Skip to main content Accessibility help
×
Home
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 30
  • Print publication year: 2010
  • Online publication date: May 2010

2 - Rapid cold-hardening: Ecological significance and underpinning mechanisms

from PART I - PHYSIOLOGICAL AND MOLECULAR RESPONSES

Summary

Introduction

Insects are constantly subjected to changes in environmental temperature. Most studies of insect acclimation to low temperature concern seasonal changes that occur over weeks or months in preparation for winter, and, accordingly, most chapters in this volume focus on seasonal cold-hardening. In contrast, during the past 10 years considerable attention has been paid to rapid acclimatory responses to both high (i.e. induction of heat shock or stress proteins (Feder et al., 2002) and low temperature. This chapter summarizes our current understanding of the rapid cold-hardening (RCH) response. When our previous book (Lee and Denlinger, 1991) was being written, the RCH response had only just been described and merited only a few scattered paragraphs. Indeed, at that time it was unclear whether this response was merely a laboratory artifact or a previously unrecognized type of rapid acclimation. Since then, the RCH response has emerged as a highly conserved trait, allowing diverse insect groups to swiftly adjust their physiological state and organismal performance to match even modest changes in environmental temperature. In this chapter, we summarize evidence supporting the ecological relevance and emerging physiological underpinnings of the RCH response.

The RCH response protects against a form of non-freezing injury known as cold-shock or direct-chilling injury. Cold-shock injury is well known among microbes, plants and animals, and represents a major obstacle for the successful cryopreservation of many types of cells and tissues (Grout, 1987). Injury is not associated with internal ice formation.

References
Bahrndorff, S., Loeschcke, V., Pertoldi, C., Beier, C., and Holmstrup, M. (2009). The rapid cold hardening response of Collembola is influenced by thermal variability of the habitat. Functional Ecology 23, 340–347
Bale, J. S. (2002). Insects and low temperatures: from molecular biology to distributions and abundance. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 357, 849–861.
Baust, J. M., Buskirk, R., and Baust, J. G. (2002). Gene activation of the apoptotic caspase cascade following cryogenic storage. Cell Preservation Technology 1, 63–80.
Broufas, G. D. and Koveos, D. S. (2001). Rapid cold hardening in the predatory mite Euseius (Amblyseius) finlandicus (Acari: Phytoseiidae). Journal of Insect Physiology 47, 699–708.
Burks, C. S. and Hagstrum, D. W. (1999). Rapid cold hardening capacity in five species of coleopteran pests of stored grain. Journal of Stored Products Research 35, 65–75.
Burton, V., Mitchell, H. K., Young, P., and Petersen, N. S. (1988). Heat shock protection against cold stress of Drosophila melanogaster. Molecular and Cellular Biology 8, 3550–3552.
Chen, C.-P. and Walker, V. K. (1994). Cold-shock and chilling tolerance in Drosophila. Journal of Insect Physiology 40, 661–669.
Chen, C. P., Denlinger, D. L., and Lee, R. E. (1987). Cold-shock injury and rapid cold hardening in the flesh fly Sarcophaga crassipalpis. Physiological Zoology 60, 297–304.
Chown, S. L. and Terblanche, J. S. (2007). Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology 33, 50–152.
Coulson, S. J. and Bale, J. S. (1990). Characterization and limitations of the rapid cold-hardening response in the house fly Musca domestica (Diptera: Muscidae). Journal of Insect Physiology 36, 207–211.
Coulson, S. J. and Bale, J. S. (1991). Anoxia induces rapid cold hardening in the house fly Musca domestica (Diptera: Muscidae). Journal of Insect Physiology 37, 497–501.
Coulson, S. C. and Bale, J. S. (1992). Effect of rapid cold hardening on reproduction and survival of offspring in the house fly Musca domestica. Journal of Insect Physiology 38, 421–424.
Coulson, S. J., Fisher, J., and Bale, J. S. (1992). A 31P NMR investigation of the energy charge of the house fly Musca domestica (Diptera: Muscidae) during rapid cold hardening and cold shock. CryoLetters 13, 183–192.
Crockett, E. L. (1998). Cholesterol function in plasma membranes from ectotherms: membrane-specific roles in adaptation to temperatures. American Zoologist 38, 291–304.
Czajka, M. C. and Lee, R. E. (1990). A rapid cold-hardening response protecting against cold shock injury in Drosophila melanogaster. Journal of Experimental Biology 148, 245–254.
David, J. R., Gibert, P., Moreteau, B., Gilchrist, G. W., and Huey, R. B. (2003). The fly that came in from the cold: geographic variation of recovery time from low-temperature exposure in Drosophila subobscura. Functional Ecology 17, 425–430.
David, R. J., Gibert, P., Pla, E., Petavy, G., Karan, D., and Moreteau, B. (1998). Cold stress tolerance in Drosophila: analysis of chill coma recovery in D. melanogaster. Journal of Thermal Biology 23, 291–299.
Denlinger, D. L., Joplin, K. H., Chen, C. P., and Lee, R. E. (1991). Cold shock and heat shock. In Insects at Low Temperature, ed. Lee, R. E., and Denlinger, D. L.. New York: Chapman and Hall, pp. 131–148.
Drobnis, E. Z., Crowe, L. M., Berger, T., Anchordoguy, T. J., Overstreet, J. W., and Crowe, J. H. (1993). Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model. Journal of Experimental Zoology 265, 432–437.
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.
Feder, M. E., Bedford, T. C., Albright, D. R., and Michalak, P. (2002). Evolvability of Hsp70 expression under artificial selection for inducible thermotolerance in independent populations of Drosophila melanogaster. Physiological and Biochemical Zoology 75, 325–334.
Fuchs, B. C. and Bode, B. P. (2006). Stressing out over survival: glutamine as an apoptotic modulator. Journal of Surgical Research 131, 26–40.
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.
Grout, B. W. (1987). Direct chilling injury. In The Effects of Low Temperatures on Biological Systems, ed. Grout, B. W.. and Morris, G. J.. London: Edward Arnold, pp. 120–146.
Hazel, J. R. (1995). Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation?Annual Review of Physiology 57, 19–42.
Jagdale, G. B., Parwinder, S. G., and Salmnen, S. O. (2005). Both heat-shock and cold-shock influence trehalose metabolism in an entomopathogenic nematode. Journal of Parasitology 91, 988–994.
Joplin, K. H. and Denlinger, D. L. (1990). Developmental and tissue specific control of the heat shock induced 70kDa related proteins in the flesh fly, Sarcophaga crassipalpis. Journal of Insect Physiology 36, 239–249.
Kelty, J. (2007). Rapid cold-hardening of Drosophila melanogaster in a field setting. Physiological Entomology 32, 343–350.
Kelty, J. D., Killian, K. A., and Lee, R. E. (1996). Cold shock and rapid cold-hardening of pharate adult flesh flies (Sarcophaga crassipalpis): effects on behaviour and neuromuscular function following eclosion. Physiological Entomology 21, 283–288.
Kelty, J. D. and Lee, R. E. (1999). Induction of rapid cold-hardening by cooling at ecologically relevant rates in Drosophila melanogaster. Journal of Insect Physiology 45, 719–726.
Kelty, J. D. and Lee, R. E. (2001). Rapid cold-hardening of Drosophila melanogaster (Diptera: Drosophilidae) during ecologically based thermoperiodic cycles. Journal of Experimental Biology 204, 1659–1666.
Kim, Y. and Kim, N. (1997). Cold hardiness in Spodoptera exigua (Lepidoptera: Noctuidae). Environmental Entomology 26, 1117–1123.
Kim, Y.-S., Denlinger, D. L., and Smith, B. (2005). Spatial conditioning in the flesh fly, Sarcophaga crassipalpis: disruption of learning by cold shock and protection by rapid cold hardening. Journal of Asia-Pacific Entomology 8, 345–351.
Klok, C. J., Chown, S. L., and Gaston, K. J. (2003). The geographical range structure of the holly leaf-miner. III. Cold-hardiness physiology. Functional Ecology 17, 858–868.
Koveos, D. S. (2001). Rapid cold hardening in the olive fruit fly Bactrocera oleae under laboratory and field conditions. Entomologia Experimentalis et Applicata 101, 257–263.
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.
Larsen, K. J., Lee, R. E., and Nault, L. R. (1993). Influence of developmental conditions on cold-hardiness of adult Dalbulus leafhoppers – implications for overwintering. Entomologia Experimentalis et Applicata 67, 99–108.
Lee, R. E., Chen, C. P., and Denlinger, D. L. (1987). A rapid cold-hardening process in insects. Science 238, 1415–1417.
Lee, R. E. and Denlinger, D. L. (1991). Insects at Low Temperature. New York: Chapman and Hall.
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.
Leopold, R. A. (1998). Cold storage of insects for 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. 235–267.
Li, A. and Denlinger, D. L. (2008). Rapid cold hardening elicits changes in brain protein profiles of the flesh fly, Sarcophaga crassipalpis. Insect Molecular Biology 17, 565–572.
Li, Y., Gong, H., and Park, H. Y. (1999). Characterization of rapid cold-hardiness response in the overwintering mature larvae of pine needle gall midge, Thecodiplosis japonensis. CryoLetters 20, 383–392.
Mangan, R. L. and Hallman, G. J. (1998). Temperature treatments for quarantine security: new approaches for fresh commodities. In Temperature Sensitivity in Insects and Application in Integrated Pest Management, ed. Hallman, G. J. and Denlinger, D. L.. Boulder: Westview Press, pp. 201–234.
Massip, A., Leibo, S. P., and Blesbios, E. (2004). Cryobiology of gametes and the breeding of domestic animals. In Life in the Frozen State, ed. Fuller, B. J., Lane, N. and Benson, E. E.. Boca Raton: CRC Press, pp. 371–392.
McDonald, J. R., Bale, J. S., and Walters, K. A. (1997). Rapid cold hardening in the western flower thrips Frankliniella occidentalis. Journal of Insect Physiology 43, 759–766.
McElhaney, R. N. (1974). The effect of alterations in the physical state of the membrane lipids on the ability of Acholeplasma laidlawii B to grow at various temperatures. Journal of Molecular Biology 84, 145–157.
Michaud, M. R. and Denlinger, D. L. (2006). Oleic acid is elevated in cell membranes during rapid cold-hardening and pupal diapause in the flesh fly, Sarcophaga crassipalpis. Journal of Insect Physiology 52, 1073–1082.
Michaud, M. R. and Denlinger, D. L. (2007). Shifts in carbohydrate, polyol, and amino acid pools during rapid cold hardening and diapause-associated cold hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. Journal of Comparative Physiology B 177, 753–763.
Monroy, A. F. and Dhindsa, R. S. (1995). Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25°C. Plant Cell 7, 321–331.
Murakami, M., Kondo, T., Sato, S., Li, Y., and Chan, P. H. (1997). Occurrence of apoptosis following cold injury-induced brain edema in mice. Neuroscience 81, 231–237.
Murata, N. and Los, D. A. (1997). Membrane fluidity and temperature perception. Plant Physiology 115, 875–879.
Nunamaker, R. A. (1993). Rapid cold-hardening in Culicoides variipennis sonorensis (Diptera: Ceratopogonidae). Journal of Medical Entomology 30, 913–917.
Orvar, B. L., Sangwan, V., Omann, F., and Dhindsa, R. S. (2000). Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant Journal 23, 785–794.
Overgaard, J., Malmendal, A., Sørenson, J. G., Bundy, J. G., Loeschcke, V., Nielsen, N. C., and Holmstrup, M. (2007). Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. Journal of Insect Physiology 53, 1218–1232.
Overgaard, J., Sørensen, J. G., Petersen, S. O., Loeschcke, V., and Holmstrup, M. (2005). Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. Journal of Insect Physiology 51, 1173–1182.
Overgaard, J. and Sørensen, J. G. (2008). Rapid thermal adaptation during field temperature variations in Drosophila melanogaster. Cryobiology 56, 159–162.
