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. 2019 Feb 27;86(1-2):77–101. doi: 10.3184/003685003783238680

Water or Ice? — the Challenge for Invertebrate Cold Survival

William Block 1
PMCID: PMC10368336  PMID: 12838605

Abstract

The ecophysiology of cold tolerance in many terrestrial invertebrate animals is based on water and its activity at low temperatures, affecting cell, tissue and whole organism functions. The normal body water content of invertebrates varies from 40 to 90% of their live weight, which is influenced by water in their immediate environment, especially in species with a water vapour permeable cuticle. Water gain from, or loss to, the surrounding atmosphere may affect animal survival, but under sub-zero conditions body water status becomes more critical for overwinter survival in many species. Water content influences the supercooling capacity of many insects and other arthropods. Trehalose is known to maintain membrane integrity during desiccation stress in several taxa. Dehydration affects potential ice nucleators by reducing or masking their activity and a desiccation protection strategy has been detected in some species. When water crystallises to ice in an animal it greatly influences the physiology of nearby cells, even if the cells remain unfrozen. A proportion of body water remains unfrozen in many cold hardened invertebrates when they are frozen, which allows basal metabolism to continue at a low level and aids recovery to normal function when thawing occurs. About 22% of total body water remains unfrozen from calculations using differential scanning calorimetry (compared with ca 19% in food materials). The ratio of unfrozen to frozen water components in insects is 1:4 (1:6 for foods). Such unfrozen water may aid recovery of freezing tolerant species after a freezing exposure. Rapid changes in cold hardiness of some arthropods may be brought about by subtle shifts in body water management. It is recognised that cold tolerance strategies of many invertebrates are related to desiccation resistance, and possibly to mechanisms inherent in insect diapause, but the role of water is fundamental to them all. Detailed experimental studies are needed to provide information which will allow a more complete and coherent understanding of the behaviour of water in biological systems and aid the cryopreservation of a wide range of biological material.

