Foraging habitats and foraging distances of bumblebees, Bombus spp. (Hym., Apidae), in an agricultural landscape

Abstract: In selected foraging habitats of an agricultural landscape flower visits of bumblebees and community structure of foraging bumblebees were studied, with special regard to the role of crops as super-abundant resources. Most crops represent temporal foraging habitats with high abundance of bumblebees but mainly with low diversity in the bumblebee forage community, in contrast to permanent foraging habitats such as, for example, a hedgerow. The high numbers of bumblebees in the monoculture of crop plantations consisted mainly of short-tongued bumblebee species. The role of foraging distances for the visitation rate of foraging habitats was studied by performing capture–recapture experiments with natural nests of Bombus terrestris , Bombus lapidarius and Bombus muscorum . Differences were found on the species as well as the individual level. The foraging distances of B. muscorum were more restricted to the neighbourhood of the nesting habitat than the foraging activity of B. terrestris and B. lapidarius . High percentages of B. terrestris workers were recaptured while foraging on super-abundant resources in distances up to 1750 m from the nest. Isolated patches of highly rewarding forage crops, in agricultural landscapes, are probably only accessed by bumblebee species with large mean foraging distances, such as the short-tongued B. terrestris . Species like the rare, long-tongued B. muscorum depend on a close connection between nesting and foraging habitat. A restricted foraging radius might be one important factor of bumblebee species loss and potential pollinator limitation in modern agricultural landscapes. Furthermore, long-distance flights of bumblebee pollinators have to be considered in the present discussion on gene flow from transgenic plant species on a landscape scale.     

Morphological variation in relation to flower use in bumblebees

To understand resource partitioning in a bumblebee community, we analyzed various morphological characters. A total of 1269 individuals of six bumblebee species, Bombus ardens, B. hypocrita, B. diversus, B. ignitus, B. honshuensis and B. beaticola, were examined and principal component analysis showed that the bumblebee species were clearly differentiated. Glossa, prementa and head lengths were positively correlated with the second component, and a longer proboscis was associated with a narrower body, which may help bees to intrude into and access deep‐lying nectar sources. Bombus diversus, with a long proboscis and narrow body, preferred flowers with a long corolla tube, whereas B. hypocrita and B. ignitus, which have short proboscises and wide bodies, visited flowers with short corollas or dish‐shaped flowers. Two pairs of consubgeneric species that have similar morphological characteristics, B. ardens and B. beaticola, and B. hypocrita and B. ignitus, divided flower resources by habitat selection and seasonal partitioning. For resource partitioning among bumblebee species, not only morphology but also other factors, such as habitat and seasonal preference, flower use, foraging behavior, and interspecific interactions, are responsible.     

Molecular and spatial analyses reveal links between colony‐specific foraging distance and landscape‐level resource availability in two bumblebee species

Foraging distance is a key determinant of colony survival and pollination potential in bumblebees Bombus spp. However this aspect of bumblebee ecology is poorly understood because of the difficulty in locating colonies of these central place foragers. Here, we used a combination of molecular microsatellite analyses, remote sensing and spatial analyses using kernel density estimates to estimate nest location and foraging distances for a large number of wild colonies of two species, and related these to the distribution of foraging habitats across an experimentally manipulated landscape. Mean foraging distances were 755 m for Bombus lapidarius and 775 m for B. pascuorum (using our most conservative estimation method). Colony‐specific foraging distances of both species varied with landscape structure, decreasing as the proportion of foraging habitats increased. This is the first time that foraging distance in wild bumblebees has been shown to vary with resource availability. Our method offers a means of estimating foraging distances in social insects, and informs the scale of management required to conserve bumblebee populations and enhance their pollination services across different landscapes.     

