Abstract
Otolithic membrane of utricles, saccules, and lagena of amphibians (Bufo bufo, Xenopus laevis, Rana temporaria) and reptiles (Teratoscincus scincus, Agama sanguinolenta, Ophisaurus apodus, Caiman crocodilus) were studied using light and scanning electron microscopy. Otolithic membrane in various otolithic organs in all studied animals was found to differ by shape, size, structure, and composition of otoconia. Otolithic membrane of utricle of amphibians and reptiles represents a thin plate of non-uniform structure. Otolithic apparatus in saccule represents a large cobble-stone-like conglomerate of otoconia. Otolithic membrane of lagena looks like a bent plate and is poorly differentiated in amphibians, but well differentiated in reptiles. Thus, transition of vertebrates to the earth surface was accompanied by a fundamental reorganization of otolithic membrane structure. Otolithic membrane containing constantly growing large otolith (in fish) was replaced by a thin structurally differentiated otolithic membrane that ceases its growth at early stages of ontogenesis. However, this replacement did not occur simultaneously in all otolithic organs. The changes initially involved otolithic membrane of utricle. Saccule of amphibians and reptiles has a typical compositional otolith. In the course of further phylogenetic development of tetrapods the process of structural differentiation of otolithic membrane was enhanced and otoliths were completely lost. In parallel, there proceeded a process of replacement of prismatic and spindle-shaped aragonitic otoconia by calcitic barrel-shaped otoconia. The data obtained confirm our hypothesis put forward earlier about two directions of evolution of otolithic membrane.
Similar content being viewed by others
REFERENCES
Lychakov, D.V., Evolution of Otolithic Membrane: the Structural Organization, Zh. Evol. Biokhim. Fiziol., 1988, vol. 24, pp. 250–261.
Lychakov, D.V., Evolution of Otolithic Membrane: the Functional Organization, Zh. Evol. Biokhim. Fiziol., 1988, vol. 24, pp. 262–268.
Lychakov, D.V., Comparative Study of Otoliths in Some Black Sea Fishes in Relation to Vestibular Function, Zh. Evol. Biokhim. Fiziol., 1990, vol. 26, pp. 550–556.
Lychakov, D.V., Study of Otolithic Membrane Structure in the Lamprey Lamperta fluviatilis in Relation to Evolution of Otoliths and Otoconia, Zh. Evol. Biokhim. Fiziol., 1995, vol. 31, pp. 175–185.
Lychakov, D.V., Study of Otolithic Apparatus of the Chondrostei Fry, Zh. Evol. Biokhim. Fiziol., 1995, vol. 31, pp. 328–336.
Fermin, C.D., Lychakov, D.V., Campos, A., Hara, H., Sondag, E., Jones, T., Jones, S., Taylor, M., Mesa-Ruiz, G., and Martin, D.S., Otoconia Biogenesis, Phylogeny, Composition and Functional Attributes, Histol. Histopathol., 1998, vol. 13, pp. 1103–1154.
Lychakov, D.V., Boyadzhieva-Mikhailova, A., Christov, I., and Evdokimov, I.I., Otolithic Apparatus in Black Sea Elasmobranchs, Fish. Res., 2000, vol. 1003, pp. 1–12.
Lychakov, D.V. and Rebane, Y.T., Otolith Regularities, Hear. Res., 2000, vol. 143, pp. 83–102.
Hudspeth, A. and Corey, D.P., Sensitivity, Polarity and Conductance Change in the Response of Vertebrate Hair Cells to Controlled Mechanical Stimuli, Proc. Natl Acad. Sci. USA, 1977, vol. 74, pp. 2407–2411.
Carlstrom, D., A Crystallographic Study of Vertebrate Otoliths, Biol. Bull., 1963, vol. 125, pp. 441–463.
Tretiakov, D.K., Sensory Organs of River Lamprey, Zap. Imperators. Novorossiis. Univ., 1917, vol. 8, pp. 1–644.
Lindeman, H.H., Anatomy of the Otolith Organs, Adv. Oto-Rhino-Laryng., 1973, vol. 20, pp. 405–433.
Lim, D.J., The Statoconia of the Non-Mammalian Species, Brain Behav. Evol., 1974, vol. 10, pp. 37–51.
Pote, K.G. and Ross, M.D., Each Otoconia Polymorph Has a Protein Unique to That Polymorph, Comp. Biochem. Physiol., 1991, vol. 98B, pp. 203–222.
Bulog, B., Tectorial Structures on the Inner Ear Sensory Epithelia of Proteus anguinus (Amphibia, Caudata), J. Morphol., 1989, vol. 201, pp. 59–68.
Steyger, P.S., Wiederhold, M.L., and Batten, J., The Morphogenetic Features of Otoconia during Larval Development of Cynops pyrrhogaster, the Japanese Red-Bellied Newt, Hear. Res., 1995, vol. 84, pp. 61–71.
Kido, T. and Takahashi, M., Scanning Electron Microscopic Study of Amphibians Otoconia, Auris Nasus Larynx, 1997, vol. 24, pp. 125–130.
Oukda, M., François, M., Membre, H., Bautz, A., and Dournon, C., Crystallographic and Chemical Composition of Otoconia in the Salamander Pleurodeles waltl, Hear. Res., 1999, vol. 132, pp. 85–93.
Lewis, E.E. and Li, C.W., Hair Cell Types and Distribution in the Otolithic and Auditory Organs of the Bullfrog, Brain Res., 1975, vol. 83, pp. 35–50.
Li, C.W. and Lewis, E.E., Structure and Development of Vestibular Hair Cells in the Larval Bullfrog, Ann. Otol. Rhinol. Laryngol., 1979, vol. 88, pp. 427–437.
