Visual pigments and environmental light

Vision Res. Vol. 24, No. 11, pp. 1539-1550, 1984 Printed in Great Britain

0042-6989/84 $3.00+ 0.00 Pergamon Press Ltd

VISUAL PIGMENTS A N D ENVIRONMENTAL LIGHT J. N. LYTHGOE Department of Zoology, Bristol University, Woodland Road, Bristol BS8 lUG, England Abstract--The visual pigments in the rods do not have a spectral absorption that gives them maximal sensitivity. The visual pigments of "deep sea" fish are an exception for these do match the environmental light to give maximum sensitivity. At the low light intensities at which the rods operate, it is the number of photons that go to make up each element of the image that limits the ability of the eye to discriminate detail and contrast. Chemically induced isomerisation of the visual pigment molecule may cause spurious visual signals that limit the ability of the eye to detect contrasts in very dim light. In bright light the spurious visual signals become insignificant in number compared to the true photon-induced visual signals. Compared to the rods, cone visual pigments do match the spectral properties of the environment except that there appear to be no visual pigments with an absorption maximum beyond the 625 nm porphyropsins in cones. U.V. absorbing pigments are know in invertebrates, birds and fish that live in very shallow water. Animals have photoreceptors in parts of the body other than the eyes. In vertebrates these sites include the pineal, chromatophores, brain, skin and harderian gland. There is evidence based on immunocytochemistry and action spectra that at least some of the skin and pineal receptors contain visual pigments, but like those of the rods, these do not match the spectral quality of the environmental light. Visual pigments

Visualnoise

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INTRODUCTION Almost as soon as it became known that the spectral absorption of visual pigments could vary between one animal and the next, there was speculation that they might be adapted to capture the maximum amount of light from the visual scene and hence enhance visual sensitivity. The prediction by Bayliss et al (1936) and Clarke (1936) that deep sea fish might have visual pigments more sensitive to short wave blue light than their inshore and terrestrial counterparts proved to be so exactly correct (Denton and Warren, 1957; Munz, 1958; Fernandez, 1979) that the idea that the visual pigments in general had evolved to confer the maximum sensitivity for the particular environment became fixed. However later work on the scotopic pigments of fish living in other environments that are scarcely less homochromatic than the deep sea, but which are relatively more transparent to longer wavelengths, began to suggest that the visual pigments did not always match the spectral properties of the light environment (for reviews see Lythgoe, 1972, 1980). Indeed the most careful calculations have only tended to confirm the mismatch between the scotopic visual pigment and the spectral properties of the environment, both on land and underwater (Dartnall, 1975). The development of microspectrophotometry (MSP) has allowed the study of visual pigment ecology to be extended to colour vision, and it is becoming apparent that colour vision, at least at the receptor level, is related to the ecology of the animal.

Extra-retinal receptors

Colour vision

Of course colour vision requires at least two types of photoreceptor each most sensitive to a different region of the spectrum, and they cannot both match the spectral radiance of the ambient light. Indeed it appears to be valuable to many animals to possess a colour vision channel in regions of the spectrum where there is very little ambient light. A good example concerns the u.v. receptors known to be present in many insects, and possibly in birds and fish as well, where the number of photons per unit frequency interval is only about 5 ~ of those at 550 nm (Dartnall, 1975). Insects may be particularly rewarding to study because visual tasks are comparatively well defined. In comparison the variety of visual tasks that a primate performs seems enormous, and even though their visual pigments have been carefully investigated (Bowmaker and Dartnell, 1980; Bowmaker et al., 1980; Jacobs, 1981), we are still some way from understanding their significance at the ecological level, perhaps because the cone complement of very few other mammals have yet been measured. Fish are one of the most interesting groups to study because they live in an environment with very pronounced optical properties. Seen from above the surface an expanse of water borrows most of its colour from the sky reflected from the water surface. But underwater it becomes apparent that the water itself is coloured, and the colour can vary from the deep blue of clear ocean water to red-brown in peat-laden lakes and rivers.

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J.N. LYTHGOE

T H E STATISTICAL A P P R O A C H Pure water itself is bue, this is partly due to absorption and partly due to Rayleigh scatter. Green At moderate and low intensities it is the number of phytoplankton can have an important influence in nutrient-rich water, especially in the summer where photons that go to make up the image that limits the temperatures are high and the days are long. The amount of information that can be got from it. The yellow products of vegetable decay, both from the photoreceptors themselves act as photon counters phytoplankton itself and from run-off from land are and the business of visual discrimination is basically the colour of tea. In small quantities these yellow a statistical problem (Pirenne, 1967; Barlow, 1964; substances (gelbstoffe), in conjunction with the blue Land, 1981). As in any statistical sampling, the larger of pure water, impart a green colour to the water. In the sample counted, the finer the differences between higher concentrations they cause the water to trans- samples that can be detected. It is therefore possible mit relatively more at long wavelengths and in to improve the detection of the difference between strongly stained waters like those of parts of the two elements of the retinal image either by increasing Amazon and some Scottish lochs the water is most the number of photons sampled (increasing the transparent to the near infra-red (Muntz, 1978; brightness) or by increasing the relative difference Muntz and Mouat, 1984). Although the colour of between the number of photons in each image elenatural water does vary from day to day, it is ment (increasing the contrast). Land (1981), has used generally true that the water of the open oceans and statistical methods based on the Poisson distribution near arid land masses transmits light maximally at to estimate the sample size required to make a shorter wavelengths than inshore water near fertile particular contrast discrimination at various probaterritory, and fresh water generally transmits max- bility levels between 80 and 99~o. For example at the imally at longer wavelengths still. At any particular 95~ level a 100-fold decrease in brightness can be wavelength the absorption of light with depth is compensated for by a 10-fold increase in contrast. At exponential, and this has the effect that as the depth the photoreceptor level contrast can be improved by increases the spectral bandwidth of the available light arranging that the visual pigment is most sensitive at becomes ever narrower and vision must function wavelengths where the relative photon catch between within a narrower spectral range (Jerlov, 1976; the object and its background is greatest (Lythgoe, 1980). It is also worth considering that the narrower Lythgoe, 1979 for reviews). Unlike the underwater environment the available the spectral sensitivity curve of the photoreceptor, the electromagnetic radiation on land extends far beyond more precisely it can be tuned to increase contrast; the narrow band that we see as light. The fact that but the number of photons that are sampled will be within each 1 nm waveband, there is more energy in correspondingly lower. The number of photons in each sample can be sunlight available for vision around 500 nm, than elsewhere in the electromagnetic spectrum, has been increased in other ways such as by increasing the presented as an example of the spectral adaptation of area of the retinal image that is sampled, or by rhodopsin to maximise visual sensitivity. The phe- increasing the time over which the sample is collected. nomenon of the Purkinje shift has in the past been Both these can be increased during dark adaptation, explained on grounds of visual sensitivity. Seen from but at the expense of acuity and the ability to see inside a lighted room the twilight sky outside looks moving objects. An animal such as a bat that capdark blue, and in late evening it is blue objects that tures small, fast moving objects, at night is faced with an impossible task, and has turned instead to acoustic appear the brightest. Nowadays it is quite uncommon to see a night-time scene without benefit of artificial detection to capture its prey. In visual systems working at very low light levels light, but a spurious memory is kept alive by countless films and TV shows where blue filters and something of the order of 10 rhodopsin molecules, under-exposed prints are used to represent night. It amongst the many millions contained in the sumcomes as something of a surprise to learn that the mation pool of about 300 rods, are all that need to ambient light at night is relatively richer in the longer be isomerised to detect a light source. (Rodieck, 1973; wavelengths than is daylight (McFarland and Munz, Ripps and Weale, 1976); and it seems reasonable to 1975; Lythgoe, 1979). Indeed Dartnall (1975) has think that very occasional isomerisations triggered by shown that when the spectrum of sunlight is agents other than photons will severely degrade viexpressed in the physiologically correct units of sual performance. Two possibilities are that infra-red photons per unit time per unit area per equal quanta, which come from within the eye itself, very frequency interval, even sunlight has its maximum occasionally induce vision-like isomerisations of the visual effectiveness at around 1500 nm rather than chromophore; and that there are chemically-induced around 500 nm. The almost universal Purkinje shift spontaneous 11-cis to all-trans isomerisations within in sensitivity towards shorter wavelengths as dark the visual pigment molecule that are indistinguishable adaptation proceeds and the rods take over from the in their effect from those that follow the absorption cones cannot therefore be explained in terms of of a photon. The black-body radiation from bodies at physsensitivity and other kinds of explanation must be iological temperatures is greatest at 10-15~, but sought.

