Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-669899f699-cf6xr Total loading time: 0 Render date: 2025-05-03T05:29:27.575Z Has data issue: false hasContentIssue false

1 - A primer on insect cold-tolerance

from PART I - PHYSIOLOGICAL AND MOLECULAR RESPONSES

Published online by Cambridge University Press:  04 May 2010

By
Richard E. Lee Jr.
Edited by
David L. Denlinger  and
Richard E. Lee, Jr
David L. Denlinger
Affiliation:
Ohio State University
Richard E. Lee, Jr
Affiliation:
Miami University
Get access

Summary

Introduction

Low temperature affects insects differently based on the severity of the cold and the duration of exposure. Life stage and acclimation state also have a major impact on an insect's response to low temperature. Many temperate and polar insects enhance their cold-tolerance seasonally in preparation for winter, as short, cool days in autumn trigger cold acclimatization, as well as entry into the metabolic depression of diapause. However, insects also have the capacity to make significant and rapid adjustments to even slight changes in environmental temperature, as would occur on a summer's day.

This introductory chapter seeks to provide a short primer on the physiology of insect cold-tolerance that will be useful to students and others new to the area of study. This overview of basic concepts in insect cold-tolerance intends to provide a context for later chapters providing in-depth reviews of specific areas. Specifically, this primer focuses on regulation of supercooling and ice nucleation, and basic adaptations promoting cold-tolerance. Suggestions for conducting and clearly reporting experimental results on insect cold-tolerance are also included. Since this volume is intended to update and complement our previous book, Insects at Low Temperature (Lee and Denlinger, 1991), this synoptic chapter will emphasize articles published during the past 20 years and topics not covered elsewhere in this volume.

Types of insect cold-tolerance

Chilling and cold are relative terms; consequently, the temperature ranges they represent vary depending on the species in question.

Type
Chapter
Information
Low Temperature Biology of Insects , pp. 3 - 34
Publisher: Cambridge University Press
Print publication year: 2010

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.)

