Skip to main content
SpringerLink
Log in

Freeze Tolerance and Freeze Avoidance in Ectotherms

  • Chapter
Animal Adaptation to Cold

Part of the book series: Advances in Comparative and Environmental Physiology ((COMPARATIVE,volume 4))

Abstract

The vast majority of ectothermic animals on earth must elude exposure to subzero temperatures to prevent the lethal freezing of body fluids. For this reason the northern ranges of many ectotherms are limited; thus, few terrestrially-hibernating reptile and amphibian species are found in northern latitudes (Behler and King 1979) and the diversity of invertebrate fauna in the intertidal zones of polar regions is low (Aarset 1982). Migration or the choice of warm hibernacula allow some species to elude subzero temperatures during winter (e.g., monarch butterflies fly to Mexico, toads dig down 1 m or more into the earth to avoid the frost line, garter snakes gather by the hundreds in undergound dens, turtles, many frogs, and various insects overwinter under water). For many other species, however, the challenges of life below 0°C are met with physiological and biochemical adaptations for cold hardiness.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aarset AV (1982) Freezing tolerance in intertidal invertebrates (a review). Comp Biochem Physiol A Comp Physiol 73:571–580.

    Google Scholar 

  • Aunaas T (1982) Nucleating agents in the haemolymph of an intertidal mollusc tolerant to freezing. Experientia (Basel) 38:1456–1457.

    Google Scholar 

  • Baust JG (1973) Mechanisms of insect freezing survival. Cryobiology 10:197–205.

    PubMed  CAS  Google Scholar 

  • Baust JG (1981) Biochemical correlates to cold hardening in insects. Cryobiology 18:186–198.

    PubMed  CAS  Google Scholar 

  • Baust JG, Lee RE (1981) Divergent mechanisms of frost hardiness in two populations of the gall fly, Eurosta solidaginis. J Insect Physiol 27:485–490.

    CAS  Google Scholar 

  • Baust JG, Zachariassen KE (1983) Seasonally active cell matrix associated ice nucleators in an insect. Cryo Lett 4:65–71.

    Google Scholar 

  • Behler JL, King FW (1979) The Audubon Society field guide to North American reptiles and amphibians. Knopf, New York.

    Google Scholar 

  • Block W (1982) Cold hardiness in invertebrate poikilotherms. Comp Biochem Physiol A Comp Physiol 73:581–593.

    Google Scholar 

  • Bock PE, Frieden C (1978) Another look at the cold lability of enzymes. Trends Biochem Sci, pp 100-103.

    Google Scholar 

  • Canty A, Driedzic WR, Storey KB (1986) Freeze tolerance of isolated ventricle strips of the wood frog, Rana sylvatica. Cryo Lett 7:81–86.

    Google Scholar 

  • Chen CP, Denlinger DL, Lee RE (1987) Cold shock injury and rapid cold-hardening in the flesh fly, Sarcophaga crassipalpis. Physiol Zool 60:297–304.

    Google Scholar 

  • Clegg JS, Seitz P, Seitz W, Hazelwood CF (1982) Cellular response to extreme water loss: the water-replacement hypothesis. Cryobiology 19:306–316.

    PubMed  CAS  Google Scholar 

  • Conradi-Larsen EM, Somme L (1973) The overwintering of Pelophila borealis Payk. II. Aerobic and anaerobic metabolism. Nor Tidsskr 20:325–332.

    Google Scholar 

  • Crowe JH, Clegg JS (1978) Dry biological systems. Academic Press, London.

    Google Scholar 

  • Crowe JH, Crowe LM, Mouradian R (1983) Stabilization of biological membranes at low water activities. Cryobiology 20:346–356.

    PubMed  CAS  Google Scholar 

  • Duman JG (1980) Factors involved in the overwintering survival of a freeze tolerant beetle, Dendroides canadensis. J Comp Physiol 136:53–59.

    CAS  Google Scholar 

  • Duman JG (1982) Insect antifreezes and ice-nucleating agents. Cryobiology 19:613–627.

    PubMed  CAS  Google Scholar 

  • Duman JG (1984) Change in overwintering mechanism of the cucujid beetle, Cucujus clavipes. J Insect Physiol 30:235–239.

    CAS  Google Scholar 

  • Duman JG, Horwath KL, Tomchaney A, Patterson JL (1982) Antifreeze agents of terrestrial arthropods. Comp Biochem Physiol A Comp Physiol 73:545–555.

