços de polinização providenciados por estes. O nosso estudo destaca a necessidade de criar uma variedade de habitats interconectados e geridos de forma que se complementem na oferta de recursos (alimento, locais de nidificação e recursos para as larvas) aos polinizadores. Para atingir este objectivo, a PAC pós­2020 deve adoptar uma visão holística na implementação das EFAs, que integre os diferentes programas destinados a protecção da biodiversidade (por exemplo, maior condicionalidade, esquemas ecológicos, e medidas agroambientais e de adaptação climática). Para melhorar a qualidade do habitat, recomendamos uma estrutura de monitorização eficaz suportada por indicadores quantitativos e qualitativos orientados para metas, que permitam facilitar a tomada de decisões direcionadas especificamente para as EFAs, e que a colaboração entre os gestores da terra (agricultores) seja incentivada.

The circadian clock uses different environmental time cues to synchronize emergence and locomotion of the solitary bee Osmia bicornis.

Life on earth adapted to the daily reoccurring changes in environment by evolving an endogenous circadian clock. Although the circadian clock has a crucial impact on survival and behavior of solitary bees, many aspects of solitary bee clock mechanisms remain unknown. Our study is the first to show that the circadian clock governs emergence in Osmia bicornis, a bee species which overwinters as adult inside its cocoon. Therefore, its eclosion from the pupal case is separated by an interjacent diapause from its emergence in spring. We show that this bee species synchronizes its emergence to the morning. The daily rhythms of emergence are triggered by temperature cycles but not by light cycles. In contrast to this, the bee's daily rhythms in locomotion are synchronized by light cycles. Thus, we show that the circadian clock of O. bicornis is set by either temperature or light, depending on what activity is timed. Light is a valuable cue for setting the circadian clock when bees have left the nest. However, for pre-emerged bees, temperature is the most important cue, which may represent an evolutionary adaptation of the circadian system to the cavity-nesting life style of O. bicornis.

How does timing of flowering affect competition for pollinators, flower visitation and seed set in an early spring grassland plant?

Knowledge on how the timing of flowering is related to plant fitness and species interactions is crucial to understand consequences of phenological shifts as they occur under climate change. Early flowering plants may face advantages of low competition for pollinators and disadvantages of low pollinator abundances and unfavourable weather conditions. However, it is unknown how this trade-off changes over the season and how the timing affects reproductive success. On eight grasslands we recorded intra-seasonal changes in pollinators, co-flowering plants, weather conditions, flower visitation rates, floral longevity and seed set of Pulsatilla vulgaris. Although bee abundances and the number of pollinator-suitable hours were low at the beginning of the season, early flowers of P. vulgaris received higher flower visitation rates and estimated total number of bee visits than later flowers, which was positively related to seed set. Flower visitation rates decreased over time and with increasing number of co-flowering plants, which competed with P. vulgaris for pollinators. Low interspecific competition for pollinators seems to be a major driver for early flowering dates. Thus, non-synchronous temporal shifts of co-flowering plants as they may occur under climate warming can be expected to strongly affect plant-pollinator interactions and the fitness of the involved plants.

A global synthesis reveals biodiversity-mediated benefits for crop production.

Human land use threatens global biodiversity and compromises multiple ecosystem functions critical to food production. Whether crop yield-related ecosystem services can be maintained by a few dominant species or rely on high richness remains unclear. Using a global database from 89 studies (with 1475 locations), we partition the relative importance of species richness, abundance, and dominance for pollination; biological pest control; and final yields in the context of ongoing land-use change. Pollinator and enemy richness directly supported ecosystem services in addition to and independent of abundance and dominance. Up to 50% of the negative effects of landscape simplification on ecosystem services was due to richness losses of service-providing organisms, with negative consequences for crop yields. Maintaining the biodiversity of ecosystem service providers is therefore vital to sustain the flow of key agroecosystem benefits to society.

Warmer temperatures advance flowering in a spring plant more strongly than emergence of two solitary spring bee species.

Climate warming has the potential to disrupt plant-pollinator interactions or to increase competition of co-flowering plants for pollinators, due to species-specific phenological responses to temperature. However, studies focusing on the effect of temperature on solitary bee emergence and the flowering onset of their food plants under natural conditions are still rare. We studied the effect of temperature on the phenology of the two spring bees Osmia cornuta and Osmia bicornis, by placing bee cocoons on eleven grasslands differing in mean site temperature. On seven grasslands, we additionally studied the effect of temperature on the phenology of the red-list plant Pulsatilla vulgaris, which was the first flowering plant, and of co-flowering plants with later flowering. With a warming of 0.1°C, the abundance-weighted mean emergence of O. cornuta males advanced by 0.4 days. Females of both species did not shift their emergence. Warmer temperatures advanced the abundance-weighted mean flowering of P. vulgaris by 1.3 days per 0.1°C increase, but did not shift flowering onset of co-flowering plants. Competition for pollinators between P. vulgaris and co-flowering plants does not increase within the studied temperature range. We demonstrate that temperature advances plant flowering more strongly than bee emergence suggesting an increased risk of pollinator limitation for the first flowers of P. vulgaris.

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.

Pollinator size and its consequences: Robust estimates of body size in pollinating insects.

Body size is an integral functional trait that underlies pollination-related ecological processes, yet it is often impractical to measure directly. Allometric scaling laws have been used to overcome this problem. However, most existing models rely upon small sample sizes, geographically restricted sampling and have limited applicability for non-bee taxa. Allometric models that consider biogeography, phylogenetic relatedness, and intraspecific variation are urgently required to ensure greater accuracy. We measured body size as dry weight and intertegular distance (ITD) of 391 bee species (4,035 specimens) and 103 hoverfly species (399 specimens) across four biogeographic regions: Australia, Europe, North America, and South America. We updated existing models within a Bayesian mixed-model framework to test the power of ITD to predict interspecific variation in pollinator dry weight in interaction with different co-variates: phylogeny or taxonomy, sexual dimorphism, and biogeographic region. In addition, we used ordinary least squares regression to assess intraspecific dry weight ~ ITD relationships for ten bees and five hoverfly species. Including co-variates led to more robust interspecific body size predictions for both bees and hoverflies relative to models with the ITD alone. In contrast, at the intraspecific level, our results demonstrate that the ITD is an inconsistent predictor of body size for bees and hoverflies. The use of allometric scaling laws to estimate body size is more suitable for interspecific comparative analyses than assessing intraspecific variation. Collectively, these models form the basis of the dynamic R package, "pollimetry," which provides a comprehensive resource for allometric pollination research worldwide.

Explaining the variability in the response of annual eusocial insects to mass-flowering events.

Empirical studies of annual eusocial insects in agricultural landscapes report contrasting findings with regard to colony responses to mass-flowering of crops such as oilseed rape. In particular, total sexual production is often unaffected by such events, whereas worker number responds with a prominent increase. To resolve these conflicting observations, we model-using an established approach-the expected change in worker and sexual numbers in response to an increased worker productivity induced by mass-flowering events at different times of the season. We find that the predicted response pattern is mainly shaped by the degree to which individual worker productivity is reduced by an increasing number of workers in the colony. Different environmental conditions and colony characteristics result in different levels of interference of workers, for example, during foraging or nest construction. Reduction in individual productivity is low, when worker interference is negligible ("weak limitation") and high when an increasing number of workers substantially decreases per-capita efficiency ("strong limitation"). For weak limitation, any mass-flowering event that ends before the production of sexuals starts has a strong multiplicative impact on both worker and sexual numbers. The magnitude of the effect is quite independent of the precise timing of such an event. After the onset of sexual production, mass-flowering has a weaker effect, as the added resource supply is only linearly transferred into production of additional sexuals. For colonies under strong limitation, the predicted impact of mass-flowering events is generally weaker, especially on the production of sexuals, and the timing of mass-flowering events becomes more influential: Production of sexuals profits more from late than from early mass-flowering events. Consequently, early mass-flowering events are predicted to have a prominent effect on worker numbers but a negligible one on the output of sexuals. The model presented provides a mechanistic explanation of why increased worker abundances do not necessarily translate into increased production of sexuals. The model is also applicable to other eusocial insects such as paper wasps whenever brief pulses of massive resource availability shortly elevate resource intake rates above the "normal" levels.

Overwintering temperature and body condition shift emergence dates of spring-emerging solitary bees.

Solitary bees in seasonal environments must align their life-cycles with favorable environmental conditions and resources; the timing of their emergence is highly fitness relevant. In several bee species, overwintering temperature influences both emergence date and body weight at emergence. High variability in emergence dates among specimens overwintering at the same temperatures suggests that the timing of emergence also depends on individual body conditions. However, possible causes for this variability, such as individual differences in body size or weight, have been rarely studied. In a climate chamber experiment using two spring-emerging mason bees (Osmia cornuta and O. bicornis), we investigated the relationship between temperature, emergence date, body weight, and body size, the last of which is not affected by overwintering temperature. Our study showed that body weight declined during hibernation more strongly in warm than in cold overwintering temperatures. Although bees emerged earlier in warm than in cold overwintering temperatures, at the time of emergence, bees in warm overwintering temperatures had lower body weights than bees in cold overwintering temperatures (exception of male O. cornuta). Among specimens that experienced the same overwintering temperatures, small and light bees emerged later than their larger and heavier conspecifics. Using a simple mechanistic model we demonstrated that spring-emerging solitary bees use a strategic approach and emerge at a date that is most promising for their individual fitness expectations. Our results suggest that warmer overwintering temperatures reduce bee fitness by causing a decrease in body weight at emergence. We showed furthermore that in order to adjust their emergence dates, bees use not only temperature but also their individual body condition as triggers. This may explain differing responses to climate warming within and among bee populations and may have consequences for bee-plant interactions as well as for the persistence of bee populations under climate change.

Desynchronizations in bee-plant interactions cause severe fitness losses in solitary bees.

Global warming can disrupt mutualistic interactions between solitary bees and plants when increasing temperature differentially changes the timing of interacting partners. One possible scenario is for insect phenology to advance more rapidly than plant phenology. However, empirical evidence for fitness consequences due to temporal mismatches is lacking for pollinators and it remains unknown if bees have developed strategies to mitigate fitness losses following temporal mismatches. We tested the effect of temporal mismatches on the fitness of three spring-emerging solitary bee species, including one pollen specialist. Using flight cages, we simulated (i) a perfect synchronization (from a bee perspective): bees and flowers occur simultaneously, (ii) a mismatch of 3 days and (iii) a mismatch of 6 days, with bees occurring earlier than flowers in the latter two cases. A mismatch of 6 days caused severe fitness losses in all three bee species, as few bees survived without flowers. Females showed strongly reduced activity and reproductive output compared to synchronized bees. Fitness consequences of a 3-day mismatch were species-specific. Both the early-spring species Osmia cornuta and the mid-spring species Osmia bicornis produced the same number of brood cells after a mismatch of 3 days as under perfect synchronization. However, O. cornuta decreased the number of female offspring, whereas O. bicornis spread the brood cells over fewer nests, which may increase offspring mortality, e.g. due to parasitoids. The late-spring specialist Osmia brevicornis produced fewer brood cells even after a mismatch of 3 days. Additionally, our results suggest that fitness losses after temporal mismatches are higher during warm than cold springs, as the naturally occurring temperature variability revealed that warm temperatures during starvation decreased the survival rate of O. bicornis. We conclude that short temporal mismatches can cause clear fitness losses in solitary bees. Although our results suggest that bees have evolved species-specific strategies to mitigate fitness losses after temporal mismatches, the bees were not able to completely compensate for impacts on their fitness after temporal mismatches with their food resources.

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.

Enhanced aphid abundance in spring desynchronizes predator-prey and plant-microorganism interactions.

Climate change leads to phenology shifts of many species. However, not all species shift in parallel, which can desynchronize interspecific interactions. Within trophic cascades, herbivores can be top-down controlled by predators or bottom-up controlled by host plant quality and host symbionts, such as plant-associated micro-organisms. Synchronization of trophic levels is required to prevent insect herbivore (pest) outbreaks. In a common garden experiment, we simulated an earlier arrival time (~2 weeks) of the aphid Rhopalosiphum padi on its host grass Lolium perenne by enhancing the aphid abundance during the colonization period. L. perenne was either uninfected or infected with the endophytic fungus Epichloë festucae var. lolii. The plant symbiotic fungus produces insect deterring alkaloids within the host grass. Throughout the season, we tested the effects of enhanced aphid abundance in spring on aphid predators (top-down) and grass-endophyte (bottom-up) responses. Higher aphid population sizes earlier in the season lead to overall higher aphid abundances, as predator occurrence was independent of aphid abundances on the pots. Nonetheless, after predator occurrence, aphids were controlled within 2 weeks on all pots. Possible bottom-up control of aphids by increased endophyte concentrations occurred time delayed after high herbivore abundances. Endophyte-derived alkaloid concentrations were not significantly affected by enhanced aphid abundance but increased throughout the season. We conclude that phenology shifts in an herbivorous species can desynchronize predator-prey and plant-microorganism interactions and might enhance the probability of pest outbreaks with climate change.

Predicting bee community responses to land-use changes: Effects of geographic and taxonomic biases.

Land-use change and intensification threaten bee populations worldwide, imperilling pollination services. Global models are needed to better characterise, project, and mitigate bees' responses to these human impacts. The available data are, however, geographically and taxonomically unrepresentative; most data are from North America and Western Europe, overrepresenting bumblebees and raising concerns that model results may not be generalizable to other regions and taxa. To assess whether the geographic and taxonomic biases of data could undermine effectiveness of models for conservation policy, we have collated from the published literature a global dataset of bee diversity at sites facing land-use change and intensification, and assess whether bee responses to these pressures vary across 11 regions (Western, Northern, Eastern and Southern Europe; North, Central and South America; Australia and New Zealand; South East Asia; Middle and Southern Africa) and between bumblebees and other bees. Our analyses highlight strong regionally-based responses of total abundance, species richness and Simpson's diversity to land use, caused by variation in the sensitivity of species and potentially in the nature of threats. These results suggest that global extrapolation of models based on geographically and taxonomically restricted data may underestimate the true uncertainty, increasing the risk of ecological surprises.

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

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

Annual dynamics of wild bee densities: attractiveness and productivity effects of oilseed rape.

Mass-flowering crops may affect long-term population dynamics, but effects on pollinators have never been studied across several years. We monitored wild bees in oilseed rape fields in 16 landscapes in Germany in two consecutive years. Effects on bee densities of landscape oilseed rape cover in the years of monitoring and in the previous years were evaluated with landscape data from three consecutive years. We fit empirical data to a mechanistic model to provide estimates for oilseed rape attractiveness and its effect on bee productivity in comparison to the rest of the landscape, and we evaluated consequences for pollinator densities in consecutive years. Our results show that high oilseed rape cover in the previous year enhances current densities of wild bees (except for bumble bees). Moreover, we show a strong attractiveness of and dilution on (i.e., decreasing bee densities with increasing landscape oilseed rape cover) oilseed rape for bees during flowering in the current year, modifying the effect of the previous year's oilseed rape cover in the case of wild bees (excluding Bombus). As long as other factors such as nesting sites or natural enemies do not limit bee reproduction, our findings suggest long-term positive effects of mass-flowering crops on bee populations, at least for non-Bombus generalists, which possibly help to maintain crop pollination services even when crop area increases. Similar effects are conceivable for other organisms providing ecosystem services in annual crops and should be considered in future studies.

Increased efficiency in identifying mixed pollen samples by meta-barcoding with a dual-indexing approach.

BACKGROUND: Meta-barcoding of mixed pollen samples constitutes a suitable alternative to conventional pollen identification via light microscopy. Current approaches however have limitations in practicability due to low sample throughput and/or inefficient processing methods, e.g. separate steps for amplification and sample indexing. RESULTS: We thus developed a new primer-adapter design for high throughput sequencing with the Illumina technology that remedies these issues. It uses a dual-indexing strategy, where sample-specific combinations of forward and reverse identifiers attached to the barcode marker allow high sample throughput with a single sequencing run. It does not require further adapter ligation steps after amplification. We applied this protocol to 384 pollen samples collected by solitary bees and sequenced all samples together on a single Illumina MiSeq v2 flow cell. According to rarefaction curves, 2,000-3,000 high quality reads per sample were sufficient to assess the complete diversity of 95% of the samples. We were able to detect 650 different plant taxa in total, of which 95% were classified at the species level. Together with the laboratory protocol, we also present an update of the reference database used by the classifier software, which increases the total number of covered global plant species included in the database from 37,403 to 72,325 (93% increase). CONCLUSIONS: This study thus offers improvements for the laboratory and bioinformatical workflow to existing approaches regarding data quantity and quality as well as processing effort and cost-effectiveness. Although only tested for pollen samples, it is furthermore applicable to other research questions requiring plant identification in mixed and challenging samples.

Delivery of crop pollination services is an insufficient argument for wild pollinator conservation.

There is compelling evidence that more diverse ecosystems deliver greater benefits to people, and these ecosystem services have become a key argument for biodiversity conservation. However, it is unclear how much biodiversity is needed to deliver ecosystem services in a cost-effective way. Here we show that, while the contribution of wild bees to crop production is significant, service delivery is restricted to a limited subset of all known bee species. Across crops, years and biogeographical regions, crop-visiting wild bee communities are dominated by a small number of common species, and threatened species are rarely observed on crops. Dominant crop pollinators persist under agricultural expansion and many are easily enhanced by simple conservation measures, suggesting that cost-effective management strategies to promote crop pollination should target a different set of species than management strategies to promote threatened bees. Conserving the biological diversity of bees therefore requires more than just ecosystem-service-based arguments.