Ice Formation in Living Organisms

  • Hans RamløvEmail author
  • Dennis Steven Friis


This chapter describes the consequences of cold exposure and ice formation on both the cellular, tissue and the organismal level in cold tolerant ectothermic organisms. This includes the direct implication of cold “per se” on various parameters such as pH, membrane fluidity and phase transitions, ionic gradients, metabolism, cold denaturation of proteins, ice nucleation, ice growth, freezing-induced cellular dehydration, the role of aquaporins and the mechanical stress caused by ice, while referring to the different aspects described in the previous chapter on ice in general. Defensive/preventive adaptations and mechanisms of the organisms are described as well, along with a description of freeze tolerance and freeze avoidance. The synthesis and mechanisms of action of low molecular weight cryoprotectants as well as their distribution are discussed. High molecular weight cryoprotectants are also described concluding with the introduction of the AFPs.


Cold damage Rapid cold hardening Freeze tolerance Freeze avoidance Membranes Cold denaturation Aquaporins Low molecular weight cryoprotectants 


  1. Alejevski F (2012) Seasonal transcription of antifreeze protein genes in larvae of Rhagium mordax and its expression in Drosophila melanogaster. M.Sc. Thesis. Department of Science and Environment, Roskilde UniversityGoogle Scholar
  2. Andersen HD, Wang C, Arleth L, Peters GH, Westh P (2011) Reconciliation of opposing views on membrane-sugar interactions. Proc Natl Acad Sci U S A 108:1874–1878PubMedPubMedCentralGoogle Scholar
  3. Angell CA (1982) Supercooled water. In: Franks F (ed) Water and aqueous solutions at subzero temperatures. Springer, Boston, MA, pp 1–81Google Scholar
  4. Angell CA (1983) Supercooled water. Annu Rev Phys Chem 34:593–630Google Scholar
  5. Anishkin A, Loukin SH, Teng J, Kung C (2014) Feeling the hidden mechanical forces in lipid bilayer is an original sense. Proc Natl Acad Sci U S A 111:7898–7905PubMedPubMedCentralGoogle Scholar
  6. Ansart A, Vernon P (2003) Cold hardiness in molluscs. Acta Oecol 24:95–102Google Scholar
  7. Avanti C, Saluja V, van Streun EL, Frijlink HW, Hinrichs WL (2014) Stability of lysozyme in aqueous extremolyte solutions during heat shock and accelerated thermal conditions. PLoS One 9:e86244PubMedPubMedCentralGoogle Scholar
  8. Bahrndorff S, Tunnacliffe A, Wise MJ, McGee B, Holmstrup M, Loeschcke V (2009) Bioinformatics and protein expression analyses implicate LEA proteins in the drought response of Collembola. J Insect Physiol 55:210–217PubMedGoogle Scholar
  9. Bayley JS, Winther CB, Andersen MK, Gronkjaer C, Nielsen OB, Pedersen TH, Overgaard J (2018) Cold exposure causes cell death by depolarization-mediated Ca(2+) overload in a chill-susceptible insect. Proc Natl Acad Sci U S A 115:E9737–E9744PubMedPubMedCentralGoogle Scholar
  10. Ben-Naim A (2013) Theory of cold denaturation of proteins. Adv Biol Chem 3:11Google Scholar
  11. Bennett VA, Sformo T, Walters K, Toien O, Jeannet K, Hochstrasser R, Pan Q, Serianni AS, Barnes BM, Duman JG (2005) Comparative overwintering physiology of Alaska and Indiana populations of the beetle Cucujus clavipes (Fabricius): roles of antifreeze proteins, polyols, dehydration and diapause. J Exp Biol 208:4467–4477PubMedGoogle Scholar
  12. Berman DI, Meshcheryakova EN, Bulakhova NA (2016) Extreme negative temperatures and body mass loss in the Siberian salamander (Salamandrella keyserlingii, amphibia, hynobiidae). Dokl Biol Sci 468:137–141PubMedGoogle Scholar
  13. Bigg EK (1953) The supercooling of water. Proc Phys Soc Sect B 66:688–694Google Scholar
  14. Bredow M, Walker VK (2017) Ice-binding proteins in plants. Front Plant Sci 8:2153–2153PubMedPubMedCentralGoogle Scholar
  15. Brown DJ, Sönnichsen FD (2002) The structure of fish antifreeze proteins. In: Fish antifreeze proteins, vol 1. World Scientific, River Edge, NJ, pp 109–138Google Scholar
  16. Calderon S, Holmstrup M, Westh P, Overgaard J (2009) Dual roles of glucose in the freeze-tolerant earthworm Dendrobaena octaedra: cryoprotection and fuel for metabolism. J Exp Biol 212:859–866PubMedGoogle Scholar
  17. Cannon RJC, Block W (1988) Cold tolerance of microarthropods. Biol Rev 63:23–77Google Scholar
  18. Cheng CC, DeVries AL (1991) The role of antifreeze glycopeptides and peptides in the freezing avoidance of cold-water fish. In: di Prisco G (ed) Life under extreme conditions. Springer, Berlin, pp 1–14Google Scholar
  19. Cheng CCM, DeVries AL (2002) Origins and evolution of fish antifreeze proteins. In: Fish antifreeze proteins, vol 1. World Scientific, River Edge, NJ, pp 83–107Google Scholar
  20. Clerc SG, Thompson TE (1995) Permeability of dimyristoyl phosphatidylcholine/dipalmitoyl phosphatidylcholine bilayer membranes with coexisting gel and liquid-crystalline phases. Biophys J 68:2333–2341PubMedPubMedCentralGoogle Scholar
  21. Cossins AR, Murray PA, Gracey AY, Logue J, Polley S, Caddick M, Brooks S, Postle T, Maclean N (2002) The role of desaturases in cold-induced lipid restructuring. Biochem Soc Trans 30:1082–1086PubMedGoogle Scholar
  22. Costanzo JP, Claussen DL (1990) Natural freeze tolerance in the terrestrial turtle, Terrapene carolina. J Exp Zool 254:228–232Google Scholar
  23. Costanzo JP, Lee RE Jr (1995) Supercooling and ice nucleation in vertebrate ectotherms. APS Press, St. Paul, pp 221–237Google Scholar
  24. Costanzo JP, Lee RE Jr (2013) Avoidance and tolerance of freezing in ectothermic vertebrates. J Exp Biol 216:1961–1967PubMedGoogle Scholar
  25. Costanzo JP, Wright MF, Lee RE (1992) Freeze tolerance as an overwintering adaptation in Cope’s grey treefrog (Hyla chrysoscelis). J Exp Zool 283(3):221–225Google Scholar
  26. Crowe JH, Crowe LM, Chapman D (1984a) Infrared spectroscopic studies on interactions of water and carbohydrates with a biological membrane. Arch Biochem Biophys 232:400–407PubMedGoogle Scholar
  27. Crowe JH, Whittam MA, Chapman D, Crowe LM (1984b) Interactions of phospholipid monolayers with carbohydrates. Biochim Biophys Acta 769:151–159PubMedGoogle Scholar
  28. DeVries AL, Wohlschlag DE (1969) Freezing resistance in some Antarctic fishes. Science 163:1073–1075PubMedGoogle Scholar
  29. Doelling AR, Griffis N, Williams JB (2014) Repeated freezing induces oxidative stress and reduces survival in the freeze-tolerant goldenrod gall fly, Eurosta solidaginis. J Insect Physiol 67:20–27PubMedGoogle Scholar
  30. Duman JG (1977) The role of macromolecular antifreeze in the darkling beetle, Meracantha contracta. J Comp Physiol 115:279–286Google Scholar
  31. Duman JG (1980) Factors involved in overwintering survival of the freeze tolerant beetle, Dendroides canadensis. J Comp Physiol 136:52–59Google Scholar
  32. Duman JG (1982) Insect antifreezes and ice-nucleating agents. Cryobiology 19:613–627PubMedGoogle Scholar
  33. Duman JG (2002) The inhibition of ice nucleators by insect antifreeze proteins is enhanced by glycerol and citrate. J Comp Physiol B 172:163–168PubMedGoogle Scholar
  34. Duman JG, Devries AL (1974) Freezing resistance in winter flounder Pseudopleuronectes americanus. Nature 247:237–238Google Scholar
  35. Duman J, Horwath K (1983) The role of hemolymph proteins in the cold tolerance of insects. Annu Rev Physiol 45:261–270PubMedGoogle Scholar
  36. Duman JG, Olsen MT (1993) Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology 30:322–328Google Scholar
  37. Duman JG, Patterson JL, Kozak JJ, DeVries AL (1980) Isopiestic determination of water binding by fish antifreeze glycoproteins. Biochim Biophys Acta 626:332–336PubMedGoogle Scholar
  38. Duman JG, Neven LG, Beals JM, Olson KR, Castellino FJ (1985) Freeze-tolerance adaptations, including haemolymph protein and lipoprotein nucleators, in the larvae of the cranefly Tipula trivittata. J Insect Physiol 31:1–8Google Scholar
  39. Duman JG, Wu DW, Xu L, Tursman D, Olsen MT (1991) Adaptations of insects to subzero temperatures. Q Rev Biol 66:387–410Google Scholar
  40. Duman JG, Olsen TM, Yeung KL, Jerva F (1995) The roles of ice nucleators in cold tolerant invertebrates. APS Press, St. Paul, pp 201–219Google Scholar
  41. Duman JG, Bennett V, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50:259–266PubMedGoogle Scholar
  42. Eastman JT (1993) 11 - Antifreeze Glycopeptides. In: Eastman JT (ed) Antarctic fish biology. Academic Press, San Diego, pp 178–201Google Scholar
  43. Elnitsky MA, Lee RE (2009) The rapid cold-hardening response in insects: ecological significance and physiological mechanisms. J Exp Biol 216:3937–3945Google Scholar
  44. Finn RN, Cerda J (2015) Evolution and functional diversity of aquaporins. Biol Bull 229:6–23PubMedGoogle Scholar
  45. Fisker KV, Overgaard J, Sorensen JG, Slotsbo S, Holmstrup M (2014) Roles of carbohydrate reserves for local adaptation to low temperatures in the freeze tolerant oligochaete Enchytraeus albidus. J Comp Physiol B 184:167–177PubMedGoogle Scholar
  46. Franks F (1985) Biophysics and biochemistry at low temperatures. Cambridge University Press, Cambridge [Cambridgeshire]Google Scholar
  47. Franks F, Mathias SF, Hatley RH (1990) Water, temperature and life. Philos Trans R Soc Lond Ser B Biol Sci 326:517–531. discussion 531–533Google Scholar
  48. Garlick KM, Robertson RM (2007) Cytoskeletal stability and heat shock-mediated thermoprotection of central pattern generation in Locusta migratoria. Comp Biochem Physiol A Mol Integr Physiol 147:344–348PubMedGoogle Scholar
  49. Gehrken U (1984) Winter survival of an adult bark beetle Ips acuminatus Gyll. J Insect Physiol 30:421–429Google Scholar
  50. Gehrken U (1992) Inoculative freezing and thermal hysteresis in the adult beetles Ips acuminatus and Rhagium inquisitor. J Insect Physiol 38:519–524Google Scholar
  51. Gehrken U, Strømme A, Lundheim R, Zachariassen KE (1991) Inoculative freezing in overwintering tenebrionid beetle, Bolitophagus reticulatus Panz. J Insect Physiol 37:683–687Google Scholar
  52. Gekko K, Timasheff SN (1981a) Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures. Biochemistry 20:4667–4676PubMedGoogle Scholar
  53. Gekko K, Timasheff SN (1981b) Thermodynamic and kinetic examination of protein stabilization by glycerol. Biochemistry 20:4677–4686PubMedGoogle Scholar
  54. Gilbert JA, Davies PL, Laybourn-Parry J (2005) A hyperactive, Ca2+-dependent antifreeze protein in an Antarctic bacterium. FEMS Microbiol Lett 245:67–72PubMedGoogle Scholar
  55. Goldstein DL, Frisbie J, Diller A, Pandey RN, Krane CM (2010) Glycerol uptake by erythrocytes from warm- and cold-acclimated Cope’s gray treefrogs. J Comp Physiol B Biochem Syst Environ Physiol 180:1257–1265Google Scholar
  56. Goto SG, Philip BN, Teets NM, Kawarasaki Y, Lee RE Jr, Denlinger DL (2011) Functional characterization of an aquaporin in the Antarctic midge Belgica antarctica. J Insect Physiol 57:1106–1114PubMedGoogle Scholar
  57. Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405PubMedPubMedCentralGoogle Scholar
  58. Griffith M, Ala P, Yang DS, Hon WC, Moffatt BA (1992) Antifreeze protein produced endogenously in winter rye leaves. Plant Physiol 100:593–596PubMedPubMedCentralGoogle Scholar
  59. Hartley LM, Packard MJ, Packard GC (2000) Accumulation of lactate by supercooled hatchlings of the painted turtle (Chrysemys picta): implications for overwinter survival. J Comp Physiol B 170:45–50PubMedGoogle Scholar
  60. Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42PubMedGoogle Scholar
  61. Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227PubMedGoogle Scholar
  62. Hazel JR, McKinley SJ, Williams EE (1992) Thermal adaptation in biological membranes: interacting effects of temperature and pH. J Comp Physiol B 162:593–601Google Scholar
  63. Hoback WW, Stanley DW (2001) Insects in hypoxia. J Insect Physiol 47:533–542PubMedGoogle Scholar
  64. Hochachka PW, Somero GN (1984) Biochemical adaptation. Princeton University Press, New JerseyGoogle Scholar
  65. Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, Oxford, New YorkGoogle Scholar
  66. Holmstrup M (2014) The ins and outs of water dynamics in cold tolerant soil invertebrates. J Therm Biol 45:117–123PubMedGoogle Scholar
  67. Holmstrup M, Westh P (1994) Dehydration of earthworm cocoons exposed to cold - a novel cold-hardiness mechanism. J Comp Physiol B 164:312–315Google Scholar
  68. Holmstrup M, Costanzo JP, Lee RE (1999) Cryoprotective and osmotic responses to cold acclimation and freezing in freeze-tolerant and freeze-intolerant earthworms. J Comp Physiol B 169:207–214Google Scholar
  69. Holmstrup M, Bayley M, Ramlov H (2002) Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable arctic invertebrates. Proc Natl Acad Sci U S A 99:5716–5720PubMedPubMedCentralGoogle Scholar
  70. Hoshino T, Kiriaki M, Ohgiya S, Fujiwara M, Kondo H, Nishimiya Y, Yumoto I, Tsuda S (2003) Antifreeze proteins from snow mold fungi. Can J Bot 81:1175–1181Google Scholar
  71. Hub JS, de Groot BL (2008) Mechanism of selectivity in aquaporins and aquaglyceroporins. Proc Natl Acad Sci U S A 105:1198–1203PubMedPubMedCentralGoogle Scholar
  72. Irwin JT, Lee RE (2000) Mild winter temperatures reduce survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae). J Insect Physiol 46:655–661PubMedGoogle Scholar
  73. Irwin JT, Lee JRE (2003) Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos 100:71–78Google Scholar
  74. Izumi Y, Sonoda S, Yoshida H, Danks HV, Tsumuki H (2006) Role of membrane transport of water and glycerol in the freeze tolerance of the rice stem borer, Chilo suppressalis Walker (Lepidoptera: Pyralidae). J Insect Physiol 52:215–220PubMedGoogle Scholar
  75. Izumi Y, Sonoda S, Tsumuki H (2007) Effects of diapause and cold-acclimation on the avoidance of freezing injury in fat body tissue of the rice stem borer, Chilo suppressalis Walker. J Insect Physiol 53:685–690PubMedGoogle Scholar
  76. Joanisse DR, Storey KB (1996) Oxidative damage and antioxidants in Rana sylvatica, the freeze-tolerant wood frog. Am J Phys 271:R545–R553Google Scholar