Mass flowering crops enhance pollinator densities at a landscape scale

To counteract the decline of pollinators in Europe, conservation strategies traditionally focus on enhancing the local availability of semi‐natural habitats, as supported by the European Union's Common Agriculture Policy. In contrast, we show that densities of bumblebees, an important pollinator group in agroecosystems, were not determined by the proportion of semi‐natural habitats in agricultural landscapes. Instead, bumblebee densities were positively related to the availability of highly rewarding mass flowering crops (i.e. oilseed rape) in the landscape. In addition, mass flowering crops were only effective determinants of bumblebee densities when grown extensively at the landscape scale, but not at smaller local scales. Therefore, future conservation measures should consider the importance of mass flowering crops and the need for management schemes at landscape level to sustain vital pollination services in agroecosystems.     

Relationships between densities of previous and simultaneous foragers and the foraging behaviour of three bumblebee species

1. The local insect composition may be as important as the local floral composition for bumblebees' foraging behaviour. However, little is known about how the local abundance of insects affects the foraging patterns of individuals. 2. Using field observations, we studied the relationships between the local density of previous and simultaneous foragers and the local foraging behaviour of Bombus pascuorum, Bombus lucorum/B. terrestris and Bombus lapidarius while pollinating Centaurea jacea. 3. The number of bumblebees foraging in the plots was positively related to the number of new individuals arriving at these plots. The number of inflorescences contacted and the duration of visits were negatively related to the number of simultaneous foragers, but only in B. lucorum/B. terrestris. The effects of previous foragers on the behaviour of other bumblebees were species‐specific and variable in their direction. Such contrasting effects can be explained in terms of bumblebee species' abundances and functional similarity. In some cases, the effect of previous foragers increased with Centaurea density. 4. The local abundance of previous and simultaneous foragers affected the foraging behaviour of particular bumblebee individuals in complex ways. Future studies on local foraging behaviour might benefit from including the abundance of co‐foragers.     

The first record of the rare oligolectic bumblebee Bombus gerstaeckeri Morawitz (Hymenoptera: Apidae: Bombini) lrom Ukraine

The oligolectic bumblebee Bombus gerstaeckeri Morawitz has been recorded in the Ukrainian Carpathians for the first time during field research from 2002 to 2007. Queens and workers of the species have been observed foraging on two Aconitum spp. within 540 m and 1400 m altitude. The additional forage resource of this species, that is Salvia glutinosa L., has been recorded at low height. Three competitor bumblebees, not confined only to Aconitum spp. have been observed foraging on monkshoods: B. hortorum (L.), B. pascuorum (Scopoli) and B. wurflenii Radoszkowski.     

Targeted agri‐environment schemes significantly improve the population size of common farmland bumblebee species

Changes in agricultural practice across Europe and North America have been associated with range contractions and local extinction of bumblebees (Bombus spp.). A number of agri‐environment schemes have been implemented to halt and reverse these declines, predominantly revolving around the provision of additional forage plants. Although it has been demonstrated that these schemes can attract substantial numbers of foraging bumblebees, it remains unclear to what extent they actually increase bumblebee populations. We used standardized transect walks and molecular techniques to compare the size of bumblebee populations between Higher Level Stewardship (HLS) farms implementing pollinator‐friendly schemes and Entry Level Stewardship (ELS) control farms. Bumblebee abundance on the transect walks was significantly higher on HLS farms than ELS farms. Molecular analysis suggested maximum foraging ranges of 566 m for Bombus hortorum, 714 m for B. lapidarius, 363 m for B. pascuorum and 799 m for B. terrestris. Substantial differences in maximum foraging range were found within bumblebee species between farm types. Accounting for foraging range differences, B. hortorum (47 vs 13 nests/km²) and B. lapidarius (45 vs 22 nests/km²) were found to nest at significantly greater densities on HLS farms than ELS farms. There were no significant differences between farm type for B. terrestris (88 vs 38 nests/km²) and B. pascuorum (32 vs 39 nests/km²). Across all bumblebee species, HLS management had a significantly positive effect on bumblebee nest density. These results show that targeted agri‐environment schemes that increase the availability of suitable forage can significantly increase the size of wild bumblebee populations.     

