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.
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.
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.
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.
Compagno, L.J.V. 1990. Alternative life-history styles of cartilaginous fishes in time and space. Env. Biol. Fish. 28: 33–75.
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.
Evans, D.H. 1981. The egg case of the oviparous elasmobranch, Raja erinacea, does osmoregulate. J. Exp. Biol. 92: 337–340.
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.
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.
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.
Hamlett, W.C. 1989. Evolution and morphogenesis of the placenta in sharks. J. Exp. Zool. Suppl. 2: 35–52.
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.
Hisaw, F.L. & A. Albert. 1947. Observations on the reproduction of the spiny dogfish, Squalus acanthias. Biol. Bull. 92: 187–199.
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.
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.
Knight, D.P. & S. Hunt. 1974. Fibril structure of collagen in the eggcase of dogfish. Nature 249: 379–380.
Koob, T.J. & D.L. Cox. 1988. Egg capsule catechol oxidase from the little skate Raja erinacea Mitchell, 1825. Biol. Bull. 175: 202–211.
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.
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.
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.
Kormanik, G.A. 1992. Ion and osmoregulation in prenatal elasmobranchs: evolutionary implications. Amer. Zool. 32: 294–302.
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.
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.
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.
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.
Needham, J.N. & D.M. Needham. 1930. Nitrogen excretion in selachian ontogeny. J. Exp. Biol. 7: 7–18.
Payan, P., L. Goldstein & R.P. Forster. 1973. Gills and kidneys in ureosmotic regulation in euryhaline skates. Amer. J. Physiol. 224: 367–372.
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.
Read, L.J. 1968. Urea and trimethylamine oxide levels in elasmobranch embryos. Biol. Bull. 135: 537–547.
Shuttleworth, T.J. 1988. Salt and water balance. pp. 171–199. In: T.J. Shuttleworth (ed.) Physiology of Elasmobranch Fishes, Springer-Verlag, Berlin.
Smith, H.W. 1936. The retention and physiological role of urea in the elasmobranchii. Biol. Rev. 11: 49–82.
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.
Von Bonde, C. 1945. Stages in the development of the picked or spiny dogfish, Squalus acanthias Linn. Biol. Bull. 88: 220–232.
Witschi, E. 1956. Development of vertebrates. Saunders Co., Philadelphia. 588 pp.
Wourms, J.P. 1977. Reproduction and development in chondrichthyan fishes. Amer. Zool. 17: 379–410.
Wourms, J.P. 1981. Viviparity: the maternal fetal relationship in fishes. Amer. Zool. 21: 473–515.
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.
Author information
Authors and Affiliations
Rights 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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00842919