Vision in the dimmest habitats on Earth

Abstract

A very large proportion of the world’s animal species are active in dim light, either under the cover of night or in the depths of the sea. The worlds they see can be dim and extended, with light reaching the eyes from all directions at once, or they can be composed of bright point sources, like the multitudes of stars seen in a clear night sky or the rare sparks of bioluminescence that are visible in the deep sea. The eye designs of nocturnal and deep-sea animals have evolved in response to these two very different types of habitats, being optimised for maximum sensitivity to extended scenes, or to point sources, or to both. After describing the many visual adaptations that have evolved across the animal kingdom for maximising sensitivity to extended and point-source scenes, I then use case studies from the recent literature to show how these adaptations have endowed nocturnal animals with excellent vision. Nocturnal animals can see colour and negotiate dimly illuminated obstacles during flight. They can also navigate using learned terrestrial landmarks, the constellations of stars or the dim pattern of polarised light formed around the moon. The conclusion from these studies is clear: nocturnal habitats are just as rich in visual details as diurnal habitats are, and nocturnal animals have evolved visual systems capable of exploiting them. The same is certainly true of deep-sea animals, as future research will no doubt reveal.

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Fig. 1a–c
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Fig. 7a–d
Fig. 8a, b
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Fig. 11a, b

Notes

  1. 1.

    As recently pointed out by Stavenga (2003), the Land sensitivity equation, despite its great usefulness, does have some limitations, especially for photoreceptors behaving as waveguides and for certain eye designs of lower F-number.

  2. 2.

    This integral is calculated between two wavelength limits: λ1 and λ2 (Warrant and Nilsson 1998). λ1 is set at 280 nm, the lowest wavelength likely to be seen by any animal (because the relative intensity of daylight below this wavelength is very low, and the internal structures of the eye absorb all wavelengths that are shorter). λ2 is the wavelength at which the spectral sensitivity R(λ) falls to 1% of its maximum at its long wavelength end. R(λ) is given by the rhodopsin template of Stavenga et al. (1993). In this template λ2 = 1.231 λmax, where λ max is the absorbance peak wavelength of the visual pigment.

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Acknowledgements

Much of the work presented in this review would not have been possible without the intelligence, generosity and friendship of so many students and colleagues with whom I have been privileged to collaborate, both in Lund and abroad. It is impossible to name them all, but in Lund it is equally impossible to omit naming seven: Marie Dacke, Almut Kelber, Dan-Eric Nilsson, and our past and present students Anna Balkenius, Rikard Frederiksen, Anna Gislén, and Birgit Greiner. With their laughter, genius and friendship, they have made the work outlined in this review a sheer pleasure to be involved in. I am also greatly indebted to the generosity of Professor Friedrich Barth and the Austrian Academy of Sciences who graciously invited me to deliver the Karl von Frisch Lecture upon which this review is based, and for promoting research undertaken on whole organisms. I am also very grateful to Mike Land and Doekele Stavenga for carefully reviewing the manuscript and suggesting many improvements. As always, I am very grateful to the many institutions that have supported our work over the years, including the Swedish Research Council, the Royal Physiographic Society of Lund, the Crafoord Foundation, the Wenner-Gren Foundation, the Swedish International Development Agency (SIDA) and the University of Lund. And finally, I wish to express my sincerest thanks to the man for whom this review is dedicated, Professor Rüdiger Wehner. Apart from his astonishing achievements in unravelling the secrets of polarised light navigation in animals—the scientific thrill from this alone is worth a standing ovation of thanks—Rüdiger Wehner has been an inexhaustible source of inspiration and support, not only for myself personally, but for the entire Vision Group in Lund. It is difficult to believe that such a youthful and vital man is nearing his retirement. I daresay it will pass as casually as any other date—the cataglyphid ants of the world have not divulged all of their secrets quite yet.

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Correspondence to Eric Warrant.

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Dedicated with gratitude to Professor Rüdiger Wehner, whose life and work has inspired a generation of organismic biologists

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Warrant, E. Vision in the dimmest habitats on Earth. J Comp Physiol A 190, 765–789 (2004). https://doi.org/10.1007/s00359-004-0546-z

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Keywords

  • Camera eye
  • Compound eye
  • Deep-sea vision
  • Nocturnal vision
  • Visual ecology