Marmo, F., Balsamo, G., and Franco, E., Calcite in the Statoconia of Amphibians: a Detailed Analysis in the Frog Rana esculenta, Cell Tiss. Res., 1983, vol. 233, pp. 35–43.
Pote, K.G. and Ross, M.D., Utricular Otoconia of Some Amphibians Have Calcitic Morphology, Hear. Res., 1993, vol. 67, pp. 189–197.
Horn, E., Lang, U.-G., and Rayer, B., The Development of the Static Vestibuloocular Reflex in the Southern Clawed Toad, Xenopus laevis. I. Intact Animals, J. Comp. Physiol., 1986, vol. 159A, pp. 879–885.
Lim, D.J., Fine Morphology of the Otoconial Membrane and Its Relationship to the Sensory Epithelium, Scan. Electron Microsc., 1979, vol. 3, pp. 929–938.
Lim, D.J., Morphogenesis and Malformation of Otoconia: A Review, Birth Defects: Original Articles Series, 1980, vol. 16, no. 4, pp. 111–146.
Johnsson, L.G. and Hawkins, J.E., Otolithic Membranes of Saccule and Utricle in Man, Science, 1967, vol. 157, pp. 1454–1456.
Johnsson, L.G., Wright, C.G., Preston, R.E., and Henry, P.J., Defects of the Otoconial Membranes in Normal Guinea Pigs, Acta Otol., 1980, vol. 89, pp. 93–104.
Tikhomirova, L.I., Structural Organization and Orientation of Macula Hair Cells of Saccule of the Membranous Labyrinth of the Brown Frog, Arkh. Anat. Gistol. Embriol., 1984, vol. 87, no. 11, pp. 37–41.
Kido, T., Identification of Calcitic and Aragonitic Otoconia by Selective Staining Methods, Acta Histochem. Cytochem., 1996, vol. 29, pp. 121–127.
Deer, W.A., Howei, R.A., and Zussman, J., Porodoobrazuyushchie mineraly, tom 5, Nesilikatnye mineraly (Rock-Forming Minerals, vol. 5, Non-Silicate Minerals), Moscow, 1966.
Corwin, J.T., Perpetual Production of Hair Cells and Maturational Changes in Hair Cell Ultrastructure Accompany Postembryonic Growth in an Amphibian Ear, Proc. Natl. Acad. Sci. USA, 1985, vol. 82, pp. 3911–3915.
Lychakov, D.V., Structure of Surface of Otolithic Organs of Larva of the Clawed Frog Xenopus laevis, Zh. Evol. Biokhim. Fiziol., 1984, vol. 20, pp. 391–397.
Oukda, M., Bautz, A., Membre, H., Ghanbaja, J., François, M., and Dournon, C., Appearance and Evolution of Calcitic and Aragonitic during Pleurodeles waltl development, Hear. Res., 1999, vol. 137, pp. 114–126.
Ross, M.D. and Pote, K.G., Some Properties of Otoconia, Phil. Trans. R. Soc. Lond B., 1984, vol. 304, pp. 445–452.
Marmo, F., Franco, E., and Balsamo, G., Scanning Electron Microscopic and X-Ray Diffraction Studies of Otoconia in the Lizard Podarcis s. sicula, Cell Tiss. Res., 1981, vol. 218, pp. 265–232.
Lychakov, D.V., Otolithic Membrane. Structural and Functional Organization, Evolution, Ecomorphological Plasticity, and Resistance to Extreme Effects, Doctorate Sci. Diss., St. Petersburg, 2002.
Gauldie, R.W., Dunlop, D., and Tse, J., The Remarkable Lungfish Otolith, New Zealand J. Mar. Freshwater Res., 1986, vol. 20, pp. 81–92.
Berg, L.S., Trudy po teorii evolyutsii, 1922–1930 (Studies on the Theory of Evolution, 1922–1930), Leningrad, 1977.
Ahlberg, P.E. and Milner, A.R., The Origin and Early Diversification of Tetrapoda, Nature (Lond.), 1994, vol. 368, pp. 507–514.
Zhu, M. and Yu, X., A Primitive Fish Close to Common Ancestor of Tetrapods and Lungfish, Nature (Lond.), 2002, vol. 418, pp. 767–770.
Myging, S.H., Continued Studies on the Functional Mechanism of the Labyrinthine Sensory Epithelia, Acta Otol., 1969, Suppl. 249, pp. 1–32.
Tsyrul'nikov, E.M., On Functional Connections of Midbrain Auditory Area and of Saccule in the Frog Rana temporaria, Zh. Evol. Biokhim. Fiziol., 1977, vol. 13, pp. 486–490.
Baird, R.A. and Lewis, E.R., Correspondences between Afferent Innervation Patterns and Response Dynamics in the Bullfrog Utricle and Lagena, Brain Res., 1986, vol. 369, pp. 48–64.
Cortopassi, K.A. and Lewis, E.R., High-Frequency Tuning Properties of Bullfrog Lagenar Vestibular Afferent Fibers, J. Vestibul. Res., 1996, vol. 6, pp. 105–119.
Smotherman, M.S. and Narins, P.M., Hair Cells, Hearing and Hopping: A Field Guide to Hair Cell Physiology in the Frog, J. Exp. Biol., 2000, vol. 203, pp. 2237–2246.
Lewis, E.R. and Narins, P.M., Do Frogs Communicate with Seismic Signals?, Science, 1985, vol. 227, pp. 187–189.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lychakov, D.V. Evolution of Otolithic Membrane. Structure of Otolithic Membrane in Amphibians and Reptilians. Journal of Evolutionary Biochemistry and Physiology 40, 331–342 (2004). https://doi.org/10.1023/B:JOEY.0000042638.35785.f3
Issue Date:
DOI: https://doi.org/10.1023/B:JOEY.0000042638.35785.f3