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-g7b4s Total loading time: 0 Render date: 2025-05-03T05:26:00.688Z Has data issue: false hasContentIssue false

6 - Oxygen: Stress and adaptation in cold-hardy insects

from PART I - PHYSIOLOGICAL AND MOLECULAR RESPONSES

Published online by Cambridge University Press:  04 May 2010

By
Kenneth B. Storey  and
Janet M. Storey
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

Oxygen is critical to insect life. Oxygen-based respiration offers a tremendous advantage for cellular energetics by supporting high-efficiency production of ATP from the complete oxidation of substrates to CO2 and H2O and is an absolute requirement for powering insect flight muscles. However, once tied to aerobic respiration, organisms have to deal with various consequences of an oxygen-based life, including oxygen limitation (hypoxia, anoxia), oxygen overabundance (hyperoxia) and oxygen in its many reactive forms (e.g. superoxide, hydroperoxides, hydroxyl radical, etc.). The last cause oxidative stress, one of the most pervasive forms of cellular stress, since reactive oxygen species (ROS) can attack and damage most types of cellular macromolecules. This chapter looks at insect cold-hardiness from the point of view of the oxygen-related issues that are important for winter survival. We examine hypoxia/anoxia, freeze-induced ischemia, mitochondria, metabolic-rate depression, oxidative stress and antioxidants as they relate to the low-temperature biology of insects.

Oxygen challenges in winter

Although there are some unique insect solutions for dealing with winter (e.g. migration of monarch butterflies to Mexico or shivering thermogenesis to provide central heating for honey bee colonies), terrestrial insects generally employ three basic options (sometimes in combination) to survive the cold winter months – underground hibernation below the frostline (in burrows or by digging), freeze-avoidance by supercooling, or freeze-tolerance.

Type
Chapter
Information
Low Temperature Biology of Insects , pp. 141 - 165
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

