Flight Durations in Bumblebees Under Manipulation of Feeding Choices

Foraging bees spend less time flying between flowers of the same species than between individuals of different species. This time saving has been suggested as a possible advantage of flower-constant foraging. We hypothesized that the time required to switch flower type increases if (a) such switches are infrequent and (b) the bees need to decide whether to switch or not. Bumblebees were taught to forage on artificial feeders that were identical in morphology and reward schedule but differed in the color of their landing surface. In the first two experiments bees foraged alternatively between two feeders. In Experiment 1 the colors of the landing surfaces were switched every two or three visits, while in Experiment 2 they were switched every six or seven visits. In the third experiment, the bees were required to decide whether to make a color-constant or a color-shift flight. Intervisit time was defined as time elapsed between consecutive visits to feeders. When feeder colors were changed frequently (Experiment 1), we detected no difference between color-constant and color-shift intervisit times. When bees were repeatedly exposed to one color (Experiment 2), color shifts required a significantly longer time. When allowed to choose (Experiment 3), bees performed more color-constant flights than color-shift flights. Intervisit times were similar for color-constant and color-shift flights in this experiment. Intervisit times in Experiment 3 were significantly longer than in Experiment 2 and slightly but nonsignificantly longer than in Experiment 1. The results suggest that bees indeed save time though flower-constant foraging but that this time savings is a small (1 s/flower visit) under laboratory conditions, and appears only when switches between flower types are infrequent. The time saved may be more significant over long foraging trips, and when morphological differences between flower species are large, as often happens under natural conditions, providing a selective advantage to flower-constant foraging.     

Floral constancy in bumble bees: handling efficiency or perceptual conditioning?

Individual bees often prefer flowers of the same species that they are already foraging on, and other individual bees prefer other flowers. This floral constancy has classically been explained as a learned behavior by which bees avoid wasting time switching between handling techniques. Choice trails were given to Bombus vagans workers that were freely foraging in mixed and pure fields of Trifolium pratense, T. repens, Viccia cracca, and Prunella vulgaris. Contrary to expectation, (1) bees showed if anything a stronger preference for their flower type in pure fields where they lacked experience than in a mixed field where they had had the opportunity to learn, (2) there was greater constancy in a mixed field of the two morphologically similar Trifolium species than in a mixed field of the morphologically disparate T. pratense and P. vulgaris, and (3) bees were more willing to switch between flowers of distinct morphologies when the colors were similar than between flowers of distinct colors when the morphologies were similar. We suggest that constancy is due to some form of perceptual conditioning whereby individual bees become temporarily sensitized to one or a few floral cues.     

Small bees overheat in sunlit flowers: do they make cooling flights?

1. Although thermoregulation by large bees in cool climates has been well studied, less is known about the very different thermoregulatory strategies of small bees, especially those subjected to heat stress. 2. Studies were carried out on small (< 20 mg fresh weight), dark‐coloured, solitary bees (mostly halictids and hylaeine colletids) experiencing an extreme radiative heat load, enhanced by the high‐altitude location and by reflection of incident radiation by the high‐albedo petals of the flowers of Potentilla lancinata. 3. When foraging in the flowers, such bees experienced peak operative temperatures exceeding 44 °C. In these conditions, males largely stopped foraging but females continued, usually limiting their flower visits to a few seconds and making frequent short flights. These flights would cool the bees down, because bees suspended in air were cooler than bees in sunlit flowers, and convective cooling during flight would further enhance the cooling effect of departure from the flower. 4. As far as is known, cooling flights in small bees have not been proposed before, providing a new avenue for exploration of bee thermoregulatory strategies.     

