Broad spectral sensitivities in the honeybee's photoreceptors limit colour constancy

Colour constancy allows for visual systems to be view stimuli independent of changes in spectral illumination. Chromatic adaptation is likely to be an important mechanism in colour constancy and can be explained by use of the von Kries coefficient law. Chromatic adaptation is compared for the honeybee and three hypothetical visual systems. It is shown that the spectral breadth and asymmetry of photoreceptors in the honeybee may limit colour constancy. In particular, it is demonstrated that the absorption of short-wavelength radiation by the cis-band of chromophore is responsible for a poorer correction for bee colours rich in ultraviolet reflectance. The results are discussed in relation to theoretical considerations of von Kries colour constancy and the physiology of eye design in some other species for which colour constancy has been demonstrated. Accepted: 14 August 1999     

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     

Flight Durations in Bumblebees Under Manipulation of Feeding Choices

Foraging bees spend less time flying between flowers of the same species than between individuals of different species. This time saving has been suggested as a possible advantage of flower-constant foraging. We hypothesized that the time required to switch flower type increases if (a) such switches are infrequent and (b) the bees need to decide whether to switch or not. Bumblebees were taught to forage on artificial feeders that were identical in morphology and reward schedule but differed in the color of their landing surface. In the first two experiments bees foraged alternatively between two feeders. In Experiment 1 the colors of the landing surfaces were switched every two or three visits, while in Experiment 2 they were switched every six or seven visits. In the third experiment, the bees were required to decide whether to make a color-constant or a color-shift flight. Intervisit time was defined as time elapsed between consecutive visits to feeders. When feeder colors were changed frequently (Experiment 1), we detected no difference between color-constant and color-shift intervisit times. When bees were repeatedly exposed to one color (Experiment 2), color shifts required a significantly longer time. When allowed to choose (Experiment 3), bees performed more color-constant flights than color-shift flights. Intervisit times were similar for color-constant and color-shift flights in this experiment. Intervisit times in Experiment 3 were significantly longer than in Experiment 2 and slightly but nonsignificantly longer than in Experiment 1. The results suggest that bees indeed save time though flower-constant foraging but that this time savings is a small (1 s/flower visit) under laboratory conditions, and appears only when switches between flower types are infrequent. The time saved may be more significant over long foraging trips, and when morphological differences between flower species are large, as often happens under natural conditions, providing a selective advantage to flower-constant foraging.     

Contributions to the theory of invariance of color under the condition of varying illumination

Any visual-processing algorithm aimed at attaining color constancy will in fact attain it only for restricted spectral classes of illuminants and reflectances. These classes constitute implicit heuristics for the physical world, in an artificial-intelligence sense. In the present work, physically reasonable spectral classes are presented which insure that von Kries's law of chromatic adaptation will — in its simplest form — restore object colors in human tristimulus space to illuminant-invariant positions in the space. Algebraic functions of the adapted tristimulus values are presented which are illuminant-invariant for some departures from the spectral heuristics. These functions, a hierarchy of invariants, may be useful in developing lighting and pigment standards for partially controlled viewing environments.     

A novel method to investigate the pollen diets of hoverflies

A novel method to investigate the pollen diets of hoverflies is described. The method dispenses with the need for dissection skills or the use of hazardous chemicals thus making it particularly useful for school, college or undergraduate projects and for amateurs. It utilises the properties of the indigestible pollen coat, or exine, which enables pollen to pass through the gut of a hoverfly intact and remain identifiable, even when defaecated. Importantly it does not require the harvesting of insects making it particularly useful for work with rare species. The method was used to investigate the pollen diet of marmalade flies (Episyrphus balteatus) caught in a meadow but it could also be used to investigate many other aspects of syrphid ecology.     

The evolutionary adaptation of flower colours and the insect pollinators' colour vision

Summary The evolutionary tuning between floral colouration and the colour vision of flower-visiting Hymenoptera is quantified by evaluating the informational transfer from the signalling flower to the perceiving pollinator. The analysis of 180 spectral reflection spectra of angiosperm blossoms reveals that sharp steps occur precisely at those wavelengths where the pollinators are most sensitive to spectral differences. Straight-forward model calculations determine the optimal set of 3 spectral photoreceptor types for discrimination of floral colour signals on the basis of perceptual difference values. The results show good agreement with the sets of photoreceptors characterized electrophysiologically in 40 species of Hymenoptera.     

Assessing the use of genomic DNA as a predictor of the maximum absorbance wavelength of avian SWS1 opsin visual pigments

Recently, in vitro mutation studies have made it possible to predict the wavelengths of maximum absorbance (λ_max) of avian UV/violet sensitive visual pigments (SWS1) from the identity of a few key amino acid residues in the opsin gene. Given that the absorbance spectrum of a cone’s visual pigment and of its pigmented oil droplet can be predicted from just the λ_max, it may become possible to predict the entire spectral sensitivity of a bird using genetic samples from live birds or museum specimens. However, whilst this concept is attractive, it must be validated to assess the reliability of the predictions of λ_max from opsin amino acid sequences. In this paper, we have obtained partial sequences covering three of the known spectral tuning sites in the SWS1 opsin and predicted λ_max of all bird species for which the spectral absorbance has been measured using microspectrophotometry. Our results validate the use of molecular data from genomic DNA to predict the gross differences in λ_max between the violet- and ultraviolet-sensitive subtypes of SWS1 opsin. Additionally, we demonstrate that a bird, the bobolink Dolichonyx oryzivorus L., can have more than one SWS1 visual pigment in its retina.     

Comparative study of the spectral sensitivities of mesopelagic crustaceans

The spectral sensitivities of 12 species of mesopelagic crustaceans were studied by means of electrophysiological recordings. Nine of the species are vertical migrators, while 3 are not, and 9 species possess bioluminescent organs, while 3 are not bioluminescent. All species had a single peak of spectral sensitivity with maxima between 470 nm and 500 nm. There was no apparent correlation between sensitivity maxima and daytime depth distribution, migratory behavior, or the presence or absence of bioluminescent organs. With the exception of the hyperiid amphipod Phronima sedentaria, the spectral sensitivities of these mesopelagic crustaceans demonstrate a better match for maximum sensitivity to bioluminescence than to downwelling light. Accepted: 29 June 1999     

Characterization of photoreceptor cell types in the little brown bat Myotis lucifugus (Vespertilionidae)

We report the expression of three visual opsins in the retina of the little brown bat (Myotis lucifugus, Vespertilionidae). Gene sequences for a rod-specific opsin and two cone-specific opsins were cloned from cDNA derived from bat eyes. Comparative sequence analyses indicate that the two cone opsins correspond to an ultraviolet short-wavelength opsin (SWS1) and a long-wavelength opsin (LWS). Immunocytochemistry using antisera to visual opsins revealed that the little brown bat retina contains two types of cone photoreceptors within a rod-dominated background. However, unlike other mammalian photoreceptors, M. lucifugus cones and rods are morphologically indistinguishable by light microscopy. Both photoreceptor types have a thin, elongated outer segment. Using microspectrophotometry we classified the absorption spectrum for the ubiquitous rods. Similar to other mammals, bat rhodopsin has an absorption peak near 500 nm. Although we were unable to confirm a spectral range, cellular and molecular analyses indicate that M. lucifugus expresses two types of cone visual pigments located within the photoreceptor layer. This study provides important insights into the visual capacity of a nocturnal microchiropteran species.     

Phytochrome-mediated effects of near-ultraviolet radiation in the induction of flowering in etiolated Lemna paucicostata T-101, a short-day plant

Induction of flowering of etiolated Lemna paucicostata Hegelm. T-101, a short-day plant, was inhibited by far-red (FR) or blue light (BL) applied at the beginning of a 72-h inductive dark period which was followed by two short days. In either case the inhibition was reversed by a subsequent exposure of the plants to near-ultraviolet radiation (NUV), with a peak of effectiveness near 380 nm. Inhibition by BL or FR and its reversion by NUV are repeatable, i.e., NUV is acting in these photoresponses like red light although with much lower effectiveness. Thus, it is considered that NUV acts through phytochrome and no specific BL and NUV photoreceptor is involved in photocontrol of floral induction on this plant.Abbreviations BL blue light - FR far-red light - NUV near ultraviolet radiation - P red-absorbing form of phytochrome - P_fr far-red absorbing form of phytochrome - R red light     

Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae)

Sexual communication between male and female fireflies involves the visual detection of species-specific bioluminescent signals. Firefly species vary spectrally in both their emitted light and in the sensitivity of the eye, depending on the time when each is active. Tuning of spectral sensitivity in three firefly species that occupy different photic niches was investigated using light and electron microscopy, microspectrophotometry, and intracellular recording to characterize the location and spectral absorption of the screening pigments that filter incoming light, the visual pigments that receive this filtered light, and the visual spectral sensitivity. Twilight-active species had similar pink screening pigments, but the visual pigment of Photinus pyralis peaked near 545 nm, while that of P. scintillans had a λ_max near 557 nm. The night-active Photuris versicolor had a yellow screening pigment that was uniquely localized, while its visual pigment was similar to that of P. pyralis. These results show that both screening and visual pigments vary among species. Modeling of spectral tuning indicates that the combination of screening and visual pigments found in the retina of each species provides the best possible match of sensitivity to bioluminescent emission. This combination also produced model sensitivity spectra that closely resemble sensitivities measured either with electroretinographic or intracellular techniques. Vision in both species of Photinus appears to be evolutionarily tuned for maximum discrimination of conspecific signals from spectrally broader backgrounds. Ph. versicolor, on the other hand, appears to have a visual system that offers a compromise between maximum sensitivity to, and maximum discrimination of, their signals. Accepted: 29 September 1999     

Colour perception of single and mixed monochromatic lights in the blowfly Lucilia cuprina

Colour perception of spectral lights and mixtures of two monochromatic lights of blue and yellow wavelengths was studied in the blowfly Lucilia cuprina by using a generalization test in which the fly had to compare these lights in memory with coloured papers (blue, green, yellow and red) represented in the test array. Flies trained to a monochromatic light in the wavelength range of 429–491 nm responded to blue; those trained to 502–511 nm to green; and those trained to 522–582 nm to yellow. The maximal generalization for blue was found at 429 nm and that for yellow at 543 nm. Flies trained to the mixtures responded neither to blue, green nor yellow, when the blue component was mixed with the yellow component in a ratio of approximately 1 3. It seems that the fly perceives the mixtures as a neutral or an achromatic light. Colour loci of coloured papers, spectral lights and mixtures of two monochromatic lights used formed blue, yellow and neutral clusters in a colour triangle with respect to generalization responses to test colours.     

Pollen grains adhere to the moist mouthparts in the flower visiting beetle Cetonia aurata (Scarabaeidae, Coleoptera)

Flower visiting beetles possess numerous structural adaptations of their mouthparts to adhere and ingest pollen grains. Using a Cryo-SEM approach the examination of the mouthparts in rapidly frozen Cetonia aurata (Scarabaeidae) indicates a previously unknown technique of pollen uptake in Coleoptera. Cryo-SEM micrographs of the mouthparts reveal a fluid covering the bristles on the buccal surface. In this way the bristles of the galeae form a wet brush which represents the primary organ of pollen uptake. The fluid improves adhesion of pollen to bristles lacking any specialized adhering surface or highly sculptured cuticle as present in other pollen feeding Coleoptera. The well developed mola region of the otherwise non-biting mandibles of C. aurata indicates that these beetles open pollen grains mechanically before ingestion. Examination of gut content demonstrated that crushed and intact pollen occur in all regions. The Cryo-SEM method represents a new approach to study functional morphology including the interaction of microstructures and fluids on cuticular surfaces of insects. Handling editor: Gimme Walter     

Photoreceptor spectral sensitivity in island and mainland populations of the bumblebee, <Emphasis Type=Italic>Bombus terrestris</Emphasis>

Most species of flower-visiting Hymenoptera are trichromatic, with photoreceptor spectral sensitivity peaks in the UV, blue and green regions of the spectrum. Red flowers, therefore, should be relatively difficult to detect for such insects. Nevertheless, in population biological studies in the bumblebee, Bombus terrestris, the Sardinian island population (B. t. sassaricus) displayed significantly higher responses to red artificial flowers (in tests of innate colour choice and detectability) than several mainland populations of the same species (Chittka et al. in Cognitive ecology of pollination, pp 106–126, 2001; Popul Ecol 46:243–251, 2004). Since there is relatively little physiological data on population differences in sensory systems, we used intracellular recording to compare photoreceptor spectral sensitivity in B. t. sassaricus and the southern European and Mediterranean population, B. t. dalmatinus. The results show both populations to be UV–blue–green trichromats, but with a small but significant increase in long-wave sensitivity in island bees. Spectral peaks were estimated at 348, 435 and 533 nm (B. t. dalmatinus) and 347, 436 and 538 nm (B. t. sassaricus) for UV, blue and green receptors, respectively. There were no significant differences in UV and blue receptor sensitivities. We found no photoreceptors maximally sensitive to red spectral light in the Sardinian population and model calculations indicate that the behavioural population differences in colour responses cannot be directly explained by receptor population differences. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Stressful colours: corticosterone concentrations in a free-living songbird vary with the spectral composition of experimental illumination

Organisms have evolved under natural daily light/dark cycles for millions of years. These cycles have been disturbed as night-time darkness is increasingly replaced by artificial illumination. Investigating the physiological consequences of free-living organisms in artificially lit environments is crucial to determine whether nocturnal lighting disrupts circadian rhythms, changes behaviour, reduces fitness and ultimately affects population numbers. We make use of a unique, large-scale network of replicated field sites which were experimentally illuminated at night using lampposts emanating either red, green, white or no light to test effect on stress hormone concentrations (corticosterone) in a songbird, the great tit (Parus major). Adults nesting in white-light transects had higher corticosterone concentrations than in the other treatments. We also found a significant interaction between distance to the closest lamppost and treatment type: individuals in red light had higher corticosterone levels when they nested closer to the lamppost than individuals nesting farther away, a decline not observed in the green or dark treatment. Individuals with high corticosterone levels had fewer fledglings, irrespective of treatment. These results show that artificial light can induce changes in individual hormonal phenotype. As these effects vary considerably with light spectrum, it opens the possibility to mitigate these effects by selecting street lighting of specific spectra.     

Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L

The honeybee, Apis mellifera L., is one of the living creatures that has its colour vision proven through behavioural tests. Previous studies of honeybee colour vision has emphasized the relationship between the spectral sensitivities of photoreceptors and colour discrimination behaviour. The current understanding of the neural mechanisms of bee colour vision is, however, rather limited. The present study surveyed the patterns of chromatic information processing of visual neurons in the lobula of the honeybee, using intracellular recording stimulated by three light-emitting diodes, whose emission spectra approximately match the spectral sensitivity peaks of the honeybee. The recorded visual neurons can be divided into two groups: non-colour opponent cells and colour opponent cells. The non-colour opponent cells comprise six types of broad-band neurons and four response types of narrow-band neurons. The former might detect brightness of the environment or function as chromatic input channels, and the latter might supply specific chromatic input. Amongst the colour opponent cells, the principal neural mechanism of colour vision, eight response types were recorded. The receptive fields of these neurons were not centre surround as observed in primates. Some recorded neurons with tonic post-stimulus responses were observed, however, suggesting temporal defined spectral opponency may be part of the colour-coding mechanisms.     

Learning and discrimination of coloured papers in the walking blowfly,Lucilia cuprina

Summary A new training and testing paradigm for walking sheep blowflies, Lucilia cuprina, is described. A fly is trained by presenting it with a droplet of sugar solution on a patch of coloured paper. After having consumed the sugar droplet, the fly starts a systematic search. While searching, it is confronted with an array of colour marks consisting of four colours displayed on the test cardboard (Fig. 1). Colours used for training and test include blue, green, yellow, orange, red, white and black.Before training, naive flies are tested for their spontaneous colour preferences on the test array. Yellow is visited most frequently, green least frequently (Table 2). Spontaneous colour preferences do not simply depend on subjective brightness (Table 1).The flies trained to one of the colours prefer this colour significantly (Figs. 5 and 9–11). This behaviour reflects true learning rather than sensitisation (Figs. 6–7). The blue and yellow marks are learned easily and discriminated well (Figs. 5, 9, 11). White is also discriminated well, although the response frequencies are lower than to blue and yellow (Fig. 11). Green is discriminated from blue but weakly from yellow and orange (Figs. 5, 9, 10). Red is a stimulus as weak as black (Figs. 8, 9). These features of colour discrimination reflect the spectral loci of colours in the colour triangle (Fig. 14).The coloured papers seem to be discriminated mainly by the hue of colours (Fig. 12), but brightness may also be used to discriminate colour stimuli (Fig. 13).