Skip to main content
SpringerLink
Log in

The Spectral Sensitivity of Photoreceptors and the Screening Function of the Cornea of Greenlings (Hexagrammidae)

  • ORIGINAL ARTICLES
  • Published:
Russian Journal of Marine Biology Aims and scope Submit manuscript

Abstract—

Corneas in different species of the greenling family Hexagrammidae can change coloration depending on the level of ambient illumination. This process is based on redistribution of carotenoid pigments in specialized chromatophores. The spectral properties of corneas and the absorbance spectra of the visual pigments in the retinal photoreceptors were measured in four species and in one inter-species hybrid of greenlings. The modifying effect of the colored corneal filters on the cone absorbance was evaluated. A positive correlation was found between the degree of the long-wave sensitivity of cones and the maximal optical density of the cornea at the same wavelengths. Comparison of the literature data on the spectral properties of photoreceptors and peculiarities of the cornea organization with the daily, seasonal, and other behavioral activities of greenlings allowed us to confirm the earlier proposal of an important light-protective role of the changeable cornea in greenlings.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Balanov, A.A., Markevich, A.I., Antonenko, D.V., and Crow, K.D., The first occurrence of hybrids of Hexagrammos otakii H. octogrammus and description of H. otakii (Hexagrammidae) from Peter the Great Bay (the Sea of Japan), J. Ichthyol., 2001, vol. 41, no. 9, pp. 728–738.

    Google Scholar 

  2. Gamburtseva, A.G., Gnyubkina, V.P., Kondrashev, S.L., and Orlov, O.Yu., Chromatography and coloration of cornea of fishes of the Sea of Japan, Sov. J. Mar. Biol., 1979, vol. 5, no. 6, pp. 495–503.

    Google Scholar 

  3. Gnyubkin, V.F., Response of pigmented corneas of whitespotted greenling to changes in light, Sov. J. Mar. Biol., 1989, vol. 15, no. 1, pp. 21–28.

    Google Scholar 

  4. Govardovskii, V.I. and Zueva, L.V., Simple highly sensitive recording spectrophotometer, Tsitologiya, 1988, vol. 30, no. 4, pp. 499–502.

    CAS  Google Scholar 

  5. Gomelyuk, V.E., The spawning behavior of the Okhotsk atka mackerel Pleurogrammus azonus in Peter the Great Bay, Vopr. Ikhtiol., 1987, vol. 27, no. 6, pp. 991–999.

    Google Scholar 

  6. Gomelyuk, V.E., Comparative analysis of everyday behavior and mode of life of three species of Hexagrammos (Hexagrammidae, Scorpaeniformes) in summer, J. Ichthyol., 2000, vol. 40, no. 1, pp. 74–85.

    Google Scholar 

  7. Gomelyuk, V.E., Gamburtseva, A.G., and Sakharov, V.B., Dynamics of changeable light filters of the cornea of the masked greenling Hexagrammos octogrammus during the day in natural habitat, Vopr. Ikhtiol., 1989, vol. 29, no. 3, pp. 483–488.

    Google Scholar 

  8. Erlov, N.G., Marine Optics, Amsterdam: Elsevier, 1976.

    Google Scholar 

  9. Kondrashev, S.L., Spectral sensitivity and visual pigments of retinal photoreceptors in near-shore fishes of the Sea of Japan, Russ. J. Mar. Biol., 2010, vol. 36, no. 6, pp. 443–451.

    Article  CAS  Google Scholar 

  10. Kondrashev, S.L. and Orlov, O.Yu., Physiological mechanisms and the ecological value of the variable color of the eye cornea in marine fish, in Fiziologiya i biokhimiya adaptatsii morskikh zhivotnykh (Physiology and Biochemistry of Adaptations of Marine Animals), Vladivostok: Dal’nevost. Otd., Akad. Nauk SSSR, 1981, pp. 154–160.

  11. Markevich, A.I., The daily distribution and population density of some fish in the coastal zone of Peter the Great Bay, Biologiya shel’fovykh i prokhodnykh ryb (Biology of Shelf and Migratory Fish), Vladivostok: Dal’nevost. Otd., Akad. Nauk SSSR, 1990, p. 16–19.

    Google Scholar 

  12. Markevich, A.I., Parental behavior of the male greenlings Hexagrammos otakii and H. octogrammus (Hexagrammidae), J. Ichthyol., 2004, vol. 44, no. 7, pp. 521–526.

    Google Scholar 

  13. Orlov, O.Yu., Colored glasses of animals, Priroda, 1974, no. 8, pp. 35–41.

  14. Orlov, O.Yu., The visual system of greenlings, in Mekhanizmy zreniya zhivotnykh (Mechanisms of Vision of Animals), Moscow: Nauka, 1978, pp. 180–199.

  15. Orlov, O.Yu. and Gamburtseva, A.G., Dynamics of coloration of the cornea in greenlings, Biofizika, 1976, vol. 21, no. 2, pp. 362–365.

    PubMed  Google Scholar 

  16. Rutenberg, E.P., Review of fish of the greenling family Hexagrammidae, in Tr. Inst. Okeanol. Akad. Nauk SSSR im. P.P. Shirshova “Terpugovye ryby i vozmozhnosti ikh mezhokeanskoi transplantatsii” (Trans. Shirshov Inst. Oceanol., Acad. Sci. USSR “Greenlings and the Possibility of Their Interocean Transplantation”), Moscow: Akad. Nauk SSSR, 1962, vol. 59, pp. 3–100.

  17. Fam, T.M. and Kondrashev, S.L., The structure and function of the light filters of the cornea of coral reef fish, in Biologiya pribrezhnykh vod V’etnama. Donnye bespozvonochnye yuzhnogo V’etnama (Biology of the Coastal Waters of Vietnam, Bottom Invertebrates of Southern Vietnam), Vladivostok: Dal’nevost. Otd., Akad. Nauk SSSR, 1989, pp. 100–106.

  18. Bridges, C.D.B., The rhodopsin-porphyropsin visual system, in Handbook of Sensory Physiology, Berlin: Springer-Verlag, 1972, vol. 7/1, pp. 417−480.

  19. Collin, S.P., Specialisations of the teleost visual system: adaptive diversity from shallow-water to deep-sea, Acta Physiol. Scand., 1997, vol. 161, suppl. 638, pp. 5−24.

    Google Scholar 

  20. Cortesi, F., Musilova, Z., Stieb, S.M., et al., Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes, Proc. Natl. Acad. Sci. U. S. A., 2015, vol. 112, pp. 1493−1498.

    Article  CAS  PubMed  Google Scholar 

  21. Douglas, R.H. and Marshall, N.J., A review of vertebrate and invertebrate ocular filters, in Adaptive Mechanisms in the Ecology of Vision, Netherlands: Kluwer Acad. Publ., 1999, pp. 95−162.

    Google Scholar 

  22. Douglas, R.H. and McGuigan, C.M., The spectral transmission of freshwater teleost ocular media − an interspecific comparison and a guide to potential ultraviolet sensitivity, Vision Res., 1989, vol. 29, pp. 871−879.

    Article  CAS  PubMed  Google Scholar 

  23. Gomelyuk, V.E. and Leunov, V.P., Changes in age-specific behavior and spatial structure of masked greenling, Hexagrammos octogrammus (Hexagrammidae), Environ. Biol. Fishes, 1999, vol. 54, no. 3, pp. 313−323.

    Article  Google Scholar 

  24. Govardovskii, V.I., Fyhrquist, N., Reuter, T., et al., In search of the visual pigment template, Visual Neurosci., 2000, vol. 17, no. 4, pp. 509−528.

    Article  CAS  Google Scholar 

  25. Hasegawa, E.I., Changes in rhodopsin-porphyropsin ratio of chum and pink salmon, Fish. Sci., 2005, vol. 71, pp. 1091−1097.

    Article  CAS  Google Scholar 

  26. Heinermann, P.H., Yellow intraocular filters in fishes, Exp. Biol., 1984, vol. 43, pp. 127−147.

    CAS  PubMed  Google Scholar 

  27. Isayama, T. and Makino, C.L., Pigment mixtures and other determinants of spectral sensitivity of vertebrate retinal photoreceptors, in Photoreceptors: Physiology, Types and Abnormalities, Hauppauge, N.Y.: Nova Science Publishers, 2012, pp. 1−13.

    Google Scholar 

  28. Iwanicki, T.W., Novales Flamarique, I., Ausió, J., et al., Fine tuning light sensitivity in the starry flounder (Platichthys stellatus) retina: regional variation in photoreceptor cell morphology and opsin gene expression, J. Comp. Neurol., 2017, vol. 525, pp. 2328–2342.

    Article  CAS  PubMed  Google Scholar 

  29. Jokela-Määttä, M., Smura, T., Aaltonen, A., et al., Visual pigments of Baltic Sea fishes of marine and limnic origin, Visual Neurosci., 2007, vol. 24, pp. 389−398.

