Does intraspecific size variation in bumblebees allow colonies to efficiently exploit different flowers?

Abstract.  1. It has long been known that foraging bumblebee workers vary greatly in size, within species, and within single nests. This phenomenon has not been adequately explained. Workers of their relatives within the Apidae exhibit much less size variation.
2. For the bumblebee Bombus terrestris size, as measured by thorax width, was found to correspond closely with tongue length, so that larger bees are equipped to feed from deeper flowers.
3. The mean size of worker bees attracted to flowers was found to differ between plant species, and larger bees with longer tongues tended to visit deeper flowers.
4. Finally, handling time depended on the match between corolla depth and tongue length: large bees were slower than small bees when handling shallow flowers, but quicker than small bees when handling deep flowers.
5. Size variation within bumblebees may be adaptive, since it enables the colony as a whole to efficiently exploit a range of different flowers. Possible explanations for the marked differences in size variation exhibited by bumblebees compared with Apis species and stingless bees (Meliponinae) 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.     

Flowers morphology and nectar concentration determine the preferred food source of stingless bee,Heterotrigona itama

Heterotrigona itama is a stingless bee species from Meliponini tribe. The bee collects nectar, pollen and resin to produce honey, bee bread, and propolis. The bee is also known to visit and collect nectar from various types of flowers but there are limited studies on why this species of bee prefers to visit certain types of flowers. This study was conducted to identify the nectar concentration in selected flowers favoured by H. itama and the relationship between the bee and the morphology of the flowers. Nectar was obtained from different species of flowers and the concentrations were measured using a digital refractometer. The tube length of each flower species and the tongue length of the bees were also measured. The results revealed that flowers preferred by H. itama have high nectar concentrations. The tube lengths of the preferred flowers were between 2.0 and 4.0 mm, which is compatible with the tongue length of the bee. This study revealed that both nectar concentration and flower morphology are important factors for the bees in choosing their food sources. The results from this study will benefit the beekeepers in the identification of flowers that should be planted in their farms to improve stingless bee beekeeping activities. Understanding the relationship between the bees and their flower preferences could also help us to understand the importance of conserving both the bee colonies and the various species of flowering plants to ensure the sustainability of flora and fauna in the ecosystem.     

Why is there variation in mean seed size among plants within single populations? test of the fertilization efficiency hypothesis

We tested the fertilization efficiency hypothesis, which attempts to explain mean seed size variation among plants within single populations, by comparing the patterns of seed size variation between chasmogamous (CH) flowers and cleistogamous (CL) flowers in Impatiens noli-tangere and Viola grypoceras, respectively. The fertilization efficiency hypothesis predicts that larger plants produce larger seeds if the number of pollen grains captured by a plant increases with increased allocation of resources to its attractive structures (e.g., corolla and nectar), but with diminishing gains. Thus, seed size should depend on plant size in seeds from CH flowers because of the diminishing gains of capturing pollen in these flowers, whereas seed size should not depend on plant size in seeds from CL flowers because CL flowers need not capture outcross pollen. We found significant positive correlations between mean seed size per plant and plant size for seeds from CH flowers in both species. However, there was no significant positive correlation between these two factors for seeds from CL flowers of both species. The results of the present investigations were thus consistent with the fertilization efficiency hypothesis.     

Diet breadth,coexistence and rarity in bumblebees

Factors that determine the relative abundance of bumblebee species remain poorly understood, rendering management of rare and declining species difficult. Studies of bumblebee communities in the Americas suggest that there are strong competitive interactions between species with similar length tongues, and that this competition determines the relative abundance of species. In contrast, in Europe it is common to observe several short-tongued species coexisting with little or no evidence for competition shaping community structure. In this study we examine patterns of abundance and distribution in one of the most diverse bumblebee communities in Europe, found in the mountains of southern Poland. We quantify forage use when collecting nectar and pollen for 23 bumblebee species, and examine patterns of co-occurrence and niche overlap to determine whether there is evidence for inter-specific competition. We also test whether rarity can be explained by diet breadth. Up to 16 species were found coexisting within single sites, with species richness peaking in mountain pasture at ~1,000 m altitude. Results concur with previous studies indicating that the majority of pollen collected by bumblebees is from Fabaceae, but that some bee species (e.g. B. ruderatus) are much more heavily dependent on Fabaceae than others (e.g. B. lucorum). Those species that forage primarily on Fabaceae tended to have long tongues. In common with studies in the UK, diet breadth was correlated with abundance: rarer species tended to visit fewer flower species, after correcting for differences in sample size. No evidence was found for similarity in tongue length or dietary overlap influencing the likelihood of co-occurrence of species. However, the most abundant species (which co-occurred at most sites) occupied distinct dietary niche space. While species with tongues of similar length tended, overall, to have higher dietary niche overlap, among the group of abundant short-tongued species that commonly co-occurred there was marked dietary differentiation which may explain their coexistence.     

