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.     

Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (<Emphasis Type="Italic">Bombus terrestris</Emphasis>) as a case study

Individual bumblebees were trained to choose between rewarded target flowers and non-rewarded distractor flowers in a controlled illumination laboratory. Bees learnt to discriminate similar colours, but with smaller colour distances the frequency of errors increased. This indicates that pollen transfer might occur between flowers with similar colours, even if these colours are distinguishable. The effect of similar colours on reducing foraging accuracy of bees is evident for colour distances high above discrimination threshold, which explains previous field observations showing that bees do not exhibit complete flower constancy unless flower colour between species is distinct. Bees tested in spectrally different illumination conditions experienced a significant decrease in their ability to discriminate between similar colours. The extent to which this happens differs in different areas of colour space, which is consistent with a von Kries-type model of colour constancy. We find that it would be beneficial for plant species to have highly distinctive colour signals to overcome limitations on the bees performance in reliably judging differences between similar colours. An exception to this finding was flowers that varied in shape, in which case bees used this cue to compensate for inaccuracies of colour vision.     

The 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     

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.     

Blue colour preference in honeybees distracts visual attention for learning closed shapes

Spatial vision is an important cue for how honeybees (Apis mellifera) find flowers, and previous work has suggested that spatial learning in free-flying bees is exclusively mediated by achromatic input to the green photoreceptor channel. However, some data suggested that bees may be able to use alternative channels for shape processing, and recent work shows conditioning type and training length can significantly influence bee learning and cue use. We thus tested the honeybees’ ability to discriminate between two closed shapes considering either absolute or differential conditioning, and using eight stimuli differing in their spectral characteristics. Consistent with previous work, green contrast enabled reliable shape learning for both types of conditioning, but surprisingly, we found that bees trained with appetitive-aversive differential conditioning could additionally use colour and/or UV contrast to enable shape discrimination. Interestingly, we found that a high blue contrast initially interferes with bee shape learning, probably due to the bees innate preference for blue colours, but with increasing experience bees can learn a variety of spectral and/or colour cues to facilitate spatial learning. Thus, the relationship between bee pollinators and the spatial and spectral cues that they use to find rewarding flowers appears to be a more rich visual environment than previously thought.     

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.     

Temporal acuity of honeybee vision: behavioural studies using flickering stimuli

ABSTRACT. Temporal resolution of freely-flying bees was measured by training bees, Apis mellifera (Linn.), to discriminate between a steady light and a flickering light. Two kinds of experiments were conducted: those using a homochromatic flicker, in which the intensity of the flickering light varied periodically with time; and ones using a heterochromatic flicker, in which the colour of the flickering light varied periodically. In either case, the time-averaged properties (intensity and colour) of the flickering light matched those of the steady light, and the bees' ability to discriminate between the two stimuli was measured for various flicker frequencies. The results indicate that bees perform poorly in the homochromatic flicker experiments, regardless of the colour of the light (u.v., blue or green), but well in those with heterochromatic flicker. Heterochromatic flicker experiments using various pairwise combinations of the colours U.V., blue and green (corresponding to the three known spectral receptor-types in the bee's retina) reveal that temporal resolution is much better when blue is one of the component colours, than when it is not. The simplest interpretation of the results is in terms of colour channels possessing different response speeds. Heterochromatic flicker promises to be a useful tool in investigating the temporal properties of colour vision in bees.     

Perception of heterochromatic flicker by honeybees: a behavioural study

Freely flying honeybees were trained to discriminate a stimulus consisting of two alternating chromatic lights (heterochromatic flicker) from a steady mixture of the same two lights, using 3 different pairs of lights: blue-UV, UV-green, and green-UV. With each light pair, training to the heterochromatic flicker was conducted at several flicker frequencies, using experimentally naive bees in each training. In subsequent tests, the trained bees were given a choice between the two lights that constituted the flicker, presented steady, as well as between either of them and the steady mixture. We find that bees trained to particular frequencies of heterochromatic flicker prefer one of the component lights over the other as well as over the steady mixture, suggesting that the colour they perceive in the heterochromatic flicker to which they have been trained is shifted in the direction of one of the lights contained in the flicker. The colour shift occurs at flicker frequencies that depend on the pair of lights used. We propose that the shift is generated by an effect similar to the Brücke-Bartley phenomenon known from human vision. This effect is based on the enhancement of the photoreceptors' response upon onset of stimulation, causing an intermittent light to appear brighter than a steady light of identical physical intensity. We propose that the degree of enhancement might differ among the 3 spectral classes of photoreceptor, causing the colour perceived in a heterochromatic flicker to differ from that perceived in a steady mixture of its two light components.     

