Short-tongued Bumblebees Research Articles

Crop and landscape factors affecting variation in composition and behaviour of the pollinator community in field bean crops

The global decline in pollinators is likely to negatively affect the yield of insect pollinated crops such as field beans (Vicia faba). To understand the impact of such declines it is important to investigate how the abundance, composition and behaviour of the pollinator community relates to crop yield. We observed pollinators (specifically Bombus spp. and Apis mellifera) foraging in field bean fields. Some bees actively pollinated flowers whereas others robbed the nectar without actively pollinating the flowers. As legitimate foraging visits are more likely to pollinate the crop, we explored infield and landscape scale factors affecting this variation in behaviour. Infield factors included sowing time (winter/spring) and plant density. Landscape factors were the area of flower-rich habitat, and of mass-flowering crops within 1 km of the bean field. We also explored how the abundance and behaviour of different functional groups (short-tongued bumblebees, long-tongued bumblebees or honeybees) responded to these factors. Finally, we assessed how the abundance and behaviour of these pollinators affected field bean yield. Pollinators were more abundant in bean crops that were spring sown and where there was a smaller area of mass-flowering crops in the landscape. Functional groups varied in their predominant foraging behaviour and in how their behaviour was influenced by external factors. There was no relationship between pollinator abundance and bean yield however the proportion of pollinators legitimately foraging was negatively related to yield. Our findings align with previous research in suggesting that the benefits of insect pollinators for field beans are context specific. Additional work is required to develop pollinator conservation measures that will facilitate crop pollination.

Partitioning pollination services to faba bean (Vicia faba L.) between managed honeybees and wild bees

Animal pollination of crops is an important ecosystem service provided especially by managed honeybees and wild bees, but the relative importance of these taxa for crop pollination remains debated. Faba bean (Vicia faba L.) is a grain legume crop grown worldwide for food and feed which is partially dependent on insects for pollination. I determined the relative contribution of honeybees and wild bees to faba bean pollination. Visitation rates and foraging behaviours of pollinators were measured in a total of 20 faba bean fields over two years (10 fields per year) in Sweden, and the bean mass per flower visit for different pollinator taxa was quantified in a field experiment which was repeated over two years in a single site. By combining information on visitation rates, foraging behaviours and gains in bean mass from single visits to flowers, I estimate that 47% of insect pollination services to faba bean is delivered by honeybees, 40% by short-tongued bumblebees, 6% by long-tongued bumblebees and 8% by solitary bees. I conclude that both managed honeybees and wild bees, especially short-tongued bumblebees, contribute substantially to faba bean pollination in Sweden, and I recommend faba bean farmers to manage for both these pollinator taxa.

Landscape composition modifies pollinator densities, foraging behavior and yield formation in faba beans

Wildlife-friendly management practices promote pollinators and pollination services in agricultural landscapes. Wild bee densities are driven by landscape composition, as they benefit from an increased availability of nesting and foraging resources at landscape scale. However, effects of landscape composition on bee foraging decisions and consequences for crop pollination have rarely been studied. We investigated, how landscape composition affects bee densities and foraging behavior in faba bean (Vicia faba L.) fields and how this impacts faba bean yield. We recorded densities and nectar robbing behavior of honeybees, long- tongued and short-tongued bumblebees in faba bean fields in eleven landscapes with varying landscape composition (e.g. land cover of oilseed rape, faba bean and semi-natural habitats). Moreover, we assessed yield components of faba beans via pollinator exclusion experiments. Increasing covers of faba bean and semi-natural habitats positively influenced bumblebee densities, while high oilseed rape covers negatively affected short-tongued bumblebee densities in bean fields. Increased faba bean covers enhanced the proportion of nectar-robbing short-tongued bumblebees. The number of beans per pod was increased by insect pollination, while the number of pods was decreased; these effects however depended on variety. Landscape composition interacted with bee densities in shaping yield components in V. faba. Our study emphasizes the importance of considering landscape management to maximize crop yields, as shown for the case of faba beans. The composition of agricultural landscape can modulate bee densities in crop fields, bees foraging behavior and pollination services.

Quantifying the attractiveness of garden flowers for pollinators

There is great interest in planting urban areas to benefit pollinating insects, with the potential that urban areas and gardens could act as an extensive network of pollinator-friendly habitats. However, there are a great many different plant cultivars available to the gardener, and a paucity of evidence-based advice as to which plants are truly most attractive to flower-visiting insects. Here, we report insect visitation to metre square plots of 111 different ornamental plant cultivars at a site in central UK. Data were collected over 5 years, and comprise over 9000 insect observations, which were identified to species (for honeybees and bumblebees) or as ‘solitary bees’, Syrphidae, Lepidoptera and ‘others’. Unlike some previous studies, we found no difference in numbers of insects attracted to native or non-native species, or according to whether plants were annuals, biennials or perennials, but we did find that native plants attracted a significantly higher diversity of flower-visiting insects. Overall, the most-visited plants were Calamintha nepeta, Helenium autumnale and Geranium rozanne. However, patterns of visitation were quite different for every insect taxa examined. For example, different species of short-tongued bumblebees showed little overlap in their most-preferred plant cultivars. Interestingly, very similar plant cultivars often attracted different insect communities; for example, 72% of visitors to Aster novi belgii were honeybees or bumblebees, while the related Anthemis tinctoria, which also has daisy-like flowers, did not attract a single honeybee or bumblebee but was popular with solitary bees, hoverflies, and ‘other’ pollinators. Some plant cultivars such as Eryngium planum and Myosotis arvensis were attractive to a broad range of insects, while others attracted only a few species but sometimes in large numbers, such as Veronicastrum virginicum and Helenium autumnale which were both visited predominantly by honey bees. It is clear that we do not yet fully understand what factors drive insect flower preferences. Recommendations are made as to which flower cultivars could be combined to provide forage for a diversity of pollinator groups over the season from early spring to autumn, though it must be born in mind that some plants are likely to perform differently when grown in different environmental conditions.

Distasteful Nectar Deters Floral Robbery

Toxic nectar is an ecological paradox [1, 2]. Plants divert substantial resources to produce nectar thatattracts pollinators [3], but toxins in this rewardcould disrupt the mutualism and reduce plant fitness [4]. Alternatively, such compounds could protect nectar from robbers [2], provided that they do not significantly alter pollinator visitation to the detriment of plant fitness [1, 5-8]. Indeed, very few studies have investigated the role of plant toxins in nectar for defense against nectar robbers [4, 9, 10]. Here, we compared two Aconitum species (A.napellus and A.lycoctonum) that have flowers specialized for long-tongued bumblebee pollinators (Bombus hortorum) but are occasionally robbed by short-tongued bumblebees (B.terrestris) [6, 11-13]. Pollinator visits to flowers were much more frequent than by robbers, but visits correlated negatively with nectar alkaloid concentration and declined sharply between 200 and 380 ppm. However, alkaloid concentrations of>20 ppm were deterrent to B.terrestris, suggesting that robbers were less tolerant of nectar alkaloids. Nectar of both plant species contained similar concentrations of carbohydrates and toxic alkaloids, but A.lycoctonum was more likely to secrete nectar in each flower and was also visited more frequently by pollinators and robbers. We conclude that alkaloids in Aconitum spp. nectar affect rates ofboth pollinator visitation and robbery but may have co-evolved with nectar availability to maintain the fitness benefits of specialized plant-pollinator relationships. Chemical defense of nectar is, however, ultimately constrained by pollinator gustatory sensitivity.

Foraging habitats and floral resource use by colonies of long- and short-tongued bumble bee species in an agricultural landscape with kabocha squash fields

Bumble bees pollinate and forage on flowers of crop and wild plants in agricultural landscapes. These interactions may depend on landscape patterns and bumble bee traits. We studied the abundance, colony density, and foraging range in long-tongued Bombus diversus Smith and short-tongued B. hypocrita Perez, and evaluated their visits to flowers of wild plants and cultivated kabocha squash (Cucurbita maxima Duchesne). In forests in a farmland, B. hypocrita workers were trapped more frequently in the canopy. Full-sibs determined by nuclear microsatellite genotypes among workers collected in the farmland showed higher colony density and a larger foraging radius in B. hypocrita (30.8 km−2 and 848 m) than in B. diversus (8.3 km−2 and 723 m), respectively. Regarding wild plants, workers more frequently visited shallow flowers in B. hypocrita and deep flowers in B. diversus. These results suggest that bumble bees with different traits forage on different wild flowers in different habitats. Squash flowers were visited by both bumble bee species at similar frequency in the latter period of colony growth when males and new queens appeared. Composition of full-sib workers visiting squash and wild flowers did not depend on the number of collected workers of individual colonies, indicating that foraging on squash flowers was not associated with colony growth. Thus, growth and reproduction of bumble bee colonies may be supported by various wild plants and cultivated squash, respectively.

Drastic historic shifts in bumble-bee community composition in Sweden

The species richness of flower-visiting insects has declined in past decades, raising concerns that the ecosystem service they provide by pollinating crops and wild plants is threatened. The relative commonness of different species with shared ecological traits can play a pervasive role in determining ecosystem functioning, but information on changes in abundances of pollinators over time is lacking. We gathered data on relative abundances of bumble-bee species in Swedish red clover fields during three periods in the last 70 years (1940s, 1960s and present), and on clover seed yields since 1921. We found drastic decreases in bumble-bee community evenness, with potential consequences for level and stability of red clover seed yield. The relative abundances of two short-tongued bumble-bees have increased from 40 per cent in the 1940s to entirely dominate present communities with 89 per cent. Average seed yield declined in recent years and variation in yield doubled, suggesting that the current dependence on few species for pollination has been especially detrimental to stability in seed yield. Our results suggest a need to develop management schemes that promote not only species-rich but also more evenly composed communities of service-providing organisms.

Is Bumblebee Foraging Efficiency Mediated by Morphological Correspondence to Flowers?

Preference for certain types of flowers in bee species may be an adaptation for efficient foraging, and they often prefer flowers whose shape fits their mouthparts. However, it is unclear whether such flowers are truly beneficial for them. We address this issue by experimentally measuring foraging efficiency of bumblebees, the volume of sucrose solution consumed over handling time (μL/second), using long-tongued Bombus diversus Smith and short-tongued B. honshuensis Tkalcu that visit Clematis stans Siebold et Zuccarini. The corolla tube length of C. stans decreases during a flowering period, and male flowers are longer than female flowers. Long- and short-tongued bumblebees frequently visited longer and shorter flowers, respectively. Based on these preferences, we hypothesized that bumblebee foraging efficiency is higher when visiting flowers that show a good morphological fit between the proboscis and the corolla tube. Foraging efficiency of bumblebees was estimated using flowers for which nectar quality and quantity were controlled, in an experimental enclosure. We show that 1) the foraging efficiency of B. diversus was enhanced when visiting younger, longer flowers, and that 2) the foraging efficiency of B. honshuensis was higher when visiting shorter female flowers. This suggests that morphological correspondence between insects and flowers is important for insect foraging efficiency. However, in contradiction to our prediction, 3) short-tongued bumblebees B. honshuensis sucked nectar more efficiently when visiting younger, longer flowers, and 4) there was no significant difference in the foraging efficiency of B. diversus between flower sexes. These results suggest that morphological fit between the proboscis and the corolla tube is not a sole determinant of foraging efficiency. Bumblebees may adjust their sucking behavior in response to available rewards, and competition over rewards between bumblebee species might change visitation patterns in the wild. Thus, the determinants of foraging efficiency and visitation frequency for bee pollinators may be more complex than previously thought.

Density and seed set in a self‐compatible forb, Penstemon digitalis (Plantaginaceae), with multiple pollinators

Seed production may be limited because flowers do not get enough suitable pollen or because plants lack the resources to make seeds. We used replicated plantings to test factors that influence effects of bumblebee behavior on pollen limitation, as measured by the difference in seed set between hand- and naturally pollinated flowers, of Penstemon digitalis in patches of four to 41 flowering individuals. Seed set per flower was 376% higher in the largest as compared with the smallest Penstemon patches. This positive density dependence reflects activity of long-tongued bees, which (1) have higher effective density as patch size increases, (2) visit greater proportions of plants as patch size increases, and (3) visit smaller proportions of flowers per visited plant as patch size increases. Our results suggest that economics of flight and maneuverability of large, long-tongued bumblebees lead them to transfer more pollen between than within Penstemon plants in large patches. Density of smaller, short-tongued bumblebees was not positively associated with Penstemon seed set, but these bees may be important pollinators at low plant densities. Our experimental system indicates a clear positive relationship between activity of effective pollinators and seed set in a species capable of pollinating itself.

Causes and consequences of floral damage in Aconitum lycoctonum at high and low elevations in Switzerland

The outcomes of interactions among plants and the insects that use their flowers are likely to vary among the physical environments and the communities in which they grow. In this study we quantified floral damage of Aconitum lycoctonum in high (>2000m) and low (c. 500m) elevation populations in Switzerland. At high elevation, floral damage was frequent and was caused by nectar-robbing short-tongued bumblebees. Nectar robbers make a hole in the flower when they collect nectar. A nectar robber exclusion experiment showed that nectar robbery by short-tongued bumblebees had no effect on the female reproductive success of plants; robbing bees rarely damaged the nectaries, and damage to the petals probably does not decrease flower longevity. In addition, nectar robbers tended to collect pollen during about 10% of their visits. Thus, these bees may act as low-efficiency pollinators and may, at times, be mutualistic associates. At low elevation, the holes in the flowers were caused by beetles (Meligethes viridescens) and not by short-tongued bumblebees. The beetles eat pollen and might also consume nectar. Since the beetles gain access to pollen and nectar by entering the flower through its opening, and later chew holes while foraging on floral tissue, the beetles are pollen eaters rather than nectar robbers. Overall, our results show that not all floral damage is caused by nectar robbers and that there can be strong altitudinal variation in the causes and consequences of floral damage.

Flowers, Nectar and Insect Visits: Evaluating British Plant Species for Pollinator-friendly Gardens

Twenty-four plant species native or naturalized in Britain were grown in the Cambridge University Botanic Garden, UK and evaluated as potential resources for nectar-foraging bees, butterflies and hoverflies. In ten plant species a series of measurements were made, at regular intervals from dawn to dusk, of nectar secretion rate and standing crop, and in all species insect visits were monitored throughout daylight hours. The study revealed differences between plant species in the composition of the assemblage of insect visitors, and in the magnitude and temporal distribution of the nectar reward. In some cases we found interesting correlations between temperature and secretion rates or patterns of insect visits. Species that received numerous insect visits in our study are potentially valuable forage plants that might be planted by gardeners to support local pollinator populations. Deep flowers whose nectar is accessible to long-tongued bumblebees (Bombus hortorum, B. pascuorum) but not to honeybees may provide long-tongued pollinators with a resource refuge relatively free from honeybee competition. Features that make some of those plant species particularly interesting to observe in the garden include robbing by short-tongued bumblebees inSaponaria,baseworking by honeybees on closed flowers inMalva sylvestris, and apparent displacement of bumblebees by territorial behaviour of the solitary beeAnthidium manicatumon species ofStachys.

Evaluation of herbaceous plants for attractiveness to bumble bees for use near cranberry farms

SUMMARYTwenty-one herbaceous bee forage species were evaluated for attractiveness to bumble bees (Bombus spp.) and honey bees (Apis mellifera) and for their potential to grow in tandem with cranberry (Vaccinium macrocarpon) plantings to increase native bee populations for pollination. Seventeen of the species were planted in four replicated plots next to a cranberry bog in Long Beach, WA, USA, and four species were already established in an area adjacent to the plots. Agastache ruposa, A. foeniculum and Lotus corniculatus were the most attractive to short-tongued bumble bees. Nepeta mussinii, Borago officinalis, Phacelia tanacetifolia and A. foeniculum were the most attractive to long-tongued bumble bees. Honey bees were most attracted to B. officinalis, P. tanacetifolia and Raphanus sativus. The major short-tongued bee species A. mellifera, B. mixtus, B. occidentalis and B. sitkensis were the only significant pollinators of cranberry. The long-tongued species B. caliginosus and B. californicus were insignificant pollinators. Bumble bees preferred purple flowers, but there was no clear relationship between bee population density and the level of available soluble carbohydrate per flower or per area. The periodicity of foraging behaviour depended on bee species and plant; honey bees peaked at 15.00 h, while bumble bees were more constant throughout the day.

Cotoneasterfor bumble bees and honey bees

Regular monitoring between May and August 1988 of a collection of 22 taxa of Cotoneaster in the UK showed that the bumble bees Bombus pratorum and B. pascuorum preferentially visited species in the section Cotoneaster. The short-tongued bumble bees B. terrestris/lucorum and honey bees visited species in both sections of the genus, concentrating on the section Cotoneaster in the dearth period of early summer and on Chaeno-petalum after mid-June. The section Cotoneaster is recommended as particularly valuable for bee forage. This phenological survey should make it possible to select groups of species for amenity plantings to give a seasonal spread of flowering, enhancing the availability of nectar plants.

An initial assessment of blueberry pollinators in New Zealand

Abstract The short tongued bumble bee, Bombus terrestris (L.), followed by the honey bee, Apis mellifera L., were the commonest blueberry pollinators at Lincoln, New Zealand. At most, 7% of honey bee visits and 24% of B. terrestris visits to blueberry flowers could have resulted in pollination. Honey bees visited flowering shelter adjacent to the blueberries more often than the bumble bees did. The long tongued bumble bees, B. hortorum (L.) and B. ruderatus (Fabr.), consistently pollinated blueberry flowers, bit low populations restricted their value in pollination. There were no other effective insect pollinators of blueberries.

Pollination ecology and seed-set in the rare annual speciesMelampyrum arvenseL. (Scrophulariaceae)

SUMMARY Pollination of Melampyrum arvense L., a large-flowered hemiparasitic annual, was investigated in populations in The Netherlands, Germany, France and Switzerland. Pollination is achieved by bumblebees, with varying tongue lengths, collecting pollen and/or nectar. Long- and medium-tongued workers pollinate the flower nototribically (head-thorax pollination) and pollen-collecting short-tongued bumblebees sternotribically (venter pollination), as analysed by the actual transfer of fluorescent powder. Short-tongued bumblebees collect nectar by robbing the flowers, and sometimes also destroying the pistil. Nectar was present in a volume of 0.26 μl, with a sugar concentration of 30% and a ratio of fructose:glucose:sucrose = 1:0.67:0.73. M. arvense is self-fertile, but caged flowers do not produce seeds by the absence of auto-deposition. Artificial pollination showed that increasing pollination intensity increased fruiting, although after three pollinations fruiting did not increase and the number of seeds per fruit did. Observations in plots with variable plant density showed that during a low visitation intensity, flowers were visited at least 6.7 times during the flower's life span (7 days), and at a high visitation intensity 39.3 times. The additional effect on the seed-set of one-hand pollination during the flower's lifetime was low. Plants in low-density plots are highly branched in contrast to plants in high density. Branching of plants, resulting in more flowers per plant, and the fact that flowers on branches produce more seeds per flower, influence the total seed production per plant. The M. arvense population in The Netherlands had a rather high fruiting percentage and seed production per plant compared to three French populations.

Temporal changes in the pollinator fauna of tristylous Pontederia cordata, an aquatic plant

Temporal changes in the composition of the pollinator fauna of the tristylous aquatic plant Pontederia cordata were documented during the flowering seasons of 1982 and 1983. A total of 18 species of insects, mainly bumblebees, and a single species of hummingbird were observed visiting flowers during the 2-month flowering period. The abundance of pollinators within each season varied greatly, with highest densities corresponding to peak flowering in both years. Although overall abundance was similar each year, the diversity of species was greater in 1983 because of the addition of short-tongued bumblebees and the longer residency periods of other species. It is suggested that low summer rainfall in 1983 decreased flowering levels in terrestrial plant communities of the region, resulting in several bee species shifting their feeding onto P. cordata. The study demonstrates that changes in the structure of a plant's pollinator fauna occur over time and that despite the possession of a specialized pollination mechanism, tristylous P. cordata is visited by a wide range of pollinator species.

Robbing of Field Bean Flowers by the Short-Tongued Bumble BeeBombus TerrestrisL.

SummaryMost flowers produced during early flowering of autumn-sown field beans had small holes in the base of the corolla which indicated that they had been robbed by Bombus terrestris. The proportion of robbed flowers decreased as flowering continued. Slightly fewer flowers of spring-sown plants were robbed. There was no evidence of damage to the reproductive structures of 100 robbed flowers of the cultivar Maris Bead. Of the flowers sampled from the third, fourth and fifth flowering nodes of field bean plants growing near shelter at the paddock margin, 62% were robbed. Of the pods which subsequently formed at these nodes 59% were from flowers which had been robbed. This suggests that robbing of the flower by short-tongued bumble bees did not prejudice either pollination by other insects or pod development.

Seed production of new cultivars of lucerne

Multiplication of new cultivars of lucerne must be rapid to keep abreast of new pests and diseases. The most important factor is to harvest high seed yields in the establishing year. Widespread use of alkali and leafcutting bees, and possible management of short-tongued bumblebees, should raise the pollination level to near maximum. Low seeding rates, early sowing, good early weed control, adequate pollination and insect pest control will be rewarding for seed growers, merchants and customers. Keywords: Seed production, Medicago sativa, Nomia melanderi, Megachile rotundata, pollination.

EFFECTS OF BUMBLEBEE VISITS ON THE SEED SET OF PEDICULARIS, RHINANTHUS AND MELAMPYRUM (SCROPHULARIACEAE) IN THE NETHERLANDS

The pollination ecology of five species of Rhinanthoideae (the annual species Rhinanthus serotinus, R. minor and Melampyrum pratense, the biennial Pedicularis sylvatica and the annual and biennial P. palustris) has been investigated. All species contain pollen and nectar and are frequently visited by sternotribically and nototribically pollinating bumblebees. The effectiveness of pollen transfer has been measured by the use of fluorescent powder. In R. serotinus and M. pratense no differences exist in percentages of fluorescent stigmas of flowers nototribically or sternotribically visited by bumblebees. R. minor flowers, visited sternotribically, have very low percentages of fluorescent stigmas. This indicates that the pollen-covered venter cannot touch stigmas enclosed by the galea; the movements of the bumblebees probably caused self-pollination. P. palustris, R. serotinus and M. pratense flowers are very frequently perforated by nectar-collecting short-tongued bumblebees. P. sylvatica and R. minor flowers are very rarely perforated. On these species nectar is mainly collected by nototribically pollinating bumblebees. Seed production and dependence upon pollination by bumblebees (Bombus Latr. spp.) are considered. A range from high dependence upon bumblebee visits for seed production in P. palustris, to medium dependence in P. sylvatica and R. serotinus and virtual independence in R. minor and M. pratense is established. No species is completely self-sterile. Seed set in caged plants is due to favourable morphology and position of flowers. Close proximity of thecae and stigma or a downward curving of the pistil under pollen chamber in Melampyrum and Rhinanthus insure seed set in caged plants. In Pedicularis these characteristics for self-pollination are absent. The importance of bumblebees for the five Rhinanthoideae and the reciprocal importance of these pollen and nectar providing plants for bumblebees is discussed. The importance of alternative pollination by honeybees, thrips and wind is evaluated.

Divergence in inflorescence height: An evolutionary response to pollinator fidelity.

The above-ground heights of inflorescences of 8 species of wild-flowers in a subalpine meadow in the Colorado Rocky Mountains were measured in two successive years. An index of overlap (of height-distributions) was computed for pairwise comparisons of all species. The species were assorted into 4 groups based on their usual pollinators: long-tongued bumblebees (3 species were pollinated by long-tongued bumblebees), short-tongued bumblebees (3 species), hummingbirds (1 species), and solitary bees (1 species). The values of the sample of overlap indices for plants pollinated by the same animals was significantly smaller than the values for plants pollinated by different animals; plants which share pollinators are less alike in height than those that don't share pollinators. It is suggested that this is a result of selection for enhancement of pollinator fidelity. The selective mechanisms, based on the 'horizontal' flight pattern of pollinators and the consequences to the plant of interspecific flights, are discussed.