Skip to main content
SpringerLink
Log in

Probable evolution of the coelacanth’s reproductive style: lecithotrophy and orally feeding embryos in cichlid fishes and in Latimeria chalumnae

  • Chapter
The biology of Latimeria chalumnae and evolution of coelacanths

Part of the book series: Developments in environmental biology of fishes ((DEBF,volume 12))

Abstract

The living coelacanth is a livebearer. Yolk seems to be the main source of nutrients and of oxygen to the embryo (fetus). Long before birth, young may also possibly feed orally on histotrophe secretion and egg debris. This type of reproduction evolved, as in most other fishes, from oviparity. The Carboniferous coelacanth Rhabdoderma exiguum had eggs of much lesser yolk volume and may represent an earlier form of oviparity with hiding, guarding or brooding type of parental care. The Jurassic coelacanth Holophagus (Undina) and the Cretaceous Axelrodichthys appear to have already evolved the internal-bearing style. Much of this evolutionary sequence is similar to that in cichlids. Ancestral cichlids are substrate tenders and nesters, with small eggs, little yolk and a feeding larva with indirect development. Mouthbrooding cichlids evolved a few, large eggs with denser yolk, direct development and, ultimately, orally feeding embryos while yolk is still in ample supply. Mixed feeding from yolk and orally ingested food in cichlids and in coelacanths is shown to be an enhanced mode of food delivery to the embryos over that from each source separately, in order to produce directly a better developed or larger young at the time of release, i.e. independence. Increase in egg size is regarded as an environmentally induced, altered pattern of yolk synthesis and an initial component of the epigenetic mechanism leading towards greater specialization. Carotenoids are incorporated within the yolk to assist the oxidative metabolism of the developing embryo.

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

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  • Anthony, J. & J. Millot. 1972. Première capture d’une femelle de coelacanthe en estat de maturité sexuelle. C.R. Acad. Sci. Paris, Ser. D 224: 1925–1927.

    Google Scholar 

  • Balon, E.K. 1960. Development of Cichlasoma nigrofasciatum (Guenther) during the embryo period of life. Věst. Čs. spol. zool. 24: 199–214. (In Slovak.)

    Google Scholar 

  • Balon, E.K. 1975a. Reproductive guilds of fishes: a proposal and definition. J. Fish. Res. Board Can. 32: 821–864.

    Article  Google Scholar 

  • Balon, E.K. 1975b. Terminology of intervals in fish development. J. Fish. Res. Board Can. 32: 1663–1670.

    Article  Google Scholar 

  • Balon, E.K. 1977. Early ontogeny of Labeotropheus Ahl, 1927 (Mbuna, Cichlidae, Lake Malawi), with a discussion on advanced protective styles in fish reproduction and development. Env. Biol. Fish. 2: 147–176.

    Article  Google Scholar 

  • Balon, E.K. 1978. Reproductive guilds and the ultimate structure of fish taxocenes: amended contribution to the discussion presented at the mini-symposium. Env. Biol. Fish. 3: 149–152.

    Article  Google Scholar 

  • Balon, E.K. 1980. Early ontogeny of the lake charr, Salvelinus (Cristivomer) namaycush. pp. 485–562. In: E.K. Balon (ed.) Charrs: Salmonid Fishes of the Genus Salvelinus, Dr W. Junk Publishers, The Hague.

    Google Scholar 

  • Balon, E.K. 1981a. About processes which cause the evolution of guilds and species. Env. Biol. Fish. 6: 129–138.

    Article  Google Scholar 

  • Balon, E.K. 1981b. Additions and amendments to the classification of reproductive styles in fishes. Env. Biol. Fish. 6: 377–389.

    Article  Google Scholar 

  • Balon, E.K. 1981c. Saltatory processes and altricial to precocial forms in the ontogeny of fishes. Amer. Zool. 21: 567–590.

    Google Scholar 

  • Balon, E.K. 1983. Epigenetic mechanisms: reflections on evolutionary processes. Can. J. Fish. Aquat. Sci. 40: 2045–2058.

    Article  Google Scholar 

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

    Google Scholar 

  • Balon, E.K. 1984b. Life histories of Arctic charrs: an epigenetic explanation of their invading ability and evolution. pp. 109–141. In: L. Johnson & B.L. Burns (ed.) Biology of the Arctic Charr, University of Manitoba Press, Winnipeg.

    Google Scholar 

  • Balon, E.K. 1985. Early life histories of fishes: new developmental, ecological and evolutionary perspectives. Developments in Env. Biol. Fish. 5, Dr W. Junk Publishers, Dordrecht. 280 pp.

    Google Scholar 

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

    Article  Google Scholar 

  • Balon, E.K. 1986b. Saltatory ontogeny and evolution. Rivista di Biologia/Biology Forum 79: 151–190.

    PubMed  CAS  Google Scholar 

  • Balon, E.K. 1988a. Tao of life: universality of dichotomy in biology. 1. The mystic awareness. Rivista di Biologia/Biology Forum 81: 185–231.

    Google Scholar 

  • Balon, E.K. 1988b. Tao of life: universality of dichotomy in biology. 2. The epigenetic mechanisms. Rivista di Biologia/ Biology Forum 81: 339–380.

    PubMed  CAS  Google Scholar 

  • Balon, E.K. 1989. The epigenetic mechanisms of bifurcation and alternative life-history styles. pp. 467–501. In: M.N. Bruton (ed.) Alternative Life-History Styles of Animals, Kluwer Academic Publishers, Dordrecht.

    Chapter  Google Scholar 

  • Balon, E.K. 1990a. The living coelacanth endangered: a personalized tale. Tropical Fish Hobbyist 39: 117–129.

    Google Scholar 

  • Balon, E.K. 1990b. Epigenesis of an epigeneticist: the development of some alternative concepts on the early ontogeny and evolution of fishes. Guelph Ichthyol. Rev. 1: 1–48.

    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.

    Article  Google Scholar 

  • Barlow, G.W. 1981. Patterns of parental investment, dispersal and size among coral-reef fishes. Env. Biol. Fish. 6: 65–85.

    Article  Google Scholar 

  • Baylis, J.R. 1981. The evolution of parental care in fishes, with reference to Darwin’s rule of male sexual selection. Env. Biol. Fish. 6: 223–251.

    Article  Google Scholar 

  • Blumer, L.S. 1979. Male parental care in the bony fishes. Quart. Rev. Biol. 54: 149–161.

    Article  Google Scholar 

  • Blumer, L.S. 1982. A bibliography and categorization of bony fishes exhibiting parental care. Zool. J. Linn. Soc. 76: 1–22.

    Article  Google Scholar 

  • Brichard, P. 1978. Fishes of Lake Tanganyika. T.F.H. Publications, Neptune City. 448 pp.

    Google Scholar 

  • Bruton, M.N. 1989a. The living coelacanth fifty years later. Trans. Roy. Soc. S. Afr. 47: 19–28.

    Article  Google Scholar 

  • Bruton, M.N. 1989b. The coelacanth-can we save it from extinction? WWF Reports (October-November): 10–12.

    Google Scholar 

  • Bruton, M. 1989c. Does the coelacanth occur in the Eastern Cape? The Naturalist (Port Elizabeth) 33: 5–13.

    Google Scholar 

  • Coates, D. 1988. Length-dependent changes in egg size and fecundity in females, and brooded embryo size in males of forktailed catfishes (Pisces: Ariidae) from the Sepik River, Papua New Guinea, with some implications for stock assessment. J. Fish Biol. 33: 455–464.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Coulter, G.W., B.R. Allanson, M.N. Bruton, P.H. Greenwood, R.C. Hart, P.B.N. Jackson & A.J. Ribbink. 1986. Unique qualities and special problems of the African Great Lakes. Env. Biol. Fish. 17: 161–183.

    Article  Google Scholar 

  • Courtenay-Latimer, M. 1988. Odd amusing bits of the coelacanth discovery. A retrospective in 1988. The Coelacanth, the Journal of the Border Historical Society 26(2): 19–24.

    Google Scholar 

  • Devys, M., S. Thierry, M. Barbier & M.M. Jonot. 1972. Premières observations du coelacanthe (Latimeria chalumnae). C.R. Acad. Sci. Paris 275(Ser. D): 2085–2087.

    CAS  Google Scholar 

  • Duellman, W.E. 1989. Alternative life-history styles in anuran amphibians: evolutionary and ecological implications. pp. 101–126. In: M.N. Bruton (ed.) Alternative Life-History Styles of Animals, Kluwer Academic Publishers, Dordrecht.

    Chapter  Google Scholar 

  • Duellman, W.E. & L. Trueb. 1986. Biology of amphibians. McGraw-Hill Book Company, New York. 670 pp.

    Google Scholar 

  • Flegler-Balon, C. 1989. Direct and indirect development in fishes-examples of alternative life-history styles. pp. 71–100. In: M.N. Bruton (ed.) Alternative Life-History Styles of Animals, Kluwer Academic Publishers, Dordrecht.

    Chapter  Google Scholar 

  • Forey, P.L. 1988. Golden jubilee for the coelacanth Latimeria chalumnae. Nature 336(6201): 727–732.

    Article  Google Scholar 

  • Fryer, G. & T.D. Iles. 1972. The cichlid fishes of the Great Lakes of Africa. T.F.H. Publications, Neptune City. 641 pp.

    Google Scholar 

  • Gorbman, A. 1983. Reproduction in cyclostome fishes and its regulation. pp. 1–29. In: W.S. Hoar, D.J. Randall & E.M. Donaldson (ed.) Fish Physiology, Vol. 9a, Academic Press, San Diego.

    Google Scholar 

  • Goto, A. 1980. Geographical distribution and variation of two types of Cottus nozawae in Hokkaido, and morphological characteristics of C. amblystomopsis from Sakhalin. Japan. J. Ichthyol. 27: 97–105.

    Google Scholar 

  • Goto, A. 1990. Alternative life-history styles of Japanese freshwater sculpins revisited. Env. Biol. Fish. 28: 101–112.

    Article  Google Scholar 

  • Greenwood, P.H. 1964. Explosive speciation in African lakes. Proc. R. Inst. G. Brit. 40: 256–269.

    Google Scholar 

  • Greenwood, P.H. 1981. The haplochromine fishes of the east African lakes. Kraus International Publications, Munich. 839 pp.

    Google Scholar 

  • Greenwood, P.H. 1988. A living fossil fish the coelacanth Latimeria chalumnae. British Museum (Natural History), London. 16 pp.

    Google Scholar 

  • Greenwood, P.H. 1989. Fifty years a ‘living fossil’ — the coelacanth fish Latimeria chalumnae. Biologist 36: 15–19.

    Google Scholar 

  • Griffith, R.W. & K.S. Thomson. 1973. Latimeria chalumnae: reproduction and conservation. Nature 242: 617–618.

    Article  PubMed  CAS  Google Scholar 

  • Heemstra, P.C. & L.J.V. Compagno. 1989. Uterine cannibalism and placental viviparity in the coelacanth? A skeptical view. S. Afr. J. Sci. 85: 485–486.

    Google Scholar 

  • Jayaram, K.C. 1978. Curious cat fishes of India. Zoologiana 1: 9–17.

    Google Scholar 

  • Karnaukhov, V.N. 1971. Carotenoids in oxidative metabolism of molluscoid neurons. Exp. Cell. Res. 64: 301–306.

    Article  PubMed  CAS  Google Scholar 

  • Karnaukhov, V.N. 1979. The role of filtrator molluscs rich in carotenoid in the self-cleaning of fresh waters. Symp. Biol. Hung. 19: 151–167.

    CAS  Google Scholar 

  • Karnaukhov, V.N. 1988. Biological functions of carotenoids. Nauka Press, Moscow. 241 pp. (In Russian).

    Google Scholar 

  • Kuwamura, T. 1986. Substratum spawning and biparental guarding of the Tanganyikan cichlid Boulengerochromis microlepis, with notes on its life history. Physiol. Ecol. Japan 23: 31–43.

    Google Scholar 

  • Kuwamura, T. 1988. Biparental mouthbrooding and guarding in a Tanganyikan cichlid Haplotaxodon microlepis. Japan. J. Ichthyol. 35: 62–68.

    Google Scholar 

  • Kuwamura, T. & N.K. Mihigo. 1988. Early ontogeny of a substrate-brooding cichlid, Boulengerochromis microlepis, compared with mouthbrooding species in Lake Tanganyika. Physiol. Ecol. Japan 25: 19–25.

    Google Scholar 

  • Kuwamura, T., M. Nagishi & T. Sato. 1989. Female-to-male shift of mouthbrooding in a cichlid fish, Tanganicodus irsacae, with notes on breeding habits of two related species in Lake Tanganyika. Env. Biol. Fish. 24: 187–198.

    Article  Google Scholar 

  • L0vtrup, S. 1982. The four theories of evolution. Rivista di Biologia 75: 53–66, 231-272, 385-409.

    PubMed  CAS  Google Scholar 

  • Løvtrup, S. 1987. Darwinism: the refutation of a myth. Croom Helm, London. 469 pp.

    Google Scholar 

  • Løvtrup, S. 1989. On divergent and progressive evolution. pp. 55–69. In: M.N. Bruton (ed.) Alternative Life-History Styles of Animals, Kluwer Academic Publishers, Dordrecht.

    Chapter  Google Scholar 

  • Lund, R. & W.L. Lund. 1985. Coelacanths from the Bear Gulch limestone (Namurian) of Montana and the evolution of the Coelacanthiformes. Bull. Carnegie Nat. Hist. 25: 1–74.

    Google Scholar 

  • Lund, W.L., R. Lund & G.A. Klein. 1985. Coelacanth feeding mechanisms and ecology of the Bear Gulch coelacanths. Compte Rendu Neuvième Congr. Internat. Stratigr. Geol. Carbonifère (Washington & Champaign-Urbana 1979) 5: 492–500.

    Google Scholar 

  • Maisey, J.G. 1986. Coelacanths from the Lower Cretaceous of Brazil. Amer. Mus. Novit. 2866: 1–30.

    Google Scholar 

  • Maisey, J.G. 1987. New fossil coelacanth named after Dr. Herbert R. Axelrod. Tropical Fish Hobbyist 36: 76–84.

    Google Scholar 

  • Marshall, N.B. 1953. Egg size in Arctic, Antarctic and deep-sea fishes. Evolution 7: 328–341.

    Article  Google Scholar 

  • Matsuda, R. 1987. Animal evolution in changing environments with special reference to abnormal metamorphosis. John Wiley & Sons, New York. 355 pp.

    Google Scholar 

  • Mikulin, A.Y. & S.G. Soin. 1975. The functional significance of carotenoids in the embryonic development of teleosts. J. of Ichthyol. 15: 749–759.

    Google Scholar 

  • Millot, J. & J. Anthony. 1960a. Le cloaque chez les coelacanthes. Bull. Mus. natn. Hist. nat. Paris 32: 287–289.

    Google Scholar 

  • Millot, J. & J. Anthony. 1960b. Appareil génital et reproduction des coelacanthes. C.r. Acad. Sci. Paris 251(Ser. D): 442–443.

    Google Scholar 

  • Millot, J. & J. Anthony. 1973a. L’appareil excréteur de Latimeria chalumnae Smith (Poisson, Coelacanthidé). Ann. Sci. nat. B 15: 293–328.

    Google Scholar 

  • Millot, J. & J. Anthony. 1973b. Variations sexuelles de l’appareil excréteur du coelacanthe, Latimeria chalumnae. Connexions avec l’appareil génital male. C.r. Acad. Sci. Paris 276(Ser. D): 2447–2448.

    Google Scholar 

  • Millot, J. & J. Anthony. 1974. Les oeufs du coelacanthe. Science et Nature 121: 3–4.

    Google Scholar 

  • Nice, M.M. 1962. Development of behavior in precocial birds. Trans. Linn. Soc. New York, Vol. 8. 211 pp.

    Google Scholar 

  • Noakes, D.L.G. & E.K. Balon. 1982. Life histories of tilapias: an evolutionary perspective. pp. 61–82. In: R.S.V. Pullin & R.H. Lowe-McConnell (ed.) The Biology and Culture of Tilapias, ICLARM Conf. Proc. 7, Manila.

    Google Scholar 

  • O’Connor, R.J. 1984. The growth and development of birds. John Wiley and Sons, Chichester. 326 pp.

    Google Scholar 

  • Peters, H.M. 1963. Eizahl, Eigewicht und Gelegeentwicklung in der Gattung Tilapia (Cichlidae, Teleostei). Int. Rev. ges. Hydrobiol. Hydrogr. 48: 547–576.

    Article  Google Scholar 

  • Poll, M. 1956. Poissons Cichlidae. Rés. sci. Explor. hydrobiol. lac Tanganika (1946–1947) 3(5b): 1–619.

    Google Scholar 

  • Ricklefs, R.E. 1979. Adaptation, constraint, and compromise in avian postnatal development. Biol. Rev. 54: 269–290.

    Article  PubMed  CAS  Google Scholar 

  • Ricklefs, R.E. 1983. Avian postnatal development. pp. 1–83. In: D.S. Farner, J.R. King & K.C. Parkes (ed.) Avian Biology, Vol. 7, Academic Press, New York.

    Chapter  Google Scholar 

  • Schultze, H-P. 1972. Early growth stages in coelacanth fishes. Nature New Biol. 236(64): 90–91.

    PubMed  CAS  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. Compte Rendu Neuvième Congr. Internat. Stratigr. Geol. Carbonifère (Washington & Champaign-Urbana 1979) 5: 326–330.

    Google Scholar 

  • Sharov, A.G. 1966. Basic arthropodan stock with special reference to insects. Pergamon Press, Oxford. 271 pp.

    Google Scholar 

  • Smirnov, A.I. 1950. The significance of carotenoid pigmentation in the embryonic-larval stages of cyprinid fishes (Pisces, Cyprinidae). Dokl. Acad. Sci. USSR 73: 609–612. (In Russian.)

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Smith, M.M. 1986. Latimeriidae. pp. 152–153. In: M.M. Smith & P.C. Heemstra (ed.) Smiths’ Sea Fishes, Macmillan, Johannesburg.

    Chapter  Google Scholar 

  • Soin, S.G. 1956. On the respiratory significance of carotenoid pigment in salmonid fish eggs and in other representatives of the order Clupeiformes. Zool. Zh. 35: 1362–1369. (In Russian.)

    Google Scholar 

  • Soin, S.G. 1962. Embryonic respiratory adaptations in fishes and their development in the Baikal sculpins (Cottoidei). Voprosy Ichtiologii 2: 127–139. (In Russian.)

    Google Scholar 

  • Soin, S.G. 1967. Ecomorphological data on the relationship of carotenoids with the embryonic respiration in fishes. pp. 340–350. In: Metabolism and Biochemistry of Fishes, Nauka Press, Moscow. (In Russian.)

    Google Scholar 

  • Stobbs, R. 1989a. The coelacanth enigma. The Phoenix, Magazine of the Albany Museum 2(2): 8–15.

    Google Scholar 

  • Stobbs, R.E. 1989b. Laxative lipids and the survival of the living coelacanth. S. Afr. J. Sci. 85: 557–558.

    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 

  • Suyehiro, Y., T. Hamada & N. Suzuki. 1983. Coelacanths, mystery of living fossil revealed. Newton (Graphic Science Magazine) 3(5): 78–93. (In Japanese.)

    Google Scholar 

  • Topp, R.W. & D.L. Girardin. 1971. An adult louvar, Luvarus imperialis (Pisces, Luvaridae), from the Gulf of Mexico. Copeia 1971: 181–182.

    Article  Google Scholar 

  • Watson, D.M.S. 1927. The reproduction of the coelacanth fish Undina. Proc. Zool. Soc. Lond. 1: 453–457.

    Google Scholar 

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

    Google Scholar 

  • Wourms, J.P. 1991. Reproduction and development of Sebastes in the context of the evolution of piscine viviparity. Env. Biol. Fish. 30: 111–126.

    Article  Google Scholar 

  • Wourms, J.P., J.W. Atz & M.D. Stribling. 1991. Viviparity and the maternal-embryonic relationship in the coelacanth Latimeria chalumnae. Env. Biol. Fish. 32: 225–248. (this volume)

    Article  Google Scholar 

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

    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.

    Google Scholar 

  • Yanagisawa, Y. & T. Sato. 1990. Active browsing by mouth-brooding females of Tropheus duboisi and Tropheus moorii (Cichlidae) to feed the young and/or themselves. Env. Biol. Fish. 27: 43–50.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Ichthyology, Department of Zoology, College of Biological Science, University of Guelph, Guelph, Ontario, N1G 2W1, Canada

    Eugene K. Balon

Authors
  1. Eugene K. Balon
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

John A. Musick Michael N. Bruton Eugene K. Balon

Rights and permissions

Reprints and permissions

Copyright information

© 1991 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Balon, E.K. (1991). Probable evolution of the coelacanth’s reproductive style: lecithotrophy and orally feeding embryos in cichlid fishes and in Latimeria chalumnae . In: Musick, J.A., Bruton, M.N., Balon, E.K. (eds) The biology of Latimeria chalumnae and evolution of coelacanths. Developments in environmental biology of fishes, vol 12. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-3194-0_16

Download citation

  • DOI: https://doi.org/10.1007/978-94-011-3194-0_16

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-0-7923-1289-5

  • Online ISBN: 978-94-011-3194-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation