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Coloration of corneas in fish. A list of species
0042-6989!86 $3.00 + 0.00 Copyright 8,’ 1986 Pergamon Press Ltd
Vision Res. Vol. 26, No. 2. pp. 287-290. 1986 Printed in Great Britain. All rights reserved
LETTER TO THE EDITORS COLORATION OF CORNEAS IN FISH. A LIST OF SPECIES (Received
28 March
1985; in revised ,form
24 July
1985)
oration was disregarded even by specialists in the eye morphology of fish but, none the less in some of the publications it was given due consideration (Niwa, 1979; van den Berg and Mooij, 1982; Cameron, 1982). Below we shall present a list of species with the aim to draw attention of investigators both to the choice of objects and to the interpretation of the results. Taxonomy is given after Lindberg (1971).
Yellow or orange coloration of the ocular media in fish has been reported by a great number of investigators. After the ability of the greenling Hexagrammos octogrammus to change cornea1 coloration depending on the illumination of the environment had been detected (Orlov et al., 1974) and a study had been made of structural bases and a mechanism of the phenomenon (Gamburtzeva and Orlov, 1976; Orlov and Gamburtzeva, 1976; Kondrashev and Orlov, 198 1; Kondrashev and Khodtsev, 1984), we searched for other fish possessing the same striking characteristic. It was found out that the greenling was not the only example since changeable coloration of the corneas had been described previously for many fish species (Gamburtzeva et al., 1979; Appleby and Muntz, 1979). In various investigations of the eye morphology, vision physiology and behaviour of fish from different taxonomic groups allowance must be made for the coloration of corneas, especially, in view of the fact that it is changeable. Until recently, the phenomenon of col-
(1) Changeable coloration of cornea Changeable coloration results from the presence in the cornea of specialized chromatophores the bodies of which are localized at the periphery (Fig. I) and single processes of the cells reach for the pupil zone. It is the reversible movement of pigments from the body to the process that is responsible for re-colouring of the cornea when illumination is altered. The cornea becomes yellow or orange in the light and colourless in the dark. For example, specimens of Hexagrammos octogrammus collected in their natural environment by day, or kept in an illu-
IO
IIa,
IIaz
.
0 ltght
Ib
continuously
(or ditksely)
at the designations peculiar distribution
II b ,
II b
Fig. I, Types of cornea colour filters. Type I-changeable;
lype II-constant.
all over the cornea: (b) pigment is distributed
(a) Pigment is distributed
in patches. Indices “I”
“a” and “b” show the presence in the cornea of one or two “pseudopupils” of pigment.
Corneas
and “2” due to
of right eyes are depicted, as seen from the outside view. The
rostra1 part of each cornea is on the right, the dorsal part at the top. 287
zxx
Letter
Table I. Fish
with
to the EdItor\ changeable
cornea1 coloratm
Blepsitdae
ORDER PERCIFORMES Family: Bathymasteridae
Biepsta.~ crrrhow~
Bath~masrer derjugou
Cyclopteridae Eunucrotremus pacifrcu~ cKh~pteru.s lunlpus
Stichaeidae Chirolophrs japonrcus Opisthocentrus dvhowskii. 0. ocellatus. 0. zonope Stichaeus no:a,c’ae. S. grigorjeci. S. punctatus Alectrias cirratu.r
ORDER TETRAODONTIFORMES Family: Balistidae Melichthvs cidua Hemibal&tes chrvsopterus Rhinecanthus aculeatus Rh. rectangulus Balistapus undulatus
Pholididae Pholis Jasciatus
ORDER SCORPAENIFORMES Family: Hexagrammidae
Hemitripterus cillosus
(4)
Tetraodontidae Frozen sample
Cottidae
Hemitripteridae
(4) (4) (2) (2)
Perragor melanocephalus Monocanthus mvlii. M. chinensis Osbeckia scripta
Neozoarces steindachneri
Myoxocephalus stelleri. hi. brandti, M. jaok, M. polyacanthocephalus. M. scorpius Argyrocottus zanderi Gymnocanthus galeatus. G. pistilliger Enophrys diceraus Cottus bubalis Bero elegans Alcichthys elongatus Hemilepidotus gilberti Paracottus kneri Batrachocottus baicalensis Cottus kessleri Procottus jeittelesi
(4)
Aluteridae
Zoarcidae
Hexagrammos stelleri. H. octogrammus. H. lagocephalus Pleurogrammus azonus
il.
