Skip to main content
Log in

Ionic and osmotic environment of developing elasmobranch embryos

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Synopsis

The elasmobranchs display a variety of ionic and osmotic environments for developing embryos. Oviparous species protect their eggs with a tough, fibrous capsule which is highly permeable to ions and urea even at oviposition. Thus the embryonic tissues are bathed by a solution ionically similar to sea water. In the more advanced reproductive style ofSqualus acanthias (a lecithotrophic live bearer) early embryos in egg capsules are retained in utero and bathed in a solution osmotically similar to maternal plasma. Several months into the 22 month gestation period the embryos can iono- and osmoregulate in a uterine solution resembling sea water. Embryos of more advanced viviparous species develop in a solution that is ionically and osmotically similar to maternal plasma. Iono- and osmoregulation by these embryos would appear to be unnecessary. Clearly, in the oviparous elasmobranchs, the ability of the embryo to regulate salts and urea is present at the earliest stage of development. The need for elasmobranch embryos to regulate osmolytes was reduced or delayed as viviparity evolved.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References cited

  • Boylan, J.W. 1967. Gill permeability in Squalus acanthias. pp. 197–206. In: P.W. Gilbert, R.F. Mathewson & D.P. Rall (ed.) Sharks, Skates and Rays, The Johnd Hopkins Press, Baltimore.

    Google Scholar 

  • Carrier, J.C. & D.H. Evans. 1972. Ion, water and urea turnover rates in the nurse shark,Ginglymostoma cirratum. Comp. Biochem. Physiol. 41A: 761–764.

    Google Scholar 

  • Chan, D.K.O. & J.G. Phillips. 1966. The embryology of the rectal gland of the spiny dogfishSqualus acanthias L. J. Anat. 100: 899–903.

    Google Scholar 

  • Compagno, L.J.V. 1990. Alternative life-history styles of cartilaginous fishes in time and space. Env. Biol. Fish. 28: 33–75.

    Google Scholar 

  • Evans, D.H. 1980. Osmotic and ionic regulation by freshwater and marine fishes. pp. 93–122. In: M.A. Ali (ed.) Environmental Physiology of Fishes, Plenum Publ. Corp., New York.

    Google Scholar 

  • Evans, D.H. 1981. The egg case of the oviparous elasmobranch, Raja erinacea, does osmoregulate. J. Exp. Biol. 92: 337–340.

    Google Scholar 

  • Evans, D.H., A. Oikari, G.A. Kormanik & L. Mansberger. 1982. Osmoregulation by the prenatal spiny dogfish, Squalus acanthias. J. Exp. Biol. 101: 295–305.

    Google Scholar 

  • Forster, R.P. 1967. Osmoregulatory role of the kidney in cartilaginous fishes (Chondrichthyes). pp 187–195. In: P.W. Gilbert, R.F. Mathewson & D.P. Rall (ed.) Sharks, Skates and Rays, The Johnd Hopkins Press, Baltimore.

    Google Scholar 

  • Forster, R.P & L. Goldstein.1969. Formation of excretory products. pp. 313–350. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology Vol. I, Academic Press, New York.

  • Foulley, M-M. & J. Mellinger. 1980. La diffusion de l"eau tritiée, de l"urée-14°C et d"autres substances à travers la coque de l"oeuf de Rousette, Scyliorhinus canicula. C.R. Acad. Sci. Paris. 290D: 427–430.

    Google Scholar 

  • Hamlett, W.C. 1989. Evolution and morphogenesis of the placenta in sharks. J. Exp. Zool. Suppl. 2: 35–52.

    Google Scholar 

  • Henderson, I.B., L.B. O"Toole & N. Hazon. 1988. Kidney function. pp. 201–214. In: T.J. Shuttleworth (ed.) Physiology of Elasmobranch Fishes, Springer-VErlag, Berlin.

    Google Scholar 

  • Hisaw, F.L. & A. Albert. 1947. Observations on the reproduction of the spiny dogfish, Squalus acanthias. Biol. Bull. 92: 187–199.

    Google Scholar 

  • Holmes, W.N. & E.M. Donaldson.1969. Body compartments and the distribution of electrolytes. pp. 1–89. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology Vol. I, Academic Press, New York.

  • Hornsey, D.J. 1978. Permeability coefficients of the eggcase membrane of Scyliorhinus canicula L. Experientia 34: 1596–1597.

    Google Scholar 

  • Hunt, S. 1985. The selection egg case collagen. pp. 409–434. In: A. Bairati & R. Garrone (ed.) Biology of Invertebrate and Lower Vertebrate Collagens, Plenum Press, New York.

    Google Scholar 

  • Knight, D.P. & S. Hunt. 1974. Fibril structure of collagen in the eggcase of dogfish. Nature 249: 379–380.

    Google Scholar 

  • Koob, T.J. & D.L. Cox. 1988. Egg capsule catechol oxidase from the little skate Raja erinacea Mitchell, 1825. Biol. Bull. 175: 202–211.

