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The Visual Ecology of Avian Photoreceptors Nathan S PII: S1350-9462(01)00009-X The Visual Ecology of Avian Photoreceptors Nathan S. Hart* Vision, Touch and Hearing Research Centre, Department of Physiology and Pharmacology, The University of Queensland, Brisbane 4072, Australia CONTENTS Abstract . 676 1. Introduction . 676 1.1. The avian visual system . 676 1.2. Microspectrophotometry and the study ofavian vision . 676 2. Avian retinal photoreceptors . 681 2.1. Visual pigments . 681 2.2. Cone oil droplets . 684 3. UVS/VS cones . 685 3.1. Microspectrophotometric data . 685 3.2. Spectral tuning and phylogeny . 685 3.3. Evolution ofSWS1 opsin-based visual pigments in birds . 686 3.4. The short wavelength limit ofphotoreception . 686 4. SWS single cones. 687 4.1. Microspectrophotometric data . 687 4.2. Dependence upon UVS/VS single cone spectral sensitivity . 688 4.3. Spectral tuning . 688 5. Rods and MWS single cones . 688 5.1. Comparison ofavian RH1 and RH2 opsins . 688 5.2. The duplex retina . 689 5.3. Factors influencing rod visual pigment kmax ........................ 689 6. LWS single and double cones . 691 6.1. Microspectrophotometric data . 691 6.2. Spectral tuning . 691 6.3. Effect ofoil droplet transmittance on spectral sensitivity . 692 6.4. Double cones and the interspecific variation in LWS visual pigment kmax ........ 692 6.5. Spectral filtering by double cone oil droplets . 694 7. Variations in the relative proportions ofdifferent cone types . 695 7.1. Interspecific variations . 695 7.2. Intraretinal variations . 696 7.3. Bilateral asymmetry . 697 8. Conclusions . 697 9. Future directions . 698 Acknowledgements . 698 References . 698 *Tel.: +61-7-3365-1867; fax: +61-7-3365-4522; e-mail: [email protected]. Progress in Retinal and Eye Research Vol. 20, No. 5, pp. 675 to 703, 2001 r 2001 Elsevier Science Ltd. All rights reserved Printed in Great Britain 1350-9462/01/$ - see front matter 676 N. S. Hart AbstractFThe spectral sensitivities ofavian retinal photoreceptors are examined with respect to microspectrophotometric measurements ofsingle cells, spectrophotometric measurements ofextracted or in vitro regenerated visual pigments, and molecular genetic analyses ofvisual pigment opsin protein sequences. Bird species fromdiverse orders are compared in relation to their evolution, their habitats and the multiplicity ofvisual tasks they must perform.Birds have five different types ofvisual pigment and seven different types ofphotoreceptor Frods, double (uneven twin) cones and four types of single cone. The spectral locations ofthe wavelengths ofmaximum absorbance ( lmax) ofthe different visual pigments, and the spectral transmittance characteristics ofthe intraocular spectral filters (cone oil droplets) that also determine photoreceptor spectral sensitivity, vary according to both habitat and phylogenetic relatedness. The primary influence on avian retinal design appears to be the range ofwavelengths available forvision, regardless ofwhether that range is determined by the spectral distribution ofthe natural illumination or the spectral transmittance ofthe ocular media (cornea, aqueous humour, lens, vitreous humour). Nevertheless, other variations in spectral sensitivity exist that reflect the variability and complexity ofavian visual ecology. r 2001 Elsevier Science Ltd. All rights reserved 1. INTRODUCTION doing so, our relatively limited knowledge ofthe avian visual system has been exposed. However, 1.1. The avian visual system many new data regarding the spectral absorption properties ofavian photoreceptors have since been As a class, birds are renowned for their colourful obtained using microspectrophotometry; the pur- F plumage and aerobatic skill traits that imply pose ofthis article is to collate the additional well-developed colour discrimination and move- information and assess our current understanding ment detection capabilities. Indeed, most birds rely in light ofrecent molecular genetic studies. primarily on their visual sense to collect informa- tion from the environment and have among the most complex retinae ofany vertebrate (Walls, 1.2. Microspectrophotometry and the study of avian 1942; Meyer, 1977). The majority ofdiurnal birds vision studied to date possess a single class ofrod, a single type ofdouble cone and fourdifferent types Microspectrophotometry is the application of ofsingle cone (see Table 1 and references therein). standard spectrophotometric techniques to micro- The retina functions as a two-dimensional scopic samples. Single cell microspectrophotome- detector array, sampling visual information from try uses modified microscope optics to pass a very images ofa three-dimensional world projected by narrow beam (ca. 2 Â 2 mm in cross section) oflight the lens and cornea (Martin, 1985); only photons through a cell, and a photoelectric device to that are absorbed by the photoreceptors can be measure the amount oflight transmitted at each used for vision. Consequently, the spectral sensi- wavelength. It is the only method by which the tivity, relative abundance and packing arrange- spectral absorption properties ofvisual pigments ment in the retinal mosaic ofdifferent can be measured in situ from individual retinal photoreceptor types define the visual capabilities photoreceptors, and has been invaluable in the ofan animal. Understanding how each ofthese study ofavian vision. aspects ofretinal design is optimised, through Soon after the technique was invented for the evolution, for the visual requirements of different study ofnucleic acids in the cell nucleus (Caspers- species is a fundamental tenet of visual ecology son, 1940), microspectrophotometry was used to (Lythgoe, 1979). measure absorption spectra from individual cone Recent studies on sexual selection (Bennett outer segments ofthe carp, Cyprinus carpio et al., 1996; Andersson and Amundsen, 1997; (Hanaoka and Fujimoto, 1957). At the same time, Bennett et al., 1997; Hunt et al., 1997; Andersson attempts to obtain absorption spectra ofavian et al., 1998) and foraging behaviour in birds cone visual pigments were thwarted by the small (Viitala et al., 1995; Koivula et al., 1997; Church size oftheir outer segments and only the absorp- et al., 1998b) have emphasised the need to tion spectra ofcone oil droplets were measured interpret visual signals on the basis ofthe visual (Fujimoto et al., 1957; Hanaoka and Fujimoto, system with which they are deconstructed. In 1957). Visual ecology ofavian photoreceptors 677 Despite improvements in the design, construc- Fukada, 1993) and at pH values and temperatures tion and use ofmicrospectrophotometers, which that do not affect rod visual pigments (Fager and had allowed high-quality spectra to be measured Fager, 1982). Although multiple cone visual from several fish, amphibian, reptile and mamma- pigments have since been separated chromatogra- lian species (see for examples Brown, 1961; Lieb- phically from retinal extracts (Fager and Fager, man, 1962; Liebman and Entine, 1964; Marks 1981, 1982; Yen and Fager, 1984; Yoshizawa et al., 1964; Marks, 1965; Liebman and Entine, et al., 1991; Yoshizawa and Fukada, 1993, see 1968; Wolken et al., 1968; Liebman and Granda, Table 2), it was results from microspectrophoto- 1971), the first microspectrophotometric measure- metry that finally invalidated Krause’s theory. In ments ofavian visual pigments were not published 1977, multiple cone visual pigments were measured until the early 1970s. Liebman (1972) showed that in situ in both the chicken (lmax 497 and 569 nm; the rod outer segments ofchickens ( Gallus gallus), Bowmaker and Knowles, 1977) and pigeon retina pigeons (Columba livia) and laughing gulls (Larus (lmax 460, 515, 567 nm; Bowmaker, 1977). These atricilla) contained a visual pigment with a findings were supported by electrophysiological wavelength ofmaximum absorbance ( lmax)at evidence which suggested that these species pos- around 500 nm. Their cones, on the other hand, sessed four cone pigments with lmax near 413, 467, appeared to contain a visual pigment maximally 507 and 562 nm (Govardovskii and Zeuva, 1977). sensitive to longer wavelengths (lmax between Moreover, it was demonstrated that Japanese about 560 and 575 nm). quail (Coturnix coturnix japonica) raised on a Colour vision (the ability to discriminate objects carotenoid-free diet, and therefore possessing only on the basis ofwavelength rather than intensity) colourless oil droplets, retained colour vision requires two or more spectrally distinct photo- (Meyer, 1971; Meyer et al., 1971; Duecker and receptors, usually cones, the outputs ofwhich can Schultz, 1977; Wallman, 1979). Liebman’s failure be compared simultaneously by the nervous to identify more than one cone visual pigment in system. In 1863, Krause (cited in Walls, 1942) birds using microspectrophotometry (Liebman, had suggested that colour vision in birds was 1972) was probably due to difficulties in measuring mediated by a single cone visual pigment in the absorption spectra ofavian cone outer conjunction with different coloured cone oil segments, which are very small (typically 1–2 mm droplets. Because each oil droplet type would in diameter; see Fig. 3) and often remain attached transmit only specific wavelengths to the outer to the pigmented epithelium when the retina is segment, he proposed that oil droplet absorption removed from the eyecup (Bowmaker, 1984; alone could differentiate cones into several spectral Levine and MacNichol, 1985). types. A failure to prove the existence of more than The presence ofup to fourspectrally distinct one cone visual pigment in birds by either cone visual pigments
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