A test of spatial memory and movement patterns of bumblebees at multiple spatial and temporal scales

Naive bumblebee foragers appear to use movement rules at smallspatial and temporal scales, but it is not clear whether theserules determine movement patterns as the scales increase. Onestrategy for efficient foraging used by bumblebees is near-farsearch, involving short flights when in good patches of flowersand longer flights when in poor patches. Bumblebees also demonstratethe use of a spatial memory strategy by returning repeatedlyto patches of flowers, and even following the same route betweenflowers, over periods of days. We attempted to determine atwhat spatial scales bumblebees use spatial memory while foragingwithin a patch and after how many flower visits spatial memoryoutweighs near-far search. Bumblebees in the laboratory foragedon a 4 x 4 array of artificial flowers with distances rangingfrom 10 to 80 cm between flowers in two simple spatial patterns.The proportion of visits to flowers containing a sucrose rewardwas monitored for either 100 or 400 flower visits in two separateexperiments, after which the locations of the rewarding andnonrewarding flowers were interchanged, producing a mirror image.A drop in accuracy after the mirror image switch would indicatethat the bees had memorized the location of rewarding flowers.Mirror image tests, and comparisons to a simulation model ofnear-far search based on actual flight distances, indicate thatnaive bumblebees used near-far search on flowers 10 cm apartbut increasingly used spatial memory as experience and spatialseparation increased. Bumblebees thus have multiple tacticsavailable to forage efficiently in different environments.     

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.     

Can flower constancy in nectaring butterflies be explained by Darwin’s interference hypothesis?

 When foraging for nectar many insects exhibit flower constancy (a preference for flower species which they have previously visited) and frequently ignore rewarding flowers of other species. Darwin proposed the favoured explanation for this behaviour, hypothesizing that learning of handling skills for one flower species interferes with the ability to recall handling skills for previously learned species. A crucial element of this hypothesis is that savings in handling time resulting from constancy must exceed increases in travelling time necessitated by ignoring other suitable species. A convincing quantification of this trade-off has not been achieved and tests to date on bumblebees indicate that savings in handling time are too small to offset an increase in travelling time. To assess further the validity of Darwin’s hypothesis, handling and flight times of the butterfly, Thymelicus flavus, were measured under natural conditions, and the abundance and reward provided by the available flower species quantified to enable estimation of foraging efficiency. Butterflies exhibited a mean increase in handling time of 0.85 s per flower associated with switching between flower species, although the magnitude of this difference varied greatly among flower species. Switching was not associated with a decrease in travelling time, contrary to expectation. Switching was more frequent following a lower than average reward from the last flower visited. In butterflies, flights serve functions other than movement between nectar sources, such as mate location (unlike worker bees). Hence constancy may be a viable strategy to reduce time spent in handling flowers and increase time available for other activities. Although savings in handling time may be small, Darwin’s interference hypothesis remains a valid explanation for flower constancy in foraging butterflies. Received: 27 January 1997 / Accepted: 5 June 1997     

Threatened pollination systems in native flora of the Ogasawara (Bonin) Islands

• Background and Aims Various alien species have been introducedto the Ogasawara Islands (Japan). A survey was made investigatingwhether the native pollination systems fit an ‘islandsyndrome’ (biasing the flora to dioecy, with subdued,inconspicuous flowers) and whether alien species have disruptedthe native pollination network. • Methods Flower visitors and floral traits were determinedin the field (12 islands) and from the literature. Associationsamong floral traits such as sexual expression, flower colourand flower shape were tested. • Key Results Among the 269 native flowering plants, 74·7% are hermaphroditic, 13·0 % are dioecious and 7·1% are monoecious. Classification by flower colour revealed that36·0 % were white, 21·6 % green and 13·8% yellow. Woody species (trees and shrubs) comprised 36·5% of the flora and were associated with dioecy and white flowers.Solitary, endemic small bees were the dominant flower visitorsand visited 66·7 % of the observed species on satelliteislands where the native pollination networks are preserved.In contrast to the situation on the satellite islands, introducedhoneybees were the most dominant pollinator (visiting 60·1% of observed species) on the two main islands, Chichi-jimaand Haha-jima, and had spread to satellite islands near Chichi-jimaIsland. • Conclusions The island syndrome for pollination systemsin the Ogasawara Islands was evident in a high percentage ofdioecious species, the subdued colour of the native flora andsolitary flower visitors on satellite islands. The shape andcolour adaptations of several flowers suggested native pollinationniches for long-proboscis moths and carpenter bees. However,the domination and expansion of introduced honeybees have thepotential for disruption of the native pollination network inthe two main, and several satellite, islands of the OgasawaraIslands.     

Honeybee (Apis mellifera ligustica) Response to Differences in Handling Time, Rewards and Flower Colours

Free flying honeybees were tested outdoors on blue–white and blue–yellow dimorphic artificial flower patches to examine the influence of reward difference, flower handling‐time difference and flower colour choice on foraging decisions. We employed different flower‐well depths to vary handling times (costs), and differences in sucrose molarity to vary reward quality. Tests were performed with 2 and 6 μl rewards to vary quantity. We show that when handling time is correlated with flower‐colour morphs on a pedicellate artificial flower patch, a honeybee's foraging behaviour is dependent on the flower colours used in the choice tests. This supports a honeybee foraging model where constraints are a significant factor in decision making. Bees visiting blue–yellow flower patches exhibited flower constancy to colour, where they restricted most visits to a single flower colour, some bees to blue and others to yellow, irrespective of handing time differences. When offered a choice of equally rewarding blue or white flowers, bees were not constrained by flower colour and chose to visit flowers with a lower handling time. When reward molarity varied with well depth between blue and white flowers, foragers chose shallow‐well flowers (short‐handling time) with a smaller net harvest rate over deep‐well flowers (long‐handling time) with a greater net harvest rate. Results using the blue–white dimorphic flower patch suggest that when foraging options simultaneously involve reward and handling‐time choices, honeybee forager behaviour is inconsistent with an absolute method of evaluating profit.     

Attractiveness of single and multiple species flower patches to beneficial insects in agroecosystems

The provision of floral resources for the enhancement of beneficial insect populations has shown promise as a strategy to enhance biological control and pollination in agroecosystems. One approach involves the provision of a single flower species while a second involves the multiple flower species, but the two have never been compared experimentally. Here we examine the influence of single and multiple species flower treatments on the abundance and foraging behaviour of key beneficial insects in two agricultural agroecosystems (broccoli and lucerne crops). The five flower treatments comprised buckwheat only, phacelia only, a simple mixture of buckwheat and phacelia, a complex mixture of buckwheat, phacelia and a commercial seed blend or the existing crop as a control. The abundance of bumble‐bees (Bombus hortorum) and honey bees (Apis mellifera) was highest in the three treatments that contained phacelia, while hoverfly (Melanostoma fasciatum) numbers were high in all four flower treatments. Bumble‐bees and honey bees probed almost exclusively phacelia flowers, even when provided with a choice of other flower species in the simple and complex mixture treatments. In contrast, hoverflies probed the flowers of all plant species in single and multiple species treatments, with no apparent difference in acceptance. However, in mixture treatments, the majority of individual bumble‐bees, honey bees and hoverflies probed the flowers from only one species, despite the presence of alternative flower species. Our results illustrate how an appreciation of insect floral attractiveness can be used to customise the species composition of floral patches to potentially maximise biological control and pollination in targeted agroecosystems.     

欧报春（Primula vulgaris）不同花色与色素关系及花色遗传初步分析

为了掌握欧报春各花色遗传规律服务于良种生产,通过对欧报春各色花进行色素吸收光谱和薄层层析分析,进行不同花色杂交研究,分析了欧报春各色花所含色素类型及各花色遗传规律。结果显示欧报春群体含多种花色素,单株也可含有多种花色素,形成多变的粉色、红色及蓝色花。黄色深浅主要由类胡萝卜素含量决定。白色对粉色及黄色为隐性遗传,黄色、粉色为显性遗传并有数量遗传特征,黄色与粉色独立遗传。蓝色为多基因控制的隐性遗传,并具有数量遗传特征。     

Flower color change accelerated by bee pollination in Tibouchina (Melastomataceae)

