Abstract
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.
Similar content being viewed by others
References
Armington JC, Thiede FC (1956) Electroretinal demonstration of a Purkinje shift in the chicken eye. Am J Physiol 186:258–262
Barber CL, Prescott NB, Jarvis JR, Le Sueur C, Perry GC, Wathes CM (2006) Comparative study of the photopic spectral sensitivity of domestic ducks (Anas platyrhynchos domesticus), turkeys (Meleagris gallopavo) and humans. Brit Poult Sci 47:365–374. doi:10.1080/00071660600753870
Berg M, Bennett ATD (2010) The evolution of plumage colouration in parrots: a review. Emu 110:10–20. doi:10.1071/MU09076
Bowmaker JK, Heath LA, Wilkie SE, Hunt DM (1997) Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vis Res 37:2183–2194. doi:10.1016/S0042-6989(97)00026-6
Campenhausen MV, Kirschfeld K (1998) Spectral sensitivity of the accessory optic system of the pigeon. J Comp Physiol A 183:1–6. doi:10.1007/s003590050229
Chen DM, Goldsmith TH (1984) Appearance of a Purkinje shift in the developing retina of the chick. J Exp Zool 229:265–271. doi:10.1002/jez.1402290212
Donner K (1992) Noise and the absolute threshold of cone and rod vision. Vis Res 32:853–866. doi:10.1016/0042-6989(92)90028-H
Field GD, Sampath AP, Rieke F (2005) Retinal processing near absolute threshold: from behaviour to mechanism. Annu Rev Physiol 67:491–514. doi:10.1146/annurev.physiol.67.031103.151256
Gellermann LW (1993) Chance orders of alternating stimuli in visual discrimination experiments. J Genet Psychol 42:206–208. doi:10.1080/08856559.1933.10534237
Goldsmith TH, Butler BK (2003) The roles of receptor noise and cone oil droplets in the photopic spectral sensitivity of the budgerigar, Melopsittacus undulatus. J Comp Physiol A 189:135–142. doi:10.1007/s00359-002-0385-8
Goldsmith TH, Butler BK (2005) Color vision of the budgerigar (Melopsittacus undulatus): hue matches, tetrachromacy, and intensity discrimination. J Comp Physiol A 191:933–951. doi:10.1007/s00359-005-0024-2
Hart NS (2001a) The visual ecology of avian photoreceptors. Prog Retin Eye Res 20:675–703. doi:10.1016/S1350-9462(01)00009-X
Hart NS (2001b) Variations in cone photoreceptor abundance and the visual ecology of birds. J Comp Physiol A 187:685–698. doi:10.1007/s00359-001-0240-3
Hart NS, Vorobyev M (2005) Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J Comp Physiol A 191:381–392. doi:10.1007/s00359-004-0595-3
Ikeda H (1965) The spectral sensitivity of the pigeon (Columba livia). Vis Res 5:19–36. doi:10.1016/0042-6989(65)90072-6
Kelber A, Lind O (2010) Limits of colour vision in dim light. Ophthal Physiol Opt 30:454–459. doi:10.1111/j.1475-1313.2010.00721.x
Kelber A, Vorobyev M, Osorio D (2003) Animal colour vision: behavioural tests and physiological concepts. Biol Rev 78:81–118. doi:10.1017/S1464793102005985
Knott B, Bowmaker JK, Berg ML, Bennett ATD (2012) Absorbance of retinal oil droplets of the budgerigar: sex, spatial and plumage morph-related variation. J Comp Physiol A 198:43–51. doi:10.1007/s00359-011-0684-z
Land MF, Osorio DC (2003) Colour vision: colouring the dark. Curr Biol 13:R83–R85. doi:10.1016/S0960-9822(03)00031-9
Lind O, Kelber A (2009a) The intensity threshold of colour vision in two species of parrot. J Exp Biol 212:3693–3699. doi:10.1242/jeb.035477
Lind O, Kelber A (2009b) Avian colour vision: effects of variation in receptor sensitivity and noise data on model predictions as compared to behavioural results. Vis Res 49:1939–1947. doi:10.1016/j.visres.2009.05.003
Lind O, Kelber A (2011) The spatial tuning of achromatic and chromatic vision in budgerigars. J Vis 11(7):1–9. doi:10.1167/11.7.2
Lind O, Sunesson T, Mitkus M, Kelber A (2012) Luminance-dependence of spatial vision in budgerigars (Melopsittacus undulatus) and Bourke’s parrots (Neopsephotus bourkii). J Comp Physiol A 198:69–77. doi:10.1007/s00359-011-0689-7
Lind O, Mitkus M, Olsson P, Kelber A (2013) Ultraviolet sensitivity and colour vision in raptor foraging. J Exp Biol 216:1819–1826. doi:10.1242/jeb.082834
Maier EJ (1992) Spectral sensitivities including the ultraviolet of the passeriform bird Leiothrix lutea. J Comp Physiol A 170:709–714. doi:10.1007/BF00198981
Manglapus MK, Uchiyama H, Buelow NF, Barlow RB (1998) Circadian rhythms of rod–cone dominance in the Japanese quail retina. J Neurosci 18:4775–4784
Manglapus MK, Iuvone PM, Underwood H, Pierce ME, Barlow RB (1999) Dopamine mediates circadian rhythms of rod–cone dominance in the Japanese quail retina. J Neurosci 19:4132–4141
Martin GR, Gordon IE (1974) Increment-threshold spectral sensitivity in the tawny owl (Strix aluco). Vis Res 14:615–621. doi:10.1016/0042-6989(74)90055-8
Osorio D, Vorobyev M (2005) Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc R Soc B 272:1745–1752. doi:10.1098/rspb.2005.3156
Osorio D, Miklósi A, Gonda ZS (1999) Visual ecology and perception of coloration patterns by domestic chicks. Evol Ecol 13:673–689. doi:10.1023/A:1011059715610
Prescott NB, Wathes CM (1999) Spectral sensitivity of the domestic fowl (Gallus g domesticus). Brit Poult Sci 40:332–339. doi:10.1080/00071669987412
Remy M, Emmerton J (1989) Behavioral spectral sensitivities of different retinal areas in pigeons. Behav Neurosci 103:170–177. doi:10.1037/0735-7044.103.1.170
Rose A (1942) The relative sensitivities of television pickup tubes, photographic film and the human eye. Proc Inst Radio Eng 30:293–300. doi:10.1109/JRPROC.1942.230998
Schaeffel F, Rohrer B, Lemmer T, Zrenner E (1991) Diurnal control of rod function in the chicken. Vis Neurosci 6:641–653. doi:10.1017/S0952523800002637
Treutwein B (1995) Adaptive psychophysical procedures. Vis Res 35:2503–2522. doi:10.1016/0042-6989(95)00016-X
Vorobyev M (1997) Costs and benefits of increasing the dimensionality of colour vision system. In: Taddei-Ferreti C (ed) Biophysics of photoreception: molecular and phototransductive events. Woted Scientific, Singapore, pp 280–289
Vorobyev M (2003) Coloured oil droplets enhance colour discrimination. Proc R Soc Lond B 270:1255–1261. doi:10.1098/rspb.2003.2381
Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265:351–358. doi:10.1098/rspb.1998.0302
Vorobyev M, Osorio D, Bennett ATD, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621–633. doi:10.1007/s003590050286
Vorobyev M, Brandt R, Peitsch D, Laughlin SB, Menzel R (2001) Colour thresholds and receptor noise: behavior and physiology compared. Vis Res 41:639–653. doi:10.1016/S0042-6989(00)00288-1
Warrant E (2004) Vision in the dimmest habitats on earth. J Comp Physiol A 190:765–789. doi:10.1007/s00359-004-0546-z
Warrant EJ, Nilsson D-E (1998) Absorption of white light in photoreceptors. Vis Res 38:195–207. doi:10.1016/S0042-6989(97)00151-X
Wilkie SE, Vissers PMAM, Das D, DeGrip WJ, Bowmaker JK, Hunt DM (1998) The molecular basis of UV vision in birds: spectral characteristics, cDNA sequence and retinal localization of the UV-sensitive visual pigment of the budgerigar (Melopsittacus undulatus). Biochem J 330:541–547
Wyndham E (1980) Diurnal cycle, behavior and social organization of the budgerigar Melopsittacus undulatus. Emu 80:25–33. doi:10.1071/MU9800025
Wyszecki G, Stiles WS (2000) Color science: concepts and methods, quantitative data and formulae, 2nd edn. Wiley, New York
Acknowledgments
We like to thank Björn Samuelsson for help with the experimental setup, and we are very grateful for the generous financial support given by the Royal Physiographic Society in Lund, the Swedish Research Council (621-2009-5683), the Knut and Alice Wallenberg Foundation, and the Royal Swedish Academy of Sciences. The experiments were approved by the Swedish Board of Agriculture (M68-11).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lind, O., Chavez, J. & Kelber, A. The contribution of single and double cones to spectral sensitivity in budgerigars during changing light conditions. J Comp Physiol A 200, 197–207 (2014). https://doi.org/10.1007/s00359-013-0878-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-013-0878-7