Ultraviolet vision in birds: what is its function?

Although UV vision was first demonstrated in birds in the early 1970s, its function is still unknown. Here we review the evidence for UV vision in birds, discuss the special properties of UV light, lay out in detail hypotheses for the function of UV vision in birds and discuss their plausibility. The main hypotheses are that UV vision functions: (i) in orientation, (ii) in foraging and (iii) in signalling. The first receives support from studies of homing pigeons, but it would be unwise to conclude that orientation is UV's primary function in all birds. It is especially important to test the signalling hypothesis because bird plumage often reflects UV and tests of theories of sexual selection have virtually always assumed that birds perceive plumage ''colours'' as humans do. A priori this assumption is unlikely to be correct, for unlike humans, birds see in the UV, have at least four types of cones and have a system of oil droplets which filters light entering individual cones.

Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors

Birds have four spectrally distinct types of single cones that they use for colour vision. It is often desirable to be able to model the spectral sensitivities of the different cone types, which vary considerably between species. However, although there are several mathematical models available for describing the spectral absorption of visual pigments, there is no model describing the spectral absorption of the coloured oil droplets found in three of the four single cone types. In this paper, we describe such a model and illustrate its use in estimating the spectral sensitivities of single cones. Furthermore, we show that the spectral locations of the wavelengths of maximum absorbance (lambda(max)) of the short- (SWS), medium- (MWS) and long- (LWS) wavelength-sensitive visual pigments and the cut-off wavelengths (lambda(cut)) of their respective C-, Y- and R-type oil droplets can be predicted from the lambda(max) of the ultraviolet- (UVS)/violet- ( VS) sensitive visual pigment.

Ultraviolet colour perception in European starlings and Japanese quail

Whereas humans have three types of cone photoreceptor, birds have four types of single cones and, unlike humans, are sensitive to ultraviolet light (UV, 320-400 run). Most birds are thought to have either a violet-sensitive single cone that has some sensitivity to UV wavelengths (for example, many non-passerine species) or a single cone that has maximum sensitivity to UV (for example, oscine passerine. species). UV sensitivity is possible because, unlike humans, avian ocular media do not absorb UV light before it reaches the retina. The different single cone types and their sensitivity to UV light give birds the potential to discriminate reflectance spectra that look identical to humans. It is clear that birds use UV signals for a number of visual tasks, but there are few studies that directly demonstrate a role for UV in the detection of chromaticity differences (i.e. colour vision) as opposed to achromatic brightness. If the output of the violet/UV cone is used in achromatic visual tasks, objects reflecting more UV will appear brighter to the bird. 11, however, the output is used in a chromatic mechanism, birds will be able to discriminate spectral stimuli according to the amount of reflected light in the UV part of the spectrum relative to longer wavelengths. We have developed a UV 'colour blindness' test, which we have given to a passerine (European starling) and a non-passerine (Japanese quail) species. Both species learnt to discriminate between a longwave control of orange vs red stimuli and UV vs 'non-UV' stimuli, which were designed to be impossible to differentiate by achromatic mechanisms. We therefore conclude that the output of the violet/UV cone is involved in a chromatic colour vision system in these two species.

North American Bird Conservation Initiative in the United States : a vision of American bird conservation /

"September 2000."

Insect and bird interactions

This unique book is the first of its kind to explore the diversity of interactions between insects and birds. A group of international experts enthusiastically agreed to contribute to the four sections of the book following the success of an Entomological Club Conference on Insect and Bird Interactions. The first section covers population management issues, discussing effects on birds highly relevant to the planting of large areas of GM crops, new opportunities for increasing biodiversity in farming landscapes, and the novel aspect of managing insects by exploiting birds as biological control agents. This is followed by a section discussing the effects of insecticides on bird populations, and includes a contribution from the RSPB, as well as a re-appraisal of the effects of DDT on raptors. Next, the foraging behaviour of birds on insects is discussed, with chapters also on 'warning' coloration in insects and learning by birds. The first chapter in this section is unusual in having been written by an ophthalmologist and covers colour vision in birds, more specifically ultraviolet vision in relation to insect coloration. Finally, the authors look at insects that are parasites of birds or feed on the detritus in nests, and review the ecology and evolution of the co-adaptation of insect ectoparasites with birds. Insect and Bird Interactions is unparalleled in scope and coverage and will be of interest to entomologists, ornithologists, and ecologists alike.

