Skip to main content

Advertisement

Springer Nature Link
Log in

Embryonic and early larval development of White Sea cod Gadus morhua marisalbi (Gadidae)

  • Published:
Journal of Ichthyology Aims and scope Submit manuscript

Abstract

Embryonic and early larval development of White Sea cod Gadus morhua marisalbi are described. The study is conducted on live material obtained after spawning of fishes in the tanks and based on artificial insemination of eggs. Dynamics of contact and mobility properties of cells in vivo and in vitro (in cell culture) is assessed. Discrete chronological parameters of the morphogenetic movements are determined. Early ontogeny of the White Sea cod is very similar to that in G. morhua of the Northeast Atlantic. However, the former subspecies differs in larger egg diameter (on average, 1.50 mm), larger buoyancy (at a salinity up to 24.22‰), and a resistance to negative temperature (−1.8°C).

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

Access this article

Log in via an institution

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.

Institutional subscriptions

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Avni, A.A. and Soin, S.G., Adaptive features of embryogenesis of Nothobranchius guentheri (Preffer) related to tropical habitats in drying reservoirs, Vopr. Ikhtiol., 1974, vol. 14, no. 5(88), pp. 846–2.

    Google Scholar 

  • Bachop, W. and Price, J., Giant nuclei formation in the yolk sac syncytium of the muskellunge, a bony fish (Salmoniformes: Esocidae: Esox masquinongy), J. Morphol., 1971, vol. 135, no. 2, pp. 239–246.

    Article  Google Scholar 

  • Ballard, W.W., Morphogenetic movements in Salmo gairdneri Richardson, J. Exp. Zool., 1973a, vol. 184, no. 1, pp. 27–2.

    Article  Google Scholar 

  • Ballard, W.W., A new fate map for Salmo gairdneri Richardson, J. Exp. Zool., 1973b, vol. 184, no. 1, pp. 49–2.

    Article  Google Scholar 

  • Ballard, W.W., A re-examination of gastrulation in teleosts, Rev. Roum. Biol. Ser. Zool., 1973c, vol. 18, no. 2, pp. 119–2.

    Google Scholar 

  • Ballard, W.W., Morphogenetic movements and fate maps of vertebrates, Am. Zool., 1981, vol. 21, pp. 391–399.

    Article  Google Scholar 

  • Balon, E.K., Terminology of intervals in fish development, J. Fish. Res. Board Can., 1975, vol. 32, no. 9, pp. 1663–1670.

    Article  Google Scholar 

  • Betchaku, T. and Trinkaus, J.P., Programmed endocytosis during epiboly of Fundulus heteroclitus, Am. Zool., 1986, vol. 26, pp. 193–199.

    Article  Google Scholar 

  • Bouvet, J., Enveloping layer and periderm of the trout embryo (Salmo trutta fario L.), Cell Tissue Res., 1976, vol. 170, pp. 367–382.

    Article  CAS  PubMed  Google Scholar 

  • Bozhkova, V.P., Pal’mbakh, L.R., Khariton, V.Yu., Chailakhyan, L.M., Adhesive properties and surface relief of division furrows on the loach embryo, Ontogenez, 1982, vol. 13, no. 5, pp. 478–488.

    Google Scholar 

  • Chernyaev, Zh.A., Method of lateral microscopy using vertical chamber for living analysis of fish egg development, in Issledovaniya razmnozheniya i razvitiya ryb (Study of Reproduction and Development of Fishes), Moscow: Nauka, 1981, pp. 216–2.

    Google Scholar 

  • Damas, D., Contribution à la biologic des Gadidés, ICES Rap. Proc. Verb., 1909, vol. 10, no. 3, pp. 1–277.

    Google Scholar 

  • Detlaf, T.A. and Detlaf, A.A., Dimensionless characteristics of duration of development in embryology, Dokl. Akad. Nauk SSSR, 1960, vol. 134, pp. 199–202.

    Google Scholar 

  • Ellertsen, B., Moksness, E., Solemdal, P., et al., Some aspects of the biology of eggs and larvae of cod (Gadus morhua L.), Fisk. Dir. Skr. Ser. Hav. Unders., 1980, vol. 17, pp. 29–47.

