Does the Flower Constancy of Bumble Bees Reflect Foraging Economics?

We examined the effects of floral reward level and spatial arrangement on the propensity of bumble bees to exhibit flower constancy. In three separate experiments, we compared the flower constancy of bees on dimorphic arrays of blue and yellow flowers that differed either in reward concentration, reward volume, or inter‐flower distance. Overall, flower choice patterns varied among bees, ranging from random selection to complete constancy. When flowers contained greater reward volumes and were spaced farther apart, bees showed less flower constancy and more moves to closely neighbouring flowers. Changes in reward concentration had no effect on flower constancy; however, more dilute rewards produced shorter flight times between flowers. In addition, there was a strong positive relationship between degree of flower constancy and net rate of energy gain when flowers were spaced farther apart, indicating that constant bees were more economic foragers than inconstant bees. Together, these results support the view that the flower constancy of pollinators reflects an economic foraging decision.     

Nectarivore foraging ecology: rewards differing in sugar types

Abstract.

• 1 Honey bees, visiting artificial flower patches, were used as a model system to study the effects of sugar type (sucrose, glucose, fructose, and mixed monosaccharide), caloric reward, and floral colour on nectarivore foraging behaviour. Observed behaviour was compared to the predictions of various (sometimes contradictory) foraging models.
• 2 Bees drank indiscriminately from flowers in patches with a blue-white flower dimorphism when caloric values of rewards were equal (e.g. 1M sucrose in both colours; 1 M sucrose versus 2 M monosaccharide of either type), but when nectar caloric rewards were unequal, they switched to the flower colour with the calorically greater reward.
• 3 In yellow-blue dimorphic flower patches, on the other hand, bees did not maximize caloric reward. Rather, bees were individually constant, some to blue, others to yellow, regardless of the sugar types or energy content of the rewards provided in the two flower morphs.
• 4 The results suggest that optimal foraging theory (maximization of net caloric gain per unit time) is a robust predictor of behaviour with regard to the sugar types common to nectars; such optimal foraging is, however, limited by a superstructure of individual constancy.

     

Can honey bees change foraging patterns?

Abstract. 1. Foraging patterns were studied using honey bees on artificial flower patches to determine if given individuals could change behaviours under differing conditions.
2. Two types of flower patches were used; those simulating a population of flowers, dimorphic for colour, and grids simulating a single colour-dimorphic inflorescence.
3. In the simulated population of flowers bees were individually constant to colour over a range of reward volumes and flower patch sizes.
4. Each bee remained individually constant to a flower morph when visiting a population-type grid but changed to random visitation on the simulated inflorescence.
5. On the simulated inflorescence, with morphs providing unequal qualities of reward, most bees foraged on the higher molarity morph.
6. Most, but not all bees, failed to minimize uncertainty on the simulated inflorescence.
7. On the simulated inflorescence, bees failed to optimize when one morph provided a greater reward volume than did the other.
8. In the population of flowers bees flew from flower to flower, whereas, they walked on the simulated inflorescence.     

Floral choices by honeybees in relation to the relative distances to flowers

ABSTRACT. Honeybees ( Apis mellifera L.) were presented with a series of binary choices between two equally rewarding yellow or blue artificial flowers. When flowers were placed equidistant from each other, the bees maintained high degrees of constancy to one flower colour. When flowers were spaced unequally, the bees most often chose to visit the closest flower, as is predicted by an optimal foraging model.     

Foraging Response of Turkish Honey Bee Subspecies to Flower Color Choices and Reward Consistency

Foraging behavior of Apis mellifera caucasica, A.m. carnica and A.m. syriaca in Turkey was studied for intrinsic subspecies-based differences. Models of forager flower-color fidelity, risk sensitive behavior and maximizing net gain were tested. Foragers were presented artificial flower patches containing blue, white and yellow flowers. Some bees of each subspecies showed high fidelity to yellow flowers, while others favored blue and white flowers. The degree of fidelity, however, differed among subspecies and was dependent upon which color was favored. Bees of all subspecies demonstrated risk indifferent behavior regardless of whether they favored yellow flowers or blue and white flowers. Flower handling time differed among subspecies and increased with reward quantity, and when a reward was present. Flight time between consecutive flowers also differed among honey bee subspecies. Foragers of all subspecies had a higher net gain when visiting flowers with consistent rewards.     

Visual cues and foraging choices: bee visits to floral colour phases in Alkanna orientalis (Boraginaceae)

When a pollination vector is required, any mechanism that contributes to floral visitation will potentially benefit the reproductive fitness of a plant. We studied the effect of floral colour change in the desert perennial Alkanna orientalis on the foraging behaviour of the solitary bee Anthophora pauperata . Flowers changed colour over time from bright yellow (with moderate nectar reward) to pale yellow/white (with significantly lower nectar reward). Bee visitation was non-random with respect to colour phase availability within the flower population and was biased towards the more rewarding flowers. At plants where the availability of colour phases had been manipulated experimentally to produce 'bright' or 'pale' plants, bees visited significantly more flowers (and for longer periods) on the bright plants. The change of flower colour was not simply age-related; we observed variation in the temporal course of colour change and our data suggest that visitation, leading to deposition of cross-pollen, can accelerate the process. In subpopulations with limited pollinators, Alkanna can influence bees by using their colour-related foraging preferences to alter visitation patterns.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 427–435.     