Avian retinal oil droplets : dietary manipulation of colour vision?

Avian vision is highly developed, with bird retinas containing rod and double-cone photoreceptors, plus four classes of single cones subserving tetrachromatic colour vision. Cones contain an oil droplet, rich in carotenoid pigments (except VS/ultraviolet-sensitive cones), that acts as a filter, substantially modifying light detected by the photoreceptor. Using dietary manipulations, we tested the effects of carotenoid availability on oil droplet absorbance properties in two species: Platycercus elegans and Taeniopygia guttata. Using microspectrophotometry, we determined whether manipulations affected oil droplet carotenoid concentration and whether changes would alter colour discrimination ability. In both species, increases in carotenoid concentration were found in carotenoid-supplemented birds, but only in the double cones. Magnitudes of effects of manipulations were often dependent on retinal location. The study provides, to our knowledge, the first experimental evidence of dietary intake over a short time period affecting carotenoid concentration of retinal oil droplets. Moreover, the allocation of carotenoids to the retina by both species is such that the change potentially preserves the spectral tuning of colour vision. Our study generates new insights into retinal regulation of carotenoid concentration of oil droplets, an area about which very little is known, with implications for our understanding of trade-offs in carotenoid allocation in birds.

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 (Pal trs 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 (lambda(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-sensitive-single 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 lambda(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.

Ultraviolet vision and band-colour preferences in female zebra finches, Taeniopygia guttata

Zebra finches have previously been found to have preferences for particular colours of both natural and artificial traits among opposite sex conspecifics. For example, in some studies female zebra finches preferred males wearing red leg bands to orange-banded and unbanded birds and rejected light green-banded males. In other studies, females also preferred males with red beaks to orange-beaked males. However, several authors have failed to replicate these results. We show that females may fail to show a colour preference because of the absence or removal of ultraviolet light under experimental conditions. In mate-choice trials, females observing males through filters that transmitted ultraviolet preferred red-banded males but where females viewed males through ultraviolet-blocking filters, no such preference was observed. Further investigation revealed that the lack of a colour preference when ultraviolet was absent was probably due to the change in overall appearance of the bird, rather than the change in appearance of the rings themselves. This work highlights the importance of proper consideration of the sensory capabilities of animals in experimental design, particularly with regard to the role of ultraviolet light in avian colour perception. (C) 1997 The Association for the Study of Animal Behaviour.

Tetrachromacy, oil droplets and bird plumage colours

There is a growing body of data on avian eyes, including measurements of visual pigment and oil droplet spectral absorption, and of receptor densities and their distributions across the retina. These data are sufficient to predict psychophysical colour discrimination thresholds for light-adapted eyes, and hence provide a basis for relating eye design to visual needs. We examine the advantages of coloured oil droplets, UV vision and tetrachromacy for discriminating a diverse set of avian plumage spectra under natural illumination. Discriminability is enhanced both by tetrachromacy and coloured oil droplets. Oil droplets may also improve colour constancy. Comparison of the performance of a pigeon's eye, where the shortest wavelength receptor peak is at 410 nm, with that of the passerine Leiothrix, where the ultraviolet-sensitive peak is at 365 nm, generally shows a small advantage to the latter, but this advantage depends critically on the noise level in the sensitivity mechanism and on the set of spectra being viewed.

Ultraviolet-sensitive vision in long-lived birds

Long-term exposure to ultraviolet (UV) light generates substantial damage, and in mammals, visual sensitivity to UV is restricted to short-lived diurnal rodents and certain marsupials. In humans, the cornea and lens absorb all UV-A and most of the terrestrial UV-B radiation, preventing the reactive and damaging shorter wavelengths from reaching the retina. This is not the case in certain species of long-lived diurnal birds, which possess UV-sensitive (UVS) visual pigments, maximally sensitive below 400 nm. The Order Psittaciformes contains some of the longest lived bird species, and the two species examined so far have been shown to possess UVS pigments. The objective of this study was to investigate the prevalence of UVS pigments across long-lived parrots, macaws and cockatoos, and therefore assess whether they need to cope with the accumulated effects of exposure to UV-A and UV-B over a long period of time. Sequences from the SWS1 opsin gene revealed that all 14 species investigated possess a key substitution that has been shown to determine a UVS pigment. Furthermore, in vitro regeneration data, and lens transparency, corroborate the molecular findings of UV sensitivity. Our findings thus support the claim that the Psittaciformes are the only avian Order in which UVS pigments are ubiquitous, and indicate that these long-lived birds have UV sensitivity, despite the risks of photodamage.