    Google Scholar 

  • Evropeitseva, N.V., Rasovyi analiz belomorskoi treski (Group Analysis of the White Sea Cod), Leningrad: Leningr. Gos. Univ., 1937.

    Google Scholar 

  • Evseenko, S.A., Laurel, B., Brown, J.A., and Malikova, D.Yu., On the Gadus taxonomy: ontogenetic evidence, J. Ichthyol., 2006, vol. 46, no. 5, pp. 351–358.

    Article  Google Scholar 

  • Fridgeirsson, E., Embryonic development of five species of gadoid fishes in Icelandic waters, Rit Fiskideildar., 1978, vol. 5, no. 6.

    Google Scholar 

  • Gorodilov, Y.N., Terjesen, B.F., Krasnov, A., and Takle, H., Description of embryogenesis of Atlantic cod Gadus morhua, Open Mar. Biol. J., 2008, vol. 2, pp. 43–53.

    Article  Google Scholar 

  • Hall, T.E., Smith, P., and Johnoston, I.A., Stages of embryonic development in the Atlantic cod Gadus morhua, J. Morphol., 2004, vol. 259, pp. 255–270.

    Article  PubMed  Google Scholar 

  • Ignat’eva, G.M., Relative duration of early embryogenesis of Teleosts, Ontogenez, 1974, vol. 5, no. 5, pp. 427–436.

    PubMed  Google Scholar 

  • Ignat’eva, G.M., Rannii embriogenez ryb i amfibii (sravnitel’nyi analiz vremennykh zakonomernostei razvitiya) (Early Embryogenesis of Fishes and Amphibians: Comparative Analysis of Time Regularities of Development), Moscow: Nauka, 1979.

    Google Scholar 

  • Ignat’eva, G.M. and Rott, N.N., Temporal ratios between some processes before gastrulation in Teleosts, Dokl. Akad. Nauk SSSR, 1970, vol. 190, no. 2, pp. 484–487.

    PubMed  Google Scholar 

  • Kageyama, T., Cellular basis of epiboly of the enveloping layer in the embryo of the medaka, Oryzias latipes. II. Evidence for cell rearrangement, J. Exp. Zool., 1982, vol. 219, pp. 241–256.

    Article  Google Scholar 

  • Kageyama, T., Origin of yolk syncytium and mitotic pattern in the syncytium and blastomers in Oryzias latipes, Zool. Mag., 1983, vol. 92, pp. 485.

    Google Scholar 

  • Keller, R.E. and Trinkaus, J.P., Rearrangement of enveloping layer cells without disruption of the epithelial permeability barrier as factor in Fundulus epiboly, Dev. Biol., 1987, vol. 120, pp. 12–24.

    Article  CAS  PubMed  Google Scholar 

  • Kostomarova, A.A., Differentiation of loach blastoderm isolated from yolk in different cultivation media, in Kletochenaya differentsirovka i induktsionnye mekhanizmy (Cell Differentiation and Induction Mechanisms), Moscow: Nauka, 1965, pp. 160–2.

    Google Scholar 

  • Kostomarova, A.A., Teleostei fishes, in Metody biologii razvitiya (Methods of Development Biology), Moscow: Nauka, 1974, pp. 160–2.

    Google Scholar 

  • Lapin, V.I. and Matsuk, V.E., Dynamics of total chemical composition of developing pelagic eggs of Breogadus saida (Lepechin) and Gadus morhua maris-albi Derjugin in the White Sea, Vopr. Ikhtiol., 1981, vol. 21, no. 3, pp. 482–488.

    Google Scholar 

  • Lentz, T.L. and Trinkaus, J.P., A fine structural study of cytodifferentiation during cleavage, blastula and gastrula stages of Fundulus heteroclitus, J. Cell Biol., 1967, vol. 2, pp. 121–138.

    Article  Google Scholar 

  • Lesseps, R.J., Geurts van Kessel, A.H.M., and Denucé, J.M., Cell patterns and cell movements during early development of an annual fish, Nothobranchius neumanni, J. Exp. Zool., 1975, vol. 193, no. 2, pp. 137–146.

    Article  CAS  PubMed  Google Scholar 

  • Long, W.L., Proliferation, growth, and migration of nuclei in the yolk syncytium of Salmo and Catostomus, J. Exp. Zool., 1980, vol. 214, no. 3, pp. 333–343.