Floral color changes are common among Melastomataceae and have been interpreted as a warning mechanism for bees to avoid old flowers, albeit increasing long-distance flower display. Here the reproductive systems of Tibouchina pulchra and T. sellowiana were investigated by controlled pollinations. Their pollinators were identified, and experiments on floral color and fragrance changes were conduced to verify if those changes affect the floral visitation. Both Tibouchina species are self compatible. The flowers lasted three days or more, and the floral color changed from white in the 1st day to pink in the following days. Pollen deposition on stigma induced floral color change. The effectiveness of the pollination is dependent on bees’ size; only large bees were regarded as effective pollinators. In experimental tests, the bees in T. pulchra preferred the natural white flowers while the visitors of T. sellowiana were attracted by both natural and mimetic 1st-day flowers (2nd-day flowers with experimentally attached 1st-day flower petals). During the experiments on floral fragrance, the bees visited both natural and mimetic 1st-day flowers (2nd-day flowers with 1st-day flower scents). In both experiments, the bees avoided natural 2nd-day flowers, but seldom visited modified 2nd-day flowers. The attractiveness of T. pulchra and T. sellowiana flowers cannot be attributed exclusively to the color or the fragrance separately, both factors seemingly act together.     

The effects of predation risk from crab spiders on bee foraging behavior

Recent studies have suggested that top–down effects ofpredation on plant–pollinator interactions may not be,as previously thought, rare and/or weak. In this paper, we explorethe effects of crab spiders (Araneae: Thomisidae) on the behaviorof 2 species of bee (Hymenoptera: Apidae) foraging for nectarand pollen on 3 different plant species in central Portugal.In 2 experiments, we found that the eusocial bee Apis melliferawas significantly less likely to inspect and accept a floweror inflorescence if it harbored a spider. In contrast, we foundno such effects of spiders on the behavior of the solitary beeEucera notata. Further experiments showed that the effects ofenvironmental cues associated with predators on flower visitationby A. mellifera were detectable even when no spider was presentat the moment a flower was encountered. Such indirect effectswere only identified, however, in bees foraging on 1 of 2 plantspecies studied. In a final experiment, A. mellifera was shownto respond negatively to the presence of the corpses of conspecificsglued to flowers. This suggests that prey corpses left exposedon petals or bracts by spiders provide an obvious cue that beescan use to avoid predators. These results add to a growing bodyof evidence that plant–pollinator interactions are notimmune to the effects of predation and suggest that the strengthof such effects vary both between and within species.     

Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (<Emphasis Type="Italic">Bombus terrestris</Emphasis>) as a case study

Individual bumblebees were trained to choose between rewarded target flowers and non-rewarded distractor flowers in a controlled illumination laboratory. Bees learnt to discriminate similar colours, but with smaller colour distances the frequency of errors increased. This indicates that pollen transfer might occur between flowers with similar colours, even if these colours are distinguishable. The effect of similar colours on reducing foraging accuracy of bees is evident for colour distances high above discrimination threshold, which explains previous field observations showing that bees do not exhibit complete flower constancy unless flower colour between species is distinct. Bees tested in spectrally different illumination conditions experienced a significant decrease in their ability to discriminate between similar colours. The extent to which this happens differs in different areas of colour space, which is consistent with a von Kries-type model of colour constancy. We find that it would be beneficial for plant species to have highly distinctive colour signals to overcome limitations on the bees performance in reliably judging differences between similar colours. An exception to this finding was flowers that varied in shape, in which case bees used this cue to compensate for inaccuracies of colour vision.     

The learning abilities of the white cabbage butterfly,Pieris rapae,foraging for flowers