Phanvijhitsiri, K., Musch, M. W., Ropeleski, M. J., and Chang, E. B. (2005). Molecular mechanisms of L-glutamine modulation of heat stimulated Hsp25 production. FASEB Journal 19, A1496–A1497.
Powell, S. J. and Bale, J. S. (2004). Cold shock injury and ecological costs of rapid cold hardening in the grain aphid Sitobion avenae (Hemiptera: Aphididae). Journal of Insect Physiology 50, 277–284.
Powell, S. J. and Bale, J. S. (2005). Low temperature acclimated populations of the grain aphid Sitobion avenae retain ability to rapidly cold harden with enhanced fitness. Journal of Experimental Biology 208, 2615–2620.
Powell, S. J. and Bale, J. S. (2006). Effect of long-term and rapid cold-hardening on the cold torpor temperature of an aphid. Physiological Entomology 31, 348–352.
Qin, W., Neal, S. J., Robertson, R. M., Westwood, J. T., and Walker, V. K. (2005). Cold hardening and transcriptional change in Drosophila melanogaster. Insect Molecular Biology 14, 607–613.
Rako, L. and Hoffman, A. A. (2006). Complexity of the cold acclimation response in Drosophila melanogaster. Journal of Insect Physiology 52, 94–104.
Rinehart, J. P., Yocum, G. D., and Denlinger, D. L. (2000). Thermotolerance and rapid cold hardening ameliorate the negative effects of brief exposures to high or low temperatures on fecundity in the flesh fly, Sarcophaga crassipalpis. Physiological Entomology 25, 330–336.
Rosales, A. L., Krafsur, E. S., and Kim, Y. (1994). Cryobiology of the face fly and house fly (Diptera: Muscidae). Journal of Medical Entomology 31, 671–680.
Shintani, Y. and Ishikawa, Y. (2007). Relationship between rapid cold-hardening and cold acclimation in the eggs of the yellow-spotted longicorn beetle, Psacothea hilaris. Journal of Insect Physiology 53, 1055–1062.
Shreve, S. M., Kelty, J. D., and Lee, R. E. (2004). Preservation of reproductive behaviors during modest cooling: rapid cold-hardening fine-tunes organismal response. Journal of Experimental Biology 207, 1797–1802.
Shreve, S. M., Yi, S.-X., and Lee, R. E. (2007) Increased dietary cholesterol enhances cold tolerance in Drosophila melanogaster. CryoLetters 28, 33–37.
Sinclair, B. J. and Chown, S. L. (2006). Rapid cold-hardening in a Karoo beetle, Afrinus sp. Physiological Entomology 31, 98–101.
Sinclair, B. J., Klok, C. J., Scott, M. B., Terblanche, J. S., and Chown, S. L. (2003). Diurnal variation in supercooling points of three species of Collembola from Cape Hallett, Antarctica. Journal of Insect Physiology 49, 1049–1061.
Smallwood, M. and Bowles, D. J. (2002). Plants in a cold climate. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 357, 831–846.
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.
Terblanche, J. S., Clusella-Trullas, S., Deere, J. A., and Chown, S. L. (2008). Thermal tolerance in a south-east African population of the tsetse fly Glossina pallidipes (Diptera, Glossinidae): implications for forecasting climate change impacts. Journal of Insect Physiology 54, 114–127.
Terblanche, J. S., Marais, E., and Chown, S. L. (2007). Stage-related variation in rapid cold hardening as a test of the environmental predictability hypothesis. Journal of Insect Physiology 53, 455–462.
ThompsonJr., G. A. Jr., G. A. (1983). Mechanisms of homeoviscous adaptation in membranes. In Cellular Acclimatisation to Environmental Change, ed. Cossins, A. R. and Sheterline, P.. Cambridge: Cambridge University Press, pp. 33–54.
Wang, X. and Kang, L. (2003). Rapid cold hardening in young hoppers of the migratory locust Locusta migratoria L. (Orthoptera: Acridiidae). CryoLetters 24, 331–340.
Watanabe, M., Kikawada, T., Minagawa, N., Yukuhiro, F., and Okuda, T. (2002). Mechanism allowing an insect to survive complete dehydration and extreme temperatures. Journal of Experimental Biology 205, 2799–2802.
Worland, M. R. and Convey, P. (2001). Rapid cold hardening in Antarctic microarthropods. Functional Ecology 15, 515–524.
Worland, M. R., Convey, P., and Lukešovà, A. (2000). Rapid cold hardening: a gut feeling. CryoLetters 21, 315–324.
Worland, M. R., Hawes, T. C., and Bale, J. S. (2007). Temporal resolution of cold acclimation and de-acclimation in the Antarctic collembolan, Cryptopygus antarcticus. Physiological Entomology 32, 233–239.
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., Yin, C. M., and Nordin, J. H. (1987). The in vitro biosynthesis and secretion of glycerol by larval fat bodies of chilled Ostrinia nubilalis. Journal of Insect Physiology 33, 523–528.
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.
Yocum, G. D. and Denlinger, D. L. 1994. Anoxia blocks thermotolerance and the induction of rapid cold hardening in the flesh fly, Sarcophaga crassipalpis. Physiological Entomology 19, 152–158.
Yoder, J., Benoit, J. B., Denlinger, D. L., and Rivers, D. B. (2006). Stress-induced accumulation of glycerol in the flesh fly, Sarcophaga bullata: Evidence indicating anti-desiccant and cryoprotectant functions of this polyol and a role for the brain in coordinating the response. Journal of Insect Physiology 52, 202–214.