The UV visual world of fishes: a review

Ultraviolet-A radiation (320–400 nm) is scattered rapidly in water. Despite this fact, UV is present in biologically useful amounts to at least 100 m deep in clear aquatic environments. Discovery of UV visual pigments with peak absorption at around 360 nm in teleost cone photoreceptors indicates that many teleost fishes may be adapted for vision in the UV range. Considering the characteristic absorption curve for visual pigments, about 18% of the downwelling light that illuminates objects at 30-m depth would be available to UV-sensitive cones. Strong scattering of UV radiation should produce unique imaging conditions as a very bright UV background in the horizontal view and a marked veiling effect that, with distance, obscures an image. Many teleosts have three, or even four, classes of cone cells mediating colour vision in their retina and one can be sensitive to UV. These UV-sensitive cones contain a visual pigment based on a unique opsin which is highly conserved between fish species. Several powerful methods exist for demonstration of UV vision, but all are rather demanding in terms of technique and equipment. Demonstration that the eye lacks UV-blocking compounds that are present in many fish eyes is a simpler method that can indicate the possibility of UV vision. The only experimental evidence for the use of UV vision by fishes is connected to planktivory: detection of UV-opaque objects at close range against a bright UV background is enhanced by the physical properties of UV light. Once present, perhaps for the function of detecting food, UV vision may well be co-opted through natural selection for other functions. Recent discovery that UV vision is critically important for mate choice in some birds and lizards is a strong object lesson for fish ecologists and behaviourists. Other possible functions amount to far more than merely adding a fourth dimension to the visible spectrum. Since UV is scattered so effectively in water, it may be useful for social signalling at short range and reduce the possibility of detection by other, illegitimate, receivers. Since humans are blind to UV light, we may be significantly in error, in many cases, in our attempts to understand and evaluate visual aspects of fish behaviour. A survey of the reflectance properties of skin pigments in fishes reveals a rich array of pigments with reflectance peaks in the UV. For example, the same yellow to our eyes may comprise two perceptually different colours to fish, yellow and UV-yellow. It is clearly necessary for us to anticipate that many fishes may have some form of UV vision.     

Bat Eyes Have Ultraviolet-Sensitive Cone Photoreceptors

Mammalian retinae have rod photoreceptors for night vision and cone photoreceptors for daylight and colour vision. For colour discrimination, most mammals possess two cone populations with two visual pigments (opsins) that have absorption maxima at short wavelengths (blue or ultraviolet light) and long wavelengths (green or red light). Microchiropteran bats, which use echolocation to navigate and forage in complete darkness, have long been considered to have pure rod retinae. Here we use opsin immunohistochemistry to show that two phyllostomid microbats, Glossophaga soricina and Carollia perspicillata, possess a significant population of cones and express two cone opsins, a shortwave-sensitive (S) opsin and a longwave-sensitive (L) opsin. A substantial population of cones expresses S opsin exclusively, whereas the other cones mostly coexpress L and S opsin. S opsin gene analysis suggests ultraviolet (UV, wavelengths <400 nm) sensitivity, and corneal electroretinogram recordings reveal an elevated sensitivity to UV light which is mediated by an S cone visual pigment. Therefore bats have retained the ancestral UV tuning of the S cone pigment. We conclude that bats have the prerequisite for daylight vision, dichromatic colour vision, and UV vision. For bats, the UV-sensitive cones may be advantageous for visual orientation at twilight, predator avoidance, and detection of UV-reflecting flowers for those that feed on nectar.     

Visual modelling suggests a weak relationship between the evolution of ultraviolet vision and plumage coloration in birds

Birds have sophisticated colour vision mediated by four cone types that cover a wide visual spectrum including ultraviolet (UV) wavelengths. Many birds have modest UV sensitivity provided by violet‐sensitive (VS) cones with sensitivity maxima between 400 and 425 nm. However, some birds have evolved higher UV sensitivity and a larger visual spectrum given by UV‐sensitive (UVS) cones maximally sensitive at 360–370 nm. The reasons for VS–UVS transitions and their relationship to visual ecology remain unclear. It has been hypothesized that the evolution of UVS‐cone vision is linked to plumage colours so that visual sensitivity and feather coloration are ‘matched’. This leads to the specific prediction that UVS‐cone vision enhances the discrimination of plumage colours of UVS birds while such an advantage is absent or less pronounced for VS‐bird coloration. We test this hypothesis using knowledge of the complex distribution of UVS cones among birds combined with mathematical modelling of colour discrimination during different viewing conditions. We find no support for the hypothesis, which, combined with previous studies, suggests only a weak relationship between UVS‐cone vision and plumage colour evolution. Instead, we suggest that UVS‐cone vision generally favours colour discrimination, which creates a nonspecific selection pressure for the evolution of UVS cones.     

The rostral micro-tooth morphology of blue marlin,Makaira nigricans

Billfish rostra potentially have several functions; however, their role in feeding is unequivocal in some species. Recent work linked morphological variation in rostral micro-teeth to differences in feeding behavior in two billfish species, the striped marlin (Kajikia audax) and the sailfish (Istiophorus platypterus). Here, we present the rostral micro-tooth morphology for a third billfish species, the blue marlin (Makaira nigricans), for which the use of the rostrum in feeding behavior is still undocumented from systematic observations in the wild. We measured the micro-teeth on rostrum tips of blue marlin, striped marlin, and sailfish using a micro–computed tomography approach and compared the tooth morphology among the three species. This was done after an analysis of video-recorded hunting behavior of striped marlin and sailfish revealed that both species strike prey predominantly with the first third of the rostrum, which provided the justification to focus our analysis on the rostrum tips. In blue marlin, intact micro-teeth were longer compared to striped marlin but not to sailfish. Blue marlin had a higher fraction of broken teeth than both striped marlin and sailfish, and broken teeth were distributed more evenly on the rostrum. Micro-tooth regrowth was equally low in both marlin species but higher in sailfish. Based on the differences and similarities in the micro-tooth morphology between the billfish species, we discuss potential feeding-related rostrum use in blue marlin. We put forward the hypothesis that blue marlin might use their rostra in high-speed dashes as observed in striped marlin, rather than in the high-precision rostral strikes described for sailfish, possibly focusing on larger prey organisms.     

Photopic spectral sensitivity of a teleost fish,the roach (Rutilus rutilus), with special reference to its ultraviolet sensitivity

Summary This study reports photopic spectral sensitivity curves (351–709 nm) for four individual roach,Rutilus rutilus, determined by two choice appetitive training. All four curves show four sensitivity maxima at 361–398 nm, 421–448 nm, 501–544 nm and 634–666 nm which are related to the four known roach photopic visual pigments (Avery et al. 1982). The overall shape of the curves at long wavelengths indicates inhibitory interactions between the red and green cone mechanisms. That the high behavioural sensitivity in the UV is caused by a specific ultraviolet visual pigment and is not due to aberrant stimulation of the other cone types is shown by the redetermination of spectral sensitivity at short wavelengths (351–501 nm) following the selective bleaching of the three longer wavelength visual pigments. This depresses the blue sensitivity to a greater degree than the relatively unaffected UV sensitivity maximum. Spectral transmission data from two corneas and four lenses show that they transmit considerable amounts of light in the near UV.     

Spectral sensitivities including the ultraviolet of the passeriform bird Leiothrix lutea

Spectral sensitivity functions of a passeriform bird, the Red-billed Leiothrix Leiothrix lutea (Timalidae) were determined in a behavioural test under different background illuminations.

Photoreceptor Spectral Sensitivity in the Bumblebee,Bombus impatiens (Hymenoptera: Apidae)

The bumblebee Bombus impatiens is increasingly used as a model in comparative studies of colour vision, or in behavioural studies relying on perceptual discrimination of colour. However, full spectral sensitivity data on the photoreceptor inputs underlying colour vision are not available for B. impatiens. Since most known bee species are trichromatic, with photoreceptor spectral sensitivity peaks in the UV, blue and green regions of the spectrum, data from a related species, where spectral sensitivity measurements have been made, are often applied to B impatiens. Nevertheless, species differences in spectral tuning of equivalent photoreceptor classes may result in peaks that differ by several nm, which may have small but significant effects on colour discrimination ability. We therefore used intracellular recording to measure photoreceptor spectral sensitivity in B. impatiens. Spectral peaks were estimated at 347, 424 and 539 nm for UV, blue and green receptors, respectively, suggesting that this species is a UV-blue-green trichromat. Photoreceptor spectral sensitivity peaks are similar to previous measurements from Bombus terrestris, although there is a significant difference in the peak sensitivity of the blue receptor, which is shifted in the short wave direction by 12–13 nm in B. impatiens compared to B. terrestris.     

