Skip to main content
  • Experimental Ecology — Its Significance As A Marine Biological Tool
  • Published:

Changes in temperature tolerance ofBalanus balanoides during its life-cycle

Veränderungen der Temperaturtoleranz vonBalanus balanoides während seines Lebenszyklus

Kurzfassung

In Nordwales weisen die oberen Letaltemperaturen des CirripediersB. balanoides nur geringe jahreszeitliche Variationen auf. Jedoch treten je nach der Jahreszeit merkbare Resistenzveränderungen bei Temperaturen unter Null auf, wobei die untere Letaltemperatur von −6,0° C im Juni bis zu −17,6° C im Januar schwankt. Eine außergewöhnlich starke Kältetoleranz wird in der Zeit von Dezember und Januar erworben und zwischen Februar und April wieder verloren. Obwohl diese Zeitspanne mit der Oviposition beziehungsweise dem Schlüpfen der Nauplien zusammenfallen, konnte festgestellt werden, daß die Kältetoleranz nicht notwendigerweise vom Brutzyklus abhing oder diesen begleitete. Unter Laboratoriumsbedingungen wurde von kalt gehaltenen Tieren eine Kälteresistenz nicht erworben, auch ging diese bei Tieren, die während des Frühlings im Labor verblieben, nicht verloren. Es ließ sich nicht beweisen, daß Veränderungen in der Ernährung oder Änderungen in der Tageslänge zu einem Verlust der Kälteresistenz führen. Die Cypriden waren wesentlich weniger widerstandsfähig, sowohl gegenüber hohen wie niedrigen Temperaturen, als überwinternde Adulte und die ältesten Embryostadien. Während der Metamorphose zeigte sich eine merkliche Erhöhung der Temperaturresistenz. Das Auftreten der Kälteresistenz beim Adultus fiel mit einer Periode „physiologischen Winterschlafs“ zusammen, wobei gewisse Gewebe reduziert wurden und Nahrungsaufnahme, Atmung und biosynthetische Aktivität nachließen. Dieser stoffwechselphysiologische Aktivitätsrückgang könnte ein Faktor sein, der die beobachtete erhöhte Kältetoleranz fördert. Außerdem wird möglicherweise auch die Zusammensetzung der Körperflüssigkeiten während des Winters so verändert, daß die Gewebe geschützt werden.

Summary

1. The barnacleBalanus balanoides exhibits little seasonal variation in upper lethal temperatures in North Wales.

2. There are marked seasonal changes in resistance to sub-zero temperatures, the lower lethal varying from −6.0° C in June to −17.6° C in January.

3. Exceptional tolerance to cold is acquired between December and January and is lost between February and April. Although these dates coincide with oviposition and naupliar liberation respectively, it was found that cold tolerance did not necessarily depend upon, or accompany, the normal breeding cycle.

4. Cold tolerance was not acquired by animals kept cold in the laboratory during winter, nor was it lost in animals kept in the laboratory during spring. There was no evidence that changes in nutrition or in the light régime led to loss of cold tolerance.

5. The cyprids were considerably less resistant to both high and low temperatures than the overwintering adults and the late-stage embryos. There was a marked increase in resistance at metamorphosis.

6. The appearance of cold tolerance in the adult coincides with a period of “physiological hibernation”, involving loss of certain tissues, diminished feeding activity, respiration and biosynthesis. The metabolic inactivity of the animal may be a factor promoting the greatly increased tolerance to cold that we have observed, while the composition of the body fluids may also be modified during the winter in such a way as to protect the tissues.

Literature cited

  • Allen, M. B., 1960. Utilisation of thermal energy by living organisms.In: Comparative biochemistry. Ed. by M. Florkin & H. S. Mason. Academic pr., New York,1, 487–514.

    Google Scholar 

  • Andrews, F. B., 1925. The resistance of marine animals of different ages.Publs Puget Sound mar. biol. Stn 3, 361–363.

    Google Scholar 

  • Asahina, E., Aoki, K. &Shinozaki, J., 1954. The freezing process of frost-hardy caterpillars.Bull. ent. Res. 45, 329–339.

    Google Scholar 

  • Bachmetjew, P., 1899. Über die Temperatur der Insecten nach Beobachtungen in Bulgarien.Z. wiss. Zool. 66, 521–604.

    Google Scholar 

  • Barnes, H., 1958. Regarding the southern limits ofBalanus balanoides (L.).Oikos 9, 139–157.

    Google Scholar 

  • —— 1959. Temperature and the life-cycle ofBalanus balanoides.In: Marine boring and fouling organisms. Ed. by D. L. Ray. Univ. of Washington pr., Seattle, 234–245.

    Google Scholar 

  • —— 1962. The so-called anecdysis inBalanus balanoides and the effect of breeding upon the growth of the calcareous shell of some common barnacles.Limnol. Oceanogr. 7, 462–473.

    Google Scholar 

  • —— &Finlayson, D. M., 1963. Seasonal changes in body weight, biochemical composition and oxygen uptake in two common boreo-arctic cirripedesBalanus balanoides andB. balanus.J. mar. biol. Ass. U. K. 43, 185–211.