Contrasting movement patterns of nectar-collecting and pollen-collecting bumble bees (Bombus terricola) on fireweed (Chamaenerion angustifolium) inflorescences

Abstract. 1. Movements of nectar and pollen-foraging bumble bees on inflorescences of Chamaenerion angustifolium (L.) J. Holub (fireweed or rosebay willow herb) were compared with predictions based on reward distributions and optimality principles. Observations suggest that nectar and pollen-gathering bumble bees behave according to the same set of reward maximization criteria when foraging from flowers of this species.
2. Both kinds of foragers matched their arrival points with the vertical positions on inflorescences in which the densities of their respective food resources were greatest. For nectar-foragers, this point was located at the lowest tier of flowers, whereas for pollen-foragers it was found in the middle of the inflorescences. Nectar and pollen-foraging bees both moved upward on inflorescences following gradients from high to low reward availability.
3. Nectar-foragers responded to decreases in inflorescence size over the season by reducing the number of flower visits made on each raceme. Number of flowers visited by pollen-foragers was low throughout and reflected the scarcity of male-phase flowers on racemes. Flower revisitation rates were low for both kinds of workers, but were slightly higher for those collecting pollen.     

Resource competition triggers the co-evolution of long tongues and deep corolla tubes

Background

It is normally thought that deep corolla tubes evolve when a plant''s successful reproduction is contingent on having a corolla tube longer than the tongue of the flower''s pollinators, and that pollinators evolve ever-longer tongues because individuals with longer tongues can obtain more nectar from flowers. A recent model shows that, in the presence of pollinators with long and short tongues that experience resource competition, coexisting plant species can diverge in corolla-tube depth, because this increases the proportion of pollen grains that lands on co-specific flowers.

Methodology/Principal Findings

We have extended the model to study whether resource competition can trigger the co-evolution of tongue length and corolla-tube depth. Starting with two plant and two pollinator species, all of them having the same distribution of tongue length or corolla-tube depth, we show that variability in corolla-tube depth leads to divergence in tongue length, provided that increasing tongue length is not equally costly for both species. Once the two pollinator species differ in tongue length, divergence in corolla-tube depth between the two plant species ensues.

Conclusions/Significance

Co-evolution between tongue length and corolla-tube depth is a robust outcome of the model, obtained for a wide range of parameter values, but it requires that tongue elongation is substantially easier for one pollinator species than for the other, that pollinators follow a near-optimal foraging strategy, that pollinators experience competition for resources and that plants experience pollination limitation.     

Going to great lengths: selection for long corolla tubes in an extremely specialized bat–flower mutualism

In a hypothesis that has remained controversial since its inception, Darwin suggested that long-tubed flowers and long-tongued pollinators evolved together in a coevolutionary race, with each selecting for increasing length in the other. Although the selective pressures that flowers impose on tongue length are relatively straightforward, in that longer tongues allow access to more nectar, selective pressures that pollinators impose on flower length are less clear. Here, we test for such selective pressures in the highly specialized mutualism between the nectar bat Anoura fistulata, which can extend its tongue twice as far as other nectar bats, and Centropogon nigricans, which has flowers of a similar length (8–9 cm). We used flight cage experiments to examine the effects of artificially manipulated flower lengths on (i) bat behaviour and (ii) pollen transfer. Increased length produced longer visits, but did not affect the force bats applied during visits. In the second experiment, flower length increased both the male and female components of flower function: long male flowers delivered more pollen grains and long female flowers received more pollen grains. However, pollen transfer was not correlated with visit duration, so the mechanism behind differences in pollen transfer remains unclear. By demonstrating that bats select for increasing flower length, these results are consistent with the hypothesis that A. fistulata evolved its remarkable tongue in a coevolutionary race with long-tubed flowers similar to that envisioned by Darwin.     

The effect of nectar production on neighborhood size

Summary Bumblebee foraging behavior was observed on two plant species with similar floral and inflorescence structures. One species produces nectar while the other does not. Bees, upon visiting nectar producing flowers tend to empty them of nectar and by frequently moving between close neighbors, create a patchily distributed resource base. Bees maximize their foraging efficiency in such an environment by using an area-restricted searching behavior and flying distances inversely correlated with the quality of reward received. Pollen collecting bumblebees do not create a patchy environment and maximize their foraging efficiency by more consistently moving shorter distances. Pollen collecting bumblebees are significantly more likely to revisit flowers and to visit more flowers per inflorescence than are nectar gathering bumblebees. These differences in foraging behavior increase the neighborhood size for nectar producing species and make it increasingly unlikely that random drift will be a dominant mode of evolution in populations of these species.     

Nectar Sugar Production across Floral Phases in the Gynodioecious Protandrous Plant Geranium sylvaticum

Many zoophilous plants attract their pollinators by offering nectar as a reward. In gynodioecious plants (i.e. populations are composed of female and hermaphrodite individuals) nectar production has been repeatedly reported to be larger in hermaphrodite compared to female flowers even though nectar production across the different floral phases in dichogamous plants (i.e. plants with time separation of pollen dispersal and stigma receptivity) has rarely been examined. In this study, sugar production in nectar standing crop and secretion rate were investigated in Geranium sylvaticum, a gynodioecious plant species with protandry (i.e. with hermaphrodite flowers releasing their pollen before the stigma is receptive). We found that flowers from hermaphrodites produced more nectar than female flowers in terms of total nectar sugar content. In addition, differences in nectar production among floral phases were found in hermaphrodite flowers but not in female flowers. In hermaphrodite flowers, maximum sugar content coincided with pollen presentation and declined slightly towards the female phase, indicating nectar reabsorption, whereas in female flowers sugar content did not differ between the floral phases. These differences in floral reward are discussed in relation to visitation patterns by pollinators and seed production in this species.     

Foraging ecology of hoverflies: morphology of the mouthparts in relation to feeding on nectar and pollen in some common urban species

Abstract. 1. Previous accounts of the feeding behaviour of hoverflies (Diptera: Syrphidae) are contradictory and in many cases do not correspond with field observations.
2. Patterns of feeding on nectar and pollen differ between species: these patterns are correlated with morphological differences.
3. The data indicate that there are two correlates of increasing tongue length: first, the proportion of pollen in the diet decreases; and second, the flies concentrate on visiting flowers with longer corollae, which contain more nectar sugar.
4. Reasons for these effects are discussed.     

Foraging efficiency and size matching in a plant–pollinator community: the importance of sugar content and tongue length

A long‐standing question in ecology is how species interactions are structured within communities. Although evolutionary theory predicts close size matching between floral nectar tube depth and pollinator proboscis length of interacting species, such size matching has seldom been shown and explained in multispecies assemblages. Here, we investigated the degree of size matching among Asteraceae and their pollinators and its relationship with foraging efficiency. The majority of pollinators, especially Hymenoptera, choose plant species on which they had high foraging efficiencies. When proboscides were shorter than nectar tubes, foraging efficiency rapidly decreased because of increased handling time. When proboscides were longer than nectar tubes, a decreased nectar reward rather than an increased handling time made shallow flowers more inefficient to visit. Altogether, this led to close size matching. Overall, our results show the importance of nectar reward and handling time as drivers of plant–pollinator network structure.     

西方蜜蜂和兰州熊蜂在设施桃园的访花偏好性比较

【目的】为了比较西方蜜蜂 Apis mellifera 和兰州熊蜂 Bombus lantschouensis 在设施桃园内对不同时期桃花的访花偏好性、以及这种偏好性与花粉活力和采集花粉花蜜之间的关系。【方法】记录2种蜂在温室桃园内访问早期花、中期花和晚期花的比例,测定桃花不同时期的花粉活力以及2种蜂携带的花粉活力,观察2种蜂采集花蜜和采集花粉的成功率,统计2种蜂访花过程中桃花所处的枝条数及植株数。【结果】桃花不同时期的花粉活力差异显著,早期花花药未开裂,花粉未释放,中期花花粉活力（58.3%）显著高于晚期花花粉活力（34.2%）（P<0.01）;西方蜜蜂更加偏好访问中期花,对中期花的访问率高达75.3%,显著高于兰州熊蜂对中期花的访问率（49.2%）（P<0.01）;西方蜜蜂携带的花粉活力（92.1%）显著高于兰州熊蜂携带的花粉活力（72.9%）,但是西方蜜蜂采集花粉和采集花蜜的成功率均低于兰州熊蜂（P<0.01）;在访问一定数量的桃花过程中,兰州熊蜂在设施桃园内访问的枝条数和植株数较多,分布范围较广（P<0.01）。【结论】和兰州熊蜂相比,西方蜜蜂对活力花粉的辨别能力更强,更加偏好访问花粉活力较高的花朵,这种偏好性导致其采集花粉花蜜的成功率降低。     

Relationship between floral tube length and nectar robbing in Duranta erecta L. (Verbenaceae)

Although nectar robbing is a common phenomenon in plant species with tubular flowers or flowers with nectar spurs, the potential effect of this illegitimate interaction on plant reproductive success has not received the deserved attention. In the present study, we analysed the functional relationship between flower morphology and nectar robbing, and examined the reproductive consequences of the interaction in a population of Duranta erecta (Verbenaceae) on the island of Cuba. The results show that nectar robbing is conducted by the carpenter bees Xylocopa cubaecola and affects up to 44% of flowers in the studied population. However, not all the flowers have the same probability of being robbed. The chance of flowers being robbed increases with flower length and flower diameter. Moreover, nectar robbing significantly decreases the chance that flowers will set fruit. Also, the impact of nectar robbing on the probability of flowers to set fruits is dependent on the plant. We suggest that nectar robbing may represent an opposite selective force that balances the selection for longer corollas often imposed by pollinators specializing in visiting tubular flowers. Such a relationship with nectar robbers would have obvious implications for the evolution of tubular or closed flowers. This preliminary finding deserves further research in light of the ecological and evolutionary consequences of nectar robbing in tubular flowers.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 392–398.     

Distribution and forage use of exotic bumblebees in South Island, New Zealand

The rapid decline in bumblebee populations within Europe has been linked to habitat loss through agricultural intensification, and a consequential reduction in the availability of preferred forage plants. The successful introduction of four European Bombus species to the South Island of New Zealand from England (in 1885 and 1906) provides an opportunity to determine how important different forage plants (also introduced from the U.K.) are to two severely threatened European bumblebee species (Bombus ruderatus and B. subterraneus). In January 2003 we conducted a survey of bumblebee populations across 70 sites in the central and southern South Island, recording which plant species were being used as pollen and nectar sources for each Bombus species. All four bumblebee species showed a clear preference for plants of European origin. Only B. terrestris, the most polylectic species, was recorded feeding on native plant species. The longer-tongued bumblebees, B. hortorum, B. ruderatus, and B. subterraneus, foraged predominantly on just two plant species; Trifolium pratense for both nectar and pollen, and Echium vulgare for nectar. These plant species are now declining in abundance in the U.K. Our results provide support for the hypothesis that the loss of flower-rich meadows, particularly those containing populations of Fabaceae species with long corollae, is responsible for the decline of bumblebee species across Europe. Comparison with earlier bumblebee surveys suggests that long-tongued bumblebees may also be in decline in New Zealand, particularly B. subterraneus which is now very localised and scarce.     

Sexual differences in reproductive characters and pollinator attractiveness in gynodioecious Glechoma longituba (Lamiaceae)

We quantified the differences in floral characters and attractiveness to flower visitors under natural conditions between the sexual types in the gynodioecious plant Glechoma longituba. We also manipulated flowers by altering corolla size or nectar volume, or by removing anthers, to examine the effect of these primary and secondary attractants (i.e. rewards and advertisements) on attractiveness. A change in corolla size and shape reduced visiting frequency and pollen load. Removal of anthers did not affect visiting rates, but significantly reduced pollination rates and stigmatic pollen load. A decrease in the nectar volume of a flower was associated with a reduction in handling time and pollen loads on stigmas. These results show that corolla size is an important advertisement to pollinators (particularly at greater distance), which associate hermaphrodite flowers with a larger corolla and a larger volume of nectar than female flowers. We found that artificial changes in population structure affected the behavior of pollinators as well as the pollination rates of flowers. We suggest that the pattern of distribution of hermaphrodite and female clones in a population may serve to avoid pollen limitation in a female clone or patch. This effect may ensure female reproductive success and allow for the maintenance of female individuals in natural populations of this gynodioecious plant.     

