Artificial Flower Patches Research Articles

Low Strength Magnetic Fields Serve as a Cue for Foraging Honey Bees but Prior Experience is More Indicative of Choice

Species of migrating insects use magnetic fields as a navigational tool that is independent of current weather conditions and non-migrating species have been shown to discriminate anomalies in magnetic field from the earth's baseline. Honey bee discrimination of magnetic field has been studied in the context of associative learning, physiology, and whole hive responses. This article uses a combination of free-flight and laboratory studies to determine how small fluctuations from Earth's magnetic field affect honey bee (Apis mellifera L.) decision-making. Honey bees were tested in three experiments: (i) recruitment to an aqueous sucrose feeder, (ii) an artificial free-flight flower patch with floral color-dependent magnetic field strength, and (iii) a Y-maze with alternating colors on a stronger magnetic field. In free-flying feeder experiments, magnetic field served as a temporary cue, but when offered an equal caloric alternative with lesser magnetic field, the latter was preferred. Flower patch experiments showed initial color biases that were abandoned as a response to magnetic field induction. In laboratory experiments, bees showed a color-dependent behavioral response to the magnetic field. The results of this study indicate that bees may use small fluctuations in magnetic fields as a cue but that it is likely low-value as compared with other stimuli. Bioelectromagnetics. 2020;41:458-470. © 2020 Bioelectromagnetics Society.

A cognitive analysis of deceptive pollination: associative mechanisms underlying pollinators\u2019 choices in non-rewarding colour polymorphic scenarios

Intraspecific floral colour polymorphism is a common trait of food deceptive orchids, which lure pollinators with variable, attractive signals, without providing food resources. The variable signals are thought to hinder avoidance learning of deceptive flowers by pollinators. Here, we analysed the cognitive mechanisms underlying the choice of free-flying stingless bees Scaptotrigona aff. depilis trained to visit a patch of artificial flowers that displayed the colours of Ionopsis utricularioides, a food deceptive orchid. Bees were trained in the presence of a non-rewarding colour and later tested with that colour vs. alternative colours. We simulated a discrete-polymorphism scenario with two distinct non-rewarding test colours, and a continuous-polymorphism scenario with three non-rewarding test colours aligned along a chromatic continuum. Bees learned to avoid the non-rewarding colour experienced during training. They thus preferred the novel non-rewarding colour in the discrete-polymorphic situation, and generalized their avoidance to the adjacent colour of the continuum in the continuous-polymorphism situation, favouring thereby the most distant colour. Bees also visited less flowers and abandoned faster a non-rewarding monomorphic patch than a non-rewarding polymorphic patch. Our cognitive analyses thus reveal that variable deceptive orchids disrupt avoidance learning by pollinators and exploit their generalization abilities, which make them favour distinct morphs.

From a sequential pattern, temporal adjustments emerge in hummingbird traplining.

Animals that feed from resources that are constant in space and that refill may benefit from repeating the order in which they visit locations. This is a behavior known as traplining, a spatial phenomenon. Hummingbirds, like other central-place foragers, use short traplines when moving between several rewarding sites. Here we investigated whether traplining hummingbirds also use relevant temporal information when choosing which flowers to visit. Wild rufous hummingbirds that were allowed to visit 3 artificial flower patches in which flowers were refilled 20 min after they had been depleted repeated the order in which they visited the 3 patches. Although they tended to visit the first 2 patches sooner than 20 min, they visited the third patch at approximately 20-min intervals. The time between visits to the patches increased across the experiment, suggesting that the birds learned to wait longer before visiting a patch. The birds appeared to couple the sequential pattern of a trapline with temporal regularity, to some degree. This suggests that there is a temporal component to the repeated spatial movements flown by foraging wild hummingbirds.

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.

The effects of ingested aqueous aluminum on floral fidelity and foraging strategy in honey bees (Apis mellifera)

Pollinator decline is of international concern because of the economic services these organisms provide. Commonly cited sources of decline are toxicants, habitat fragmentation, and parasites. Toxicant exposure can occur through uptake and distribution from plant tissues and resources such as pollen and nectar. Metals such as aluminum can be distributed to pollinators and other herbivores through this route especially in acidified or mined areas. A free-flying artificial flower patch apparatus was used to understand how two concentrations of aluminum (2mg/L and 20mg/L) may affect the learning, orientation, and foraging behaviors of honey bees (Apis mellifera) in Turkey. The results show that a single dose of aluminum immediately affects the floral decision making of honey bees potentially by altering sucrose perception, increasing activity level, or reducing the likelihood of foraging on safer or uncontaminated resource patches. We conclude that aluminum exposure may be detrimental to foraging behaviors and potentially to other ecologically relevant behaviors.

Stingless bees (Melipona scutellaris) learn to associate footprint cues at food sources with a specific reward context.

Foraging insects leave chemical footprints on flowers that subsequent foragers may use as indicators for recent flower visits and, thus, potential resource depletion. Accordingly, foragers should reject food sources presenting these chemical cues. Contrasting this assumption, experimental studies in stingless bees (Apidae, Meliponini), so far, demonstrated an attractive effect of footprints. These findings lead to doubts about the meaning of these chemical cues in natural foraging contexts. Here, we asked whether foragers of stingless bees (Melipona scutellaris) use footprints according to the previously experienced reward level of visited food sources. Bees were trained to artificial flower patches, at which the reward of a flower either decreased or, alternatively, increased after a visit by a forager. Individuals were allowed a total of nine foraging bouts to the patch, after which their preference for visited or unvisited flowers was tested. In the choice tests, bees trained under the decreasing reward context preferred unvisited flowers, whereas individuals trained under the increasing reward context preferred visited flowers. Foragers without experience chose randomly between visited and unvisited flowers. These results demonstrate that M. scutellaris learns to associate unspecific footprint cues at food sources with differential, specific reward contexts, and uses these chemical cues accordingly for their foraging decisions.

Conditional discrimination and response chains by worker bumblebees (Bombus impatiens Cresson, Hymenoptera: Apidae).

We trained worker bumblebees to discriminate arrays of artificial nectaries (one, two, and three microcentrifuge tubes inserted into artificial flowers) from which they could forage in association with their location in a three-compartmental maze. Additionally, we challenged bees to learn to accomplish three different tasks in a fixed sequence during foraging. To enter the main three-compartmented foraging arena, they had first to slide open doors in an entry box to be able to proceed to an artificial flower patch in the main arena where they had to lift covers to the artificial nectaries from which they then fed. Then, the bees had to return to the entrance way to their hive, but to actually enter, were challenged to rotate a vertically oriented disc to expose the entry hole. The bees were adept at associating the array of nectaries with their position in the compartmental maze (one nectary in compartment one, two in two, and three in three), taking about six trials to arrive at almost error-free foraging. Over all it took the bees three days of shaping to become more or less error free at the multi-step suite of sequential task performances. Thus, they had learned where they were in the chain sequence, which array and in which compartment was rewarding, how to get to the rewarding array in the appropriate compartment, and finally how to return as directly as possible to their hive entrance, open the entrance, and re-enter the hive. Our experiments were not designed to determine the specific nature of the cues the bees used, but our results strongly suggest that the tested bees developed a sense of subgoals that needed to be achieved by recognizing the array of elements in a pattern and possibly chain learning in order to achieve the ultimate goal of successfully foraging and returning to their colony. Our results also indicate that the bees had organized their learning by a hierarchy as evidenced by their proceeding to completion of the ultimate goal without reversing their foraging paths so as to return to the colony without food.

Time–place learning in wild, free-living hummingbirds

Animals can learn to revisit locations at which foraging resources will renew over time. This ability is known as ‘time–place’ learning. Although there is clear evidence for time–place learning from animals trained and tested in the laboratory, not all species learn time–place tasks with similar ease. Since hummingbirds feed from food sources that are constant in space and that renew with time, it seems plausible these birds might learn time–place associations and do so readily. Here, then, we tested whether wild, free-living rufous hummingbirds, Selasphorus rufus , could learn the time and place at which four artificial flower patches were rewarded. Flowers in each of the four patches contained reward for only 1 h each day but the time and sequence in which patches were rewarded were repeated across days. Most birds learned when to visit each patch. To determine whether the birds used ordinal or circadian timing to choose the correct patch at the correct time, we ended the experiment with a single test trial in which we presented the patches (all flowers empty) only at the fourth hour of the day. The birds visited neither the patch that was normally rewarded first (daily ordinal timing) nor the fourth patch (time of day). These results suggest that the time component of the time–place learning in these birds requires both ordinal and circadian information.