An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species

Bumblebees are major pollinators of crops and wildflowers in northern temperate regions. Knowledge of their ecology is vital for the design of effective management and conservation strategies but key aspects remain poorly understood. Here we employed microsatellite markers to estimate and compare foraging range and nest density among four UK species: Bombus terrestris, Bombus pascuorum, Bombus lapidarius, and Bombus pratorum. Workers were sampled along a 1.5-km linear transect across arable farmland. Eight or nine polymorphic microsatellite markers were then used to identify putative sisters. In accordance with previous studies, minimum estimated maximum foraging range was greatest for B. terrestris (758 m) and least for B. pascuorum (449 m). The estimate for B. lapidarius was similar to B. pascuorum (450 m), while that of B. pratorum was intermediate (674 m). Since the area of forage available to bees increases as the square of foraging range, these differences correspond to a threefold variation in the area used by bumblebee nests of different species. Possible explanations for these differences are discussed. Estimates for nest density at the times of sampling were 29, 68, 117, and 26/km2 for B. terrestris, B. pascuorum, B. lapidarius and B. pratorum, respectively. These data suggest that even among the most common British bumblebee species, significant differences in fundamental aspects of their ecology exist, a finding that should be reflected in management and conservation strategies.     

The influence of relative plant density and floral morphological complexity on the behaviour of bumblebees

We assessed the combined effects of varying the relative density and the relative floral morphological complexity of plant species on the behaviour of their bumblebee pollinators. Three species of bumblebee (Bombus pascuorum, B. terrestris and B. hortorum) were observed foraging on experimental arrays consisting of pair-wise combinations of four plant species: Borago officinalis, Phacelia tanacetifolia (both with simple flowers), Antirrhinum majus and Linaria vulgaris (both with complex flowers). Plant arrangements consisted of either two simple-flower species, a simple with a complex species or two complex species. The number of plants in each array was constant, while the frequency of each species was manipulated so that it was either rare, equal or common compared with its competitor. Contrary to predictions, rare plants were actually at an advantage in terms of the number of bees attracted per plant. However, rare plants were at a disadvantage in terms of pollen wastage because foragers more often went to a flower of another species after visiting a rare plant. The behaviour of bees on each plant species was further affected by plant floral complexity and the identity of the other species in the array. The three bumblebee species were markedly different in their foraging behaviour and in their responses to varying floral density and complexity. Each species preferred particular flower species. The results are discussed with reference to resource partitioning among bumblebee species. Received: 29 July 1998 / Accepted: 5 October 1998     

Filtering across Spatial Scales: Phylogeny,Biogeography and Community Structure in Bumble Bees

Despite the expansion of phylogenetic community analysis to understand community assembly, few studies have used these methods on mobile organisms and it has been suggested the local scales that are typically considered may be too small to represent the community as perceived by organisms with high mobility. Mobility is believed to allow species to mediate competitive interactions quickly and thus highly mobile species may appear randomly assembled in local communities. At larger scales, however, biogeographical processes could cause communities to be either phylogenetically clustered or even. Using phylogenetic community analysis we examined patterns of relatedness and trait similarity in communities of bumble bees (Bombus) across spatial scales comparing: local communities to regional pools, regional communities to continental pools and the continental community to a global species pool. Species composition and data on tongue lengths, a key foraging trait, were used to test patterns of relatedness and trait similarity across scales. Although expected to exhibit limiting similarity, local communities were clustered both phenotypically and phylogenetically. Larger spatial scales were also found to have more phylogenetic clustering but less trait clustering. While patterns of relatedness in mobile species have previously been suggested to exhibit less structure in local communities and to be less clustered than immobile species, we suggest that mobility may actually allow communities to have more similar species that can simply limit direct competition through mobility.     

