The pollination efficiency of a pollinator depends on its foraging strategy,flowering phenology,and the flower characteristics of a plant species

Honey bees and stingless bees are generalist visitors of several wild and cultivated plants. They forage with a high degree of floral fidelity and thereby help in the pollination services of those plants. We hypothesized that pollination efficiency might be influenced by flowering phenology, floral characteristics, and resource collection modes of the worker bees. In this paper, we surveyed the foraging strategies of honey bees (Apis cerana, Apis dorsata, and Apis florea) and stingless bees (Tetragonula iridipennis) concerning their pollination efficiencies. Bees showed different resource gathering strategies, including legitimate (helping in pollination as mixed foragers and specialized foragers) and illegitimate (serving as nectar robbers and pollen thieves) types of flower visitation patterns. Foraging strategies are influenced by the shape of flowers, the timing of the visitation, floral richness, and bee species. Honey bees and stingless bees mainly acted as legitimate visitors in most plants studied. Sometimes honey bees served as nectar robbers in tubular flowers and stingless bees as pollen thieves in large-sized flowers. Among the legitimate categories, mixed foragers have a comparatively lower flower visitation rate than the specialized nectar and pollen foragers. However, mixed foragers have greater abundance and higher values of the single-visit pollination efficiency index (PEi) than nectar and pollen foragers. The value of the combined parameter ‘importance in pollination (PI)’ was thus higher in mixed foragers than in nectar and pollen foragers.     

Bumble bees exhibit daily behavioral patterns in pollen foraging

In response to global declines in bee populations, several studies have focused on floral resource provisioning schemes to support bee communities and maintain their pollination services. Optimizing host-plant selection for supplemental floral provisioning requires an understanding of bee foraging behavior and preferences for host-plant species. However, fully characterizing these preferences is challenging due to multiple factors influencing foraging, including the large degree of spatiotemporal variability in floral resources. To understand bee pollen foraging patterns, we developed a highly controlled mechanistic framework to measure pollen foraging preferences of the bumble bee Bombus impatiens to nine plant species native to Pennsylvania. We recorded continuous observations of foraging behavior of the experimental bee community and individual bees, while simultaneously standardizing for the number of foragers in the environment and differences in floral display of each plant species, while controlling for flowering phenology such that bees only foraged when all plant species’ flowers were open. Our results demonstrate that B. impatiens exhibit predictable daily patterns in their pollen foraging choices, and their preferences are dominated by the host-plants they visit first. We hypothesize that these patterns at the community and individual levels are driven by the interplay between pollen abundance and quality. We recommend that daily cycles of host-plant visitation be considered in future studies to ensure precise and accurate interpretations of host-plant preference. Such precision is critical for comprehensive analyses of the proximate and ultimate mechanisms driving bee foraging behavior and the selection of host-plant species to use in habitat restoration protocols.     

Reduced visitation to buzz‐pollinated Cyanella hyacinthoides in the presence of other pollen sources in the hyperdiverse Cape Floristic Region

Many plant species have floral morphologies that restrict access to floral resources, such as pollen or nectar, and only a subset of floral visitors can perform the handling behaviors required to extract restricted resources. Due to the time and energy required to extract resources from morphologically complex flowers, these plant species potentially compete for pollinators with co‐flowering plants that have more easily accessible resources. A widespread floral mechanism restricting access to pollen is the presence of tubular anthers that open through small pores or slits (poricidal anthers). Some bees have evolved the capacity to remove pollen from poricidal anthers using vibrations, giving rise to the phenomenon of buzz‐pollination. These bee vibrations that are produced for pollen extraction are presumably energetically costly, and to date, few studies have investigated whether buzz‐pollinated flowers may be at a disadvantage when competing for pollinators’ attention with plant species that present unrestricted pollen resources. Here, we studied Cyanella hyacinthoides (Tecophilaeaceae), a geophyte with poricidal anthers in the hyperdiverse Cape Floristic Region of South Africa, to assess how the composition and relative abundance of flowers with easily accessible pollen affect bee visitation to a buzz‐pollinated plant. We found that the number of pollinator species of C. hyacinthoides was not influenced by community composition. However, visitation rates to C. hyacinthoides were reduced when the relative abundances of flowers with more accessible resources were high. Visitation rates were strongly associated with petal color, showing that flower color is important in mediating these interactions. We conclude that buzz‐pollinated plants might be at a competitive disadvantage when many easily accessible pollen sources are available, particularly when competitor species share its floral signals.     

Factors governing flower visitation patterns and quality of pollination services delivered by social and solitary bee species to coffee in central Uganda

In Uganda, information on visitation frequency of pollinator species visiting coffee flowers is absent, although such information is critical for the stability of coffee yield through the enhancement of pollination services. This study was conducted to understand the role played by local and environmental factors on the visitation intensity of coffee flowers by different bee species. Stepwise multiple regressions were used to investigate the effects of light intensity, distance to forest, foraging time of the day, coffee blooming season and abundance of coffee floral resources on the flower visitation frequency of different bee species. Results indicated contrasting responses of different bee species. The most important factors for social bees included forest distance, light intensity and the time of the day, whereas most determinant factors for solitary bee species were the length of the flowering season and the abundance of coffee floral resources. There is a need for developing habitat and landscape management strategies for the conservation of frequent native species in the vicinity of coffee fields to increase the delivery of pollination services to coffee. It is recommended to farmers to grow their coffee farms in the adjacent of forest habitats and related semi‐natural habitats to receive high bee visitations.     

Pollinator Interactions with Yellow Starthistle (Centaurea solstitialis) across Urban,Agricultural, and Natural Landscapes

Pollinator-plant relationships are found to be particularly vulnerable to land use change. Yet despite extensive research in agricultural and natural systems, less attention has focused on these interactions in neighboring urban areas and its impact on pollination services. We investigated pollinator-plant interactions in a peri-urban landscape on the outskirts of the San Francisco Bay Area, California, where urban, agricultural, and natural land use types interface. We made standardized observations of floral visitation and measured seed set of yellow starthistle (Centaurea solstitialis), a common grassland invasive, to test the hypotheses that increasing urbanization decreases 1) rates of bee visitation, 2) viable seed set, and 3) the efficiency of pollination (relationship between bee visitation and seed set). We unexpectedly found that bee visitation was highest in urban and agricultural land use contexts, but in contrast, seed set rates in these human-altered landscapes were lower than in natural sites. An explanation for the discrepancy between floral visitation and seed set is that higher plant diversity in urban and agricultural areas, as a result of more introduced species, decreases pollinator efficiency. If these patterns are consistent across other plant species, the novel plant communities created in these managed landscapes and the generalist bee species that are favored by human-altered environments will reduce pollination services.     

Variation in composition of two bumble bee species across communities affects nectar robbing but maintains pollinator visitation rate to an alpine plant,Salvia przewalskii

1. In many flowering plants, bumble bees may forage as both pollinators and nectar robbers. This mixed foraging behaviour may be influenced by community context and consequently, potentially affect pollination of the focal plant. 2. Salvia przewalskii is both pollinated and robbed exclusively by bumble bees. In the present study area, it was legitimately visited by two species of bumble bees with different tongue length, Bombus friseanus and Bombus religiosus, but it was only robbed by Bombus friseanus, the shorter‐tongued bumble bee. The intensity of nectar robbing and pollinator visitation rate to the plant were investigated across 26 communities in the Hengduan Mountains in East Himalaya during a 2‐year project. For each of these communities, the floral diversity, and the population size and floral resource of S. przewalskii were quantified. The abundances of the two bumble bee species were also recorded. 3. Both nectar robbing and pollinator visitation rate were influenced by floral diversity. However, pollinator visitation rate was not affected by nectar robbing. The results revealed that relative abundance of the two bumble bee species significantly influenced the incidence of nectar robbing but not the pollinator visitation rate. Increased abundance of B. religiosus, the legitimate visitors, exacerbated nectar robbing, possibly by causing B. friseanus to shift to robbing; however, pollinator visitation remained at a relatively high level. 4. The results may help to explain the persistence of both nectar robbing and pollination, and suggest that, in comparison to pollination, nectar robbing is a more unstable event in a community.     

Floral resources,body size,and surrounding landscape influence bee community assemblages in oak‐savannah fragments

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Supporting crop pollinators with floral resources: network‐based phenological matching

The production of diverse and affordable agricultural crop species depends on pollination services provided by bees. Indeed, the proportion of pollinator‐dependent crops is increasing globally. Agriculture relies heavily on the domesticated honeybee; the services provided by this single species are under threat and becoming increasingly costly. Importantly, the free pollination services provided by diverse wild bee communities have been shown to be sufficient for high agricultural yields in some systems. However, stable, functional wild bee communities require floral resources, such as pollen and nectar, throughout their active season, not just when crop species are in flower. To target floral provisioning efforts to conserve and support native and managed bee species, we apply network theoretical methods incorporating plant and pollinator phenologies. Using a two‐year dataset comprising interactions between bees (superfamily Apoidea, Anthophila) and 25 native perennial plant species in floral provisioning habitat, we identify plant and bee species that provide a key and central role to the stability of the structure of this community. We also examine three specific case studies: how provisioning habitat can provide temporally continuous support for honeybees (Apis mellifera) and bumblebees (Bombus impatiens), and how resource supplementation strategies might be designed for a single genus of important orchard pollinators (Osmia). This framework could be used to provide native bee communities with additional, well‐targeted floral resources to ensure that they not only survive, but also thrive.     

Bee Species Diversity Enhances Productivity and Stability in a Perennial Crop

Wild bees provide important pollination services to agroecoystems, but the mechanisms which underlie their contribution to ecosystem functioning—and, therefore, their importance in maintaining and enhancing these services—remain unclear. We evaluated several mechanisms through which wild bees contribute to crop productivity, the stability of pollinator visitation, and the efficiency of individual pollinators in a highly bee-pollination dependent plant, highbush blueberry. We surveyed the bee community (through transect sampling and pan trapping) and measured pollination of both open- and singly-visited flowers. We found that the abundance of managed honey bees, Apis mellifera, and wild-bee richness were equally important in describing resulting open pollination. Wild-bee richness was a better predictor of pollination than wild-bee abundance. We also found evidence suggesting pollinator visitation (and subsequent pollination) are stabilized through the differential response of bee taxa to weather (i.e., response diversity). Variation in the individual visit efficiency of A. mellifera and the southeastern blueberry bee, Habropoda laboriosa, a wild specialist, was not associated with changes in the pollinator community. Our findings add to a growing literature that diverse pollinator communities provide more stable and productive ecosystem services.     

The Potential Influence of Bumble Bee Visitation on Foraging Behaviors and Assemblages of Honey Bees on Squash Flowers in Highland Agricultural Ecosystems

Bee species interactions can benefit plant pollination through synergistic effects and complementary effects, or can be of detriment to plant pollination through competition effects by reducing visitation by effective pollinators. Since specific bee interactions influence the foraging performance of bees on flowers, they also act as drivers to regulate the assemblage of flower visitors. We selected squash (Cucurbita pepo L.) and its pollinators as a model system to study the foraging response of honey bees to the occurrence of bumble bees at two types of sites surrounded by a high amount of natural habitats (≥ 58% of land cover) and a low amount of natural habitats (≤ 12% of land cover) in a highland agricultural ecosystem in China. At the individual level, we measured the elapsed time from the departure of prior pollinator(s) to the arrival of another pollinator, the selection of honey bees for flowers occupied by bumble bees, and the length of time used by honey bees to explore floral resources at the two types of sites. At the community level, we explored the effect of bumble bee visitation on the distribution patterns of honey bees on squash flowers. Conclusively, bumble bee visitation caused an increase in elapsed time before flowers were visited again by a honey bee, a behavioral avoidance by a newly-arriving honey bee to select flowers occupied by bumble bees, and a shortened length of time the honey bee takes to examine and collect floral resources. The number of overall bumble bees on squash flowers was the most important factor explaining the difference in the distribution patterns of honey bees at the community level. Furthermore, decline in the number of overall bumble bees on the squash flowers resulted in an increase in the number of overall honey bees. Therefore, our study suggests that bee interactions provide an opportunity to enhance the resilience of ecosystem pollination services against the decline in pollinator diversity.     

Native bees provide insurance against ongoing honey bee losses

One of the values of biodiversity is that it may provide 'biological insurance' for services currently rendered by domesticated species or technology. We used crop pollination as a model system, and investigated whether the loss of a domesticated pollinator (the honey bee) could be compensated for by native, wild bee species. We measured pollination provided to watermelon crops at 23 farms in New Jersey and Pennsylvania, USA, and used a simulation model to separate the pollen provided by honey bees and native bees. Simulation results predict that native bees alone provide sufficient pollination at > 90% of the farms studied. Furthermore, empirical total pollen deposition at flowers was strongly, significantly correlated with native bee visitation but not with honey bee visitation. The honey bee is currently undergoing extensive die-offs because of Colony Collapse Disorder. We predict that in our region native bees will buffer potential declines in agricultural production because of honey bee losses.     

Effects of grazing intensity on pollinator abundance and diversity,and on pollination services

1. Pollinating insects provide important ecosystem services and are influenced by the intensity of grazing. Based on the Intermediate Disturbance Hypothesis (IDH), pollinator diversity is expected to peak at intermediate grazing intensities. However, this hump‐shaped relationship is rarely found. 2. The effect of grazing intensity was tested on flower cover, on the abundance and richness of bees, hoverflies and bee flies, and on pollination services to early‐flowering bee‐pollinated Asphodelus ramosus L. For that, we used data on 11 plant–pollinator phryganic communities from Lesvos Island (Greece) widely differing in grazing intensities. 3. Flower abundance and richness showed hump‐shaped relationships with grazing intensity. Grazing affected the abundance and richness of bees and hoverflies directly and also indirectly, through changes in the flower community. Grazing influenced directly the richness but not the abundance of bee flies. Overall, pollinator abundance and richness showed hump‐shaped relationships with grazing intensity, but variations in strength (hoverfly abundance) and direction (bee community) of the effect appeared along the season. Early in the season, grazing increased bee abundance but decreased richness, resulting in increased pollen limitation in A. ramosus. 4. The effects of grazing on pollinators vary with the intensity of the disturbance, generally supporting the IDH, and the timing of land‐use activities may influence pollination services. Management strategies should include moderate grazing levels to preserve overall diversity in this area, however, the conservation of particular early bee or bee‐pollinated species may benefit from reduced grazing in early spring.     

Diverse pollinator communities enhance plant reproductive success

Understanding the functional consequences of biodiversity loss is a major goal of ecology. Animal-mediated pollination is an essential ecosystem function and service provided to mankind. However, little is known how pollinator diversity could affect pollination services. Using a substitutive design, we experimentally manipulated functional group (FG) and species richness of pollinator communities to investigate their consequences on the reproductive success of an obligate out-crossing model plant species, Raphanus sativus. Both fruit and seed set increased with pollinator FG richness. Furthermore, seed set increased with species richness in pollinator communities composed of a single FG. However, in multiple-FG communities, highest species richness resulted in slightly reduced pollination services compared with intermediate species richness. Our analysis indicates that the presence of social bees, which showed roughly four times higher visitation rates than solitary bees or hoverflies, was an important factor contributing to the positive pollinator diversity–pollination service relationship, in particular, for fruit set. Visitation rate at different daytimes, and less so among flower heights, varied among social bees, solitary bees and hoverflies, indicating a niche complementarity among these pollinator groups. Our study demonstrates enhanced pollination services of diverse pollinator communities at the plant population level and suggests that both the niche complementarity and the presence of specific taxa in a pollinator community drive this positive relationship.     

Bombus terrestris in a mass‐flowering pollinator‐dependent crop: A mutualistic relationship?

Bumblebees (Bombus spp.) rely on an abundant and diverse selection of floral resources to meet their nutritional requirements. In farmed landscapes, mass‐flowering crops can provide an important forage resource for bumblebees, with increased visitation from bumblebees into mass‐flowering crops having an additional benefit to growers who require pollination services. This study explores the mutualistic relationship between Bombus terrestris L. (buff‐tailed bumblebee), a common species in European farmland, and the mass‐flowering crop courgette (Cucurbita pepo L.) to see how effective B. terrestris is at pollinating courgette and in return how courgette may affect B. terrestris colony dynamics. By combining empirical data on nectar and pollen availability with model simulations using the novel bumblebee model Bumble‐BEEHAVE, we were able to quantify and simulate for the first time, the importance of courgette as a mass‐flowering forage resource for bumblebees. Courgette provides vast quantities of nectar to ensure a high visitation rate, which combined with abundant pollen grains, enables B. terrestris to have a high pollination potential. While B. terrestris showed a strong fidelity to courgette flowers for nectar, courgette pollen was not found in any pollen loads from returning foragers. Nonetheless, model simulations showed that early season courgette (nectar) increased the number of hibernating queens, colonies, and adult workers in the modeled landscapes. Synthesis and applications. Courgette has the potential to improve bumblebee population dynamics; however, the lack of evidence of the bees collecting courgette pollen in this study suggests that bees can only benefit from this transient nectar source if alternative floral resources, particularly pollen, are also available to fulfill bees’ nutritional requirements in space and time. Therefore, providing additional forage resources could simultaneously improve pollination services and bumblebee populations.     

The evolution of floral sonication,a pollen foraging behavior used by bees (Anthophila)

Over 22,000 species of biotically pollinated flowering plants, including some major agricultural crops, depend primarily on bees capable of floral sonication for pollination services. The ability to sonicate (“buzz”) flowers is widespread in bees but not ubiquitous. Despite the prevalence of this pollinator behavior and its importance to natural and agricultural systems, the evolutionary history of floral sonication in bees has not been previously studied. Here, we reconstruct the evolutionary history of floral sonication in bees by generating a time‐calibrated phylogeny and reconstructing ancestral states for this pollen extraction behavior. We also test the hypothesis that the ability to sonicate flowers and thereby efficiently access pollen from a diverse assemblage of plant species, led to increased diversification among sonicating bee taxa. We find that floral sonication evolved on average 45 times within bees, possibly first during the Early Cretaceous (100–145 million years ago) in the common ancestor of bees. We find that sonicating lineages are significantly more species rich than nonsonicating sister lineages when comparing sister clades, but a probabilistic structured rate permutation on phylogenies approach failed to support the hypothesis that floral sonication is a key driver of bee diversification. This study provides the evolutionary framework needed to further study how floral sonication by bees may have facilitated the spread and common evolution of angiosperm species with poricidal floral morphology.     

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.     

Pollination and seed set of an obligatory outcrossing plant in an urban–peri-urban gradient

Urban land use strongly affects pollinators and plant pollination due to fragmentation and isolation of natural plant populations. On the other hand, urban land use can potentially be beneficial to pollinators through the presence of urban gardens and parks which are usually designed to ensure abundant flowering. However, little is known about the effects of urban land use on bees and the pollination services they provide. In an urban–peri-urban gradient around Leuven, Belgium we studied flower visitation rates to, and seed set of Trifolium repens (white clover) in public lawns. T. repens is an obligatory outcrossing plant and is therefore sensitive to reductions in pollinator services. We related our results to both local and regional variables using Boosted Regression Trees. The two variables that best explained the variability in visitation rates and seed set were the amount of green areas (gardens, parks, grasslands) in the surroundings and the abundance of T. repens in the lawns. Surprisingly, an increasing amount of green areas in the surroundings had a negative effect on both flower visitation rates to, and seed set of T. repens. Flower visitation rates by bumblebees responded positively to urban land use resulting in higher visitation rates and increased seed set in the more urban sites. This may point either to increased abundance of bumblebees in more urban sites or to a concentration effect of bumblebees in our urban study sites due to a lack of alternative forage resources. Responses will likely differ for other bee and plant species, but this shows that at least for T. repens, pollination is not compromised by urban land use.     

