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7 - Interactions between cold, desiccation and environmental toxins

from PART I - PHYSIOLOGICAL AND MOLECULAR RESPONSES

Published online by Cambridge University Press:  04 May 2010

David L. Denlinger
Affiliation:
Ohio State University
Richard E. Lee, Jr
Affiliation:
Miami University
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Summary

Introduction

Climatic stressors are environmental factors of paramount importance for biological systems. Numerous examples from terrestrial plants and animals show that, in particular, cold and drought are factors that dictate the distribution of species (for a review see Hoffmann and Parsons, 1991). Indeed, sediment records of insect remains have been convincingly used to reconstruct past climates (e.g. Atkinson et al., 1987). Other important types of stress that should also be considered are environmental toxins. These may be of anthropogenic origin, but most originate from natural sources. Potentially toxic trace metals are released into ground water by demineralization of rocks and minerals and enter the food chain via plants. A wide variety of toxic organic compounds are produced by aquatic as well as terrestrial plants and animals as protection against herbivory or predation. Insects (and all other animals) have, during evolution, developed adaptive detoxifying mechanisms to cope with toxic stress. These protective systems are further challenged due to increasing levels of anthropogenic chemical pollution (e.g. pesticides and heavy metals) that have been inflicted on the biosphere at a global scale. Environmental toxins per se can have negative effects on the functioning of organisms, but the possibility also exists that some of these chemicals can impact tolerance mechanisms to dominating climatic variables such as cold and drought.

Insects and other organisms have evolved sophisticated physiological and biochemical mechanisms to cope with different environmental stressors.

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Publisher: Cambridge University Press
Print publication year: 2010