Baird, N. A., Turnbull, D. W. and Johnson, E. A. (2006). Induction of the heat shock pathway during hypoxia requires regulation of heat shock factor by hypoxia-inducible factor-1. Journal of Biological Chemistry 281, 38675–38681.CrossRefGoogle ScholarPubMed
Bennett, V. V., Pruitt, N. L. and Lee, R. E. (1997). Seasonal changes in fatty acid composition associated with cold-hardening in third instar larvae of Eurosta solidaginis. Journal of Comparative Physiology B 167, 249–255.CrossRefGoogle Scholar
Burg, M. B. (1995). Molecular basis of osmotic regulation. American Journal of Physiology 268, F983–F996.Google ScholarPubMed
Burmester, T. and Hankeln, T. (2007). The respiratory proteins of insects. Journal of Insect Physiology 53, 285–294.CrossRefGoogle ScholarPubMed
Cadenas, E. (1995). Mechanism of oxygen activation and reactive oxygen species detoxification. In Oxidative Stress and Antioxidant Defenses in Biology, ed. Ahmad, S.. New York: Chapman & Hall, pp. 1–61.Google Scholar
Chen, B., Kayukawa, T., Monteiro, A. and Ishikawa, Y. (2006). Cloning and characterization of the HSP70 gene and its expression in response to diapauses and thermal stress in the onion maggot, Delia antiqua. Journal of Biochemistry and Molecular Biology 39, 749–58.Google ScholarPubMed
Churchill, T. A. and Storey, K. B. (1989). Metabolic consequences of rapid cycles of temperature change for freeze avoiding versus freeze tolerant insects. Journal of Insect Physiology 35, 579–586.CrossRefGoogle Scholar
Danks, H. V. (1971). Overwintering in some north temperate and arctic Chironomidae. Canadian Entomologist 103, 1875–1901.CrossRefGoogle Scholar
Danks, H. V. (2007). How aquatic insects live in cold climates. Canadian Entomologist 139, 443–447.CrossRefGoogle Scholar
Denlinger, D. L. (2002). Regulation of diapause. Annual Review of Entomology 47, 93–122.CrossRefGoogle ScholarPubMed
English, T. E. and Storey, K. B. (2003). Freezing and anoxia stresses induce expression of metallothionein in the foot muscle and hepatopancreas of the marine gastropod, Littorina littorea. Journal of Experimental Biology 206, 2517–2524.CrossRefGoogle Scholar
Feng, Q. L., Davey, K. G., Pang, A. S. D., Ladd, T. R., Retnakaran, A., Tomkins, B. L., Zheng, S. and Palli, S. R. (2001). Developmental expression and stress induction of glutathione S-transferase in the spruce budworm, Choristoneura fumiferana: developmental expression and the induction by various stresses. Journal of Insect Physiology 47, 1–10.CrossRefGoogle Scholar
Fielenbach, N. and Antebi, A. (2008). C. elegans dauer formation and the molecular basis of plasticity. Genes and Development 22, 2149–2165.CrossRefGoogle ScholarPubMed
Fridovich, I. (1998). Oxygen toxicity: a radical explanation. Journal of Experimental Biology 201, 1203–1209.Google ScholarPubMed
Furusawa, T., Shikata, M. and Yamashita, O. (1982). Temperature dependent sorbitol utilization in diapause eggs of the silkworm, Bombyx mori. Journal of Comparative Physiology B 147, 21–26.CrossRefGoogle Scholar
Gorr, T. A., Gassmann, M. and Wappner, P. (2006). Sensing and responding to hypoxia via HIF in model invertebrates. Journal of Insect Physiology 52, 349–364.CrossRefGoogle ScholarPubMed
Gulevsky, A. K., Relina, L. I., and Grishchenkova, Y. A. (2006). Variations of the antioxidant system during development of the cold-tolerant beetle, Tenebrio molitor. Cryo-Letters 27, 283–290.Google ScholarPubMed
Harrison, J., Frazier, M. R., Henry, J. R., Kaiser, A., Klok, C. J. and Rascón, B. (2006). Responses of terrestrial insects to hypoxia or hyperoxia. Respiratory Physiology and Neurobiology 154, 4–17.CrossRefGoogle ScholarPubMed
Hentze, M. W., Muckenthaler, M. U. and Andrews, N. C. (2004). Balancing acts: molecular control of mammalian iron metabolism. Cell 117, 285–297.CrossRefGoogle ScholarPubMed
Hermes-Lima, M. (2004). Oxygen in biology and biochemistry: role of free radicals. In Functional Metabolism: Regulation and Adaptation, ed. Storey, K. B.. Hoboken, N. J.: Wiley-Liss, pp. 319–368.Google Scholar
Hermes-Lima, M. and Zenteno-Savín, T. (2002). Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comparative Biochemistry and Physiology 133, 537–556.Google ScholarPubMed
Hermes-Lima, M., Storey, J. M. and Storey, K. B. (2001). Antioxidant defenses and animal adaptation to oxygen availability during environmental stress. In Cell and Molecular Responses to Stress, ed. Storey, K. B. and Storey, J. M.. vol. 2: Protein Adaptations and Signal Transduction. Amsterdam: Elsevier Press, pp. 263–287.Google Scholar
Hoback, W. W. and Stanley, D. W. (2001). Insects in hypoxia. Journal of Insect Physiology 47, 533–542.CrossRefGoogle ScholarPubMed
Hochachka, P. W. and Somero, G. N. (1984) Biochemical Adaptation. Princeton, N. J.: Princeton University Press.CrossRefGoogle Scholar