Book purchase

Temporarily unavailable

References

Acker, J. P. and McGann, L. E. (2003). Protective effect of intracellular ice during freezing?Cryobiology 46, 197–202.CrossRefGoogle ScholarPubMed
Anderson, J. B. and Brower, L. P. (1996). Freeze-protection of overwintering monarch butterflies in Mexico: critical role of the forest as a blanket and an umbrella. Ecological Entomology 21, 107–116.CrossRefGoogle Scholar
Angell, A. (1982). Supercooled water. In Water: A Comprehensive Treatise, ed. Franks, F., vol. 7. New York: Plenum Press, pp. 1–81.Google Scholar
Bennett, V. A. and Lee, R. E. (1997). Modeling seasonal changes in intracellular freeze-tolerance of fat body cells of the gall fly Eurosta solidaginis (Diptera, Tephritidae). Journal of Experimental Biology 200, 185–192.Google Scholar
Bennett, V. A., Sformo, T., Walters, K., Toien, O., Jeannet, K., Hochstrasser, R., Pan, Q., Serianni, A. S., Barnes, B. M., and Duman, J. G. (2005). Comparative overwintering physiology of Alaska and Indiana populations of the beetle Cucujus clavipes (Fabricius): role of antifreeze proteins, polyols, dehydration and diapause. Journal of Experimental Biology 208, 4467–4477.CrossRefGoogle Scholar
Bokor, M., Csizmok, V., Kovacs, D., Banki, P., Friedrich, P., Tompa, P., and Tompa, K. (2005). NMR relaxation studies on the hydrate layer of intrinsically unstructured proteins. Biophysical Journal 88, 2030–2037.CrossRefGoogle ScholarPubMed
Borgnia, M., Nielsen, S., Engel, A., and Agre, P. (1999). Cellular and molecular biology of the aquaporin water channels. Annual Review of Biochemistry 68, 425–458.CrossRefGoogle ScholarPubMed
Borovskii, G. B., Stupnikova, I. V., Antipina, A. I., Vladimirova, S. V., and Voinikov, V. K. (2002). Accumulation of dehydrin-like proteins in the mitochondria of cereals in response to cold, freezing, drought and ABA treatment. BMC Plant Biology 2, 5–12.CrossRefGoogle ScholarPubMed
Campbell, E. M., Ball, A., Hoppler, S., and Bowman, A. (2008). Invertebrate aquaporins: a review. Journal of Comparative Physiology B 178, 935–955.CrossRefGoogle ScholarPubMed
Castrillo, L. A., Lee, R. E., Lee, M. R., and Rutherford, S. T. (2000). Identification of ice-nucleating active Pseudomonas fluorescens strains for biological control of overwintering Colorado potato beetles (Coleoptera: Chrysomelidae). Journal of Economic Entomology 93, 226–233.CrossRefGoogle Scholar
Castrillo, L. A., Lee, R. E., Wyman, J. A., Lee, M. R., and Rutherford, S. T. (2001). Field persistence of ice-nucleating bacteria in overwintering Colorado potato beetles. Biological Control 21, 11–18.CrossRefGoogle Scholar
Chen, C. P. and Denlinger, D. L. (1992). Reduction of cold injury in flies using an intermittent pulse of high temperature. Cryobiology 29, 138–143.CrossRefGoogle Scholar
Chown, S. L. and Nicolson, S. W. (2004). Insect Physiological Ecology: Mechanisms and Patterns. New York: Oxford University Press.CrossRefGoogle Scholar
Chown, S. L., Sorensen, J. G., and Sinclair, B. J. (2008). Physiological variation and phenotypic plasticity: a response to ‘Plasticity in arthropod cryotypes’ by Hawes and Bale. Journal of Experimental Biology 211, 3353–3357.CrossRefGoogle ScholarPubMed
Chown, S. L. and Terblanche, J. S. (2007). Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology 33, 50–152.CrossRefGoogle Scholar
Clarke, C. J., Buckley, S. L., and Lindner, N. (2002). Ice structuring proteins: a new name for antifreeze proteins. CryoLetters 23, 89–92.Google ScholarPubMed
Colinet, H., Nguyen, T. T. A., Cloutier, C., Michaud, D., and Hance, T. (2007). Proteomic profiling of a parasitic wasp exposed to constant and fluctuating cold exposure. Insect Biochemistry and Molecular Biology 37, 1177–1188.CrossRefGoogle ScholarPubMed
Colinet, H., Renault, D., Hance, T., and Vernon, P. (2006). The impact of fluctuating thermal regimes on the survival of a cold-exposed parasitic wasp, Aphidius colemani. Physiological Entomology 31, 234–240.CrossRefGoogle Scholar
Costanzo, J. P., Humphreys, T. L., Lee, R. E., Moore, J. B., Lee, M. R., and Wyman, J. A. (1998a). Long-term reduction of cold hardiness following ingestion of ice-nucleating bacteria in the Colorado potato beetle, Leptinotarsa decemlineata. Journal of Insect Physiology 44, 1173–1180.CrossRefGoogle Scholar
Costanzo, J. P. and Lee, R. E. (2005). Cryoprotection by urea in a terrestrially hibernating frog. Journal of Experimental Biology 208, 4079–4089.CrossRefGoogle Scholar
Costanzo, J. P., Litzgus, J. D., Iverson, J. B., and Lee, R. E. (1998b). Soil hydric characteristics and environmental ice nuclei influence supercooling capacity of hatchling turtles Chrysemys picta. Journal of Experimental Biology 201, 3105–3112.Google ScholarPubMed
Costanzo, J. P., Moore, J. B., Lee, R. E., Kaufman, P. E., and Wyman, J. A. (1997). Influence of soil hydric parameters on the winter cold hardiness of a burrowing beetle, Leptinotarsa decemlineata (Say). Journal of Comparative Physiology B 167, 169–176.CrossRefGoogle Scholar