Visual pigments and environmental light there is significant radiation at shorter wavelengths, although this does not extend in any significant way into the visible. At the relatively long wavelengths of the near infra-red the quanta do not have enough energy by themselves to trigger visual isomerisations (see Dartnall, 1975 for a discussion). However Stiles (1948) and Barlow (1957) have developed the suggestion that thermal energy from molecular movements might contribute some energy to the visual pigment molecule, such that energy from this source together with the energy from an infra-red quantum combine to give enough to isomerise the chromophore. At present this idea is difficult to test because at wavelengths longer than about 700 nm the absorption of visual pigment is too small to be measured. However if such a system is significant one might expect that fish living in cold fresh water would have visual pigments of longer ~max than those of reasonably close relatives living in warm tropical waters. It is possible that there is some evidence to support this view (Schwanzara, 1967) but it is by no means conclusive. Groenendijk et al. (1980), have shown that when the 11-cis chromophore is exposed to homogenised disc-protein or in particular to phosphatidylethanolamine there is a dark isomerisation to the all-trans form, that would normally require the absorption of a photon to bring about. If such dark isomerisations do occur within the normal living outer segment, the effect is likely to be indistinguishable from a true visual response. Careful measurements of the number of photons required for a light to be just detectable point to the conclusion that between 4 and 20 photons are required to be absorbed within the retinal integration time to get a reasonably reliable just detectable response (see Ripps and Weale, 1976, for a review). It might be that this number of photons is required to distinguish the light signal from the constant background noise of "spontaneous" isomerisations. In effect the level of dark isomerisations sets the lower threshold for vision at very low light levels. For a molecule to induce the dark isomerisation of the 11-cis chromophore, it must first be able to reach it within the rhodopsin molecule. Some molecules such as hydroxylamine (Wald et al., 1955), sodium borohydride (Bownds and Wald, 1965) and ethanolamine (Fager et al., 1979), are able to penetrate to the chromophore embedded within the hydrophobic core of the rhodopsin molecule in the cones, but not, apparently so easily into the rhodopsins of most kinds of rod (Wald and Brown, 1954; Knowles and Dartnall, 1977; Fager and Fager, 1981). However it is known that the short-wave sensitive rods of deep sea fish, the green rods of frogs and the rather long-wave sensitive rods in gekkos are also susceptible to hydroxylamine (Knowles and Dartnall, 1977; Crescitelli, 1974). It could be argued that because cone rhodopsins regenerate more rapidly than in the rods, they need to offer easier passage to

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the chromophore group which is isomerised back to the active 11-eis form outside the outer segment, and that a path is left open for the very occasional invasion of molecules in the disc that cause chemical isomerisations from the 11-cis to the all-trans form. One of the problems with this type of argument is that there is no evidence to suggest that if a rhodopsin has a protected chromophore, it is constrained to have a /~maxnear 500 nm. However if it is really true that absorption at long or at short wavelengths or the ability for fast regeneration is obtained at the expense of a noisy signal, then the disadvantage will be much less for cones which are required to function at moderate or high light intensity, than for rods that function in dim light. VISUAL PIGMENTS AND THE SPECTRAL RADIANCE OF THE ENVIRONMENT

Fish

The early prediction that animals that live in strongly blue coloured visual environments might have unusually blue-sensitive visual pigments has proved exactly correct for many "deep sea" fish (see above). A similar situation holds for freshwater fish, except that maximum transmission occurs at longer wavelengths, often between about 530 and 650 nm. There is a corresponding shift in visual pigment absorption maxima to around 500 to 545 nm (Fig. 1), but the shift falls short of the near perfect match shown by the deep-sea rhodopsins. If the/]'max of visual pigments could be explained in terms of sensitivity alone, then it would be reasonable to expect that the Purkinje shift in freshwater teleosts would be towards longer wavelengths, but as in terrestrial vertebrates, the shift appears to be in the opposite direction. Compared to the rods some classes of cone, especially the twin cones of fish, show an unequivocal match to the spectral quality of the underwater light (Fig. 2). Two correlations can be clearly recognised, first the spread of cone 2max within the spectrum depends upon the bandwidth of the available light, and secondly the most red-sensitive cones containing 620-625nm porphyropsins have been found only in fish living in waters that are relatively rich in red light. In Fig. 3 a series of freshwater fish have been sorted according to the depth at which they live. Most of the fish were not taken from the wild and there is no data about the spectral properties of the water in which they naturally live. However it is reasonable to assume that none of the waters in their natural home has a maximum transmission less than about 530 nm, and it is very likely that some at least would normally live in water that is most transparent to wavelengths well in excess of 600 nm. It is clear from Fig. 3, that the deeper living species, which experience a narrow bandwidth of ambient light, have only a narrow spread of visual pigments (Levine and MacNicholl, 1979). The same situation was noticed by Loew and Lythgoe (1978) for tidepool fish that are sensitive to

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Fig. 1. Histograms of the numbers of fish species containing single rod visual pigments of known wavelength of maximum absorption (~'max) from different environments. The horizontal bars show the possible range of visual pigment )'max that would give maximum sensitivityin each water type. The shaded areas show the most likely range. The open triangles indicate that the 2max of the most blue-sensitiveand the most red sensitive visual pigments measured in the cones of fish inhabiting that water type (after Lythgoe, 1980). a wide spectra band compared to fish living in the same type of water, but at depths of 40 or 50 m. Considered as a class the twin cones, both identical and non identical, show a good match to the spectral irradiance under water. In comparison the rods show only a slight shift and this underlines the difficulty of explaining the )-m,x of rod pigments on sensitivity grounds alone. It is noticeable that no cone pigments yet measured either in extracts, or in the intact outer segments have a 2max longer than 625 nm in the porphyropsin series or 565 in the rhodopsin series. Large twin cones have been associated with a crepuscular habit and are characteristic of ambush predators (Engstrom, 1963; Lythgoe, 1979) and it is possible that wavelength matching for maximum sensitivity is to be found more amongst cones than amongst rods. It appears from Fig. 3 that the shorter-wave cone pigments are possessed by fish that live in the shallowest water. There are also recent reports that the roach, which often feeds in very shallow water (Avery et al., 1982), has a true u.v. absorbing pigment as does the Japanese dace (Harosi and Hashimoto, 1983). Humans cannot naturally see into the ultraviolet and thus we have little intuitive understanding of what information it may convey. But it certainly cannot be discounted in the belief that little or no u.v. light penetrates into the water. In fact the transparency of pure water to 350 nm light is about the same as to 550nm light (Jerlov, 1976). It is the colouring agents derived from living and dead plant life that are responsible for absorbing most of the u.v. light and the u.v. absorption of inshore and fresh water is much higher than in the clear oceans (Table 1). However it can be seen that even in fresh water, there is ample u.v. light available in the surface layers.

On clear evenings u.v. light is even less in short supply relative to longer wavelengths. This is because light rays reaching the water surface at oblique angles are mostly reflected back off the surface and never enter the water at all. The oblique rays of the evening sun contain proportionally more red light than does the vault of the sky above giving light that is mostly composed of the more highly scattered short wavelengths. Mostly for this reason the global reflection of light from the water surface can be three times greater for red light than blue (Jerlov, 1976). For a fish swimming a few centimeters below the surface the dominant visual feature is likely to be Snell's window through which it will be able to see the above-water world compressed into a circle with an angular radius of about 48 °. At greater angles total internal reflection at the air-water interface causes an inverted reflection of the bottom, looking horizontally there is often nothing to be seen but water, which has a spacelight derived from scattered light. Looking down, the bottom may be visible depending on the depth, the clarity of the water and the nature of the bottom. The spectral radiance of the spacelight depends upon a combination of absorption and Rayleigh scatter from the water molecules themselves and from larger suspended particles that range in size from small molecules to plankters easily visible to the naked eye. Spacelight can be considered as backreflected light; the spectral radiance of upwelling spacelight I ( + ) being divided by the downwelling spacelight I ( - ) . Spacelight reflectance measurements I ( + ) / I ( - ) for two types of water; the clear blue waters of the Gulf Stream, and San Vicente Reservoir, which is typical of green fresh water, are shown in Fig. 4. Further reflectance measurements for three Scottish Lochs are

