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  • Cited by 96
  • Print publication year: 2010
  • Online publication date: May 2010

1 - A primer on insect cold-tolerance

from PART I - PHYSIOLOGICAL AND MOLECULAR RESPONSES

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.

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References
Acker, J. P. and McGann, L. E. (2003). Protective effect of intracellular ice during freezing?Cryobiology 46, 197–202.
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.
Angell, A. (1982). Supercooled water. In Water: A Comprehensive Treatise, ed. Franks, F., vol. 7. New York: Plenum Press, pp. 1–81.
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.
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.
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.
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.
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.
Campbell, E. M., Ball, A., Hoppler, S., and Bowman, A. (2008). Invertebrate aquaporins: a review. Journal of Comparative Physiology B 178, 935–955.
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.
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.
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.
Chown, S. L. and Nicolson, S. W. (2004). Insect Physiological Ecology: Mechanisms and Patterns. New York: Oxford University Press.
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.
Chown, S. L. and Terblanche, J. S. (2007). Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology 33, 50–152.
Clarke, C. J., Buckley, S. L., and Lindner, N. (2002). Ice structuring proteins: a new name for antifreeze proteins. CryoLetters 23, 89–92.
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.
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.
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.
Costanzo, J. P. and Lee, R. E. (2005). Cryoprotection by urea in a terrestrially hibernating frog. Journal of Experimental Biology 208, 4079–4089.
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.
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.
Crowe, J. H., Carpenter, J. F., and Crowe, L. M. (1998). The role of vitrification in anhydrobiosis. Annual Review of Physiology 60, 73–103.
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.
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.
Danks, H. V. (1971). Overwintering of some north temperate and arctic Chironomidae. II. Chironomid biology. Canadian Entomologist 103, 1875–1910.
Danks, H. V. (2000). Dehydration in dormant insects. Journal of Insect Physiology 46, 837–852.
Danks, H. V. (2007). How aquatic insects live in cold climates. Canadian Entomologist 139, 443–471.
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.
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.
Duman, J. G. (2001). Antifreeze and ice nucleator proteins in terrestrial arthropods. Annual Review of Physiology 63, 327–357.
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.
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.
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.
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.
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.
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.
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.
Fields, P. G. (1993). Reduction of cold tolerance of stored-product insects by ice-nucleating-active bacteria. Environmental Entomology 22, 470–476.
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.
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.
Fuller, B. J., Lane, N., and Benson, E. E. (eds.) (2004). Life in the Frozen State, Boca Raton: CRC Press.
Gehrken, U. and Southon, T. E. (1992). Supercooling in a freeze-tolerant cranefly larva, Tipula sp. Journal of Insect Physiology 38, 131–137.
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.
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.
Hawes, T. C. and Bale, J. S. (2007). Plasticity in arthropod cryotypes. Journal of Experimental Biology 210, 2585–2592.
Heinrich, B. (1993). The Hot-Blooded Insects: Strategies and Mechanisms of Thermoregulation. Cambridge, MA: Harvard University Press.
Hirsh, A. G., Williams, R. J., and Meryman, H. T. (1985). A novel method of natural cryoprotection. Plant Physiology 79, 41–56.
Holmstrup, M. (1995). Polyol accumulation in earthworm cocoons induced by dehydration. Comparative Biochemistry and Physiology A 111, 251–255.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Karow, A. M. (1991). Chemical cryoprotection of metazoan cells. BioScience 41, 155–160.
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.
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.
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.
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.
Kohshima, S. (1984). A novel cold-tolerant insect found in a Himalayan glacier. Nature 310, 225–227.
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.
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.
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.
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.
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.
Larcher, W. (2001). Physiological Plant Ecology: Ecophysiology and Stress Physiology of Functional Groups, 4th edn. New York: Springer.
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.
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.
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.
Lee, R. R. (1989). Insect cold-hardiness: to freeze or not to freeze. BioScience 39, 308–313.
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.
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.
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.
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.
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.
Lee, R. E. and Denlinger, D. L. (eds.) (1991). Insects at Low Temperature. New York: Chapman and Hall.
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.
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.
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.
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.
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.
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.
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.
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.
Levitt, J. (1980). Responses of Plants to Environmental Stresses, 2nd edn. New York: Academic Press, Inc.
Lindow, S. E. (1983). The role of bacterial ice nucleation in frost injury to plants. Annual Review of Phytopathology 21, 363–384.
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.
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.
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.
Meryman, H. T. (1968). Modified model for the mechanism of freezing injury in erythrocytes. Nature 218, 333–336.
Moore, M. V. and Lee, R. E. (1991). Surviving the big chill: overwintering strategies of aquatic and terrestrial insects. American EntomologistSummer111–118.
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.
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.
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.
Nedved, O. (2000). Snow White and the Seven Dwarfs: a multvariate approach to classification of cold tolerance. CryoLetters 21, 339–348.
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.
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.
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.
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.
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.
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.
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.
Ramlov, H. (1998). Letter to editor. CryoLetters 19, 4.
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.
Régnière, J. and Bentz, B. (2007). Modeling cold tolerance in the mountain pine beetle, Dendroctonus ponderosae. Journal of Insect Physiology 53, 559–572.
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.
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.
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.
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.
Ring, R. A. and Tesar, D. (1981). Adaptations to cold in Canadian Arctic insects. Cryobiology 18, 199–211.
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.
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.
Salt, R. W. (1959). Survival of frozen fat body cells in an insect. Nature 184, 1426.
Salt, R. W. (1961). Principles of insect cold-hardiness. Annual Review of Entomology 6, 55–74.
Salt, R. W. (1962). Intracelluar freezing in insects. Nature 193, 1207–1208.
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.
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.
Sinclair, B. J. (1999). Insect cold tolerance: how many kinds of frozen?European Journal of Entomology 96, 157–164.
Sinclair, B., Addo-Bediako, A., and Chown, S. L. (2003). Climatic variability and the evolution of insect freeze tolerance. Biological Reviews 78, 181–195.
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.
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.
Sømme, L. (1982). Supercooling and winter survival in terrestrial arthropods. Comparative Biochemistry and Physiology 73A, 519–543.
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.
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.
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.
Storey, K. B. and Storey, J. M. (1988). Freeze tolerance in animals. Physiological Reviews 68, 27–84.
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.
Storey, K. B. and Storey, J. M. (1996). Natural freezing survival in animals. Annual Review of Ecology and Systematics 27, 365–386.
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.
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.
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.
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.
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.
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.
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.
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.
Turnock, W. J. and Fields, P. G. (2005). Winter climates and cold hardiness in terrestrial insects. European Journal of Entomology 102, 561–576.
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.
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.
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.
Vernon, P. and Vannier, G. (2002). Evolution of freezing susceptibility and freezing tolerance in terrestial arthropods. Comptes Rendus Biologies 325, 1185–1190.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Zachariassen, K. E. (1985). Physiology of cold tolerance in insects. Physiological Reviews 65, 799–832.
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.
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.
Zachariassen, K. E. and Hammel, H. T. (1976). Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262, 285–287.
Zachariassen, K. E. and Husby, J. A. (1982). Antifreeze effect of thermal hysteresis agents protects highly supercooled insects. Nature 298, 865–867.
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.