Getting to the start line: how bumblebees and honeybees are visually guided towards their first floral contact

Much of the literature on foraging behaviour in bees focuses on what they learn after they have had rewarded experience with flowers. This review focuses on how honeybees and bumblebees are drawn to candidate food sources in the first place: the foundation on which learning is built. Prior to rewarded foraging experience, flower-naïve bumblebees and honeybees rely heavily on visual cues to discover their first flower. This review lists methodological issues that surround the study of flower-naïve behaviour and describes technological advances. The role of distinct visual properties of flowers in attracting bees is considered: colour, floral size, patterning and social cues. The research reviewed is multi-disciplinary and takes the perspectives of both the bees and the plants they visit. Several avenues for future research are proposed.     

Possible Mechanisms for the Formation of Flower Size Preferences by Foraging Bumblebees

Large flowers often contain larger nectar rewards, and receive more pollinator visits, than small flowers. We studied possible behavioral mechanisms underlying the formation of flower size preferences in bumblebees, using a two-phase laboratory experiment. Experimentally naive Bombus terrestris (L.) foraged on artificial flowers that bore either a large (3.8 cm diameter) or a small (2.7 cm diameter) display of a uniform color. Only flowers of one display size contained nectar rewards. We changed the display color and the locations of large and small flowers in the second experimental phase. We recorded the bees' choices in both phases. Almost half of the bees (41%) made their first visit to a small flower. The bees learned to associate display size with food reward, and chose rewarding flowers with >85% accuracy by the end of each experimental phase. Some learning occurred within the bees' first three flower visits. Learning of the size–reward association was equally good for large and small displays in the first experimental phase, but better for small displays in the second phase. Formation of size–reward associations followed a similar course in both phases. This suggests that the bees did not apply their experience from the first learning phase to the new situation of the second phase. Rather, they treated each phase of the experiment as an independent learning task. Our results suggest that associative learning is involved in the formation of preferences for large displays by bees. Moreover, bees that had learned to prefer large displays in one foraging situation may not transfer this preference to a novel situation that is sufficiently different. We propose that this feature of the bees' behavior can select for honest advertising in flowers.     

Bumblebees Do Not Respond to Variance in Nectar Concentration

Worker bumblebees (Bombus fervidus) were given repeated binary choices between two colors of artificial flowers with the same associated mean nectar concentration (X? = 20%), but with different variances in nectar concentration. Flowers of one color, yellow or blue, rewarded a bee with 1 μl of 20% sucrose solution (low-variance flower type) on each visit (p = 1) and flowers of the other color rewarded a bee on each visit with 1 μl of either 10% or 30% sucrose (p = 0.5; high-variance flower type). Of the 10 bees tested, nine showed no preference for either the high- or low-variance flowers (indifferent or risk-insensitive). This result is similar to honeybee responses to variation in nectar concentration, despite differences in foraging ecology between bumblebees and honeybees. Flower-choice behaviour in the presence of variance in nectar concentration is a response to the expected concentration of the alternative flower types. Possible mechanisms of risk-sensitive foraging behaviour in bees are discussed.     

Predator crypsis enhances behaviourally mediated indirect effects on plants by altering bumblebee foraging preferences

Predators of pollinators can influence pollination services and plant fitness via both consumptive (reducing pollinator density) and non-consumptive (altering pollinator behaviour) effects. However, a better knowledge of the mechanisms underlying behaviourally mediated indirect effects of predators is necessary to properly understand their role in community dynamics. We used the tripartite relationship between bumblebees, predatory crab spiders and flowers to ask whether behaviourally mediated effects are localized to flowers harbouring predators, or whether bees extend their avoidance to entire plant species. In a tightly controlled laboratory environment, bumblebees (Bombus terrestris) were exposed to a random mixture of equally rewarding yellow and white artificial flowers, but foraging on yellow flowers was very risky: bees had a 25 per cent chance of receiving a simulated predation attempt by ‘robotic’ crab spiders. As bees learnt to avoid ‘dangerous’ flowers, their foraging preferences changed and they began to visit fewer yellow flowers than expected by chance. Bees avoided spider-free yellow flowers as well as dangerous yellow flowers when spiders were more difficult to detect (the colour of yellow spiders was indistinguishable from that of yellow flowers). Therefore, this interaction between bee learning and predator crypsis could lead flower species harbouring cryptic predators to suffer from reduced reproductive success.     