Thermal Imagery Applied to Reducing Bird Hazards to Aircraft at Airports

Airports worldwide are at a disadvantage when it comes to being able to spot birds and warn aircrews about the location of flocks either on the ground or close to the airfield. Birds simply cannot be easily seen during the day and are nearly invisible targets for planes at night or during low visibility. Thermal imaging (infrared) devices can be used to allow ground and tower personnel to pinpoint bird locations day or night, thus giving the airport operators the ability to launch countermeasures or simply warn the aircrews. This technology is available now, though it has been predominately isolated to medical and military system modifications. The cost of these devices has dropped significantly in recent years as technology, capability, and availability have continued to increase. Davison Army Airfield (DAAF), which is located about 20 miles south of Ronald Reagan National Airport in Washington, DC, is the transient home to many bird species including an abundance of ducks, seagulls, pigeons, and migrating Canadian geese. Over the past few years, DAAF implemented a variety of measures in an attempt to control the bird hazards on the airfield. Unfortunately, when it came to controlling these birds on or near our runways and aircraft movement areas we were more reactive than proactive. We would do airfield checks several times an hour to detect and deter any birds in these areas. The deterrents used included vehicle/human presence, pyrotechnics, and the periodic use of a trained border collie. At the time, we felt like we were doing all we could to reduce the threat to aircraft and human life. It was not until a near fatal accident in October 1998, when we truly realized how dangerous our operating environment really was to aircraft at or near the airfield. It was at this time, we had a C-12 (twin-engine passenger plane) land on our primary runway at night. The tower cleared the aircraft to land, and upon touchdown to the runway the aircraft collided with a flock of geese. Neither the tower nor the crew of the aircraft saw the geese because they were obscured in the darkness. The end result was 12 dead geese and $374,000 damage to the C-12. Fortunately, there were no human fatalities, but it was painfully clear we needed to improve our method of clearing the runway at night and during low visibility conditions. It was through this realization that we ventured to the U.S. Army Communications and Electronics Command for ideas on ways to deal with our threat. It was through a sub-organization within this command, Night Vision Labs, that we realized the possibilities of modifying thermal imagery and infrared technology to detecting wildlife on airports.

Microspectrophotometry of visual pigments and oil droplets in a marine bird, the wedge-tailed shearwater Puffinus pacificus: Topographic variations in photoreceptor spectral characteristics

Microspectrophotometric examination of the retina of a procellariiform marine bird, the wedge-tailed shearwater Puffinus pacificus, revealed the presence of five different types of vitamin A(1)-based visual pigment in seven different types of photoreceptor. A single class of rod contained a medium-wavelength sensitive visual pigment with a wavelength of maximum absorbance (lambda(max)) at 502 nm. Four different types of single cone contained visual pigments maximally sensitive in either the violet (VS, lambda(max) 406 nm), short (SWS, lambda(max) 450 nm), medium (MWS, lambda(max) 503 nm) or long (LWS, lambda(max) 566 nm) spectral ranges. In the peripheral retina, the SWS, MWS and LWS single cones contained pigmented oil droplets in their inner segments with cut-off wavelengths (lambda(cut)) at 445 (C-type), 506 (Y-type) and 562 nm (R-type), respectively. The VS visual pigment was paired with a transparent (T-type) oil droplet that displayed no significant absorption above at least 370 run. Both the principal and accessory members of the double cone pair contained the same 566 nm lambda(max) visual pigment as the LWS single cones but only the principal member contained an oil droplet, which had a lambda(cut) at 413 nm. The retina had a horizontal band or 'visual streak' of increased photoreceptor density running across the retina approximately 1.5 mm dorsal to the top of the pecten. Cones in the centre of the horizontal streak were smaller and had oil droplets that were either transparent/colourless or much less pigmented than at the periphery. It is proposed that the reduction in cone oil droplet pigmentation in retinal areas associated with high visual acuity is an adaptation to compensate for the reduced photon capture ability of the narrower photoreceptors found there. Measurements of the spectral transmittance of the ocular media reveal that wavelengths down to at least 300 nm would be transmitted to the retina.