Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-27T14:43:10.891Z Has data issue: false hasContentIssue false
  • English
  • Français

Factors Controlling Cold Tolerance and Breeding in Balanus Balanoides

Published online by Cambridge University Press:  11 May 2009

D. J. Crisp  and
A. H. Lewis
D. J. Crisp
Affiliation:
N.E.R.C. Unit of Marine Invertebrate Biology, Marine Science Laboratories, Menai Bridge, Gwynedd, LL EH
A. H. Lewis
Affiliation:
N.E.R.C. Unit of Marine Invertebrate Biology, Marine Science Laboratories, Menai Bridge, Gwynedd, LL EH
Get access Rights & Permissions [Opens in a new window]

Extract

Measurements during autumn and winter of the lower median lethal temperature of the barnacle Balanus balanoides (L.) under natural and modified environmental conditions in field and laboratory, show that the cold resistant state is advanced by three factors: short day photoperiod, reduced food assimilation and reduced temperature. Their relative efficacy is in that order.

These factors combine in promoting breeding and the acquisition of the cold tolerant state during autumn and winter. Although normally associated, breeding and cold tolerance are not mutually dependent; the one can be induced without the other under abnormal conditions.

Similar measurements made in the spring show that only a single factor is required to terminate the cold tolerant state — resumption of food assimilation. If feeding is discontinued in the spring, however, the cold tolerant state tends to return, but animals that have bred do not breed again until the following autumn.

Of the three well established mechanisms for seasonal cold tolerance — production of substances to cause freezing hysteresis, production of cryoprotective agents, and nucleating agents to promote freezing in the intercellular compartment — only the last can be entertained since the cold tolerant animal survives some 80% of the body fluids being converted to ice. The cold tolerant condition may also relate to higher levels of polyunsaturated fatty acids being present in the membrane lipid fraction in winter, so rendering cell membranes less prone to damage by ice crystals.

The suggestion is made that normal metabolic activity and tolerance of low chemical potential of water - the common factor in freezing and desiccation - are not compatible.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 64 , Issue 1 , February 1984 , pp. 125 - 145
Copyright
Copyright © Marine Biological Association of the United Kingdom 1984