Visual pigments and environmental light

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Fig. 2. The visual pigments in the cones of fish from different types of environment as defined by Levine and MacNicholl Jr (1979). Fish from freshwater which is relatively more transparent to red light, have visual pigments that are more red sensitive than fish from the more blue and blue-green coastal water. In comparison to the cones the rods show relatively little variation in their visual pigments. Rectangles = rods; circles = single cones; half circles = one member of a twin cone; divided circle = twin cones with each partner having the same visual pigment. Blue, tropical, marine: (A) Chaetodon sp. (B) Pomacentrus rnelanochir. (C) Gramma loreto. (D) Dendrochirus zebra. Green, coastal, marine: (A) Brevoortia tyranus. (B) Pornolobus pseudoharengus. (C) Opsanus tau. (D) Stenotomus versicolor. (E) Limanda limanda. (F) Microstomus kitt. (G) Pleuronectes platessa. (H) Pseudopleuronectes americanus. (I) Poralichthys dentatus. (J) Prionotus carolinus. (K) Trigla lucerna. (L) Eutrigla gurnadus. Freshwater (group II, Fig. 3): (A) Scardinius erythropthalmus. (B) Carassius auratus. (C) Tinca tinca. (D) Barbus schwanefeldi. (E) Barbus tetrazona. (F) Cichlasoma citrinellum. (G) Cichlasoma longimanus. (H) Hemiodus sp. (I) Heterotillapia multispinosa. (J) Jordanella floridae. (K) Leporinus fasciatus. (L) Paracheirodon innesi. (M) Pterophyllum sp. (N) Saratherodon aurea. (0) Saratheredon melanotheron. Data from Loew and Lythgoe (1978), Levine and MacNicholl Jr (1979). given by Muntz (1984). The wavelengths where reflections are low is of particular interest in the present context, for these are the wavelengths where objects in the water seen against the horizontal spacelight or against the reflection of the bottom in the surface will appear brightest relative to the background spacelight. It is interesting that for this type of visual task a violet or near-u.v, sensitive pigment will do better in green and brown fresh water than in blue ocean water. However at depths greater than 5 or 10 m the colouring matter in the water will have absorbed almost all the short-wave light, and a u.v. receptor will be worse than useless because it occupies valuable space in the retinal mosaic. As M u n t z (1984) has pointed out, rhodopsins tend to be more blue-sensitive, and are more c o m m o n in shallow-living freshwater fish. In the particular case

of the brown trout, the presence of rhodopsin is correlated with a shallow feeding habit in the summer, where the water is, if anything, relatively more transparent to red light than it is in the winter. In both the rudd and trout, rhodopsins are concentrated in the dorsal retina and will therefore receive light that has been reflected upwards from deeper water (Muntz, 1984). For shallow-living fish, and only for them, a blue-sensitive dorsal retina will "see" the background as dark, but suspended objects will look relatively brighter. However it needs to be borne in mind that it is only at wavelengths longer than about 465 n m that rhodopsins are known to be more bluesensitive than their porphyropsin analogues. At shorter wavelengths the position may be reversed and it is the porphyropsins that are likely to be the more blue-sensitive (Dartnall and Lythgoe, 1965). An in-

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Fig. 3. The visual pigments of freshwater fish arranged in behavioural ecological groups. Note the occurrence of more blue-sensitive visual pigments in shallow water, and a confinement of pigments to a narrower spectral bandwidth in deeper-living species. Group 1, very shallow living diurnal species: (A) Cynolebias. (B) Cyprinodon macularius. (C) Danio malabaricus. (D) Fundulus heteroclitus. (E) Gambusia sp. (F) Osteoglossum sp. (G) Pantadon sp. (H) Poecilia latipinna. (I) Poecilia reticulata. (J) Telmatherina sp. Group 2, Generalised, diurnal mid-water species: (A) Barbus schwanefeldi. (B) Barbus tetrazona. (C) Cichlasoma citrinellum. (D) Cichlasoma longimanus. (E) Herniodus sp. (F) Heterotillapia multispinosa. (G) Jordanella floridae. (H) Leporinus fasciatus. (I) Paracheirodon innesi. (J) Pterophyllum sp. (K) Saratherodon aurea. (L) Saratherodon melanotheron. Group 3, typically crepuscular mid-water predators: (A) Ctenoluchius sp. (B) Hoplias malabaricus. (C) Luciocephalus pulchur. (D) Metynnus sp. (E) Ophicephalus sp. (F) Serrasalmus sp. (G) Amia calva. (H) Enneacanthus obesus. (I) Esox americanus. (J) Lepisosteus sp. (K) Lepornis gibbosus. (L) Notemigonius crysoleucas. (M) Stizostedion vitreum. Group 4, crepuscular and nocturnal bottom-living species: (A) Ancistrus sp. (B Corydoras sp. (C) Ictalurus nebulosum. (D) Kryptopterus sp. (E) Labeo sp. Data from Kcvine and MacNicholl Jr (1979). teresting consequence of this is that the porphyropsins span a larger spectral bandwidth than the rhodopsins. If this type of argument is valid, it will be interesting to look at the cone pigments of very shallowliving blue-water fish like needle fish and gars, for although these live in very clear blue water, they may possess a class of offset cones absorbing around 560 nm. A further factor that might possibly be of interest is to do with the dispersion of light as it traverses the air-water interface at oblique angles. Because the refractive index of short wave light is

greater than for long (Lauscher, 1955), Snell's window subtends a solid angle about 2 ° wider for red light than for blue, and even to our eyes the edge of the window shows a spectrum. Effects of this kind are likely to be more pronounced in the u.v. than in the visible, but the significance, if any, of these spectral fringes remains to be seen. Birds and reptiles

Taking a broad systematic view birds and reptiles are quite closely related and a small manifestation of this is that both classes have prominent and varied

Visual pigments and environmental light

for colour vision because the action spectra of individual cones will differ (see M u n t z , 1972, for a review). T h e presence of any optical filter necessarily reduces sensitivity at all wavelengths, a l t h o u g h at some m o r e t h a n others, a n d they c a n n o t be a n a d a p t a t i o n to increase sensitivity. It is more likely t h a t their p u r p o s e is to cut o u t parts o f the spectrum where the signal-to-noise ratio is low, or where the object o f interest has a radiance nearly equal to t h a t o f the b a c k g r o u n d . The cone pigments o f few birds have been studied in detail. There are at least three cone pigments in the chicken ( B o w m a k e r a n d Knowles, 1977), the pigeon (Bowmaker, 1977; F a g e r a n d Fager, 1981) the Aylesb u r y duck (Jane a n d Bowmaker, 1984) a n d the penguin ( B o w m a k e r a n d M a r t i n , 1984). But in the primitive e m u a n d t i n a m o u only one rhodopsin, which is m o d u l a t e d by two types of oil globule, has been f o u n d (Sillman et al., 1981). In m o s t cases the spectral a b s o r b a n c e of b o t h the oil globules a n d visual p i g m e n t m u s t be k n o w n before the spectral sensitivity of a cone can be calculated. However the

Table 1. Percentage absorption of near u.v. (362 nm) surface light in clear blue water, (Gulf Stream), coastal water (Gulf of California) and fresh water (San Vicente Reservoir) at three different depths 0.1M 1M 10M Gulf Stream 99.3 93.3 49.8 Coastal water 97.3 76.3 6.7 Fresh water 71.0 3.3 -These waters are most transparent at about 40ff480, 520-560 and 560-580 nm, respectively. Data calculated from measurements by Tyler and Smith (1970) for the diffuse attenuation coefficient of downwelling light for the Gulf Stream. Average values for 3 July 1967, Gulf of California 8.5M, 10 May 1968, and San Vicente Reservoir average values for 20 January 1967. coloured oil globules in their cones. These oil globules act as very effective cut-off (edge) filters, a n d even if only one type of r h o d o p s i n is present in the cones, the possession o f two or more different oil globules t h a t cut-off at different wavelengths confer the potential