Effects of Experience on Short‐ and Long‐term Foraging Performance in Bumblebees

Honeybees in natural settings show a gradual increase in foraging performance similar to the general pattern of lifetime performance seen in a wide variety of animals including humans. To quantify the factors contributing to such gradual increase in foraging success, we studied bumblebees foraging on pepper plants inside a greenhouse. This allowed us to combine the global measure of the net rate of food delivery to the hive with a detailed examination of bees’ performance at flowers over time. Although bees exhibited short‐term improvements in foraging ability during their first few foraging trips, we did not observe the predicted long‐term increase in performance over days. Our results suggest that a variety of flower‐handling tasks, flower choice and movements between plants can be learned quickly under the simple greenhouse settings. The long‐term increase in performance under natural settings may be caused by factors including spatial orientation and locating the best plant species, flower patches and individual plants over a large area.     

The role of pollinators in maintaining variation in flower colour in the Rocky Mountain columbine,Aquilegia coerulea

Background and Aims Flower colour varies within and among populations of the Rocky Mountain columbine, Aquilegia coerulea, in conjunction with the abundance of its two major pollinators, hawkmoths and bumble-bees. This study seeks to understand whether the choice of flower colour by these major pollinators can help explain the variation in flower colour observed in A. coerulea populations.Methods Dual choice assays and experimental arrays of blue and white flowers were used to determine the preference of hawkmoths and bumble-bees for flower colour. A test was made to determine whether a differential preference for flower colour, with bumble-bees preferring blue and hawkmoths white flowers, could explain the variation in flower colour. Whether a single pollinator could maintain a flower colour polymorphism was examined by testing to see if preference for a flower colour varied between day and dusk for hawkmoths and whether bumble-bees preferred novel or rare flower colour morphs.Key Results Hawkmoths preferred blue flowers under both day and dusk light conditions. Naïve bumble-bees preferred blue flowers but quickly learned to forage randomly on the two colour morphs when similar rewards were presented in the flowers. Bees quickly learned to associate a flower colour with a pollen reward. Prior experience affected the choice of flower colour by bees, but they did not preferentially visit novel flower colours or rare or common colour morphs.Conclusions Differences in flower colour preference between the two major pollinators could not explain the variation in flower colour observed in A. coerulea. The preference of hawkmoths for flower colour did not change between day and dusk, and bumble-bees did not prefer a novel or a rare flower colour morph. The data therefore suggest that factors other than pollinators may be more likely to affect the flower colour variation observed in A. coerulea.     

Colour association influences honey bee choice between sucrose concentrations

Certain colours associated with floral food resources are more quickly learned by honey bees (Apis mellifera) than are other colours. But the impact of colour, and other floral cues, on bee choice behaviour has not yet been determined. In these experiments, colour association and sugar concentration of reward were varied to assess how they interact to affect bee choice behaviour. Thirty-five bees were individually given binary choices between blue and yellow artificial flowers that contained either the same rewards or rewards of different sucrose concentrations. Honey bee choice between sucrose concentrations was affected by colour association and this effect was greatest when absolute difference between rewards was the lowest. The honey bee's ability to maximize energetic profitability during foraging is constrained by floral cue effectiveness.     

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.     

Trade-off between travel distance and prioritization of high-reward sites in traplining bumblebees

1.Animals exploiting renewable resource patches are faced with complex multi-location routing problems. In many species, individuals visit foraging patches in predictable sequences called traplines. However, whether and how they optimize their routes remains poorly understood.2.In this study, we demonstrate that traplining bumblebees (Bombus terrestris) make a trade-off between minimizing travel distance and prioritizing the most rewarding feeding locations.3.Individual bees trained to forage on five artificial flowers of equal reward value selected the shortest possible route as a trapline. After introducing a single highly rewarding flower to the array, they re-adjusted their routes visiting the most rewarding flower first provided the departure distance from the shortest possible route remained small (18%). When routes optimizing the initial rate of reward intake were much longer (42%), bees prioritized short travel distances.4.Under natural conditions, in which individual flowers vary in nectar productivity and replenish continuously, it might pay bees to prioritize highly rewarding locations, both to minimize the overall number of flowers to visit and to beat competitors.5.We discuss how combined memories of location and quality of resource patches could allow bees and other traplining animals to optimize their routing decisions in heterogeneous environments.     

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.     

The adaptive significance of sensory bias in a foraging context: floral colour preferences in the bumblebee Bombus terrestris

Innate sensory biases could play an important role in helping na?ve animals to find food. As inexperienced bees are known to have strong innate colour biases we investigated whether bumblebee (Bombus terrestris) colonies with stronger biases for the most rewarding flower colour (violet) foraged more successfully in their local flora. To test the adaptive significance of variation in innate colour bias, we compared the performance of colour-na?ve bees, from nine bumblebee colonies raised from local wild-caught queens, in a laboratory colour bias paradigm using violet (bee UV-blue) and blue (bee blue) artificial flowers. The foraging performance of the same colonies was assessed under field conditions. Colonies with a stronger innate bias for violet over blue flowers in the laboratory harvested more nectar per unit time under field conditions. In fact, the colony with the strongest bias for violet (over blue) brought in 41% more nectar than the colony with the least strong bias. As violet flowers in the local area produce more nectar than blue flowers (the next most rewarding flower colour), these data are consistent with the hypothesis that local variation in flower traits could drive selection for innate colour biases.     

Use of Flower Color-Cue Memory by Honey Bee Foragers Continues when Rewards No Longer Differ between Flower Colors

Honey bees (Hymenoptera: Apidae) were used as a model insect system to explore forager use of a learned color-cue memory over several subsequent days. Experiments used artificial flower patches of blue and white flowers. Two experiments were performed, each beginning with a learning experience where 2 M sucrose was present in one flower color and 1 M sucrose in the alternative flower color. The first experiment followed flower color fidelity over a series of sequential days when rewards no longer differed between flowers of different color. The second examined the effect of intervening days without the forager visiting the flower patch. Results showed that color-cue memory decline was not a passive time-decay process and that information update in honey bees does not occur readily without new experiences of difference in rewarding flowers. Further, although the color cue learned was associated with nectar reward in long term memory, it did not seem to be specifically associated with the 2 M sucrose nectar reward when intervening nights occurred between learning and revisiting the flower patch.     

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.     

Where have all the blue flowers gone: pollinator responses and selection on flower colour in New Zealand Wahlenbergia albomarginata

Although pollinators are thought to select on flower colour, few studies have experimentally decoupled effects of colour from correlated traits on pollinator visitation and pollen transfer. We combined selection analysis and phenotypic manipulations to measure the effect of petal colour on visitation and pollen export at two spatial scales in Wahlenbergia albomarginata. This species is representative of many New Zealand alpine herbs that have secondarily evolved white or pale flowers. The major pollinators, solitary bees, exerted phenotypic selection on flower size but not colour, quantified by bee vision. When presented with manipulated flowers, bees visited flowers painted blue to resemble a congener over white flowers in large, but not small, experimental arrays. Pollen export was higher for blue flowers in large arrays. Pollinator preference does not explain the pale colouration of W. albomarginata, as commonly hypothesized. Absence of bright blue could be driven instead by indirect selection of correlated characters.     

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     

Odour and colour information in the foraging choice behaviour of the honeybee

1. Honeybees Apis mellifera ligustica were trained to work on a patch with artificial rewarding and non-rewarding flowers, coupled to an air extractor. The perceptual colour distance between the rewarding and the non-rewarding flowers was varied and the flower choice and the repellent scent-marking behaviour of the bees were recorded. 2. The discrimination between rewarding and non-rewarding flowers depended on their colour distance, improving with a greater colour difference. This task was guided thus visually and was not affected by activating the air extractor. 3. The scent-marking activity was only observable when the colour information of both groups of flowers was the same or very similar. This thus represents the first reported case of a modulation of an olfactory activity through the visual input provided by colour distances. When the air extractor was activated, rejections associated with the scent-marking behaviour disappeared, thus confirming the olfactory nature of this behaviour. 4. Honeybees are thus capable of using one or more sensory cues to enhance their foraging efficiency, according to the environmental situation. This great plasticity allows them to attain an enhanced efficiency while foraging. 5. We successfully applied the model of colour choice behaviour of the honeybee. Since the original theory was developed for Apis mellifera carnica, this work also constitutes the first attempt to describe the behaviour of the honeybee race, Apis mellifera ligustica, using the postulated model, and reaffirms thus its generality.     

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.     

Floral Temperature and Optimal Foraging: Is Heat a Feasible Floral Reward for Pollinators?

As well as nutritional rewards, some plants also reward ectothermic pollinators with warmth. Bumble bees have some control over their temperature, but have been shown to forage at warmer flowers when given a choice, suggesting that there is some advantage to them of foraging at warm flowers (such as reducing the energy required to raise their body to flight temperature before leaving the flower). We describe a model that considers how a heat reward affects the foraging behaviour in a thermogenic central-place forager (such as a bumble bee). We show that although the pollinator should spend a longer time on individual flowers if they are warm, the increase in total visit time is likely to be small. The pollinator's net rate of energy gain will be increased by landing on warmer flowers. Therefore, if a plant provides a heat reward, it could reduce the amount of nectar it produces, whilst still providing its pollinator with the same net rate of gain. We suggest how heat rewards may link with plant life history strategies.