    Article  Google Scholar 

  • Mahotin, V.V., Morphogenetic differentiation in embryonal development of some Gadidae fishes, in II Vses. konf. “Voprosy rannego ontogeneza ryb,” Tezisy dokladov (II All-Union Conf. “Problems of Early Ontogenesis of Fishes,” Abstracts of Papers), Kiev: Naukova Dumka, 1978, pp. 44–2.

    Google Scholar 

  • Mahotin, V.V. and Burykin, Yu.B., Specific biology and distribution of the White Sea cod on early stages of development, in II Vses. konf. po morskoi biologii, Tezisy dokladov (II All-Union Conf. on Marine Biology, Abstracts of Papers), Vladivostok, 1982, part 3, pp. 30–2.

    Google Scholar 

  • Mahotin, V.V., Burykin, Yu.B., and Novikov, G.G., The White Sea cod: biology of reproduction and development, Vopr. Ikhtiol., 1986, vol. 26, no. 1, pp. 74–79.

    Google Scholar 

  • Mahotin, V.V. and Pavlov, D.A., Specific development of telolecithal eggs of Teleostei fishes, in VI Vses. soveshchaniya embriologov, Tezisy dokladov (VI All-Union Meeting of Embryologists, Abstracts of Papers), Moscow: Nauka, 1981, p. 114.

    Google Scholar 

  • Makhotin, V.V., Novikov, G.G., Soin, S.G., and Timeiko, V.N., The peculiarity of the development of White Sea cod, in The Propagation of Cod Gadus morhua L., Dahl, E., et al., Eds., Arendal, Norway: Inst. Mar. Res., 1984, vol. 1, pp. 105–120.

    Google Scholar 

  • Meek, J.A., The development of the cod (Gadus callarias), Fish. Invest. London, Ser. 2, 1924, vol. 7, pp. 1–25.

    Google Scholar 

  • Mikhin, V.S., The White Sea and Murmansk cod, Izv. Otd., Prikl. Ikhtiol., 1925, vol. 3, no. 2, pp. 189–208.

    Google Scholar 

  • Mina, M.V., Forms of the White Sea cod, in Materialy po ekologii treski severnoi Atlantiki (The Data on Ecology of the North Atlantic Cod), Moscow: Nauka, 1968, pp. 79–2.

    Google Scholar 

  • Mishin, A.V., Evseenko, S.A., and Evdokimov, Yu.V., Species composition and distribution of summer ichthyoplankton in Chupa estuary (Kandalaksha Bay of the White Sea), J. Ichthyol., 2008, vol. 48, no. 9, pp. 810–816.

    Article  Google Scholar 

  • Morrison, C.M., Histology of Atlantic cod, Gadus morhua: an atlas. Part 4. Eleutheroembryo and larva, Can. Spec. Publ. Fish. Aquat. Sci., 1993, vol. 119.

    Google Scholar 

  • Neifakh, A.A., Geneticheskie osnovy razvitiya organizma (Genetic Principles of Organism Development), Moscow: Znanie, 1969.

    Google Scholar 

  • Neifakh, A.A. and Timofeeva, M.Ya., Problemy regulyatsii v molekulyarnoi biologii razvitiya (Problems of Regulation in Molecular Biology of Development), Moscow: Nauka, 1978.

    Google Scholar 

  • Novikov, G.G., Rost i energetika razvitiya kostistykh ryb v rannem ontogeneze (Growth and Energy of Development of Teleostei Fishes in Early Ontogenesis), Moscow: Editorial URSS, 2000.

    Google Scholar 

  • Novikov, G.G., Ponomarenko, V.P., Mahotin, V.V., et al., Biology of the White Sea cod, in Biologicheskie resursy shel’fovykh i okrainnykh morei (Biological Resources of Shelf and Marginal Seas), Moscow: VNIRO, 1990, pp. 282–2.

    Google Scholar 

  • Pal’mbakh, L.R. and Ozernyuk, N.D., Structural features of cellular layers at the beginning of differentiation of Teleostei fishes, Ontogenez, 1983, vol. 14, no. 5, pp. 542–548.

    Google Scholar 

  • Parin, N.V., Evseenko, S.A., and Vasil’eva, E.D., Ryby morei Rossii: annotirovannyi katalog (Fishes of Russian Seas: Annotated Catalogue), Moscow: KMK, 2014.

    Google Scholar 

  • Pertseva, T.A., Spawning, eggs, and juveniles of commercial fish species in the Motovskoy Bay, Tr. VNIRO, 1939, vol. 4, pp. 417–467.

    Google Scholar 

  • Ponomarenko, V.P. and Khokhlina, N.S., Spawning of cod at the Murman coast in 1967 and 1968, Mater. Rybokhoz. Issled. Sev. Basseina, 1970, no. 16, part 1, pp. 132–2.

    Google Scholar 

  • Purchase, C.F., Goddard, S.V., and Brown, J.A., Production of antifreeze glycoproteins in cultured and wild juvenile Atlantic cod (Gadus morhua L.) in a common laboratory environment, Can. J. Zool., 2001, vol. 79, pp. 610–615.

    Article  CAS  Google Scholar 

  • Rass, T.S., Instruktsiya po sboru ikry i mal’kov ryb (Instruction on Collection of Fish Egg and Juveniles), Moscow: Pishchepromizdat, 1939.

    Google Scholar 

  • Rass, T.S., The data on reproduction and distribution of egg, larvae, and juveniles of Gadus morhua morhua L. in the Barents Sea, Tr. VNIRO, 1949, vol. 17, pp. 67–157.

    Google Scholar 

  • Rollefsen, G., Observations on cod eggs, Rapp. Proc.-Verb. Reun. Cons. Int. Explor. Sci. Mer. Medit., 1930, vol. 65, pp. 31–34.

    Google Scholar 

  • Rollefsen, H., Atlantic cod, in Mater. mezhd. konf. po okhrane zapasov ryb i drugikh morskikh zhivotnykh (Proc. Int. Conf. on Protection of Fish Reserves and Other Marine Animals), Moscow: VNIRO, 1957, vol. 1, pp. 198–199.

    Google Scholar 

  • Rott, N.N., Cell cycles in early ontogenesis of the peled, Ontogenez, 1979, vol. 10, no. 3, pp. 209–218.

    CAS  PubMed  Google Scholar 

  • Rott, N.N., Cellular divisions in pre-gastrulation development, Ontogenez, 1980, vol. 11, no. 1, pp. 3–23.

    CAS  Google Scholar 

  • Ruzzante, D.E., Taggart, Ch.T., Cook, D., and Goddard, S.V., Genetic differentiation between inshore and offshore Atlantic cod (Gadus morhua) off Newfoundland: a test and evidence of temporal stability, Can. J. Fish. Aquat. Sci., 1997, vol. 54, pp. 2700–2708.

    Article  Google Scholar 

  • Serebryakov, V.P., Reproduction of cod in northwestern Atlantic, Tr. Polar. Inst. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 1967, no. 20, pp. 205–242.

    Google Scholar 

  • Soin, S.G., New classification of structure of mature fish eggs by the ration of yolk quantity and ooplasm, Ontogenez, 1981, vol. 12, no. 4, pp. 21–26.

    Google Scholar 

  • Solemdal, P., Makhotin, V., and Fonn, M., Long-term studies on spawning in Arcto-Norwegian cod mortality pattern of eggs and early larvae, in International Council for the Exploration of the Sea Council Meeting 1998/DD:8, 1998.

    Google Scholar 

  • Sonina, M.L., The White Sea cod, in Matererialy po kompleksnomu izucheniyu Belogo morya (The Data on Complex Study of the White Sea), Moscow: Akad. Nauk SSSR, 1957, no. 1, pp. 230–242.

    Google Scholar 

  • Stroganov, A.N., Cherenkova, N.N., Semenova, A.V., Andreeva, A.P., and Afanas’ev, K.I., Comparative analysis of genetic variability of white sea cod (Gadus morhua marisalbi) at allozyme and microsatellite markers, Russ. J. Genet., 2013, vol. 49, no. 12, pp. 1207–1212.

    Article  CAS  Google Scholar 

  • Suvorov, E.K., The Motovskoy Bay as the spawning place of cod, Izv. Leningr. Ikhtiol. Inst., 1931, vol. 13, no. 2, pp. 61–89.

