Fine‐scale spatial genetic structure of common and declining bumble bees across an agricultural landscape

Land‐use changes have threatened populations of many insect pollinators, including bumble bees. Patterns of dispersal and gene flow are key determinants of species' ability to respond to land‐use change, but have been little investigated at a fine scale (<10 km) in bumble bees. Using microsatellite markers, we determined the fine‐scale spatial genetic structure of populations of four common Bombus species (B. terrestris, B. lapidarius, B. pascuorum and B. hortorum) and one declining species (B. ruderatus) in an agricultural landscape in Southern England, UK. The study landscape contained sown flower patches representing agri‐environment options for pollinators. We found that, as expected, the B. ruderatus population was characterized by relatively low heterozygosity, number of alleles and colony density. Across all species, inbreeding was absent or present but weak (F_IS = 0.01–0.02). Using queen genotypes reconstructed from worker sibships and colony locations estimated from the positions of workers within these sibships, we found that significant isolation by distance was absent in B. lapidarius, B. hortorum and B. ruderatus. In B. terrestris and B. pascuorum, it was present but weak; for example, in these two species, expected relatedness of queens founding colonies 1 m apart was 0.02. These results show that bumble bee populations exhibit low levels of spatial genetic structure at fine spatial scales, most likely because of ongoing gene flow via widespread queen dispersal. In addition, the results demonstrate the potential for agri‐environment scheme conservation measures to facilitate fine‐scale gene flow by creating a more even distribution of suitable habitats across landscapes.     

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.     

Spatial and temporal dynamics of the male effective population size in bumblebees (Hymenoptera: Apidae)

Eusociality and male haploidy of bumblebees (Bombus spp.) enhance the deleterious effects of population decline and aggravate the degeneration of population fitness compared to solitary and diploid species. The highly dispersive male sex may be the prime driver to connect otherwise isolated populations. We therefore studied the temporal and spatial structure of the male population of Bombus terrestris (Linnaeus 1758) and Bombus lapidarius (Linnaeus 1758) using microsatellite DNA markers. We found that the majority of the males in a 1000 m2 sampling area originated from colonies located outside of the workers foraging range, which was consistent with the genetic distances among colonies. The analyses of temporal population sub-structure based on both colony detection rate over time and the clustering software STRUCTURE consistently suggested one large and temporally unstructured male population. Our results indicate an extended male flight distance for both species. Though the range of queen dispersal remains to be studied, the effective size (N _e) of bumblebees is increased by extended male mating flight ranges (A _m ) exceeding worker foraging distance by factor 1.66 (A _m  = 69.75 km²) and 1.74 (A _m  = 13.41 km²), B. terrestris and B. lapidarius, respectively. Thus this behaviour may counteract genetic deprivation and its effects. All populations were genetically highly diverse and showed no signs of inbreeding. We discuss the implications of our findings in context of bumblebee population dynamics and conservation. We also highlight the effects and benefits of sampling both workers and males for population genetic studies.     

Bumblebees experience landscapes at different spatial scales: possible implications for coexistence

Coexistence in bumblebee communities has largely been investigated at local spatial scales. However, local resource partitioning does not fully explain the species diversity of bumblebee communities. Theoretical studies provide new evidence that partitioning of space can promote species coexistence, when species interact with their environment at different spatial scales. If bumblebee species possess specific foraging ranges, different spatial resource utilisation patterns might operate as an additional mechanism of coexistence in bumblebee communities. We investigated the effects of the landscape-wide availability of different resources (mass flowering crops and semi-natural habitats) on the local densities of four bumblebee species at 12 spatial scales (landscape sectors with 250–3,000 m radius) to indirectly identify the spatial scales at which the bumblebees perceive their environment. The densities of all bumblebee species were enhanced in landscapes with high proportions of mass flowering crops (mainly oilseed rape). We found the strongest effects for Bombus terrestris agg. and Bombus lapidarius at large spatial scales, implying foraging distances of 3,000 and 2,750 m, respectively. The densities of Bombus pascuorum were most strongly influenced at a medium spatial scale (1,000 m), and of Bombus pratorum (with marginal significance) at a small spatial scale (250 m). The estimated foraging ranges tended to be related to body and colony sizes, indicating that larger species travel over larger distances than smaller species, presumably enabling them to build up larger colonies through a better exploitation of food resources. We conclude that coexistence in bumblebee communities could potentially be mediated by species-specific differences in the spatial resource utilisation patterns, which should be considered in conservation schemes.     