Keywords: cold tolerance, invertebrate survival

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References

  • 1.Block W. (1995) Insects and freezing. Science Progress, 78, 349–372. [Google Scholar]
  • 2.Réamur R.A. (1734) Memoires pour servir à l'histoire des insectes, tome 2, 170, pp. 141–147. d'Imprimerie Royal, Paris. [Google Scholar]
  • 3.Bale J.S. (1993) Classes of insect cold hardiness. Funct. Ecol., 7, 751–753. [Google Scholar]
  • 4.Block W. (1990) Cold tolerance of insects and other arthropods. Phil. Trans. R. Soc. B, 326, 613–633. [Google Scholar]
  • 5.Wharton D.A., & Ferns D.J. (1995) Survival of intracellular freezing by the Antarctic nematode Panagrolaimus davidi. J. expt. Biol. 198, 1381–1387. [DOI] [PubMed] [Google Scholar]
  • 6.Wasylyk J.M., Tice A.R., & Baust J.G. (1988) Partial glass formation: a novel mechanism of insect cryoprotection. Cryobiology, 25, 451–458. [Google Scholar]
  • 7.Zachariassen K.E. (1985) Physiology of cold tolerance in insects. Physiol. Rev., 65, 799–832. [DOI] [PubMed] [Google Scholar]
  • 8.Hadley N.F. (1994) Water relations of terrestrial arthropods. Academic Press, London. [Google Scholar]
  • 9.Drost-Hansen W., & Singleton J.L. (1992) Our aqueous heritage: evidence for vicinal water in cells. In: Bittar E.E. (ed.) Chemistry of the living cell. Fundamentals of medical cell biology, 3A, 157–180. JAI Press, Greenwich, Connecticut. [Google Scholar]
  • 10.Zachariassen K.E., Hammel H.T., & Schmidek W. (1979) Osmotically inactive water in relation to tolerance to freezing in Eleodes blanchardi beetles. Comp. Biochem. Physiol., 63A, 203–206. [Google Scholar]
  • 11.Bachmetjew P. (1899) Über die temperatur der Insekten nach Beobachtungen in Bulgarien. Z wiss. Zool., 66, 521–604. [Google Scholar]
  • 12.Block W. (1996) Cold or drought–the lesser of two evils for terrestrial arthropods? Eur. J. Entomol., 93, 325–339. [Google Scholar]
  • 13.Bayley M., & Holmstrup M. (1999) Water vapor absorption in arthropods by accumulation of myoinositol and glucose. Science, N.Y., 285, 1909–1911. [DOI] [PubMed] [Google Scholar]
  • 14.Block W., Harrisson P.M., & Vannier G. (1990) A comparative study of patterns of water loss from two Antarctic springtails (Insecta, Ciollembola). J. Insect Physiol., 36, 181–187. [Google Scholar]
  • 15.Harrisson P.M., Block W., & Worland M.R. (1990) Moisture and temperature dependent changes in the cuticular permeability of the Antarctic springtail Parisotoma octooculata (Willem). Rev. Écol. Biol. Sol., 27, 435–448. [Google Scholar]
  • 16.Todd C.M., & Block W. (1997) Responses to desiccation in four coleopterans from sub-Antarctic South Georgia J. Insect Physiol., 43, 905–913. [DOI] [PubMed] [Google Scholar]
  • 17.Pugh P.J.A. (1994) Supercooling points and water content in Acari. Acta Oecol., 15, 71–77. [Google Scholar]
  • 18.Block W., & Harrisson P.M. (1995) Collembolan water relations and environmental change in the maritime Antarctic. Global Change Biol., 1, 347–359. [Google Scholar]
  • 19.Worland M.R., & Block W. (1986) Survival and water loss in some Antarctic arthropods. J. Insect Physiol., 32, 579–584. [Google Scholar]
  • 20.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. [Google Scholar]
  • 21.Worland M.R., Grubor-Lajsic G., & Montiel P.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. [DOI] [PubMed] [Google Scholar]
  • 22.Crowe J.H., Crowe L.M., Carpenter J.F., & Aurell Wistrom C. (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem. J., 242, 1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Kawai H., Sakurai M., Inoue Y., Chûjô R., & Kobayashi S. (1992) Hydration of oligosaccharides: anomalous hydration ability of trehalose. Cryobiology, 29, 599–606. [DOI] [PubMed] [Google Scholar]
  • 24.Cannon R.J., Block W., & Collett G.D. (1985) Loss of supercooling ability in Cryptopygus antarcticus (Collembola: Isotomidae) associated with water uptake. Cryo-Letters, 6, 73–80. [Google Scholar]
  • 25.Cannon R.J. (1986) Diet and acclimation effects on the cold tolerance and survival of an Antarctic springtail. Br. Antarct. Surv. Bull., 71, 19–30. [Google Scholar]