Hochachka, P. W., Buck, L. T., Doll, C. J. and Land, S. C. (1996). Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proceedings of the National Academy of Sciences, USA 93, 9493–9498.CrossRefGoogle ScholarPubMed
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
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
Joanisse, D. R. and Storey, K. B. (1994). Mitochondrial enzymes during overwintering in two species of cold-hardy gall insects. Insect Biochemistry and Molecular Biology 24, 145–150.CrossRefGoogle Scholar
Joanisse, D. R. and Storey, K. B. (1996a). Fatty acid content and enzymes of fatty acid metabolism in overwintering cold-hardy gall insects. Physiological Zoology 69, 1079–1095.CrossRefGoogle Scholar
Joanisse, D. R. and Storey, K. B. (1996b). Oxidative stress and antioxidants during overwintering in larvae of cold-hardy goldenrod gall insects. Journal of Experimental Biology 199, 1483–1491.Google ScholarPubMed
Joanisse, D. R. and Storey, K. B. (1998). Oxidative stress and antioxidants in stress and recovery of cold-hardy insects. Insect Biochemistry and Molecular Biology 28, 23–30.CrossRefGoogle Scholar
Jovanovic-Galovic, A., Blagojevic, D. P., Grubor-Lajsic, G., Worland, M. R. and Spasic, M. B. (2007). Antioxidant defense in mitochondria during diapause and postdiapause development of European corn borer (Ostrinia nubilalis, Hubn.). Archives of Insect Biochemistry and Physiology 64, 111–119.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
Kukal, O., Duman, J. G. and Seriani, A. S. (1989). Cold-induced mitochondrial degradation and cryoprotectant synthesis in freeze-tolerant arctic caterpillars. Journal of Comparative Physiology B 158, 661–671.CrossRefGoogle ScholarPubMed
Larade, K. and Storey, K. B. (2004). Accumulation and translation of ferritin heavy chain transcripts following anoxia exposure in a marine invertebrate. Journal of Experimental Biology 207, 1353–1360CrossRefGoogle Scholar
Lavista-Llanos, S., Centanin, L., Irisarri, M., Russo, D. M., Gleadle, J. M.Bocca, S. N., Muzzopappa, M., Ratcliffe, P. J. and Wappner, P. (2002). Control of the hypoxic response in Drosophila melanogaster by the basic helix-loop-helix PAS protein similar. Molecular and Cellular Biology 22, 6842–6853.CrossRefGoogle ScholarPubMed
Lee, K. S., Kim, B. Y., Kim, H. J., Seo, S. J., Yoon, H. J., Choi, Y. S., Kim, I., Han, Y. S., Je, Y. H., Lee, S. M., Kim, D. H., Sohn, H. D. and Jin, B. R. (2006). Transferrin inhibits stress-induced apoptosis in a beetle. Free Radicals in Biology and Medicine 41, 1151–1161.CrossRefGoogle Scholar
Levin, D. B., Danks, H. V. and Barber, S. A. (2003). Variations in mitochondrial DNA and gene transcription in freezing-tolerant larvae of Eurosta solidaginis (Diptera: Tephritidae) and Gynaephora groenlandica (Lepidoptera: Lymantriidae). Insect Molecular Biology 12, 281–289.CrossRefGoogle Scholar
Lighton, J. R. and Schilman, P. E. (2007). Oxygen reperfusion damage in an insect. PLoS ONE 2(12):e1267.CrossRefGoogle Scholar
Lundheim, R. and Zachariassen, K. E. (1993). Water balance of overwintering beetles in relation to strategies for cold tolerance. Journal of Comparative Physiology B 163, 1–4.CrossRefGoogle Scholar
McMullen, D. C. (2004). Molecular and biochemical adaptations conferring cold hardiness in two gall insects. Ph. D. thesis, Carleton University.
McMullen, D. C. and Storey, K. B. (2008a). Mitochondria of cold hardy insects: responses to cold and hypoxia assessed at enzymatic, mRNA and DNA levels. Insect Biochemistry and Molecular Biology 38, 367–373.CrossRefGoogle ScholarPubMed
McMullen, D. C. and Storey, K. B. (2008b). 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
Michaud, R. M. 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.CrossRefGoogle ScholarPubMed
Morin, P., McMullen, D. C. and Storey, K. B. (2005). HIF-1α involvement in low temperature and anoxia survival by a freeze tolerant insect. Molecular and Cellular Biochemistry 280, 99–106.CrossRefGoogle ScholarPubMed
Morin, P. and Storey, K. B. (2008). Mammalian hibernation: differential gene expression and novel application of epigenetic controls. International Journal of Developmental Biology 53, 433–442.CrossRefGoogle Scholar
Nambu, J. R., Chen, W., Hu, S. and Crews, S. T. (1996). The Drosophila melanogaster similar bHLH-PAS gene encodes a protein related to human hypoxia inducible factor 1 alpha and Drosophila single-minded. Gene 172, 249–254.CrossRefGoogle ScholarPubMed
Pedersen, S. A., Kristiansen, E., Andersen, R. A. and Zachariassen, K. E. (2007). Isolation and preliminary characterization of a Cd-binding protein from Tenebrio molitor (Coleoptera). Comparative Biochemistry and Physiology C 145, 457–463.Google Scholar
Pedersen, S. A., Kristiansen, E., Hansen, B. H., Andersen, R. A. and Zachariassen, K. E. (2006). Cold hardiness in relation to trace metal stress in the freeze-avoiding beetle Tenebrio molitor. Journal of Insect Physiology 52, 846–853.CrossRefGoogle ScholarPubMed
