Skip to main content
Log in

Heat resistance of gametes of marine invertebrates in relation to temperature conditions under which the species exist

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

It is the purpose of this paper to elucidate the possible role of the heat resistance level of mature gametes and embryos of poikilotherms in the adaptation of a species to environmental temperature conditions. Within a species, heat resistance of gametes does not undergo any recognisable changes even in the presence of significant fluctuations in temperature. Evidence in support of this statement was obtained on gametes of invertebrates belonging to different populations of the same species collected in different seasons, and on invertebrates maintained under different temperatures. The heat resistance of gametes is correlated with the degree of thermophily of the species concerned. Species living under similar temperature conditions exhibit minimal, if any, differences in heat resistance. Hence, the heat resistance level of their gametes is a function of temperature conditions of formation and existence of the species as a whole. During the ontogenesis of poikilotherms, eggs, zygotes and early stages of embryonic development are most susceptible to heat injury. The upper thermal limit for the normal development of eggs and embryos is only 1 to 3Co higher than the temperatures encountered under natural conditions. It is concluded that the heat resistance level of gametes and embryos represents an adjustment to temperatures at which spawning, fertilisation and earlier embryonal development occur. Temperatures which, throughout the year, exceed the upper thermal limit or remain below the lower thermal limit for the development of embryos, act as limiting factors for the species' distribution.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Literature cited

  • Alexandrov, V.Y.: The relation between thermostability of protoplasm and environmental temperature conditions. [Russ.] Dokl. Akad. Nauk SSSR 83, 149–152 (1952)

    Google Scholar 

  • —: On the biological significance of the correlation between the heat resistance level of proteins and the environmental temperature conditions of a species. [Russ.] Usp. sovrem. Biol. 60, 28–44 (1965)

    Google Scholar 

  • Andronikov, V.B.: Thermostability of the sexual cells and zygotes of sea urchins. [Russ.] Citologija 5, 234–237 (1963)

    Google Scholar 

  • —: Heat resistance of sexual cells and embryos of poikilothermic animals. [Russ., Summary in English] In: Heat resistance of cells of animals, pp 125–139. Ed. by B.P. Ushakov. Moscow-Leningrad: Academy of Sciences 1965

    Google Scholar 

  • —: Heat resistance of gametes of poikilothermic animals. In: The cell and environmental temperature, pp 398–402. Ed. by A.S. Troshin. Oxford: Pergamon Press 1967a

    Google Scholar 

  • —: The character of changes in thermostability of embryos of poikilotherms at early stages of ontogenesis. [Russ., Summary in English] In: Variability in cellular heat resistance of animals in ontogenesis and phylogenesis, pp 4–12. Ed. by B.P. Ushakov. Leningrad: Academy of Sciences 1967b

    Google Scholar 

  • Appellöf, A.: Über die Beziehungen zwischen Fortpflanzung und Verbreitung mariner Tierformen. Int. Congr. Zool. (8, Graz, 1910), pp 303–311. Jena: 1912

  • Bhaud, M.: Quelques données sur le déterminisme écologique de la reproduction des annélides polychètes. Mar. Biol. 17, 115–136 (1972)

    Google Scholar 

  • Bowler, K.: A study of the factors involved in acclimatization to temperature and death at high temperatures in Astacus pallipes. I. Experiments on intact animals. J. cell. comp. Physiol. 63, 119–132 (1963a)

    Google Scholar 

  • —: A study of the factors involved in acclimatization to temperature and death at high temperatures in Astacus pallipes. II. Experiments at the tissue level. J. cell. comp. Physiol. 63, 133–146 (1963b)

    Google Scholar 

  • Brett, J.R.: Temperature: animals-fishes; functional responses. In: Marine ecology. Vol. I. Environmental factors, Pt 1. pp 515–560. Ed. by O. Kinne. London: Wiley Interscience 1970

    Google Scholar 

  • Buzhinskaya, G.N.: A contribution to the ecology of reproduction of Polychaeta in the Posjet Bay (Sea of Japan). [Russ.] Zool. Zh. 52, 1777–1782 (1973)

    Google Scholar 

  • Calabrese, A.: Individual and combined effects of salinity and temperature on embryos and larvae of the coot clam, Mulinia lateralis (Say). Biol. Bull. mar. biol. Lab., Woods Hole 137, 417–428 (1969)

    Google Scholar 

  • Davis, H.C. and A. Calabrese: Combined effect of temperature and salinity on development of eggs and growth of larvae of Mercenaria mercenaria and Crassostrea virginica. Fishery Bull. Fish. Wildl. Serv. U.S. 63, 643–655 (1964)

    Google Scholar 

  • Dregolskaya, I.N.: Heat resistance of ciliated epithelium of gills of Mytilus galloprovincialis L. from the Black Sea. [Russ., Summary in English]. In: Problems of cytoecology of animals, pp 43–50. Ed. by B.P. Ushakov. Moscow: Academy of Sciences 1963

    Google Scholar 

  • Dzhamusova, T.A.: Thermostability of sea mollusc muscle tissue. [Russ.] Citologija 2, 274–286 (1960)