Long Term Effects of Aversive Reinforcement on Colour Discrimination Learning in Free-Flying Bumblebees

The results of behavioural experiments provide important information about the structure and information-processing abilities of the visual system. Nevertheless, if we want to infer from behavioural data how the visual system operates, it is important to know how different learning protocols affect performance and to devise protocols that minimise noise in the response of experimental subjects. The purpose of this work was to investigate how reinforcement schedule and individual variability affect the learning process in a colour discrimination task. Free-flying bumblebees were trained to discriminate between two perceptually similar colours. The target colour was associated with sucrose solution, and the distractor could be associated with water or quinine solution throughout the experiment, or with one substance during the first half of the experiment and the other during the second half. Both acquisition and final performance of the discrimination task (measured as proportion of correct choices) were determined by the choice of reinforcer during the first half of the experiment: regardless of whether bees were trained with water or quinine during the second half of the experiment, bees trained with quinine during the first half learned the task faster and performed better during the whole experiment. Our results confirm that the choice of stimuli used during training affects the rate at which colour discrimination tasks are acquired and show that early contact with a strongly aversive stimulus can be sufficient to maintain high levels of attention during several hours. On the other hand, bees which took more time to decide on which flower to alight were more likely to make correct choices than bees which made fast decisions. This result supports the existence of a trade-off between foraging speed and accuracy, and highlights the importance of measuring choice latencies during behavioural experiments focusing on cognitive abilities.     

Can honey bees change foraging patterns?

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

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.     

Discrimination of coloured patterns by honeybees through chromatic and achromatic cues

We investigated pattern discrimination by worker honeybees, Apis mellifera, focusing on the roles of spectral cues and the angular size of patterns. Free-flying bees were trained to discriminate concentric patterns in a Y-maze. The rewarded pattern could be composed of either a cyan and a yellow colour, which presented both different chromatic and achromatic L-receptor contrast, or an orange and a blue colour, which presented different chromatic cues, but the same L-receptor contrast. The non-rewarded alternative was either a single-coloured disc with the colour of the central disc or the surrounding ring of the pattern, a checkerboard pattern with non-resolvable squares, the reversed pattern, or the elements of the training pattern (disc or ring alone). Bees resolved and learned both colour elements in the rewarded patterns and their spatial properties. When the patterns subtended large visual angles, this discrimination used chromatic cues only. Patterns with yellow or orange central discs were generalised toward the yellow and orange colours, respectively. When the patterns subtended a visual angle close to the detection limit and L-receptor contrast was mediating discrimination, pattern perception was reduced: bees perceived only the pattern element with higher contrast.     

Spectral tuning by opsin coexpression in retinal regions that view different parts of the visual field

Vision frequently mediates critical behaviours, and photoreceptors must respond to the light available to accomplish these tasks. Most photoreceptors are thought to contain a single visual pigment, an opsin protein bound to a chromophore, which together determine spectral sensitivity. Mechanisms of spectral tuning include altering the opsin, changing the chromophore and incorporating pre-receptor filtering. A few exceptions to the use of a single visual pigment have been documented in which a single mature photoreceptor coexpresses opsins that form spectrally distinct visual pigments, and in these exceptions the functional significance of coexpression is unclear. Here we document for the first time photoreceptors coexpressing spectrally distinct opsin genes in a manner that tunes sensitivity to the light environment. Photoreceptors of the cichlid fish, Metriaclima zebra, mix different pairs of opsins in retinal regions that view distinct backgrounds. The mixing of visual pigments increases absorbance of the corresponding background, potentially aiding the detection of dark objects. Thus, opsin coexpression may be a novel mechanism of spectral tuning that could be useful for detecting prey, predators and mates. However, our calculations show that coexpression of some opsins can hinder colour discrimination, creating a trade-off between visual functions.     

Environmental factors which may have led to the appearance of colour vision

It is hypothesized that colour vision and opponent processing of colour signals in the visual system evolved as a means of overcoming the extremely unfavourable lighting conditions in the natural environment of early vertebrates. The significant flicker of illumination inherent in the shallow-water environment complicated the visual process in the achromatic case, in particular preventing early detection of enemies. The presence of two spectral classes of photoreceptors and opponent interaction of their signals at a subsequent retinal level allowed elimination of the flicker from the retinal image. This new visual function provided certain advantages concerning reaction times and favoured survival. This assumption explains why the building blocks for colour vision arose so early, i.e. just after the active predatory lifestyle was mastered. The principal functions of colour vision inherent in extant animals required a more complex neural machinery for colour processing and evolved later as the result of a change in visual function favouring colour vision.     

The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency

Summary A chromaticity diagram which plots the 3 photoreceptor excitations of trichromatic colour vision systems at an angle of 120° is presented. It takes into acount the nonlinear transduction process in the receptors. The resulting diagram has the outline of an equilateral hexagon. It is demonstrated by geometrical means that excitation values for any type of spectrally opponent mechanism can be read from this diagram if the weighting factors of this mechanism add up to zero. Thus, it may also be regarded as a general representation of colour opponent relations, linking graphically the Young-Helmholtz theory of trichromacy and Hering's concept of opponent colours. It is shown on a geometrical. basis that chromaticity can be coded unequivocally by any two combined spectrally opponent mechanisms, the main difference between particular mechanisms being the extension and compression of certain spectral areas. This type of graphical representation can qualitatively explain the Bezold-Brücke phenomenon. Furthermore, colour hexagon distances may be taken as standardized perceptual colour distance values for trichromatic insects, as is demonstrated by comparison with behavioural colour discrimination data of 3 hymenopteran species.     

Thermal constraints for stingless bee foragers: the importance of body size and coloration

In the dry tropics, foraging bees face significant thermal constraints as a result of high ambient temperatures and direct insolation. In order to determine the potential importance of body size and body coloration in heat gain and heat loss, passive warm-up and cooling rates were measured for freshly killed workers of 24 stingless bee species. Results accorded with biophysical principles. Small bees reached lower temperature excesses (T_exc) and warmed up and lost heat much more rapidly than larger bees. In addition to body size, body coloration had a clear effect on thermal parameters. Light-coloured bees warmed up less rapidly and had lower T_exc than dark bees. An intraspecific comparison of Melipona costaricensis and Cephalotrigona capitata colour morphs confirmed that body coloration influences thermal characteristics. This study is the first to indicate that abdominal coloration in stingless bees might be involved in the regulation of body temperature in extreme thermal conditions. However, body temperatures of foraging bees of colour morphs were not very different. This is probably due to behavioural adaptations (e.g. foraging strategies) or differences in convective and evaporative heat loss or the production of metabolic heat during flight, that all mask the effect of body colour. Notwithstanding such effects and potential thermoregulatory capabilities, stingless bees show niche differentiation and biogeographic distributions that correlate with body coloration and body size. This also suggests that, in general, light bees have an advantage over black bees in hot open lowland habitats, whereas black bees might have an advantage in wet habitats and mountains. The origin, occurrence and function of flavinism (yellow integument colouring) are discussed.     

Fruits, foliage and the evolution of primate colour vision

Primates are apparently unique amongst the mammals in possessing trichromatic colour vision. However, not all primates are trichromatic. Amongst the haplorhine (higher) primates, the catarrhines possess uniformly trichromatic colour vision, whereas most of the platyrrhine species exhibit polymorphic colour vision, with a variety of dichromatic and trichromatic phenotypes within the population. It has been suggested that trichromacy in primates and the reflectance functions of certain tropical fruits are aspects of a coevolved seed-dispersal system: primate colour vision has been shaped by the need to find coloured fruits amongst foliage, and the fruits themselves have evolved to be salient to primates and so secure dissemination of their seeds. We review the evidence for and against this hypothesis and we report an empirical test: we show that the spectral positioning of the cone pigments found in trichromatic South American primates is well matched to the task of detecting fruits against a background of leaves. We further report that particular trichromatic platyrrhine phenotypes may be better suited than others to foraging for particular fruits under particular conditions of illumination; and we discuss possible explanations for the maintenance of polymorphic colour vision amongst the platyrrhines.     

Cone contrast computations: physical versus perceived background and colour constancy

The light reflected from an object depends both on the object's surface and on the illuminant. Visual systems attempt to resolve this intrinsic ambiguity by comparing the light reflected from the object with respect to the background by computing the difference between the object-background light sampled by three cones. The cone-contrasts for the sample-background stimulus under the test illumination should correspond to the cone-contrasts for samples matched in appearance under the standard background (C). The validity of this cone-contrast rule (Whittle, 2003) and its possible link with stability of perceived colour was studied here using six test illuminants. A successive asymmetric colour-matching task with 40 simulated Munsell samples (value 7, chroma 4) on a neutral background (N7) was used. The subject adjusted the sample under standard illuminant C to match the colour appearance of the test sample under one of the test illuminants. Brunswik Ratio (BR) was used as an index of stability of colour appearance. When computed with respect to the reference illuminant C, the cone contrast rule was violated (particularly for S-cone-contrast). However, if a new reference point based on the perceived colour of the neutral background under the test illumination was used, the cone contrast rule applied. That is, when cone contrasts of the matching samples are computed with respect to this perceived background, they correspond to cone contrasts of the test stimuli. This represents a form of discounting the illuminant for the purpose of determining an object's cone-contrast against the background, which does not vary with background illumination. These cone contrasts, however, do not provide any information about the colour appearance of objects under particular viewing conditions, unless calibrated against a standard by allowing subjects to learn particular colours.     

Number-Based Visual Generalisation in the Honeybee

Although the numerical abilities of many vertebrate species have been investigated in the scientific literature, there are few convincing accounts of invertebrate numerical competence. Honeybees, Apis mellifera, by virtue of their other impressive cognitive feats, are a prime candidate for investigations of this nature. We therefore used the well-established delayed match-to-sample paradigm, to test the limits of honeybees'' ability to match two visual patterns solely on the basis of the shared number of elements in the two patterns. Using a y-maze, we found that bees can not only differentiate between patterns containing two and three elements, but can also use this prior knowledge to differentiate three from four, without any additional training. However, bees trained on the two versus three task could not distinguish between higher numbers, such as four versus five, four versus six, or five versus six. Control experiments confirmed that the bees were not using cues such as the colour of the exact configuration of the visual elements, the combined area or edge length of the elements, or illusory contours formed by the elements. To our knowledge, this is the first report of number-based visual generalisation by an invertebrate.     

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.