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Asahina, E. 1966. Freezing and frost resistance in insects. In Cryobiology (ed. H. T. Merryman), pp. 451–486. Academic Press.Google Scholar
Asahina, E. 1969. Frost resistance in insects. Advances in Insect Physiology, 6, 1–49.Google Scholar
Aunaas, T. 1982. Nucleating agents in the haemolymph of intertidal invertebrates tolerant to freezing. Cryoletters, 3.Google Scholar
Barnes, H. 1958. Regarding the southern limits of Balanus balanoides (L.). Oikos, 9, 129–157.Google Scholar
Barnes, H. 1963. Light, temperature and the breeding of Balanus balanoides. Journal of the Marine Biological Association of the United Kingdom, 43, 717–727.Google Scholar
Barnes, H. & Barnes, M. 1967. The effect of starvation and feeding on the time of production of egg masses in the boreo-arctic cirripede, Balanus balanoides (L.). Journal of Experimental Marine Biology and Ecology, 1, 1–6.CrossRefGoogle Scholar
Clare, A. S.Walker, G.Holland, D. L. & Crisp, D. J. 1982. Barnacle egg hatching: a novel role for a prostaglandin-like compound. Marine Biology Letters, 3, 113–120.Google Scholar
Cook, P. A. & Gabbott, P. A. 1972. Seasonal changes in the biochemical composition of the adult barnacle, Balanus balanoides, and the possible relationships between biochemical composition and cold-tolerance. Journal of the Marine Biological Association of the United Kingdom, 52, 805–825.Google Scholar
Cook, P. A. & Lewis, A. H. 1971. Acquisition and loss of cold-tolerance in adult barnacles {Balanus balanoides) kept under laboratory conditions. Marine Biology, 9, 26–30.Google Scholar
Crisp, D. J. 1956. A substance promoting hatching and liberation of young cirripedes. Nature, London, 178, 263.Google Scholar
Crisp, D. J. 1957. Effect of low temperature on the breeding of marine animals. Nature, London, 179, 1138–1139.Google Scholar
Crisp, D. J. 1959a. Factors influencing the time of breeding of Balanus Balanoides. Oikos, 10, 275–298.Google Scholar
Crisp, D. J. 1959b. The rate of development of Balanus balanoides (L.) embryos in vitro. Journal of Animal Ecology, 28, 119–132.CrossRefGoogle Scholar
Crisp, D. J. 1964. An assessment of plankton grazing by barnacles. In Grazing in Terrestrial and Marine Environments. Proceedings of the Fourth Symposium of the British Ecological Society (ed. D. J. Crisp), pp. 251–264. Blackwell.Google Scholar
Crisp, D. J. 1965. Observations on the effects of climate and weather on marine communities. In Biological Significance of Climatic Changes in Britain (ed. C. G. Johnson and L. P. Smith), pp. 63–77. Academic Press.Google Scholar
Crisp, D. J. & Clegg, D. J. 1960. The induction of the breeding condition in Balanus balanoides. Oikos, 11, 265–275.Google Scholar
Crisp, D. J.Davenport, J. & Gabbott, P. A. 1977. Freezing tolerance in Balanus balanoides. Comparative Biochemistry and Physiology, 57A, 359–361.CrossRefGoogle Scholar
Crisp, D. J. & Patel, B. S. 1960. The moulting cycle in Balanus balanoides (L.). Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 118, 31–47.Google Scholar
Crisp, D. J. & Patel, B. S. 1969. Environmental control of the breeding of three boreo-arctic cirripedes. Marine Biology, 2, 283–295.Google Scholar
Crisp, D. J. & Ritz, D. A. 1967. Changes in temperature tolerance of Balanus balanoides during its life-cycle. Helgoländer wissenschaftliche Meeresuntersuchungen, 15, 98–115.Google Scholar
Crisp, D. J. & Southward, A. J. 1961. Different types of cirral activity of barnacles. Philosophical Transactions of the Royal Society (B), 243, 271–307.Google Scholar
Crisp, D. J. & Spencer, C. P. 1958. The control of the hatching process in barnacles. Proceedings of the Royal Society (B), 148, 278–299.Google Scholar
Devries, A. L. 1980. Biological antifreezes and survival in freezing environments. In Animals and Environmental Fitness, vol. 1 (ed. R. Gilles), pp. 583–607. Pergamon Press.Google Scholar
Duman, J. G. 1977. Role of macromolecular antifreeze in the darkling beetle, Meracantha contracta. Journal of Comparative Physiology, 115, 279–286.CrossRefGoogle Scholar
Duman, J. G. 1980. Factors involved in the overwintering survival of the freeze tolerant beetle Dendroides canedinsis. Journal of Comparative Physiology, 136, 653–659.Google Scholar
Foster, B. A. 1971. Desiccation as a factor in the intertidal zonation of barnacles. Marine Biology, 8, 12–29.Google Scholar
Gardner, D. & Riley, J. P. 1972. Seasonal variations in the component fatty acid distributions of the lipids of Balanus balanoides. Journal of the Marine Biological Association of the United Kingdom, 52, 839–845.CrossRefGoogle Scholar
Heilbrunn, L. V. 1945. An Outline of General Physiology, 2nd edition, xii, 748 pp. W. B. Saunders Co.Google Scholar
Levitt, J. 1966. Winter hardiness in plants. In Cryobiology (ed. H. T. Merryman), pp. 495–563. Academic Press.Google Scholar
Mazur, P. 1966. Physical and chemical basis of injury in single celled micro organisms subjected to freezing and thawing. In Cryobiology (ed. H. T. Merryman,) pp. 214–315. Academic Press.Google Scholar
Murphy, D. J. 1977. Metabolic and tissue solute changes associated with changes in the freezing tolerance of the bivalve mollusc Modiolus demissus. Journal of Experimental Biology, 69, 1–12.CrossRefGoogle Scholar
Ring, R. A. 1980. Insects and their cells. In Low Temperature Preservation in Medicine and Biology (ed. M. J. Ashwood-Smith and J. Farrant,) pp. 187–217. London: Pitman Medical Ltd.Google Scholar
Ritz, D. A. & Crisp, D. J. 1970. Seasonal changes in feeding rate in Balanus balanoides. Journal of the Marine Biological Association of the United Kingdom, 50, 223–240.CrossRefGoogle Scholar
Salt, R. W. 1961. Principles of insect cold hardiness. Annual Review of Entomology, 6, 55–74.Google Scholar
SøMme, L. 1966. Seasonal changes in the freezing-tolerance of some intertidal animals. Nytt magazinfor zoologi, 13, 52–55.Google Scholar
Tighe-Ford, D. J. 1967. Possible mechanism for the endocrine control of breeding in a cirripede. Nature, London, 216, 920–921.Google Scholar
Tooke, N. E.Holland, D. L. & Gabbott, P. A. 1982. The role of membrane lipids in the freezing tolerance of intertidal barnacles. Cryoletters, 3, 288.Google Scholar
Zachariassen, K. E. 1980. Role of polyols and nucleating agents in cold-hardy beetles. Journal of Comparative Physiology, 140, 227–234.Google Scholar
Zachariassen, K. E. & Hammel, H. T. 1976. Nucleating agents in the haemolymph of insects tolerant to freezing. Nature, London, 262, 285–287.CrossRefGoogle ScholarPubMed
Zachariassen, K. E. & Husby, J. A. 1982. Stabilisation of highly supercooled insects by thermal hysteresis antifreeze agents. Cryoletters, 3, 316.Google Scholar