Negative effects of urbanisation on diurnal and nocturnal pollen-transport networks

Pollinating insects are declining due to habitat loss and climate change, and cities with limited habitat and floral resources may be particularly vulnerable. The effects of urban landscapes on pollination networks remain poorly understood, and comparative studies of taxa with divergent niches are lacking. Here, for the first time, we simultaneously compare nocturnal moth and diurnal bee pollen-transport networks using DNA metabarcoding and ask how pollination networks are affected by increasing urbanisation. Bees and moths exhibited substantial divergence in the communities of plants they interact with. Increasing urbanisation had comparable negative effects on pollen-transport networks of both taxa, with significant declines in pollen species richness. We show that moths are an important, but overlooked, component of urban pollen-transport networks for wild flowering plants, horticultural crops, and trees. Our findings highlight the need to include both bee and non-bee taxa when assessing the status of critical plant-insect interactions in urbanised landscapes.     

Contrasting responses of bee communities to coffee flowering at different spatial scales

While investigating biodiversity patterns on different spatial scales, ecological processes determining these patterns have been rarely analysed. Flower visitation by bees is an important ecological process that is related to floral resource availability. However, little is known about whether responses of bee communities to floral resource availability change at different spatial scales. We studied density and species richness of flower-visiting bees in relation to floral resource availability, provided by coffee, in traditional agroforestry systems on a field, shrub, and branch scale. On a field scale, mean bee density per shrub increased with decreasing proportion of flowering coffee shrubs per site, showing a dilution effect. Conversely, on shrub and branch scales bee density per shrub, or shrub part, increased with increasing number of inflorescences, showing a concentration effect. Additionally, bee density per shrub was higher on those that were only partly, rather than totally surrounded by other flowering coffee shrubs. Species richness of flower-visiting bees was positively affected by high resource availability on a shrub and a branch scale, expressed by a high number of inflorescences, but at the field scale the proportion of flowering shrubs per site did not have any effect on species richness. Our results show contrasting responses of the community of flower-visiting bees to floral resource availability, depending on the spatial scale considered. We conclude that patterns of flower-visiting bee communities of only one spatial scale can not be generalized, since the number of pollinators may be limited on a field scale, but not on smaller scales.     

Proximity to wildflower strips did not boost crop pollination on small,diversified farms harboring diverse wild bees

The yield of many agricultural crops depends on pollination services provided by wild and managed bees, many of which are experiencing declines due to factors such as reductions in floral resources. Thus, improving pollinator habitat on farmlands using management strategies like planting wildflower strips is vital for wild bee conservation and sustainable crop pollination. Yet, few studies have examined whether and at what spatial scales wildflower strips enhance crop pollination and yields, and most research has been conducted in large-scale commercial agriculture. Therefore, we investigated the effects of wildflower strips on crop pollination on small, diversified farms (i.e., those growing a variety of crop species) where wild bee diversity and abundance is predicted to be comparatively high. Over three years, on four diversified farms in Montana USA, we tested the hypothesis that distance (20, 60, and 180 m) of crops from native perennial wildflower strips planted alongside crop fields affected wild bee visitation, pollination, and yields of squash and sunflower crop plants. We found that distance to wildflower strips did not affect bee visitation or pollination in crops. Squash yield was pollen-limited in the growing season prior to wildflower strip establishment, and in one of the two years after wildflower strip establishment, but proximity to wildflower strips did not influence the magnitude of pollen limitation. Sunflower seed production was not pollen-limited in any year. Our findings demonstrate that even on diverse farms with wildflower strips and a demonstrated high diversity of bees, some crops do not necessarily receive maximum pollination, regardless of distance from the wildflower strips. However, the value of wildflower strips for supporting wild bee diversity, and other ecological or economic benefits, needs consideration for a full understanding of this pollinator habitat management strategy.