Effects of nectar robbing on pollinator behavior and plant reproductive success of Pitcairnia angustifolia (Bromeliaceae)

Nectar robbers may have direct and indirect effects on plant reproductive success but the presence of nectar robbing is not proof of negative fitness effects. We combined census data and field experiments to disentangle the complex effects of nectar robbing on nectar production rates, pollinator behavior, pollen export, and female reproductive success of Pitcairnia angustifolia. Under natural conditions flowers were visited by four different animal species including a robber‐like pollinator and a secondary robber. Natural levels of nectar robbing ranged from 40 to 100%. Natural variation in nectar robbing was not associated with fruit set in any year whereas seed set was weakly positively associated for 1 year only. Artificial nectar robbing did not increase nectar production or concentration, did not affect the behavior of long‐billed hummingbirds, and when faced with artificially robbed flowers, these visitors behaved as secondary nectar robbers. The number of stigmas within a patch that received pollen dye analogs and the average distance traveled by these analogs were not significantly different between robbing treatments (robbed flowers versus unrobbed flowers), but the maximum distance traveled by these pollen analogs was higher when nectar robbing was not prevented. Overall, the proportion of robbed flowers on an inflorescence had a neutral effect to a weak positive effect on the reproduction of individual plants (i.e. positive association between nectar robbing and fruit set in 2002) even when it clearly changed the behavior of its most efficient pollinator potentially increasing the frequency of nectar robbing within a plant.     

Bumblebee-pollination and temporal change of the calyx tube length in Clematis stans(Ranunculaceae)

Clematis stans is dioecious semi-arboreal, with pale purple–blue, nodding, tubulous flowers in a paniculate inflorescence. Both male and female flowers produce nectar from the base of the calyx tube during a flowering period of 3 or 4 days, and are pollinated by two bumblebee species, Bombus diversus and B. honshuensis, with different proboscis lengths. When the flowers open, four sepals constructing a calyx tube separate at the top and their respective tips gradually curl up, so that a tubular part shortens. Observations at two field sites showed that B. diversus (with a longer proboscis) most often visits the flowers with a longer calyx tube, and B. honshuensis (with a shorter proboscis) the flowers with a shorter calyx tube, i.e., later in the flowering period. By changing the calyx tube length, the flowers of C. stans accept the two bumblebee species with different proboscis length as pollinators and thus increase the chance of pollination for each flower. It was also found that the two bumblebee species prefer the male flowers to the female flowers, although the female flowers secrete more nectar as a reward than male flowers. This is likely because they visit the male flowers to collect pollen grains in addition to nectar. Electronic Publication     

A trade-off between the amount and distance of pollen dispersal triggered by the mixed foraging behaviour of Sephanoides sephaniodes (Trochilidae) on Lapageria rosea (Philesiaceae)

Nectar thieves may increase or decrease pollinator-mediated pollen flow and thus may have positive or negative effects on plant reproductive success. In temperate rainforests of South America, the hummingbird Sephanoides sephaniodes acts as both a pollinator and non-destructive nectar thief on Lapageria rosea. Although pollinators that also act as nectar thieves have the potential to significantly modify plant reproductive success, no previous study has addressed this. To determine how the mixed behaviour of S. sephanoides affects pollen flow, we experimentally exposed some flowers to nectar theft and excluded nectar thieves from other flowers. We then assessed pollen dispersal into the floral neighbourhood. Thieved flowers exported less pollen, but the pollen exported was transferred farther into the neighbourhood. Our findings indicate a trade-off between distance and amount of pollen flow.     

Flower choice by honey bees (Apis mellifera L.): sex-phase of flowers and preferences among nectar and pollen foragers

Bees foraging for nectar should choose different inflorescences from those foraging for both pollen and nectar, if inflorescences consist of differing proportions of male and female flowers, particularly if the sex phases of the flowers differ in nectar content as well as the occurrence of pollen. This study tested this prediction using worker honey bees (Apis mellifera L.) foraging on inflorescences of Lavandula stoechas. Female flowers contained about twice the volume of nectar of male flowers. As one would predict, bees foraging for nectar only chose inflorescences with disproportionately more female flowers: time spent on the inflorescence was correlated with the number of female flowers, but not with the number of male flowers. Inflorescence size was inversely correlated with the number of female flowers, and could be used as a morphological cue by these bees. Also as predicted, workers foraging for both pollen and nectar chose inflorescences with relatively greater numbers of both male and female flowers: time spent on these inflorescences was correlated with the number of male flowers, but not with the number of females flowers. A morphological cue inversely associated with such inflorescences is the size of the bract display. Choice of flowers within inflorescences was also influenced predictably, but preferences appeared to be based upon corolla size rather than directly on sex phase.