  30. Kondrashev, S.L., Long-wave sensitivity in the masked greenling (Hexagrammos octogrammus), a shallow-water marine fish, Vision Res., 2008, vol. 48, pp. 2269–2274.

    Article  PubMed  Google Scholar 

  31. Kondrashev, S.L., Gamburtzeva, A.G., Gnjubkina, V.P., et al., Coloration of corneas in fish: a list of species, Vision Res., 1986, vol. 26, pp. 287−290.

    Article  CAS  PubMed  Google Scholar 

  32. Kondrashev, S.L. and Gnyubkin, V.F., The effect of temperature on the light-induced pigment movement in fish corneal chromatophores, Pigm. Cell Res., 1999, vol. 12, pp. 193−198.

    Article  CAS  Google Scholar 

  33. Kondrashev, S.L. and Lamash, N.E., Two ways of A1/A2-visual pigments conversion during light/dark adaptation in fish, Abstr. Eur. Retina Meeting 2017 (ERM 2017), October 5−7, 2017, Paris, p. 225.

  34. Kondrashev, S.L. and Orlov, O.Yu., Changeable Coloration of the Fish Eyes: Corneal Spectacles, 2006. http://cool.iitp.ru/projects/posters/cornea.

  35. Losey, G.S., McFarland, W.N., Loew, E.R., et al., Visual biology of Hawaiian coral reef fishes. I. Ocular transmission and visual pigments, Copeia, 2003, no. 3, pp. 433−454.

  36. Miyazaki, T., Kondrashev, S.L., and Tsuchiya, T., Visual pigment genes and absorbance spectra in the Japanese sardine Sardinops melanostictus (Teleostei: Clupeiformes), Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2018, vol. 218, pp. 54–63.

    Article  CAS  Google Scholar 

  37. Orlov, O.Y. and Gamburtzeva, A.G., Changeable coloration of cornea in the fish Hexagrammos octogrammus, Nature, 1976, vol. 263, pp. 405−406.

    Article  CAS  PubMed  Google Scholar 

  38. Orlov, O.Yu. and Kondrashev, S.L., Changeable coloration of cornea in fishes and its distribution, Iugosl. Physiol. Pharmacol. Acta, 1998, vol. 34, pp. 359−369.

    Google Scholar 

  39. Sabbah, S., Troje, N.F., Gray, S.M., and Hawryshyn, C.W., High complexity of aquatic irradiance may have driven the evolution of four-dimensional colour vision in shallow-water fish, J. Exp. Biol., 2013, vol. 216, pp. 1670−1682.

    Article  PubMed  Google Scholar 

  40. Siebeck, U.E. and Marshall, N.J., Transmission of ocular media in labrid fishes, Philos. Trans. R. Soc. London, B, 2000, vol. 355, pp. 1257−1261.

    Article  CAS  Google Scholar 

  41. Siebeck, U.E. and Marshall, N.J., Ocular media transmission of coral reef fish − can coral reef fish see ultraviolet light?, Vision Res., 2001, vol. 41, pp. 133−149.

    Article  CAS  PubMed  Google Scholar 

  42. Siebeck, U.E., Collin, S.P., Ghoddusi, M., and Marshall, N.J., Occlusable corneas in toadfishes: light transmission, movement and ultrastructure of pigment during light- and dark-adaptation, J. Exp. Biol., 2003, vol. 206, pp. 2177−2190.

    Article  PubMed  Google Scholar 

  43. Temple, S.E., Why different regions of the retina have different spectral sensitivities: A review of mechanisms and functional significance of intraretinal variability in spectral sensitivity in vertebrates, Visual Neurosci., 2011, vol. 28, pp. 281−293.

    Article  CAS  Google Scholar 

  44. Walls, G.L. and Judd, H.D., The intraocular colour-filters of vertebrates, Br. J. Ophthalmol., 1933, vol. 17, pp. 641−675, 705−725.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Yokoyama, S., Molecular evolution of vertebrate visual pigments, Prog. Retinal Eye Res., 2000, vol. 19, pp. 385–419.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zhirmunsky Institute of Marine Biology, National Scientific Center of Marine Biology, Far East Branch, Russian Academy of Sciences, 690041, Vladivostok, Russia

    S. L. Kondrashev

Authors
  1. S. L. Kondrashev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. L. Kondrashev.

Additional information

Translated by I. Barsegova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kondrashev, S.L. The Spectral Sensitivity of Photoreceptors and the Screening Function of the Cornea of Greenlings (Hexagrammidae). Russ J Mar Biol 45, 22–30 (2019). https://doi.org/10.1134/S1063074019010036

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1063074019010036

Keywords:

Search

Navigation