Pollination Biology of Hosta sieboldiana (Lodd.) Engler and H. sieboldii (Paxton) J. Ingram (Liliaceae)

Abstract The pollination biology of Hosta sieboldiana and H. sieboldii is investigated comparatively in Central Japan. Both species have homogamous, one-day flowers pollinated by bumblebees. The abdomens of the bees touch the stigma on the extended style when they land on the anthers inside the herkogamous flower, and autogamy is effectively prevented. However, the flowers are fairly self-compatible, and geitonogamy may occur rather frequently because two or more flowers on a scape very often bloom at the same time and many ramets are contiguous. The pollen/ovule ratios suggest that these species are facultative outbreeders. The flower of H. sieboldii seems completely suited to bumblebee pollination. In H. sieboldiana the stigma of the flower, whose style strongly protrudes, is not always touched by bumblebees, but frequent visitation of bumblebees results in pollination of almost all the flowers. Both species have similar pollination systems but seem reproductively isolated by blooming times and habitats. Their common pollinators, however, may sometimes cause introgressive hybridization in contiguous populations.     

Consequences of floral complexity for bumblebee-mediated geitonogamous self-pollination in Salvia nipponica Miq. (Labiatae)

Abstract.— I address how floral complexity influences geitonogamous self-pollination through manipulation of pollinator behavior in Salvia nipponica . The pivoting stamens of S. nipponica hinder nectar-collecting bumblebees from crawling into flowers, increasing the probing time per flower. I predicted that longer probing times would reduce the relative cost of moving between plants, causing bees to leave plants earlier. To test this prediction, I simplified S. nipponica flowers by removing the stamens from all open flowers within a 75-m² quadrat. Bumblebees probed these flowers more quickly than intact flowers, but the stamen removal affected neither the frequency of flower revisitation nor the flight distance between plants. In response to the decrease in the probing time per flower, bees probed more flowers on these plants. Therefore, in S. nipponica , floral complexity reduces the opportunity for geitonogamous self-pollination. Stamen removal also increased bee visitation per flower, suggesting that this sort of complexity deters visitation. To keep complex flowers attractive, therefore, selection might increase floral rewards or longevity. Floral complexity might evolve in an integrative manner with the rest of the floral phenotype.     

Floral preferences of bumblebees (Bombus edwardsii) in relation to intermittent versus continuous rewards

Worker bumblebees, Bombus edwardsii, preferably feed from artificial flowers yielding the same (continuous) reward on each visit rather than from flowers yielding variable (intermittent) rewards, even though the long-term expectation of reward is the same at each type of flower. However, variation in degree of preference among individual bees is high. Preferences after long foraging experience correspond closely to early preferences. Rate of flower visitation increases as mean reward increases, and may accelerate preference formation. Preferences are discussed in light of processes thought to control learning in honeybees. From these findings we propose that reward variance and expected time between reinforcements be considered as constraints in models of optimal foraging behaviour.     

Remote perception of floral nectar by bumblebees

Summary On both artificial flowers in the laboratory and certain plant species in the field, bumblebees often closely approached flowers and then departed without probing for nectar. In laboratory experiments where nectar rewards were associated with subtle visual or olfactory cues, bumblebees approached and avoided non-rewarding flowers. Flowers that bees entered and probed for nectar contained rewards much more frequently than predicted by chance alone. When there were no external cues associated with nectar content, bees visited rewarding flowers by chance alone, provided rewarding flowers were not spatially clumped. In the field, bumblebees approached and rejected a large proportion of dogbane flowers and red clover inflorescences. On both species, flowers or inflorescences probed by bees contained more nectar than those rejected by bees or those that I chose at random. On fireweed and monkshood, bees rarely or never approached and rejected healthy-looking flowers. Predictions generated by an optimal foraging model were tested on data from four bumblebee species foraging on red clover. The model was highly successful in qualitatively predicting the relationship between handling time and proportion of inflorescences rejected by individual bees, and the relationship between threshold nectar content for acceptance by bees and average resource availability. Thus, bees appeared to use remotely perceived cues to maximize their rates of nectar intake.     

