Changeable Coloration of the Fish Eyes:
Corneal Spectacles

S.L. Kondrashev, O.Yu. Orlov

1. GENERAL

Yellow or orange coloration of the ocular media in fish has been reported by a great number of investigators. In some species the pattern of this coloration could be rather curious - see fig.1 (20K) and fig.2 (26K). The fish, masked greenling Hexagrammos octogrammus (see left picture), inhabiting boreal West Pacific shallow waters was the first in which the phenomenon of the changeable corneal coloration was discovered and investigated in many details (Orlov and Gamburtzeva, 1976). It was found that corneal coloration change reversibly follows the changes of the ambient illumination: from intensely colored in the bright light to colorless in the dark. The process of full de- and re-coloration lasts appr. 1-1.5 hours.

Since that time, we searched for other fish possessing the same striking characteristic during expeditions in the Sea of Japan, Okhotsk Sea, South China Sea, Black Sea, White Sea and Baikal Lake. Some specimens were collected by US colleagues in Friday Harbour and in freshwater streams in States of Oregon and NY. It was found that greenlings were not the only example and many representatives of the fish class are shown below in the LIST. We put on the list also some species which had been earlier reported to have corneal coloration, but no indication had been given of its changeability (Muntz, 1973; Lythgoe, 1975). We have no reason to doubt its rightfulness since the ability of the corneas to change coloration has been proved significantly for other fish from the same genera and families.

2. MORE MORPHOLOGY

Dark adapted cornea of Hexagrammos octogrammus

Changeable coloration results from the presence in the cornea of specialized chromatophores (corneal staining cells) the bodies of which are localized at the periphery and single processes of the cells reach for the pupil zone. As it is seen from the montage of the cornea images in the dark adaptated state at left, the number of cells in the dorsal part of the cornea is usually greater than in the ventral region. In big eyes and corneas this single cell process can reach up to 1 cm long - see fig.3 (56K). It is interesting to note, that such unusual chromatophores were, obviously, described for the first time in fish, Cottus bairdi, by G.L.Walls, but without touching their sophisticated light-shading functions. This classic of visual science compared the pattern of the “very long heavily pigmented” cell processes with an effect of “yellow waterfall” (Walls, Judd, 1933).

It is the reversible movement of carothenoid pigments in yellow or orange cells from the body to the process that is responsible for recoloring of the cornea when illumination is altered. Hundreds and thousands processes coming from the corneal margins (right picture) make a colored film. In most of species the coloration is uniform, but in one species - Irish lord, Hemilepidotus gilberti (Cottidae) it appears that in the light adapted state all the pigment from the body “leaks” into some lacunes at the tips of the cell processes, thus making a fascinating “patch”-pattern over the whole cornea - see fig.4 (99K), resembling a dotted pattern of a constant corneal coloration in Labrid fishes Crenilabrus sp. from the Black Sea (see fig.1).

3. DEVELOPMENT

4. LIST

of fishes with changeable corneal coloration

ACKNOWLEDGEMENTS

We give our sincere thanks to our colleagues, V.P.Gnyubkina, T.N.Manchenko, A.V.Levin, A.S.Sokolovskii, D.L.Pitruk and S.Sh.Dautov (all at the Institute of Marine Biology, Vladivostok) who helped much to catch fish, Prof. Neil Bourne (Nanaimo Bilogical Station, Canada) and Dr. R. Daniels (N.Y. State Education Department, Albany, NY, USA) who helped to get some of the fish specimens, Igor I. Sheremetjev (Kiev, Ukraine) who provided us with a valuable information about tropical aquarium fishes, and also to Dr. V.V.Maximov (IPIT RAS, Moscow) who stimulated us to use the advantages of the Internet.

5. REFERENCES

Appleby S.J., Muntz W.R.A, Occlusable yellow corneas in Tetraodontidae, J.Exp.Biol., 1979, v. 83, pp. 249-259.

Gamburtzeva A.G., Svitkina T.M., Tint I.S., Kondrashev S.L., Sakharov V.B., Pecularities of the chromatophore surface structure in the fish cornea with changeable coloration, Tsitologiya, 1993, v. 35, pp. 49-53 (in Russian).

Gnyubkina V.P., Kondrashev S.L. The development of specialized chromatophores and a changeable light filter in the cornea of the sculpin, Porocottus allisi. Russian Journal of Marine Biology, 2001, v. 27, N 1, pp. 31-35.

Kondrashev S.L., Gamburtzeva A.G., Gnyubkina V.P., Orlov O.Yu., Pham Thi My, Coloration of corneas in fish. A list of species, Vision Res., 1986,v. 26,pp. 287-290.

Lythgoe J.N., The structure and function of iridescent corneas in teleost fishes, Proc. Roy.Soc. London, 1975, B188, pp. 437-457.

Moreland J.D., Lythgoe J.N., Yellow corneas in fishes, Vision Res., 1968, v. 8, pp. 1377-1380.

Muntz W.R.A., Yellow filters and the absorption of light by the visual pigments of some Amazonian fishes, Vision. Res., 1973, v. 12, pp. 2235-2254.

Orlov O.Yu., Gamburtzeva A.G., Changeable coloration of cornea in the fish Hexagrammos octogrammus, Nature, 1976, vol. 263, pp. 405-406.

Walls G.L., Judd, H.D., The intraocular colour filters of vertebrates, Br. J. Ophthal., 1933, v. 17, pp. 641-675, 705-725.

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