From spectral information to animal colour vision: experiments and concepts

Many animals use the spectral distribution of light to guide behaviour, but whether they have colour vision has been debated for over a century. Our strong subjective experience of colour and the fact that human vision is the paradigm for colour science inevitably raises the question of how we compare with other species. This article outlines four grades of ‘colour vision’ that can be related to the behavioural uses of spectral information, and perhaps to the underlying mechanisms. In the first, even without an (image-forming) eye, simple organisms can compare photoreceptor signals to locate a desired light environment. At the next grade, chromatic mechanisms along with spatial vision guide innate preferences for objects such as food or mates; this is sometimes described as wavelength-specific behaviour. Here, we compare the capabilities of di- and trichromatic vision, and ask why some animals have more than three spectral types of receptors. Behaviours guided by innate preferences are then distinguished from a grade that allows learning, in part because the ability to learn an arbitrary colour is evidence for a neural representation of colour. The fourth grade concerns colour appearance rather than colour difference: for instance, the distinction between hue and saturation, and colour categorization. These higher-level phenomena are essential to human colour perception but poorly known in animals, and we suggest how they can be studied. Finally, we observe that awareness of colour and colour qualia cannot be easily tested in animals.

[1]  G. H. Jacobs Comparative Color Vision , 1981 .

[2]  T. Wachtler,et al.  Modeling color percepts of dichromats , 2004, Vision Research.

[3]  Doekele G Stavenga,et al.  Sexual Dimorphism of Short-Wavelength Photoreceptors in the Small White Butterfly, Pieris rapae crucivora , 2005, The Journal of Neuroscience.

[4]  Julia Poralla,et al.  Generalization and categorization of spectral colors in goldfish. II. Experiments with two and six training wavelengths , 2005, Journal of Comparative Physiology A.

[5]  R. Menzel Spectral Sensitivity and Color Vision in Invertebrates , 1979 .

[6]  T. S. Collett,et al.  Honeybees learn the colours of landmarks , 2004, Journal of Comparative Physiology A.

[7]  George Mather,et al.  Foundations of Perception , 2006 .

[8]  E. Schrödinger Grundlinien einer Theorie der Farbenmetrik im Tagessehen , 1920 .

[9]  J. Lubbock,et al.  Ants, bees, and wasps , 1889 .

[10]  Leo Maurice Hurvich,et al.  Color vision , 1981 .

[11]  G. H. Jacobs,et al.  Dichromacy in the Ground Squirrel , 1969, Nature.

[12]  Barbara Webb Transformation, encoding and representation , 2006, Current Biology.

[13]  E. Macagno,et al.  UV photoreceptors in the compound eye of Daphnia magna (Crustacea, Branchiopoda). A fourth spectral class in single ommatidia , 1990, Journal of Comparative Physiology A.

[14]  Petra Stoerig 7. Wavelength Information Processing versus Color Perception: Evidence from Blindsight and Color-Blind Sight , 1998 .

[15]  W. H. Miller,et al.  Comparative Physiology and Evolution of Vision in Invertebrates , 2011, Handbook of Sensory Physiology.

[16]  M. Sanders Handbook of Sensory Physiology , 1975 .

[17]  Gunther Wyszecki,et al.  Color Science: Concepts and Methods, Quantitative Data and Formulae, 2nd Edition , 2000 .

[18]  Martina Wicklein,et al.  Bees encode behaviorally significant spectral relationships in complex scenes to resolve stimulus ambiguity. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[19]  E. Maier,et al.  The spectral sensitivity of a passerine bird is highest in the UV , 1989, Naturwissenschaften.

[20]  A. Wallace The Colour Sense: its Origin and Development An Essay in Comparative Psychology , 1879, Nature.

[21]  D. Stavenga,et al.  Sexual dichroism and pigment localization in the wing scales of Pieris rapae butterflies , 2007, Proceedings of the Royal Society B: Biological Sciences.

[22]  Laurence T. Maloney,et al.  Photoreceptor spectral sensitivities and color correction , 1990, Electronic Imaging.

[23]  Almut Kelber,et al.  Nocturnal bees learn landmark colours in starlight , 2008, Current Biology.

[24]  A. Briscoe,et al.  A butterfly eye's view of birds , 2008, BioEssays : news and reviews in molecular, cellular and developmental biology.

[25]  Q. Zaidi,et al.  Limits of lightness identification for real objects under natural viewing conditions. , 2004, Journal of vision.

[26]  A. Kelber,et al.  Ovipositing butterflies use a red receptor to see green , 1999, The Journal of experimental biology.

[27]  M. Vorobyev,et al.  A review of the evolution of animal colour vision and visual communication signals , 2008, Vision Research.

[28]  Michael Kalloniatis,et al.  The Perception of Color , 2007 .

[29]  A. Hurlbert,et al.  Perception of three-dimensional shape influences colour perception through mutual illumination , 1999, Nature.

[30]  S. S. Stevens On the psychophysical law. , 1957, Psychological review.

[31]  C. Campenhausen Photoreceptors, lightness constancy and color vision , 1986, Naturwissenschaften.

[32]  R M Boynton,et al.  Vision: The Additivity Law Made To Work for Heterochromatic Photometry with Bipartite Fields , 1968, Science.

[33]  R. Traynier Associative learning in the ovipositional behaviour of the cabbage butterfly, Pieris rapae , 1984 .

[34]  Jules Davidoff,et al.  Language and perceptual categorisation , 2001, Trends in Cognitive Sciences.

[35]  P. Kay,et al.  Basic Color Terms: Their Universality and Evolution , 1973 .

[36]  A. Cowey,et al.  Blindsight in man and monkey. , 1997, Brain : a journal of neurology.

[37]  M. Lehrer,et al.  Spatial acuity of honeybee vision and its spectral properties , 2004, Journal of Comparative Physiology A.

[38]  A. Kelber Receptor based models for spontaneous colour choices in flies and butterflies , 2001 .

[39]  K. Voderberg Christian Konrad SPRENGEL (1750–1816):Das entdeckte Geheimnis der Natur im Bau und in der Befruchtung der Blumen 1793 , 1966 .

[40]  D. Osorio,et al.  Colour vision in the glow-worm Lampyris noctiluca (L.) (Coleoptera: Lampyridae): evidence for a green-blue chromatic mechanism , 2004, Journal of Experimental Biology.

[41]  M. Vorobyev,et al.  Tetrachromacy in a butterfly that has eight varieties of spectral receptors , 2008, Proceedings of the Royal Society B: Biological Sciences.

[42]  J. Lythgoe The Ecology of vision , 1979 .

[43]  M. Vorobyev,et al.  Discrimination of coloured patterns by honeybees through chromatic and achromatic cues , 2002, Journal of Comparative Physiology A.

[44]  K. Frisch Der Farbensinn und Formensinn der Biene , 1914 .

[45]  M. Schneider,et al.  Speciation through sensory drive in cichlid fish , 2008, Nature.

[46]  M. Vorobyev,et al.  Photoreceptor sectral sensitivities in terrestrial animals: adaptations for luminance and colour vision , 2005, Proceedings of the Royal Society B: Biological Sciences.

[47]  Lars Chittka,et al.  Is colour cognitive , 2011 .

[48]  T. Detto The fiddler crab Uca mjoebergi uses colour vision in mate choice , 2007, Proceedings of the Royal Society B: Biological Sciences.

[49]  Robert W. Kentridge,et al.  Cortical Color Blindness is Not “Blindsight for Color” , 1998, Consciousness and Cognition.

[50]  Barry B. Lee,et al.  Processing of Natural Temporal Stimuli by Macaque Retinal Ganglion Cells , 2002, The Journal of Neuroscience.

[51]  J. Boughman How sensory drive can promote speciation , 2002 .

[52]  R. Andrew,et al.  Short article: Sensory generalization and learning about novel colours by poultry chicks , 2009, Quarterly journal of experimental psychology.

[53]  The Phototactic Response and Spectral Sensitivity of Chroiviadorina Viridis (Nematoda, Chromadorida) With a Note On the Nature of the Paired Pigment Spots , 1966 .

[54]  S. Harnad Psychophysical and cognitive aspects of categorical perception: A critical overview , 1987 .

[55]  J. Endler Signals, Signal Conditions, and the Direction of Evolution , 1992, The American Naturalist.

[56]  Almut Kelber,et al.  Nocturnal colour vision – not as rare as we might think , 2006, Journal of Experimental Biology.

[57]  T. Ichikawa,et al.  Distribution of color receptors in the larval eyes of four species of lepidoptera , 2004, Journal of comparative physiology.

[58]  D. Foster,et al.  Relational colour constancy from invariant cone-excitation ratios , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[59]  I. Cuthill,et al.  Sexual Selection and the Mismeasure of Color , 1994, The American Naturalist.

[60]  Karl R Gegenfurtner,et al.  Color vision. , 2003, Annual review of neuroscience.

[61]  C. Bridges,et al.  Evolution of visual pigments , 1974 .

[62]  V. Wigglesworth Insects And The Life Of Man , 1964 .

[63]  T. Goldsmith,et al.  Color vision of the budgerigar (Melopsittacus undulatus): hue matches, tetrachromacy, and intensity discrimination , 2005, Journal of Comparative Physiology A.

[64]  H. Barlow What causes trichromacy? A theoretical analysis using comb-filtered spectra , 1982, Vision Research.

[65]  W. Stiles Colour Vision , 1957, Nature.

[66]  K. Frisch Christian Konrad Sprengels Blumentheorie vor 150 Jahren und heute , 1943, Naturwissenschaften.

[67]  C. von Campenhausen Photoreceptors, lightness constancy and color vision. , 1986, Die Naturwissenschaften.

[68]  David H Brainard,et al.  Perception of color and material properties in complex scenes. , 2004, Journal of vision.

[69]  F. Varela,et al.  Ways of coloring: Comparative color vision as a case study for cognitive science , 1992, Behavioral and Brain Sciences.

[70]  D. Osorio,et al.  Colour preferences and colour vision in poultry chicks , 2007, Proceedings of the Royal Society B: Biological Sciences.

[71]  R. Baddeley,et al.  Colour categorization by domestic chicks , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[72]  J. Kevin O'Regan,et al.  What it is like to see: A sensorimotor theory of perceptual experience , 2001, Synthese.

[73]  R. Wehner The Hymenopteran Skylight Compass: Matched Filtering and Parallel Coding , 1989 .

[74]  G. Jékely Evolution of phototaxis , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[75]  A A Wright,et al.  Color-naming functions for the pigeon. , 1971, Journal of the experimental analysis of behavior.

[76]  T. Nagel Mortal Questions: What is it like to be a bat? , 2012 .

[77]  A. Pickering,et al.  Cross-species differences in color categorization , 2006, Psychonomic bulletin & review.

[78]  J. Goyret,et al.  Why do Manduca sexta feed from white flowers? Innate and learnt colour preferences in a hawkmoth , 2008, Naturwissenschaften.

[79]  Julian C. Partridge,et al.  On the visual pigments of deep‐sea fish , 1997 .

[80]  A. Kelber,et al.  Colour perception in a dichromat , 2007, Journal of Experimental Biology.

[81]  T. Cronin,et al.  The unique visual world of mantis shrimps , 2004 .

[82]  Daniel Osorio,et al.  Colourful objects through animal eyes , 2001 .

[83]  Jun Xiao,et al.  Hue maps in primate striate cortex , 2007, NeuroImage.

[84]  H. Cronin,et al.  The ant and the peacock : altruism and sexual selection from Darwin to today , 1991 .

[85]  D. Ruderman,et al.  Statistics of cone responses to natural images: implications for visual coding , 1998 .

[86]  Dan-Eric Nilsson,et al.  The evolution of eyes and visually guided behaviour , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[87]  M. Vorobyev,et al.  Receptor noise as a determinant of colour thresholds , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[88]  M. Vorobyev Coloured oil droplets enhance colour discrimination , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[89]  Tom Troscianko,et al.  On the role of blue shadows in the visual behaviour of tsetse flies , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[90]  G. D. Bernard,et al.  Positive selection of a duplicated UV-sensitive visual pigment coincides with wing pigment evolution in Heliconius butterflies , 2010, Proceedings of the National Academy of Sciences.

[91]  C. Scherer,et al.  The influence of color stimuli on visually controlled behavior inAglais urticae L. andPararge aegeria L. (Lepidoptera) , 1987, Journal of Comparative Physiology A.

[92]  T. Guilford,et al.  Receiver psychology and the evolution of animal signals , 1991, Animal Behaviour.

[93]  V. Maximov,et al.  Environmental factors which may have led to the appearance of colour vision. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[94]  J. Mollon John Elliot MD (1747–1787) , 1987, Nature.

[95]  S. Vogel Christian Konrad Sprengel’s Theory of the Flower: The Cradle of Floral Ecology , 1996 .

[96]  J. Spudich,et al.  Mechanism of colour discrimination by a bacterial sensory rhodopsin , 1984, Nature.

[97]  R. Menzel,et al.  Colour preferences of flower-naive honeybees , 1995, Journal of Comparative Physiology A.

[98]  R. Baddeley,et al.  Generalization of Color by Chickens: Experimental Observations and a Bayesian Model , 2007, The American Naturalist.

[99]  L. Maloney Evaluation of linear models of surface spectral reflectance with small numbers of parameters. , 1986, Journal of the Optical Society of America. A, Optics and image science.

[100]  J. Lubbock On the Senses, Instincts, and Intelligence of Animals, with Special Reference to Insects . (The International Scientific Series, No. LXIV.) By Sir John Lubbock. New York, Appleton. 8° , 1888, Science.

[101]  R. M. Evans The Perception of Color , 1974 .

[102]  M. Vorobyev,et al.  Animal colour vision — behavioural tests and physiological concepts , 2003, Biological reviews of the Cambridge Philosophical Society.

[103]  Á. Miklósi,et al.  Visual Ecology and Perception of Coloration Patterns by Domestic Chicks , 1999, Evolutionary Ecology.

[104]  R. Prokopy,et al.  Visual Detection of Plants by Herbivorous Insects , 1983 .

[105]  N. Justin Marshall,et al.  Stomatopod photoreceptor spectral tuning as an adaptation for colour constancy in water , 1997, Vision Research.