Foliage affects colour preference in bumblebees (<Emphasis Type="Italic">Bombus impatiens</Emphasis>): a test in a three-dimensional artificial environment

Red flowers are a defining character of the bird-pollination syndrome. Birds do not, however, innately prefer red, suggesting that rather than attracting birds, red flowers may serve to exclude other visitors (e.g., bumblebees). Bees are sometimes considered “blind” to red, but studies have in fact documented both blue and red preferences in various bee species. These mixed results may be an effect of overly simplistic lab settings. We hypothesized that bees might readily locate red flowers in a simple laboratory environment, but struggle to find the same flowers in a complex, foliated setting. We tested the effects of environmental complexity on visitation to red and blue artificial flowers and on the foraging rate of captive worker bumblebees (Bombus impatiens). Bees made significantly fewer visits to red flowers when foraging in a complex environment with artificial green foliage, suggesting that red becomes harder to locate in this context than in a simple, leafless environment. Bees also foraged more slowly, on average, in the complex environment, although the difference was apparent only among experienced bees. Our findings provide a possible explanation for previous laboratory tests finding no colour preference in bumblebees. This “contextual colour-blindness” of bees supports the hypothesis that red evolved as a mechanism for plants to avoid visitation by bees, favouring bird pollination instead.     

How long to stay on a plant: the response of bumblebees to encountered nectar levels

This field study shows that the number of flowers visited per bee per plant (Anchusa officinalis) increases with the instantaneous nectar level at the plant. Observations during the season showed that a bee visits more flowers per plant of given nectar level, the lower the overall mean nectar level in the study area. These results agree with predictions from a model based on the ‘marginal value theorem’, but with assumptions and constraints adapted for nectar-foraging bees. It suggests that bumblebees assess the nectar level at a plant by sampling one or a few flowers, which is possible because within-plant nectar volumes are correlated. The bees compare encountered gains to an optimal plant switching threshold equal to the overall mean nectar level and leave an unrewarding plant as soon as possible, but continue to visit the flowers on a rewarding plant. However, the bees leave before having visited all flowers due to a searching constraint. The bees’ response to plant nectar levels results in systematic flower visitation, because visitation to recently depleted flowers is reduced, which reduces the variation of the inter-visit time per flower. Systematic flower visitation implies that the overall mean encountered gain per flower is higher than the overall mean standing crop, as predicted by a model of systematic foraging. However, the sampling and searching constraints on the bees’ response to plant nectar levels increase the variation of the inter-visit time per flower, and thereby limit the degree of systematic flower visitation and the effect on the mean encountered gain.     

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 movement patterns of carpenter beesXylocopa micans and bumblebeesBombus pennsylvanicus onPontederia cordata inflorescences

The movement patterns of carpenter bees (Xylocopa micans) and bumblebees (Bombus pennsylvanicus) foraging for nectar on vertical inflorescences ofPontederia cordata were studied near Miami, Florida. The floral biology ofP. cordata is unique in several ways: (a) many short-lived flowers per inflorescence, (b) constant nectar production throughout the life span of each flower, and (c) abscence of vertical patterning of nectar and age of flowers. Inflorescences ranged between 3.5 and 15.8 cm long and had between 9 and 55 open flowers. Both carpenter bees and bumblebees arrived mostly on the bottom third of the inflorescence and left after visiting flowers on the top third of the inflorescence. The departure position from the inflorescence was higher up than observed in studies of other insect pollinators foraging on other speces of plants. This pattern of departure probably occurs in the absence of a vertical gradient of nectar or floral morphology.     