  77. Kawarasaki Y, Teets NM, Denlinger DL, Lee RE Jr (2013) The protective effect of rapid cold-hardening develops more quickly in frozen versus supercooled larvae of the Antarctic midge, Belgica antarctica. J Exp Biol 216:3937–3945PubMedGoogle Scholar
  78. Kent B, Hunt T, Darwish TA, Hauss T, Garvey CJ, Bryant G (2014) Localization of trehalose in partially hydrated DOPC bilayers: insights into cryoprotective mechanisms. J R Soc Interface 11:20140069PubMedPubMedCentralGoogle Scholar
  79. Kikawada T, Saito A, Kanamori Y, Nakahara Y, Iwata K, Tanaka D, Watanabe M, Okuda T (2007) Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells. Proc Natl Acad Sci U S A 104:11585–11590PubMedPubMedCentralGoogle Scholar
  80. Kim M, Robich RM, Rinehart JP, Denlinger DL (2006) Upregulation of two actin genes and redistribution of actin during diapause and cold stress in the northern house mosquito, Culex pipiens. J Insect Physiol 52:1226–1233PubMedPubMedCentralGoogle Scholar
  81. King PA, Rosholt MN, Storey KB (1993) Adaptations of plasma membrane glucose transport facilitate cryoprotectant distribution in freeze-tolerant frogs. Am J Phys 265:R1036–R1042Google Scholar
  82. King PA, Rosholt MN, Storey KB (1995) Seasonal changes in plasma membrane glucose transporters enhance cryoprotectant distribution in the freeze-tolerant wood frog. Can J Zool 73:1–9Google Scholar
  83. Knight CA, Wen D, Laursen RA (1995) Nonequilibrium antifreeze peptides and the recrystallization of ice. Cryobiology 32:23–34PubMedPubMedCentralGoogle Scholar
  84. Kostál V, Tamura M, Borovanska M, Zahradníčková H (2004) Enzymatic capacity for accumulation of polyol cryoprotectants changes during diapause development in the adult red firebug, Pyrrhocoris apterus. Physiol Entomol 29(4):344–355Google Scholar
  85. Kristiansen E, Zachariassen KE (2001) Effect of freezing on the transmembrane distribution of ions in freeze-tolerant larvae of the wood fly Xylophagus cinctus (Diptera, Xylophagidae). J Insect Physiol 47:585–592PubMedGoogle Scholar
  86. Kristiansen E, Ramlov H, Hojrup P, Pedersen SA, Hagen L, Zachariassen KE (2011) Structural characteristics of a novel antifreeze protein from the longhorn beetle Rhagium inquisitor. Insect Biochem Mol Biol 41:109–117PubMedGoogle Scholar
  87. Kristiansen E, Wilkens C, Vincents B, Friis D, Lorentzen AB, Jenssen H, Lobner-Olesen A, Ramlov H (2012) Hyperactive antifreeze proteins from longhorn beetles: some structural insights. J Insect Physiol 58:1502–1510PubMedGoogle Scholar
  88. Krog JO, Zachariassen KE, Larsen B, Smidsrød O (1979) Thermal buffering in afro-alpine plants due to nucleating agent-induced water freezing. Nature 282:300–301Google Scholar
  89. Lange R, Staaland H, Mostad A (1972) The effect of salinity and temperature on solubility of oxygen and respiratory rate in oxygen-dependent marine invertebrates. J Exp Mar Biol Ecol 9:217–229Google Scholar
  90. Layne JR Jr, Jones AL (2001) Freeze tolerance in the gray treefrog: cryoprotectant mobilization and organ dehydration. J Exp Zool 290:1–5PubMedGoogle Scholar
  91. Layne JR Jr, Lee RE Jr (1987) Freeze tolerance and the dynamics of ice formation in wood frogs (Rana sylvatica) from southern Ohio. Can J Zool 65:2062–2065Google Scholar
  92. Layne JR Jr, Lee RE Jr (1989) Seasonal variation in freeze tolerance and ice content of the tree frog Hyla versicolor. J Exp Zool 249:133–137PubMedGoogle Scholar
  93. Lee AG (2004) How lipids affect the activities of integral membrane proteins. Biochim Biophys Acta 1666:62–87PubMedGoogle Scholar
  94. Lee RE, Denlinger DL (2010) Rapid cold-hardening: ecological significance and underpinning mechanisms. In: Denlinger DL, Lee JRE (eds) Low temperature biology of insects. Cambridge University Press, Cambridge, pp 35–58Google Scholar
  95. Lee RE, Chen C-P, Denlinger DL (1987) A rapid cold-hardening process in insects. Science 238:1415PubMedGoogle Scholar
  96. Lee RE, McGrath JJ, Todd Morason R, Taddeo RM (1993) Survival of intracellular freezing, lipid coalescence and osmotic fragility in fat body cells of the freeze-tolerant gall fly Eurosta solidaginis. J Insect Physiol 39:445–450Google Scholar
  97. Lee MR, Lee RE Jr, Strong-Gunderson JM, Minges SR (1995) Isolation of ice-nucleating active bacteria from the freeze-tolerant frog, Rana sylvatica. Cryobiology 32:358–365PubMedGoogle Scholar
  98. Lee JK, Park KS, Park S, Park H, Song YH, Kang S-H, Kim HJ (2010) An extracellular ice-binding glycoprotein from an Arctic psychrophilic yeast. Cryobiology 60:222–228PubMedGoogle Scholar
  99. Lee RE Jr (2010) A primer on insect cold-tolerance. Cambridge University Press, CambridgeGoogle Scholar
  100. Lee RE Jr, Costanzo JP (1998) Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Annu Rev Physiol 60:55–72PubMedGoogle Scholar