Crowe, J. H., Carpenter, J. F., and Crowe, L. M. (1998). The role of vitrification in anhydrobiosis. Annual Review of Physiology 60, 73–103.CrossRefGoogle ScholarPubMed
Crowe, L. M. (2002). Lessons from nature: the role of sugars in anhydrobiosis. Comparative Biochemistry and Physiology A – Molecular and Integrative Physiology 131, 505–513.CrossRefGoogle ScholarPubMed
Dahlhoff, E. P., Fearnley, S. L., Bruce, D. A., Gibbs, A. G., Stoneking, R., McMillan, D. M., Deiner, K., Smiley, J. T., and Rank, N. E. (2008). Effects of temperature on physiology and reproductive success of a montane leaf beetle: implications for persistence of native populations enduring climate change. Physiological and Biochemical Zoology 81, 718–732.CrossRefGoogle ScholarPubMed
Danks, H. V. (1971). Overwintering of some north temperate and arctic Chironomidae. II. Chironomid biology. Canadian Entomologist 103, 1875–1910.CrossRefGoogle Scholar
Danks, H. V. (2000). Dehydration in dormant insects. Journal of Insect Physiology 46, 837–852.CrossRefGoogle ScholarPubMed
Danks, H. V. (2007). How aquatic insects live in cold climates. Canadian Entomologist 139, 443–471.CrossRefGoogle Scholar
Davis, D. J. and Lee, R. E. (2001). Intracellular freezing, viability, and composition of fat body cells from freeze-intolerant larvae of Sarcophaga crassipalpis. Archives of Insect Biochemistry and Physiology 48, 199–205.CrossRefGoogle ScholarPubMed
Denlinger, D. L. and Lee, R. E. (1998). Physiology of cold sensitivity. In Temperature Sensitivity in Insects and Application in Integrated Pest Management, ed. Hallman, G. J., and Denlinger, D. L.. Boulder: Westview Press, pp. 55–95.Google Scholar
Duman, J. G. (2001). Antifreeze and ice nucleator proteins in terrestrial arthropods. Annual Review of Physiology 63, 327–357.CrossRefGoogle ScholarPubMed
Duman, J. G. (2002). The inhibition of ice nucleators by insect antifreeze proteins is enhanced by glycerol and citrate. Journal of Comparative Physiology B 172, 163–168.Google ScholarPubMed
Duman, J. G., Bennett, V., Sformo, T., Hochstrasser, R., and Barnes, B. M. (2004). Antifreeze proteins in Alaskan insects and spiders. Journal of Insect Physiology 50, 259–266.CrossRefGoogle ScholarPubMed
Dure, L. (1993). Structural motifs in LEA proteins of higher plants. In Response of Plants to Cellular Dehydration during Environmental Stress, ed. Close, T. J. and Bray, E. A.. Rockville, MD: American Society of Plant Physiologists, pp. 91–103.Google Scholar
Edashige, K., Yamaji, Y., Kleinhans, F.W., and Kasai, M. (2003). Artificial expression of aquaporin-3 improves the survival of mouse oocytes after cryopreservation. Biology of Reproduction 68, 87–94.CrossRefGoogle ScholarPubMed
Egerton-Warburton, L. M., Balsamo, R. A., and Close, T. J. (1997). Temporal accumulation and ultrastructural localization of dehydrins in Zea mays. Physiologia Plantarum 101, 545–555.CrossRefGoogle Scholar
Elnitsky, M. A., Hayward, S. A. L., Rinehart, J. P., Denlinger, D. L., and Lee, R. E. (2008). Cryoprotective dehydration and the resistance to inoculative freezing in the Antarctic midge, Belgica antarctica. Journal of Experimental Biology 211, 524–530.CrossRefGoogle ScholarPubMed
Fields, P. G. (1990). The cold-hardiness of Cryptolestes ferrugineus and the use of ice nucleation-active bacteria as a cold-synergist. Proceedings of the Fifth International Working Conference on Stored-Product Protection, pp. 1183–1191.Google Scholar
Fields, P. G. (1993). Reduction of cold tolerance of stored-product insects by ice-nucleating-active bacteria. Environmental Entomology 22, 470–476.CrossRefGoogle Scholar
Frisbie, M. P. and Lee, R. E. (1997). Inoculative freezing and the problem of winter survival for freshwater macroinvertebrates. Journal of the North American Benthological Society 16, 635–650.CrossRefGoogle Scholar
Fujiwara, Y. and Denlinger, D. L. (2007). p38 MAP kinase is a likely component of the signal transduction pathway triggering rapid cold-hardening in the flesh fly, Sarcophaga crassipalpis. Journal of Experimental Biology 210, 3295–3300.CrossRefGoogle Scholar
Fuller, B. J., Lane, N., and Benson, E. E. (eds.) (2004). Life in the Frozen State, Boca Raton: CRC Press.CrossRefGoogle ScholarPubMed
Gehrken, U. and Southon, T. E. (1992). Supercooling in a freeze-tolerant cranefly larva, Tipula sp. Journal of Insect Physiology 38, 131–137.CrossRefGoogle Scholar
Gehrken, U., Stromme, A., Lundheim, R., and Zachariassen, K. E. (1991). Inoculative freezing in overwintering tenebrionid beetle, Bolitophagus reticulatus Panz. Journal of Insect Physiology 37, 683–687.CrossRefGoogle Scholar
Hallman, G. J. and Denlinger, D. L. (1998). Introduction: temperature sensitivity and integrated pest management. In Temperature Sensitivity in Insects and Application in Integrated Pest Management, ed. Hallman, G. J. and Denlinger, D. L.. Boulder: Westview Press, pp. 1–5.Google Scholar
Hawes, T. C. and Bale, J. S. (2007). Plasticity in arthropod cryotypes. Journal of Experimental Biology 210, 2585–2592.CrossRefGoogle ScholarPubMed
Heinrich, B. (1993). The Hot-Blooded Insects: Strategies and Mechanisms of Thermoregulation. Cambridge, MA: Harvard University Press.Google Scholar
Hirsh, A. G., Williams, R. J., and Meryman, H. T. (1985). A novel method of natural cryoprotection. Plant Physiology 79, 41–56.CrossRefGoogle ScholarPubMed
Holmstrup, M. (1995). Polyol accumulation in earthworm cocoons induced by dehydration. Comparative Biochemistry and Physiology A 111, 251–255.CrossRefGoogle Scholar
Holmstrup, M., Bayley, M., and Ramlov, H. (2002). Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable arctic invertebrates. Proceedings of the National Academy of Sciences, USA 99, 5716–5720.CrossRefGoogle ScholarPubMed
Holmstrup, M., Costanzo, J. P., and Lee, R. E. (1999). Cryoprotective and osmotic responses to cold acclimation and freezing in freeze-tolerant and freeze-intolerant earthworms. Journal of Comparative Physiology B 169, 207–214.CrossRefGoogle Scholar
Holmstrup, M. and Sømme, L. (1998). Dehydration and cold hardiness in the Arctic collembolan Onychiurus arcticus Tullberg 1876. Journal of Comparative Physiology B 168, 197–203.CrossRefGoogle Scholar
Holmstrup, M. and Westh, P. (1994). Dehydration of earthworm cocoons exposed to cold: a novel cold hardiness mechanism. Journal of Comparative Physiology B 164, 312–315.CrossRefGoogle Scholar
Irwin, J. T., Bennett, V. A., and Lee, R. E. (2001). Diapause development in frozen larvae of the goldenrod gall fly, Eurosta solidaginis (Fitch) (Diptera: Tephritidae). Journal of Comparative Physiology B 171, 181–188.CrossRefGoogle Scholar
Irwin, J. T. and Lee, R. E. (2002). Energy and water conservation in frozen vs. supercooled larvae of the goldenrod gall fly, Eurosta solidaginis (Fitch) (Diptera: Tephritidae). Journal of Experimental Zoology 292, 345–350.CrossRefGoogle Scholar
Izumi, Y., Sonoda, S., and 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. Journal of Insect Physiology 53, 685–690.CrossRefGoogle ScholarPubMed
Izumi, Y., Sonoda, S., Yoshida, H., Danks, H. V., and 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). Journal of Insect Physiology 52, 215–220.CrossRefGoogle Scholar
Jepsen, J. U., Hagen, S. B., Ims, R. A., and Yoccoz, N. G. (2008). Climate change and outbreaks of geometrids Operophtera brumata and Epirrita autumnata in subarctic birch forest: evidence of a recent outbreak range expansion. Journal of Animal Ecology 77, 257–264.CrossRefGoogle ScholarPubMed
Kaneko, J., Kita, K., and Tanno, K. (1991a). INA bacteria isolated from diamondback moth, Plutella xylostella L. pupae (Lepidoptera: Yponomeutidae). Japanese Journal of Applied Entomology and Zoology 35, 7–11.CrossRefGoogle Scholar
Kaneko, J., Toyohira-ku, H., Owada, T., and Tanno, K. (1991b). Erwinia herbicola: ice nucleation active bacteria isolated from diamondback moth, Plutella xylostella L. pupae. Japanese Journal of Applied Entomology and Zoology 35, 247–251.CrossRefGoogle Scholar
Karow, A. M. (1991). Chemical cryoprotection of metazoan cells. BioScience 41, 155–160.CrossRefGoogle Scholar
Kayukawa, T., Chen, B., Hoshizaki, S., and Ishikawa, Y. (2007). Upregulation of a desaturase is associated with the enhancement of cold hardiness in the onion maggot, Delia antiqua. Insect Biochemistry and Molecular Biology 37, 1160–1167.CrossRefGoogle ScholarPubMed
Kelty, J. D. and Lee, R. E. (2000). Diapausing pupae of the flesh fly Sarcophaga crassipalpis (Diptera: Sarcophagidae) are more resistant to inoculative freezing than non-diapausing pupae. Physiological Entomology 25, 120–126.CrossRefGoogle Scholar
Kikawada, T., Nakahara, Y., Kanamori, Y., Iwata, K., Watanabe, M., McGee, B., Tunnacliffe, A., and Okuda, T. (2006). Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochemical and Biophysical Research Communications 348, 56–61.CrossRefGoogle Scholar
Kikawada, T., Saito, A., Kanamori, Y., Nakahara, Y., Iwata, K., Tanaka, D., Watanabe, M., and Okuda, T. (2007). Trehalose transporter 1, a facilitated and high-capacity trehalose transporter allows exogenous trehalose uptake into cells. Proceedings of the National Academy of Sciences, USA 104, 11585–11590.CrossRefGoogle ScholarPubMed
Kohshima, S. (1984). A novel cold-tolerant insect found in a Himalayan glacier. Nature 310, 225–227.CrossRefGoogle Scholar
Kostal, V., Slachta, M., and Simek, P. (2001). Cryoprotective role of polyols independent of the increase in supercooling capacity in diapausing adults of Pyrrhocoris apterus (Heteroptera: Insecta). Comparative Biochemistry and Physiology Part B 130, 365–374.CrossRefGoogle Scholar
Kostal, V., Vambera, J., and Bastl, J. (2004). On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in adults of Pyrrhocoris apterus. Journal of Experimental Biology 207, 1509–1521.CrossRefGoogle ScholarPubMed
Kostal, V., Renault, D., Mehrabianová, A., and Bastl, J. (2007). Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of ion homeostasis. Comparative Biochemistry and Physiology, Part A 147, 231–238.CrossRefGoogle ScholarPubMed