    Google Scholar 

  • Ekman, S.: Zoogeography of the sea, 417 pp. London: Sidgwick & Jackson 1953

    Google Scholar 

  • Giese, G.C.: Comparative physiology: annual reproductive cycles of marine invertebrates. A. Rev. Physiol. 21, 547–576 (1959)

    Google Scholar 

  • Golikov, A.N.: Species and speciation in poikilothermal animals. Mar. Biol. 21, 257–268 (1973)

    Google Scholar 

  • — and O.G. Kussakin: Fauna and ecology of gastropod molluscs (Gastropoda, Prosobranchia) of the littoral of the Kuril Islands. [Russ.] Issled. dal'nevost. More i SSSR (Leningrad) 8, 248–346 (1962)

    Google Scholar 

  • — and O.A. Scarlato: Method for indirectly defining optimum temperatures of inhabitancy for marine cold-blooded animals. Mar. Biol. 20, 1–5 (1973)

    Google Scholar 

  • Gorodilov, Y.N.: The study of sensitivity of fishes to high temperatures during embryogenesis. I. Changes in the sensitivity of developing eggs of autumn-spawning fish species to the action of high temperature. [Russ.] Citologija 11, 169–179 (1969)

    Google Scholar 

  • Gunter, G.: Temperature. In: Treatise on marine ecology and paleoecology. Vol. I. Ecology, pp 159–184. Ed. by J.W. Hedgpeth. New York: Geological Society of America 1957. (Mem. geol. Soc. Am. No. 67)

    Google Scholar 

  • Heinonen, A.: Reproduction of Mytilus edulis (L) in the Finnish southwestern archipelago in summer 1960. Suomal. eläin-ja kasvit. Seur. van. Tiedon. Pöytäk. 16, 137–142 (1961)

    Google Scholar 

  • Kinne, O.: The effects of temperature and salinity on marine and brackish water animals. I. Temperature. Oceanogr. mar. Biol. A. Rev. 1, 301–340 (1963)

    Google Scholar 

  • —: Temperature: animals-invertebrates. In: Marine ecology, Vol. I. Environmental factors, Pt 1. pp 407–514. Ed. by O. Kinne. London: Wiley Interscience 1970

    Google Scholar 

  • Korringa, P.: Water temperature and breeding throughout the geographical range of Ostrea edulis. Année biol. (sér. III) 33, 1–17 (1957)

    Google Scholar 

  • Largen, M.J.: The influence of water temperature upon the life of the dog whelk Thais lapillus (Gastropoda: Prosobranchia). J. Anim. Ecol. 36, 207–215 (1967)

    Google Scholar 

  • Lønning, S.: Variations in the thermal sensitivity during the early development of the sea urchin embryo. Ark. Zool. 12, 359–381 (1959)

    Google Scholar 

  • Loosanoff, V.: Spawning of Venus mercenaria (L). Ecology 18, 506–515 (1937)

    Google Scholar 

  • Mileikovsky, S.A.: On the relation between thermal limits of spawning and zoogeography of species of marine invertebrates. [Russ.] Zool. Zh. 39, 666–669 (1960)

    Google Scholar 

  • —: Reproduction and spawning in marine shelf benthic invertebrates and the water temperature. [Russ.] Trudÿ Inst. Okeanol. 88, 113–149 (1970)

    Google Scholar 

  • Moore, A.R.: Some effect of temperature on development in the sea urchin Allocentrotus fragilis. Biol. Bull. mar. biol. Lab., Woods Hole 117, 150–153 (1959)

    Google Scholar 

  • Moore, J.A.: Temperature tolerance and rates of development in the eggs of Amphibia. Ecology 20, 459–478 (1939)

    Google Scholar 

  • —: The role of temperature in speciation of frogs. Biol. Symp. 6, 189–213 (1942)

    Google Scholar 

  • Orton, J.H.: Sea temperature, breeding and distribution in marine animals. J. mar. biol. Ass. U.K. 12, 339–366 (1920)

    Google Scholar 

  • Ropes, J.W.: Reproductive cycle of the surf clam Spisula solidissima in offshore New Jersey. Biol. Bull. mar. biol. Lab., Woods Hole 135, 349–365 (1968)

    Google Scholar 

  • Runnström, S.: Über die Thermopathie der Fortpflanzung und Entwicklung mariner Tiere in Beziehung zu ihrer geographischen Verbreitung Bergens Mus. Årb. 2, 1–67 (1927)

    Google Scholar 

  • —: Weitere Studien über die Temperaturanpassung der Fortpflanzung und Entwicklung mariner Tiere. Bergens Mus. Årb. (naturvid.) 1929 (10), 1–46 (1929)

    Google Scholar 

  • —: Die Anpassung der Fortpflanzung und Entwicklung mariner Tiere an die Temperaturverhältnisse verschiedener Verbreitungsgebiete. Bergens Mus. Årb. 1936 (3), 3–36 (1936)

    Google Scholar 

  • Schlieper, C.: Genotypische und phaenotypische Temperature- und Salzgehaltsadaptionen bei marinen Bodeninvertebraten der Nord- und Ostsee. Kieler Meeresforsch. 16, 180–185 (1960)

