Bumblebees (<Emphasis Type="Italic">Bombus terrestris</Emphasis>) sacrifice foraging speed to solve difficult colour discrimination tasks

The performance of individual bumblebees at colour discrimination tasks was tested in a controlled laboratory environment. Bees were trained to discriminate between rewarded target colours and differently coloured distractors, and then tested in non-rewarded foraging bouts. For the discrimination of large colour distances bees made relatively fast decisions and selected target colours with a high degree of accuracy, but for the discrimination of smaller colour distances the accuracy decreased and the bees response times to find correct flowers significantly increased. For small colour distances there was also significant linear correlations between accuracy and response time for the individual bees. The results show both between task and within task speed-accuracy tradeoffs in bees, which suggests the possibility of a sophisticated and dynamic decision-making process.     

Simultaneous and successive colour discrimination in the honeybee (Apis mellifera)

The colour discrimination of individual free-flying honeybees (Apis mellifera) was tested with simultaneous and successive viewing conditions for a variety of broadband reflectance stimuli. For simultaneous viewing bees used form vision to discriminate patterned target stimuli from homogeneous coloured distractor stimuli, and for successive discrimination bees were required to discriminate between homogeneously coloured stimuli. Bees were significantly better at a simultaneous discrimination task, and we suggest this is explained by the inefficiency with which the bees brain can code and retrieve colour information from memory when viewing stimuli successively. Using simultaneous viewing conditions bees discriminated between the test stimuli at a level equivalent to 1 just-noticeable-difference for human colour vision. Discrimination of colours by bees with simultaneous viewing conditions exceeded previous estimates of what is possible considering models of photoreceptor noise measured in bees, which suggests spatial and/or temporal summation of colour signals for fine discrimination tasks. The results show that when behavioural experiments are used to collect data about the mechanisms facilitating colour discrimination in animals, it is important to consider the effects of the stimulus viewing conditions on results.     

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.     

A generalised mimicry system involving angiosperm flower colour, pollen and bumblebees’ innate colour preferences

Flower colour is a major advertisement signal of zoophilous plants for pollinators. Bees, the main pollinators, exhibit innate colour preferences, which have often been attributed to only one single floral colour, though most flowers display a pattern of two or several colours. The existing studies of floral colour patterns are mostly qualitative studies. Using a model of bee colour vision we quantitatively investigate two questions: whether or not component colours of floral colour patterns may mimic pollen signals, and whether or not bumblebees exhibit innate preferences for distinct parameters of naturally existing floral colour patterns. We analysed the spectral reflectances of 162 plant species with multicoloured flowers and inflorescences, distiniguishing between inner and outer colours of floral colour patterns irrespective of the particular structures so coloured.We found that:– The inner colour of radially symmetrical flowers and inflorescences and of zygomorphic flowers appears less diverse to bees than the peripheral colour.– The inner colour of most radial flowers and inflorescences as well as the inner colour of a large number of non-related zygomorphic flowers appears to bees to be very similar to that of pollen.– Bumblebees (Bombus terrestris) exhibit innate preferences for two-coloured over single-coloured dummy flowers in a spontaneous choice test.– Bumblebees exhibit innate preferences for dummy flowers with a large over those with a small centre area.– Bumblebees exhibit innate preferences for dummy flowers with a centre colour similar to that of pollen over those with another centre colour.Our findings support the hypotheses that the inner component of floral colour patterns could be interpreted as a generalised and little recognised form of mimicry of the colour of visually displayed pollen, that bumblebees exhibit innate preferences regarding colour and size parameters of floral colour patterns, and that these correspond to visually displayed pollen. These findings together suggest a prominent role of floral colour patterns in advertisement to and guidance of naive flower visitors.     

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.     

The colour of flowers in spectrally variable illumination and insect pollinator vision

The spectral reflectance of differently coloured Australian native plant flowers and foliage was measured and plotted in a colour triangle to represent the colour space of the honeybee. Spectral variations in illumination are shown to significantly change plant colours for bee vision without colour constancy. A model of chromatic adaptation based upon the von Kries coefficient law shows a reduction in plant colour shift, with the degree of correction depending upon position in colour space. A set of artificial reflectances is used to map relative colour shift caused by spectrally variable illumination for the entire colour space of the honeybee. The rarity of some flower colours in nature shows a correlation to a larger colour shift for these colours when illuminated by spectrally variable radiation. The model of chromatic adaptation is applied to illuminations used in a behavioural study on honeybee colour constancy by Neumeyer 1981. Surface colours used by Neumeyer are plotted in colour space for the various illuminations. The results show that an illumination-dependent colour shift correlates to a decrease in the frequency of bees correctly choosing a colour to which it was trained. Accepted: 23 February 1998     

Flower colours along an alpine altitude gradient, seen through the eyes of fly and bee pollinators

Alpine flowers face multiple challenges in terms of abiotic and biotic factors, some of which may result in selection for certain colours at increasing altitude, in particular the changing pollinator species composition, which tends to move from bee-dominated at lower elevations to fly-dominated in high-alpine regions. To evaluate whether growing at altitude—and the associated change in the dominant pollinator groups present—has an effect on the colour of flowers, we analysed data collected from the Dovrefjell National Park in Norway. Unlike previous studies, however, we considered the flower colours according to ecologically relevant models of bee and fly colour vision and also their physical spectral properties independently of any colour vision system, rather than merely looking at human colour categories. The shift from bee to fly pollination with elevation might, according to the pollination syndrome hypothesis, lead to the prediction that flower colours should shift from more bee-blue and UV-blue flowers (blue/violet to humans, i.e. colours traditionally associated with large bee pollinators) at low elevations to more bee-blue-green and green (yellow and white to humans—colours often linked to fly pollination) flowers at higher altitude. However, although there was a slight increase in bee-blue-green flowers and a decrease in bee-blue flowers with increasing elevation, there were no statistically significant effects of altitude on flower colour as seen either by bees or by flies. Although flower colour is known to be constrained by evolutionary history, in this sample we also did not find evidence that phylogeny and elevation interact to determine flower colours in alpine areas. Handling editor: Neal Williams     

Bumblebees directly perceive variations in the spectral quality of illumination

Individual bumblebees were tested on a task of walking along a test tunnel to collect sucrose solution in an initial training illumination condition that simulated natural daylight, and in two spectrally different illumination conditions. Compared to the training condition the bees took a significantly longer time to complete the task in conditions that simulated either an ultraviolet negative illumination environment, or an illumination environment that represented blue skylight. In a control condition, bees did not derive this cue from spectral information reflected from the dark background material. This result shows that bees can directly perceive spectral changes in illumination conditions, even in the context of a task that does not require colour processing. This potentially enables the visual system of bees to have prior knowledge about the spectral quality of illumination conditions in which they may forage. The findings are discussed in relation to both theoretical models and empirical evidence of colour constancy, and it is concluded that bees can use multiple mechanisms to solve the dilemma posed by having to find colour targets in the spectrally different illumination conditions that exist for insects visiting flowers.     

Colour choices of naive bumble bees and their implications for colour perception

The innate preferences of inexperienced bumble bees, Bombus terrestris, for floral colour stimuli were studied using artificial flowers. The artificial flowers provided a colour pattern and consisted of a star-shaped corolla and of central colour patches similar to the nectar guide of natural flowers. The innate choice behaviour was assessed in terms of the number of approach flights from some distance towards the artificial flowers and the percentage of approach flights terminating in antennal contact with the floral guide. The colours of the floral guide, the corolla and the background were varied. It was shown that the innate flower colour preference in bumble bees has two components. 1. The frequency of approaches from a distance is correlated with the colour difference between the corolla and the background against which it is presented. If the corolla colour was constant but its background colour varied, the relative attractiveness of the corolla increased with its colour difference to the background. The colour difference assessment underlying this behaviour on a perceptual basis can be attained by means of colour opponent coding, a system well-established in Hymenoptera. 2. The frequency of antennal contacts with the floral guides relative to that of approach flights cannot be accounted for by colour opponent coding alone. Whether the approach flights are interrupted, or whether they end in an antennal contact with the nectar guide is strongly dependent on the direction (sign) of the colour difference, not only its magnitude. The choice behaviour requires a unique perceptual dimension, possibly that of colour saturation or that of hue perception comparable to components of colour perception in humans.     

Floral colour diversity in plant communities,bee colour space and a null model

Evolutionary biologists have long hypothesized that the diversity of flower colours we see is in part a strategy to promote memorization by pollinators, pollinator constancy, and therefore, a directed and efficient pollen transfer between plants. However, this hypothesis has never been tested against a biologically realistic null model, nor were colours assessed in the way pollinators see them. Our intent here is to fill these gaps. Throughout one year, we sampled floral species compositions at five ecologically distinct sites near Berlin, Germany. Bee-subjective colours were quantified for all 168 species. A model of colour vision was used to predict how similar the colours of sympatric and simultaneously blooming flowers were for bees. We then compared flower colour differences in the real habitats with those of random plant communities. We did not find pronounced deviations from chance when we considered common plants. When we examined rare plants, however, we found significant divergence in two of the five plant communities. At one site, similarly coloured species were found to be more frequent than expected, and at the other two locations, flower colours were indistinguishable from a random distribution. These results fit theoretical considerations that rare plants are under stronger selective pressure to secure pollination than common plants. Our study illustrates the power of linking such distinct biological traditions as community ecology and the neuroethology of bee vision.     

Colour similarity to rewarding model plants affects pollination in a food deceptive orchid, Orchis boryi

We studied the pollination of Orchis boryi at five different locations on the Greek mainland. Orchis boryi is food deceptive and obligatorily insect pollinated. Primary pollinators were Apis mellifera and Bombus spp., which foraged on rewarding plant species nearby and visited O. boryi in between. To analyse floral colour similarity among rewarding plants and O. boryi as perceived by bees, a model of bee colour vision was employed. For each food plant an index was calculated that described the probability of a bee foraging on it to subsequently choose an orchid flower. This choice probability correlated to colour distance according to the model of bee colour vision, indicating that bees chose the deceptive orchid more frequently if they foraged on more similarly coloured species. At different sites different plant species served as models. Bees foraging on food plants from which a high choice rate to the orchid was observed visited the orchid less often after approaching it than other bees, which is likely to reflect avoidance learning. In general, the pollination syndrome appears to be a generalized form of Batesian mimicry, in which similarity to rewarding plants determines reproductive success. As expected by negative density-dependent selection, individual fruit set and pollinia export rate correlated negatively with orchid density, but were unaffected by food plant density, orchid frequency, individual variation of labellum colour, labellum size, or mouth width of the flowers.     

Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision

Flowering plants in Australia have been geographically isolated for more than 34 million years. In the Northern Hemisphere, previous work has revealed a close fit between the optimal discrimination capabilities of hymenopteran pollinators and the flower colours that have most frequently evolved. We collected spectral data from 111 Australian native flowers and tested signal appearance considering the colour discrimination capabilities of potentially important pollinators. The highest frequency of flower reflectance curves is consistent with data reported for the Northern Hemisphere. The subsequent mapping of Australian flower reflectances into a bee colour space reveals a very similar distribution of flower colour evolution to the Northern Hemisphere. Thus, flowering plants in Australia are likely to have independently evolved spectral signals that maximize colour discrimination by hymenoptera. Moreover, we found that the degree of variability in flower coloration for particular angiosperm species matched the range of reflectance colours that can only be discriminated by bees that have experienced differential conditioning. This observation suggests a requirement for plasticity in the nervous systems of pollinators to allow generalization of flowers of the same species while overcoming the possible presence of non-rewarding flower mimics.     

Butterflies show flower colour preferences but not constancy in foraging at four plant species

1. The extent to which flower colour and other visual cues influence butterfly flower choice in the field is poorly understood, especially in comparison with choices by Hymenoptera. 2. Using a novel approach to studies of visitation behaviour by butterflies, flower colour of four Asteraceae species was phenotypically manipulated to decouple the influence of that trait from others (including morphology and nectar rewards) on visitation by Lycaena heteronea, Speyeria mormonia, Cercyonis oetus, and Phyciodes campestris. 3. Flower visits were recorded to experimental flower arrays in subalpine meadows to measure (i) spontaneous preference by butterflies for particular colours and other traits and (ii) flower constancy (longer than expected strings of visits made to flowers of the same species), a behaviour that can reduce interspecific gene flow in plants. 4. Over three field seasons, 3558 individual flower visits in 1386 foraging bouts were observed for free‐flying butterflies. All four butterfly species responded to the phenotypic manipulations of flower colour, although in different ways. Speyeria mormonia and L. heteronea also exhibited preferences based on other flower traits. Lycaena heteronea responded to combinations of traits such that the other traits it preferred depended upon the context of flower colour. 5. None of the butterfly species exhibited flower constancy in any of the arrays employed. 6. The observed preferences show that butterflies, like some other pollinators, are potentially capable of exerting selection on colour and other floral traits. Moreover, these flower preferences can depend on the context of other flower traits. The absence of constancy contrasts with reports of high constancy in many bees.     

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.     

Pattern discrimination by the honeybee (Apis mellifera ) is colour blind for radial / tangential cues

Bees were trained to discriminate between two patterns, one of which was associated with a reward, in a Y-choice apparatus with the targets presented vertically at a distance at an angular subtense of 50°. Previous work with this apparatus has found discrimination between two patterns of coloured gratings or radial sectors that are fixed in different orientations during the training. When there was contrast to the blue receptors alone, gratings of period 6° were resolved, and 4° when there was contrast to the green receptors. In the present work, bees discriminate between a pattern containing tangentially arranged edges and one containing radially arranged edges, both with no average edge orientation. The targets were rotated every 5 min to make the locations of areas useless as cues. The edges remained consistently radial or tangential and were therefore the only cues. Tests with patterns of selected colours and various levels of grey show that for each colour there is a level of grey at which discrimination fails. Discrimination is therefore colour-blind. The same patterns were made with combinations of coloured papers that give no contrast to the green receptors or alternatively to the blue receptors. The bees discriminate only if the edges between colours present a contrast to the green receptors. The system that discriminates generalized radial and tangential cues is therefore colour blind because the inputs are restricted to the green receptors, not because receptor outputs are added together. The same result was obtained with a very coarse pattern of period 20°. Accepted: 10 January 1999     

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.

     

Visual discrimination by the honeybee (Apis mellifera): the position of the common centre as the cue

Abstract. Bees can be trained to discriminate between a target with a 20° spot above a 10° spot of the same colour, and another target with the spots exchanged in position. Tests show that they do not remember the separate positions of spots of the same colour (including black) on the same target. The bees discriminate the difference in positions, in the vertical direction, of the common centres of the spots taken together, with or without green contrast.
Similar results are obtained in discriminations of a fixed T shape, each composed of two broad black bars subtending 8 by 24°, vs the same shape inverted. The trained bees fail to discriminate between the T shapes when the centroids are at the same level in the vertical direction. Moving the shapes in the horizontal direction in tests has less effect. Quite different results are obtained when the two bars of the T shape differ in colour. The bees discriminate the positions of the two colours separately, but they still fail to discriminate the shape of the T. The results can be explained by filters that detect the intensities within their fields, irrespective of shape, and weigh them according to their vertical angles from the horizontal midline. The normal function of these filters could be to detect the levels of objects relative to the horizon when the bee is in flight.     

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.     

Colour constancy in insects

Colour constancy is the perceptual phenomenon that the colour of an object appears largely unchanged, even if the spectral composition of the illuminating light changes. Colour constancy has been found in all insect species so far tested. Especially the pollinating insects offer a remarkable opportunity to study the ecological significance of colour constancy since they spend much of their adult lives identifying and choosing between colour targets (flowers) under continuously changing ambient lighting conditions. In bees, whose colour vision is best studied among the insects, the compensation provided by colour constancy is only partial and its efficiency depends on the area of colour space. There is no evidence for complete ‘discounting’ of the illuminant in bees, and the spectral composition of the light can itself be used as adaptive information. In patchy illumination, bees adjust their spatial foraging to minimise transitions between variously illuminated zones. Modelling allows the quantification of the adaptive benefits of various colour constancy mechanisms in the economy of nature. We also discuss the neural mechanisms and cognitive operations that might underpin colour constancy in insects.     

Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts

Honeybees Apis mellifera were trained to distinguish between the presence and the absence of a rewarded coloured spot, presented on a vertical, achromatic plane in a Y-maze. They were subsequently tested with different subtended visual angles of that spot, generated by different disk diameters and different distances from the decision point in the device. Bees were trained easily to detect bee-chromatic colours, but not an achromatic one. Chromatic contrast was not the only parameter allowing learning and, therefore, detection: _min, the subtended visual angle at which the bees detect a given stimulus with a probability P ₀ = 0.6, was 5° for stimuli presenting both chromatic contrast and contrast for the green photoreceptors [i.e. excitation difference in the green photoreceptors, between target and background (green contrast)], and 15° for stimuli presenting chromatic but no green contrast. Our results suggest that green contrast can be utilized for target detection if target recognition has been established by means of the colour vision system. The green-contrast signal would be used as a far-distance signal for flower detection. This signal would always be detected before chromatic contrast during an approach flight and would be learned in compound with chromatic contrast, in a facilitation-like process.