Colour vision and visual ecology of the blue-spotted maskray, <Emphasis Type="Italic">Dasyatis kuhlii</Emphasis> Müller &; Henle, 1814

Relatively little is known about the physical structure and ecological adaptations of elasmobranch sensory systems. In particular, elasmobranch vision has been poorly studied compared to the other senses. Virtually nothing is known about whether elasmobranchs possess multiple cone types, and therefore the potential for colour vision, or how the spectral tuning of their visual pigments is adapted to their different lifestyles. In this study, we measured the spectral absorption of the rod and cone visual pigments of the blue-spotted maskray, Dasyatis kuhlii, using microspectrophotometry. D. kuhlii possesses a rod visual pigment with a wavelength of maximum absorbance (λ_max) at 497 nm and three spectrally distinct cone types with λ_max values at 476, 498 and 552 nm. Measurements of the spectral transmittance of the ocular media reveal that wavelengths below 380 nm do not reach the retina, indicating that D. kuhlii is relatively insensitive to ultraviolet radiation. Topographic analysis of retinal ganglion cell distribution reveals an area of increased neuronal density in the dorsal retina. Based on peak cell densities and using measurements of lens focal length made using laser ray tracing and sections of frozen eyes, the estimated spatial resolving power of D. kuhlii is 4.10 cycles per degree.     

The contribution of single and double cones to spectral sensitivity in budgerigars during changing light conditions

Bird colour vision is mediated by single cones, while double cones and rods mediate luminance vision in bright and dim light, respectively. In daylight conditions, birds use colour vision to discriminate large objects such as fruit and plumage patches, and luminance vision to detect fine spatial detail and motion. However, decreasing light intensity favours achromatic mechanisms and eventually, in dim light, luminance vision outperforms colour vision in all visual tasks. We have used behavioural tests in budgerigars (Melopsittacus undulatus) to investigate how single cones, double cones and rods contribute to spectral sensitivity for large (3.4°) static monochromatic stimuli at light intensities ranging from 0.08 to 63.5 cd/m². We found no influences of rods at any intensity level. Single cones dominate the spectral sensitivity function at intensities above 1.1 cd/m², as predicted by a receptor noise-limited colour discrimination model. Below 1.1 cd/m², spectral sensitivity is lower than expected at all wavelengths except 575 nm, which corresponds to double cone function. We suggest that luminance vision mediated by double cones restores visual sensitivity when single cone sensitivity quickly decreases at light intensities close to the absolute threshold of colour vision.     

Blue tits are ultraviolet tits

The blue tit (Parus caeruleus) has been classified as sexually monochromatic. This classification is based on human colour perception yet, unlike humans, most birds have four spectrally distinct classes of cone and are visually sensitive to wavelengths in the near-ultraviolet (300 to 400 nm). Reflectance spectrophotometry reveals that blue tit plumage shows considerable reflection of UV light. For example, the blue crest shows peak reflectance at wavelengths around 352 nm. Furthermore, the blue tit is sexually dichromatic for multiple regions of plumage, including the crest. Choice trials performed in the laboratory indicate that females prefer males with the brightest crests. This study has implications for both intra- and interspecific studies of sexual selection, as well as future classification of dichromatism, which should not ignore the possibility of variation in reflectance in the UV.     

