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.

Ultraviolet vision, fluorescence and mate choice in a parrot, the budgerigar Melopsittacus undulatus

As in many parrots, the plumage of the budgerigar Melopsittacus undulatus reflects near-ultraviolet (UVA) wavelengths (300-400 nm) and exhibits UVA-induced fluorescence. However, there have, to our knowledge, been no tests of whether the yellow fluorescence observed under intense UVA illumination has any role in signalling. Four experiments were carried out on wild-type budgerigars, where the presence and absence of UV reflectance and fluorescence were manipulated using filters. Few studies have attempted to separate the contribution of UV reflectance to plumage hue as opposed to brightness or distinguish between a role in sexual as opposed to social preferences. However, our first experiments show that not only do females consistently prefer UV-reflecting males, but also that the observed preferences are due to removal of UV affecting the perceived hue rather than brightness. Furthermore, we found no effect Of the light environment on male response to females, suggesting that the female preferences relate to plumage colour per se. Whilst UV reflectance appears important in heterosexual choice by, females, it has no detectable influence on same-sex association preferences. The results from the second series of experiments suggest that enhancement of the budgerigar's yellow coloration through fluorescence has no effect on male attractiveness. However, the fluorescent plumage may play a role in signalling by virtue of the fact that it absorbs UVA and so increases contrast with nearby UV-reflecting plumage. Our study provides convincing evidence that UV reflectances can play a role in mate choice in non-passerines, but no evidence that the yellow fluorescence observed under UVA illumination is itself important as a signal.

Animal visual systems and the evolution of color patterns; sensory processing illuminates signal evolution

Animal color pattern phenotypes evolve rapidly. What influences their evolution? Because color patterns are used in communication, selection for signal efficacy, relative to the intended receiver's visual system, may explain and predict the direction of evolution. We investigated this in bowerbirds, whose color patterns consist of plumage, bower structure, and ornaments and whose visual displays are presented under predictable visual conditions. We used data on avian vision, environmental conditions, color pattern properties, and an estimate of the bowerbird phylogeny to test hypotheses about evolutionary effects of visual processing. Different components of the color pattern evolve differently. Plumage sexual dimorphism increased and then decreased, while overall (plumage plus bower) visual contrast increased. The use of bowers allows relative crypsis of the bird but increased efficacy of the signal as a whole. Ornaments do not elaborate existing plumage features but instead are innovations (new color schemes) that increase signal efficacy. Isolation between species could be facilitated by plumage but not ornaments, because we observed character displacement only in plumage. Bowerbird color pattern evolution is at least partially predictable from the function of the visual system and from knowledge of different functions of different components of the color patterns. This provides clues to how more constrained visual signaling systems may evolve.

Absorbance of retinal oil droplets of the budgerigar : sex, spatial and plumage morph-related variation

Intraspecific variation in photoreceptor physiology is known in several vertebrate taxa, but is currently unknown in birds, despite many avian traits varying intraspecifically, and avian visual ecology encompassing a wide range of environments and visual stimuli, which might influence spectral sensitivity. Avian retinal photoreceptors contain light absorbing carotenoid-rich oil droplets that affect vision. Carotenoids are also important plumage components. However, our understanding of the regulation of carotenoids in oil droplets remains rudimentary. Among birds, Melopsittacus undulatus has probably the best-studied colour vision, shows profound intraspecific variation in plumage colour, and increased plasma carotenoids during moult. We used microspectrophotometry to determine whether a relationship exists between oil droplet carotenoid concentration and plumage pigmentation, and tested for sex and spatial variation in droplet absorbance across the retina. Absorbance of one variety of P-type droplets was higher in males. No relationship was found between droplet absorbance and plumage colour. We found a spatial pattern of droplets absorbance across the retina that matched a pattern found in another parrot, and other avian species. Our work provides insights into the development and maintenance of retinal oil droplets and suggests a common mechanism and function for carotenoid deposition in the retina across bird species.

Characterizing background heterogeneity in visual communication

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Distinctive Convergence in Australian Floral Colours Seen Through the Eyes of Australian Birds

We used a colour-space model of avian vision to assess whether a distinctive bird pollination syndrome exists for floral colour among Australian angiosperms. We also used a novel phylogenetically based method to assess whether such a syndrome represents a significant degree of convergent evolution. About half of the 80 species in our sample that attract nectarivorous birds had floral colours in a small, isolated region of colour space characterized by an emphasis on long-wavelength reflection. The distinctiveness of this 'red arm' region was much greater when colours were modelled for violet-sensitive (VS) avian vision than for the ultraviolet-sensitive visual system. Honeyeaters (Meliphagidae) are the dominant avian nectarivores in Australia and have VS vision. Ancestral state reconstructions suggest that 31 lineages evolved into the red arm region, whereas simulations indicate that an average of five or six lineages and a maximum of 22 are likely to have entered in the absence of selection. Thus, significant evolutionary convergence on a distinctive floral colour syndrome for bird pollination has occurred in Australia, although only a subset of bird-pollinated taxa belongs to this syndrome. The visual system of honeyeaters has been the apparent driver of this convergence.

Animal visual systems and the evolution of color patterns: Sensory processing illuminates signal evolution

Animal color pattern phenotypes evolve rapidly. What influences their evolution? Because color patterns are used in communication, selection for signal efficacy, relative to the intended receiver's visual system, may explain and predict the direction of evolution. We investigated this in bowerbirds, whose color patterns consist of plumage, bower structure, and ornaments and whose visual displays are presented under predictable visual conditions. We used data on avian vision, environmental conditions, color pattern properties, and an estimate of the bowerbird phylogeny to test hypotheses about evolutionary effects of visual processing. Different components of the color pattern evolve differently. Plumage sexual dimorphism increased and then decreased, while overall (plumage plus bower) visual contrast increased. The use of bowers allows relative crypsis of the bird but increased efficacy of the signal as a whole. Ornaments do not elaborate existing plumage features but instead are innovations (new color schemes) that increase signal efficacy. Isolation between species could be facilitated by plumage but not ornaments, because we observed character displacement only in plumage. Bowerbird color pattern evolution is at least partially predictable from the function of the visual system and from knowledge of different functions of different components of the color patterns. This provides clues to how more constrained visual signaling systems may evolve.

Avian color vision and coloration : multidisciplinary evolutionary biology

A fundamental issue in biology is explaining the diversity of coloration found in nature. Birds provide some of the best-studied examples of the evolution and causes of color variation and some of the most arresting color displays in the natural world. They possess perhaps the most richly endowed visual system of any vertebrate, including UV-A sensitivity and tetrachromatic color vision over the 300-700-nm waveband. Birds provide model systems for the multidisciplinary study of animal coloration and color vision. Recent advances in understanding avian coloration and color vision are due to recognition that birds see colors in a different way than humans do and to the ready availability of small spectrometers. We summarize the state of the current field, recent trends, and likely future directions.

The role of visual landmarks in the avian familiar area map - Commentary

The question of whether homing pigeons use visual landmarks for orientation from distant, familiar sites is an unresolved issue in the field of avian navigation. Where evidence has been found, the question still remains as to whether the landmarks are used independent of the map and compass mechanism for orientation that is so important to birds. Recent research has challenged the extent to which experiments that do not directly manipulate the visual sense can be used as evidence for compass-independent orientation. However, it is proposed that extending a new technique for research on vision in homing to include manipulation of the compasses used by birds might be able to resolve this issue. The effect of the structure of the visual sense of the homing pigeon on its use of visual landmarks is also considered.

Ultraviolet vision and mate choice in zebra finches

SEXUAL selection is one of the most actively studied areas of evolutionary biology(1-3), and ever since Darwin(1) birds have been probably the most popular taxon for testing the predictions about colour variation. Humans have been used to assess 'colour', an approach which may be flawed(4,5) as many birds see in the ultraviolet (to which humans are blind), and have at least four spectral classes of retinal cone cells (humans have only three), Here we report experiments on zebra finches which test the hypothesis that the ultraviolet waveband (300-400 nm) is used in avian mate-choice decisions. We found that the ultraviolet is used, and that it probably contributes to hue perception. This finding may have,vide implications for future studies of avian sexual selection and colour, and supports one hypothesized function of avian ultraviolet vision, the role of which is largely unknown.(4,6,7)

Plumage reflectance and the objective assessment of avian sexual dichromatism

Assessment of color using human vision (or standards based thereon) is central to tests of many evolutionary hypotheses. Yet fundamental differences in color Vision between humans and other animals call this approach into question. Here we use techniques for objectively assessing color patterns that avoid reliance on species-specific (e.g., human) perception. Reflectance spectra are the invariant features that we expect the animal's color cognition to have evolved to extract. We performed multivariate analyses on principal components derived from >2,600 reflectance spectra (300-720 nm) sampled in a stratified random design from different body regions of male and female starlings in breeding plumage. Starlings possess spatially complex plumage patterns and extensive areas of iridescence. Our study revealed previously unnoticed sex differences in plumage coloration and the nature of iridescent and noniridescent sex differences. Sex differences occurred in some body regions bur not others, were more pronounced at some wavelengths (both ultraviolet and human visible), and involved differences in mean reflectance and spectral shape. Discriminant analysis based on principal components were sufficient to sex correctly 100% of our sample. If hidden sexual dichromatism is widespread, then it has important implications for classifications of animals as mono- or dimorphic and for taxonomic and conservation purposes.

Is the ultraviolet waveband a special communication channel in avian mate choice?

There is growing evidence that ultraviolet (UV) wavelengths play an important role in avian mate choice. One of the first experiments to support this idea showed that female zebra finches (Taeniopygia guttata) prefer UV-reflecting males to males whose ultraviolet reflection has been removed. The effect was very strong despite little or no UV reflection from several plumage areas. However, it is not clear how the importance of the UV waveband compares to other regions of the bird-visible spectrum. We tested whether the response of female zebra finches to the removal of male UV reflection is greater than to the removal of other wavebands. We presented females with a choice of males whose appearance was manipulated using coloured filters. The filters removed single blocks of the avian visible spectrum corresponding closely to the spectral sensitivities of each of the zebra finch's single cone classes. This resulted in males that effectively had no UV (UV-), no short-wave (SW-), no medium-wave (MW-) or no long-wave (LW-) plumage reflection. Females preferred UV- and SW- males. LW- and MW- males were least preferred, suggesting that female zebra finches show the greatest response to the removal of longer wavelengths. Quantal catches of the single cone types viewing body areas of the male zebra finch are presented for each treatment. Our study suggests it is important to consider the role of the UV waveband in avian mate choice in conjunction with the rest of the avian visible spectrum.

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.

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.