Andrew T. D. Bennett

Ultraviolet Vision in Birds

Publisher Summary Birds can see ultraviolet (UV) light because, unlike humans, their lenses and other ocular media transmit UV, and they possess a class of photoreceptor, which is maximally sensitive to violet or UV light, depending on the species. Birds have a tetrachromatic color space, as compared to the trichromacy of humans. Birds, along with some reptiles and fish, also possess double cones in large numbers and a cone class. This chapter discusses a range of behavioral experiments, from several species, which show that UV information is utilized in behavioral decisions, notably in foraging and signaling. Removal of UV wavelengths affects mate choice even in species that are colorful to humans. These studies emphasize that avian and human color perceptions are different and that the use of human color standards, and even artificial lighting, may produce misleading results. However, genuinely objective measures of color are available, as are, importantly, models for mapping the measured spectra into an avian color space.

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.)

Abstract 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 (λmax) 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 λmax 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.

Sexual Selection and the Mismeasure of Color

Many long-standing evolutionary hypotheses make predictions about trends in color patterns. Examples of these include crypsis, mimicry and warning coloration, fruit coloration, flower coloration, the handicap principle of honest advertisement, Fishers runaway process, the parasite theory of sexual selection, and sensory drive theories of signaling. The majority of tests of these hypotheses, particularly with regard to sexual selection, have been conducted on objects that birds perceive visually, with human vision used to assess color. This assumes that birds see color patterns as humans do, an assumption that is seriously flawed. First, birds see very well parts of the spectrum that humans cannot. Second, birds have at least four dimensions to their color vision, compared to only three in humans. Third, birds have a complex system of oil droplets in their retinas, which may alter the number of hues they perceive. Thus, an object will not appear to have the same hues for a human and a bird, and maybe not even the same relative brightness or saturation. Despite this, human vision is routinely, and almost without exception, the method used for assessment of color patterns seen by birds. We argue that the error in this assumption may well be a major reason that support for various evolutionary hypotheses involving color is an area of controversy. We also suggest methods for overcoming the shortcomings of existing studies and suggest which previous approaches are likely to have been most erroneous. As part of this, it is apparent that a research program in color cognition is necessary, for if we wish to understand evolutionary hypotheses involving color we need to understand how animals perceive color. Color is not an inherent property of the object; it is a product of the brain of the animal perceiving the object. Humans can see hues seen by birds as much as knowledge of x and y coordinates can predict the position of a point in three-dimensional space.

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.

Egg colour matching in an African cuckoo, as revealed by ultraviolet-visible reflectance spectrophotometry

Despite major differences between human and avian colour vision, previous studies of cuckoo egg mimicry have used human colour vision (or standards based thereon) to assess colour matching. Using ultraviolet–visible reflectance spectrophotometry (300–700 nm), we measured museum collections of eggs of the red–chested cuckoo and its hosts. The first three principal components explained more than 99% of the variance in spectra, and measures of cuckoo–host egg similarity derived from these transformations were compared with measures of cuckoo–host egg similarity estimated by human observers unaware of the hypotheses we were testing. Monte Carlo methods were used to simulate laying of cuckoo eggs at random in nests. Results showed that host and cuckoo eggs were very highly matched for an ultraviolet versus greenness component, which was not detected by humans. Furthermore, whereas cuckoo and host were dissimilar in achromatic brightness, humans did not detect this difference. Our study thus reveals aspects of cuckoo–host egg colour matching which have hitherto not been described. These results suggest subtleties and complexities in the evolution of host–cuckoo egg mimicry that were not previously suspected. Our results also have the potential to explain the longstanding paradox that some host species accept cuckoo eggs that are non–mimetic to the human eye.

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 consider-ation of the sensory capabilities of animals in experimental design, particularly with regard to the role of ultraviolet light in avian colour perception.Copyright 1997 The Association for the Study of Animal BehaviourCopyright 1997The Association for the Study of Animal Behaviour.

Ultraviolet cues affect the foraging behaviour of blue tits

The function of avian ultraviolet (UV) vision is only just beginning to be understood. One plausible hypothesis is that UV vision enhances the foraging ability of birds. To test this, we carried out behavioural experiments using wild–caught blue tits foraging for cabbage moth and winter moth caterpillars on natural and artificial backgrounds. The light environment in our experiments was manipulated using either UV–blocking or UV–transmitting filters. We found that the blue tits tended to find the first prey item (out of four) more quickly when UV cues were present. This suggests that UV vision offers benefits to birds when searching for cryptic prey, despite the prey and backgrounds reflecting relatively little UV. Although there was no direct effect of UV on the time taken to find all four prey items in a trial, search performance in the absence of UV wavelengths tended to increase over the course of an experiment. This may reflect changes in the search tactics of the birds. To our knowledge, these are the first data to suggest that birds use UV cues to detect cryptic insect prey, and have implications for our understanding of protective coloration.

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 budgerigars 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.

An Integrative Framework for the Appraisal of Coloration in Nature

The world in color presents a dazzling dimension of phenotypic variation. Biological interest in this variation has burgeoned, due to both increased means for quantifying spectral information and heightened appreciation for how animals view the world differently than humans. Effective study of color traits is challenged by how to best quantify visual perception in nonhuman species. This requires consideration of at least visual physiology but ultimately also the neural processes underlying perception. Our knowledge of color perception is founded largely on the principles gained from human psychophysics that have proven generalizable based on comparative studies in select animal models. Appreciation of these principles, their empirical foundation, and the reasonable limits to their applicability is crucial to reaching informed conclusions in color research. In this article, we seek a common intellectual basis for the study of color in nature. We first discuss the key perceptual principles, namely, retinal photoreception, sensory channels, opponent processing, color constancy, and receptor noise. We then draw on this basis to inform an analytical framework driven by the research question in relation to identifiable viewers and visual tasks of interest. Consideration of the limits to perceptual inference guides two primary decisions: first, whether a sensory-based approach is necessary and justified and, second, whether the visual task refers to perceptual distance or discriminability. We outline informed approaches in each situation and discuss key challenges for future progress, focusing particularly on how animals perceive color. Given that animal behavior serves as both the basic unit of psychophysics and the ultimate driver of color ecology/evolution, behavioral data are critical to reconciling knowledge across the schools of color research.

Mimicry and the eye of the beholder

Recent experiments (Dittrich et al. ( Proc.R. Soc. Lond. B 251, 195 (1993))) suggest that pigeon perception of wasp mimicry by hoverflies is similar to that of humans and of computer-based image matching. However, the relations are nonlinear and may explain why some species are abundant despite their being poor mimics to the human eye. We suggest that these discrepancies between pigeon and human categorization may lie in the differences between avian and primate colour vision. As pigeon categorization and computer image analysis were both assessed by using colour slides designed for human vision, they lacked the natural colour information available to wild birds, in particular that from ultraviolet (uv) wavelengths.