  • 26.Sastry S. (2002) Sculpting ice out of water. Nature, (Lond.), 416, 376–377. [DOI] [PubMed] [Google Scholar]
  • 27.Clarke C.J., Buckley S.L., & Lindner N. (2002) Ice structuring proteins–a new name for antifreeze proteins. CryoLetters, 23, 89–92. [PubMed] [Google Scholar]
  • 28.Vali G. (1995) Principles of ice nucleation. In: Lee R., Warren G.J., & Gusta L.V. (eds), Biological ice nucleation and its applications, pp. 1–28. APS Press, St Paul, Minnesota. [Google Scholar]
  • 29.Matsumoto M., Saito S., & Ohmine I. (2002) Molecular dynamics simulation of ice nucleation and growth process leading to water freezing. Nature, (Lond.), 416, 409–413. [DOI] [PubMed] [Google Scholar]
  • 30.Zachariassen K.E., & Kristiansen E. (2000) Ice nucleation and antinucleation in nature. Cryobiology, 41, 257–279. [DOI] [PubMed] [Google Scholar]
  • 31.DeVries A.L. (1971) Glycoproteins as biological antifreeze agents in Antarctic fishes. Science, N.Y., 172, 1152–1155. [DOI] [PubMed] [Google Scholar]
  • 32.Liou Y-C., Tocilj A., Davies P.L., & Jia Z. (1000) Mimicry of ice structure by surface hydroxyls and water of the β-helix antifreeze protein. Nature, (Lond.), 406, 322–324. [DOI] [PubMed] [Google Scholar]
  • 33.Graether S.P., Kuiper M.J., Gagnés S.M., Walker V.K., Jia Z., Sykes B.D., & Davies P.L. (2000) β-Helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect. Nature, (Lond.), 406, 325–328. [DOI] [PubMed] [Google Scholar]
  • 34.Block W. (1994) Differential scanning calorimetry in ecophysiological research. Acta Oecol., 15, 13–22. [Google Scholar]
  • 35.Knight J.D., Bale J.S., Franks F., Mathias S.F., & Baust J.G. (1986) Insect cold hardiness: supercooling points and pre-freeze mortality. Cryo-Letters, 7, 194–203. [Google Scholar]
  • 36.Hansen T.N., & Baust J.G. (1989) Differential scanning calorimetric analysis of Tenebrio molitor antifreeze protein activity. Cryobiology, 26, 383–388. [DOI] [PubMed] [Google Scholar]
  • 37.Block W. (2002) Interactions of water, ice nucleators and desiccation in invertebrate cold survival. Eur. J. Entomol., 99, 259–266. [Google Scholar]
  • 38.Worland M.R., & Lukesova A. (2001) The application of differential scanning calorimetry and ice nucleation spectrometry to ecophysiological studies of algae. Nova Hedwigia, 123, 571–583. [Google Scholar]
  • 39.Dumet D., Block W., Worland R., Reed B.M., & Benson E.E. (2000) Profiling cryopreservation protocols for Ribes ciliatum using differential scanning calorimetry. CryoLetters, 21, 367–378. [PubMed] [Google Scholar]
  • 40.McAllen R., & Block W. (1997) Aspects of the cryobiology of the intertidal harpacticoid copepod Tigriopus brevicornis (O.F. Müller). Cryobiology, 35, 309–317. [DOI] [PubMed] [Google Scholar]
  • 41.Wharton D.A., & Block W. (1997) Differential scanning calorimetry studies on an Antarctic nematode (Panagrolaimus davidi) which survives intracellular freezing. Cryobiology, 34, 114–121. [DOI] [PubMed] [Google Scholar]
  • 42.Block W., & Bauer R. (2000) DSC studies of freezing in terrestrial enchytraeids (Annelida: Oligochaeta). CryoLetters, 21, 99–106. [PubMed] [Google Scholar]
  • 43.Holmstrup M., & Westh P. (1994) Dehydration of earthworm cocoons exposed to cold: a novel cold hardiness mechanism. J. comp. Physiol. B, 164, 312–315. [Google Scholar]
  • 44.Westh P., & Kristensen R.M. (1992) Ice formation in the free-tolerant eutardigrades Adorybiotus coronifer and Amphibolus nebulosus studied by differential scanning calorimetry. Pol. Biol., 12, 693–699. [Google Scholar]
  • 45.Dumet D., & Benson E.E. (2000) The use of physical and biochemical studies to elucidate and reduce cryopreservation-induced damage in hydrated/desiccated plant germplasm. In: Engelmann F., and Takagi H. (eds.) Cryopreservation of tropical plant germplasm, current progress and applications, pp. 43–56. Japanese International Research Centre for Agricultural Sciences, Tsukuba Japan and International Plant Genetic Resources Institute, Rome, Italy. [Google Scholar]
  • 46.Benson E.E. (ed.) (1999) Plant conservation biotechnology. Taylor & Francis, London. [Google Scholar]
  • 47.Pritchard H.W., & Manger K.R. (1998) A calorimetric perspective on desiccation stress during preservation procedures with recalcitrant seeds of Quercus robur L. Cryo-Letters, Supplement no. 1, (March 1998), 23–30. [Google Scholar]
  • 48.Williams R.J., & Hirsch A.G. (1986) On the freezing of water and the melting of ice in scanning calorimeters. Cryo-Letters, 7, 146–161. [Google Scholar]
  • 49.Franks F. (1986) Unfrozen water: yes; unfreezable water: hardly; bound water: certainly not. An editorial note. Cryo-Letters, 7, 207. [Google Scholar]
  • 50.Wolfe J., Bryant G., & Koster K.L. (2002) What is ‘unfreezable water’, how unfreezable is it and much is there? CryoLetters, 23, 157–166. [PubMed] [Google Scholar]
  • 51.Aktas N., Tülek Y., & Gökalp H.Y. (1997) Determination of freezable water content of beef semimembranous muscle, DSC study. J. Therm. Anal., 48, 259–266. [Google Scholar]
  • 52.Roos Y.H. (1986) Phase transitions and unfreezable water content of carrots, reindeer meat and white bread studied using differential scanning calorimetry. J. Food Sci., 51, 684–686. [Google Scholar]
  • 53.Block W., Wharton D.A., & Sinclair B. (1998) Cold tolerance of a new Zealand alpine cockroach, Celatoblatta quinquemaculata (Dictyoptera, Blattidae). Physiol. Ent., 23, 1–6. [DOI] [PubMed] [Google Scholar]
  • 54.Worland M.R., Block W., & Grubor-Lajsic G. (2000) Survival of Heleomyza borealis (Diptera, Heleomyzidae) larvae down to −60°C. Physiol. Ent., 25, 1–5. [Google Scholar]
  • 55.Storey K.B., & Storey J.M. (1988) Freeze tolerance in animals. Physiol. Rev., 68, 27–84. [DOI] [PubMed] [Google Scholar]
  • 56.Bauer R., Worland M.R., & Block W. (2001) Experimental studies on cold survival of enchytraeid cocoons. Pedobiologia, 45, 561–571. [Google Scholar]
  • 57.Storey K.B., Baust J.G., & Buescher P. (1981) Determination of water “bound” by soluble subcellular components during low temperature acclimation of the overwintering gall fly larva, Eurosta solidaginis. Cryobiology, 18, 315–321. [DOI] [PubMed] [Google Scholar]
  • 58.Sano F., Asakawa N., Inoue Y., & Sakurai M. (1999) A dual role for intracellular trehalose in the resistance of yeast cells to water stress. Cryobiology, 39, 80–87. [DOI] [PubMed] [Google Scholar]
  • 59.Ring R.A., & Danks H.V. (1994) Desiccation and cryoprotection: overlapping adaptations. Cryo-Letters, 15, 181–190. [Google Scholar]
  • 60.Pullin A.S. 1996. Physiological relationships between insect diapause and cold tolerance: coevolution or coincidence? Eur. J. Entomol., 93, 121–129. [Google Scholar]
  • 61.Holmstrup M., Bayley M., & Ramløv H. (2002) Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable Arctic invertebrates. Proc. natn. Acad. Sci. U.S.A., 99, 5716–5720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Holmstrup M., & Sømme L. (1998) Dehydration and cold hardiness in the Arctic collembolan Onychiurus arcticus Tullberg 1876. J. comp. Physiol. B, 168, 197–203. [Google Scholar]
  • 63.Block W., Webb N.R., Coulson S.J., Hodkinson I.D., & Worland M.R. (1994) Thermal adaptation in the Arctic collembolan Onychiurus arcticus (Tullberg). J. Insect Physiol., 40, 715–722. [Google Scholar]
  • 64.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. Arct. alp. Res., 27, 364–370. [Google Scholar]
  • 65.Bale J.S., Worland M.R., & Block W. (2001) Effects of summer frost exposures on the cold tolerance strategy of a sub-Antarctic beetle. J. Insect Physiol., 47, 1161–1167. [DOI] [PubMed] [Google Scholar]
  • 66.Worland M.R., & Convey P. (2001) Rapid cold hardening in Antarctic microarthropods. Funct. Ecol., 15, 515–524. [Google Scholar]
  • 67.Bowles D.J., Lillford P.J., Rees D.A., & Shanks I.A. (eds.) (2002) Coping with cold: the molecular and structural biology of cold stress survivors. Phil. Trans. R. Soc. Ser. B, 357, 827–956. [Google Scholar]

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