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.     

Colour-dependent target detection by bees

The distance over which an object is detected by bees depends on the subtended visual angle and on spectral cues. At large angular subtenses detection is mediated only by chromatic cues. Achromatic targets, however, are also detectable. We investigated how chromatic and achromatic cues interact in detecting large-size targets. Coloured targets were used, with varied chromatic contrast that either did or did not present L-receptor contrast. Better detection correlated with higher chromatic contrast. Adding L-receptor contrast did not affect detection. It did allow the detection of achromatic targets, but at a lower level than most coloured ones, which indicates that the input from the achromatic system is negligible due to low sensitivity.     

The angular range of achromatic target detection by honey bees

Honeybees Apis mellifera were trained to enter a Y-maze and choose the arm with a rewarded disc presented against a grey background. The alternative arm displayed the unrewarded grey background alone. Training and testing were performed with the rewarding disc subtending different visual angles. The training disc was either achromatic and provided green contrast, or chromatic and provided the same amount of green contrast as the achromatic one. The bee-achromatic disc could be learned and detected by the bees whenever it subtended 5° or 10°, but not if it subtended 30°. The chromatic disc was learned well and detected at all three visual angles. However, at 5° the maximum level of correct choices was ca. 75% with the achromatic disc whilst it was ca. 90% with the chromatic one. Thus, the presence of chromatic contrast enhances considerably the level of correct choices for the same amount of green contrast. The lower threshold of achromatic target detection lies between 3.7° and 5°; the upper threshold between 15° and 10°. At the upper threshold, detection switches from chromatic-based to achromatic-based. Thus, in the context of target detection, the achromatic green contrast channel specialises in the detection of objects of reduced angular size, whilst the chromatic channels are specialised for objects of large angular size. We suggest that achromatic detectors with a centre-surround organisation are involved in the task of detecting achromatic targets. Accepted: 23 February 1998     

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.     

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.     

How bees detect coloured targets using different regions of their compound eyes

Honeybees Apis mellifera detect coloured targets presented to the frontal region of their compound eyes using their colour vision system at larger visual angles (α > 15°), and an achromatic visual system based on the long-wave photoreceptor type at smaller visual angles (5° < α < 15°). Here we examine the capability of the dorsal, ventral and frontal regions of the eye for colour detection. The minimum visual angle α_min at which the bees detect a stimulus providing both chromatic contrast and receptor-specific contrasts to the three receptor types varies for the different regions of the eye: 7.1 ± 0.5° for the ventral region, 8.2 ± 0.6° for the dorsal region and 4.0 ± 0.5° for the frontal region. Flight trajectories show that when the target was presented in the horizontal plane, bees used only the ventral region of their eyes to make their choices. When the targets appeared dorsally, bees used the frontodorsal region. This finding suggests that pure dorsal detection of coloured targets is difficult in this context. Furthermore, α_min in the ventral plane depends on receptor-specific contrasts. The absence of S-receptor contrast does not affect the performance (α_min = 5.9 ± 0.5°), whilst the absence of M- and L-receptor contrast significantly impairs the detection task. Minimal visual angles of 10.3 ± 0.9° and 17.6 ± 3°, respectively, are obtained in these cases. Thus, as for many visual tasks, the compound eye of the honeybee shows a regionalisation of colour detection that might be related to peripheral or central specialisations. Accepted: 28 September 1999     

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     

Corner effect in induced hue: evidence for chromatic band-pass filters

An experiment is described which investigates the spatial determinants of the apparent difference in hue between the central grey patches of chromatic 'H' pattern pairs, an effect similar to that first demonstrated by Wright (1969, The Measurement of Colour, Hilger, London) in coloured gratings. The hue difference is shown to be analogous to the brightness difference in achromatic 'H' patterns demonstrated by Moulden and Kingdom (1989, Vision Res. 29, 1245-1259). The origin of both effects is argued to be the presence of the corner intersections in the 'H' patterns, which are powerful stimuli for cells with circularly-symmetric, centre-surround organization. It is suggested that the results of the experiment with the chromatic 'H' patterns implicates the operation of cells with a spectrally double-opponent, rather than single-opponent receptive field organization.     

How Bees Discriminate a Pattern of Two Colours from Its Mirror Image

A century ago, in his study of colour vision in the honeybee (Apis mellifera), Karl von Frisch showed that bees distinguish between a disc that is half yellow, half blue, and a mirror image of the same. Although his inference of colour vision in this example has been accepted, some discrepancies have prompted a new investigation of the detection of polarity in coloured patterns. In new experiments, bees restricted to their blue and green receptors by exclusion of ultraviolet could learn patterns of this type if they displayed a difference in green contrast between the two colours. Patterns with no green contrast required an additional vertical black line as a landmark. Tests of the trained bees revealed that they had learned two inputs; a measure and the retinotopic position of blue with large field tonic detectors, and the measure and position of a vertical edge or line with small-field phasic green detectors. The angle between these two was measured. This simple combination was detected wherever it occurred in many patterns, fitting the definition of an algorithm, which is defined as a method of processing data. As long as they excited blue receptors, colours could be any colour to human eyes, even white. The blue area cue could be separated from the green receptor modulation by as much as 50°. When some blue content was not available, the bees learned two measures of the modulation of the green receptors at widely separated vertical edges, and the angle between them. There was no evidence that the bees reconstructed the lay-out of the pattern or detected a tonic input to the green receptors.     

Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds

The colors of fruits and flowers are traditionally viewed as an adaptation to increase the detectability of plant organs to animal vectors. The detectability of visual signals increases with increasing contrasts between target and background. Contrasts consist of a chromatic aspect (color) and an achromatic aspect (light intensity), which are perceived separately by animals. To evaluate the relative importance of fruits’ chromatic and achromatic contrasts for the detection by avian fruit consumers we conducted an experiment with artificial fruits of four different colors in a tropical forest. We displayed the fruits against two different backgrounds, an artificial background and a natural one, because they differed in achromatic properties. We found no effect of the type of background on fruit detection rates. Detection rates differed for the four fruit colors. The probability of detection was explained by the chromatic contrast between fruits and their background, not by the achromatic contrasts. We suggest that birds attend primarily to chromatic contrast probably because these are more reliably detected under variable light conditions. Consistent with this hypothesis, we found habitat-specific differences in the conspicuousness of natural fruit colors in the study area. Fruits of understory species that are subjected to the variable light conditions within a forest displayed higher chromatic contrasts than species growing in the open restinga forest with constant bright illumination. There was no such difference for achromatic contrasts. In sum, we suggest that fruit colors differ between habitats because fruit colors that have strong chromatic contrasts against background can increase plants’ reproductive success, particularly under variable light conditions.     

Flower patterns are adapted for detection by bees

We have demonstrated previously that honeybees use brightness vision mediated by green (or L-) receptor to detect targets from a long distance. They detect circular targets having a dim, for the L-receptor, centre and bright surround from a longer distance than targets having bright centre and dim surround. Here we show that a majority of bee-pollinated flowers have a centre that, for the L-receptor, is dim with bright surround, i.e. have patterns that are easy for a bee to detect. Flowers with dim for the L-receptor surrounds tend to be larger than those with bright surrounds, indicating that flowers compensate for the impaired visibility of their patterns by increasing the size of their displays.     

The butterfly Papilio xuthus detects visual motion using chromatic contrast

Many insects’ motion vision is achromatic and thus dependent on brightness rather than on colour contrast. We investigate whether this is true of the butterfly Papilio xuthus, an animal noted for its complex retinal organization, by measuring head movements of restrained animals in response to moving two-colour patterns. Responses were never eliminated across a range of relative colour intensities, indicating that motion can be detected through chromatic contrast in the absence of luminance contrast. Furthermore, we identify an interaction between colour and contrast polarity in sensitivity to achromatic patterns, suggesting that ON and OFF contrasts are processed by two channels with different spectral sensitivities. We propose a model of the motion detection process in the retina/lamina based on these observations.     

Decoding colouration of begging traits by the experimental addition of the appetite enhancer cyproheptadine hydrochloride in magpie Pica pica nestlings

The colouration of some traits in nestlings of altricial birds may influence parental food allocation as it may reflect physical condition or hunger. There is increasing evidence of the relationship between colouration of begging traits and nestling performance. However, evidence of the influence of hunger level on nestling colouration is scarce, mainly because of difficulty of distinguishing between the effects of physical condition and hunger levels. Here, we used the appetite stimulant cyproheptadine hydrochloride to increase the sensation of hunger of magpie Pica pica nestlings for eight days and assessed the effect on the colouration of rictal flanges, mouth and body skin. We found that nestlings administered with cyproheptadine had flanges more conspicuous (chromatic visual contrast), more UV coloured and less yellow coloured than their control nestmates. Conversely, mouths of experimental nestlings were more yellow coloured and less UV coloured than controls. Our pharmacological experiment affected the strength of the relationship between body mass and some colour components of body skin (chromatic and achromatic visual contrasts, UV–chroma and yellow–chroma) and of rictal flanges (chromatic visual contrasts, UV–chroma and yellow–chroma), but not for mouth colouration. These results taken together suggest that the effect of the cyproheptadine on nestling colourations is probably mediated by an increase in hunger levels of nestlings for rictal flanges and body skin colourations, and by an increase in physical condition in the case of mouth coloration.     

Pattern vision of the honeybee (Apis mellifera): the effect of pattern on the discrimination of location

This paper investigates how the pattern influences the discrimination of different locations of two or more areas of black, white or colour. The coloured patterns were made from two calibrated coloured papers that give contrast only to green receptors, or alternatively only to blue receptors. The patterns are fixed during training. It is found that the discrimination of translocation of two areas of colour involves green receptors and also blue receptors, and the resolution depends strongly on the pattern. Patterns that offer horizontal strips and up-down differences in locations are well resolved, even with no green contrast. Resolution of left-right reversal is greatly improved when the patterns promote fixation in the horizontal plane, as if green contrast is essential to stabilize the eye in yaw. The addition of radial bars with green contrast, a central black spot or a black surround, is particularly effective. The additions promote fixation, and would aid the detection of natural symmetrical objects. Accepted: 30 May 1999     

Enhancement of chromatic contrast increases predation risk for striped butterflies

Many prey species have evolved defensive colour patterns to avoid attacks. One type of camouflage, disruptive coloration, relies on contrasting patterns that hinder predators' ability to recognize an object. While high contrasts are used to facilitate detection in many visual communication systems, they are thought to provide misleading information about prey appearance in disruptive patterns. A fundamental tenet in disruptive coloration theory is the principle of 'maximum disruptive contrast', i.e. disruptive patterns are more effective when higher contrasts are involved. We tested this principle in highly contrasting stripes that have often been described as disruptive patterns. Varying the strength of chromatic contrast between stripes and adjacent pattern elements in artificial butterflies, we found a strong negative correlation between survival probability and chromatic contrast strength. We conclude that too high a contrast leads to increased conspicuousness rather than to effective camouflage. However, artificial butterflies that sported contrasts similar to those of the model species Limenitis camilla survived equally well as background-matching butterflies without these stripes. Contrasting stripes do thus not necessarily increase predation rates. This result may provide new insights into the design and characteristics of a range of colour patterns such as sexual, mimetic and aposematic signals.     

Discrimination of closed coloured shapes by honeybees requires only contrast to the long wavelength receptor type

Floral shape is a visual cue used by pollinators to discriminate between competing flower species. We investigated whether discrimination is possible between closed shapes presenting the same colour and lacking a centrally presented fixation point. Free-flying honeybees, Apis mellifera L., had to discriminate between a solid square and a solid triangle of the same colour presented on the back walls of a Y-maze. Different colours were used to vary chromatic contrast and receptor-specific contrasts. Discrimination was possible whenever shapes presented contrast to the long wavelength receptor but was independent of chromatic contrast, overall intensity contrast or short and middle wavelength receptor contrast. We suggest that the bees used the edges of the closed shapes to solve the task. Bees failed when shapes were rotated, showing that a single shape edge was not sufficient for recognition. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Separate colour-opponent mechanisms underlie the detection and discrimination of moving chromatic targets.

Current opinion holds that human colour vision is mediated primarily via a colour-opponent pathway that carries information about both wavelength and luminance contrast (type I). However, some authors argue that chromatic sensitivity may be limited by a different geniculostriate pathway, which carries information about wavelength alone (type II). We provide psychophysical evidence that both pathways may contribute to the perception of moving, chromatic targets in humans, depending on the nature of the visual discrimination. In experiment 1, we show that adaptation to drifting, red-green stimuli causes reductions in contrast sensitivity for both the detection and direction discrimination of moving chromatic targets. Importantly, the effects of adaptation are not directionally specific. In experiment 2, we show that adaptation to luminance gratings results in reduced sensitivity for the direction discrimination, but not the detection of moving chromatic targets. We suggest that sensitivity for the direction discrimination of chromatic targets is limited by a colour-opponent pathway that also conveys luminance-contrast information, whereas the detection of such targets is limited by a pathway with access to colour information alone. The properties of these pathways are consistent with the known properties of type-I and type-II neurons of the primate parvocellular lateral geniculate nucleus and their cortical projections. These findings may explain the known differences between detection and direction discrimination thresholds for chromatic targets moving at low to moderate velocities.     