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References

Atkinson, T. C., Briffa, K. R., and Coope, G. R. (1987). Seasonal temperatures in Britain during the past 22 000 years, reconstructed using beetle remains. Nature 325, 587–592.CrossRefGoogle Scholar
Bahrndorff, S., Petersen, S. O., Loeschcke, V., Overgaard, J., and Holmstrup, M. (2007). Differences in cold and drought tolerance of high arctic and subarctic populations of Megaphorura arctica (Collembola). Cryobiology 55, 315–323.CrossRefGoogle Scholar
Bahrndorff, S., Tunnacliffe, A., Wise, M. J., McGee, B., Holmstrup, M., and Loeschcke, V. (2009). Bioinformatics and protein expression analyses implicate LEA proteins in the drought response of Collembola. Journal of Insect Physiology, 55, 210–217.CrossRefGoogle ScholarPubMed
Bayley, M. and Holmstrup, M. (1999). Water vapor absorption in arthropods by accumulation of myoinositol and glucose. Science 285, 1909–1911.CrossRefGoogle ScholarPubMed
Bayley, M., Petersen, S. O., Knigge, T., Köhler, H. R., and Holmstrup, M. (2001). Drought acclimation confers cold tolerance in the soil collembolan Folsomia candida. Journal of Insect Physiology 47, 1197–1204.CrossRefGoogle ScholarPubMed
Bennett, V. A., Sformo, T., Walters, K., Toien, O., Jeannet, K., Hochstrasser, R., Pan, Q. F., 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): roles of antifreeze proteins, polyols, dehydration and diapause. Journal of Experimental Biology 208, 4467–4477.CrossRefGoogle ScholarPubMed
Bindesbøl, A. M., Holmstrup, M., Damgaard, C., and Bayley, M. (2005). Stress synergy between environmentally realistic levels of copper and frost in the earthworm Dendrobaena octaedra. Environmental Toxicology and Chemistry 24, 1462–1467.CrossRefGoogle ScholarPubMed
Bindesbøl, A. M., Bayley, M., Damgaard, C., Hedlund, K., and Holmstrup, M. (2009). Changes in membrane phospholipids as a mechanistic explanation for decreased freeze tolerance in earthworms exposed to sublethal copper concentrations. Environmental Science and Technology, 43, 5495–5500.CrossRefGoogle Scholar
Block, W. (1996). Cold or drought – the lesser of two evils for terrestrial arthropods. European Journal of Entomology 93, 325–339.Google Scholar
Browne, J., Tunnacliffe, A., and Burnell, A. (2002). Plant desiccation gene found in a nematode. Nature 416, 38.CrossRefGoogle Scholar
Chaisuksant, Y., Yu, Q. M., and Connell, D. W. (1999). The internal critical level concept of nonspecific toxicity. Reviews of Environmental Contamination and Toxicology 162, 1–41.Google ScholarPubMed
Clark, M. S., Thorne, M. A. S., Purac, J., Grubor-Lasjic, G., Kube, M., Reinhardt, R., and Worland, M. R. (2007). Surviving extreme polar winters by desiccation: clues from Arctic springtail (Onychiurus arcticus) EST libraries. BMC Genomics 8, 475.CrossRefGoogle ScholarPubMed
Crowe, J. H. and Crowe, L. M. (1986). Stabilization of membranes in anhydrobiotic organisms. In Membranes, Metabolism and Dry Organisms, ed. Leopold, C. A., London: Comstock Publishing Association, pp. 188–209Google Scholar
Crowe, J. H., Hoekstra, F., and Crowe, L. M. (1992). Anhydrobiosis. Annual Review of Physiology 54, 579–599.CrossRefGoogle ScholarPubMed
Danks, H. V. (1971). Overwintering of some north temperate and Arctic Chironomidae. II. Chironomid biology. Canadian Entomologist 103, 1875–1910.CrossRefGoogle Scholar
Elnitsky, M. A., Hayward, S. A. L., Rinehart, J. P., Denlinger, D. L., and Lee, R. E. (2008a). Cryoprotective dehydration and the resistance to inoculative freezing in the Antarctic midge, Belgica antarctica. Journal of Experimental Biology 211, 524–530.CrossRefGoogle ScholarPubMed
Elnitsky, M. A., Benoit, J. B., Denlinger, D. L., and LeeJr., R. E. Jr., R. E. (2008b) Desiccation tolerance and drought acclimation in the Antarctic collembolan Cryptopygus antarcticus. Journal of Insect Physiology 54, 1432–1439.CrossRefGoogle ScholarPubMed
Gehrken, U. (1989). Supercooling and thermal hysteresis in the adult bark beetle, Ips acuminatus Gyll. Journal of Insect Physiology 35, 347–352.CrossRefGoogle Scholar
Gehrken, U. (1992). Inoculative freezing and thermal hysteresis in the adult beetles Ips acuminatus and Rhagium inquisitor. Journal of Insect Physiology 38, 519–524.CrossRefGoogle Scholar
Goto, S., Yoshida, K., and Kimura, M. (1998). Accumulation of Hsp70 mRNA under environmental stresses in diapausing and nondiapausing adults of Drosophila triauraria. Journal of Insect Physiology 44, 1009–1015.CrossRefGoogle Scholar
Hadley, N. (1994). Water Relations of Terrestrial Arthropods. San Diego, CA: Academic Press.Google Scholar
Hawes, T. C. and Bale, J. S. (2007). Plasticity in arthropod cryotypes. Journal of Experimental Biology 210, 2585–2592.CrossRefGoogle ScholarPubMed
Hayward, S. A. L., Rinehart, J. P., and Denlinger, D. L. (2004). Desiccation and rehydration elicit distinct heat shock protein transcript responses in flesh fly pupae. Journal of Experimental Biology 207, 963–971.CrossRefGoogle ScholarPubMed