This study examines the role of learning and memory in the butterflyPieris rapae crucivora Boisduval during foraging for flowers. In an outdoor cage with 6 flower species,P. rapae showed various visiting patterns: some visited only one species, while others visited several species in a day. The foraging process for flowers ofErigeron annuus (L.) Pers. could be divided into two successive steps: (1) landing on the nectaring caputs, and (2) finding the source of nectar in the caput. Butterflies learned to proceed through the two steps more efficiently with successive attempts: they gradually decreased landings on nectarless caputs and probings on the nectarless petals of ligulate flowers respectively. As a result, handling time per unit caputs became shorter, and apparent rewards per unit time, i.e. the efficiency of collecting nectar, increased. In addition, once learned,P. rapae could remember a rewarding flower color for 3 days, which was not interfered with by learning another flower color. This indicates thatP. rapae keeps memory for a period longer than 3 days, and that they can remember at least two flower species as suitable flower resources. Furthermore, data indicated that they sometimes can apply the foraging skills obtained on other flower species to a novel one. These abilities could enable butterflies to easily switch flower species, or to enhance labile preference. It has been known thatP. rapae also shows flower constancy, which may be due to memory constraints. Therefore, they may appropriately use two foraging tactics: visit consistency and labile preference, to get enough nectar according to their circumstances.     

Different responses of pollinating bees to size variation and sexual phases in flowers ofCampanula

To examine the response of pollinating bees to size and sexual phases of flowers, we constructed an artificial population ofCampanula having large flower variation and presented it to potentially pollinating bees in nurseries. The pollinating bee groups (halictid, megachilid and bumble bees) responded differentially to both the flower size and to the sexual phases of the flowers. Whereas visitation rate of megachilid bees increased with the flower size, those of halictid bees and bumble bees did not show particular trends; for example, bumble bees visited almost all of the flowers consistently. Visitation frequencies to male-and female-phased flowers were significantly different between megachilids at Tokyo and halictids. This study indicates that pollinator attraction could not solely explain the evolution of the flower size inCampanula, and that other factors such as pollen transfer efficiency, should be considered.     

Assessment of pollen reward and pollen availability in Solanum stramoniifolium and Solanum paniculatum for buzz‐pollinating carpenter bees

The two widespread tropical Solanum species S. paniculatum and S. stramoniifolium are highly dependent on the visits of large bees that pollinate the flowers while buzzing them. Both Solanum species do not offer nectar reward; the rewarding of bees is thus solely dependent on the availability of pollen. Flower visitors are unable to visually assess the amount of pollen, because the pollen is hidden in poricidal anthers. In this study we ask whether and how the amount of pollen determines the attractiveness of flowers for bees. The number of pollen grains in anthers of S. stramoniifolium was seven times higher than in S. paniculatum. By contrast, the handling time per five flowers for carpenter bees visiting S. paniculatum was 3.5 times shorter than of those visiting S. stramoniifolium. As a result foraging carpenter bees collected a similar number of pollen grains per unit time on flowers of both species. Experimental manipulation of pollen availability by gluing the anther pores showed that the carpenter bees were unable to detect the availability of pollen by means of chemical cues before landing and without buzzing. Our study shows that the efficiency of pollen collecting on S. paniculatum is based on large inflorescences with short between‐flower search times and short handling time of individual flowers, whereas that of S. stramoniifolium relies on a large amount of pollen per flower. Interestingly, large carpenter bees are able to adjust their foraging behaviour to drastically different strategies of pollen reward in otherwise very similar plant species.     

Nonrandom Composition of Flower Colors in a Plant Community: Mutually Different Co-Flowering Natives and Disturbance by Aliens

When pollinators use flower color to locate food sources, a distinct color can serve as a reproductive barrier against co-flowering species. This anti-interference function of flower color may result in a community assembly of plant species displaying mutually different flower colors. However, such color dispersion is not ubiquitous, suggesting a variable selection across communities and existence of some opposing factors. We conducted a 30-week study in a plant community and measured the floral reflectances of 244 species. The reflectances were evaluated in insect color spaces (bees, swallowtails, and flies), and the dispersion was compared with random expectations. We found that co-existing colors were overdispersed for each analyzed pollinator type, and this overdispersion was statistically significant for bees. Furthermore, we showed that exclusion of 32 aliens from the analysis significantly increased the color dispersion of native flowers in every color space. This result indicated that aliens disturbed a native plant–pollinator network via similarly colored flowers. Our results demonstrate the masking effects of aliens in the detection of color dispersion of native flowers and that variations in pollinator vision yield different outcomes. Our results also support the hypothesis that co-flowering species are one of the drivers of color diversification and affect the community assembly.     