    Google Scholar 

  • Duman JG, Morris JP, Castellino FJ (1984) Purification and composition of an ice nucleating protein from queens of the hornet, Vespula maculata. J Comp Physiol 154:79–83.

    CAS  Google Scholar 

  • 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 31:1–8.

    CAS  Google Scholar 

  • Fink AL (1986) Effects of cryoprotectants on enzyme structure. Cyrobiology 23:28–37.

    CAS  Google Scholar 

  • Franks F (1985) Biophysics and biochemistry at low temperatures. Cambridge University Press, Cambridge.

    Google Scholar 

  • Furusawa T, Shikata M, Yamashita O (1982) Temperature dependent sorbitol utilization in diapause eggs of the silkworm, Bombyx mori. J Comp Physiol 147:21–26.

    CAS  Google Scholar 

  • Gehrken U (1984) Winter survival of an adult bark beetle Ips acuminatus Gyll. J Insect Physiol 30:421–429.

    CAS  Google Scholar 

  • Gekko K (1983) Mechanism of protein stabilization by polyols: thermodynamics of transfer of amino acids and proteins from water to aqueous polyol solutions. In: Tanaka N, Ohtaki H, Tamamushi R (eds) Ions and molecules in solution. Elsevier, Amsterdam, pp 339–358.

    Google Scholar 

  • Hargens AR, Shabica SV (1973) Protection against lethal freezing temperatures by mucus in an Antarctic limpet. Cryobiology 10:331–337.

    PubMed  CAS  Google Scholar 

  • Hayakawa Y (1985) Activation mechanism of insect fat body phosphorylase by cold. Insect Biochem 15:123–128.

    CAS  Google Scholar 

  • Hayakawa Y, Chino H (1981) Temperature-dependent interconversion between glycogen and trehalose in diapausing pupae of Philosamia cynthia ricini and pryeri. Insect Biochem 11:41–47.

    Google Scholar 

  • Hayakawa Y, Chino H (1982a) Temperature-dependent activation or inactivation of glycogen phosphorylase and synthase of fat body of the silkworm Philosamia cynthia: the possible mechanism of the temperature-dependent interconversion between glycogen and trehalose. Insect Biochem 12:361–366.

    CAS  Google Scholar 

  • Hayakawa Y, Chino H (1982b) Phosphofructokinase as a possible key enzyme regulating glycerol or trehalose accumulation in diapausing insects. Insect Biochem 12:639–642.

    CAS  Google Scholar 

  • Hayes DR, Loomis SH (1985) Evidence for a proteinaceous ice nucleator in the hemolymph of the pulmonate gastropod, Melampus bidentatus. Cryo Lett 6:418–421.

    Google Scholar 

  • Hazel JR (1984) Effects of temperature on the structure and metabolism of cell membranes in fish. Am J Physiol 246:R460–R470.

    Google Scholar 

  • Hew CL, Kao MH, So YP (1983) Presence of cystine-containing antifreeze proteins in the spruce budworm Choristoneura fumiferana. Can J Zool 61:2324–2328.

    CAS  Google Scholar 

  • Hew CL, Scott GK, Davies PL (1986) Molecular biology of antifreezes. In: Heller HC, Musacchia XJ, Wang LCH (eds) Living in the cold. Elsevier, Amsterdam, pp 117–123.

    Google Scholar 

  • Hochachka PW (1986) Defense strategies against hypoxia and hypothermia. Science 231:234–241.

    PubMed  CAS  Google Scholar 

  • Hochachka PW, Somero GN (1984) Biochemical adaptation. Princeton University Press, Princeton.

    Google Scholar 

  • Horwath KL, Duman JG (1983a) Photoperiodic and thermal regulation of antifreeze protein levels in the beetle Dendroides canadensis. J Insect Physiol 29:907–917.

    CAS  Google Scholar 

  • Horwath KL, Duman JG (1983b) Induction of antifreeze protein production by juvenile hormone in larvae of the beetle Dendroides canadensis. J Comp Physiol 151:233–240.

    CAS  Google Scholar 

  • Horwath KL, Duman JG (1984) Yearly variations in the overwintering mechanisms of the coldhardy beetle Dendroides canadensis. Physiol Zool 57:40–45.

    Google Scholar 

  • Horwath KL, Duman JG (1986) Thermoperiodic involvement in antifreeze protein production in the cold hardy beetle Dendroides canadensis: implications for photoperiodic time measurement. J Insect Physiol 32:799–806.

    CAS  Google Scholar 

  • Jacobsen IA, Pegg DE (1984) Cryopreservation of organs. Cryobiology 21:377–384.

    PubMed  CAS  Google Scholar 

  • Johnson IA (1983) Cellular responses to an altered body temperature: the role of alterations in the expression of protein isoforms. In: Cossins A, Sheterline P (eds) Cellular acclimatisation to environmental change. Cambridge University Press, ambridge, pp 121–143.

    Google Scholar 

  • Kelleher MJ, Rickards J, Storey KB (1987) Strategies of freeze avoidance in larvae of the goldenrod gall moth, Epiblema scudderiana: laboratory investigations of temperature cues in the regulation of cold hardiness. J Insect Physiol 3(8):581–586.

    Google Scholar 

  • Knight CA, Duman JG (1986) Inhibition of recrystallization of ice by insect thermal hysteresis proteins: a possible cryoprotective role. Cyrobiology 23:256–262.

    CAS  Google Scholar 

  • Layne JR, Lee RE (1987) Freeze tolerance and the dynamics of ice formation in wood frogs (Rana sylvatica) from southern Ohio. Can J Zool 65(8):2062–2065.

    Google Scholar 

  • Lee RE, Lewis EA (1985) Effect of temperature and duration of exposure on tissue ice forma-tion in the gall fly, Eurosta solidaginis (Diptera, Tephritidae). Cryo Lett 6:25–34.

    Google Scholar 

  • Mazur P (1984) Freezing of living cells: mechanisms and implications. Am J Physiol 247:C125–C142.

    PubMed  CAS  Google Scholar 

  • Meryman HT (1974) Freezing injury and its prevention in living cells. Annu Rev Biophys 3:341–363.

    CAS  Google Scholar 

  • Miller LK (1978) Physical and chemical changes associated with seasonal alterations in freezing tolerance in the adult northern tenebrionid Upis ceramboides. J Insect Physiol 24:791–796.

    CAS  Google Scholar 

  • Morrissey RE, Baust JG (1976) The ontogeny of cold tolerance in the gall fly, Eurosta solidaginis. J Insect Physiol 22:431–437.

    CAS  Google Scholar 

  • Murphy DJ (1983) Freezing resistance in intertidal invertebrates. Annu Rev Physiol 45:289–299.

    PubMed  CAS  Google Scholar 

  • 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 156:707–716.

    CAS  Google Scholar 

  • Nordin JH, Cui Z, Yin CM (1984) Cold-induced glycerol accumulation by Ostrinia nubilalis larvae is developmentaly regulated. J Insect Physiol 30:563–566.

    CAS  Google Scholar 

  • Rickards J, Kelleher MJ, Storey KB (1987) Strategies of freeze avoidance in larvae of the goldenrod gall moth, Epiblema scudderiana: winter profiles of a natural population. J Insect Physiol 33(6):443–450.

    Google Scholar 

  • Riddle WA (1981) Cold hardiness in the woodland snail, Anguispira alternata (Say) (Endodon-tidae). J Therm Biol 6:117–120.

    Google Scholar 

  • Ring RA (1980) Insects and their cells. In: Ashwood-Smith MJ, Farrant J (eds) Low temperature preservation in medicine and biology. Pitman, Tunbridge Wells, pp 187–217.

    Google Scholar 

  • Ring RA (1981) The physiology and biochemistry of cold tolerance in Arctic insects. J Therm Biol 6:219–229.

    CAS  Google Scholar 

  • Ring RA (1982) Freezing-tolerant insects with low supercooling points. Comp Biochem Physiol A Comp Physiol 73:605–612.

    Google Scholar 

  • Ring RA, Tesar D (1981) Adaptations to cold in Canadian Arctic insects. Cryobiology 18:199–211.

    PubMed  CAS  Google Scholar 

  • Rojas RR, Lee RE, Lua TA, Baust JG (1983) Temperature dependence-independence of antifreeze turnover in Eurosta solidaginis (Fitch). J Insect Physiol 29:865–869.

    CAS  Google Scholar 

  • Rojas RR, Lee RE, Baust JG (1986) Relationship of environmental water content to glycerol accumulation in the freeze tolerant larvae of Eurosta solidaginis (Fitch). Cryo Lett 7:234–245.

    CAS  Google Scholar 

  • Rudolph AS, Crowe JH (1985) Membrane stabilization during freezing: the role of two natural cryoprotectancts, trehalose and proline. Cryobiology 22:367–377.

    PubMed  CAS  Google Scholar 

  • Rudolph AS, Crowe JH, Crowe LM (1986) Effects of three stabilizing agents — proline, betaine, and trehalose — on membrane phospholipids. Arch Biochem Biophys 245:134–143.

    PubMed  CAS  Google Scholar 

  • Sakagami SF, Tanno K, Tfcutsui H, Honma K (1985) The role of cocoons in overwintering of the soybean pod borer Leguminivora glycinivorella (Lepidoptera: Tortricidae). J Kans En-tomol Soc 58:240–247.

    Google Scholar 

  • Sidell B (1983) Cellular acclimatisation to environmental change by quantitative alterations in enzymes and organelles. In: Cossins A, Sheterline P (eds) Cellular acclimatisation to environmental change. Cambridge University Press, Cambridge.

    Google Scholar 

  • Somme L (1982) Supercooling and winter survival in terrestrial arthropods. Comp Biochem Physiol A Comp Physiol 73:519–543.

    Google Scholar 

  • Steponkus PL, Dowgert MF, Gordon-Kamm WJ (1983) Destabilization of the plasma membrane of isolated plant protoplasts during a freeze-thaw cycle: the influence of cold acclimation. Cryobiology 20:448–465.

    PubMed  CAS  Google Scholar 

  • Storey JM, Storey KB (1983) Regulation of cryoprotectant metabolism in the overwintering gall fly larvae, Eurosta solidaginis: temperature control of glycerol and sorbitol levels. J Comp Physiol 149:495–502.

    CAS  Google Scholar 

  • Storey JM, Storey KB (1985a) Triggering of cyroprotectant synthesis by the initiation of ice nu-cleation in the freeze tolerant frog, Rana sylvatica. J Comp Physiol 155:191–195.

    Google Scholar 

  • Storey JM, Storey KB (1985b) Freezing and cellular metabolism in the gall fly larva, Eurosta solidaginis. J Comp Physiol 155:333–337.

    CAS  Google Scholar 

  • Storey JM, Storey KB (1986a) Winter survival of the gall fly larva, Eurosta solidaginis: profiles of fuel reserves and cryoprotectants in a natural population. J Insect Physiol 32:549–556.

    CAS  Google Scholar 

  • Storey KB (1982) Phosphofructokinase from the overwintering gall fly larva, Eurosta solidaginis: control of cryoprotectant polyol synthesis. Insect Biochem 12:501–505.

    CAS  Google Scholar 

  • Storey KB (1983) Metabolism and bound water in overwintering insects. Cryobiology 20:365–379.

    PubMed  CAS  Google Scholar 

  • Storey KB (1985a) Freeze tolerance in terrestrial frogs. Cryo Lett 6:115–134.

    Google Scholar 

  • Storey KB (1985b) A re-evaluation of the Pasteur effect: new mechanisms in anaerobic metabolism. Mol Physiol 8:439–461.

    CAS  Google Scholar 

  • Storey KB (1986) Freeze tolerance in vertebrates: biochemical adaptation of terrestrially hibernating frogs. In: Heller HC, Musacchia XJ, Wang LCH (eds) Living in the cold. Elsevier, Amsterdam, pp 131–138.

    Google Scholar 

  • Storey KB (1988) Suspended animation: the molecular basis of metabolic depression. Can J Zool 66(1):124–132.

    CAS  Google Scholar 

  • Storey KB, Storey JM (1981) Biochemical strategies of overwintering in the gall fly larva, Eurosta solidaginis: effect of low temperature acclimation on the activities of enzymes of intermediary metabolism. J Comp Physiol 144:191–199.

    CAS  Google Scholar 

  • Storey KB, Storey JM (1984) Biochemical adaptation for freezing tolerance in the wood frog, Rana sylvatica. J Comp Physiol 155:29–36.

    CAS  Google Scholar 

  • Storey KB, Storey JM (1986b) Freeze tolerance and intolerance as strategies of winter survival in terrestrially-hibernating amphibians. Comp Biochem Physiol A Comp Physiol 83:613–617.

    PubMed  CAS  Google Scholar 

  • Storey KB, Storey JM (1986c) Freeze tolerant frogs: cryoprotectants and tissue metabolism during freeze/cycles. Can J Zool 64:49–56.

    CAS  Google Scholar 

  • Storey KB, Storey JM (1988a) Freeze tolerance in animals. Physiol Rev 68(1):27–84.

    PubMed  CAS  Google Scholar 

  • Storey KB, Storey JM (1988b) Freeze tolerance: constraining forces, adaptive mechanisms. Can J Zool 66:1122–1127.

