Hajnalka Szentgyörgyi

Stability of pollination services decreases with isolation from natural areas despite honey bee visits

Sustainable agricultural landscapes by definition provide high magnitude and stability of ecosystem services, biodiversity and crop productivity. However, few studies have considered landscape effects on the stability of ecosystem services. We tested whether isolation from florally diverse natural and semi-natural areas reduces the spatial and temporal stability of flower-visitor richness and pollination services in crop fields. We synthesised data from 29 studies with contrasting biomes, crop species and pollinator communities. Stability of flower-visitor richness, visitation rate (all insects except honey bees) and fruit set all decreased with distance from natural areas. At 1 km from adjacent natural areas, spatial stability decreased by 25, 16 and 9% for richness, visitation and fruit set, respectively, while temporal stability decreased by 39% for richness and 13% for visitation. Mean richness, visitation and fruit set also decreased with isolation, by 34, 27 and 16% at 1 km respectively. In contrast, honey bee visitation did not change with isolation and represented > 25% of crop visits in 21 studies. Therefore, wild pollinators are relevant for crop productivity and stability even when honey bees are abundant. Policies to preserve and restore natural areas in agricultural landscapes should enhance levels and reliability of pollination services.

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.

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.

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.

Diversity of wild bees in wet meadows: Implications for conservation

Substantial industrial development, agricultural intensification, and an increasing human population have led to the demise of many seminatural habitats, such as wet meadows, in many countries of Europe. This process can cause the extinction and decline of associated insect species. The present paper is the first study analyzing wild bee diversity and abundance patterns in wet meadows. We surveyed bees using pan traps, transect walks, and nest traps in four Molinietum (Poaceae) meadows near Kraków, Poland. During one season, we identified a relatively high γ-diversity of wild bees, consisting of 105 species (13 from the Polish Red List) belonging to 22 genera, which represent almost one-fourth of the Polish bees. The wild bee fauna between sites was not variable, which was indicated by low ß-diversity. We found that nesting preference of bees did not differ between the study area and xerothermic meadows, which suggests that differentiation in bee fauna of wet and dry grasslands is mostly due to food specialization rather than nesting preference. Abundance analysis of the bee community showed that the least abundant species were disproportionately comprised of oligolectic species, indicating that species closely associated to plants of wet meadows are especially threatened. Moreover, using occurrence data we found that 34% of the species belonging to the families Halictidae, Melittidae, and the tribe Nomadini found in wet meadows are considered rare in Poland. Our results highlight an urgent need to perform further investigations and develop specific protection plans for bees not only in Kraków’s Molinietum meadows, but also in wetlands throughout Europe.

Survival, reproduction and population growth of the bee pollinator, Osmia rufa (Hymenoptera: Megachilidae), along gradients of heavy metal pollution

Bees are one of the most important groups of pollinators in the temperate zone. Although heavy metal pollution is recognised to be a problem affecting large parts of the European Union, we currently lack insights into the effects of heavy metals on wild bee survival and reproduction. We investigated the impact of heavy metal pollution on the wild bee Osmia rufa (Hymenoptera: Megachilidae) by comparing their survival, reproduction and population dynamics along two independent gradients of heavy metal pollution, one in Poland and the other in the United Kingdom. We used trap nests to evaluate the response of fitness and survival parameters of O. rufa. To quantify the levels of pollution, we directly measured the heavy metal concentration in provisions collected by O. rufa. We found that with increasing heavy metal concentration, there was a steady decrease in number of brood cells constructed by females and an increase in the proportion of dead offspring. In the most polluted site, there were typically 3–4 cells per female with 50–60% dead offspring, whereas in unpolluted sites there were 8 to 10 cells per female and only 10–30% dead offspring. Moreover, the bee population growth rate (R0) decreased along the heavy metal pollution gradients. In unpolluted sites, R0 was above 1, whereas in contaminated sites, the values tended to be below 1. Our findings reveal a negative relationship between heavy metal pollution and several fitness parameters of the wild bee O. rufa, and highlight a mechanism whereby the detrimental effects of heavy metal pollution may severely impact wild bee communities.

Establishment of a cross-European field site network in the ALARM project for assessing large-scale changes in biodiversity

The field site network (FSN) plays a central role in conducting joint research within all Assessing Large-scale Risks for biodiversity with tested Methods (ALARM) modules and provides a mechanism for integrating research on different topics in ALARM on the same site for measuring multiple impacts on biodiversity. The network covers most European climates and biogeographic regions, from Mediterranean through central European and boreal to subarctic. The project links databases with the European-wide field site network FSN, including geographic information system (GIS)-based information to characterise the test location for ALARM researchers for joint on-site research. Maps are provided in a standardised way and merged with other site-specific information. The application of GIS for these field sites and the information management promotes the use of the FSN for research and to disseminate the results. We conclude that ALARM FSN sites together with other research sites in Europe jointly could be used as a future backbone for research proposals.

Mite species inhabiting commercial bumblebee (Bombus terrestris) nests in Polish greenhouses

Nests of social insects are usually inhabited by various mite species that feed on pollen, other micro-arthropods or are parasitic. Well-known negative effects of worldwide economic importance are caused by mites parasitizing honeybee colonies. Lately, attention has focused on the endoparasitic mite Locustacarus buchneri that has been found in commercial bumblebees. However, little is known of other mites associated with commercial bumblebee nests. Transportation of commercial bumblebee colonies with unwanted residents may introduce foreign mite species to new localities. In this study, we assessed the prevalence and species composition of mites associated with commercial bumblebee nests and determined if the mites are foreign species for Poland and for Europe. The study was conducted on 37 commercial bumblebee nests from two companies (Dutch and Israeli), originating from two greenhouses in southern Poland, and on 20 commercial bumblebee colonies obtained directly from suppliers. The species composition and abundance of mites inhabiting commercial bumblebee nests were determined. Seven mite species from three families were found in nests after greenhouse exploitation. The predominant mite species was Tyrophagus putrescentiae (Acaridae) that was a 100-fold more numerous than representatives of the family Laelapidae (Hypoaspis marginepilosa, H. hyatti, H. bombicolens). Representatives of Parasitidae (Parasitellus fucorum, P. crinitus, P. ignotus) were least numerous. All identified mite species are common throughout Europe, foreign species were not found. Mites were not detected in nests obtained directly from suppliers. We conclude that probably bumblebee nests are invaded by local mite species during greenhouse exploitation.