Hostname: page-component-7bb8b95d7b-2h6rp Total loading time: 0 Render date: 2024-09-13T14:04:24.516Z Has data issue: false hasContentIssue false
  • English
  • Français

Naturalistic color discriminations in polymorphic platyrrhine monkeys: Effects of stimulus luminance and duration examined with functional substitution

Published online by Cambridge University Press:  11 April 2007

MICKEY P. ROWE  and
GERALD H. JACOBS
MICKEY P. ROWE
Affiliation:
Neuroscience Research Institute, University of California, Santa Barbara, California
GERALD H. JACOBS
Affiliation:
Neuroscience Research Institute, University of California, Santa Barbara, California Department of Psychology, University of California, Santa Barbara, California
Get access Rights & Permissions [Opens in a new window]

Abstract

X-linked photopigment polymorphism produces six different color vision phenotypes in most species of New World monkey. In the subfamily Callitrichinae, the three M/L alleles underlying these different phenotypes are present at unequal frequencies suggesting that selective pressures other than heterozygous-advantage operate on these alleles. Earlier we investigated this hypothesis with functional substitution, a technique using a computer monitor to simulate colors as they would appear to humans with monkey visual pigments (Visual Neuroscience21:217–222, 2004). The stimuli were derived from measurements of ecologically relevant fruit and foliage. We found that discrimination performance depended on the relative spectral positioning of the substituted M and L pigment pair. Here we have undertaken a systematic examination of two simulation parameters—test field luminance and stimulus duration. Discriminability of the fruit colors depended on which phenotype was simulated but only at short stimulus durations and/or low luminances. Under such conditions, phenotypes with the larger pigment peak separations performed better. At longer durations and higher luminances, differences in performance across different substitutions tended to disappear. The stimuli used in this experiment were analyzed with several color discrimination models. There was limited agreement among the predictions made by these models regarding the capabilities of animals with different pigment pairs and none predicted the dependence of discrimination on changes in luminance and stimulus duration.

Keywords

New World monkeysOpsin genesColor visionCone pigmentsFruit discrimination
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 1 , January 2007 , pp. 17 - 23
Copyright
© 2007 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Caine, N.G., Surridge, A.K. & Mundy, N.I. (2003). Dichromatic and trichromatic Callithrix geoffroyi differ in relative foraging ability for red-green color-camouflaged and non-camouflaged food. International Journal of Primatology 24, 1163–1175.Google Scholar
Caine, N.G. & Mundy, N.I. (2000). Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proceedings of the Royal Society of London Series B-Biological Sciences 267, 439–444.Google Scholar
Carroll, J., Neitz, J. & Neitz, M. (2002). Estimates of L:M cone ratio from ERG flicker photometry and genetics. Journal of Vision 2, 531–542.Google Scholar
Chiao, C.C., Cronin, T.W. & Osorio, D. (2000). Color signals in natural scenes: characteristics of reflectance spectra and effects of natural illuminants. Journal of the Optical Society of America A-Optics Image Science and Vision 17, 218–224.Google Scholar
Chittka, L. & Briscoe, A. (2001). Why sensory ecology needs to become more evolutionary—inset color vision as a case in point. In Ecology of sensing, eds. Barth, F.G. & Schmid, A., pp. 19–37. Berlin: Springer.
Curcio, C.A., Allen, K.A., Sloan, K.R., Lerea, C.L., Hurley, J.B., Klock, I.B. & Milam, A.H. (1991). Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. Journal of Comparative Neurology 312, 610–624.Google Scholar
Dominy, N.J., Garber, P.A., Bicca-Marques, J.C. & de O.Azevedo-Lopes, M.A. (2003). Do female tamarins use visual cues to detect fruit rewards more successfully than do males? Animal Behaviour 66, 829–837.Google Scholar
Dominy, N.J. & Lucas, P.W. (2001). Ecological importance of trichromatic colour vision to primates. Nature 410, 363–365.Google Scholar
Dyer, A.G. & Neumeyer, C. (2005). Simultaneous and successive colour discrimination in the honeybee (Apis mellifera). Journal of Comparative Physiology A 191, 547–557.Google Scholar
Fain, G.L., Matthews, H.R., Cornwall, M.C. & Koutalos, Y. (2001). Adaptation in Vertebrate Photoreceptors. Physiological Reviews 81, 117–151.Google Scholar
Geisler, W.S. & Diehl, R.L. (2002). Bayesian natural selection and the evolution of perceptual systems. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 357(1420), 419–448.Google Scholar
Håstad, O., Victorsson, J. & Ödeen, A. (2005). Differences in colour vision make passerines less conspicuous in the eyes of their predators. Proceedings of the National Academy of Sciences of the USA 102, 6391–6394.Google Scholar
Jacobs, G.H. (1998). A perspective on color vision in platyrrhine monkeys. Vision Research 38, 3307–3313.Google Scholar
Jacobs, G.H., Neitz, J. & Crognale, M. (1987). Color vision polymorphism and its photopigment basis in a callitrichid monkey (Saguinus fuscicollis). Vision Research 27, 2089–2100.Google Scholar
Kelber, A., Vorobyev, M. & Osorio, D. (2003). Animal colour vision—behavioural tests and physiological concepts. Biological Reviews 78, 81–118.Google Scholar
Kuss, M., Jäkel, F. & Wichman, F.A. (2005). Bayesian inference for psychometric functions. Journal of Vision 5, 478–492. http://journalofvision.org/5/5/8/.Google Scholar
Leal, M. & Fleishman, L.J. (2004). Differences in visual signal design and detectability between allopatric populations of anolis lizards. American Naturalist 163, 26–39.Google Scholar
Lucas, P.W., Dominy, N.J., Riba-Hernandez, P., Stoner, K.E., Yamashita, N., Loría-Calderón, E., Petersen-Pereira, W., Rojas-Durán, Y., Salas-Pena, R., Solis-Madrigal, S., Osorio, D. & Darvell, B.W. (2003). Evolution and function of routine trichromatic vision in primates. Evolution 57, 2636–2643.Google Scholar
Lythgoe, J.N. & Partridge, J.C. (1989). Visual pigments and the acquisition of visual information. Journal of Experimental Biology 146, 1–20.Google Scholar
Lythgoe, J.N. & Partridge, J.C. (1991). The modeling of optimal visual pigments of dichromatic teleosts in green coastal waters. Vision Research 31, 361–371.Google Scholar
Marshall, N.J., Jennings, K., McFarland, W.N., Loew, E.R. & Losey, G.S. (2003). Visual biology of hawaiian coral reef fishes. III. Environmental light and an integrated approach to the ecology of reef fish vision. Copeia 2003, 467–480.Google Scholar
Mollon, J.D. (1989). “Tho' she kneel'd in that place where they grew…” the uses and origins of primate colour vision. Journal of Experimental Biology 146, 21–38.Google Scholar
Nagle, M.G. & Osorio, D. (1993). The tuning of human photopigments may minimize red-green chromatic signals in natural conditions. Proceedings of the Royal Society of London Series B-Biological Sciences 252, 209–213.Google Scholar
Neumeyer, C. (1981). Chromatic adaptation in the honeybee: successive color contrast and color constancy. Journal of Comparative Physiology 144, 543–553.Google Scholar
Osorio, D., Smith, A.C., Vorobyev, M. & Buchanan-Smith, H.M. (2004). Detection of fruit and the selection of primate visual pigments for color vision. American Naturalist 164, 696–708.Google Scholar
Osorio, D. & Vorobyev, M. (1996). Colour vision as an adaptation to frugivory in primates. Proceedings of the Royal Society of London Series B-Biological Sciences 263, 593–599.Google Scholar
Regan, B.C., Julliot, C., Simmen, B., Viénot, F., Charles-Dominique, P. & Mollon, J.D. (2001). Fruits, foliage and the evolution of primate colour vision. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 356, 229–283.Google Scholar
Riba-Hernandez, P., Stoner, K.E. & Lucas, P.W. (2005). Sugar concentration of fruits and their detection via color in the Central American spider monkey (Ateles geoffroyi). American Journal of Primatology 67, 411–423.Google Scholar
Rowe, M.P., Baube, C.L. & Phillips, J.B. (2006). Trying to see red through stickleback photoreceptors: Functional substitution of receptor sensitivities. Ethology 112, 218–229.Google Scholar
Rowe, M.P. & Jacobs, G.H. (2004). Cone pigment polymorphism in New World monkeys: Are all pigments created equal? Visual Neuroscience 21, 217–222.Google Scholar
Saito, A., Mikami, A., Kawamura, S., Ueno, Y., Hiramatsu, C., Widayati, K.A., Suryobroto, B., Teramoto, M., Mori, Y., Nagano, K., Fujita, K., Kuroshiima, H. & Hasegawa, T. (2005). Advantage of dichromats over trichromats in discrimination of color-camouflaged stimuli in nonhuman primates. American Journal of Primatology 67, 425–436.Google Scholar
Schiller, P.H., True, S.D. & Conway, J.L. (1980). Deficits in eye movements following frontal eye-field and superior colliculus ablations. Journal of Neurophysiology 44, 1175–1189.Google Scholar
Siddiqi, A., Cronin, T.W., Loew, E.R., Vorobyev, M. & Summers, K. (2004). Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio, Journal of Experimental Biology 207, 2471–2485.Google Scholar
Smith, A.C., Buchanan-Smith, H.M., Surridge, A.K., Osorio, D. & Mundy, N.I. (2003). The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinus spp.). Journal of Experimental Biology 206, 3159–3165.Google Scholar
Stoner, K.E., Riba-Hernandez, P. & Lucas, P.W. (2005). Comparative use of color vision for frugivory by sympatric species of primates. American Journal of Primatology 67, 399–409.Google Scholar
Stuart-Fox, D.M., Moussalli, A., Johnston, G.R. & Owens, I.P.F. (2004). Evolution of color variation in dragon lizards: Quantitative tests of the role of crypsis and local adaptation. Evolution 58, 1549–1559.Google Scholar
Sumner, P. & Mollon, J.D. (2000). Chromaticity as a signal of ripeness in fruits taken by primates. Journal of Experimental Biology 203, 1987–2000.Google Scholar
Sumner, P. & Mollon, J.D. (2003). Did primate trichromacy evolve for frugivory or folivory? In Normal and Defective Colour Vision, eds. Mollon, J.D., Pokorny, J. & Knoblauch, K., pp. 21–30. Oxford: Oxford University Press.
Vorobyev, M., Brandt, R., Peitsch, D., Laughlin, S.B. & Menzel, R. (2001). Colour thresholds and receptor noise: Behaviour and physiology compared. Vision Research 41, 639–653.Google Scholar
Vorobyev, M. & Osorio, D. (1998). Receptor noise as a determinant of colour thresholds. Proceedings of the Royal Society of London Series B-Biological Sciences 265, 351–358.Google Scholar
Wilder, H.D., Grunert, U., Lee, B.B. & Martin, P.R. (1996). Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus. Visual Neuroscience 13, 335–352.Google Scholar
Wyszecki, G. & Stiles, W.S. (1982). Color Science, Concepts and Methods, Quantitative Data and Formulae, 2nd Edition, New York: John Wiley & Sons, Inc.
Yamashita, N., Stoner, K.E., Riba-Hernández, P., Dominy, N.J. & Lucas, P.W. (2005). Light levels used during feeding by primate species with different color vision phenotypes. Behavioral Ecology and Sociobiology 58, 618–629.Google Scholar