  101. Lee RE Jr, Lewis EA (1985) Effect of temperature and duration of exposure on tissue ice formation in the gall fly Eurosta solidaginis diptera tephritidae. Cryo Letters 6:25–34Google Scholar
  102. Lee RE Jr, Elnitsky MA, Rinehart JP, Hayward SAL, Sandro LH, Denlinger DL (2006a) Rapid cold-hardening increases the freezing tolerance of the Antarctic midge Belgica antarctica. J Exp Biol 209:399PubMedGoogle Scholar
  103. Lee RE Jr, Damodaran K, Yi SX, Lorigan GA (2006b) Rapid cold-hardening increases membrane fluidity and cold tolerance of insect cells. Cryobiology 52:459–463PubMedGoogle Scholar
  104. Li N, Andorfer CA, Duman JG (1998) Enhancement of insect antifreeze protein activity by solutes of low molecular mass. J Exp Biol 201:2243–2251PubMedGoogle Scholar
  105. Loomis SH (1985) Seasonal changes in the freezing tolerance of the intertidal pulmonate gastropod Melampus bidentatus say. Can J Zool 63:2021–2025Google Scholar
  106. Low W-K, Lin Q, Ewart KV, Fletcher GL, Hew CL (2002) The skin-type antifreeze polypeptides: a new class of type I AFPs. In: Fish antifreeze proteins, vol 1. World Scientific, River Edge, NJ, pp 161–186Google Scholar
  107. Luzardo MC, Amalfa F, Nunez AM, Diaz S, Biondi De Lopez AC, Disalvo EA (2000) Effect of trehalose and sucrose on the hydration and dipole potential of lipid bilayers. Biophys J 78:2452–2458PubMedPubMedCentralGoogle Scholar
  108. Lytvyak E, Olstad DL, Schopflocher DP, Plotnikoff RC, Storey KE, Nykiforuk CI, Raine KD (2016) Impact of a 3-year multi-centre community-based intervention on risk factors for chronic disease and obesity among free-living adults: the healthy Alberta communities study. BMC Public Health 16:344PubMedPubMedCentralGoogle Scholar
  109. Mackenzie AP, Derbyshire W, Reid DS, Richards Rex E, Franks F (1977) Non-equilibrium freezing behaviour of aqueous systems. Philos Trans R Soc Lond B Biol Sci 278:167–189PubMedGoogle Scholar
  110. MacMillan HA, Findsen A, Pedersen TH, Overgaard J (2014) Cold-induced depolarization of insect muscle: differing roles of extracellular K+ during acute and chronic chilling. J Exp Biol 217:2930–2938PubMedGoogle Scholar
  111. Marshall KE, Sinclair BJ (2011) The sub-lethal effects of repeated freezing in the woolly bear caterpillar Pyrrharctia isabella. J Exp Biol 214:1205–1212PubMedGoogle Scholar
  112. Martino M, Otero L, Sanz P, Zaritzky N (1998) Size and location of ice crystals in pork frozen by high-pressure-assisted freezing as compared to classical methods. Meat Sci 50(3):303–313PubMedGoogle Scholar
  113. Mazur P (1977) The role of intracellular freezing in the death of cells cooled at supraoptimal rates. Cryobiology 14:251–272PubMedGoogle Scholar
  114. Mazur P, Leibo SP, Chu EH (1972) A two-factor hypothesis of freezing injury. Evidence from Chinese hamster tissue-culture cells. Exp Cell Res 71:345–355PubMedGoogle Scholar
  115. Meier P, Zettel J (1997) Cold hardiness in Entomobrya nivalis (Collembola, Entomobryidae): annual cycle of polyols and antifreeze proteins, and antifreeze triggering by temperature and photoperiod. J Comp Physiol B 167:297–304Google Scholar
  116. Mellanby K, Gardiner JS (1939) Low temperature and insect activity. Proc R Soc L Ser B 127:473–487Google Scholar
  117. Meryman HT (1970) The exceeding of a minimum tolerable cell volume in hypertonic suspension as a cause of freezing injury. In: Ciba foundation symposium - the frozen cell. Ciba, Churchill, pp 51–67Google Scholar
  118. Mesa ML, Vacchi M (2001) Age and growth of high Antarctic notothenioid fish. Antarct Sci 13:227–235Google Scholar
  119. Michaud MR, Benoit JB, Lopez-Martinez G, Elnitsky MA, Lee RE, Denlinger DL (2008) Metabolomics reveals unique and shared metabolic changes in response to heat shock, freezing and desiccation in the Antarctic midge, Belgica antarctica. J Insect Physiol 54:645–655Google Scholar
  120. Miller LK, Smith JS (1975) Production of threitol and sorbitol by an adult insect: association with freezing tolerance. Nature 258:519–520PubMedGoogle Scholar
  121. Miller LK, Werner R (1987) Extreme supercooling as an overwintering strategy in three species of willow gall insects from interior Alaska USA. Oikos 49:253–260Google Scholar
  122. Morris GJ, Clarke A (1987) Cells at low temperatures. In: Grout BWW, Morris GJ (eds) The effects of low temperatures on biological systems. Edward Arnold, London, pp 72–119Google Scholar
  123. Morrissey RE, Baust JG (1976) The ontogeny of cold tolerance in the gall fly, Eurosta solidagensis. J Insect Physiol 22:431–437Google Scholar
  124. Mugnano J, Lee R, Taylor R (1996) Fat body cells and calcium phosphate spherules induce ice nucleation in the freeze-tolerant larvae of the gall fly Eurosta solidaginis (Diptera, Tephritidae). J Exp Biol 199:465–471PubMedGoogle Scholar
  125. Neven LG, Duman JG, Beals JM, Castellino FJ (1986) Overwintering adaptations of the stag beetle, Ceruchus piceus: removal of ice nucleators in the winter to promote supercooling. J Comp Physiol B 156:707–716Google Scholar
  126. Newsted JW, Polvi S, Papish B, Kendall E, Saleem M, Koch M, Hussain A, Cutler AJ, Georges F (1994) A low molecular weight peptide from snow mold with epitopic homology to the winter flounder antifreeze protein. Biochem Cell Biol 72:152–156PubMedGoogle Scholar
  127. Nickell PK, Sass S, Verleye D, Blumenthal EM, Duman JG (2013) Antifreeze proteins in the primary urine of larvae of the beetle Dendroides canadensis. J Exp Biol 216:1695–1703PubMedGoogle Scholar
  128. O’Grady SM, DeVries AL (1982) Osmotic and ionic regulation in polar fishes. J Exp Mar Biol Ecol 57:219–228Google Scholar
  129. Olsen TM, Duman JG (1997) Maintenance of the supercooled state in the gut fluid of overwintering pyrochroid beetle larvae, Dendroides canadensis  : role of ice nucleators and antifreeze proteins. J Comp Physiol B 167:114–122Google Scholar
  130. Olsen T, Sass S, Li N, Duman J (1998) Factors contributing to seasonal increases in inoculative freezing resistance in overwintering fire-colored beetle larvae Dendroides canadensis. J Exp Biol 201(Pt 10):1585–1594PubMedGoogle Scholar
  131. Overgaard J, MacMillan HA (2017) The integrative physiology of insect chill tolerance. Annu Rev Physiol 79:187–208PubMedGoogle Scholar
  132. Pessin JE, Bell GI (1992) Mammalian facilitative glucose transporter family: structure and molecular regulation. Annu Rev Physiol 54:911–930PubMedGoogle Scholar
  133. Philip BN, Kiss AJ, Lee RE Jr (2011) The protective role of aquaporins in the freeze-tolerant insect Eurosta solidaginis: functional characterization and tissue abundance of EsAQP1. J Exp Biol 214:848–857PubMedGoogle Scholar
  134. Præbel K, Hunt B, Hunt LH, DeVries AL (2009) The presence and quantification of splenic ice in the McMurdo Sound Notothenioid fish, Pagothenia borchgrevinki (Boulenger, 1902). Comp Biochem Physiol A Mol Integr Physiol 154:564–569PubMedGoogle Scholar
  135. Ramlov H (1999) Microclimate and variations in haemolymph composition in the freezing-tolerant New Zealand alpine weta Hemideina maori Hutton (Orthoptera : Stenopelmatidae). J Comp Physiol B 169:224–235Google Scholar
  136. Ramlov H (2000) Aspects of natural cold tolerance in ectothermic animals. Hum Reprod 15(Suppl 5):26–46PubMedGoogle Scholar
  137. Ramlov H, Westh P (1993) Ice formation in the freeze-tolerant alpine weta Hemideina maori Hutton (Orthoptera, Stenopelmatidae). Cryo-Letters 14:169–176Google Scholar
  138. Ramlov H, Bedford J, Leader J (1992) Freezing tolerance of the New-Zealand Alpine weta, Hemideina maori Hutton [Orthoptera, Stenopelmatidae]. J Therm Biol 17:51–54Google Scholar
  139. Ramlov H, Wharton DA, Wilson PW (1996) Recrystallization in a freezing tolerant antarctic nematode, Panagrolaimus davidi, and an alpine weta, Hemideina maori (Orthoptera: Stenopelmatidae). Cryobiology 33:607–613PubMedGoogle Scholar
  140. Raymond JA, Fritsen CH (2001) Semipurification and ice recrystallization inhibition activity of ice-active substances associated with Antarctic photosynthetic organisms. Cryobiology 43:63–70PubMedGoogle Scholar
  141. Raymond MR, Wharton DA (2016) The ability to survive intracellular freezing in nematodes is related to the pattern and distribution of ice formed. J Exp Biol 219:2060–2065PubMedGoogle Scholar
  142. Raymond JA, Janech MG, Fritsen CH (2009) Novel ice-binding proteins from a psychrophilic Antarctic alga (Chlamydomonadaceae, chlorophyceae)1. J Phycol 45:130–136Google Scholar
  143. Rojek A, Praetorius J, Frokiaer J, Nielsen S, Fenton RA (2008) A current view of the mammalian aquaglyceroporins. Annu Rev Physiol 70:301–327PubMedGoogle Scholar
  144. Rudolph AS, Crowe JH (1985) Membrane stabilization during freezing: the role of two natural cryoprotectants, trehalose and proline. Cryobiology 22:367–377PubMedGoogle Scholar
  145. Rudolph AS, Crowe JH, Crowe LM (1986) Effects of three stabilizing agents--proline, betaine, and trehalose--on membrane phospholipids. Arch Biochem Biophys 245:134–143PubMedGoogle Scholar
  146. Salt RW (1961) Principles of insect cold-hardiness. Annu Rev Entomol 6:55–74Google Scholar
  147. Scholander PF, Flagg W, Hock RJ, Irving L (1953) Studies on the physiology of frozen plants and animals in the Arctic. J Cell Physiol Suppl 42:1–56PubMedGoogle Scholar
  148. Semper K (1883) Natural conditions of existence as they affect animal life. Kegan Paul, Trench & CO., LondonGoogle Scholar
  149. Sformo T, Walters K, Jeannet K, Wowk B, Fahy GM, Barnes BM, Duman JG (2010) Deep supercooling, vitrification and limited survival to −100{degrees}C in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae) larvae. J Exp Biol 213:502–509PubMedGoogle Scholar
  150. Shimada K, Riihimaa A (1988) Cold acclimation, inoculative freezing and slow cooling: essential factors contributing to the freezing-tolerance in diapausing larvae of Chymomyza costata. Drosophilidae, DipteraGoogle Scholar
  151. Sidebottom CM, Smallwood MF, Byass LJ (1999) Frozen product, vol. WO99/37673Google Scholar
  152. Sinclair BJ, Klok CJ, Scott MB, Terblanche JS, Chown SL (2003) Diurnal variation in supercooling points of three species of Collembola from Cape Hallett, Antarctica. J Insect Physiol 49:1049–1061PubMedGoogle Scholar
  153. Sinclair BJ, Klok CJ, Chown SL (2004) Metabolism of the sub-Antarctic caterpillar Pringleophaga marioni during cooling, freezing and thawing. J Exp Biol 207:1287–1294PubMedGoogle Scholar
  154. Sinclair BJ, Gibbs AG, Lee WK, Rajamohan A, Roberts SP, Socha JJ (2009) Synchrotron x-ray visualisation of ice formation in insects during lethal and non-lethal freezing. PLoS One 4(12):e8259PubMedPubMedCentralGoogle Scholar
  155. Sømme L (1982) Supercooling and winter survival in terrestrial arthropods. Comp Biochem Physiol A Mol Integr Physiol 73:519–543Google Scholar
  156. Sømme L, Zachariassen KE (1981) Adaptations to low temperature in high altitude insects from Mount Kenya. Ecol Entomol 6:199–204Google Scholar
  157. Storey KB (2004) Strategies for exploration of freeze responsive gene expression: advances in vertebrate freeze tolerance. Cryobiology 48:134–145PubMedGoogle Scholar
  158. Storey JM, Storey KB (1985) Freezing and cellular metabolism in the gall fly larva, Eurosta solidaginis. J Comp Physiol B 155:333–337Google Scholar
  159. Storey KB, Storey JM (1988) Freeze tolerance in animals. Physiol Rev 68:27–84PubMedGoogle Scholar
  160. Storey KB, Storey JM (1992) Natural freeze tolerance in ectothermic vertebrates. Annu Rev Physiol 54:619–637PubMedGoogle Scholar
  161. Storey KB, Storey JM (1993) Cellular adaptations for freezing survival of amphibians and reptiles, vol 2. JAI Press, London, pp 101–129Google Scholar
  162. Storey KB, Storey JM (1996) Natural freezing survival in animals. Annu Rev Ecol Syst 27:365–386Google Scholar
  163. Storey KB, Storey JM (2013) Molecular biology of freezing tolerance. Compr Physiol 3:1283–1308PubMedGoogle Scholar
  164. Tantos A, Friedrich P, Tompa P (2009) Cold stability of intrinsically disordered proteins. FEBS Lett 583:465–469PubMedGoogle Scholar
  165. Taylor MJ (1987) Physico-chemical principles in low temperature biology. In: Grout BWW, Morris GJ (eds) The effects of low temperatures on biological systems. Edmond Arnold, London, pp 3–71Google Scholar
  166. Teets NM, Denlinger DL (2013) Physiological mechanisms of seasonal and rapid cold-hardening in insects. Physiol Entomol 38:105–116Google Scholar
  167. Teets NM, Kawarasaki Y, Lee RE Jr, Denlinger DL (2011) Survival and energetic costs of repeated cold exposure in the Antarctic midge, Belgica antarctica: a comparison between frozen and supercooled larvae. J Exp Biol 214:806–814PubMedGoogle Scholar
  168. Teets NM, Yi SX, Lee RE Jr, Denlinger DL (2013) Calcium signaling mediates cold sensing in insect tissues. Proc Natl Acad Sci U S A 110:9154–9159PubMedPubMedCentralGoogle Scholar
  169. Toxopeus J, Sinclair BJ (2018) Mechanisms underlying insect freeze tolerance. Biol Rev Camb Philos Soc 93:1891–1914PubMedGoogle Scholar
  170. Tsumuki H (2000) Review of low temperature tolerance and ice nuclei in insects, with special emphasis on larvae of the rice stem borer, Chilo suppressalis Walker. Jpn J Appl Entomol Zool 44(3):149–154Google Scholar
  171. Tsumuki H, Konno H (1991) Tissue distribution of the ice-nucleating agents in larvae of the rice stem borer, Chilo suppressalis Walker (Lepidoptera: Pyralidae). Cryobiology 28(4):376–381Google Scholar
  172. Turner JD, Schrag JD, Devries AL (1985) Ocular freezing avoidance in antarctic fish. J Exp Biol 118:121Google Scholar
  173. Tursman D, Duman JG (1995) Cryoprotective effects of thermal hysteresis protein on survivorship of frozen gut cells from the freeze-tolerant centipede Lithobius forficatus. J Exp Zool 272(4):249–257Google Scholar
  174. Vali G (1995) Principles of ice nucleation. APS Press, St. Paul, pp 1–28Google Scholar
  175. van der Laak S (1982) Physiological adaptations to low temperature in freezing-tolerant Phyllodecta laticollis beetles. Comp Biochem Physiol A Physiol 73:613–620Google Scholar
  176. Voituron Y, Paaschburg L, Holmstrup M, Barre H, Ramlov H (2009) Survival and metabolism of Rana arvalis during freezing. J Comp Physiol B 179:223–230PubMedGoogle Scholar
  177. Waagner D, Bouvrais H, Ipsen JH, Holmstrup M (2013) Linking membrane physical properties and low temperature tolerance in arthropods. Cryobiology 67:383–385PubMedGoogle Scholar
  178. Webb MS, Uemura M, Steponkus PL (1994) A comparison of freezing injury in oat and rye: two cereals at the extremes of freezing tolerance. Plant Physiol 104:467PubMedPubMedCentralGoogle Scholar
  179. Wharton DA, Ferns DJ (1995) Survival of intracellular freezing by the Antarctic nematode Panagrolaimus davidi. J Exp Biol 198:1381–1387PubMedGoogle Scholar
  180. Wharton DA, Barrett J, Goodall G, Marshall CJ, Ramlov H (2005) Ice-active proteins from the Antarctic nematode Panagrolaimus davidi. Cryobiology 51:198–207PubMedGoogle Scholar
  181. Wharton DA, Pow B, Kristensen M, Ramlov H, Marshall CJ (2009) ICE-active proteins and cryoprotectants from the New Zealand alpine cockroach, Celatoblatta quinquemaculata. J Insect Physiol 55:27–31PubMedGoogle Scholar
  182. Wilkens C, Ramlov H (2008) Seasonal variations in antifreeze protein activity and haemolymph osmolality in larvae of the beetle Rhagium mordax (Coleoptera : Cerambycidae). CryoLetters 29:293–300PubMedGoogle Scholar
  183. Wilson PW, Leader JP (1995) Stabilization of supercooled fluids by thermal hysteresis proteins. Biophys J 68:2098–2107PubMedPubMedCentralGoogle Scholar
  184. Wilson P, Ramlov H (1995) Hemolymph ice nucleating proteins from the New-Zealand alpine Weta Hemideina maori (Orthoptera, Stenopelmatidae). Comp Biochem Physiol B 112:535–542Google Scholar
  185. Wilson PW, Heneghan AF, Haymet AD (2003) Ice nucleation in nature: supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology 46:88–98Google Scholar
  186. Worland MR, Convey P (2001) Rapid cold hardening in Antarctic microarthropods. Funct Ecol 15:515–524Google Scholar
  187. Worland MR, Block WI, Grubor-Lajsic G (2000) Survival of Heleomyza borealis (Diptera, Heleomyzidae) larvae down to −  60°C. Physiol Entomol 25:1–5Google Scholar
  188. Worland MR, Wharton DA, Byars SG (2004) Intracellular freezing and survival in the freeze tolerant alpine cockroach Celatoblatta quinquemaculata. J Insect Physiol 50:225–232PubMedGoogle Scholar
  189. Yamashita Y, Nakamura N, Omiya K, Nishikawa J, Kawahara H, Obata H (2002) Identification of an antifreeze lipoprotein from Moraxella sp. of Antarctic origin. Biosci Biotechnol Biochem 66:239–247PubMedGoogle Scholar
  190. Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830PubMedGoogle Scholar
  191. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222PubMedGoogle Scholar
  192. Yi SX, Lee RE Jr (2003) Detecting freeze injury and seasonal cold-hardening of cells and tissues in the gall fly larvae, Eurosta solidaginis (Diptera: Tephritidae) using fluorescent vital dyes. J Insect Physiol 49:999–1004PubMedGoogle Scholar
  193. Zachariassen KE (1973) Seasonal variation in hemolymph osmolality and osmotic contribution of glycerol in adult Rhagium inquisitor L. (Col., Cerambycidae). Cryo Letters 29(4):293–300Google Scholar
  194. Zachariassen KE (1979) The mechanism of the cryoprotective effect of glycerol in beetles tolerant to freezing. J Insect Physiol 25:29–32Google Scholar
  195. Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev 65:799–832PubMedGoogle Scholar
  196. Zachariassen KE, Hammel HT (1976) Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262:285–287PubMedGoogle Scholar
  197. Zachariassen KE, Husby JA (1982) Antifreeze effect of thermal hysteresis agents protects highly supercooled insects. Nature 298:865–867Google Scholar
  198. Zachariassen KE, Kristiansen E (2000) Ice nucleation and antinucleation in nature. Cryobiology 41:257–279PubMedGoogle Scholar
  199. Zachariassen KE, Kristiansen E, Pedersen SA, Hammel HT (2004) Ice nucleation in solutions and freeze-avoiding insects-homogeneous or heterogeneous? Cryobiology 48:309–321PubMedGoogle Scholar
  200. Zachariassen KE, Li NG, Laugsand AE, Kristiansen E, Pedersen SA (2008) Is the strategy for cold hardiness in insects determined by their water balance? A study on two closely related families of beetles: Cerambycidae and Chrysomelidae. J Comp Physiol B 178:977–984PubMedGoogle Scholar
  201. Zimmerman SL, Frisbie J, Goldstein DL, West J, Rivera K, Krane CM (2007) Excretion and conservation of glycerol, and expression of aquaporins and glyceroporins, during cold acclimation in Cope’s gray tree frog Hyla chrysoscelis. Am J Physiol Regul Integr Comp Physiol 292:R544–R555PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Natural SciencesRoskilde UniversityRoskildeDenmark
  2. 2.CopenhagenDenmark

Personalised recommendations