    Google Scholar 

  • Sveshnikov, V.A.: Types of reproduction and development of polychaetes and their geographical distribution. [Russ.] Zool. Zh. 38, 829–841 (1959)

    Google Scholar 

  • Svinkin, V.B.: Heat resistance of spermatozoa of the grass frog and the lake frog. [Russ.] Citologija 1, 580–586 (1959)

    Google Scholar 

  • —: Heat resistance of spermatozoa of some Unio species. [Russ.] Dokl. Akad. Nauk SSSR 139, 1227–1230 (1961)

    Google Scholar 

  • Thompson, T.E.: The influence of temperature on spawning in Adalaria proxima (A. & N.) (Gastropoda, Nudibranchia). Oikos 9, 246–252 (1958)

    Google Scholar 

  • Thorson, G.: The larval development, growth and metabolism of arctic marine bottom invertebrates compared with those of other seas. Meddr. Grønland 100, 5–155 (1936)

    Google Scholar 

  • —: Reproductive and larval ecology of marine bottom invertebrates. Biol. Rev. 25, 1–45 (1950)

    Google Scholar 

  • Ushakov, B.P.: Heat resistance of somatic muscles of amphibians as related to the environmental conditions of a species. [Russ.] Zool. Zh. 34, 578–588 (1955)

    Google Scholar 

  • —: Heat resistance of cellular proteins of poikilotherms as related to the adaptation of a species to environmental temperature conditions. [Russ.] Zh. obshch. Biol. 17, 154–160 (1956)

    Google Scholar 

  • —: On the conservatism of the protoplasm of a species in poikilotherms. [Russ.] Zool. Zh. 37, 693–706 (1958a)

    Google Scholar 

  • —: The problem of tissue and substantial adaptation of poikilotherms to the environmental temperature conditions of existence of a species. In: The evolution of functions of nervous system, pp 57–66. Ed. by D.A. Biryukov. Leningrad: Publishing House of Medical Literature 1958b

    Google Scholar 

  • —: Heat resistance of different tissues of the frog as related to environmental temperature. In: Problems of cytology and protozoology, pp 84–99. Ed. by Y.I. Polyansky. Moscow-Leningrad: Academy of Sciences 1960a

    Google Scholar 

  • —: Eine zytophysiologische Analyse der Anpassung der Reptilien an das Leben in der Wüste Karakum. Zool. Jb. 87, 507–524 (1960b)

    Google Scholar 

  • —: Thermostability of cells and proteins of poikilotherms and its significance in speciation. Physiol. Rev. 44, 518–560 (1964)

    Google Scholar 

  • —: The present-day state of the problem of heat injury mechanism and causes of changes in cell thermostability. [Russ.] In: Heat resistance of cells of animals, pp 5–52. Ed. by B.P. Ushakov. Moscow-Leningrad: Academy of Sciences 1965

    Google Scholar 

  • Valli, G.: Cyclo di maturitá sessuale in Mytilus galloprovincialis Lam. di Duino (Trieste). Boll. Pesca Piscic. Idrobiol. 26, 259–265 (1972)

    Google Scholar 

  • Vernberg, F.J., C. Schlieper and D.E. Schneider: The influence of temperature and salinity on ciliary activity of excised gill tissue of molluscs from North Carolina. Comp. Biochem. Physiol. 8, 271–285 (1963)

    Google Scholar 

  • Volpe, E.P.: Embryonic temperature adaptations and relationships in toads. Physiol. Zoöl. 26, 344–354 (1953)

    Google Scholar 

  • Zakhvatkina, K.A.: Phenology of larvae of bivalves of Sevastopol Bay. [Russ.] Trudÿ sevastopol. biol. Sta. 16, 173–176 (1963)

    Google Scholar 

  • Zhirmunsky, A.V.: A study of temperature adaptation of invertebrates from the South China Sea. [Russ.] Citologija 2, 675–691 (1960)

    Google Scholar 

  • —: A comparative study of cellular thermostability of marine invertebrates in relation to their geographical distribution and ecology. In: The cell and environmental temperature, pp 142–150. Ed. by B.P. Ushakov. Moscow-Leningrad: Academy of Sciences 1964

    Google Scholar 

  • —: Cellular thermostability of marine invertebrates in relation to vertical distribution of the species in the upper sublittoral of Possiet Bay (Japan Sea). In: Scientific papers of the Institute of Marine Biology, pp 65–67. Ed. by A.V. Zhirmunsky. Vladivostock: Academy of Sciences of the USSR, Far Eastern Scientific Center 1969

    Google Scholar 

  • — and Tsu-Li-Tsun: The heat resistance of the ciliated epithelium of sympatric species of tropical molluscs of the Nerita species as related to the environmental temperature conditions. [Russ.] Citologija 2, 478–482 (1960)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by M.E. Vinogradov, Moscow

Rights and permissions

Reprints and permissions

About this article

Cite this article

Andronikov, V.B. Heat resistance of gametes of marine invertebrates in relation to temperature conditions under which the species exist. Mar. Biol. 30, 1–11 (1975). https://doi.org/10.1007/BF00393747

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00393747

Keywords

Navigation