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J.N. LYTHGOE

red oil globule type cuts off at 610 nm, and it appears report that a freshwater crayfish has a mixture of that only the most red-sensitive rhodopsins of 2max rhodopsin and porphyropsin in its eye in a manner near 567 nm will retain any sensitivity when teamed characteristic of freshwater fish and amphibian tadwith a red oil globule. In the pigeon and chicken the poles (Suzuki and Makino-Tasaka, 1984). Although longest 2max visual pigment is indeed teamed with the some birds and fish appear to possess u.v.-sensitive red oil globule. The presence of red oil globules visual pigments (see above), they are well known in almost certainly means that there is a red-sensitive insects (see for example Menzel, 1975; Stavenga, colour channel with a maximum sensitivity at around 1980) and there is no doubt that some have evolved 619 nm at this peripheral level. If it should turn out patterns that are only visible in the u.v. to exploit this that there are other "rules" governing particular oil sensitivity. Insect pollinated flowers have also evolved globule and visual pigment combinations, our under- u.v. patterns that guide the visiting insects in towards standing of the colour vision ecology of birds should the stores of nectar, and in so doing, service the advance quite rapidly because the colour of the oil pollination mechanisms of the flower. globules can be easily seen in the fresh retina and Each species of North American firefly flashes with nearly as easily measured. its own particular colour of bioluminescence; the Some correlations between oil globules and life- evening active species tending to emit yellow light and style have already been noted (Muntz, 1972; Lythgoe, the night active ones emitting green (Lall et al., 1980; 1979, for reviews). For example night-feeding birds, Seliger et al., 1982a, b). The night active species are such as owls and nighthawks, and underwater skilled maximally sensitive to green light and probably have hunters, such as auks, cormorants and penguins a rhodopsin of 2max n e a r 550 nm. The evening species (Bowmaker and Martin, 1984), have a very low probably have the same rhodopsin, but it is screened proportion of red and orange oil globules, pre- with an inert magenta pigment within the rhabsumably because their possession would reduce sensi- domere causing the peak spectral sensitivity to be tivity. It is interesting that Bowmaker and Martin shifted to 580 nm. There is a consequential narrowing (1984) estimate that the known oil globule and visual of the spectral sensitivity curve, and a reduction of pigment combinations in the penguin will give it best absolute sensitivity. In the night-time species the colour discrimination in the 400-500 nm waveband, green bioluminescence matches the unscreened greenwhich would fit it for seeing through the clear waters sensitive rhodopsin, making the firefly very sensitive of the antarctic ocean. In complete contrast plunge- to the light of its fellows. At night one firefly sees diving sea birds have an unusually high proportion of another against a dark background, but in the evered oil globules which may enable them to see objects ning there is a background radiance provided by the at or just below the water surface (Lythgoe, 1979). skylight reflected from green foliage. Seliger et al. The colour of the water may also play its part and it (1982a, b) calculate that it would be maladaptive for may be significant that the freshwater turtle (Pseud- evening species to be most sensitive to green light emys scripta) has many red and orange oil globules, because the contrast between the green firefly light whereas the blue-water green turtle (Chelonia mydas) and the green foliage would be low at the wavelengths has no red globules (Liebman and Granda, 1971). where the firefly is most sensitive. It is better for the Behavioural studies have shown that the pigeon firefly to emit longer wavelength yellow light, and to (Wright, 1972; Kreithen and Eisner, 1980; Emmerton be maximally sensitive to that yellow light, because and Delius, 1980), and the hummingbird (Goldsmith, then contrast between firefly and its green back1980) are sensitive to u.v. light. The only mea- ground is increased, even though the presence of surements of the visual pigment itself have been made screening pigment means that sensitivity is decreased. from extracts of the cone fraction of pigeon retina, where a visual pigment of 2max near 417 nm has been EXTRA-RETINAL RECEPTORS recorded (Fager and Fager, 1981). The benefit that In vertebrates, extra-retinal receptors have been the bird might gain from u.v. sensitivity is uncertain, but there might be some advantage in intercepting the described in various parts of the body (Fig. 5) visual display signals between one insect and another, including the skin, nervous tissue, the pineal, the or indeed it may be that birds with u.v. sensitivity harderian gland and the brain. They are also suspected to occur in the iris of some species, and it is have u.v. patterns not visible to us. possible that the retinal melanophores may also be Invertebrates sensitive to the direct action of light (for reviews see Although there are very real differences between Steven, 1963; Wolken and Mogus, 1979; Menaker, the visual systems of vertebrates and invertebrates, it 1977; Weber, 1983). Like those of the retina itself, the ciliary photoseems to be broadly true that insects adapt to the spectral quality of the ambient light in much the same receptors of the pineal contain enough opsin to be way as vertebrates. For example deep-sea crustacea detected by relatively insensitive immunofluorescence possess short-wave sensitive rhodopsins that resemble techniques (Vigh et al., 1982); but the nature of the those of deep-sea fish (Goldsmith, 1972; Knowles and photoreceptors in the harderian gland and the skin of Dartnall, 1977, for reviews); and there is a very recent birds and cyclosomes is enigmatic to say the least. It

Visual pigments and environmental light M

P

Fig. 5. Some of the known extra-retinal receptors in fish, larval amphibia and birds. More information is given in Table 2. B = brain, I = iridophore, M = melanophore, P = pineal.

is almost certain that the chromatophores of several species are directly sensitive to light (van der Lek, 1967; Wakamatsu et al., 1980; Iga and Takabatake, 1983; Bagnara et al., 1973), but no cilia-like structures have yet been reported. Immunofluorescent studies of fish iridocytes make it seem likely that these

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contain an opsin-based visual pigment (Lythgoe et al., 1984), and action spectra from both fish iridocytes and amphibian melanophores certainly suggest the presence of rhodopsin or porphyropsin (Lythgoe and Shand, 1984; Lythgoe and Thompson, 1984). However Wakamatsu et al. (1980) have suggested that a pteridine might be responsible in cultured platyfish melanophores. The nature of some of the known extra-retinal photoreceptors is summarised in Table 2. The effects of chromatic adaptation on the electrophysiological action spectra of amphibian and reptilian pineal, and the electrodermogram of the frog make it seem likely that these photoreceptors have a system resembling the rhodopsin-metarhodopsin system of insects and cephalopods, where light of one wavelength causes the 11-cis to all-trans isomerisation of rhodopsin to metarhodopsin at short wavelengths, and a reverse isomerisation, within the photoreceptor cell itself at longer wavelengths (Eldred and Nolte, 1978). Most experiments are not well designed to detect photoreversal, and indeed it has as yet only been those experiments that use electrophysiological techniques that have demonstrated the phenomenon with any degree of confidence. One advantage of a photoreversal (photochromic) system might be that it enables the rhodopsin to be continually regenerated even in very bright light which the animal is unable