Bees assess pollen returns while sonicating Solanum flowers

Summary Can bees accurately gauge accumulating bodily pollen as they harvest pollen from flowers? Several recent reports conclude that bees fail to assess pollen harvest rates when foraging for nectar and pollen. A native nightshade (Solanum elaeagnifolium Cavanilles) that is visited exclusively for pollen by both solitary and social bees (eg. Ptiloglossa and Bombus) was studied in SE Arizona and SW New Mexico. The flowers have no nectaries. Two experiments were deployed that eliminated pollen feedback to the bees by experimentally manipulating flowers prior to bee visits. The two methods were 1) plugging poricidal anthers with glue and 2) emptying anthers of pollen by vibration prior to bee visitation. Both experiments demonstrated that bees directly assess pollen harvest on a flower-by-flower basis, and significantly tailor their handling times, number of vibratile buzzes per flower and grooming bouts according to the ongoing harvest on a given flower. In comparison to experimental flowers, floral handling times were extended for both Bombus and Ptiloglossa on virgin flowers. Greater numbers of intrafloral buzzes and numbers of times bees groomed pollen and packed it into their scopae while still on the flower were also more frequent at virgin versus experimental flowers. Flowers with glued andreocia received uniformly brief visits from Bombus and Ptiloglossa with fewer sonications and virtually no bouts of grooming. Curtailed handling with few buzzes and grooms also characterized visits to our manually harvested flowers wherein pollen was artificially depleted. Sonicating bees respond positively to pollen-feedback while harvesting from individual flowers, and therefore we expect them to adjust their harvesting tempo according to the currency of available pollen (standing crop) within Solanum floral patches.     

Two alien invasive acacias in Italy: Differences and similarities in their flowering and insect visitors

In Italy, alien acacias have been introduced for ornamental and reforestation purposes, and some species became invasive occupying patches of the Mediterranean landscape. On the Island of Elba (Central Italy), Acacia dealbata and A. pycnantha form dense stands at short distance, showing an impressive massive flowering at the end of the winter/early spring. Our aim was to investigate the behaviour of the two species in relation to the flowering features, from phenology to floral characteristics, and their replay to the observed flower visitors. Differences between the two species emerged on all the parameters considered. A. pycnantha peak of flowering occurred later than A. dealbata and showed larger flower heads (FHs), more flowers/head, stamens/flower and polyads. On A. dealbata, we recorded longer racemes and more FHs/raceme, determining a more flower-dense crown. Even if contacts with flower visitors were generally low on both species, A. dealbata showed a more heterogeneous visitor assemblage. Both acacias species interacted with local generalist pollinators, as bumblebees and honey bees. Flower handling and resource collection strategy by the honey bee indicate a long-term relationship between the bee and the acacias, with bees investing longer time on the larger A. pycnantha flower heads.     

Departure rules used by bees foraging for nectar: A field test

Summary Departure rules used by solitary long-tongued bees (Anthophora spp. andEucera spp.) collecting nectar from flowers ofAnchusa strigosa (Boraginaceae) were studied. The amount of nectar a bee receives from an individual flower was estimated by measuring the time elapsed since the previous bee visit to that flower. Measurements of nectar accumulation in experimentally emptied flowers indicated that this time interval is an accurate predictor of nectar volumes in flowers. We found that nectar rewards influence the probability of departure from individual plants, as well as distances of movements within plants. The probability of departure from individual plants was negatively related to the amount of reward received at the two lastvisited flowers. This result indicates that the bees used a probabllistic departure rule, rather than a simple threshold departure rule, and that rewards from both the current and the previously visited flower were important in determining departure points. Distances of inter-flower movements within plants were negatively related to the amount of reward received at the current flower. The overall results suggest that the pollinators ofA. strigosa make two types of departure decisions-departures from the whole plant and departures from the neighbourhood of individual flowers-and that they use different departure rules for each scale. Factors influencing the decision-making processes of the observed foraging behaviour are discussed.