    Google Scholar 

  • Thompson, B.M. and Riley, J.D., Gadus morhua. Egg and larval development studies in the North Sea cod (Gadus morhua L.), Rapp. Proc.-Verb. Reun. Cons. Int. Explor. Sci. Mer. Medit., 1981, vol. 178, pp. 553–559.

    Google Scholar 

  • Thorsen, A., Kjesbu, O.S., Fyhn, H.Y., and Solemdal, P., Physiological mechanisms of buoyancy in eggs from brackish water cod, J. Fish Biol., 1996, vol. 48, pp. 457–477.

    Article  CAS  Google Scholar 

  • Timofeeva, M.Ya., Kafiani, K.A., and Neifakh, A.A., Change of RNA-synthesizing function of nuclei at the first stages of embryogenesis, in Struktura i funktsii kletochnogo yadra (Structure and Functions of Cellular Nucleus), Moscow: Nauka, 1967, pp. 201–2.

    Google Scholar 

  • Trinkaus, J.P., Differentiation in vitro of isolated blastoderms of Fundulus heteroclitus, Anat. Rec., 1953, vol. 115, pp. 375–376.

    Google Scholar 

  • Trinkaus, J.P., Cells into Organs. The Forces That Shape the Embryo, Englewood Cliffs, N. J.: Prentice-Hall, 1969.

    Google Scholar 

  • Trinkaus, J.P., Surface activity and locomotion of Fundulus deep cells during blastula and gastrula stages, Dev. Biol., 1973, vol. 30, pp. 68–103.

    Article  Google Scholar 

  • Trinkaus, J.P., Mechanism of Fundulus epiboly, Am. Zool., 1984, vol. 24, pp. 673–688.

    Article  Google Scholar 

  • Trinkaus, J.P., Some contributions of research on early Teleost embryogenesis to general problems of development, in Experimental Embryology in Aquatic Plants and Animals. Series A: Life Science, Marthy, H.-J., Ed., New York: Plenum, 1990, vol. 195, pp. 315–327.

    Chapter  Google Scholar 

  • Trinkaus, J.P., Ingression during early gastrulation in Fundulus, Dev. Biol., 1996, vol. 117, pp. 356–370.

    Article  Google Scholar 

  • Trinkaus, J.P. and Lentz, T.L., Surface specializations of Fundulus cells and their relation to cell movements during gastrulation, J. Cell. Biol., 1967, vol. 32, pp. 139–154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valerio, P.F., Goddard, S.V., Kao, M.H., and Fletcher, G.L., Survival of northern Atlantic cod (Gadus morhua) eggs and larvae when exposed to ice and low temperature, Can. J. Fish. Aquat. Sci., 1992, vol. 49, pp. 2588–2595.

    Article  Google Scholar 

  • Vasnetsov, V.V., The stages of development of Teleosts, in Ocherki po obshchim voprosam ikhtiologii (Essays on General Problems of Ichthyology), Moscow: Akad. Nauk SSSR, 1953, pp. 207–2.

    Google Scholar 

  • Wourms, J.P., Naturally occurring phased of cellular dispersion and re-aggregation during early vertebrate development, Am. Zool., 1965, vol. 5, pp. 662–663.

    Google Scholar 

  • Wourms, J.P., The developmental biology of annual fishes. II. Naturally occurring dispersion and re-aggregation of blastomeres during the development of annual fish eggs, J. Exp. Zool., 1972, vol. 182, no. 2, pp. 169–200.

    Article  CAS  PubMed  Google Scholar 

  • Zaitsev, Yu.P., Determination of floating abilities of pelagic eggs of some species of the Black Sea fishes, Dokl. Akad. Nauk SSSR, 1954, vol. 94, no. 3, pp. 577–579.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biological Faculty, Moscow State University, Moscow, 119899, Russia

    V. V. Makhotin

Authors
  1. V. V. Makhotin
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to V. V. Makhotin.

Additional information

Original Russian Text © V.V. Makhotin, 2016, published in Voprosy Ikhtiologii, 2016, Vol. 56, No. 2, pp. 177–199.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Makhotin, V.V. Embryonic and early larval development of White Sea cod Gadus morhua marisalbi (Gadidae). J. Ichthyol. 56, 259–280 (2016). https://doi.org/10.1134/S0032945216020119

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0032945216020119

Keywords