(1)
Lythgoe. 1975
(3)
Fugu niphobles Sphaeroides lunaris Colomesus asellus Tetraodon nigroriridis. T. steindachneri T. cutcutia, T. .fahaka. T. ervthrotaenia. T. mbu. T. lemrus. T. miurus, T. palembangensis. T. pustulatus. T. schontedeni. 7. samphongsi Chonerinus naritus Canthigaster cinctus. C. ealentini Arothron hispidus. A. stellarus. A. meleagris, A. acrostaiicus. A. nrgropunctutus. A. imnutculatu.~. A. citrinellus Gastrophysis sceleratus
Appleby and Muntz, 1979
1. I. Sheremetjev. personal communication and also Lythgoe. 1975
(4) (2)
(4)
(2.4) (4)
Coloration of Type I a (see Fig. I) is characteristic of all species but Irish lord (Hemilepidotur gilberti) with cornea coloration of Type lb. In cases when no information is given as for the sampting IocaIity or the source of information the species presented was found by the authors in the Sea of Japan (Bay of Peter the Great). In the rest of the cases the species were caught in the White Sea-(l). Indian Ocean (Isle of Aldabra-Moreland, Lythgoe. 196X: Muntz. 1973~(2). Baikal Like-(3). South China Sea+4).
minated aquarium, have deep orange (or almost red) cornea. If a light-adapted fish is placed in the dark, its cornea gradually pales. becoming yellow and then colourless. We put on the list (Table I) also some species which had been earlier reported to have cornea1 coloration, but no indication had been given of its changeability (three species-Muntz, 1973; Cottus huhulis-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 species from the same genera and families.
(2) Constant coloration qf‘ cornea
Constant yellow and orange coloration of corneas in 44 species of fish families Amiidae. Esocidae, Percidae. Cyprinidae, Poecilidae, Cichlidae, Labridae and Scaridae has been mentioned in several pubhcations (Walls and Judd, 1933; Moreland and Lythgoe, 1968; Muntz, 1973, 1976; Lythgoe 1975). Additionally we made a list of fish species we had investigated in the reefs of the Nhatrang Bay (South China Sea) and in the Black Sea. All these species have yellow or yellow-orange cornea1 coloration of different complexity due to the presence of a
Letter to the Editors Table 2. Fish with constant cornea1 coloration
Familv. soecies
Type of coloration (see Fin. I)
Localitv
Scaridae Calotomus spinidens Callyodon sp. Scarus dubius ghobban fasciatus
Labridae Cheilinus arilobatus chlorurus Pseudocheilinus sp. Thalliurus chlorurus Hemigymnus melapterus ,fasciarus Thalassoma lunare Cheilio inermis Halichoeres notopteris Anampses meleagrides diadematus twistii caeruleopuncialus prerophthalmus
Ilb IIb IIb
IIaz IIa, IIaz IIa,
IIa IIa + IIb Ha,
1973; Appleby and Muntz, 1979; Shukolyukov and Tyurin. 1975: Kondrashev and Orlov. 198 I ; Cameron. 1982) led us to conclude that another singularity of light filters is the presence of carotenoids with the characteristic absorption maxima at 470-480, 446~450 and 425-430nm. In this case coloration density in the dorsal parts of many of the corneas is by l-l.5 log units higher than in the ventral regions. Some common properties of cornea1 colour filters permit the supposition that they perform similar functions. The filters are suggested to protect retina from too bright a light in shallow waters, eliminate the effect of lightscattering, reduce the chromatic aberration of eye optics and thus improve the acuity of vision. Up to now, however, the biological role of yellow eye filters has not been confirmed experimentally. Acknoic~edgemenr-The authors express their sincere thanks to Asalia A. Staviskaya for translating this paper into English.
IIa
REFERENCES
Ha,
Labridae Crenilabrus quinquemaculatus ocellarus griseus
289
IIb,
Sampling locality: I-South China Sea; 2-Black Sea. A wrasse Cheiho inermis has an “intermediate” coloration: ventral part of its cornea is coloured as Type IIa, but dorsal part as Type IIb. If the type of coloration is mentioned for genus but lacks for succeedingspecies names, it means that all the studied representatives of the genus have the cornea colour of the mentioned type.
pigment combined with chromatophores 1).
(Fig.
(3) Some common properiies of cornea1 jilters
Appleby S. J. and Muntz W. R. A. (1979) Occlusable yellow corneas in Tetraodontidae. J. erp. Biol. 83. 249-259. van den Berg T. J. T. P. and Mooij J. E. M. (1982) Eye media absorption in goldfish. Vision Res. 22. 1229-1231. Cameron N. E. (1982) The photopic spectral sensitivity of a dichromatic fish (Perca jhaiarilis). Vision Res. 22, 1341-1348. Gamburtzeva A. G.. Gnjubkina V. P.. Kondrashev S. L. and Orlov 0. Ju. (1979) Chromatophores and cornea1 coloration in fishes of the Sea of Japan. Mur. Biol. Vladirosrok 6, 445 I (in Russian). [Engl. Truns.-Ser. J. Mar.
Biol. 5, 4955503
(l979).]
Gamburtzeva A. G. and Orlov 0. Ju. (1976) Staining cells of the cornea in Hexagrammos octogrammus (Pisces: Hexagrammidae). Tvimlogia 18, 676-682 (in Russian). Kondrashev S. L. and Khodtsev A. S. (1984) Lightdependent and humoral control of pigment transport in cornea1 chromatophores in marine fishes. Zool. Jh. Ph~,siol. 88, 317-325.
In spite of a number of species specific characters and a considerable diversity of the morphological structure of cornea1 filters, one may single out only a few types of their organization (Fig. I). The distinguishing trait of various types of filters is the existence in the cornea1 rostra1 zone of an oval region devoid of pigmentation. It looks like a cornea1 “pseudopupil” and its meaning is still uncertain (Fig. I : types Ila, , Ila,, IIb, ). Comparison of the spectral absorbance of corneas measured by the authors for IO species of the Labridae and Tetraodontidae with the available literature data on the spectral properties of coloured corneas of other fishes (Muntz,
Kondrashev S. L. and Orlov 0. Ju. (1981) Physiological mechanisms and ecological role of changeable cornea1 coloration in marine fishes. In Ph~~.tiolog,r turd Biochemi.srrj, of Aduprutionr in Murinc Animals (Edited by Zhirmunsky A. V.). Proc. XIV Pacific Sci. Cong.. 3. pp. 154161. Far East Science Center. Vladivostok (in Russian). Lindberg G. U. (1971) Families of the lishes of the world. A check list and a key. Nuu!iu. f_eningrad (in Russian). Lythgoe J. N. (1975) The structure and function of iridescent corneas in teleost fishes. PUK. R. SW. Land.. B 188. 437 457. Moreland J. D. and Lythgoe J. N. (1968) Yellow corneas in fishes. Vltion Res. 8. I377 1380. Muntz W. R. A. (1973) Yellow filters and the absorption of light by the visual pigments of some Amasonian fishes. Vision Res. 12, 2235 ~2254.
Muntz W. R. A. (1976) Visual pigments of cichlid fishes from Malawi. Vision Rev. 16, X97 903.
290
Lctrer to the Ednor\
Niwa H. (1979) Scotopic ERG and photopic S-potential m
fish-compartson with behavioural data. Camp. Biochent. Phpiol. 64A, 58 I-584 Orlov 0. Ju. and Gamburtzeva A. G. (1976) Changeable coloration of COfnm in the fish ~~.~~~~u~7~7(7.~ ocfopmnmus. Nartm 263, 405406. Oriov 0. Ju.. Gamburtzeva A. G. and Alexandrova M. A. (1974) Coloured glasses of greenling. Prirodu 4, I I I - I I2 (in Russian). Shukolyukov S. A. and Tyurin V. A. (1975) Retinal pigments and carotenoids of the light-shading “spectacles” of the greenling Hexagrammos octopammus. J. &WI. Biochem. Phyiol. 11, 140-146 (in Russian). Walls G. L. and Judd H. D. (1933) The intraocular colour filters of vertebrates. Br. J. Qphlhal. 17, 641-675: 705-725.