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.     

Evidence for competition between honeybees and bumblebees; effects on bumblebee worker size

Numerous studies suggest that honeybees may compete with native pollinators where introduced as non-native insects. Here we examine evidence for competition between honeybees and four bumblebee species in Scotland, a region that may be within the natural range of honeybees, but where domestication greatly increases the honeybee population. We examined mean thorax widths (a reliable measure of body size) of workers of Bombus pascuorum, B. lucorum, B. lapidarius and B. terrestris at sites with and without honeybees. Workers of all four species were significantly smaller in areas with honeybees. We suggest that reduced worker size is likely to have implications for bumblebee colony success. These results imply that, for conservation purposes, some restrictions should be considered with regard to placing honeybee hives in or near areas where populations of rare bumblebee species persist.     

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.     

Nectar robbing,forager efficiency and seed set: Bumblebees foraging on the self incompatible plant Linaria vulgaris (Scrophulariaceae)

In southern England, Linaria vulgaris (common yellow toadflax) suffers from high rates of nectar robbery by bumblebees. In a wild population of L. vulgaris we found that 96 % of open flowers were robbed. Five species of bumblebee were observed foraging on these flowers, although short-tongued species (Bombus lapidarius, B. lucorum and B. terrestris) robbed nectar whilst longer-tongued ones behaved as legitimate pollinators (B. hortorum and B. pascuorum). Nectar rewards were highly variable; on average there was less nectar in robbed than in unrobbed flowers, but this difference was not statistically significant. The proportion of flowers containing no nectar was significantly higher for robbed flowers compared with unrobbed flowers. Secondary robbers and legitimate pollinators had similar handling times on flowers and, assuming they select flowers at random to forage on, received approximately the same nectar profit per minute, largely because most flowers had been robbed. There was no significant difference in the number of seeds in pods of robbed flowers and in pods of flowers that were artificially protected against robbing. However, more of the robbed flowers set at least some seed than the unrobbed flowers, possibly as a consequence of the experimental manipulation. We suggest that nectar robbing has little effect on plant fecundity because legitimate foragers are present in the population, and that seed predation and seed abortion after fertilization may be more important factors in limiting seed production in this species.     

Bumblebee foraging rhythms under the midnight sun measured with radiofrequency identification

Background  

In the permanent daylight conditions north of the Arctic circle, there is a unique opportunity for bumblebee foragers to maximise intake, and therefore colony growth, by remaining active during the entire available 24-h period. We tested the foraging rhythms of bumblebee (Bombus terrestris and B. pascuorum) colonies in northern Finland during the summer, when the sun stays above the horizon for weeks. We used fully automatic radio-frequency identification to monitor the foraging activity of more than 1,000 workers and analysed their circadian foraging rhythms.     

Effective population size as a driver for divergence of an antimicrobial peptide (Hymenoptaecin) in two common European bumblebee species

Social insects are the target of numerous pathogens. This is because the high density of closely‐related individuals frequently interacting with each other enhances the transmission and establishment of pathogens. This high selective pressure results in the rapid evolution of immune genes, which might be counteracted by a reduced effective population size (N_e) lowering the effectiveness of selection. We tested the effect of N_e on the evolutionary rate of an important immune gene for the antimicrobial peptide Hymenoptaecin in two common central European bumblebee species: Bombus terrestris and Bombus lapidarius. Both species are similar in their biology and are expected to be under similar selective pressures because pathogen prevalence does not differ between species. However, previous studies indicated a higher N_e in B. terrestris compared to B. lapidarius. We found high intraspecific variability in the coding sequence but low variability for silent polymorphisms in B. lapidarius. Estimates of long‐ and short‐term N_e were three‐ to four‐fold higher N_e in B. terrestris, although the species did not differ in census population sizes. The difference in N_e might result in less efficient selection and suboptimal adaptation of immune genes (e.g. hymenoptaecin) in B. lapidarius, and thus this species might become less resistant and more tolerant, turning into a superspreader of diseases.     

Forage use and niche partitioning by non-native bumblebees in New Zealand: implications for the conservation of their populations of origin

Bumblebees were introduced into New Zealand from the UK approximately 120 years ago and four species became established. Two of these, Bombus terrestris and B. hortorum, are common in Europe whilst two, B. ruderatus and B. subterraneus, have experienced declines, and the latter is now extinct in the UK. The presence of these species in New Zealand presents an opportunity to study their ecology in a contrasting environment. Forage visits made by bumblebees in New Zealand were recorded across a season. Ninety-six percent of visits were to six non-native forage plants (Cirsium vulgare, Echium vulgare, Hypericum perforatum, Lotus corniculatus, Lupinus polyphyllus and Trifolium pratense). All but L. polyphyllus are European plant species, and three are noxious weeds in New Zealand. Several of these plants have decreased in abundance in the UK, providing a potential explanation for the declines of B. ruderatus and B. subterraneus in Britain. In contrast to studies conducted elsewhere, B. ruderatus, B. terrestris and B. hortorum did not differ in diet breadth and overlap in forage use was high, probably due to the reduced diversity of bumblebee forage plants present in New Zealand. Diel partitioning of forage use between the species was observed, with foraging activity of B. hortorum greatest in the morning and evening, B. ruderatus greatest in the middle of the day and B. terrestris intermediate between the two. These patterns correspond to the climatic preferences of each species as evidenced by their geographic ranges. Implications for bumblebee conservation in the UK are discussed.     

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.     

Abundance,body size,and morphology of bumblebees in an area where an exotic species, <Emphasis Type="Italic">Bombus terrestris</Emphasis>, has colonized in Japan

An exotic bumblebee species, Bombus terrestris, has colonized in Japan and becomes dominant in some local communities. We examined the effects of land use and bumblebee abundance on the number and body size of bumblebees collected using window traps in a lowland area in the southern Ishikari district, Hokkaido. In 2004, we collected 922 bumblebees of six species using 70 traps at 17 sites. A statistical model fitted to the data demonstrated that dispersion from commercial B. terrestris colonies used in greenhouses positively affected the number of B. terrestris caught by each trap. This exotic species was abundant in sites where paddy fields were prevalent, but three native species, B. hypocrita, B. ardens, and B. diversus, were abundant in sites where farms and woodlands were widespread. The local abundance of B. terrestris was not associated negatively with the number and body size of native bumblebees. Thus, we did not find any competitive interactions between exotic and native bumblebees although habitat conditions seem to be common determinants of the bumblebee populations. A morphological analysis showed that B. terrestris had intermediate tongue length between B. hypocrita and B. ardens.     

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     

Molecular identification of cryptic bumblebee species from degraded samples using PCR–RFLP approach

The worldwide decline and local extinctions of bumblebees have raised a need for fast and accurate tools for species identification. Morphological characters are often not sufficient, and molecular methods have been increasingly used for reliable identification of bumblebee species. Molecular methods often require high‐quality DNA which makes them less suitable for analysis of low‐quality or older samples. We modified the PCR–RFLP protocol for an efficient and cost‐effective identification of four bumblebee species in the subgenus Bombus s. str. (B. lucorum, B. terrestris, B. magnus and B. cryptarum). We used a short partial mitochondrial COI fragment (446 bp) and three diagnostic restriction enzymes (Hinf I, Hinc II and Hae III) to identify species from degraded DNA material. This approach allowed us to efficiently determine the correct species from all degraded DNA samples, while only a subset of samples 64.6% (31 of 48) resulted in successful amplification of a longer COI fragment (1064 bp) using the previously described method. This protocol can be applied for conservation and management of bumblebees within this subgenus and is especially useful for fast species identification from degraded samples.     

The provision of winter bird food by the English Environmental Stewardship scheme

Environmental Stewardship (ES) is the main mechanism for reversing the decline in farmland birds in England, and includes a range of options designed to provide winter foraging for seed‐eating species. We estimated granivorous songbird densities on ES options designed to provide winter food, on farms within the Entry Level (ELS) or Higher Level (HLS) strata of ES. ES Wild Bird Mixtures (WBMs) hosted higher densities and a wider range of granivores than non‐ES game covers, although in East Anglia the enhanced HLS WBM was used no more than the basic ELS WBM. In the West Midlands there were low densities of granivores on all WBMs and game covers. The widespread ELS WBM appeared to provide little food for buntings but supported finches, partially through greater weed burdens. There was a weak, non‐significant trend for Skylarks Alauda arvensis to make greater use of ELS cereal stubbles than non‐ES stubbles, possibly because of post‐harvest herbicide restrictions allowing overwinter weed growth. At the field scale, this work demonstrates that although some ES options provide winter food resources for birds, there is limited evidence for additional benefits of Higher Level vs. Entry Level Stewardship to wintering farmland songbirds.     

Evidence for hilltopping in bumblebees?

1. Male bumblebees are known to exhibit a range of mate‐location behaviours, including perching on prominent objects and darting at passing queens, patrolling of scent‐marked flight routes, and waiting outside nest entrances for virgin queens to emerge. Here we provide evidence for a fourth strategy, known as hilltopping. This behaviour is widely known from a range of invertebrates, but has not previously been described in bumblebees. 2. We studied the distribution of bumblebees along transects ascending four hills in Scotland and demonstrate that, relative to workers, males of four bumblebee species or species groups (Bombus lapidarius, B. monticola, B. pascuorum, and B. lucorum/magnus/cryptarum/terrestris) tend to congregate at or near the tops of hills. This is, to our knowledge, the first evidence for hilltopping in bumblebees and the first record of any putative mate‐locating behaviour for male B. pascuorum, a very common species in Europe. 3. We note that, in common with most previous studies of mate‐locating behaviour in bumblebees, attraction of virgin queens and mating were not observed.     

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     

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.     

Successful pollination of the Neotropical crop Solanum quitoense by Bombus terrestris: behaviour,efficiency and yield

The South American lulo (Solanum quitoense Lam.) is a crop plant of the Andes of Ecuador and Colombia, pollinated by South American bumblebees, such as, Bombus atratus Franklin. The cultivation of lulo outside of its native range, for example in European glasshouses, requires the presence of efficient pollinators to enable high fruit set and yield. Until now, the suitability of Bombus terrestris L., native to Europe and commonly used in agriculture, has been untested for this purpose. In this study, the pollen‐collecting behaviour of B. terrestris when visiting lulo flowers was investigated. It was shown that B. terrestris adopted the lulo as a pollen source, and on average visited three flowers per minute, had five buzzing events per stay and foraged for 15 s on a single flower, independently of the previous number of visits and level of bruising to the anthers. The pollination efficiency of five different treatments was evaluated: (i) exclusion of bees, (ii) single and (iii) multiple visits of B. terrestris, (iv) self‐ and (v) cross‐pollination by hand. The results clearly demonstrated that, for fruit set, pollination is crucial. It was also found that lulo flowers can be successfully self‐pollinated, but give 25% fewer fruit set compared with pollination via multiple bumblebee visits, or cross‐pollination by hand. Fruit set, seed set and fruit size were as high with pollination by B. terrestris as with cross‐pollination by hand, indicating that this bumblebee is an appropriate pollinator for lulo. However, B. terrestris was conspicuously less effective when a flower was visited only once. Therefore, when growing lulos commercially, multiple bumblebee visits should be encouraged, but it is likely that the behaviour of B. terrestris would ensure this anyway. Our results indicate that B. terrestris is a suitable and efficient pollinator for the production of lulo fruits.