Limits to the salience of ultraviolet: lessons from colour vision in bees and birds
1 Department of Environmental Biology and Department of Botany, University of Guelph, Guelph, ON, Canada N1G 2W1,
2 Biozentrum, Zoologie II, Am Hubland, Universität Würzburg, 97074 Würzburg, Germany and
3 Faculty of Science, Monash University, Victoria 3800, Australia
*Author for correspondence (e-mail: adrian.dyer{at}sci.monash.edu.au)
Accepted April 19, 2001
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Summary |
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Key words: colour constancy, evolution, flower colour, illumination, insect.
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Introduction |
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Numerous botanical studies have examined the ultraviolet reflections from flowers without reference to the colour perception of the flowers visitors (see references in Kevan and Backhaus, 1998). Studies of ultraviolet patterns from flowers may have some value for taxonomic purposes. For ecological and ethological analyses, however, this approach is erroneous (Kevan, 1972; Kevan, 1978; Kevan, 1979a; Kevan, 1983; Kevan and Backhaus, 1998; Chittka, 1992; Chittka and Menzel, 1992; Chittka et al., 1994; Menzel and Shmida, 1993). It seems that some vertebrate biologists have also fallen into similarly inappropriately constrained approaches by recording ultraviolet reflections from objects without considering the rest of their subjects colour vision. Investigation of the ultraviolet channel of a visual system alone can only provide limited information about the reflectance spectra of a stimulus, as this type of data does not consider the multiple photoreceptors involved in colour vision (Kevan, 1979a).
Colour measurement requires that the reflectance spectra of a stimulus is measured across the entire wavelength range of an animals visual system and that those data are plotted in an appropriate colour space. For humans, various colour spaces have been proposed, and the science of colorimetry is well developed (Wyszecki and Stiles, 1967). Colour spaces have also been developed for honeybees (Apis mellifera) (e.g. Daumer, 1956; Backhaus, 1991) and trichromatic insects in general (Kevan, 1972; Kevan, 1978; Kevan, 1983; Chittka, 1992; Vorobyev and Brandt, 1997). These colour spaces started with relatively simple Maxwell triangles and have progressed through to colour planes that explain the colour opponency mechanism that appears to operate in many species of bees (Backhaus, 1991; Chittka, 1992; Vorobyev and Brandt, 1997). Tetrachromatic colour vision based on four receptor classes, for example, the colour visual systems of goldfish (Carassius auratus) and pigeons (Columba livia), require the construction of a tetrahedron colour space (e.g. Goldsmith, 1990; Neumeyer, 1991; Neumeyer, 1992; Neumeyer, 1998; Vorobyev et al., 1998).
For the trichromatic colour vision of humans the problem of representing colour brightness creates a fourth dimension in colour space, and the possibility exists that tetrachromatic colour vision requires a fifth dimension. Bees lack brightness perception so that the colour space can be accurately represented in two dimensions (Backhaus, 1992). Some animals have been shown to have more than four waveband-specific optical sensors (Briscoe and Chittka, 2001). For example, some butterflies may have five colour receptors (Arikawa et al., 1987), and stomatopod Crustacea show a remarkable array of ten or more narrow band sensors (Cronin and Marshall, 1989; Cronin et al., 1994). It remains unknown whether all these receptors are somehow interconnected neurally to provide the integration of information that is required for colour vision, or whether some of the individual sensors provide waveband-specific information that is processed neurally outside the paradigms of colour vision.
Vision and colours that include ultraviolet have excited great scientific interest, but is special interest warranted from evolutionary and ecological standpoints? The answer to this appears to be no, as ultraviolet-sensitive receptors appear to be extremely common in insects, crustaceans, avians, fishes and reptiles, as well as being present in some mammals and amphibians (Jacobs, 1992; Tovée, 1995). Rather, it appears that vision in the red part of the spectrum is more derived and special (Briscoe and Chittka, 2001).
Ever since the discovery of ultraviolet vision in ants by Sir J. Lubbock (Lord Avebury) in the 19th century (Lubbock, 1881), and in bees a few decades later (Kühn, 1924), it has been assumed by many workers that ultraviolet sensitivity must be an adaptation to a particular lifestyle. This is because, until recently, the only other species whose vision was understood in detail was Homo sapiens, which lacks ultraviolet vision. Comparisons between remotely related taxa (such as bees and humans), however, make little sense in interpreting adaptation (Chittka and Dornhaus, 1999).
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Evolution and phylogeny |
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To understand why animals have particular sensory capacities, such as ultraviolet sensitivity, we must compare these animals with close relatives that do not share the same lifestyle. For example, to explore whether ultraviolet vision in bees is an adaptation to flower visitation, it is necessary to investigate insects with lineages divergent from those of bees at a time before there were flowers, and from lineages that do not feed from flowers today. Chittka (Chittka, 1996) made such an analysis and found that ultraviolet receptors with maximum sensitivity (max) around 340nm are present not only throughout the Pterygota (winged insects) but also in Chelicerata and several Crustacea. Phylogenetic analysis reveals that the Cambrian ancestor of Chelicerata, Crustacea and Insecta probably saw ultraviolet light (Chittka and Briscoe, 2001). In addition, it can be inferred that these ancient arthropods had receptors most sensitive in the green part of the spectrum (
max around 520nm) and that a blue receptor with a sensitivity around 430nm was acquired only later, possibly in Mandibulata, but certainly in Pterygota. Thus, the input layer of bee color vision with three colour receptor types (see Fig.1) dates back at least to the Devonian (>360 million years ago).
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Ecology and ethology |
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"The primary necessity which led to the development of the sense of colour was probably the need of distinguishing objects much alike in form and size, but differing in important properties, such as ripe and unripe, or eatable and poisonous fruits, flowers with honey [=nectar] or without, the sexes of the same or closely allied species. In most cases the strongest contrast would be the most useful, especially as the colours of objects to be distinguished would form but minute spots or points when compared with the broad masses of tint of sky, earth, or foliage against which they would be set." (Wallace 1878, p. 243).
Wallace brings into focus the importance of colour contrast. Studies with honeybees have shown that the detectability of a stimulus (a training target or a flower) depends on the reflections of the background against which neural colorimetric comparisons are made (Backhaus, 1993; Giurfa et al., 1996). The sensitivity of bees, bats and birds to ultraviolet radiation exceeds that in other spectral ranges (von Helversen, 1972; Burkhardt and Maier, 1989; Goldsmith, 1994; Maier, 1992; Winter and von Helversen, 2001). At least in bees, this is simply a consequence of the physiological photoreceptor adaptation process: because daylight is relatively weak in the ultraviolet (and many natural subtrates reflect ultraviolet light poorly), short-wave receptors upregulate their sensitivity (Kevan, 1978; Burkhardt and Maier, 1989) to increase photon capture (Chittka, 1997). Relatively high ultraviolet sensitivity has led some scientists to assume that ultraviolet signals might be highly detectable for some animals. For example, Lutz (Lutz, 1924) suggested that flowers with ultraviolet reflectance should be more readily detectable than other flowers, but lamented that he knew "of no measure of the readiness with which they [the flowers] were found". Since then, many authors have assumed that ultraviolet-reflecting flowers should be particularly easy for insects to find, but no one has quantified detectability, even though colorimetric differences between flowers have been presented in appropriately designed colour spaces (Daumer, 1958; Kevan, 1972; Kevan, 1983; Chittka et al., 1994; Kevan and Backhaus, 1998). Recently developed quantitative measures can be used to determine how readily bees detect flowers of different colours. The results from their application indicate a complex picture: whether ultraviolet reflectance increases or decreases the detectability of an object for a bee depends on the reflectance in other parts of the spectrum.
One way to measure the detectability of a target is to let bees fly into a Y-shaped maze, one of whose arms contains the target and the other does not. One can then determine the probability of choosing the correct arm, depending on the spectral qualities and size of the stimulus. Using this method it was found that in honeybees, detectability of targets from a distance is independent of ultraviolet-specific contrast between target and background (Giurfa et al., 1996). Rather, bees seem to require colour contrast (using input from all three bee receptor types) to find the target. The relative stimulation of the green receptor (target versus background) facilitates detectability, but if colour contrast is absent, bees have difficulty detecting the target at all, even if green contrast is present. Thus, if adding ultraviolet to a given reflectance spectrum diminishes the colour contrast of that target to the background, ultraviolet could actually impair detectability.
The effect of ultraviolet in diminishing the detectability of targets was recently demonstrated using white targets with and without ultraviolet reflectance (Spaethe et al., 2001). To quantify the readiness with which differently coloured targets are detected, the search time taken by bees to find the flowers situated at variable locations within a flight arena was determined. White targets with ultraviolet reflectance in front of a green, foliage-type background yield a strong brightness contrast as well as a strong green contrast. Nevertheless, search times for such flowers were approximately twice as long as those for the white model flowers without ultraviolet reflectance. Daumer (Daumer, 1956) also noted that honeybees did not respond quickly to bee-white stimuli, and Engländer (Engländer, 1941) found that training honeybees to detect white against an ultraviolet target was very difficult. The reason is that, for bees, bee-white-reflecting flowers make poor colour contrast with a green foliage-type background, and that bees ignore brightness differences in the detection and identification of targets (Backhaus, 1992; Kevan et al., 1996), unless the targets are small (Spaethe et al., 2001).
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Colour constancy |
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How is colour constancy implemented on a mechanistic level? One possible mechanism of colour constancy is chromatic adaptation, where the spectral sensitivity of different photoreceptor classes is invariable, but the relative sensitivity of photoreceptors vary to achieve constancy following the von Kries coefficient law (Hurvich, 1981). Theoretical analyses of von Kries colour constancy show that the ability of a visual system to correct for changes in illumination colour may be limited by the spectral breadth and overlap of different photoreceptor classes (Worthey and Brill, 1986; Dyer, 1999a). In the honeybee, the absorption spectra of the blue and green photoreceptors overlap extensively with that of the ultraviolet photoreceptor. This is explained by the secondary ß-peak of the visual pigments (Fig.1), which is caused by the absorption of short-wavelength radiation by the cis-band of the chromophore. Dyer (Dyer, 1999a) demonstrated that this increased spectral overlap of photoreceptors limits von Kries-type colour constancy for the honeybee, especially for pure ultraviolet colours. Fig.3 shows the predicted colour shift of loci in a hexagon colour space for a trichromatic insect with ultraviolet, blue and green photoreceptors (based on photoreceptors maximally sensitive at 350, 440 and 540nm) when considering spectrally variable illumination and von Kries colour constancy (Dyer, 1999b). The contours are derived from 99 theoretical stimuli that provide a good coverage of bee colour space (Dyer, 1998) and the colour shift of their loci for illumination varying from a correlated colour temperature of 480010000K (considering von Kries colour constancy). The predicted colour shift is small in the centre right-hand side of colour space, but is larger for pure ultraviolet-coloured flowers lying on the left-hand side of colour space. Indeed, these flowers are rare in nature (Chittka et al., 1994; see Fig.4), although it is also possible that their scarcity can also be attributed to phylogenetic or biochemical constraints (Chittka, 1997).
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The possibility of variations in atmospheric O3 concentration affecting the distribution of ultraviolet radiation available as illumination for insects has been suggested (Utech and Kawano, 1975; Meyer-Rochow and Järvilehto, 1997). Ozone in the stratosphere is chiefly responsible for the attenuation of short-wavelength solar radiation reaching the Earths surface (Kondratyev, 1969). Ozone concentration is naturally variable with both season and latitude, and may also be affected by the release into the atmosphere of carbon dioxide, chlorofluorocarbons, methane and nitrogen oxides (Molina and Rowland, 1974; Alyea et al., 1975; Bruce, 1986; Bowman, 1988). Concerns over the biological damage that can be caused by high-energy, short-wavelength radiation have led to widespread public awareness of O3 depletion and increased ultraviolet radiation levels (Bowman, 1988; Diffey, 1991). The potential effects of variations in atmospheric O3 concentration on colour vision in insects were evaluated with computational models (Dyer, 1999c). The results showed that even a very large variation in O3 concentration would have only a negligible effect on colour vision. This is because, within the range of visual pigments, variations in O3 concentration mainly affect 300320nm radiation, and photoreceptor sensitivity to these wavelengths is relatively low (Fig.1). Also, the relative amount of 300320nm radiation in natural daylight is very small compared with the rest of the visible spectrum (Henderson, 1977) and, hence, variations in illumination levels at these wavelengths have only a very small influence on the relative stimulation of photoreceptors. However, the findings of Dyer (Dyer, 1999c) do not exclude the possibility of increases in 300320nm radiation affecting wavelength-specific behavioural mechanisms in some animals. For example, the regulation of circadian physiology in some mammals appears to be controlled by ultraviolet radiation (Brainard et al., 1994). The ultraviolet photoreceptor is sensitive to polarised radiation in some arthropods, fish and amphibians (Wehner, 1984), and the phototactic escape responses in some insects shows a maximum sensitivity in the ultraviolet (Wehner, 1981). Recently Mazza et al. (Mazza et al., 1999) have reported that thrips (Caliothrips phaseoli) were able to perceive changes in the relative quantity of 290320nm radiation, although they suggest that the mechanism for this detection may be through receptors other than visual ones.
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Innate responses to specific colours |
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Even though honeybees can be trained to distinguish between targets that are equally reflective at blue and green wavelengths and differ only in ultraviolet reflection, or to targets that reflect only ultraviolet radiation, their capacity to do so does not fall outside colour vision and colour opponency coding. It is expected that other animals that can be trained to recognise colours will also process ultraviolet wavelengths as they would any other primary-coloured signal. The importance of ultraviolet reflections is known for floral recognition by insects, even in the few flowers that are pure ultraviolet-coloured for bees (e.g. Papaver spp.). It is worth referring to the observation of Lutz (Lutz, 1924) who wrote as follows: "After finding that there are numerous ultraviolet flowers and that flower-visiting insects are keenly sensitive to ultraviolet, I supposed that it would follow, as the night the day that ultraviolet flowers would be... more abundantly visited than those which reflected only ordinary colors... but certainly they are not... more abundantly visited." Lutz (Lutz, 1924) referred to ultraviolet reflections as apparently non-adaptive, but in doing so, he failed to recognise that it was ultraviolet in combination with other reflections from flowers that elicited flower-visiting behaviour.
The absence of ultraviolet reflection from almost all white flowers (as they appear to human beings) perhaps has more special meaning because if flowers reflected ultraviolet, blue and green radiations in similar proportions they would occupy much the same colour locus in colour space for trichromatic insects as vegetation. This means that these flowers would be difficult to detect because brightness is not coded by bees (Kevan et al., 1996). The rarity of pure ultraviolet-reflecting flowers might also be partially explained by limitations of colour constancy in insects, as explained above. Indeed, pure ultraviolet-reflecting flowers are very rare in nature, and those that are ultraviolet-reflective in the insect trichromatic colour space appear red to humans. They represent only 1.6% of 1063 flower reflection spectra measured by Chittka et al. (Chittka et al., 1994; Fig.4).
Ultraviolet reflections are also important in mate recognition in butterflies (Lepidoptera) (Knüttel and Fiedler, 2001), dragonflies and other insects (Silberglied, 1979). In vertebrates, for example birds, ultraviolet reflections are important in mate recognition (Bennett et al., 2001) and food detection (Church et al., 2001), but not outside the purview of colour vision in general. In stomatopod shrimps, it has been suggested that ultraviolet sensitivity might be involved in the detection of objects swimming overhead because of contrast with the bright, ultraviolet-rich skylight (Cronin et al., 1994). Similarly, ultraviolet-bright patches have been invoked as representing escape routes for insects (Menzel, 1979), but other wavebands may also be involved (Kevan, 1979b). Ultraviolet photoreceptors in some insects are used to analyse polarised light, but this task is performed by either blue or green receptors in other insects (Labhart and Meyer, 1999).
In the blue waveband there are only a few examples of special functions. Training experiments with naïve honeybees show that blue targets are learned faster than targets of other colours, such as ultraviolet or green, but less rapidly than targets that stimulate both ultraviolet and blue receptors (Menzel, 1967; Menzel, 1985; Giurfa et al., 1995). Blue light appears to be of primary importance in detection of polarised light in some Orthoptera (Labhart and Meyer, 1999). For some butterflies (Papilio spp. and Pieris brassicae), it has been suggested that blue reflections are important in eliciting feeding activity (Ilse, 1928; Ilse and Vaidya, 1956; Scherer and Kolb, 1987a).
The reflection of green radiation and the green receptor is known to be extremely important in the vision of insects, especially for honeybees. It is important in the detection of motion and in the recognition of size, shape and form (Dafni et al., 1997; Lehrer, 1997). Coloured targets of equal size that combine colour contrast with contrast in the green part of the spectrum (with respect to their backgrounds) are visible to honeybees from approximately three times the distance as coloured targets that lack green contrast (Giurfa et al., 1996).
It has been suggested that green reflections stimulate butterflies to oviposit (Kolb and Scherer, 1982; Scherer and Kolb, 1987b). Green light has also been suggested as important in the detection of polarised light by some beetles (Coleoptera) (Labhart and Meyer, 1999).
Naïve hoverflies (Eristalis tenax Diptera: Syrphidae) land only on human-yellow targets (Ilse, 1949; Lunau, 1988) although they can be trained to choose other coloured targets (Kugler, 1950). Even so, proboscis extension for feeding is elicited only by stimulation between 520 and 600nm, corresponding to the spectral reflection of pollen (Lunau and Wacht, 1994). Lunau and Maier (Lunau and Maier, 1995) discuss these phenomena on the basis of what is known about the physiology of colour vision in Diptera.
Red reflections have received special attention because some physiologists and ecologists have asserted that bees, and even insects in general, are red-blind (see references in Chittka and Waser, 1997). However, not only are there multiple insect species with specialised red receptors (Bernard, 1979; Peitsch et al., 1992, Briscoe and Chittka, 2001), but red flowers are not invisible to insects that lack a specific red receptor, and trichromatic insects including the honeybee do visit red flowers (Chittka and Waser, 1997).
Red stimuli also elicit feeding responses from some butterflies (Gonopteryx rhamni and Pieris brassicae; Kühn and Ilse, 1925; Scherer and Kolb, 1987a). The red bowl-shaped flowers of the Mediterranean are pollinated extensively by Amphicoma beetles (Dafni et al., 1990), and these animals possess red receptors (Briscoe and Chittka, 2001).
The meaning of black objects (achromatic stimuli of very low reflectance throughout the entire spectrum) is less clear and has rarely been examined with respect to insect or bird colour vision. Certain flowers have black patterns within their corollas (e.g. Iris spp.), and presumably these patterns provide information to flower visitors when perceived in relation to the rest of the corollas reflectance spectra. Black flowers are almost unknown in nature. One possible exception is the putatively hummingbird-pollinated Lisianthus spp. of southern Mexico (Markham et al., 2001). Fruits that appear black to humans are common, although some of these fruits reflect ultraviolet (Burkhardt, 1982).
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Biogeography and floral forms |
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Concluding remarks |
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Acknowledgments |
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