Colour preferences and colour vision in poultry chicks

The dramatic colours of biological communication signals raise questions about how animals perceive suprathreshold colour differences, and there are long-standing questions about colour preferences and colour categorization by non-human species. This study investigates preferences of foraging poultry chicks (Gallus gallus) as they peck at coloured objects. Work on colour recognition often deals with responses to monochromatic lights and how animals divide the spectrum. We used complementary colours, where the intermediate is grey, and related the chicks' choices to three models of the factors that may affect the attractiveness. Two models assume that attractiveness is determined by a metric based on the colour discrimination threshold either (i) by chromatic contrast against the background or (ii) relative to an internal standard. An alternative third model is that categorization is important. We tested newly hatched and 9-day-old chicks with four pairs of (avian) complementary colours, which were orange, blue, red and green for humans. Chromatic contrast was more relevant to newly hatched chicks than to 9-day-old birds, but in neither case could contrast alone account for preferences; especially for orange over blue. For older chicks, there is evidence for categorization of complementary colours, with a boundary at grey.     

Chromatic signals control proboscis movements during hovering flight in the hummingbird hawkmoth Macroglossum stellatarum

Most visual systems are more sensitive to luminance than to colour signals. Animals resolve finer spatial detail and temporal changes through achromatic signals than through chromatic ones. Probably, this explains that detection of small, distant, or moving objects is typically mediated through achromatic signals. Macroglossum stellatarum are fast flying nectarivorous hawkmoths that inspect flowers with their long proboscis while hovering. They can visually control this behaviour using floral markings known as nectar guides. Here, we investigate whether this is mediated by chromatic or achromatic cues. We evaluated proboscis placement, foraging efficiency, and inspection learning of naïve moths foraging on flower models with coloured markings that offered either chromatic, achromatic or both contrasts. Hummingbird hawkmoths could use either achromatic or chromatic signals to inspect models while hovering. We identified three, apparently independent, components controlling proboscis placement: After initial contact, 1) moths directed their probing towards the yellow colour irrespectively of luminance signals, suggesting a dominant role of chromatic signals; and 2) moths tended to probe mainly on the brighter areas of models that offered only achromatic signals. 3) During the establishment of the first contact, naïve moths showed a tendency to direct their proboscis towards the small floral marks independent of their colour or luminance. Moths learned to find nectar faster, but their foraging efficiency depended on the flower model they foraged on. Our results imply that M. stellatarum can perceive small patterns through colour vision. We discuss how the different informational contents of chromatic and luminance signals can be significant for the control of flower inspection, and visually guided behaviours in general.     

Size,shape and hue modulate attraction and landing responses of the braconid parasitoid <Emphasis Type="Italic">Fopius arisanus</Emphasis> to fruit odour-baited visual targets

Female parasitoids are guided by multisensory information, including chemical and physical cues during host location. In the present study, we investigated the behavioural responses of naïve Fopius arisanus (Sonan) females to visual targets baited with guava odour. In non-choice wind tunnel tests, the attraction and landing responses of parasitoids to spheres painted with different colours, and targets of different shapes and sizes were evaluated. Females were more frequently attracted and landed more often on dark yellow targets than on targets with other colours. There was no correlation between the brightness of each colour and the attraction or landing responses. In contrast, both responses were correlated with relative reflectance (hue) of the coloured targets. A positive correlation was observed between attraction and hue, and a negative correlation between landing and hue. F. arisanus was attracted to and landed more often on spheres than on other shape models. The attraction response of this parasitoid was affected by the size of the targets, with spheres of 10 and 12 cm diameter being more attractive than spheres of 8, 6 and 4 cm diameter. The fact that F. arisanus females were able to discriminate among visual targets that differ in colour, shape and size stresses the importance of vision during host location by this species.