Spatial and temporal variations in floral resource availability affect bumblebee communities in heathlands

Modifications of landscape structure and composition can decrease the availability of floral resources, resulting in the decline of many pollinator species, including bumblebees. These declines may have significant ecological consequences, because bumblebees pollinate a large range of plant species. Our study was carried out in heathlands, open semi-natural habitats that have decreased considerably due to human activities. We analysed how floral resources affect bumblebee communities throughout the colony lifetime at three scales: plot scale, heathland patch scale, and landscape scale. Floral density at the plot scale and spruce plantations at the landscape scale influenced bumblebee communities. The abundance of bumblebees on ericaceous species was higher when the landscape included a substantial proportion of unsuitable foraging habitat (i.e., spruce plantations). Both life history traits and colony life cycle stage influenced bumblebee responses to the availability of floral resources. Bumblebees were more affected by floral resources during the colony development phase than during the nest-foundation or mating phases. Moreover, bumblebees of species that form large colonies needed larger quantities of favourable foraging habitat, compared with small-colony bees, and their proportion decreased in habitats dominated by spruce plantations. In conclusion, the conservation of plant–bumblebee interactions will require management at a larger spatial scale than the restricted protected habitats. Moreover, at the landscape scale, both quantity of favourable foraging patches and their ecological continuity are important to conserve both small- and large- colony species.     

Niche partitioning at multiple scales facilitates coexistence among mosquito larvae

A theoretical dichotomy in community ecology distinguishes between mechanisms that stabilize species coexistence and those that cause neutral drift. Stable coexistence is predicted to occur in communities where competing species have niche-partitioning mechanisms that reduce interspecific competition. Neutral communities are predicted to be structured by stochastic processes that are not influenced by species identity, but that may be influenced by priority effects and dispersal limitation. Recent developments have suggested that neutral interactions may be more common at local scales, while niche structuring may be more common at larger scales. We tested for mechanisms that could promote either stable coexistence or neutral drift in a bromeliad-dwelling mosquito community by evaluating A) if a hypothesized within-bromeliad niche partitioning mechanism occurs in the community, B) if this mechanism correlates with local species co-occurrence patterns, and C) if patterns of coexistence at the larger (metacommunity) scale were consistent with those at the local scale. We found that mosquitoes in this community do partition space within containers, and that species with the strongest potential for competition co-occurred least. Species with overlapping spatial niches minimized co-occurrence by specialising in bromeliads of differing sizes, effectively changing the scale at which they coexist. In contrast, we found no evidence to support neutral dynamics in mosquito communities at either scale. In this community, a niche-based mechanism that is predicted to stabilize species coexistence explains co-occurrence patterns within and among bromeliads.     

Distribution and flower visitation records of bumblebees in Lebanon (Hymenoptera: Apidae)

Summary

West Palearctic bumblebees are common wildflowers and crop pollinators that are well studied in their central and northern distribution ranges, but fewer information is available on their southern distribution areas. Lebanon falls on the southern limit of their distribution and no published information is available on the local bumblebees. Our study aims to produce a data baseline of the local bumblebee species. In order to do so we grouped available old records of bumblebees in Lebanon with recent author collections and produced preliminary distribution maps. We listed four species: Bombus terrestris, B. argillaceus, B. niveatus vorticosus and B. melanurus. Preliminary distribution shows that Bombus terrestris and B. argillaceus are widespread and have a large foraging range, whereas B. niveatus vorticosus and B. melanurus have a restricted distribution to altitudes above 1800 m with a smaller foraging range. The male cephalic labial gland secretions analysis of local Bombus terrestris specimens provides preliminary evidence that the local subspecies could be Bombus terrestris calabricus. Therefore, we highlight the importance of regulating foreign Bombus terrestris subspecies importation for agriculture purposes, as well as monitoring B. niveatus vorticosus and B. melanurus that are rendered vulnerable by their isolated populations.     

Resource partitioning facilitates coexistence in sympatric cetaceans in the California Current

Resource partitioning is an important process driving habitat use and foraging strategies in sympatric species that potentially compete. Differences in foraging behavior are hypothesized to contribute to species coexistence by facilitating resource partitioning, but little is known on the multiple mechanisms for partitioning that may occur simultaneously. Studies are further limited in the marine environment, where the spatial and temporal distribution of resources is highly dynamic and subsequently difficult to quantify. We investigated potential pathways by which foraging behavior may facilitate resource partitioning in two of the largest co‐occurring and closely related species on Earth, blue (Balaenoptera musculus) and humpback (Megaptera novaeangliae) whales. We integrated multiple long‐term datasets (line‐transect surveys, whale‐watching records, net sampling, stable isotope analysis, and remote‐sensing of oceanographic parameters) to compare the diet, phenology, and distribution of the two species during their foraging periods in the highly productive waters of Monterey Bay, California, USA within the California Current Ecosystem. Our long‐term study reveals that blue and humpback whales likely facilitate sympatry by partitioning their foraging along three axes: trophic, temporal, and spatial. Blue whales were specialists foraging on krill, predictably targeting a seasonal peak in krill abundance, were present in the bay for an average of 4.7 months, and were spatially restricted at the continental shelf break. In contrast, humpback whales were generalists apparently feeding on a mixed diet of krill and fishes depending on relative abundances, were present in the bay for a more extended period (average of 6.6 months), and had a broader spatial distribution at the shelf break and inshore. Ultimately, competition for common resources can lead to behavioral, morphological, and physiological character displacement between sympatric species. Understanding the mechanisms for species coexistence is both fundamental to maintaining biodiverse ecosystems, and provides insight into the evolutionary drivers of morphological differences in closely related species.     

The Value of Uncropped Field Margins For Foraging Bumblebees

The intensification of agriculture has led to declines in species diversity and abundance within groups of certain flora and fauna. Bumblebees (Bombus spp.) are one group where a decline has been documented, and it is thought to be attributable to a decrease in forage resources and potential nest sites. As bumblebees play an important role in the pollination of many entomophilous crops, this decline could impact on agricultural productivity. We examined the role of naturally regenerated field margins in providing forage plants on land where nectar resources are otherwise impoverished. The following question was addressed – Are naturally regenerated unsprayed field margins more attractive to foraging bumblebees and honeybees than cropped field margins managed as conservation headlands? Significantly more bees visited naturally regenerated field margins than cropped field margins. Honeybees (Apis mellifera), Bombus terrestris, and Bombus lapidarius were the most commonly observed bee species. Different wildflower species within the naturally regenerated margins varied greatly in relative number of visits received, and bumblebee species were found to prefer different flower species to honeybees. The potential role that naturally regenerated field margins could play in the conservation of bumblebee species, and the implications for other species of flora and fauna, are discussed.     

Genetic diversity and mass resources promote colony size and forager densities of a social bee (Bombus pascuorum) in agricultural landscapes

Although habitat fragmentation and agricultural intensification are known as threads to pollinator diversity, little is known about consequences for population size and genetic diversity. Here, we combined detailed field observations, molecular approaches and GIS-based quantification of landscape structure (measured by proportions of seminatural habitats and proportions of mass flowering crops) to get new insights into driving forces of population dynamics of the bumblebee species Bombus pascuorum. Comparing 13 agriculturally dominated landscape sectors, we found the proportion of mass flowering crops to positively influence bumblebee abundance whereas the proportion of seminatural habitats was of minor importance. We used microsatellites to quantify landscape-related colony densities, inbreeding and population substructure. Detected colony densities did not correlate with landscape parameters or with local worker abundance, measured by field observations. These results indicate that increased worker abundances within landscapes are rather due to greater colony sizes than due to an increased number of nests. We found significant population substructure, measured by F(ST) and seven landscape sectors to bear significantly increased inbreeding values (F(IS)). F(IS) was strongly varying between sectors but did not correlate with landscape structure. Moreover, F(IS) had a significantly negative effect on colony size, demonstrating the importance of genetic diversity on population fitness at a landscape scale. We suggest that inbreeding levels might be related to the temporal variation of food resources and population sizes in agricultural landscapes.     