    Google Scholar 

  • Storey KB, Baust JG, Storey JM (1981a) Intermediary metabolism during low temperature acclimation in the overwintering gall fly larva, Eurosta solidaginis. J Comp Physiol 144:183–190.

    CAS  Google Scholar 

  • Storey KB, Baust JG, Buescher P (1981b) Determination of water “bound” by soluble subcellu-lar components during low temperature acclimation of the overwintering gall fly larva, Eurosta solidaginis. Cryobiology 18:315–321.

    PubMed  CAS  Google Scholar 

  • Storey KB, Park IRA, Storey JM (1981c) Isozyme composition and low temperature acclimation in the overwintering gall fly larva, Eurosta solidaginis. Cryo Lett 2:279–284.

    CAS  Google Scholar 

  • Theede H, Schneppenheim R, Beress L (1976) Frostschutzglykoproteine bei Mytilus edulisl? Mar Biol 136:183–189.

    Google Scholar 

  • Tooke NE, Holland DL (1985) Phospholipid fatty acid composition and cold tolerance in two species of barnacle, Balanus balanoides (L.) and Elminius modestus Darwin. L Summer versus winter variations in phospholipid fatty acid composition of whole animals. J Exp Mar Biol Ecol 87:241–253.

    CAS  Google Scholar 

  • Tsumuki H, Rojas RR, Storey KB, Baust JG (1987) Fate of 14C-glucose during cold hardening of Eurosta solidaginis. Insect Biochem 17:347–352.

    CAS  Google Scholar 

  • Vries AL de (1982) Biological antifreeze agents in coldwater fishes. Comp Biochem Physiol A Comp Physiol 73:627–640.

    Google Scholar 

  • Wharton DA, Young SR, Barrett J (1984) Cold tolerance in nematodes. J Comp Physiol 154:73–77.

    Google Scholar 

  • Wigglesworth VB (1972) The principles of insect physiology. Chapman amp; Hall, London.

    Google Scholar 

  • Williams RJ (1970) Freezing tolerance in Mytilus edulis. Comp Biochem Physiol 35:145–161.

    Google Scholar 

  • Williams RJ, Willemot C, Hope HJ (1981) The relationship between cell injury and osmotic volume reduction. IV. The behavior of hardy wheat membrane lipids in monolayer. Cryobiology 18:146–154.

    PubMed  CAS  Google Scholar 

  • Womersley C, Uster PS, Rudolph AS, Crowe JH (1986) Inhibition of dehydration-induced fusion between liposomal membranes by carbohydrates as measured by fluorescence energy transfer. Cryobiology 23:245–255.

    PubMed  CAS  Google Scholar 

  • Wood FE, Nordin JH (1980) Activation of the hexose monophosphate shunt during cold-induced gylcerol accumulation by Protophormia terranovae. Insect Biochem 10:87–93.

    CAS  Google Scholar 

  • Zachariassen KE (1980) The role of polyols and nucleating agents in cold-hardy beetles. J Comp Physiol 140:227–234.

    CAS  Google Scholar 

  • Zachariassen KE (1982) Nucleating agents in cold-hardy insects. Comp Biochem Physiol A Comp Physiol 73:557–562.

    Google Scholar 

  • Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev,65:799–832.

    Google Scholar 

  • Zachariassen KE, Hammel HT (1976) Nucleating agents in the hemolymph of insects tolerant to freezing. Nature 262:285–287.

    PubMed  CAS  Google Scholar 

  • Zachariassen KE, Baust JG, Lee RE (1982) A method for quantitative determination of ice nucleating agents in insect hemolymph. Cryobiology 19:180–184.

    PubMed  CAS  Google Scholar 

  • Ziegler R, Ashida M, Fallon AM, Wimer LT, Silver Wyatt S, Wyatt GR (1979) Regulation of glycogen phosphorylase in fat body of cecropia silkmoth pupae. J Comp Physiol 131:321–332.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Biochemistry and Department of Biology, Carleton University, Ottawa, Ontario, Canada, K1S 5B6

    J. M. Storey

Authors
  1. K. B. Storey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. M. Storey
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Zoology, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9

    Lawrence C. H. Wang

Rights and permissions

Reprints and permissions

Copyright information

© 1989 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Storey, K.B., Storey, J.M. (1989). Freeze Tolerance and Freeze Avoidance in Ectotherms. In: Wang, L.C.H. (eds) Animal Adaptation to Cold. Advances in Comparative and Environmental Physiology, vol 4. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-74078-7_2

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-74078-7_2

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-74080-0

  • Online ISBN: 978-3-642-74078-7

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation