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.     

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.     

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.     

The influence of reward sequence on flight directionality in bees

Honeybees (Apis mellifera L.) were trained to collect food from arrays of artificial flowers. Experiments were carried out to investigate how different sequences of rewards (sugar solution) affect the flight directionality in the next inter-flower move (i.e. the tendency to keep to the same direction as in the preceding flight). In the texts, bees could visit a row of four or five flowers. At the end of the row, bees were given a choice of direction for their next flight (i.e. forward, left, right, or backward). I investigated the effect of a reward sequence in relation to (1) the average amount of ‘nectar’ gathered in the last few flower visits, regardless of the sequence of occurrence, or to (2) the reward received in the most recent flower visits. A reward given at the choice point itself reduced flight directionality. Effects of rewards offered on preceding flowers, i.e. one, two, or three steps before the choice point, were not significant. There was, however, evidence for their additional effect. It is concluded that the influence of a reward on flight directionality vanishes rapidly as more flower visits are made.     

Risk‐averse inflorescence departure in hummingbirds and bumble bees: could plants benefit from variable nectar volumes?

Most hermaphroditic, many-flowered plants should suffer reduced fitness from within-plant selfing (geitonogamy). Large inflorescences are most attractive to pollinators, but also promote many flower visits during a single plant visit, which may increase selfing and decrease pollen export. A plant might avoid the negative consequences of attractiveness through modification of the floral display to promote fewer flower visits, while retaining attractiveness. This report shows that increasing only the variance in nectar volume per flower results in fewer flower visits per inflorescence by wild hummingbirds ( Selasphorus rufus ) and captive bumble bees ( Bombus flavifrons ) foraging on artificial inflorescences. Inflorescences were either constant (all flowers contained the same nectar volume) or variable (half the flowers were empty, the other half contained twice as much nectar as in the constant flowers). Both types of inflorescence were simultaneously available to foragers. Risk-averse foraging behaviour was expressed as a patch departure preference: birds and bees visited fewer flowers on variable inflorescences, and this preference was expressed when resource variability could be determined only by concurrent sampling. When variance treatments were clearly labelled with colour and offered to hummingbirds, the departure effect was maintained; however, when preference was measured by inflorescence choice, birds did not consistently prefer to visit constant inflorescences. The reduced visitation lengths on variable inflorescences by both birds and bees documented in this study imply that variance in nectar production rates within inflorescences may represent an adaptive trait to avoid the costs of geitonogamy.     

Changes in food source profitability affect Nasonov gland exposure in honeybee foragers Apis mellifera L.

Summary. When arriving at a known artificial food source, foraging honeybees usually perform circular flights around the feeding place prior to landing. During these flights bees expose their Nasonov gland, an exocrine gland located at the base of the 7^th tergum, that releases a complex blend of volatiles. This behavior may continue even after the bee starts food ingestion. The proportion of bees exposing the Nasonov gland and the duration of its exposure before and during feeding for individual bees were quantified. Trained bees collected sugar solution during 12 visits from a feeder located at 160 m from the hive. Five different reward programs were presented: three constant and two variable. The constant programs offered 0.6, 1.2 or 2.4 M sugar for all 12 visits, while the variable programs delivered either 0.6, 1.2, 0.6 M or 0.6, 2.4, 0.6 M, four visits for each molarity. Results showed that sugar concentration changed the thresholds and durations of Nasonov gland exposure. However, this relationship was found only for Nasonov exposure before bees began to feed. During feeding, a protruded Nasonov gland was only observed for bees that had exposed it prior to feeding; suggesting that Nasonov gland exposure before feeding is a releaser of the during-feeding exposure. In variable reward programs, changes in sugar concentration were followed by changes in both thresholds and durations of exposure. However, Nasonov gland exposure during feeding did not appear to decrease based on measurements of the low profitability during the current foraging visit. These results suggest that Nasonov gland exposure is programmed on the basis of reward expectations, with the bees having acquired this information in the previous foraging visits to the food source.     

