Skip to main content
SpringerLink
Log in

Viviparity and the maternal-embryonic relationship in the coelacanth Latimeria chalumnae

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

Synopsis

Embryos of Latimeria chalumnae develop in well-vascularized compartments in the uterine region of the right oviduct. Compartments conform to the shape of their embryos and yolksacs; they represent a stable, gestation-induced oviductal modification. Late-term pups possess large, flaccid, vascular yolksacs almost devoid of yolk. The sac is in close contact with, but does not adhere to, the lumenal uterine surface. A massive vascular plexus occurs in the wall of the compartment at the site of contact with the yolksac; together they constitute a non-adherent, transposable placenta. The exterior surface of the yolksac is bounded by an attenuated, single-layered, squamous epithelium that surrounds an intercommunicating bed of cortical sinuses. The cortex of the sac is composed mostly of connective tissue stroma. The inner surface is bounded by a layer of yolk-digesting merocytes. Residual yolk occurs as yolk platelets that include yolk crystals. The interior surface of the sac is invested by an uniquely specialized vitelline circulation; no connection seems to exist between the interior of the yolksac and gut. The uterine wall consists of: (1) a lumenal surface composed of an anastomosing network of capillaries with a layer of attenuated, very thin, squamous epithelium, (2) a well-vascularized connective tissue stroma, (3) alternating transverse and longitudinal layers of smooth muscle, also well-vascularized, and (4) an external epithelial layer. Comparison of egg dry weight (184 g) with the estimated dry weights of a late-term pup (171 to 239 g) and a neonate (200 to 280 g) reveals a weight change of − 7 to + 30% and + 9 to + 52%, respectively. This is indicative of matrotrophy. In one female specimen, 19 remarkably large ovulated eggs were found and in another about 30 somewhat smaller ovarian ones. These are many more than ever could be accommodated in the uterine space. During the early and middle phases of development, embryos must be lecithotrophic, using their yolk reserves, with oophagy of fragmented supernumerary eggs as the most probable source of additional nutrients. The well-developed embryonic gut contains brown, amorphous yolk-like material. The limited amount of metachromatic secretory product of the uterine glands can play little or no role in embryonic nutrition.

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

Similar content being viewed by others

References cited

  • Amoroso, E.C. 1981. Viviparity, pp. 3–25. In: S.R. Glasser & D.W. Bullock(ed.) Cellular and Molecular Aspects of Implantation, Plenum Press, New York.

    Google Scholar 

  • Anthony, J. & J. Millot. 1972. Première capture d'une femelle de coelacanthe en état de maturité sexuelle. C.R. Acad. Sc. Paris Sér. D 274: 1925–1926.

    Google Scholar 

  • Anthony, J. & D. Robineau. 1976. Sur quelques caractères juvéniles de Latimeria chalumnae Smith (Pisces, Crossopterygii, Coelacanthidae). C.R. Acad. Sc. Paris Ser. D 283: 1739–1742.

    Google Scholar 

  • Atz, J.W. 1976. Latimeria babies are born, not hatched. Underwater Naturalist 9 (4): 4–7.

    Google Scholar 

  • Balon, E.K. 1984. Patterns in the evolution of reproductive styles in fishes. pp. 35–53. In: G.W. Potts & R.J. Wootton(ed.) Fish Reproduction: Strategies and Tactics, Academic Press, London.

    Google Scholar 

  • Balon, E.K. 1985. The theory of saltatory ontogeny and life history models revisited. pp. 13–30. In: E.K. Balon(ed.) Early Life History of Fishes: New Developmental, Ecological and Evolutionary Perspectives, Developments in Env. Biol. Fish. 5, Dr W. Junk Publishers, Dordrecht.

    Google Scholar 

  • Balon, E.K. 1986. Types of feeding in the ontogeny of fishes and the life-history model. Env. Biol. Fish. 16: 11–24.

    Google Scholar 

  • Balon, E.K. 1991. Probable evolution of the coelacanth's reproductive style: lecithotrophy and orally feeding embryos in cichlid fishes and in Latimeria chalumnae. Env. Biol. Fish. 32: 249–265. (this volume)

    Google Scholar 

  • Balon, E.K., M.N. Bruton & H. Fricke. 1988. A fiftieth anniversary reflection on the living coelacanth, Latimeria chalumnae: some new interpretations of its natural history and conservation status. Env. Biol. Fish. 23: 241–280.

    Google Scholar 

  • Bemis, W.E. & R.G. Northcutt. 1991. Innervation of the basicranial muscle of Latimeria chalumnae. Env. Biol. Fish. 32: 147–158. (this volume)

    Google Scholar 

  • Compagno, L.J.V. 1984. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. FAO Fish. Synop. No. 125 (4, Pt. 1) viii + 249.

  • Devys, M., A. Thierry, M. Barbier & M.M. Janot. 1972. Premières observations sur les lipides de l'ovocyte du coelacanthe (Latimeria chalumnae). C.R. Acad. Se. Paris Ser. D 275: 2085–2087.

    Google Scholar 

  • Fricke, H., O. Reinicke, H. Hofer & W. Nachtigall. 1987. Locomotion of the coelacanth Latimeria chalumnae in its natural environment. Nature 329: 331–333.

    Google Scholar 

  • Fritzsch, B. 1987. Inner ear of the coelacanth fish Latimeria has tetrapod affinities. Nature 327: 153–154.

    Google Scholar 

  • Gilbert, P.W. & D.A. Schlernitzauer. 1966. The placenta and gravid uterus of Carcharhinus falciformis. Copeia 1966: 451–457.

  • Grodziński, Z. 1972. The yolk of Latimeria chalumnae Smith. Folia histochem. cytochem. 10: 11–18.

    Google Scholar 

  • Hamlett, W.C., J.P. Wourms & J.W. Smith. 1985. Sting-ray placental analogue: structure of the trophonemata in Rhinoptera honasus. J. submicrosc. Cytol. 17: 31–40.

    Google Scholar 

  • Hensel, K. 1986. Morphologie et interprétation des canaux et canalicules sensoriels céphaliques de Latimeria chalumnae Smith, 1939 (Osteichthyes, Crossopterygii, Coelacanthiformes). Bull. Mus. natn. Hist. nat. Paris Ser. 4, 8: 379–407.

    Google Scholar 

  • Hoar, W.S. 1969. Reproduction. pp. 1–72. In: W.S. Hoar&D.J. Randall led.) Fish Physiology, Volume 3, Academic Press, New York.

  • Jollie, W.P. & L.G. Jollie. 1967. Electron microscopic observations on accommodations to pregnancy in the uterus of the spiny dogfish, Squalus acanthias. J. Ultrastruct. Res. 20: 161–178.

    Google Scholar 

  • Kessel, R.G. & R.H. Kardon. 1979. Tissues and organs. W.H. Freeman and Co., San Francisco. 317 pp.

    Google Scholar 

  • Knight, F.M., J. Lombardi, J.P. Wourms & J.R. Burns. 1985. Follicular placenta and embryonic growth of the viviparous four-eyed fish (Anableps). J. Morph. 185: 131–142.

    Google Scholar 

  • Lange, R.H. 1983. Les cristaux de lipovitelline-phosvitine dans l'ovocyte de Latimeria chalumnae Smith 1939 (Coelacanthidae, Pisces). Étude comparative. C.R. Acad. Se. Paris Ser. III 297: 393–396.

    Google Scholar 

  • Locket, N.A. 1976. A future for the coelacanth? New Scientist 70: 456–458.

    Google Scholar 

  • Locket, N.A. 1980. Some advances in coelacanth biology. Proc. R. Soc. Lond. B208: 265–307.

    Google Scholar 

  • McAllister, D.E. & C.L. Smith. 1978. Mensurations morphologiques, dénombrements méristiques et taxonomic du coelacanth, Latimeria chalumnae. Naturalists can. 105: 63–76.

    Google Scholar 

  • McCosker, J.E. & M.D. Lagios (ed.) 1979. The biology and physiology of the living coelacanth. Occ. Pap. Calif. Acad. Sci. 134. 175 pp.

  • Millot, J. & J. Anthony. 1974. Les oeufs du coelacanths. Science et Nature 121: 3–4 (+ color cover photograph).

    Google Scholar 

  • Millot, J., J. Anthony & D. Robineau. 1978. Anatomic de Latimeria chalumnae, Vol. 3, Appareil digestif, appareil respiratoire, appareil urogénital, glandes endocrines, appareil circulatoire, téguments, écailles, conclusions générales. C.N.R.S., Paris. 198 pp.

    Google Scholar 

  • Mossman, H.W. 1937. Comparative morphogenesis of the fetal membranes and accessory uterine structures. Contrib. Fmbryol. Carnegie Inst. 26: 129–246.

    Google Scholar 

  • Mossman, H.W. 1987. Vertebrate fetal membranes. Rutgers University Press, New Brunswick. 383 pp.

    Google Scholar 

  • Myking, L.M. 1977. Old four legs: the living fossil. Sea Frontiers 23: 334–341.

    Google Scholar 

  • Needham, J. 1942. Biochemistry and morphogenesis. Cambridge University Press, London. 785 pp.

    Google Scholar 

  • Ranzi, S. 1932. The physio-morphological basis of embryonic development in sharks. (Le basi fisio-morfologische dello sviluppo embrionale dei selaci.) Parti I. Pubbl. St. Zool. Napoli 13: 209–290. (In Italian).

    Google Scholar 

  • Ranzi, S. 1934. The physio-morphological basis of embryonic development in sharks. (Le basi fisio-morfologische dello sviluppo embrionale dei selaci.) Parti II, III. Pubbl. St. Zool. Napoli 13: 331–437. (In Italian).

    Google Scholar 

  • Schultze, H.-P. 1980. Eier legende und lebend gebärende Quastenflosser. Natur und Museum 110: 101–108. (English translation from the Department of Geology, Field Museum of Natural History, Chicago).

    Google Scholar 

  • Schultze, H.-P. 1985. Reproduction and spawning sites of Rhabdoderma (Pisces, Osteichthyes, Actinistia) in Pennsylvanian deposits of Illinois, USA. Neuvième Congr. Internat. Stratigr. Geol. Carbonifere, Washington, Compte Rendu 5: 326–330.

    Google Scholar 

  • Smith, C.L., C.S. Rand, B. Schaeffer & J.W. Atz. 1975. Latimeria, the living coelacanth, is ovoviviparous. Science 190: 1105–1106.

    Google Scholar 

  • Suyehiro, Y., T. Uyeno & N. Suzuki. 1982. Coelacanth: dissecting a living fossil. Newton graphic Science Magazine 2 (8): 82–93. (In Japanese).

    Google Scholar 

  • Suzuki, N., Y. Suvehiro & T. Hamada. 1985. Initial report of expeditions for coelacanth — Part I — Field studies in 1981 and 1983. Sci. Pap. Coll. Arts Sci. Univ. Tokyo 35: 37–79.

    Google Scholar 

  • Tanaka, S. 1989. Extant frilled sharks. Collecting and Breeding 51: 50, 61–63. (In Japanese).

    Google Scholar 

  • Watson, D.M.S. 1927. The reproduction of the coelacanth fish, Undina. Proc. Zool. Soc. Lond. 1927: 453–457.

    Google Scholar 

  • Wourms, J.P. 1977. Reproduction and development of 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. & A.B. Bodine. 1984. Structure and function of trophonemata, a placental analogue, during early gestation of the butterfly ray. p. 407. In: S. Seno & Y. Orada(ed.) International Cell Biology 1984, Academic Press, Orlando. (Abstract).

    Google Scholar 

  • Wourms, J.P. & D.M. Cohen. 1975. Trophotaeniae, embryonic adaptations in the viviparous ophidioid fish, Oligopus longhursti: a study of museum specimens. J. Morph. 147: 385–401.

    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, Volume 11B, Academic Press, San Diego.

    Google Scholar 

  • Wourms, J.P., M.D. Stribling & J.W. Atz. 1980. Maternal fetal nutrient relationships in the coelacanth, Latimeria. Amer. Zool. 20: 962. (Abstract).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Clemson University, Clemson, SC, 29634, U.S.A.

    John P. Wourms & M. Dean Stribling

  2. American Museum of Natural History, Department of Herpetology and Ichthyology, New York, NY, 10024, U.S.A.

    James W. Atz

Authors
  1. John P. Wourms
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James W. Atz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Dean Stribling
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wourms, J.P., Atz, J.W. & Stribling, M.D. Viviparity and the maternal-embryonic relationship in the coelacanth Latimeria chalumnae . Environ Biol Fish 32, 225–248 (1991). https://doi.org/10.1007/BF00007456

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00007456

Key words

Search

Navigation