Table 2. Extra-retinal photoreceptors in vertebrates

Species Neon tetra

Type of action spectrum

Pigments present

Photoreceptor

Cil

Iridophore

?No

Spectralreflection

461" ?545*

Lythgoe and Shand (1984)

Melanophore

No

Morphology

425

Melanophore

No

Morphology

461"

van der Lek (1967) Lythgoe and Thompson (1984)

Melanophore

No

Morphology

420

Paracheirodon innesi Xenopus

tadpole

Authors

Platyfish Xiphophorus

Wakamatsu et al. (1980)

Hagfish

Skin

?No

Behaviour

520

Steven (1955)

Skin

?No

Behaviour

530

Steven (1950)

Skin

?No

Electrodermogram

385 500

Hypothalamus

?Yes

Hormone, LH

494*

Rayport and Wald (1978) ex Shropshire (1980) Foster (1984)

Pineal

Yes

EPG

500 533

Morita (1966)

Minnow

Pineal

Yes

EPG

ca 530

Shaefer (1964)

Phoxinus Rana spp. Xenopus laevis

Pineal Pineal

Yes Yes

EPG EPG

355 515 520

tadpole Lizard

Pineal

Yes

EPG

450 520

Pineal

Yes

Hormone, serotonin

500

Dodt (1973) Foster and Roberts (1982) Dodt and Sherer (1968) Deguchi (1981)

Myxine glutinosa

Lamprey Lampetra fluviatilis

Frog Rana

Quail Corturnix

Trout Salmo irideus

Lacer ta sicula

Chicken

The location of the photoreceptor, whether there is a ciliary-type known to be present, how the action spectra were obtained, and the absorption maxima of the suspected visual pigments are given• In the case of the neon tetra iridophore and the pineal receptors, an opsin-based visual pigment is suspected on the basis of immunocytochemistry. There are good reasons for thinking that photoreversal takes place in frog skin (Rayport and Wald, 1978) and frog pineal (Eldred and Nolte, 1978), and probably in the lizard pineal. Action spectra marked *, have been corrected to take into account the width of the equal-frequency waveband as recommended by Dartnall (1975) rather than the more usual equal-wavelength waveband. This has the effect of somewhat reducing the apparent wavelength of maximum sensitivity.

1548

J . N . LYTHGOE

either to escape, or to shield the photoreceptor from. The relative amount of rhodopsin versus metarhodopsin depends not upon the light intensity, but upon its spectral quality, and it might be interesting to know if a period in dim reddish light, as may prevail before dawn in stained flesh water, is particularly effective in allowing the build up of rhodopsin in the photoreceptor in anticipation of the dawn. The extra-retinal photoreceptors that are not designed to detect transient changes in illumination may be able to enhance their sensitivity by increasing their integration time rather than by increasing pigment density or receptive area. Integration times of 120min in the hypothalamus receptor in the quail (Follett and Milette, 1982), and 1-4 min in the hagfish (Newth and Ross, 1955; Steven, 1955) have been measured. In both animals there is a reciprocal relationship between the intensity and the duration of the light stimulus. If this allows the photopigment to be present in only very small amounts, it might well make it difficult to find where, or indeed if, it is present in the tissues. As yet there does not seem to be any reason to think that the spectral absorbance of extra-retinal photopigments are located in the spectrum to maximise the capture of photons (Table 2). In c o m m o n with the presumptive extra-retinal photopigments of invertebrates (Nultsch, 1980; Shropshire, 1980; Wakamatsu et al., 1980), they tend to be too blue sensitive to confer maximum sensitivity, and in this echo the situation in vertebrate rods. There is one situation, however, where spectral matching is likely to be relevant, and that is when the photoreceptor is buried deep within the tissue as it is in the hypothalamus photoreceptor in the bird. Here the thick layer of blood-laden skin, muscle, bone and brain has a significant modifying effect on the spectral radiance of the light that reaches the receptors, a short-wave sensitive photopigment would receive very little light and the most red-sensitive visual pigment such as an iodopsin would give the greatest sensitivity. Even so, careful action spectra that take into account the absorptive properties of the bird's head suggest that the photopigment may be a rhodopsin of ']*max near 4 9 2 n m (Foster, 1984), and it may be that this is about the shortest possible 2ma× that can be used without an unacceptible sacrifice in sensitivity.

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