Trophallaxis in the honeybee Apis mellifera (L.): the interaction between flow of solution and sucrose concentration of the exploited food sources

Forager bees arriving at the hive after visiting a nectar source, unload the collected liquid food to recipient hivemates through mouth-to-mouth contact (trophallaxis). We analysed whether the main characteristics that define nectar in energetic terms, that is, rate of production (flow of solution), sucrose concentration and rate of sucrose production (sucrose flow) influence trophallactic behaviour. Individual bees trained to feed at a regulated-flow feeder offering sucrose solution were captured once the foraging visit was complete and placed in an acrylic arena with a recipient bee that had not been fed. The rate at which liquid was transferred during the subsequent trophallactic contact (transfer rate) was analysed as a function of the different solution flows and sucrose concentrations offered at the feeder. A relationship was found between transfer rate during trophallaxis and the flow of solution previously presented at the feeder. This relationship was independent of sucrose concentration when above a certain threshold value (ca. 22% weight on weight). We also analysed whether the rate of sucrose deliverance of the food source (sucrose flow) influenced the rate at which the solution was transferred. No clear relationship was found between the rate of sucrose deliverance during trophallactic events (sucrose transfer rate) and the sucrose flow presented at the feeder. The possibility that trophallaxis could be a communication channel through which quantitative information on food source profitability is transmitted among hivemates is discussed. Copyright 2000 The Association for the Study of Animal Behaviour.     

Individual recruitment in honeybees, <Emphasis Type="Italic">Apis mellifera</Emphasis> L.

The recruitment of honeybee foragers individually exploiting a low-flow rate-feeder that presented different temporal reward programs was experimentally analyzed. By capturing hive bees that landed at the feeder in a 2-h period, the arrival rate of incoming bees could be obtained. With this procedure we quantitatively analyzed the maximum number of hive bees that can be brought to the feeding station by single foragers. Test bees collected sucrose solution during 12 visits to a rate-feeder located 160 m from the hive. The constant programs offered 0.6, 1.2, or 2.4 M sugar for all 12 visits, while the variable programs delivered either 0.6, 1.2, or 0.6 M or 0.6, 2.4, or 0.6 M, with four visits for each molarity. Results showed that the sucrose concentration exploited by single foragers increased the arrival rate. Moreover, there was a linear relationship within this range of sucrose concentrations that presented a slope of 1.58. Since the sugar solutions were provided at the same flow rate (5 μl/min) in all the programs, the arrival rate expressed in terms of sucrose flow rate (milligrams of sucrose/minute) shows that one additional incoming bee per hour arrived when the single forager assessed an increase in the sucrose flow rate of 0.75 mg sucrose/min at the rate-feeder. The absence of differences in the frequency of visits of the single foragers during the constant programs suggests that the differences observed in the arrival rate can mainly be explained by a more intensive display of the recruitment mechanisms performed per foraging trip instead of by their iterativeness throughout different foraging cycles. Variable reward programs showed that arrival rate is rapidly adjusted according to the reward change and is independent of its magnitude. Received in revised form: 17 August 2001 Electronic Publication     

Oxygen consumption in the foraging honeybee depends on the reward rate at the food source

Oxygen consumption of the honeybee Apis mellifera ligustica was measured as a function of the flow rate supply of sucrose solution at an automatic feeder located inside a respirometric chamber. Trained bees freely entered the respirometric chamber and collected the sucrose solution supplied. The mean value of the O₂ consumption rate per visit increased with the sucrose flow rate, and for a given flow rate, with increasing locomotor activity. However, when no locomotor activity was displayed, O₂ consumption also increased with increasing nectar flow rate. Crop load attained at the end of the visit showed a positive relationship with the nectar flow rate; however, for a given flow rate, O₂ consumption showed either no correlation or a negative one with the final crop load attained. It is concluded that the energy expenditure of the foraging bee is controlled by a motivational drive whose intensity depends on the reward rate at the food source. Accepted: 30 July 1996     

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.     

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.     

Selective choice of sucrose solution concentration by the hovering hawk mothMacroglossum stellatarum

To determine the preference of the hovering hawk mothMacroglossum stellatarum for different sugar concentrations, the foraging behavior of adults were analyzed under laboratory conditions. Six sucrose concentrations (range, 10–60%, w/w) were simultaneously offered in six artificial ab libitum feeders. The number of feeding bouts and the duration of each visit were automatically recorded and stored in a computer. Results showed that the frequency of visits to the feeders did not vary among the different solutions offered, but the gathered volume by the group attained a maximum at between 20 and 50% (w/w). Moths invested more time in front of the feeder with the more concentrated sugar solutions. It was assumed that factors different from maximizing energy intake, such as water balance and viscosity of concentrated nectars, have to be considered in order to understand the observed patterns of nectar choice.     

Motivational state and reward content determine choice behavior under risk in mice

Risk is a ubiquitous feature of the environment for most organisms, who must often choose between a small and certain reward and a larger but less certain reward. To study choice behavior under risk in a genetically well characterized species, we trained mice (C57BL/6) on a discrete trial, concurrent-choice task in which they must choose between two levers. Pressing one lever (safe choice) is always followed by a small reward. Pressing the other lever (risky choice) is followed by a larger reward, but only on some of the trials. The overall payoff is the same on both levers. When mice were not food deprived, they were indifferent to risk, choosing both levers with equal probability regardless of the level of risk. In contrast, following food or water deprivation, mice earning 10% sucrose solution were risk-averse, though the addition of alcohol to the sucrose solution dose-dependently reduced risk aversion, even before the mice became intoxicated. Our results falsify the budget rule in optimal foraging theory often used to explain behavior under risk. Instead, they suggest that the overall demand or desired amount for a particular reward determines risk preference. Changes in motivational state or reward identity affect risk preference by changing demand. Any manipulation that increases the demand for a reward also increases risk aversion, by selectively increasing the frequency of safe choices without affecting frequency of risky choices.     

Olfactory conditioning of the proboscis extension in bumble bees

The foraging behaviour of bumble bees is well documented for nectar and/or pollen gathering, but little is known about the learning processes underlying such behaviour. We report olfactory conditioning in worker bumble bees Bombus terrestris L. (Hymenoptera: Apidae) obtained under laboratory conditions on restrained individuals. The protocol was adapted from the proboscis extension conditioning previously described in the honey bee Apis mellifera L. Bumble bees were found to be able to learn a pure odorant when it was presented in paired association with a sugar reward, but not when odour and reward were presented in an explicitly unpaired procedure. This suggests an associative basis for this olfactory learning. Bumble bees showed similar conditioning abilities when stimulated with two different floral odours. An effect of the sugar reward concentration on the learning performances was found.     

Inter‐individual variation in honey bee dance intensity correlates with expression of the foraging gene

Individual behavioural differences in responding to the same stimuli is an integral part of division of labour in eusocial insect colonies. Amongst honey bee nectar foragers, individuals strongly differ in their sucrose responsiveness, which correlates with strong differences in behavioural decisions. In this study, we explored whether the mechanisms underlying the regulation of foraging are linked to inter‐individual differences in the waggle dance activity of honey bee foragers. We first quantified the variation in dance activity amongst groups of foragers visiting an artificial feeder filled consecutively with different sucrose concentrations. We then determined, for these foragers, the sucrose responsiveness and the brain expression levels of three genes associated with food search and foraging; the foraging gene Amfor, octopamine receptor gene AmoctαR1 and insulin receptor AmInR‐2. As expected, foragers showed large inter‐individual differences in their dance activity, irrespective of the reward offered at the feeder. The sucrose responsiveness correlated positively with the intensity of the dance activity at the higher reward condition, with the more responsive foragers having a higher intensity of dancing. Out of the three genes tested, Amfor expression significantly correlated with dance activity, with more active dancers having lower expression levels. Our results show that dance and foraging behaviour in honey bees have similar mechanistic underpinnings and supports the hypothesis that the social communication behaviour of honey bees might have evolved by co‐opting behavioural modules involved in food search and foraging in solitary insects.     