    Google Scholar 

  • Bělehrádek, J., 1935. Temperature and living matter.Protoplasma-Monogr. 8, 1–277.

    Google Scholar 

  • —— 1957. Physiological aspects of heat and cold.A. Rev. Physiol. 19, 59–82.

    Google Scholar 

  • Bodenheimer, F. S. &Klein, H. Z., 1930. Über die Temperaturabhängigkeiten von Insekten. 2. Die Abhängigkeit der Aktivität bei der Ernteameise,Messor semirufus,E. André, von Temperatur und anderen Faktoren.Z. vergl. Physiol. 11, 345–385.

    Google Scholar 

  • Bovbjerg, R. V., 1952. Comparative physiology and ecology of the crayfishOrconectes propinquus andCambarus fodiens.Physiol. Zool. 25, 34–55.

    Google Scholar 

  • Bovee, E. C., 1949. Studies on the thermal death ofHyalella azteca Saussare.Biol. Bull. mar. biol. Lab., Woods Hole 96, 123–128.

    Google Scholar 

  • Chambers, R. &Hale, H. P., 1932. The formation of ice in protoplasm.Proc. R. Soc. Lond. (B)110, 336–352.

    Google Scholar 

  • Crisp, D. J., 1954. The breeding ofBalanus porcatus (Da Costa) in the Irish Sea.J. mar. biol. Ass. U. K. 33, 473–496.

    Google Scholar 

  • —— 1955. The rate of development ofBalanus balanoides (L.) embryosin vitro.J. Anim. Ecol. 28, 119–132.

    Google Scholar 

  • —— 1956. A substance promoting hatching and liberation of young in cirripedes.Nature, Lond. 178, 263.

    Google Scholar 

  • —— 1957. Effect of low temperature on the breeding of marine animals.Nature, Lond. 179, 1138–1139.

    Google Scholar 

  • -- Ed. 1963. The effects of the severe winter of 1962–63 on marine life in Britain.J. Anim. Ecol. 33, 165–210.

  • —— &Clegg, D. J., 1960. The induction of the breeding condition inBalanus balanoides (L.).Oikos 11, 265–275.

    Google Scholar 

  • —— &Patel, B. S., 1960. The moulting cycle inBalanus balanoides (L.).Biol. Bull. mar. biol. Lab., Woods Hole 118, 31–47.

    Google Scholar 

  • —— &Spencer, C. P., 1958. The control of the hatching process in barnacles.Proc. R. Soc. Lond. (B) 148, 275–299.

    Google Scholar 

  • Dawson, R. M. C. &Barnes, H., 1966. Studies in the biochemistry of cirripede eggs. 2. Changes in lipid composition during development ofBalanus balanoides andB. balanus.J. mar. biol. Ass. U. K. 46, 249–261.

    Google Scholar 

  • Dickie, L. M., 1958. Effects of high temperature on survival of the giant scallop.J. Fish. Res. Bd Can. 15, 1189–1211.

    Google Scholar 

  • —— &Medcof, J. C., 1963. Causes of mass mortalities of scallops(Placopecten magellanicus) in the South-western Gulf of St. Lawrence.J. Fish. Res. Bd Can. 20, 451–482.

    Google Scholar 

  • Doebbler, G. F. &Cowley, C. W., 1964. Cryobiology.Int. Sci. Technol. No 30 (June), 58–71.

  • Doudoroff, P., 1942. The resistance and acclimatisation of marine fishes to temperature changes. 1. Experiments withGirella nigricans (Ayres).Biol. Bull. mar. biol. Lab., Woods Hole 83, 219–244.

    Google Scholar 

  • Edwards, G. A. &Irving, L., 1943. The influence of temperature and season upon the oxygen consumption of the sand crabEmerita talpoida Say.J. cell. comp. Physiol. 21, 169–182.

    Google Scholar 

  • Evans, R. G., 1948. The lethal temperatures of some common British littoral molluscs.J. Anim. Ecol. 17, 165–173.

    Google Scholar 

  • Fry, F. E. J., 1947. Effects of the environment on animal activity.Univ. Toronto Stud. (Biol. Ser.) = (Publs Ont. Fish. Res. Lab. 68)55, 1–62.

    Google Scholar 

  • —— 1957. The lethal temperature as a tool in taxonomy.Année biol. 33, 205–219.

    Google Scholar 

  • Gunter, G., 1957. Temperature.In: Treatise on marine ecology and paleoecology. Vol. 1: Ecology. Ed. by J. W. Hedgpeth.Mem. Geol. Soc. Am. 67, 159–184.

    Google Scholar 

  • Hathaway, E. S., 1927. Quantitative studies of the changes produced by acclimatisation in the tolerance of high temperatures by fishes and amphibians.Bull. Bur. Fish., Wash. 43, 169–192.

    Google Scholar 

  • Hoff, J. G. &Westman, J. R., 1966. The temperature tolerance of three species of marine fishes.J. mar. Res. 24, 131–140.