Kostal, V., Yanagimoto, M., and Bastl, J. (2006). Chilling-injury and disturbance of ion homeostasis in the coxal muscle of the tropical cockroach (Nauphoeta cinerea). Comparative Biochemistry and Physiology B 143, 173–179.CrossRefGoogle Scholar
Lacoume, S., Bressac, C., and Chevrier, C. (2007). Sperm production and mating potential of males after a cold shock on pupae of the parasitoid wasp Dinarmus basalis. Journal of Insect Physiology 53, 1008–1015.CrossRefGoogle ScholarPubMed
Larcher, W. (2001). Physiological Plant Ecology: Ecophysiology and Stress Physiology of Functional Groups, 4th edn. New York: Springer.Google Scholar
Larsen, K. J. and Lee, R. E. (1994). Cold tolerance including rapid cold-hardening and inoculative freezing in migrant monarch butterflies in Ohio. Journal of Insect Physiology 40, 859–864.CrossRefGoogle Scholar
Layne, J. R., Lee, R. E., and Huang, J. L. (1990). Inoculation triggers at high subzero temperatures in a freeze-tolerant frog (Rana sylvatica) and insect (Eurosta solidaginis). Canadian Journal of Zoology 68, 506–510.CrossRefGoogle Scholar
Lee, M. R., Lee, R. E., Strong-Gunderson, J. M., and Minges, S. R. (1995a). Isolation of ice-nucleating active bacteria from the freeze tolerant frog, Rana sylvatica. Cryobiology 32, 358–365.CrossRefGoogle ScholarPubMed
Lee, R. R. (1989). Insect cold-hardiness: to freeze or not to freeze. BioScience 39, 308–313.CrossRefGoogle Scholar
Lee, R. E. (1991). Principles of insect low temperature tolerance. In Insects at Low Temperature, ed. Lee, R. E. and Denlinger, D. L.. New York and London: Chapman and Hall, pp. 17–46.CrossRefGoogle Scholar
Lee, R. E., Castrillo, L. A., Lee, M. L., Wyman, J., and Costanzo, J. P. (2001). Using ice-nucleating bacteria to reduce winter survival of Colorado potato beetles: development of a novel strategy for biological control. In Insect Timing: Circadian Rhythmicity to Seasonality, ed. Denlinger, D. L., Giebultowicz, J. M. and Saunders, D. S.. Amsterdam: Elsevier, pp. 213–227.CrossRefGoogle Scholar
Lee, R. E. and Costanzo, J. P. (1998). Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Annual Review of Physiology 60, 55–72.CrossRefGoogle ScholarPubMed
Lee, R. E., Costanzo, J. P., Kaufman, P. E., Lee, M. R., and Wyman, J. A. (1994). Ice-nucleating active bacteria reduce the cold-hardiness of the freeze-intolerant Colorado potato beetle (Coleoptera, Chrysomelidae). Journal of Economic Entomology 87, 377–381.CrossRefGoogle Scholar
Lee, R. E., Damodaran, K., Yi, S.-X., and Lorigan, G. A. (2006). Rapid cold-hardening increases membrane fluidity and cold tolerance of insect cells. Cryobiology 52, 459–463.CrossRefGoogle ScholarPubMed
Lee, R. E. and Denlinger, D. L. (eds.) (1991). Insects at Low Temperature. New York: Chapman and Hall.CrossRef
Lee, R. E., Lee, M. L., and Strong-Gunderson, J. M. (1993a). Insect cold-hardiness and ice nucleating active microorganisms including their potential use for biological control. Journal of Insect Physiology 39, 1–12.CrossRefGoogle Scholar
Lee, R. E., Lee, M. R., and Strong-Gunderson, J. M. (1995b). Biological control of insect pests using ice-nucleating microorganisms. In Biological Ice Nucleations and its Applications, ed. Lee, R. E., Warren, G. J. and Gusta, L. V.. St. Paul: APS Press, pp. 257–269.Google Scholar
Lee, R. E. and Lewis, E. A. (1985). Effect of temperature and duration of exposure on tissue ice formation in the gall fly, Eurosta solidaginis (Diptera, Tephritidae). CryoLetters 6, 24–34.Google Scholar
Lee, R. E., McGrath, J. J., Morason, R. T., and Taddeo, R. M. (1993b). Survival of intracellular freezing, lipid coalescence and osmotic fragility in fat-body cells of the freeze-tolerant gall fly Eurosta solidaginis. Journal of Insect Physiology 39, 445–450.CrossRefGoogle Scholar
Lee, R. E., Steigerwald, K. A., Wyman, J. A., Costanzo, J. P., and Lee, M. R. (1996). Anatomic site of application of ice-nucleating active bacteria affects supercooling in the Colorado potato beetle (Coleoptera: Chrysomelidae). Environmental Entomology 25, 465–469.CrossRefGoogle Scholar
Lee, R. E., Strong-Gunderson, J. M., Lee, M. R., and Davidson, E. C. (1992). Ice-nucleating active bacteria decrease the cold-hardiness of stored grain insects. Journal of Economic Entomology 85, 371–374.CrossRefGoogle Scholar
Lee, R. E., Strong-Gunderson, J. M., Lee, M. R., Grove, K. S., and Riga, T. J. (1991). Isolation of ice nucleating active bacteria from insects. Journal of Experimental Zoology 257, 124–127.CrossRefGoogle Scholar
Lee, R. E., Warren, G. J., and Gusta, L. V. (eds.) (1995c). Biological Ice Nucleation and its Applications. St. Paul: APS Press.
Leopold, R. A., Rojas, R. R., and Atkinson, P. W. (1998). Post pupariation cold storage of three species of flies: increasing chilling tolerance by acclimation and recurrent recovery periods. Cryobiology 36, 213–224.CrossRefGoogle ScholarPubMed
Levitt, J. (1980). Responses of Plants to Environmental Stresses, 2nd edn. New York: Academic Press, Inc.Google Scholar
Lindow, S. E. (1983). The role of bacterial ice nucleation in frost injury to plants. Annual Review of Phytopathology 21, 363–384.CrossRefGoogle Scholar
Lovelock, J. E. (1953). The mechanism of the protective action of glycerol against haemolysis by freezing and thawing. Biochimica et Biophysica Acta 11, 28–36.CrossRefGoogle ScholarPubMed
Mazur, P. (2004). Principles of cryobiology. In Life in the Frozen State, ed. Fuller, B. J., Lane, N. and Benson, E. E.. Boca Raton: CRC Press, pp. 3–66.CrossRefGoogle Scholar
McMullen, D. C. and Storey, K. B. (2008). Suppression of Na+K+-ATPase activity by reversible phosphorylation over the winter in a freeze-tolerant insect. Journal of Insect Physiology 54, 1023–1027.CrossRefGoogle Scholar
Meryman, H. T. (1968). Modified model for the mechanism of freezing injury in erythrocytes. Nature 218, 333–336.CrossRefGoogle ScholarPubMed
Moore, M. V. and Lee, R. E. (1991). Surviving the big chill: overwintering strategies of aquatic and terrestrial insects. American EntomologistSummer111–118.CrossRefGoogle Scholar
Morason, T. R., Allenspach, A., and Lee, R. E. (1994). Comparative ultrastructure of fat body cells of freeze-susceptible and freeze-tolerant Eurosta solidaginis larvae after chemical fixation and high pressure freezing. Journal of Insect Physiology 40, 155–164.CrossRefGoogle Scholar
Mugnano, J. A., Lee, R. E., and Taylor, R. T. (1996). Fat body cells and calcium phosphate spherules induce ice nucleation in the freeze-tolerant larvae of the gall fly Eurosta solidaginis (Diptera, Tephritidae). Journal of Experimental Biology 199, 465–471.Google Scholar
Muldrew, K., Acker, J. P., Elliott, J. A., and McGann, L. E. (2004). The water to ice transition: implications for living cells. In Life in the Frozen State, ed. Fuller, B., Lane, N. and Benson, E.. Boca Raton: CRC Press, pp. 67–108.CrossRefGoogle Scholar
Nedved, O. (2000). Snow White and the Seven Dwarfs: a multvariate approach to classification of cold tolerance. CryoLetters 21, 339–348.Google Scholar
Neufeld, D. S. and Leader, J. P. (1997). Freezing survival by isolated Malpighian tubules of the New Zealand alpine weta Hemideina maori. Journal of Experimental Biology 201, 227–236.Google Scholar
Oberhauser, K. and Peterson, A. (2003). Modeling current and future potential wintering distributions of eastern North American monarch butterflies. Proceedings of the National Academy of Sciences, USA 100, 14063–14068.CrossRefGoogle ScholarPubMed
Olsen, T. M., Sass, S. J., Li, N., and Duman, J. G. (1998). Factors contributing to seasonal increases in inoculative freezing resistance in overwintering fire-colored beetle larvae Dendroides canadensis (Pyrochroidae). Journal of Experimental Biology 201, 1585–1594.Google Scholar
Oswood, M. W., Miller, L. K., and Irons, J. G. (1991). Overwintering of freshwater benthic marcoinvertebrates. In Insects at Low Temperature, ed. Lee, R. E. and Denlinger, D. L.. New York: Chapman and Hall, pp. 360–375.CrossRefGoogle Scholar
Philip, B. N., Yi, S.-X., Elnitsky, M. A., and Lee, R. E. (2008). Aquaporins play a role in desiccation and freeze tolerance in larvae of the goldenrod gall fly, Eurosta solidaginis. Journal of Experimental Biology 211, 1114–1119.CrossRefGoogle ScholarPubMed
Pruitt, N. L., Moqueet, N., and Shapiro, C. A. (2007). Evidence for a novel cryoprotective protein from freeze-tolerant larvae of the goldenrod gall fly Eurosta solidaginis. Cryobiology 54, 125–128.CrossRefGoogle ScholarPubMed
Qi, X.-L., Wang, X.-H., Xu, H.-F., and Kang, L. (2007). Influence of soil moisture on egg cold hardiness in the migratory locust Locusta migratoria (Orthoptera: Acrididae). Physiological Entomology 32, 219–224.CrossRefGoogle Scholar
Ramlov, H. (1998). Letter to editor. CryoLetters 19, 4.Google Scholar
Ramlov, H. and Lee, R. E. (2000). Extreme resistance to desiccation in overwintering larvae of the gall fly Eurosta solidaginis (Diptera: Tephritidae). Journal of Experimental Biology 203, 983–789.Google Scholar
Régnière, J. and Bentz, B. (2007). Modeling cold tolerance in the mountain pine beetle, Dendroctonus ponderosae. Journal of Insect Physiology 53, 559–572.CrossRefGoogle ScholarPubMed
Renault, D., Nedved, O., Hervant, F., and Vernon, P. (2004). The importance of fluctuating thermal regimes for repairing chill injuries in the tropical beetle Alphitobius diaperinus (Coleoptera: Tenebrionidae) during exposure to low temperature. Physiological Entomology 29, 139–145.CrossRefGoogle Scholar
Rinehart, J. P., Hayward, S. A. L., Einitsky, M. A., Sandro, L. H., Lee, R. E., and Denlinger, D. L. (2006). Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect. Proceedings of the National Academy of Sciences, USA 103, 14223–14227.CrossRefGoogle Scholar
Rinehart, J. P., Li, A., Yocum, G. D., Robich, R. M., Hayward, S. A. L., and Denlinger, D. L. (2007). Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proceedings of the National Academy of Sciences, USA 104, 11130–11137.CrossRefGoogle ScholarPubMed
