Skip to main content
Log in

Early ontogeny of Adinia xenica (Pisces, Cyprinodontiformes): 3. Comparison and evolutionary significance of some patterns in epigenesis of egg-scattering, hiding and bearing cyprinodontiforms

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

Synopsis

Developmental patterns as seen in cyprinodontiforms fishes with different reproductive styles are compared, and discussed in relation to ecology and evolutionary significance. The discussion centres around Adinia xenica (its detailed ontogeny presented in two previous sequels to this paper), and, from the existing literature, Fundulus heteroclitus (closely related), Austrofundulus myersi (an annual) and Platypoecilus maculatus (a livebearer). The embryonic resting interval is present in various forms in the first three species, and differences in it and the overall patterns of development are shown to be consistent with ecological conditions. Termination of the resting interval leads immediately to hatching, a process in A. xenica, as in F. heteroclitus, apparently initiated by the appropriate summation of internal and external factors. These factors include any or all of: metabolic changes and increased oxygen requirements, response to light, reduced environmental oxygen, agitation, and increased hydrostatic pressure. They all can cause increased movement by the embryo which is credited with rupturing hatching gland cells and releasing the enzyme(s). Annual fishes experience 3 pronounced resting intervals, termed diapauses. These are discussed in the context of apparent steps and thresholds, and evolutionary ecology. A possible evolutionary sequence, from a simple fractional spawning pattern to diapause, is presented. Morphological differences in primary embryonic respiratory surfaces, as seen in the four species, are related to environmental conditions. The above illustrate ways in which the same basic structures and events are modified to cope with different habitats.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Similar content being viewed by others

References cited

  • Able, K.W. 1984. Variation in spawning site selection of the mummichog, Fundulus heteroclitus. Copeia 1984: 522–525.

    Article  Google Scholar 

  • Alberch, P. 1980. Ontogenesis and morphological diversification. Amer. Zool. 20: 653–667.

    Article  Google Scholar 

  • Alderdice, D.F., W.P. Wickett & J.R. Brett. 1958. Some effects of temporary exposure to low dissolved oxygen levels on Pacific salmon eggs. J. Fish. Res. Board Can. 15: 229–249.

    Article  CAS  Google Scholar 

  • Alderdice, D.F. & C.R. Forrester. 1968. Some effects of salinity and temperature on early development and survival of the English sole (Parophrys vetulus). J. Fish. Res. Board Can. 25: 495–521.

    Article  Google Scholar 

  • Amberson, W.R. & P.B. Armstrong 1933. The respiratory metabolism of Fundulus heteroclitus during embryonic development. J. Cell. Comp. Physiol. 2: 381–397.

    Article  CAS  Google Scholar 

  • Armstrong, P.B. 1936. Mechanism of hatching in Fundulus heteroclitus. Biol. Bull. 71: 407.

    Google Scholar 

  • Armstrong, P.B. & J.S. Child. 1965. Stages in the normal development of Fundulus heteroclitus. Biol. Bull. 128: 143–168.

    Article  Google Scholar 

  • Avni, A.A. & S.G. Soin. 1974. Adaptive characteristics of the embryogeny of Nothobranchius guentheri in connection with existence in temporary tropical habitats. J. Ichthyol. 14: 735–746.

    Google Scholar 

  • Bailey, R.J. 1933. The ovarian cycle in the viviparous teleost Xiphophorus helleri. Biol. Bull. 64: 206–225.

    Article  Google Scholar 

  • Ballard, W.W. & L.M. Dodes. 1968. The morphogenetic movements at the lower surface of the blastodisc in salmonid embryos. J. Exp. Zool. 168: 67–84.

    Article  Google Scholar 

  • Balon, E.K. 1979a. The theory of saltation and its application in the ontogeny of fishes: steps and thresholds. Env. Biol. Fish. 4: 97–101.

    Article  Google Scholar 

  • Balon, E.K. 1979b. The juvenilization process in phylogeny and the altricial to precocial forms in the ontogeny of fishes. Env. Biol. Fish. 4: 193–198.

    Article  Google Scholar 

  • Balon, E.K. 1980a. Early ontogeny of 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 Hauge.

    Google Scholar 

  • Balon, E.K. 1980b. Early ontogeny of North American landlocked arctic charr — sunapee, Salvelinus (Salvelinus) alpinus oquassa. In: E.K. Balon(ed.) Charrs: Salmonid Fishes of the Genus Salvelinus, Dr W. Junk Publishers, The Hauge pp. 563–606.

    Google Scholar 

  • Balon, E.K. 1980c. Early ontogeny of the brook charr, Salvelinus (Baione) fontinalis. In: E.K. Balon(ed.) Charrs: Salmonid Fishes of the Genus Salvelinus, Dr W. Junk Publishers, The Hauge pp. 631–666.

    Google Scholar 

  • Balon E.K. 1980d. Comparative ontogeny of charrs. In: E.K. Balon(ed.) Charrs: Salmonid Fishes of the Genus Salvelinus, Dr W. Junk Publishers, The Hauge pp. 703–720.

    Google Scholar 

  • Balon, E.K. 1981a. Saltatory processes and altricial to precocial forms in the ontogeny of fishes. Amer. Zool. 21: 573–596.

    Article  Google Scholar 

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

    Article  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. Reflections on some decisive events in the early life of fishes. Trans. Amer. Fish. Soc. 113: 178–185.

    Article  Google Scholar 

  • Balon, E.K. 1984b. 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. Early life histories of fishes: new developmental, ecological and evolutionary perspectives. Developments in Env. Biol. Fish. 5, Dr W. Junk Publishers, Dordrecht. 280 pp.

    Book  Google Scholar 

  • Boulekbache, H. 1981. Energy metabolism in fish development. Amer. Zool. 21: 377–389.

    Article  CAS  Google Scholar 

  • Bourdin, J. 1926. Le mechanism de l'éclosion chez les Téléostéens. I. Etude biologique et anatomique. Compt. Rend. Soc. Biol. 95: 1149–1151.

    Google Scholar 

  • Boyd, J.F. & R.C. Simmonds. 1974. Continuous laboratory production of fertile Fundulus heteroclitus (Walbaum) eggs lacking chorionic fibrils. J. Fish Biol. 6: 389–394.

    Article  Google Scholar 

  • Byrne, D.M. 1978. Life history of the spotfin killifish, Fundulus luciae (Pisces: Cyprinodontidae), in Fox Creek Marsh, Virginia. Estuaries 1: 211–227.

    Article  Google Scholar 

  • Champion, M.J., J.B. Shaklee & G.S. Whitt. 1975. Developmental genetics of teleost isozymes. pp. 417–437. In: C.L. Markert(ed.) Isozymes Vol. 3, Developmental Biology, Academic Press, New York.

    Google Scholar 

  • Crawford, R.B., C.E. Wilde, M.H. Heinemann & F.J. Hendler. 1973. Morphogenetic disturbances from timed inhibitions of protein synthesis in Fundulus. J. Embryol. exp. Morph. 29: 363–382.

    CAS  PubMed  Google Scholar 

  • Cunningham, J.E.R. & E.K. Balon. 1985. Early ontogeny of Adinia xenica (Pisces, Cyprinodontiformes): 1. The development of embryos in hiding. Env. Biol. Fish. 14: 115–166.

    Article  Google Scholar 

  • Cunningham, J.E.R. & E.K. Balon. 1986. Early ontogeny of Adinia xenica (Pisces, Cyprinodontiformes): 2. Implications of embryonic resting interval for larval development. Env. Biol. Fish. 15: 15–45.

    Article  Google Scholar 

  • David, L.R. 1939. Embryonic and early larval stages of the grunion, Leuresthes tenuis, and of the sculpin, Scorpaena guttata. Copeia 1939: 75–81.

  • DiMichele, L. 1980. The hatching mechanism of Fundulus heteroclitus. Ph.D. Thesis, University of Delaware, Newmark. 125 pp.

  • Dziekońska, J. 1956. Studies on embryonic development of fish. I. Observations on the spawning and embryonic development of bream in the Vistula Lagoon. Pol. Arch. Hydrobiol. 3: 291–305.

    Google Scholar 

  • Eaton, R.C. & J. Nissanov. 1985. A review of Mauthner-initiated escape behavior and its possible role in hatching in the immature zebrafish, Brachydanio rerio. Env. Biol. Fish. 12: 265–279.

    Article  Google Scholar 

  • Hass, R. 1976. Behavioural biology of the annual killifish, Nothobranchius guentheri. Copeia 1976: 80–91.

  • Hagenmaier, H.E. 1974. The hatching process in fish embryos. VI. Development, structure and function of the hatching gland cells of the rainbow trout, Salmo gairdneri. Z. Morphol. Tiere 79: 233–244.

    Article  Google Scholar 

  • Harrington, R.J. Jr. 1959. Delayed hatching in stranded eggs of marsh killifish, Fundulus confluentus. Ecology 40: 430–437.

    Article  Google Scholar 

  • Hubbs, C. 1966. Fertilization, initiation of cleavage and developmental temperature tolerance of the cottid fish Clinocottus analis. Copeia 1966: 29–42.

  • Ishida, J. 1944. Hatching enzyme in the fresh-water fish, Oryzias latipes. Annot. Zool. Jap. 22: 137–154.

    Google Scholar 

  • Kotlyarevskaya, N.V. 1967. Hatching dates of the loach Misgurnus fossilis L. as affected by oxygen conditions. Doklady Biol. Sci. Acad. Nauk SSSR 17: 746–749. (In Russian).

    Google Scholar 

  • Kotlyarevskaya, N.V. 1969. The hatching process in the pike (Esox lucius L.). J. Ichthyol. 9: 85–94.

    Google Scholar 

  • Lees, A.D. 1955. The physiology of diapause in arthropods. Cambridge University Press, Cambridge. 151 pp.

    Google Scholar 

  • Markofsky, J. & J.R. Matias. 1977. The effects of temperature and season of collection on the onset and duration of diapause in embryos of the annual fish Nothobranchius guentheri. J. Exp. Zool. 202: 49–56.

    Article  CAS  PubMed  Google Scholar 

  • Markofsky, J., J.R. Matias, K. Inglima, J.H. Vogelman & N. Orentreich. 1979. The variable effects of ambient and artificial light: dark cycles on embryonic diapause in a laboratory population of the annual fish Nothobranchius guentheri. J. Exp. Biol. 83: 203–215.

    Google Scholar 

  • Martin, R.A. & J.H. Finucane. 1968. Reproduction and ecology of the longnose killifish. Quart. J. Fla. Acad. Sci. 31: 101–111.

    Google Scholar 

  • McElman, J.F. & E.K. Balon. 1979. Early ontogeny of walleye, Stizostedion vitreum, with steps of saltatory development. Env. Biol. Fish. 4: 390–348.

    Article  Google Scholar 

  • McElman, J.F. & E.K. Balon. 1980. Early ontogeny of white sucker, Catostomus commersoni, with steps of saltatory development. Env. Biol. Fish. 5: 191–224.

    Article  Google Scholar 

  • Milkman, R. 1954. Controlled observations of hatching in Fundulus. Biol. Bull. 107: 300.

    Google Scholar 

  • Misitano, D.A. 1980. A record of internal fertilization in the roughback sculpin Chitinotus pugetensis with descriptions of their early larvae. Copeia 1980: 162–165.

  • Morenski, B. 1974. A new forced hatching method for killifish eggs. J. Amer. Killifish Assoc. 7: 296.

    Google Scholar 

  • Morin, R.P. & K.W. Able. 1983. Patterns of geographic variation in the egg morphology of the fundulid fish, Fundulus heteroclitus. Copeia 1983: 726–740.

  • 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.

  • Oppenheimer, J.M. 1937. The normal stages of Fundulus heteroclitus. Anat. Rec. 68: 1–16.

    Article  Google Scholar 

  • Peters, N. Jr. 1963. Embryonale Anpassungen oviparer Zahnkarpfen aus periodisch austrocknenden Gewässern. Int. Revue ges. Hydrobiol. 48: 257–313.

    Article  Google Scholar 

  • Schultz, L.P. & E.M. Stern. 1948. The ways of fishes. D. van Nostrand, Toronto. 264 pp.

    Google Scholar 

  • Shaklee, J.B., M.J. Champion & G.S. Whitt. 1974. Developmental genetics of teleosts: a biochemical analysis of lake chubsucker ontogeny. Devel. Biol. 38: 356–382.

    Article  CAS  Google Scholar 

  • Shaklee, J.B. & G.S. Whitt. 1977. Patterns of enzyme ontogeny in developing sunfish. Differentiation 9: 85–95.

    Article  CAS  PubMed  Google Scholar 

  • Smirnov, A.I. 1975. Biology, reproduction and development of Pacific salmons. Izd. Moskovskogo Univ., Moskva. 335 pp. (In Russian).

    Google Scholar 

  • Smith, S. 1957. Early development and hatching. pp. 323–359. In: M.E. Brown (ed.) The Physiology of Fishes, Vol. 1, Academic Press, New York.

  • Stelzer, R., H. Rosenthal & D. Seegers. 1971. Einfluss von 2,4-Dinitrophenol auf die Atmung und die Konzentration einiger Metabolite bei Embryonen des Herings Clupea harengus. Mar. Biol. 11: 369–378.

    Article  Google Scholar 

  • Sytina, L.A. & N.G. Nikolskaya. 1980. Changes of some temperature reactions in the embryogenesis of sturgeons and anuran amphibians. pp. 87–102. In: Morph. Aspects Evol., Nauka Press, Moscow. (In Russian).

    Google Scholar 

  • Tavolga, W.N. 1949. Embryonic development of the platyfish (Platypoecilus), swordtail (Xiphophorus) and their hybrids. Bull. Amer. Mus. Nat. Hist. 94: 165–229.

    Google Scholar 

  • Taylor, M.H., L. DiMichele & G.L. Leach. 1977. Egg stranding in the life cycle of the mummichog, Fundulus heteroclitus. Copeia 1977: 397–399.

  • Trifonova, A.N. 1937. La physiologic de la différenciation et de la croissance. I. L'équilibre Pasteur-Meyerhof dans le développement des poissons. Acta. Zool. 18: 375–445.

    Article  Google Scholar 

  • Turner, C.L. 1940a. Pseudoamnion, pseudochorion and follicular pseudoplacenta in poeciliid fishes. J. Morph. 67: 58–89.

    Google Scholar 

  • Turner, C.L. 1940b. Follicular pseudoplacenta and gut modifications in anablepid fishes. J. Morph. 67: 91–105.

    Article  Google Scholar 

  • Turner C.L. 1940c. Pericardial sac, trophotaeniae and alimentary tract in the embryos of goodeid fishes. J. Morph. 67: 271–289.

    Article  Google Scholar 

  • Turner, C.L. 1940d. Adaptations for viviparity in jenynsiid fishes. J. Morph. 67: 291–297.

    Article  Google Scholar 

  • Waddington, C.H. 1975. The evolution of an evolutionist. Edinburgh University Press, Edinburgh. 328 pp.

    Google Scholar 

  • Wilde, C.E. & R.B. Crawford. 1963. Cellular differentiation in the anamniota. I. Initial studies on the aerobic pathways of differentiation and morphogenesis in teleosts and urodeles. Devel. Biol. 7: 578–594.

    Article  CAS  Google Scholar 

  • Wilde, C.E. & R.B. Crawford. 1966. Cellular differentiation in the anamniota. III. Effects of actinomycin D and cyanide on the morphogenesis of Fundulus. Exp. Cell. Res. 44: 471–488.

    Article  CAS  PubMed  Google Scholar 

  • Wourms, J.P. 1972a. The developmental biology of annual fishes. I. Stages in the normal development of Austrofundulus myersi Dahl. J. Exp. Zool. 182: 143–168.

    Article  CAS  PubMed  Google Scholar 

  • Wourms, J.P. 1972b. Developmental biology of annual fishes. II. Naturally occurring dispersion and reaggregation of blastomeres during the development of annual fish eggs. J. Exp. Zool. 182: 169–200.

    Article  CAS  PubMed  Google Scholar 

  • Wourms, J.P. 1972c. The developmental biology of annual fishes. III. Pre-embryonic and embryonic diapause of variable duration in the eggs of annual fishes. J. Exp. Zool. 182: 389–414.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Yamamoto, T. 1975. Medaka (killifish) biology and strains. Kaigaku Publishing Co, Tokyo. 365 pp.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cunningham, J.E.R., Balon, E.K. Early ontogeny of Adinia xenica (Pisces, Cyprinodontiformes): 3. Comparison and evolutionary significance of some patterns in epigenesis of egg-scattering, hiding and bearing cyprinodontiforms. Environ Biol Fish 15, 91–105 (1986). https://doi.org/10.1007/BF00005425

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00005425

Keywords

Navigation