Opsin switch reveals function of the ultraviolet cone in fish foraging

Although several studies have shown that ultraviolet (UV) wavelengths are important in naturally occurring, visually guided behaviours of vertebrates, the function of the UV cone in such behaviours is unknown. Here, I used thyroid hormone to transform the UV cones of young rainbow trout into blue cones, a phenomenon that occurs naturally as the animal grows, to test whether the resulting loss of UV sensitivity affected the animal''s foraging performance on Daphnia magna, a prey zooplankton. The distances and angles at which prey were located (variables that are known indicators of foraging performance) were significantly reduced for UV knock-out fish compared with controls. Optical measurements and photon-catch calculations revealed that the contrast of Daphnia was greater when perceived by the visual system of control versus that of thyroid-hormone-treated fish, demonstrating that the UV cone enhanced the foraging performance of young rainbow trout. Because most juvenile fishes have UV cones and feed on zooplankton, this finding has wide implications for understanding the visual ecology of fishes. The enhanced target contrast provided by UV cones could be used by other vertebrates in various behaviours, including foraging, mate selection and communication.     

Photoreceptor processing speed and input resistance changes during light adaptation correlate with spectral class in the bumblebee, Bombus impatiens

Colour vision depends on comparison of signals from photoreceptors with different spectral sensitivities. However, response properties of photoreceptor cells may differ in ways other than spectral tuning. In insects, for example, broadband photoreceptors, with a major sensitivity peak in the green region of the spectrum (>500 nm), drive fast visual processes, which are largely blind to chromatic signals from more narrowly-tuned photoreceptors with peak sensitivities in the blue and UV regions of the spectrum. In addition, electrophysiological properties of the photoreceptor membrane may result in differences in response dynamics of photoreceptors of similar spectral class between species, and different spectral classes within a species. We used intracellular electrophysiological techniques to investigate response dynamics of the three spectral classes of photoreceptor underlying trichromatic colour vision in the bumblebee, Bombus impatiens, and we compare these with previously published data from a related species, Bombus terrestris. In both species, we found significantly faster responses in green, compared with blue- or UV-sensitive photoreceptors, although all 3 photoreceptor types are slower in B. impatiens than in B. terrestris. Integration times for light-adapted B. impatiens photoreceptors (estimated from impulse response half-width) were 11.3 ± 1.6 ms for green photoreceptors compared with 18.6 ± 4.4 ms and 15.6 ± 4.4 for blue and UV, respectively. We also measured photoreceptor input resistance in dark- and light-adapted conditions. All photoreceptors showed a decrease in input resistance during light adaptation, but this decrease was considerably larger (declining to about 22% of the dark value) in green photoreceptors, compared to blue and UV (41% and 49%, respectively). Our results suggest that the conductances associated with light adaptation are largest in green photoreceptors, contributing to their greater temporal processing speed. We suggest that the faster temporal processing of green photoreceptors is related to their role in driving fast achromatic visual processes.     

Light emitting diode(LED)‐based trapping of the greenhouse whitefly (Trialeurodes vaporariorum)

Visual traps like yellow sticky card traps are used for monitoring and control of the greenhouse whitefly (Trialeurodes vaporariorum). However, reflected intensity (brightness) and hence, attractiveness depend on the ambient light conditions, and the colour (wavelength) might not fit with the sensitivity of whitefly photoreceptors. The use of light emitting diodes (LEDs) is a promising approach to increase the attractiveness, specificity and adaptability of visual traps. We constructed LED‐based visual traps equipped with blue and green high‐power LEDs and ultraviolet (UV) standard LEDs according to the putative spectral sensitivities of the insects' photoreceptors. In a series of small‐scale choice and no‐choice recapture experiments, the factors time of day as well as light intensity and light quality (colour) of LED traps were studied in terms of attractiveness compared to yellow traps without LEDs. Green LED traps (517 nm peak wavelength) were comparably attractive in no‐choice experiments but clearly preferred over yellow traps in all choice experiments. The time of day had a clear effect on the flight activity of the whiteflies and thereby on the trapping success. Blue LEDs (474 nm) suppressed the attractiveness of the light traps when combined with green LEDs suggesting that a yet undetected photoreceptor, sensitive for blue light, and an inhibiting interaction with the green receptor, might exist in T. vaporariorum. In choice experiments between LED traps emitting green light only or in combination with UV (368 nm), the green‐UV combination was preferred. In no‐choice night‐time experiments, UV LEDs considerably increased whitefly flight activity and efficacy of trapping. Most likely, the reason for the modifying effect of UV is the stimulating influence on flight activity. In conclusion, it seems that the use of green LEDs alone or in combination with UV LEDs could be an innovative option for improving attractiveness of visual traps.     

Distribution and habitat associations of billfish and swordfish larvae across mesoscale features in the Gulf of Mexico

Ichthyoplankton surveys were conducted in surface waters of the northern Gulf of Mexico (NGoM) over a three-year period (2006-2008) to determine the relative value of this region as early life habitat of sailfish (Istiophorus platypterus), blue marlin (Makaira nigricans), white marlin (Kajikia albida), and swordfish (Xiphias gladius). Sailfish were the dominant billfish collected in summer surveys, and larvae were present at 37.5% of the stations sampled. Blue marlin and white marlin larvae were present at 25.0% and 4.6% of the stations sampled, respectively, while swordfish occurred at 17.2% of the stations. Areas of peak production were detected and maximum density estimates for sailfish (22.09 larvae 1000 m(-2)) were significantly higher than the three other species: blue marlin (9.62 larvae 1000 m(-2)), white marlin (5.44 larvae 1000 m(-2)), and swordfish (4.67 larvae 1000 m(-2)). The distribution and abundance of billfish and swordfish larvae varied spatially and temporally, and several environmental variables (sea surface temperature, salinity, sea surface height, distance to the Loop Current, current velocity, water depth, and Sargassum biomass) were deemed to be influential variables in generalized additive models (GAMs). Mesoscale features in the NGoM affected the distribution and abundance of billfish and swordfish larvae, with densities typically higher in frontal zones or areas proximal to the Loop Current. Habitat suitability of all four species was strongly linked to physicochemical attributes of the water masses they inhabited, and observed abundance was higher in slope waters with lower sea surface temperature and higher salinity. Our results highlight the value of the NGoM as early life habitat of billfishes and swordfish, and represent valuable baseline data for evaluating anthropogenic effects (i.e., Deepwater Horizon oil spill) on the Atlantic billfish and swordfish populations.     

Vision in elasmobranchs and their relatives: 21st century advances

This review identifies a number of exciting new developments in the understanding of vision in cartilaginous fishes that have been made since the turn of the century. These include the results of studies on various aspects of the visual system including eye size, visual fields, eye design and the optical system, retinal topography and spatial resolving power, visual pigments, spectral sensitivity and the potential for colour vision. A number of these studies have covered a broad range of species, thereby providing valuable information on how the visual systems of these fishes are adapted to different environmental conditions. For example, oceanic and deep-sea sharks have the largest eyes amongst elasmobranchs and presumably rely more heavily on vision than coastal and benthic species, while interspecific variation in the ratio of rod and cone photoreceptors, the topographic distribution of the photoreceptors and retinal ganglion cells in the retina and the spatial resolving power of the eye all appear to be closely related to differences in habitat and lifestyle. Multiple, spectrally distinct cone photoreceptor visual pigments have been found in some batoid species, raising the possibility that at least some elasmobranchs are capable of seeing colour, and there is some evidence that multiple cone visual pigments may also be present in holocephalans. In contrast, sharks appear to have only one cone visual pigment. There is evidence that ontogenetic changes in the visual system, such as changes in the spectral transmission properties of the lens, lens shape, focal ratio, visual pigments and spatial resolving power, allow elasmobranchs to adapt to environmental changes imposed by habitat shifts and niche expansion. There are, however, many aspects of vision in these fishes that are not well understood, particularly in the holocephalans. Therefore, this review also serves to highlight and stimulate new research in areas that still require significant attention.     

Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.)

The spectral absorption characteristics of the retinal photoreceptors of the blue tit (Parus caeruleus) and blackbird (Turdus merula) were investigated using microspectrophotometry. The retinae of both species contained rods, double cones and four spectrally distinct types of single cone. Whilst the visual pigments and cone oil droplets in the other receptor types are very similar in both species, the wavelength of maximum sensitivity (λ_max) of long-wavelength-sensitive single and double cone visual pigment occurs at a shorter wavelength (557 nm) in the blackbird than in the blue tit (563 nm). Oil droplets located in the long-wavelength-sensitivesingle cones of both species cut off wavelengths below 570–573 nm, theoretically shifting cone peak spectral sensitivity some 40 nm towards the long-wavelength end of the spectrum. This raises the possibility that the precise λ_max of the long-wavelength-sensitive visual pigment is optimised for the visual function of the double cones. The distribution of cone photoreceptors across the retina, determined using conventional light and fluorescence microscopy, also varies between the two species and may reflect differences in their visual ecology. Accepted: 8 January 2000     

VISUAL ACUITY AND ILLUMINATION IN DIFFERENT SPECTRAL REGIONS

The relation between visual acuity and illumination was measured in red and blue light, using a broken circle or C and a grating as test objects. The red light data fall on single continuous curves representing pure cone vision. The blue light data fall on two distinct curves with a transition at about 0.03 photons. Values below this intensity represent pure rod vision. Those immediately above represent the cooperative activity of rods and cones, and yield higher visual acuities than either. Pure cone vision in this intensity region is given by central fixation (C test object). All the rest of the values above this transition region represent pure cone vision. In blue light the rod data with the C lie about 1.5 log units lower on the intensity axis (cone scale) than they do in white light, while with the grating they lie about 1.0 log unit lower than in white light. Both the pure rod and cone data with the C test object are precisely described by one form of the stationary state equation. With the grating test object and a non-limiting pupil, the pure rod and cone data are described by another form of the same equation in which the curve is half as steep. The introduction of a small pupil, which limits maximum visual acuity, makes the relation between visual acuity and illumination appear steeper. Determinations of maximum visual acuities under a variety of conditions show that for the grating the pupil has to be larger, the longer the wavelength of the light, in order for the pupil not to be the limiting factor. Similar measurements with the C show that when intensity discrimination at the retina is experimentally made the limiting factor in resolution, visual acuity is improved by conditions designed to increase image contrast. However, intensity discrimination cannot be the limiting factor for the ordinary test object resolution because the conditions designed to improve image contrast do not improve maximum visual acuity, while those which reduce image contrast do not produce proportional reductions of visual acuity.     

Spectral sensitivities of photoreceptors and their role in colour discrimination in the green-backed firecrown hummingbird (<Emphasis Type="Italic">Sephanoides sephaniodes</Emphasis>)

We studied the photopic spectral sensitivity in the green-backed firecrown, Sephanoides sephaniodes, a South American hummingbird, and its possible ecological relationship with preferred flowers and body colouration. Avian colour vision is in general tetrachromatic with at least four types of cones, which vary in sensitivity from the near ultraviolet (UV) to the red wavelength range. Hummingbirds represent an important family of birds, yet little is known about their eye sensitivity, especially about the role of photoreceptors and their oil droplet complements. The photopic electroretinogram shows a main sensitivity peak at 560 nm and a secondary peak in the UV, and may be explained by the presence of four single cones (lambda (max) at ~370, 440, 508 and 560 nm), and a double cone (lambda (max) at 560 nm) screened by oil droplets. The flowers preferred by the firecrown are those in which the red-green wavelength region predominates and have higher contrast than other flowers. The crown plumage of males is highly iridescent in the red wavelength range (peak at 650 nm) and UV; when plotted in a high-dimensional tetrachromatic space, it falls in a "red + UV" purple hue line, suggesting a potential significant communication signal for sexual differentiation.     

Ultraviolet vision and foraging in dip and plunge diving birds

Many fishes are sensitive to ultraviolet (UV) light and display UV markings during courtship. As UV scatters more than longer wavelengths of light, these signals are only effective at short distances, reducing the risk of detection by swimming predators. Such underwater scattering will be insignificant for dip and plunge diving birds, which prey on fishes just below the water surface. One could therefore expect to find adaptations in the eyes of dip and plunge diving birds that tune colour reception to UV signals. We used a molecular method to survey the colour vision tuning of five families of dip or plunge divers and compared the results with those from sister taxa of other foraging methods. We found evidence of extended UV vision only in gulls (Laridae). Based on available evidence, it is more probable that this trait is associated with their terrestrial foraging habits rather than piscivory.