Ring, R. A. and Tesar, D. (1980). Cold-hardiness of the arctic beetle, Pytho americanus Kirby Coleoptera, Pythidae (Salpingidae). Journal of Insect Physiology 26, 763–774.CrossRefGoogle Scholar
Ring, R. A. and Tesar, D. (1981). Adaptations to cold in Canadian Arctic insects. Cryobiology 18, 199–211.CrossRefGoogle ScholarPubMed
Rojas, R. R. and Leopold, R. A. (1996). Chilling injury in the housefly: evidence for the role of oxidative stress between pupariation and emergence. Cryobiology 33, 447–458.CrossRefGoogle Scholar
Sakurai, M., Furuki, T., Akao, K., Tanaka, D., Nakahara, Y., Kikawada, T., Watanabe, M., and Okuda, T. (2008). Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki. Proceedings of the National Academy of Sciences, USA 105, 5093–5098.CrossRefGoogle Scholar
Salt, R. W. (1959). Survival of frozen fat body cells in an insect. Nature 184, 1426.CrossRefGoogle Scholar
Salt, R. W. (1961). Principles of insect cold-hardiness. Annual Review of Entomology 6, 55–74.CrossRefGoogle Scholar
Salt, R. W. (1962). Intracelluar freezing in insects. Nature 193, 1207–1208.CrossRefGoogle Scholar
Scholander, P. F., Flagg, W., Hock, R. J., and Irving, L. (1953). Studies on the physiology of frozen plants and animals in the Arctic. Journal of Cellular Comparative Physiology 42, 1–56.CrossRefGoogle ScholarPubMed
Shimada, K. and Riihimaa, A. (1988). Cold acclimation, inoculative freezing and slow cooling: essential factors contributing to the freezing-tolerance in diapausing larvae of Chymomyza costata (Diptera: Drosophilidae). CryoLetters 9, 5–10.Google Scholar
Sinclair, B. J. (1999). Insect cold tolerance: how many kinds of frozen?European Journal of Entomology 96, 157–164.Google Scholar
Sinclair, B., Addo-Bediako, A., and Chown, S. L. (2003). Climatic variability and the evolution of insect freeze tolerance. Biological Reviews 78, 181–195.CrossRefGoogle ScholarPubMed
Sinclair, B. and Wharton, D. A. (1997). Avoidance of intracellular freezing by the freezing-tolerant New Zealand Alpine weta Hemideina maori (Orthoptera: Stenopelmatidae). Journal of Insect Physiology 43, 621–625.CrossRefGoogle Scholar
Somero, G. N. (1992). Adapting to water stress: convergence on common solutions. In Water and Life, ed. Somero, G. N., Osmond, C. B., and Bolis, C. L.. London: Springer-Verlag, pp. 3–18.CrossRefGoogle Scholar
Sømme, L. (1982). Supercooling and winter survival in terrestrial arthropods. Comparative Biochemistry and Physiology 73A, 519–543.CrossRefGoogle Scholar
Steigerwald, K. A., Lee, M. R., Lee, R. E., and Marshall, J. C. (1995). Effect of biological ice nucleators on insect supercooling capacity varies with anatomic site of application. Journal of Insect Physiology 41, 603–608.CrossRefGoogle Scholar
Steponkus, P. L. and Lynch, D. V. (1989). Freeze/thaw-induced destabilization of the plasma membrane and the effects of cold acclimation. Journal of Bioenergetics and Biomembranes 21, 21–41.CrossRefGoogle ScholarPubMed
Storey, K. B., Baust, J. G., and Storey, J. M. (1981). Intermediary metabolism during low temperature acclimation in the overwintering gall fly larva, Eurosta solidaginis. Journal of Comparative Physiology B 144, 183–190.CrossRefGoogle Scholar
Storey, K. B. and Storey, J. M. (1988). Freeze tolerance in animals. Physiological Reviews 68, 27–84.CrossRefGoogle ScholarPubMed
Storey, K. B. and Storey, J. M. (1991). Biochemistry of cryoprotectants. In Insects at Low Temperature, ed. Lee, R. E., and Denlinger, D. L.. New York and London: Chapman and Hall, pp. 64–93.CrossRefGoogle Scholar
Storey, K. B. and Storey, J. M. (1996). Natural freezing survival in animals. Annual Review of Ecology and Systematics 27, 365–386.CrossRefGoogle Scholar
Strong-Gunderson, J. M., Lee, R. E., Lee, M. R., and Riga, T. J. (1990). Ingestion of ice-nucleating active bacteria increases the supercooling point of the lady beetle Hippodamia convergens. Journal of Insect Physiology 36, 153–157.CrossRefGoogle Scholar
Tanaka, K. and Watanabe, M. (2003). Transmission of ice-nucleating active bacteria from a prey reduces cold hardiness of a predator (Araneae: Theridiidae). Naturwissenschaften 90, 449–451.CrossRefGoogle Scholar
Tanghe, A., Dijck, P., Dumortier, F., Teunissen, A., Hohmann, S., and Thevelein, J. M. (2002). Aquaporin expression correlates with freeze tolerance in baker's yeast, and overexpression improves freeze tolerance in industrial strains. Applied and Environmental Microbiology 68, 5981–5989.CrossRefGoogle ScholarPubMed
Taylor, M. J., Song, Y. C., and Brockbank, K. G. (2007). Vitrification in tissue preservation: new developments. In Life in the Frozen State, ed. Fuller, B. J., Lane, N. and Benson, E. E.. Boca Raton: CRC Press, pp. 603–642.Google Scholar
Teets, N. M., Elnitsky, M. A., Benoit, J. B., Lopez-Martinez, G., Denlinger, D. L., and Lee, R. E. (2008). Rapid cold-hardening in larvae of the Antarctic midge, Belgica antarctica: cellular cold-sensing and a role for calcium. American Journal of Physiology 294, R1938–R1946.Google Scholar