Hayward, S. A. L., Rinehart, J. P., Sandro, L. H., Lee, R. E., and Denlinger, D. L. (2007). Slow dehydration promotes desiccation and freeze tolerance in the Antarctic midge Belgica antarctica. Journal of Experimental Biology 210, 836–844.CrossRefGoogle ScholarPubMed
Hazel, J. R. and Williams, E. E. (1990). The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Progress in Lipid Research 29, 167–227.CrossRefGoogle ScholarPubMed
Hetz, S. K. and Bradley, T. J. (2005). Insects breathe discontinuously to avoid oxygen toxicity. Nature 433, 516–519.CrossRefGoogle ScholarPubMed
Hoffmann, A. A. and Parsons, P. A. (1991). Evolutionary Genetics and Environmental Stress. Oxford: Oxford University Press.Google Scholar
Højer, R., Bayley, M., Damgaard, C. F., and Holmstrup, M. (2001). Stress synergy between drought and a common environmental contaminant: studies with the collembolan Folsomia candida. Global Change Biology 7, 485–494.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
Holmstrup, M., Petersen, B. F., and Larsen, M. M. (1998). Combined effects of copper, desiccation, and frost on the viability of earthworm cocoons. Environmental Toxicology and Chemistry 17, 897–901.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., Bayley, M., and Ramløv, 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., Aubail, A., and Damgaard, C. (2008). Mercury reduces cold tolerance in the springtail Folsomia candida. Comparative Biochemistry and Physiology C 148, 172–177.Google ScholarPubMed
Horton, D. R., Lewis, T. M., and Neven, L. G. (1996). Reduced cold-hardiness of pear psylla (Homoptera: Psyllidae) caused by exposure to external water and surfactants. Canadian Entomologist 128, 825–830.CrossRefGoogle Scholar
Ishibashi, K., Sasaki, S., Fushimi, K., Uchida, S., Kuwahara, M., Saito, H., Furukawa, T., Nakajima, K., Yamaguchi, Y., Gojobori, T., and Marumo, F. (1994). Molecular-cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells. Proceedings of the National Academy of Sciences, USA 91, 6269–6273.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
Kanwisher, J. W. (1959). Histology and metabolism of frozen intertidal animals. Biological Bulletin 116, 258–264.CrossRefGoogle Scholar
Kikawada, T., Nakahara, Y., Kanamori, Y., Iwata, K. I., 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
Kosova, K., Vitamvas, P., and Prasil, I. T. (2007). The role of dehydrins in plant response to cold. Biologia Plantarum 51, 601–617.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: Chapman and Hall, pp. 17–46.CrossRefGoogle Scholar
Lighton, J. (1994). Discontinous ventilation in terrestrial insects. Physiological Zoology 67, 142–162.CrossRefGoogle Scholar
Lovelock, J. E. (1953). The mechanism of the cryoprotective effect of glycerol against freezing and thawing. Biochimica et Biophysica Acta 11, 28–36.CrossRefGoogle ScholarPubMed
Lundheim, R. and Zachariassen, K. E. (1993). Water balance of over-wintering beetles in relation to strategies for cold tolerance. Journal of Comparative Physiology B 163, 1–4.CrossRefGoogle Scholar
Mazur, P. (1977). The role of intracellular freezing in the death of cells cooled at supraoptimal rates. Cryobiology 14, 251–272.CrossRefGoogle ScholarPubMed
McLaughlin, S. and Percy, K. (1999). Forest health in North America: Some perspectives on actual and potential roles of climate and air pollution. Water, Air and Soil Pollution 116, 151–197.CrossRefGoogle Scholar
Miller, K. (1982). Cold-hardiness strategies of some adult and immature insects overwintering in interior Alaska. Comparative Biochemistry and Physiology 73A, 595–604.CrossRefGoogle Scholar
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
Pedersen, P. G. and Holmstrup, M. (2003). Freeze or dehydrate: only two options for the survival of subzero temperatures in the arctic enchytraeid Fridericia ratzeli. Journal of Comparative Physiology B 173, 601–609.CrossRefGoogle ScholarPubMed
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
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
Preston, G. M., Carroll, T. P., Guggino, W. B., and Agre, P. (1992). Appearance of water channels in Xenopus oocytes expressing red-cell chip28 protein. Science 256, 385–387.CrossRefGoogle ScholarPubMed
Ring, R. (1982). Freezing-tolerant insects with low supercooling points. Comparative Biochemistry and Physiology 73A, 605–612.CrossRefGoogle Scholar
Ring, R. and Danks, H. (1994). Desiccation and cryoprotection: Overlapping adaptations. Cryo-Letters 15, 181–190.Google Scholar
Ring, R. and Danks, H. (1998). The role of trehalose in cold-hardiness and desiccation. Cryo-Letters 19, 275–282.Google Scholar
Schmidt-Nielsen, K. (1997). Animal Physiology. New York: Cambridge University Press.Google 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 and Comparative Physiology 42, 1–56.CrossRefGoogle ScholarPubMed
Skovlund, G., Damgaard, C., Bayley, M., and Holmstrup, M. (2006). Does lipophilicity of toxic compounds determine effects on drought tolerance of the soil collembolan Folsomia candida? Environmental Pollution 144, 808–815.CrossRefGoogle ScholarPubMed
Sømme, L. and Birkemoe, T. (1997). Cold tolerance and dehydration in Enchytraeidae from Svalbard. Journal of Comparative Physiology B 167, 264–269.Google Scholar
Sømme, L. and Conradi-Larsen, E.-M. (1977). Cold-hardiness of collembolans and oribatid mites from wind-swept mountain ridges. Oikos 29, 118–126.CrossRefGoogle Scholar
Tammariello, S., Rinehart, J., and Denlinger, D. L. (1999). Desiccation elicits heat shock protein transcription in the flesh fly, Sarcophaga crassipalpis, but does not enhance tolerance to high or low temperatures. Journal of Insect Physiology 45, 933–938.CrossRefGoogle ScholarPubMed
Thurberg, F. P., Dawson, M. A., and Collier, R. S. (1973). Effects of copper and cadmium on osmoregulation and oxygen-consumption in two species of estuarine crabs. Marine Biology 23, 171–175.CrossRefGoogle Scholar
Tunnacliffe, A., Lapinski, J., and McGee, B. (2005). A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers. Hydrobiologia 546, 315–321.CrossRefGoogle Scholar
Laak, S. (1982). Physiological adaptations to low temperature in freezing-tolerant Phyllodecta laticollis beetles. Comparative Biochemistry and Physiology 73A, 613–620.CrossRefGoogle Scholar
Gestel, C. A. M. (1997). Scientific basis for extrapolating results from soil ecotoxicity tests to field conditions and the use of bioassays. In Ecological Risk Assessment of Contaminants in Soil, ed. Straalen, N. M. and Løkke, H.. London: Chapman and Hall, pp. 25–50.CrossRefGoogle Scholar
Valko, M., Morris, H., and Cronin, M. T. D. (2005). Metals, toxicity and oxidative stress. Current Medicinal Chemistry 12, 1161–1208.CrossRefGoogle ScholarPubMed
Wang, L. and Duman, J. G. (2005). Antifreeze proteins of the beetle Dendroides canadensis enhance one another's activities. Biochemistry 44, 10305–10312.CrossRefGoogle ScholarPubMed
Weast, R. C. (1989). Handbook of Chemistry and Physics. Cleveland: CRC Press.Google Scholar
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
Worland, M., Grubor-Lajsic, G., and Montiel, P. (1998). Partial desiccation induced by subzero temperatures as a component of the survival strategy of the Arctic collembolan Onychiurus arcticus (Tullberg). Journal of Insect Physiology 44, 211–219.CrossRefGoogle Scholar
Wu, D. W. and Duman, J. G. (1991). Activation of antifreeze proteins from larvae of the beetle Dendroides canadensis. Journal of Comparative Physiology 161B, 279–281.CrossRefGoogle Scholar
Wu, D. W., Duman, J. G., Cheng, C.-H. C., and Castellino, F. J. (1991). Purification and characterization of antifreeze proteins from larvae of the beetle Dendroides canadensis. Journal of Comparative Physiology 161B, 271–278.CrossRefGoogle Scholar
Zachariassen, K. E. (1979). The mechanism of the cryoprotective effect of glycerol in beetles tolerant to freezing. Journal of Insect Physiology 25, 29–32.CrossRefGoogle Scholar
Zachariassen, K. E. (1980). The role of polyols and nucleating agents in cold-hardy beetles. Journal of Comparative Physiology 140, 227–234.CrossRefGoogle Scholar
Zachariassen, K. E. (1985). Physiology of cold tolerance of insects. Physiological Reviews 65, 799–832.CrossRefGoogle ScholarPubMed
Zachariassen, K. E. (1991). The water relations of overwintering insects. In Insects at Low Temperature, ed. Lee, R. E., and Denlinger, D. L.. New York: Chapman and Hall, pp. 47–63.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., Hammel, H. T., and Schmidek, W. (1979). Osmotically inactive water in relation to tolerance to freezing in Eleodes blanchardi beetles. Comparative Biochemistry and Physiology 63A, 203–206.CrossRefGoogle Scholar
Zachariassen, K. E., Andersen, J., Maloiy, G. M. O., and Kamau, J. M. Z. (1987). Transpiratory water loss and metabolism of beetles from arid areas in East Africa. Comparative Biochemistry and Physiology 68A, 403–408.CrossRefGoogle Scholar
Zachariassen, K. E. and Maloiy, G. M. O. (1989). Water balance of beetles as an indicator of environmental humidity. Fauna Norvegica 36B, 27–31.Google Scholar
Zachariassen, K. E. and Einarson, S. (1993). Regulation of body fluid compartments during dehydration of the tenebrionid beetle Rhytinota praelonga. Journal of Experimental Biology 182, 283–289.Google Scholar
Zachariassen, K. E., Kristiansen, E., and Pedersen, S. A. (2004). Inorganic ions in cold-hardiness. Cryobiology 48, 126–133.CrossRefGoogle ScholarPubMed
Zelenina, M., Tritto, S., Bondar, A. A., Zelenin, S., and Aperia, A. (2004). Copper inhibits the water and glycerol permeability of aquaporin-3. Journal of Biological Chemistry 279, 51939–51943.CrossRefGoogle ScholarPubMed

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