    Google Scholar 

  • Huntsman, A. G. &Sparks, M. I., 1924. Limiting factors for marine animals. 3. Relative resistance to high temperatures.Contr. Can. Biol. Fish. (N. S.)2, 97–114.

    Google Scholar 

  • Iljin, W. S., 1935. The relation of cell sap concentration to cold resistance in plants.Zap. naučno-issled. Ob'ed. russk. svob. Univ. Prage (Bull. Ass. russ. Rech. scient. Prague) 3 (8) No. 13, 33–55.

    Google Scholar 

  • Kanwisher, J. W., 1955. Freezing in intertidal animals.Biol. Bull. mar. biol. Lab., Woods Hole 109, 56–63.

    Google Scholar 

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

    Google Scholar 

  • Krog, J., 1954. The influence of seasonal environmental changes upon the metabolism, lethal temperature and rate of heart beat ofGammarus limnaeus Smith taken from an Alaskan lake.Biol. Bull. mar. biol. Lab., Woods Hole 107, 397–410.

    Google Scholar 

  • Luyet, B. J. &Gehenio, P., 1940. The mechanism of injury and death by low temperature. A review.Biodynamica 3, 33–99.

    Google Scholar 

  • Mcleese, D. W., 1956. Effects of temperature, salinity and oxygen on the survival of the American lobster.J. Fish. Res. Bd Can. 13, 247–272.

    Google Scholar 

  • Marlier, G., 1949. Relation entre température léthale et habitat normal chez les larves de trichoptères.C. r. Séanc. Soc. Biol. 143, 100–101.

    Google Scholar 

  • Marshall, S. M., Nicholls, A. G. &Orr, A. P., 1935. On the biology ofCalanus finmarchicus. 6. Oxygen consumption in relation to environmental conditions.J. mar. biol. Ass. U. K. 20, 1–27.

    Google Scholar 

  • Moore, H. B., 1935. The biology ofBalanus balanoides. 3. The soft parts.J. mar. biol. Ass. U. K. 20, 263–274.

    Google Scholar 

  • Orr, P. R., 1955. Heat death of whole animals and tissues.Physiol. Zool. 28, 290–302.

    Google Scholar 

  • Petersen, G. H., 1962. The distribution ofBalanus balanoides (L.) andLittorina saxatilis (Olivi) var.groenlandica Menke in northern west Greenland.Meddr Grønland 159 (No 9), 1–47.

    Google Scholar 

  • Polge, C., 1957. Low temperature storage of mammalian spermatozoa.Proc. R. Soc. Lond. (B) 147, 498–508.

    Google Scholar 

  • Precht, H., 1964. Über die Resistenzadaptation wechselwarmer Tiere an extreme Temperaturen und ihre Ursachen.Helgoländer wiss. Meeresunters. 9, 392–411.

    Google Scholar 

  • Salt, R. W., 1950. Time as a factor in the freezing of undercooled insects.Can. J. Res. (D)28, 285–291.

    Google Scholar 

  • —— 1959. Role of glycerol in the cold-hardening ofBracon cephi (Gahan).Can. J. Zool. 37, 59–69.

    Google Scholar 

  • —— 1961. A comparison of injury and survival of larvae ofCephus cinctus Nort after intracellular and extracellular freezing.Can. J. Zool. 39, 349–357.

    Google Scholar 

  • Scholander, P. F., Flagg, W., Hock, R. J. &Irving, L., 1953. Studies on the physiology of frozen plants and animals in the arctic.J. cell. comp. Physiol. 42 (Suppl. 1), 1–56.

    Google Scholar 

  • Smith, A. U., 1956. Studies on golden hamsters during cooling to and rewarming from body temperatures below 0° C. 1. Observations during chilling, freezing and supercooling.Proc. R. Soc. Lond. (B) 145, 391–407.

    Google Scholar 

  • Southward, A. J., 1958. Note on the temperature tolerance of some intertidal animals in relation to environmental temperatures and geographical distribution.J. mar. biol. Ass. U.K. 37, 49–66.

    Google Scholar 

  • Sprague, J. B., 1963. Resistance of four freshwater crustaceans to lethal high temperature and low oxygen.J. Fish. Res. Bd Can. 20, 387–415.

    Google Scholar 

  • Todd, M. E. &Dehnel, P. A., 1960. The influence of temperature and salinity on heat tolerance in two grapsoid crabs,Hemigrapsus nudus andHemigrapsus oregonensis.Biol. Bull. mar. biol. Lab., Woods Hole 118, 150–172.

    Google Scholar 

  • Vernon, H. M., 1899. The death temperature of certain marine organisms.J. Physiol. 25, 131–136.

    Google Scholar 

  • Walley, L. J., 1967. The cirral glands: a new type of epidermal gland in cirripedes.Crustaceana 12, 151–158.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crisp, D.J., Ritz, D.A. Changes in temperature tolerance ofBalanus balanoides during its life-cycle. Helgolander Wiss. Meeresunters 15, 98–115 (1967). https://doi.org/10.1007/BF01618612

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01618612

Keywords