Reversal Learning and Risk‐Averse Foraging Behavior in the Monarch Butterfly,Danaus plexippus (Lepidoptera: Nymphalidae)

Learning ability allows insects to respond to a variable environment, and to adjust their behaviors in response to positive or negative experiences. Pollinating insects readily learn to associate floral characteristics, such as color, shape, or pattern, with appetitive stimuli, such as the presence of a nectar reward. However, in nature pollinators may also encounter flowers that contain distasteful or toxic nectar, or offer highly variable nectar volumes, providing opportunities for aversive learning or risk‐averse foraging behavior. Whereas some bees learn to avoid flowers with unpalatable or unreliable nectar rewards, little is known about how Lepidoptera respond to such stimuli. We used a reversal learning paradigm to establish that monarch butterflies learn to discriminate against colored artificial flowers that contain salt solution, decreasing both number of probes and probing time on flowers of a preferred color and altogether avoiding artificial flowers of a non‐preferred color. In addition, when we offered butterflies artificial flowers of two different colors, both of which contained the same mean nectar volume but which differed in variance, the monarchs exhibited risk‐averse foraging: they probed the constant flowers significantly more than the variable ones, regardless of flower color or butterfly sex. Our results add to our understanding of butterfly foraging behavior, as they demonstrate that monarchs can respond to aversive as well as appetitive stimuli, and can also adjust their foraging behavior to avoid floral resources with high variance rewards.     

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.     

Complex memories in honeybees: can there be more than two?

Foraging honeybees are likely to learn visual and chemical cues associated with many different food sources. Here, we explore how many such sources can be memorized and recalled. Marked bees were trained to visit two (or three) sugar feeders, each placed at a different outdoor location and carrying a different scent. We then tested the ability of the bees to recall these locations and fly to them, when the training scents were blown into the hive, and the scents and food at the feeders were removed. When trained on two feeder locations, each associated with a different scent, the bees could correctly recall the location associated with each scent. However, this ability broke down when the number of scents and feeder locations was increased to three. Performance was partially restored when each of the three training feeders was endowed with an additional cue, namely, a distinct colour. Our results suggest that bees can recall a maximum of two locations when each is associated with a different scent. However, this number can be increased if the scent cues are augmented by visual cues. These findings have implications for the ways in which associations are established and laid down in honeybee memory.     

Behavioural correlate of choice confidence in a discrete trial paradigm

How animals make choices in a changing and often uncertain environment is a central theme in the behavioural sciences. There is a substantial literature on how animals make choices in various experimental paradigms but less is known about the way they assess a choice after it has been made in terms of the expected outcome. Here, we used a discrete trial paradigm to characterise how the reward history shaped the behaviour on a trial by trial basis. Rats initiated each trial which consisted of a choice between two drinking spouts that differed in their probability of delivering a sucrose solution. Critically, sucrose was delivered after a delay from the first lick at the spouts--this allowed us to characterise the behavioural profile during the window between the time of choice and its outcome. Rats' behaviour converged to optimum choice, both during the acquisition phase and after the reversal of contingencies. We monitored the post-choice behaviour at a temporal precision of 1 millisecond; lick-response profiles revealed that rats spent more time at the spout with the higher reward probability and exhibited a sparser lick pattern. This was the case when we exclusively examined the unrewarded trials, where the outcome was identical. The differential licking profiles preceded the differential choice ratios and could thus predict the changes in choice behaviour.     

Haemolymph sugars and the control of the proventriculus in the honey bee Apis mellifera

Crop emptying and rectal filling rates were investigated in bees trained to collect defined amounts of sucrose solution. Crop emptying rates strongly depended on the sucrose concentration of the collected solution. There was a close match between the energy expenditure of the bees and the amount of sucrose transported through the proventriculus, irrespective of the fluid dilution. Results indicated that the controlling variable was the amount of sucrose flowing through the proventriculus rather than the volume flow. In order to distinguish between haemolymph osmolality and haemolymph carbohydrate levels as factors controlling the activity of the proventriculus, bees were injected with either metabolizable or non-metabolizable carbohydrates. Only the injection of metabolizable carbohydrates modulated the activity of the proventriculus, indicating that the titers of metabolizable carbohydrates are involved in the feedback loop controlling crop emptying, and that haemolymph osmolality alone does not influence the activity of the proventriculus.