Effects of three flower field types on bumblebees and their pollen diets

Agri-environment schemes, like flower fields, have been implemented in the EU to counteract the dramatic decline of farmland biodiversity. Farmers in Lower Saxony, Germany, may receive payments for three flower field types: annual, perennial (five years old), and mixed flower fields composed of yearly alternating annual and biannual parts. We assessed the effectiveness of these flower field types in providing bumblebee foraging habitat compared to control cereal fields. We sampled bumblebees with transect walks and assessed the richness of exploited pollen plants using DNA meta-barcoding and direct observations.All flower field types enhanced bumblebee abundance and species richness compared to control fields but attracted mostly three generalist species. Although we expected highest benefits from the more heterogeneous mixed flower fields, abundance was highest in annual, only intermediate in mixed, and lowest in perennial flower fields. Bumblebee species richness did not differ between flower field types.Overall, the proportion of sown plants in pollen loads was surprisingly low (< 50%). Bombus pascuorum, but not B. terrestris agg., exploited 10% of the sown plant species in perennial, 36% in annual and 45% in mixed flower fields, respectively. Compared to direct observations, pollen samples revealed 4.5 times more visited plant species and thus assessed floral resource use more reliably. Plant species richness in pollen loads decreased with local flowering plant species richness and increased with proportion of annual crops in the landscape, potentially due to the exploitation of more diverse and scattered resources, including flowering crops, in homogenized landscapes to fulfil dietary requirements.Our results indicate that under the current management, both annual and mixed flower fields provide the most attractive food resources, while perennial flower fields offered the poorest foraging habitats. Conclusively, flower fields seem important but resources from the surrounding landscape are still needed to sustain bumblebees in agricultural landscapes.     

Estimation of bumblebee queen dispersal distances using sibship reconstruction method

Dispersal ability is a key determinant of the propensity of an organism to cope with habitat fragmentation and climate change. Here we quantify queen dispersal in two common bumblebee species in an arable landscape. Dispersal was measured by taking DNA samples from workers in the spring and summer, and from queens in the following spring, at 14 sites across a landscape. The queens captured in the spring must be full sisters of workers that were foraging in the previous year. A range of sibship reconstruction methods were compared using simulated data sets including or no genotyping errors. The program Colony gave the most accurate reconstruction and was used for our analysis of queen dispersal. Comparison of queen dispersion with worker foraging distances was used to take into account an expected low level of false identification of sister pairs which might otherwise lead to overestimates of dispersal. Our data show that Bombus pascuorum and B. lapidarius queens can disperse by at least 3 and 5 km, respectively. These estimates are consistent with inferences drawn from studies of population structuring in common and rare bumblebee species, and suggest that regular gene flow over several kilometres due to queen dispersal are likely to be sufficient to maintain genetic cohesion of ubiquitous species over large spatial scales whereas rare bumblebee species appear unable to regularly disperse over distances greater than 10 km. Our results have clear implications for conservation strategies for this important pollinator group, particularly when attempting to conserve fragmented populations.     

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.     

Foraging interactions between native and exotic bumblebees: enclosure experiments using native flowering plants

To assess the impact of Bombus terrestris invasion on the foraging efficiency of native Japanese bumblebees, consumption and acquisition of floral resources during foraging on flowers of native Japanese plant species were investigated using enclosures with three treatments: one with only B. terrestris (exotic), one with both B. terrestris and native Japanese bumblebee species (mixed), and one with only Japanese species (native), but with the bumblebee density held constant. Changes in the body mass of queens and the nest mass of colonies for two days did not significantly differ among four combinations of the species and treatment, B. terrestris in the exotic and mixed treatments and Japanese species in the mixed and native treatments. Thus, it is not clear that B. terrestris has higher foraging efficiency than native species and that B. terrestris individuals more negatively affect the foraging efficiency of native species than individuals of the native species themselves. The nectar standing crop of Cirsium kamtschaticum was smaller in the exotic treatment than in the mixed and native treatments. However, this may have been an artifact of differences in the numbers of flowers in the various treatments. T. Nagamitsu and T. Kenta contributed equally to this work