Redecker, B. and Zebe, E. (1988). Anaerobic metabolism in aquatic insect larvae – studies on Chironomus thummi and Culex pipiens. Journal of Comparative Physiology B 158, 307–315.CrossRefGoogle Scholar
Rhee, S. G., Kang, S. W., Jeong, W., Chang, T. S., Yang, K. S. and Woo, H. A. (2005). Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Current Opinion in Cell Biology 17, 183–189.CrossRefGoogle ScholarPubMed
Rickards, J., Kelleher, M. J. and Storey, K. B. (1987). Strategies of freeze avoidance in larvae of the goldenrod gall moth, Epiblema scudderiana: winter profiles of a natural population. Journal of Insect Physiology 33, 443–450.CrossRefGoogle Scholar
Rinehart, J. P., Li, A., Yocum, G. D., Robich, R. M., Hayward, S. A. 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
Roelofs, D., Aarts, M. G. M., Schat, H. and Straalen, N. M. (2008). Functional ecological genomics to demonstrate general and specific responses to abiotic stress. Functional Ecology 22, 8–18.Google Scholar
Semenza, G. L. (2003). Targeting HIF-1 for cancer therapy. Nature Reviews on Cancer 3, 721–732.CrossRefGoogle ScholarPubMed
Sim, C. and Denlinger, D. L. (2008). Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proceedings of the National Academy of Sciences, USA 105, 6777–6781.CrossRefGoogle ScholarPubMed
Sonoda, S., Fukumoto, K., Izumi, Y., Yoshida, H. and Tsumuki, H. (2006). Cloning of heat shock protein genes (hsp90 and hsc70) and their expression during larval diapause and cold tolerance acquisition in the rice stem borer, Chilo suppressalis Walker. Archives of Insect Biochemistry and Physiology 63, 36–47.CrossRefGoogle ScholarPubMed
Storey, K. B. (2004). Strategies for exploration of freeze responsive gene expression: advances in vertebrate freeze tolerance. Cryobiology 48, 134–145.CrossRefGoogle ScholarPubMed
Storey, K. B. (2006). Reptile freeze tolerance: metabolism and gene expression. Cryobiology 52, 1–16.CrossRefGoogle ScholarPubMed
Storey, J. M. and Storey, K. B. (1985). Freezing and cellular metabolism in the gall fly larva, Eurosta solidaginis. Journal of Comparative Physiology B 155, 333–337.CrossRefGoogle Scholar
Storey, K. B. and Storey, J. M. (1990a). Carbon balance and energetics of cryoprotectant synthesis in a freeze-tolerant insect: responses to perturbation by anoxia. Journal of Comparative Physiology B 160, 77–84.CrossRefGoogle Scholar
Storey, K. B. and Storey, J. M. (1990b). Facultative metabolic rate depression: molecular regulation and biochemical adaptation in anaerobiosis, hibernation, and estivation. Quarterly Review of Biology 65, 145–174.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.. New York: 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
Storey, K. B. and Storey, J. M. (2004). Metabolic rate depression in animals: transcriptional and translational controls. Biological Reviews of the Cambridge Philosophical Society 79, 207–233.CrossRefGoogle ScholarPubMed
Storey, K. B. and Storey, J. M. (2007). Putting life on “pause” – molecular regulation of hypometabolism. Journal of Experimental Biology 210, 1700–1714.CrossRefGoogle ScholarPubMed
Storey, K. B. and Storey, J. M. (1981). Biochemical strategies of overwintering in the gall fly larva, Eurosta solidaginis: effect of low temperature acclimation on the activities of enzymes of intermediary metabolism. Journal of Comparative Physiology B 144, 191–199.CrossRefGoogle Scholar
Viarengo, A., Burlando, B., Cavaletto, M., Marchi, B., Ponzano, E. and Blasco, J. (1999). Role of metallothionein against oxidative stress in the mussel Mytilus galloprovincialis. American Journal of Physiology 277, R1612–R1619.Google ScholarPubMed
Woodman, J. D., Cooper, P. D. and Haritos, V. S. (2007). Cyclic gas exchange in the giant burrowing cockroach, Macropanesthia rhinoceros: effect of oxygen tension and temperature. Journal of Insect Physiology 53, 497–504.CrossRefGoogle ScholarPubMed
Zachariassen, K. E., Kristiansen, E. and Pedersen, S. A. (2004). Inorganic ions in cold-hardiness. Cryobiology 48, 126–133.CrossRefGoogle ScholarPubMed
Zachariassen, K. E., Li, N. G., Laugsand, A. E., Kristiansen, E., and Pedersen, S. A. (2008). Is the strategy for cold hardiness in insects determined by their water balance? A study on two closely related families of beetles: Cerambycidae and Chrysomelidae. Journal of Comparative Physiology B 178, 977–984.CrossRefGoogle ScholarPubMed
Zhang, G. J. (2006). Protein chaperones and winter cold hardiness in insects: heat shock proteins and glucose regulated proteins in freeze-tolerant and freeze-avoiding species. M.Sc. thesis, Department of Chemistry, Carleton University.Google Scholar

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
×