    Google Scholar 

  • Koob, T.J. & D.L. Cox. 1990. Introduction and oxidation of catechols during the formation of the skate (Raja erinacea) egg capsule. J. Mar. Biol. Ass. U.K. 70: 395–411.

    Google Scholar 

  • Kormanik, G.A. 1988. Time course of the establishment of uterine seawater conditions in late-term pregnant spiny dogfish (Squalus acanthias). J. Exp. Biol. 137: 443–456.

    Google Scholar 

  • Kormanik, G.A. 1989. The egg case of Raja erinacea plays only a minimal role as an ionic/osmotic barrier. Bull. Mt. Desert Isl. Biol. Lab. 28: 12–13.

    Google Scholar 

  • Kormanik, G.A. 1992. Ion and osmoregulation in prenatal elasmobranchs: evolutionary implications. Amer. Zool. 32: 294–302.

    Google Scholar 

  • Kormanik, G.A. & D.H. Evans. 1986. The acid-base status of prenatal pups of the dogfish, Squalus acanthias, in the uterine environment. J. Exp. Biol. 125: 173–179.

    Google Scholar 

  • Kormanik, G.A., A. Lofton & N. O"Leary-Liu. 1992. Egg case permeability to ammonia and urea in two species of skates (Raja sp.). Bull. Mt. Desert Isl. Biol. Lab. 31: 27–28.

    Google Scholar 

  • Kormanik, G.A., A.J. Lofton & D.E. Vibbard. 1991. The ontogeny of mitochondria-rich cells in embryos of the spiny dogfish, Squalus acanthias. Bull. Mt. Desert Isl. Biol. Lab. 30: 4–7.

    Google Scholar 

  • Krukenberg, C.F.W. 1888. La rétention de l"urée chez les selaciens. Ann. Mus. Hist. nat., Marseille 3.

  • Laurent, P. 1984. Gill internal morphology. pp.73–183. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology Vol. 10A, Academic Press, San Diego.

  • Mellinger, J., F. Wrisez & M.-J. Alluchon-Gérard. 1986. Developmental biology of an oviparous shark, Scyliorhinus canicula. pp. 310–332. In: T. Uyeno, R. Arai, T. Taniuchi & K. Matsuura (ed.) Proceedings, Second International Conference on Indo-Pacific Fishes, Ichthyological Soc. Japan, Tokyo.

    Google Scholar 

  • Needham, J.N. & D.M. Needham. 1930. Nitrogen excretion in selachian ontogeny. J. Exp. Biol. 7: 7–18.

    Google Scholar 

  • Payan, P., L. Goldstein & R.P. Forster. 1973. Gills and kidneys in ureosmotic regulation in euryhaline skates. Amer. J. Physiol. 224: 367–372.

    Google Scholar 

  • Price, Jr., K.S. & F.C. Daiber. 1967. Osmotic environments during fetal development of dogfish,Mustelus canis (Mitchill) andSqualus acanthias Linnaeus, and some comparisons with skates and rays. Physiol. Zool. 40: 248–260.

    Google Scholar 

  • Read, L.J. 1968. Urea and trimethylamine oxide levels in elasmobranch embryos. Biol. Bull. 135: 537–547.

    Google Scholar 

  • Shuttleworth, T.J. 1988. Salt and water balance. pp. 171–199. In: T.J. Shuttleworth (ed.) Physiology of Elasmobranch Fishes, Springer-Verlag, Berlin.

    Google Scholar 

  • Smith, H.W. 1936. The retention and physiological role of urea in the elasmobranchii. Biol. Rev. 11: 49–82.

    Google Scholar 

  • Thorson, T.B. & J.W. Gerst. 1972. Comparison of some parameters of serum and uterine fluid of pregnant, viviparous sharks (Carcharhinus leucas) and serum of their near-term young. Comp. Biochem. Physiol. 42A: 33–40.

    Google Scholar 

  • Von Bonde, C. 1945. Stages in the development of the picked or spiny dogfish, Squalus acanthias Linn. Biol. Bull. 88: 220–232.

    Google Scholar 

  • Witschi, E. 1956. Development of vertebrates. Saunders Co., Philadelphia. 588 pp.

    Google Scholar 

  • Wourms, J.P. 1977. Reproduction and development in chondrichthyan fishes. Amer. Zool. 17: 379–410.

    Google Scholar 

  • Wourms, J.P. 1981. Viviparity: the maternal fetal relationship in fishes. Amer. Zool. 21: 473–515.

    Google Scholar 

  • Wourms, J.P, B.D. Grove & J. Lombardi. 1988. The maternal-embryonic relationship in viviparous fishes. pp. 1–134. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, Vol. 11b, Academic Press, San Diego.

  • Wourms, J.P. & J. Lombardi. 1992. Reflections on the evolution of piscine viviparity. Amer. Zool. 32: 276–293.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kormanik, G.A. Ionic and osmotic environment of developing elasmobranch embryos. Environ Biol Fish 38, 233–240 (1993). https://doi.org/10.1007/BF00842919

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00842919

Key words

Navigation