Effect of flower visual angle on flower constancy: a test of the search image hypothesis

Pollinators often sequentially visit 1 flower type while bypassing other equally rewarding flower types, behavior known as flower constancy. One explanation for flower constancy is that pollinators use the search image of a specific flower type to efficiently find flowers because they are often cryptic. The so-called search image hypothesis predicts that temporal specialization to 1 flower type by an individual pollinator declines as flower conspicuousness increases because if flowers are conspicuous, pollinators can divide their attention among different flower types. To test this prediction, we investigated visitation sequences of individual bumble bees (Bombus ignitus) to a patch of blue and yellow artificial flowers. We used different flower sizes and interflower distances as independent determinants of flower visual size and noisiness of the background and, thus, of flower crypsis. Flower color selectivity and flower search time decreased and subsequently increased with visual size of the nearest flowers, with a minimum of approximately 15° of the visual angle. Within-bout constancy, measured as the tendency of flying to the same flower types in succession compared with the expectation of a given flower selectivity within a bout, increased with visual size of the nearest flowers. Flower selectivity and within-bout constancy did not differ among arrays that shared the same floral visual angle, indicating that visual size, rather than flight distance or flower size itself, had a substantial effect on flower choices. Our results suggest that flower visual size and background noisiness affect flower crypsis and constancy, providing support for the search image hypothesis.

Relationship between Spatial Working Memory Performance and Diet Specialization in Two Sympatric Nectar Bats

Behavioural ecologists increasingly recognise spatial memory as one the most influential cognitive traits involved in evolutionary processes. In particular, spatial working memory (SWM), i.e. the ability of animals to store temporarily useful information for current foraging tasks, determines the foraging efficiency of individuals. As a consequence, SWM also has the potential to influence competitive abilities and to affect patterns of sympatric occurrence among closely related species. The present study aims at comparing the efficiency of SWM between generalist (Glossophaga soricina) and specialist (Leptonycteris yerbabuenae) nectarivorous bats at flowering patches. The two species differ in diet – the generalist diet including seasonally fruits and insects with nectar and pollen while the specialist diet is dominated by nectar and pollen yearlong – and in some morphological traits – the specialist being heavier and with proportionally longer rostrum than the generalist. These bats are found sympatrically within part of their range in the Neotropics. We habituated captive individuals to feed on artificial flower patches and we used infrared video recordings to monitor their ability to remember and avoid the spatial location of flowers they emptied in previous visits in the course of 15-min foraging sequences. Experiments revealed that both species rely on SWM as their foraging success attained significantly greater values than random expectations. However, the nectar specialist L. yerbabuenae was significantly more efficient at extracting nectar (+28% in foraging success), and sustained longer foraging bouts (+27% in length of efficient foraging sequences) than the generalist G. soricina. These contrasting SWM performances are discussed in relation to diet specialization and other life history traits.

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.

Different solutions by bees to a foraging problem

Honeybees ( Apis mellifera ) were used as a model insect system to explore how foragers solve problems involving cost as well as reward. Reward difference was created by varying sucrose molarity, whereas cost difference was created by varying flower-handling time in artificial flower patches. Unlike earlier work, flower-handling time was a function of stamen length rather than corolla length, such that longer stamens increased flower-handling time. When changing from short- to long-stamen flowers, access to nectar becomes limited to specific routes, which differ in difficulty. Experiments were performed with 2 μl and 6 μl sucrose rewards. Differences in reward and/or handling time were associated with flower colour difference (blue versus white flowers). Higher energy reward (2 M) and shorter handling time were preferred by bees when foraging problems involved only a reward or a handling-time difference, which followed energy maximization expectations. However, when the two variables were combined so that greater handling time was combined with higher reward, behaviour differed between individuals. Some bees made choices based solely on reward, some only on effort (handling time), and some simply on flower colour. These results contrast with early work where handling time was a function of corolla length and all bees avoided longer corollas. Results suggest that honeybees do not always behave as predicted by simple energy maximization principles; rather, individuality in choice arises when the foraging problem becomes more difficult because of increased complexity (dimensionality) of the problem.

Floral reward production is timed by an insect pollinator

Interval timing--sensitivity to elapsing durations--has recently been found to occur in an invertebrate pollinator, the bumble-bee (Bombus impatiens). Here, bumble-bees were required to time the interval between the start of foraging in a patch of low-quality artificial flowers providing 25% sucrose and the availability of a high-quality flower (HQF) that provided 50% sucrose after a fixed delay. The delay changed after every 20 foraging bouts in the order 30-150-30 s. Bees visited the HQF sooner when the delay was 30 s than when it was 150 s, and visits to the HQF peaked near the end of both delays. When the delay changed to 150 s, bees appeared to time both the previous 30 s delay and the new delay. To examine whether bees also learned what kind of reward was provided at the HQF, its usual reward was replaced with 25% sucrose in a final foraging bout. Bumble-bees rejected the HQF on the reward-replacement test. These results show that bumble-bees remembered both when reward was produced by the HQF and what type of reward was produced. These findings indicate that bumble-bees can learn both the timing and content of reward production.

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

AbstractFree 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.

The effect of intrinsic and extrinsic factors on flower constancy in stingless bees

To enhance our understanding of the variability of flower constancy, we studied the influence of foraging conditions on the level of individual constancy in two species of stingless bees, Trigona dorsalis and Oxytrigona mellicolor, using a dimorphic artificial flower patch with equal reward in both flower types. Flower constancy increased greatly when the flower types were more dissimilar, and then approached constancy levels found for European honey bees. Sugar concentration had little effect on flower constancy. The presence of nestmates enhanced flower constancy somewhat in O. mellicolor but not in T. dorsalis, probably because of species-specific differences in local enhancement. The individual variability within treatments could be explained partly by individual variation in foraging tempo, with faster foraging leading to higher flower constancy. flower constancy / foraging conditions / stingless bee

Africanized honey bee response to differences in reward frequency

SUMMARYDifferences in predation pressure and floral resources exist among the endemic ranges of Apis mellifera subspecies. Those environmental differences should select for heterogeneity in forager flower fidelity among honey bee subspecies, particularly when reward frequency differences are associated with competing flower types. We tested that evolutionary model by examining the foraging behaviour of Africanized honey bees (AHB), and by comparing our observations with those recorded for Italian (A. m. ligustica) and Caucasian honey bees (A. m. caucasica). The response of AHB (A. m. scutel- lata hybrid/introgressant) to reward frequency differences among flower colours was examined using artificial flower patches. Each patch contained blue, white, and yellow flowers. When rewards offered by all three flower- morphs were identical, some foragers restricted visitation to blue and white flowers, while others showed fidelity to yellow flowers. Bees visiting blue and white flowers did not show a preference for either the blue or white colour morph under those conditions. However, forager behaviour changed when they were presented with different reward frequencies associated with the alternative flower colours. Bees frequenting blue and white flowers favoured blue when it offered a reward more frequently than white, and favoured white when the reverse was true. That behaviour occurred not only when the more frequently rewarding flower colour offered a higher harvest rate, but also when harvest rates obtained from all flower colours were equal. A change in flower colour fidelity involving yellow vs. blue and white flowers was observed only when reward frequency difference was linked to maximizing harvest rate. Those results contrast sharply to reported A. m. ligustica and A. m. caucasica honey bee behaviour: neither Italian nor Caucasian bees respond to reward frequency differences among flower colours, even between blue and white flowers.

Floral constancy in Trigona stingless bees foraging on artificial flower patches: a comparative study

SUMMARYFlower constancy is described qualitatively and quantitatively for stingless bees (Apidae, Meliponinae). Flower constancy has been reported for various insects, but the degree of constancy seems to differ from species to species. To test the hypotheses that the degree of flower constancy depends on colony size and foraging strategy, flower constancy was measured in three species of stingless bees that differed in colony size and foraging strategies. When the artificial flower types differed in colour or odour, most bees preferred one of the two flower types. On average, 77% of successive visits were directed towards the previously visited flower type without major differences between the species. Constancy on odour was not generally overruled by constancy on colour or vice versa. When flower types differed in shape, the majority of the bees visited the two types in a random way. Thus, differences in colony size and foraging strategy did not relate to flower choice performance in the Trigona species. The degree of flower constancy in the stingless bee species studied was lower than that reported for European honey bees (Apis mellifera), but comparable with that reported for Asian honey bees (Apis cerana). We hypothesize that bees of tropical climates will be generally less constant than bees of temperate climates, due to different (environmentally imposed) optimal foraging strategies.

Spontaneous flower constancy and learning in honey bees as a function of colour

When presented with an artificial flower patch of blue and yellow pedicellate flowers, individual honey bees,Apis melliferaL., became constant to one of the two flower colours, rarely even sampling the alternative colour. Some bees visited only blue flowers while others visited only yellow flowers. This paper describes the onset of constancy for bees that had had no experience with the experimental apparatus. In 3020 visits, bees failed to land on or drink from the flower colour on which they first landed only 17 times. This behaviour was not modified by quality or quantity of reward, training to the experimental site, group effects or presence of odour during trials. However, when we trained bees to a target painted with two colours and then forced them to sample monomorphic flower patches in sequence, all bees visited the only colour present: yellow or blue. When we subsequently offered these same bees yellow and blue flowers simultaneously (rewarded choices), they became constant. Eleven of 23 bees showed constancy to the less rewarding flower morph without even sampling the alternative. Those bees failed to sample even though they had previously been forced to visit the alternative flower morph, which offered a reward with twice the calories/volume. Constancy is thus spontaneous in honey bees, but it can be hidden by some experimental protocols designed to study learning.

Movement Patterns of Honeybee Foragers: Motivation and Decision Rules Dependent On the Rate of Reward

[The movement pattern of honeybees Apis mellifera working on a patch of artificial flowers and its dependence on food-source profitability were analysed by varying the flow rate of sucrose solution provided by a set of artificial flowers. Three sucrose flow rates were used (0.085, 0.17 and 0.34 μl/min per flower) and twenty bees per flow rate were measured over one entire visit to the patch. It is shown that 1) bees had the same landing rate at the lower and the intermediate flow rates but foraged significantly faster at the higher flow rate. 2) For the three flow rates tested, the landing rate remained constant throughout the entire foraging visit, thus being unaffected by the progressive increase in the weight transported in the crop. 3) Only the probability of an immediate return to a previously visited flower significantly increased with the flow rate. Such immediate returns occurred whenever the reward experienced at a flower greatly surpassed the mean reward expectation per flower. 4) However, bees returning immediately to the last visited flower did not find reward in it. It is suggested that bees go faster when the offer becomes better as a result of an increase in the foraging motivation that would lead to an incitement of foraging movements and that the progressive increase in the weight transported does not change the motivational levels, primarily defined by the food-source profitability. Finally, the immediate return to the flower just depleted is interpreted as a win-stay strategy, in which bees return to places where they previously found food though there is no differential reinforcement for such repetition. Such a response depends on the quantity of the reinforcer., The movement pattern of honeybees Apis mellifera working on a patch of artificial flowers and its dependence on food-source profitability were analysed by varying the flow rate of sucrose solution provided by a set of artificial flowers. Three sucrose flow rates were used (0.085, 0.17 and 0.34 μl/min per flower) and twenty bees per flow rate were measured over one entire visit to the patch. It is shown that 1) bees had the same landing rate at the lower and the intermediate flow rates but foraged significantly faster at the higher flow rate. 2) For the three flow rates tested, the landing rate remained constant throughout the entire foraging visit, thus being unaffected by the progressive increase in the weight transported in the crop. 3) Only the probability of an immediate return to a previously visited flower significantly increased with the flow rate. Such immediate returns occurred whenever the reward experienced at a flower greatly surpassed the mean reward expectation per flower. 4) However, bees returning immediately to the last visited flower did not find reward in it. It is suggested that bees go faster when the offer becomes better as a result of an increase in the foraging motivation that would lead to an incitement of foraging movements and that the progressive increase in the weight transported does not change the motivational levels, primarily defined by the food-source profitability. Finally, the immediate return to the flower just depleted is interpreted as a win-stay strategy, in which bees return to places where they previously found food though there is no differential reinforcement for such repetition. Such a response depends on the quantity of the reinforcer.]

Flower Color, Nectar Reward, and the Flower Fidelity of the Caucasus Honey Bee (Apis mellifera caucasica)

The foraging of Apis mellifera caucasica was examined on trimorphic (blue, yellow, white) artificial flower patches in the eastern region of the Black Sea. Foraging was defined by a superstructure where some bees visited only yellow flowers, and other bees limited visitation to blue and white flowers. That flower fidelity persisted in spite of reward quality, quantity, or frequency differences between flower colors (Individual Constancy Behavior). Blue-White constant bees foraged randomly between blue and white flowers when reward quantity and frequency differed between color morphs. However, bees whose fidelity was to blue and white flowers limited visitation to the color morph (blue or white) offering the higher quality reward. Thus, energy maximization represented a sub-behavior restricted by individual constancy. Results were consistent with predictions of a model based upon environment, colony size, and bee size, and have important applications for agricultural settings both when hybrid seed is (and is not) desired.