Bumblebees (Bombus terrestris) and honeybees (Apis mellifera) prefer similar colours of higher spectral purity over trained colours

Differences in the concentration of pigments as well as their composition and spatial arrangement cause intraspecific variation in the spectral signature of flowers. Known colour preferences and requirements for flower-constant foraging bees predict different responses to colour variability. In experimental settings, we simulated small variations of unicoloured petals and variations in the spatial arrangement of colours within tricoloured petals using artificial flowers and studied their impact on the colour choices of bumblebees and honeybees. Workers were trained to artificial flowers of a given colour and then given the simultaneous choice between three test colours: either the training colour, one colour of lower and one of higher spectral purity, or the training colour, one colour of lower and one of higher dominant wavelength; in all cases the perceptual contrast between the training colour and the additional test colours was similarly small. Bees preferred artificial test flowers which resembled the training colour with the exception that they preferred test colours with higher spectral purity over trained colours. Testing the behaviour of bees at artificial flowers displaying a centripetal or centrifugal arrangement of three equally sized colours with small differences in spectral purity, bees did not prefer any type of artificial flowers, but preferentially choose the most spectrally pure area for the first antenna contact at both types of artificial flowers. Our results indicate that innate preferences for flower colours of high spectral purity in pollinators might exert selective pressure on the evolution of flower colours.     

Floral visitors and ant scent marks: noticed but not used?

1. Bee behaviour when visiting flowers is mediated by diverse chemical cues and signals, from the flower itself and from previous visitors to the flower. Flowers recently visited by bees and hoverflies may be rejected for a period of time by subsequent bee visitors. 2. Nectar‐thieving ants also commonly visit flowers and could potentially influence the foraging decisions of bees, through the detection of ant trail pheromones or footprint hydrocarbons. 3. Here we demonstrate that, while naÏve bumblebees in laboratory trials are not inherently repelled by ant scent marks, they can learn to use them as informative signals while foraging on artificial flowers. 4. To test for similar activity in the wild, visitor behaviours at the flowers of Digitalis purpurea Linnaeus, Bupleurum fruticosum Linnaeus, and Brassica juncea (Linnaeus) Czernajew were compared between flowers that had been in contact with ants and those that had not. No differences were found between the two treatments. 5. The use of chemical foraging cues by bees would appear to be strongly dependent on previous experience and in the context of these plant species bees did not associate ant scent mark cues with foraging costs.     

Frequency-dependent selection by pollinators: mechanisms and consequences with regard to behaviour of bumblebees Bombus terrestris (L.) (Hymenoptera: Apidae)

Bombus terrestris , a typical pollinating insect species, was offered artificial flowers of two different corolla colours with the same sucrose solution reward in an array. Common colours were significantly preferred, and the strength of the frequency-dependent response increased as a result of learning. There were also frequency-independent biases towards blue flowers, probably because blue flowers appeared more conspicuous to bumblebees than yellow flowers, and the degree of preference for blue was greater when flowers had low nectar rewards. Flower-to-flower movements by individual bumblebees between flowers were non-random, were biased to movements within the same flower colour, and were also dependent on morph frequency. The mechanisms governing flower selection in bumblebees are discussed. Pollinators foraging similarly in a natural situation would induce positive frequency-dependent selection, assortative mating, and directional selection on different corolla colour morphs of the plant population being visited, resulting in stabilizing selection for a single flower colour.     

Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebee perception of Antirrhinum majus flower colour

We wished to understand the effects on pollinator behaviour of single mutations in plant genes controlling flower appearance. To this end, we analysed snapdragon flowers (Antirrhinum majus), including the mixta and nivea mutants, in controlled laboratory conditions using psychophysical tests with bumblebees. The MIXTA locus controls petal epidermal cell shape, and thus the path that incident light takes within the pigment-containing cells. The effect is that mixta mutant flowers are pink in comparison to the wild type purple flowers, and mutants lack the sparkling sheen of wild type flowers that is clearly visible to human observers. Despite their fundamentally different appearance to humans, and even though bees could discriminate the flowers, inexperienced bees exhibited no preference for either type, and the flowers did not differ in their detectability in a Y-maze—either when the flowers appeared in front of a homogeneous or a dappled background. Equally counterintuitive effects were found for the non-pigmented, UV reflecting nivea mutant: even though the overall reflectance intensity and UV signal of nivea flowers is several times that of wild type flowers, their detectability was significantly reduced relative to wild type flowers. In addition, naïve foragers preferred wild type flowers over nivea mutants, even though these generated a stronger signal in all receptor types. Our results show that single mutations affecting flower signal can have profound effects on pollinator behaviour—but not in ways predictable by crude assessments via human perception, nor simple quantification of UV signals. However, current models of bee visual perception predict the observed effects very well.     

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.     

Bumblebees (Bombus terrestris) use social information as an indicator of safety in dangerous environments

Avoiding predation is one of the most important challenges that an animal faces. Several anti-predation behaviours can be employed, yet simply using the presence of conspecifics can be a good signal of safety in an environment with potential predation hazards. Here, we show, for the first time, that past experience of predation causes bumblebees (Bombus terrestris) to aggregate with conspecifics, facilitating the identification of safe foraging patches. Bees were trained to differentiate between flowers that harboured predators and flowers that were predator free. When test subjects were subsequently presented solely with the previously predator-infested flower species, there was a significant preference to only land on flowers occupied by other feeding conspecifics. Yet, when safe flowers were made available to subjects previously entrained to discriminate safe from predator-occupied flowers, subjects ignored other bees and the social information potentially provided by them, demonstrating that attraction towards conspecifics is confined to dangerous situations. Our findings demonstrate a previously unknown social interaction in pollinators which may have important implications for plant–pollinator interactions.     

Recognition and avoidance of contaminated flowers by foraging bumblebees (Bombus terrestris)

Bumblebee colonies are founded by a single-mated queen. Due to this life history trait, bumblebees are more susceptible to parasites and diseases than polyandrous and/or polygynous social insects. A greater resistance towards parasites is shown when the genetic variability within a colony is increased. The parasite resistance may be divided into different levels regarding the step of the parasite infection (e.g. parasite uptake, parasite intake, parasite's establishment in the nest, parasite transmission). We investigate the prophylactic behaviour of bumblebees. Bumblebees were observed during their foraging flights on two artificial flowers; one of these was contaminated by Crithidia bombi, a naturally occurring gut parasite of bumblebees (in a control experiment the non-specific pathogen Escherichia coli was used). For C. bombi, bumblebees were preferentially observed feeding on the non-contaminated flower. Whereas for E. coli, the number of visits between flowers was the same, bumblebees spent more time feeding on the non-contaminated flower. These results demonstrate the ability of bumblebees to recognise the contamination of food sources. In addition, bumblebees have a stronger preference for the non-contaminated flower when C. bombi is present in the other flower than with E. coli which might be explained as an adaptive behaviour of bumblebees towards this specific gut parasite. It seems that the more specific the parasite is, the more it reduces the reward of the flower.     

Selection of trait combinations through bee and fly visitation to flowers of Polemonium foliosissimum

Pollinators are known to exert natural selection on floral traits, but the extent to which combinations of floral traits are subject to correlational selection (nonadditive effects of two traits on fitness) is not well understood. Over two years, we used phenotypic manipulations of plant traits to test for effects of flower colour, flower shape and their interaction on rates of pollinator visitation to Polemonium foliosissimum. We also tested for correlational selection based on weighting visitation by the amount of conspecific pollen delivered per visit by each category of insect visitor. Although bumblebees were the presumed pollinators, solitary bees and flies contributed substantially (42%) to pollination. In manipulations of one trait at a time, insects visited flowers presenting the natural colour and shape over flowers manipulated to present artificial mutants with either paler colour or a more open or more tubular flower. When both colour and shape were manipulated in combination, selection on both traits arose, with bumblebees responding mainly to colour and flies responding mainly to shape. Despite selection on both floral traits, in a year with many bumblebees, we saw no evidence for correlational selection of these traits. In a year when flies predominated, fly visitation showed a pattern of correlational selection, but not favouring the natural phenotype, and correlational selection was still not detected for expected pollen receipt. These results show that flower colour and shape are subject to pollinator‐mediated selection and that correlational selection can be generated based on pollinator visitation alone, but provide no evidence for correlational selection specifically for the current phenotype.