Vision Res. Vol. 26, No. 2. pp. 287-290. 1986 Printed in Great Britain. All rights reserved
LETTER TO THE EDITORS COLORATION OF CORNEAS IN FISH. A LIST OF SPECIES (Received
28 March
1985; in revised ,form
24 July
1985)
oration was disregarded even by specialists in the eye morphology of fish but, none the less in some of the publications it was given due consideration (Niwa, 1979; van den Berg and Mooij, 1982; Cameron, 1982). Below we shall present a list of species with the aim to draw attention of investigators both to the choice of objects and to the interpretation of the results. Taxonomy is given after Lindberg (1971).
Yellow or orange coloration of the ocular media in fish has been reported by a great number of investigators. After the ability of the greenling Hexagrammos octogrammus to change cornea1 coloration depending on the illumination of the environment had been detected (Orlov et al., 1974) and a study had been made of structural bases and a mechanism of the phenomenon (Gamburtzeva and Orlov, 1976; Orlov and Gamburtzeva, 1976; Kondrashev and Orlov, 198 1; Kondrashev and Khodtsev, 1984), we searched for other fish possessing the same striking characteristic. It was found out that the greenling was not the only example since changeable coloration of the corneas had been described previously for many fish species (Gamburtzeva et al., 1979; Appleby and Muntz, 1979). In various investigations of the eye morphology, vision physiology and behaviour of fish from different taxonomic groups allowance must be made for the coloration of corneas, especially, in view of the fact that it is changeable. Until recently, the phenomenon of col-
(1) Changeable coloration of cornea Changeable coloration results from the presence in the cornea of specialized chromatophores the bodies of which are localized at the periphery (Fig. I) and single processes of the cells reach for the pupil zone. It is the reversible movement of pigments from the body to the process that is responsible for re-colouring of the cornea when illumination is altered. The cornea becomes yellow or orange in the light and colourless in the dark. For example, specimens of Hexagrammos octogrammus collected in their natural environment by day, or kept in an illu-
IO
IIa,
IIaz
.
0 ltght
Ib
continuously
(or ditksely)
at the designations peculiar distribution
II b ,
II b
Fig. I, Types of cornea colour filters. Type I-changeable;
lype II-constant.
all over the cornea: (b) pigment is distributed
(a) Pigment is distributed
in patches. Indices “I”
“a” and “b” show the presence in the cornea of one or two “pseudopupils” of pigment.
Corneas
and “2” due to
of right eyes are depicted, as seen from the outside view. The
rostra1 part of each cornea is on the right, the dorsal part at the top. 287
zxx
Letter
Table I. Fish
with
to the EdItor\ changeable
cornea1 coloratm
Blepsitdae
ORDER PERCIFORMES Family: Bathymasteridae
Biepsta.~ crrrhow~
Bath~masrer derjugou
Cyclopteridae Eunucrotremus pacifrcu~ cKh~pteru.s lunlpus
Stichaeidae Chirolophrs japonrcus Opisthocentrus dvhowskii. 0. ocellatus. 0. zonope Stichaeus no:a,c’ae. S. grigorjeci. S. punctatus Alectrias cirratu.r
ORDER TETRAODONTIFORMES Family: Balistidae Melichthvs cidua Hemibal&tes chrvsopterus Rhinecanthus aculeatus Rh. rectangulus Balistapus undulatus
Pholididae Pholis Jasciatus
ORDER SCORPAENIFORMES Family: Hexagrammidae
Hemitripterus cillosus
(4)
Tetraodontidae Frozen sample
Cottidae
Hemitripteridae
(4) (4) (2) (2)
Perragor melanocephalus Monocanthus mvlii. M. chinensis Osbeckia scripta
Neozoarces steindachneri
Myoxocephalus stelleri. hi. brandti, M. jaok, M. polyacanthocephalus. M. scorpius Argyrocottus zanderi Gymnocanthus galeatus. G. pistilliger Enophrys diceraus Cottus bubalis Bero elegans Alcichthys elongatus Hemilepidotus gilberti Paracottus kneri Batrachocottus baicalensis Cottus kessleri Procottus jeittelesi
(4)
Aluteridae
Zoarcidae
Hexagrammos stelleri. H. octogrammus. H. lagocephalus Pleurogrammus azonus
il.
(1)
Lythgoe. 1975
(3)
Fugu niphobles Sphaeroides lunaris Colomesus asellus Tetraodon nigroriridis. T. steindachneri T. cutcutia, T. .fahaka. T. ervthrotaenia. T. mbu. T. lemrus. T. miurus, T. palembangensis. T. pustulatus. T. schontedeni. 7. samphongsi Chonerinus naritus Canthigaster cinctus. C. ealentini Arothron hispidus. A. stellarus. A. meleagris, A. acrostaiicus. A. nrgropunctutus. A. imnutculatu.~. A. citrinellus Gastrophysis sceleratus
Appleby and Muntz, 1979
1. I. Sheremetjev. personal communication and also Lythgoe. 1975
(4) (2)
(4)
(2.4) (4)
Coloration of Type I a (see Fig. I) is characteristic of all species but Irish lord (Hemilepidotur gilberti) with cornea coloration of Type lb. In cases when no information is given as for the sampting IocaIity or the source of information the species presented was found by the authors in the Sea of Japan (Bay of Peter the Great). In the rest of the cases the species were caught in the White Sea-(l). Indian Ocean (Isle of Aldabra-Moreland, Lythgoe. 196X: Muntz. 1973~(2). Baikal Like-(3). South China Sea+4).
minated aquarium, have deep orange (or almost red) cornea. If a light-adapted fish is placed in the dark, its cornea gradually pales. becoming yellow and then colourless. We put on the list (Table I) also some species which had been earlier reported to have cornea1 coloration, but no indication had been given of its changeability (three species-Muntz, 1973; Cottus huhulis-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 species from the same genera and families.
(2) Constant coloration qf‘ cornea
Constant yellow and orange coloration of corneas in 44 species of fish families Amiidae. Esocidae, Percidae. Cyprinidae, Poecilidae, Cichlidae, Labridae and Scaridae has been mentioned in several pubhcations (Walls and Judd, 1933; Moreland and Lythgoe, 1968; Muntz, 1973, 1976; Lythgoe 1975). Additionally we made a list of fish species we had investigated in the reefs of the Nhatrang Bay (South China Sea) and in the Black Sea. All these species have yellow or yellow-orange cornea1 coloration of different complexity due to the presence of a
Letter to the Editors Table 2. Fish with constant cornea1 coloration
Familv. soecies
Type of coloration (see Fin. I)
Localitv
Scaridae Calotomus spinidens Callyodon sp. Scarus dubius ghobban fasciatus
Labridae Cheilinus arilobatus chlorurus Pseudocheilinus sp. Thalliurus chlorurus Hemigymnus melapterus ,fasciarus Thalassoma lunare Cheilio inermis Halichoeres notopteris Anampses meleagrides diadematus twistii caeruleopuncialus prerophthalmus
Ilb IIb IIb
IIaz IIa, IIaz IIa,
IIa IIa + IIb Ha,
1973; Appleby and Muntz, 1979; Shukolyukov and Tyurin. 1975: Kondrashev and Orlov. 198 I ; Cameron. 1982) led us to conclude that another singularity of light filters is the presence of carotenoids with the characteristic absorption maxima at 470-480, 446~450 and 425-430nm. In this case coloration density in the dorsal parts of many of the corneas is by l-l.5 log units higher than in the ventral regions. Some common properties of cornea1 colour filters permit the supposition that they perform similar functions. The filters are suggested to protect retina from too bright a light in shallow waters, eliminate the effect of lightscattering, reduce the chromatic aberration of eye optics and thus improve the acuity of vision. Up to now, however, the biological role of yellow eye filters has not been confirmed experimentally. Acknoic~edgemenr-The authors express their sincere thanks to Asalia A. Staviskaya for translating this paper into English.
IIa
REFERENCES
Ha,
Labridae Crenilabrus quinquemaculatus ocellarus griseus
289
IIb,
Sampling locality: I-South China Sea; 2-Black Sea. A wrasse Cheiho inermis has an “intermediate” coloration: ventral part of its cornea is coloured as Type IIa, but dorsal part as Type IIb. If the type of coloration is mentioned for genus but lacks for succeedingspecies names, it means that all the studied representatives of the genus have the cornea colour of the mentioned type.
pigment combined with chromatophores 1).
(Fig.
(3) Some common properiies of cornea1 jilters
Appleby S. J. and Muntz W. R. A. (1979) Occlusable yellow corneas in Tetraodontidae. J. erp. Biol. 83. 249-259. van den Berg T. J. T. P. and Mooij J. E. M. (1982) Eye media absorption in goldfish. Vision Res. 22. 1229-1231. Cameron N. E. (1982) The photopic spectral sensitivity of a dichromatic fish (Perca jhaiarilis). Vision Res. 22, 1341-1348. Gamburtzeva A. G.. Gnjubkina V. P.. Kondrashev S. L. and Orlov 0. Ju. (1979) Chromatophores and cornea1 coloration in fishes of the Sea of Japan. Mur. Biol. Vladirosrok 6, 445 I (in Russian). [Engl. Truns.-Ser. J. Mar.
Biol. 5, 4955503
(l979).]
Gamburtzeva A. G. and Orlov 0. Ju. (1976) Staining cells of the cornea in Hexagrammos octogrammus (Pisces: Hexagrammidae). Tvimlogia 18, 676-682 (in Russian). Kondrashev S. L. and Khodtsev A. S. (1984) Lightdependent and humoral control of pigment transport in cornea1 chromatophores in marine fishes. Zool. Jh. Ph~,siol. 88, 317-325.
In spite of a number of species specific characters and a considerable diversity of the morphological structure of cornea1 filters, one may single out only a few types of their organization (Fig. I). The distinguishing trait of various types of filters is the existence in the cornea1 rostra1 zone of an oval region devoid of pigmentation. It looks like a cornea1 “pseudopupil” and its meaning is still uncertain (Fig. I : types Ila, , Ila,, IIb, ). Comparison of the spectral absorbance of corneas measured by the authors for IO species of the Labridae and Tetraodontidae with the available literature data on the spectral properties of coloured corneas of other fishes (Muntz,
Kondrashev S. L. and Orlov 0. Ju. (1981) Physiological mechanisms and ecological role of changeable cornea1 coloration in marine fishes. In Ph~~.tiolog,r turd Biochemi.srrj, of Aduprutionr in Murinc Animals (Edited by Zhirmunsky A. V.). Proc. XIV Pacific Sci. Cong.. 3. pp. 154161. Far East Science Center. Vladivostok (in Russian). Lindberg G. U. (1971) Families of the lishes of the world. A check list and a key. Nuu!iu. f_eningrad (in Russian). Lythgoe J. N. (1975) The structure and function of iridescent corneas in teleost fishes. PUK. R. SW. Land.. B 188. 437 457. Moreland J. D. and Lythgoe J. N. (1968) Yellow corneas in fishes. Vltion Res. 8. I377 1380. Muntz W. R. A. (1973) Yellow filters and the absorption of light by the visual pigments of some Amasonian fishes. Vision Res. 12, 2235 ~2254.
Muntz W. R. A. (1976) Visual pigments of cichlid fishes from Malawi. Vision Rev. 16, X97 903.
290
Lctrer to the Ednor\
Niwa H. (1979) Scotopic ERG and photopic S-potential m
fish-compartson with behavioural data. Camp. Biochent. Phpiol. 64A, 58 I-584 Orlov 0. Ju. and Gamburtzeva A. G. (1976) Changeable coloration of COfnm in the fish ~~.~~~~u~7~7(7.~ ocfopmnmus. Nartm 263, 405406. Oriov 0. Ju.. Gamburtzeva A. G. and Alexandrova M. A. (1974) Coloured glasses of greenling. Prirodu 4, I I I - I I2 (in Russian). Shukolyukov S. A. and Tyurin V. A. (1975) Retinal pigments and carotenoids of the light-shading “spectacles” of the greenling Hexagrammos octopammus. J. &WI. Biochem. Phyiol. 11, 140-146 (in Russian). Walls G. L. and Judd H. D. (1933) The intraocular colour filters of vertebrates. Br. J. Qphlhal. 17, 641-675: 705-725.