Michal Woyciechowski

MEASURING BEE DIVERSITY IN DIFFERENT EUROPEAN HABITATS AND BIOGEOGRAPHICAL REGIONS

Bee pollinators are currently recorded with many different sampling methods. However, the relative performances of these methods have not been systematically evaluated and compared. In response to the strong need to record ongoing shifts in pollinator diversity and abundance, global and regional pollinator initiatives must adopt standardized sampling protocols when developing large-scale and long-term monitoring schemes. We systematically evaluated the performance of six sampling methods (observation plots, pan traps, standardized and variable transect walks, trap nests with reed internodes or paper tubes) that are commonly used across a wide range of geographical regions in Europe and in two habitat types (agricultural and seminatural). We focused on bees since they represent the most important pollinator group worldwide. Several characteristics of the methods were considered in order to evaluate their performance in assessing bee diversity: sample coverage, observed species richness, species richness estimators, collector biases (identified by subunit-based rarefaction curves), species composition of the samples, and the indication of overall bee species richness (estimated from combined total samples). The most efficient method in all geographical regions, in both the agricultural and seminatural habitats, was the pan trap method. It had the highest sample coverage, collected the highest number of species, showed negligible collector bias, detected similar species as the transect methods, and was the best indicator of overall bee species richness. The transect methods were also relatively efficient, but they had a significant collector bias. The observation plots showed poor performance. As trap nests are restricted to cavity-nesting bee species, they had a naturally low sample coverage. However, both trap nest types detected additional species that were not recorded by any of the other methods. For large-scale and long-term monitoring schemes with surveyors with different experience levels, we recommend pan traps as the most efficient, unbiased, and cost-effective method for sampling bee diversity. Trap nests with reed internodes could be used as a complementary sampling method to maximize the numbers of collected species. Transect walks are the principal method for detailed studies focusing on plant-pollinator associations. Moreover, they can be used in monitoring schemes after training the surveyors to standardize their collection skills.

Non-bee insects are important contributors to global crop pollination

Significance Many of the world’s crops are pollinated by insects, and bees are often assumed to be the most important pollinators. To our knowledge, our study is the first quantitative evaluation of the relative contribution of non-bee pollinators to global pollinator-dependent crops. Across 39 studies we show that insects other than bees are efficient pollinators providing 39% of visits to crop flowers. A shift in perspective from a bee-only focus is needed for assessments of crop pollinator biodiversity and the economic value of pollination. These studies should also consider the services provided by other types of insects, such as flies, wasps, beetles, and butterflies—important pollinators that are currently overlooked. Wild and managed bees are well documented as effective pollinators of global crops of economic importance. However, the contributions by pollinators other than bees have been little explored despite their potential to contribute to crop production and stability in the face of environmental change. Non-bee pollinators include flies, beetles, moths, butterflies, wasps, ants, birds, and bats, among others. Here we focus on non-bee insects and synthesize 39 field studies from five continents that directly measured the crop pollination services provided by non-bees, honey bees, and other bees to compare the relative contributions of these taxa. Non-bees performed 25–50% of the total number of flower visits. Although non-bees were less effective pollinators than bees per flower visit, they made more visits; thus these two factors compensated for each other, resulting in pollination services rendered by non-bees that were similar to those provided by bees. In the subset of studies that measured fruit set, fruit set increased with non-bee insect visits independently of bee visitation rates, indicating that non-bee insects provide a unique benefit that is not provided by bees. We also show that non-bee insects are not as reliant as bees on the presence of remnant natural or seminatural habitat in the surrounding landscape. These results strongly suggest that non-bee insect pollinators play a significant role in global crop production and respond differently than bees to landscape structure, probably making their crop pollination services more robust to changes in land use. Non-bee insects provide a valuable service and provide potential insurance against bee population declines.

Combined effects of global change pressures on animal-mediated pollination

Pollination is an essential process in the sexual reproduction of seed plants and a key ecosystem service to human welfare. Animal pollinators decline as a consequence of five major global change pressures: climate change, landscape alteration, agricultural intensification, non-native species, and spread of pathogens. These pressures, which differ in their biotic or abiotic nature and their spatiotemporal scales, can interact in nonadditive ways (synergistically or antagonistically), but are rarely considered together in studies of pollinator and/or pollination decline. Management actions aimed at buffering the impacts of a particular pressure could thereby prove ineffective if another pressure is present. Here, we focus on empirical evidence of the combined effects of global change pressures on pollination, highlighting gaps in current knowledge and future research needs.

Life expectancy and onset of foraging in the honeybee (Apis mellifera)

Predictions that precocious foraging in honeybee workers is a result of shortening of their life expectancy were tested in both laboratory and field experiments. In the laboratory experiment, we assessed the impact of anaesthesia with CO2 and infection with Nosema apis on the lifespan of workers. In the field experiment, the age at onset of foraging was observed in groups of workers with different expected lifespans. In both the experiments, workers originating from one queen inseminated with the semen of one drone were divided into five groups. The first group was anaesthetized with CO2 on the first day of life. Workers from the other three groups were individually inoculated with a constant number of N. apis spores on the 1st, 6th and 11th days of life. Workers from the fifth control group were neither treated with CO2 nor inoculated in any way. Both the laboratory and field experiments revealed that anaesthetized and infected workers had shorter expected lifespans compared to control bees. Amongst infected workers, those inoculated earlier in life survived for a significantly shorter period of time in comparison to those infected later in life. In agreement with the expectation, the field experiment showed that anaesthetized and infected workers with shorter expected lifespan start foraging earlier than control workers. Amongst the infected workers, age at inoculation correlated with age at onset of foraging. This means that short-lived workers complete safe nest tasks and begin riskier foraging earlier in life. Our results provide a strong support for the hypothesis that the division of labour in eusocial insects is a consequence of the different expected worker lifespan and different risk associated with their tasks; however, they do not contradict other existing explanations.

Assessing bee species richness in two Mediterranean communities: importance of habitat type and sampling techniques

The decline of bees has raised concerns regarding their conservation and the maintenance of ecosystem services they provide to bee-pollinated wild flowers and crops. Although the Mediterranean region is a hotspot for bee species richness, their status remains poorly studied. There is an urgent need for cost-effective, reliable, and unbiased sampling methods that give good bee species richness estimates. This study aims: (a) to assess bee species richness in two common Mediterranean habitat types: semi-natural scrub (phrygana) and managed olive groves; (b) to compare species richness in those systems to that of other biogeographic regions, and (c) to assess whether six different sampling methods (pan traps, variable and standardized transect walks, observation plots and trap nests), previously tested in other European biogeographic regions, are suitable in Mediterranean communities. Eight study sites, four per habitat type, were selected on the island of Lesvos, Greece. The species richness observed was high compared to other habitat types worldwide for which comparable data exist. Pan traps collected the highest proportion of the total bee species richness across all methods at the scale of a study site. Variable and standardized transect walks detected the highest total richness over all eight study sites. Trap nests and observation plots detected only a limited fraction of the bee species richness. To assess the total bee species richness in bee diversity hotspots, such as the studied habitats, we suggest a combination of transect walks conducted by trained bee collectors and pan trap sampling.

Developing European Conservation and Mitigation Tools for Pollination Services: Approaches of the STEP (Status and Trends of European Pollinators) Project

Summary Pollinating insects form a key component of European biodiversity, and provide a vital ecosystem service to crops and wild plants. There is growing evidence of declines in both wild and domesticated pollinators, and parallel declines in plants relying upon them. The STEP project (Status and Trends of European Pollinators, 2010–2015, www.step-project.net) is documenting critical elements in the nature and extent of these declines, examining key functional traits associated with pollination deficits, and developing a Red List for some European pollinator groups. Together these activities are laying the groundwork for future pollinator monitoring programmes. STEP is also assessing the relative importance of potential drivers of pollinator declines, including climate change, habitat loss and fragmentation, agrochemicals, pathogens, alien species, light pollution, and their interactions. We are measuring the ecological and economic impacts of declining pollinator services and floral resources, including effects on wild plant populations, crop production and human nutrition. STEP is reviewing existing and potential mitigation options, and providing novel tests of their effectiveness across Europe. Our work is building upon existing and newly developed datasets and models, complemented by spatially-replicated campaigns of field research to fill gaps in current knowledge. Findings are being integrated into a policy-relevant framework to create evidence-based decision support tools. STEP is establishing communication links to a wide range of stakeholders across Europe and beyond, including policy makers, beekeepers, farmers, academics and the general public. Taken together, the STEP research programme aims to improve our understanding of the nature, causes, consequences and potential mitigation of declines in pollination services at local, national, continental and global scales.

Contribution of insect pollinators to crop yield and quality varies with agricultural intensification

Background. Up to 75% of crop species benefit at least to some degree from animal pollination for fruit or seed set and yield. However, basic information on the level of pollinator dependence and pollinator contribution to yield is lacking for many crops. Even less is known about how insect pollination affects crop quality. Given that habitat loss and agricultural intensification are known to decrease pollinator richness and abundance, there is a need to assess the consequences for different components of crop production. Methods. We used pollination exclusion on flowers or inflorescences on a whole plant basis to assess the contribution of insect pollination to crop yield and quality in four flowering crops (spring oilseed rape, field bean, strawberry, and buckwheat) located in four regions of Europe. For each crop, we recorded abundance and species richness of flower visiting insects in ten fields located along a gradient from simple to heterogeneous landscapes. Results. Insect pollination enhanced average crop yield between 18 and 71% depending on the crop. Yield quality was also enhanced in most crops. For instance, oilseed rape had higher oil and lower chlorophyll contents when adequately pollinated, the proportion of empty seeds decreased in buckwheat, and strawberries’ commercial grade improved; however, we did not find higher nitrogen content in open pollinated field beans. Complex landscapes had a higher overall species richness of wild pollinators across crops, but visitation rates were only higher in complex landscapes for some crops. On the contrary, the overall yield was consistently enhanced by higher visitation rates, but not by higher pollinator richness. Discussion. For the four crops in this study, there is clear benefit delivered by pollinators on yield quantity and/or quality, but it is not maximized under current agricultural intensification. Honeybees, the most abundant pollinator, might partially compensate the loss of wild pollinators in some areas, but our results suggest the need of landscape-scale actions to enhance wild pollinator populations.

Trait matching of flower visitors and crops predicts fruit set better than trait diversity

Understanding the relationships between trait diversity, species diversity and ecosystem functioning is essential for sustainable management. For functions comprising two trophic levels, trait matching between interacting partners should also drive functioning. However, the predictive ability of trait diversity and matching is unclear for most functions, particularly for crop pollination, where interacting partners did not necessarily co-evolve. World-wide, we collected data on traits of flower visitors and crops, visitation rates to crop flowers per insect species and fruit set in 469 fields of 33 crop systems. Through hierarchical mixed-effects models, we tested whether flower visitor trait diversity and/or trait matching between flower visitors and crops improve the prediction of crop fruit set (functioning) beyond flower visitor species diversity and abundance. Flower visitor trait diversity was positively related to fruit set, but surprisingly did not explain more variation than flower visitor species diversity. The best prediction of fruit set was obtained by matching traits of flower visitors (body size and mouthpart length) and crops (nectar accessibility of flowers) in addition to flower visitor abundance, species richness and species evenness. Fruit set increased with species richness, and more so in assemblages with high evenness, indicating that additional species of flower visitors contribute more to crop pollination when species abundances are similar.Synthesis and applications. Despite contrasting floral traits for crops world-wide, only the abundance of a few pollinator species is commonly managed for greater yield. Our results suggest that the identification and enhancement of pollinator species with traits matching those of the focal crop, as well as the enhancement of pollinator richness and evenness, will increase crop yield beyond current practices. Furthermore, we show that field practitioners can predict and manage agroecosystems for pollination services based on knowledge of just a few traits that are known for a wide range of flower visitor species. Despite contrasting floral traits for crops world-wide, only the abundance of a few pollinator species is commonly managed for greater yield. Our results suggest that the identification and enhancement of pollinator species with traits matching those of the focal crop, as well as the enhancement of pollinator richness and evenness, will increase crop yield beyond current practices. Furthermore, we show that field practitioners can predict and manage agroecosystems for pollination services based on knowledge of just a few traits that are known for a wide range of flower visitor species. Editors Choice

Division of labour among workers with different life expectancy in the ant Myrmica scabrinodis

Workers present in the colony of social insects differ in age. The strategy of engaging younger workers in safer intranidal tasks, and older individuals in riskier tasks, for example, foraging, increases the average longevity of workers, and thus colony fitness. The transition to becoming a forager can be influenced by many environmental and social factors, but it has remained unclear whether the onset of foraging is also directly dependent on life expectancy. We tested this hypothesis with laboratory colonies of the ant Myrmica scabrinodis by creating groups of workers with reduced life expectancy. Ants were either anaesthetized with carbon dioxide or injured by removing their propodeal spines. Both treatments significantly shortened worker life expectancy in comparison to untreated control workers. Next, we showed that workers with an experimentally reduced life span became foragers earlier in life than control workers. This implies that ant workers adjust their threshold for engaging in risky foraging according to their life expectancy.

Plant establishment and invasions: an increase in a seed disperser combined with land abandonment causes an invasion of the non-native walnut in Europe.

Successful invasive species often are established for a long time period before increasing exponentially in abundance. This lag phase is one of the least understood phenomena of biological invasions. Plant invasions depend on three factors: a seed source, suitable habitat and a seed disperser. The non-native walnut, Juglans regia, has been planted for centuries in Central Europe but, until recently, has not spread beyond planted areas. However, in the past 20 years, we have observed a rapid increase in walnut abundance, specifically in abandoned agricultural fields. The dominant walnut disperser is the rook, Corvus frugilegus. During the past 50 years, rooks have increased in abundance and now commonly inhabit human settlements, where walnut trees are planted. Central Europe has, in the past few decades, experienced large-scale land abandonment. Walnut seeds dispersed into ploughed fields do not survive, but when cached into ploughed and then abandoned fields, they successfully establish. Rooks preferentially cache seeds in ploughed fields. Thus, land-use change combined with disperser changes can cause rapid increase of a non-native species, allowing it to become invasive. This may have cascading effects on the entire ecosystem. Thus, species that are non-native and not invasive can become invasive as habitats and dispersers change.