Eur. J. Entomol. 99 (2): 259-266, 2002 | DOI: 10.14411/eje.2002.035
Interactions of water, ice nucleators and desiccation in invertebrate cold survival
- Biological Sciences Division, British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK; e-mail: wcb@bas.ac.uk
Four case studies are used to examine the relationships of water, ice nucleators and desiccation in the cold survival of invertebrates and the viability of frozen plant material: the freeze intolerant Antarctic springtail Cryptopygus antarcticus (Willem) (Collembola, Isotomidae), the freeze tolerant larvae of the fly Heleomyza borealis Boh. (Diptera: Heleomyzidae), the freeze intolerant Arctic springtail Onychiurus arcticus (Tullberg) (Collembola, Onychiuridae) and meristems of the currant Ribes ciliatum Humb. & Bonpl.(Grossulariaceae) from Mexico. Prevention of ice nucleation, lowering the water content by removal of osmotically active (freezable) water are critical features of the different cold survival strategies of the three species of invertebrates. In C. antarcticus, which desiccates rapidly by losing water via the cuticle to the atmosphere, the number of ice nucleators (and their activity) increases with lowered ambient temperature. During prolonged cold exposure ice nucleators are masked, but re-activated rapidly by water uptake in this species. Larval H. borealis do not readily desiccate and conserve their body water, 20-25% of it being bound (osmotically inactive). Experiments showed that a high proportion (c. 80%) of slowly cooled larvae survived exposure to -60°C. By comparison O. arcticus is able to sustain up to 40% loss of its body water and desiccation lowers its supercooling point to promote over winter survival. Dehydration leading to partial vitrification of currant (R. ciliatum) meristems improves their viability after cryopreservation in liquid nitrogen. From this comparison of four biological systems, it is concluded that the role of water and its activity at sub-zero temperatures are fundamental to the survival of freezing conditions by all the species studied. Although similar features exist in the four systems, no common basic mechanism was found.
Keywords: Cold, survival, water, ice nucleators, desiccation, Cryptopygus antarcticus, Heleomyza borealis, Onychiurus arcticus, Ribes ciliatum, vitrification, cryopreservation
Received: November 23, 2001; Revised: June 18, 2002; Accepted: June 20, 2002; Published: June 30, 2002 Show citation
References
- Benson E.E. (ed) 1999: Plant Conservation Biotechnology. Taylor and Francis, London, 309 pp
Go to original source...
- Block W. 1995: Insects and freezing. Science Progress 78: 349-372
- Block W. & Harrisson P.M. 1995: Collembolan water relations and environmental change in the maritime Antarctic. Global Change Biology 1: 347-359
Go to original source...
- Block W., Webb N.R., Coulson S., Hodkinson I.D. & Worland M.R. 1994: Thermal adaptations in the Arctic collembolan Onychiurus arcticus (Tullberg). J. Insect Physiol. 40: 715-722
Go to original source...
- Block W. & Worland M.R. 2001: Experimental studies of ice nucleation in an Antarctic springtail (Collembola: Isotomidae). Cryobiology 42: 176-181
Go to original source...
- Cannon R.J.C., Block W. & Collett G.D. 1985: Loss of supercooling ability in Cryptopygus antarcticus (Collembola: Isotomidae) associated with water uptake. CryoLetters 6: 73-80
- Coulson S.J., Hodkinson I.D., Strathdee A.T., Block W., Webb N.R., Bale J.S. & Worland M.R. 1995: Thermal environments of Arctic soil organisms during winter. Arctic & Alpine Res. 27: 364-370
Go to original source...
- Dumet D., Block W., Worland M. R., Reed B. M. & Benson E. E. 2000a: Profiling cryopreservation protocols for Ribes ciliatum using Differential Scanning Calorimetry. CryoLetters 21: 367-378
- Dumet D., Chang Y., Reed B.M. & Benson E.E. 2000b: Replacement of cold acclimatization with high sucrose pretreatment in black currant cryopreservation. In: Engelmann F. & Takagi H. (eds): Current Research Progress and its Applications. IPGRI, Rome, pp. 385-387
- Hodkinson I.D., Webb N.R., Bale J.S. & Block W. 1999: Hydrology, water availability and tundra ecosystem function in a changing climate: the need for a closer integration of ideas? Global Change Biology 5: 359-369
Go to original source...
- Holmstrup M. & Somme L. 1998: Dehydration and cold hardiness in the Arctic collembolan Onychiurus arcticus Tullberg 1876. J. Comp. Physiol. B, 168: 197-203
Go to original source...
- Holmstrup M. & Westh P. 1994: Dehydration of earthworm cocoons exposed to cold: a novel cold hardiness mechanism. J. Comp. Physiol. B, 164: 312-315
Go to original source...
- Kennedy A.D. 1993: Water as a limiting factor in the Antarctic terrestrial environment: a biogeographical synthesis. Arctic & Alpine Res. 25: 308-315
Go to original source...
- Lee R.E. 1991: Principles of insect low temperature tolerance. In: Lee R.E. & Denlinger D.L. (eds): Insects at Low Temperature. London, Chapman & Hall, pp. 17-46
Go to original source...
- Luo J. & Reed B.M. 1997: Abscisic-acid responsive protein, bovine serum albumin, and proline pretreatments improve recovery of in vitro currant shoot-tip meristems and callus preserved by vitrification. Cryobiology 34: 240-250
Go to original source...
- Vali G. 1971: Quantitative evaluation of experimental results on the heterogeneous freezing nucleation of supercooled liquids. J. Atmospheric Sci. 28: 402-409
Go to original source...
- Worland M.R. 1996: The relationship between water content and cold tolerance in the Arctic collembolan Onychiurus arcticus (Collembola: Onychiuridae). Eur. J. Entomol. 93: 341-348
- Worland M.R., Grubor-Lajsic G. & Montiel M.O. 1998: Partial desiccation induced by sub-zero temperatures as a component of the survival strategy of the Arctic collembolan Onychiurus arcticus (Tullberg). J. Insect Physiol. 44: 211-219
Go to original source...
- Worland M. R., Block W. & Grubor-Lajsic G. 2000: Survival of Heleomyza borealis (Diptera, Heleomyzidae) larvae down to -60°C. Physiol. Entomol. 25: 1-5
Go to original source...
- Zachariassen K.E. 1985: Physiology of cold tolerance in insects. Physiol. Rev. 65: 799-832
Go to original source...
- Zachariassen K.E. & Husby J.A. 1982: Antifreeze effect of thermal hysteresis agents protects highly supercooled insects. Nature 298: 865-867
Go to original source...
- Zachariassen K.E. & Kristiansen E. 2000: Ice nucleation and antinucleation in nature. Cryobiology 41: 257-279
Go to original source...
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