Tran, K., Ylioja, T., Billings, R. F., Regniere, J., and Ayres, M. P. (2007). Impact of minimum winter temperatures on the population dynamics of Dendroctonus frontalis. Ecological Applications 17, 882–899.CrossRefGoogle ScholarPubMed
Tsumuki, H., Konno, H., Maeda, T., and Okamoto, Y. (1992). An ice-nucleating active fungus isolated from the gut of the rice stem borer, Chilo suppressalis Walker (Lepidoptera: Pyralidae). Journal of Insect Physiology 38, 119–125.CrossRefGoogle Scholar
Turnock, W. J. and Bodnaryk, R. P. (1993). The reversal of cold injury and its effect on the response to subsequent cold exposures. CryoLetters 14, 251–256.Google Scholar
Turnock, W. J. and Fields, P. G. (2005). Winter climates and cold hardiness in terrestrial insects. European Journal of Entomology 102, 561–576.CrossRefGoogle Scholar
Tursman, D., Duman, J. G., and Knight, C. A. (1994). Freeze tolerance adaptations in the centipede, Lithobius forficatus. Journal of Experimental Zoology 268, 347–353.CrossRefGoogle Scholar
Umina, P. A., Weeks, A. R., Kearney, M. R., McKechnie, S. W., and Hoffmann, A. A. (2005). A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Science 308, 691–693.CrossRefGoogle Scholar
Vali, G. (1995). Principles of ice nucleation. In Biological Ice Nucleation and its Applications, ed. Lee, R. E., Warren, G. J. and Gusta, L. V.. St. Paul: APS Press, pp. 1–28.Google Scholar
Vernon, P. and Vannier, G. (2002). Evolution of freezing susceptibility and freezing tolerance in terrestial arthropods. Comptes Rendus Biologies 325, 1185–1190.CrossRefGoogle Scholar
Voituron, Y., Mouquet, N., Mazancourt, C., and Clobert, J. (2002). To freeze or not to freeze? An evolutionary perspective on the cold-hardiness strategies of overwintering ectotherms. American Naturalist 160, 255–270.Google ScholarPubMed
Walters, K. R., Sformo, T., Barnes, B. M., and Duman, J. G. (2009). Freeze tolerance in an Alaska stonefly. Journal of Experimental Biology 212, 305–312.CrossRefGoogle Scholar
Wharton, D. A. and Ferns, D. J. (1995). Survival of intracellular freezing by the antarctic nematode Panagrolaimus davidi. Journal of Experimental Biology 198, 1381–1387.Google ScholarPubMed
Wharton, D. A., Goodall, G., and Marshall, C. J. (2003). Freezing survival and cryoprotective dehydration as cold tolerance mechanisms in the Antarctic nematode Panagrolaimus davidi. Journal of Experimental Biology 206, 215–221.CrossRefGoogle ScholarPubMed
Wilson, P. W., Heneghan, A. F., and Haymet, A. D. J. (2003). Ice nucleation in nature: supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology 46, 88–98.CrossRefGoogle ScholarPubMed
Worland, M. R., Grubor-Lajsic, G., and 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). Journal of Insect Physiology 44, 211–219.CrossRefGoogle Scholar
Worland, M. R., Wharton, D. A., and Byars, S. G. (2004). Intracellular freezing and survival in the freeze tolerant alpine cockroach Celatoblatta quinquemaculata. Journal of Insect Physiology 50, 225–232.CrossRefGoogle ScholarPubMed
Yancey, P. H. (2005). Organic osmolytes as compatible, metabolic and counteracting cryoprotectants in high osmolarity and other stresses. Journal of Experimental Biology 208, 2819–2830.CrossRefGoogle Scholar
Yi, S.-X. and Lee, R. E. (2004). In vivo and in vitro rapid cold hardening protects cells from cold-shock injury in the flesh fly. Journal of Comparative Physiology B 174, 611–615.CrossRefGoogle ScholarPubMed
Yi, S.-X. and Lee, R. E. (2005). Changes in gut and Malpighian tubule transport during seasonal acclimatization and freezing in the gall fly Eurosta solidaginis. Journal of Experimental Biology 208, 1895–1904.CrossRefGoogle ScholarPubMed
Yi, S.-X., Moore, C. W., and Lee, R. E. (2007). Rapid cold-hardening protects Drosophila melanogaster from cold-induced apoptosis. Apoptosis 12, 1183–1193.CrossRefGoogle ScholarPubMed
Zachariassen, K. E. (1985). Physiology of cold tolerance in insects. Physiological Reviews 65, 799–832.CrossRefGoogle ScholarPubMed
Zachariassen, K. E. (1991). The water relations of terrestrial arthropods. In Insects at Low Temperature, ed. Lee, R. E. and Denlinger, D. L.. New York and London: Chapman and Hall, pp. 47–63.CrossRefGoogle Scholar
Zachariassen, K. E. (1992). Ice nucleating agents in cold-hardy insects. In Water and Life, ed. Somero, G. N., Osmond, C. B. and Bolis, C. L.. Berlin: Springer-Verlag, pp. 261–281.CrossRefGoogle Scholar
Zachariassen, K. E. and Hammel, H. T. (1976). Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262, 285–287.CrossRefGoogle ScholarPubMed
Zachariassen, K. E. and Husby, J. A. (1982). Antifreeze effect of thermal hysteresis agents protects highly supercooled insects. Nature 298, 865–867.CrossRefGoogle Scholar
Zachariassen, K. E., Kristiansen, E., Perdersen, S. A., and Hammel, H. T. (2004). Ice nucleation in solutions and freeze-avoiding insects: homogeneous or heterogeneous?Cryobiology 48, 309–321.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×