Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Scotopic colour vision in nocturnal hawkmoths

Abstract

Humans are colour-blind at night, and it has been assumed that this is true of all animals. But colour vision is as useful for discriminating objects1 at night as it is during the day. Here we show, through behavioural experiments, that the nocturnal hawkmoth Deilephila elpenor uses colour vision to discriminate coloured stimuli at intensities corresponding to dim starlight (0.0001 cd m-2). It can do this even if the illumination colour changes, thereby showing colour constancy—a property of true colour vision systems2. In identical conditions humans are completely colour-blind. Our calculations show that the possession of three photoreceptor classes reduces the absolute sensitivity of the eye, which indicates that colour vision has a high ecological relevance in nocturnal moths. In addition, the photoreceptors of a single ommatidium absorb too few photons for reliable discrimination, indicating that spatial and/or temporal summation must occur for colour vision to be possible. Taken together, our results show that colour vision occurs at nocturnal intensities in a biologically relevant context.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Choice frequencies in tests after training to blue.
Figure 2: Choice frequencies in tests after training to yellow.
Figure 3: Colour constancy in D. elpenor.
Figure 4: Quantum catches of all D. elpenor photoreceptors in the two types of ommatidium (two ultraviolet and seven green receptors, two blue and seven green receptors) viewing six of the test colours (including the blue training colour) at the dimmest light intensity used (10-4 cd m-2).

Similar content being viewed by others

References

  1. Kelber, A., Vorobyev, M. & Osorio, D. Animal colour vision—behavioural tests and physiological concepts. Biol. Rev. (in the press)

  2. Neumeyer, C. Perceptual Constancy: Why Things Look as They Do (eds Walsh, V. & Kulikowski, J.) 323–351 (Cambridge Univ. Press, Cambridge, 1998)

    Google Scholar 

  3. Höglund, G., Hamdorf, K. & Rosner, G. Trichromatic visual system in an insect and its sensitivity control by blue light. J. Comp. Physiol. 86, 265–279 (1973)

    Article  Google Scholar 

  4. Schwemer, J. & Paulsen, R. Three visual pigments in Deilephila elpenor (Lepidoptera, Sphingidae). J. Comp. Physiol. 86, 215–229 (1973)

    Article  CAS  Google Scholar 

  5. Schlecht, P. Colour discrimination in dim light. An analysis of the photoreceptor arrangement in the moth Deilephila. J. Comp. Physiol. 129, 257–267 (1979)

    Article  CAS  Google Scholar 

  6. Pittaway, A. R. The Hawkmoths of the Western Palaearctic (Harley Books, Colchester, 1993)

    Google Scholar 

  7. Vogel, S. Blütenbiologische Typen als Elemente der Sippengliederung (G. Fischer, Jena, 1954)

    Google Scholar 

  8. White, R. H., Stevenson, R. D., Bennett, R. R., Cutler, D. E. & Haber, W. A. Wavelength discrimination and the role of ultraviolet vision in the feeding behaviour of hawkmoths. Biotropica 26, 427–435 (1994)

    Article  Google Scholar 

  9. Raguso, R. A. & Willis, M. A. Proceedings of the Third International Symposium on Butterfly Ecology and Evolution (eds Watt, W. B., Boggs, C. & Ehrlich, P. R.) (Univ. of Chicago Press, Chicago, in the press)

  10. Kelber, A. & Hénique, U. Trichromatic colour vision in the hummingbird hawkmoth, Macroglossum stellatarum. J. Comp. Physiol. A 184, 535–541 (1999)

    Article  Google Scholar 

  11. Knoll, F. Lichtsinn und Blütenbesuch des Falters von Deilephila livornica. Z. vergl. Physiol. 2, 328–380 (1926)

    Google Scholar 

  12. Frisch, K. von Der Farbensinn und Formensinn der Biene. Zool. Jb. Abt. Allg. Zool. Physiol. 35, 1–188 (1914)

    Google Scholar 

  13. Minnaert, M. G. J. Light and Color in the Outdoors (Springer, New York, 1993)

    Book  Google Scholar 

  14. Land, M. F. Handbook of Sensory Physiology (ed. Autrum, H.) Vol. VII/6B 471–592 (Springer, Berlin, 1981)

    Google Scholar 

  15. Rose, A. The relative sensitivities of television pickup tubes, photographic film and the human eye. Proc. Inst. Radio Eng. NY 30, 293–300 (1942)

    Google Scholar 

  16. De Vries, H. The quantum character of light and its bearing upon threshold of vision, the differential sensitivity and visual acuity of the eye. Physica 10, 553–564 (1943)

    Article  ADS  Google Scholar 

  17. Warrant, E., Porombka, T. & Kirchner, W. H. Neural image enhancement allows honeybees to see at night. Proc. R. Soc. Lond. B 263, 1521–1526 (1996)

    Article  ADS  Google Scholar 

  18. Warrant, E. J. Seeing better at night: life-style, eye design and the optimum strategy of spatial and temporal summation. Vision Res. 39, 1611–1630 (1999)

    Article  CAS  Google Scholar 

  19. Menzel, R. Achromatic vision in the honeybee at low light intensities. J. Comp. Physiol. A 141, 389–393 (1981)

    Article  Google Scholar 

  20. Powers, M. K. & Easter, S. S. Wavelength discrimination by the goldfish near absolute visual threshold. Vision Res. 18, 1149–1154 (1978)

    Article  CAS  Google Scholar 

  21. Welsch, B. Ultrastruktur und funktionelle Morphologie der Augen des Nachtfalters Deilephila elpenor (Lepidoptera, Sphingidae). Cytobiologie 14, 378–400 (1977)

    Google Scholar 

  22. Warrant, E. J. & Nilsson, D.-E. Absorption of white light in photoreceptors. Vision Res. 38, 195–207 (1998)

    Article  CAS  Google Scholar 

  23. Warrant, E. J. & McIntyre, P. D. Screening pigment, aperture and sensitivity in the dung beetle superposition eye. J. Comp. Physiol. A 167, 804–816 (1990)

    Google Scholar 

  24. Stavenga, D. G., Smits, R. P. & Hoenders, B. J. Simple exponential functions describing the absorbance bands of visual pigment spectra. Vision Res. 33, 1011–1017 (1993)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank D.-E. Nilsson for critically reading the manuscript; M. Pfaff for insights into hawkmoth behaviour; the human volunteers for participating in experiments; and everybody in the Vision Group for inspiration. We are grateful for the financial support of the Swedish Research Council.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Almut Kelber.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kelber, A., Balkenius, A. & Warrant, E. Scotopic colour vision in nocturnal hawkmoths. Nature 419, 922–925 (2002). https://doi.org/10.1038/nature01065

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01065

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing