Behavioral and Physiological Adaptations to Cold in a Freeze-Tolerant Arctic Insect
Insects inhabiting the polar and temperate zones commonly overwinter in diapause or quiescent states (Tauber et al., 1986). Although diapause has traditionally been implicated with cold hardiness, diapause is probably phylogeneti-cally unrelated to cold hardiness (see Chapter 8). Nevertheless, both diapause and cold hardiness are usually induced by the same environmental cues, such as temperature, photoperiod, thermoperiod, or nutrition (Beck, 1983). Despite the vast differences in environmental constraints between arctic and temperate bi-omes, cold-tolerant insects typical of these regions have adopted similar modes of overwintering: freeze tolerance or freeze avoidance. In response to a different set of environmental stimuli, have the arctic species evolved any mechanisms of overwintering that differ from their temperate relatives? Arctic insects that survive inclement winters and short summer seasons show adaptations to cold that are uncommon or unique to cold tolerant species (Miller, 1982). One such species is Gynaephora groenlandica.
KeywordsNuclear Magnetic Resonance Freeze Tolerance Nuclear Magnetic Resonance Spectroscopy Gypsy Moth Cold Hardiness
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Abraham, R. J., J. Fisher, and T. Loftus. 1988. Introduction to NMR Spectroscopy
. Wiley, New York.Google Scholar
Ayres, M. P. and S. F. MacLean. 1987. Development of birch leaves and the growth energetics of Epirrita autumnata
Baust, J. G. and R. R. Rojas. 1985. Review—insect cold-hardiness: Facts and fancy. J. Insect Physiol
Beck, S. D. 1983. Insect thermoperiodism. Annu. Rev. Entomol.
Bertram, G. C. L. 1935. The low temperature limit of activity of arctic insects. J. Anim. Ecol.
Bliss, L. C., ed. 1977. Truelove Lowland, Devon Island, Canada: A High Arctic Ecosystem
. University of Alberta Press, Edmonton.Google Scholar
Brett, J. R. 1971. Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka
). Am. Zool.
Buchanan, G. W. and K. B. Storey. 1983. In vivo
detection of cryoprotectants and lipids in overwintering larvae using carbon-13 NMR spectroscopy. Can. J. Cell. Biol.
Campbell, R. W. 1981. Population dynamics. In The Gypsy Moth: Research Toward Integrated PestManagement
, eds. C. C. Doane and M. L. McManus, pp. 65–214. US Department of Agriculture, Washington, DC.Google Scholar
Chapin, F. S., J. D. McKendrick, and D. A. Johnson. 1986. Seasonal changes in carbon fractions in Alaskan tundra plants of differing growth form: Implications for herbivory. J. Ecol.
Chen, C. -P., D. L. Denlinger, and R. E. Lee. 1987. Cold-shock injury and rapid cold hardening in the flesh fly Sarcophaga crassipalpis. Physiol. Zool.
Chino, H. 1957a. Carbohydrate metabolism in diapause egg of the silkworm, Bombyx mori
I. Diapause and the change in glycogen content. Embryologia
Chino, H. 1957b. Conversion of glycogen to sorbitol and glycerol in the diapause egg of the Bombyx
Chino, H. 1958. Carbohydrate metabolism in diapause eggs of the silkworm, Bombyx mori
. II. Conversion of glycogen into sorbitol and glycerol during diapause. J. Insect Physiol.
Crowe, J. H. and L. M. Crowe. 1982. Induction of anhydrobiosis: membrane changes during drying. Cryobiol.
Danks, H. V. 1986. Insect plant interactions in arctic regions. Rev. Entomol. Quebec
Danks, H. V. 1981. Arctic Arthropods. A Review of Systematics and Ecology with Particular Reference to the North American Fauna. Entomological Society of Canada
, Ottawa.Google Scholar
Dawson, T. E. 1987. Comparative ecophysiological adaptations in arctic and alpine populations of a dioecious shrub, Salix árctica
Pall. PhD Thesis, University of Washington, Seattle.Google Scholar
Feeny, P. 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology
Ferguson, D. C. 1978. Noctuoidea, Lymantriidae. In The Moths of North America North of Mexico
, ed. R. B. Dominick, pp. 17–21. E. W. Classey and The Wedge Entomological Research Foundation, London.Google Scholar
Gadian, D. G. 1982. Nuclear Magnetic Resonance and its Applications to Living Systems
. Oxford University Press, London.Google Scholar
Hamilton, W. J. 1973. Life’s Color Code
. McGraw-Hill, New York.Google Scholar
Haukioja, E., P. Hiemela, and S. Siren. 1985. Foliage phenols and nitrogen in relation to growth, insect damage, and ability to recover after defoliation in the mountain birch Betula pubescens
spp tortuosa. Oecologia
Hayakawa, Y. and H. Chino. 1982. Phosphofructokinase as a possible key enzyme regulating glycerol and trehalose accumulation in diapausing insects. Insect Biochem
. 12:639–692.CrossRefGoogle Scholar
Hochachka, P. W. and G. N. Somero. 1985. Biochemical Adaptation
. Princeton University Press, Princeton.Google Scholar
Keeley, L. L. 1981. Neuroendocrine regulation of mitochondrial development and function in the insect fat body. In Energy Metabolism in Insects
, ed. R. G. H. Downer, pp. 207–239. Plenum. Press, New York.CrossRefGoogle Scholar
Kevan, P. G., T. J. Jensen, and J. D. Shorthouse. 1982. Body temperatures and behavioral thermoregulation of high arctic wooly-bear caterpillars and pupae (Gynaephora rossii
, Lymantriidae: Lepi-doptera) and the importance of sunshine. Arctic Alpine Res
. 14:125–213.CrossRefGoogle Scholar
Kevan, P. G. 1975. Sun tracking solar furnaces in high arctic flowers: significance for pollination and insects. Science
Kevan, P. G. and J. D. Shorthouse. 1970. Behavioral thermoregulation by high arctic butterflies. Arctic
Knapp, R. and T. M. Casey. 1986. Thermal ecology, behavior, and growth of gypsy moth and eastern tent caterpillars. Ecology
Krog, J. 1955. Notes on temperature measurements indicative of special organization in arctic and subarctic plants for utilization of radiated heat from the sun. Physiol. Plant.
Kukal, O. 1984. Life history and adaptations of a high arctic insect, Gynaephora groenlandica
(Wöcke) (Lepidoptera: Lymantriidae). MS thesis, University of Guelph, Guelph.Google Scholar
Kukal, O. 1988. Behavioral and physiological adaptations to cold in a freeze tolerant high arctic insect, Gynaephora groenlandica
(Wöcke) (Lepidoptera: Lymantriidae). PhD Thesis, University of Notre Dame, Notre Dame.Google Scholar
Kukal, O. and P. G. Kevan. 1987. The influence of parasitism on the life history of a high arctic insect, Gynaephora groenlandica
(Wöcke) (Lepidoptera: Lymantriidae). Can. J. Zool.
Kukal, O., B. Heinrich and J. G. Duman. 1988a. Behavioral thermoregulation in the freeze tolerant arctic caterpillar, Gynaephora groenlandica. J. Exp. Biol.
Kukal, O., A. S. Serianni, and J. G. Duman. 1988b. Glycerol metabolism in a freeze-tolerant arctic insect: An in vivo
13-C NMR study. J. Comp. Physiol.
B 158:175–183.CrossRefGoogle Scholar
Kukal, O., Duman, J. G. and A. S. Serianni. 1989. Cold-induced mitochondrial degradation and cryoprotectant synthesis in freeze-tolerant arctic caterpillars. J. Comp. Physiol. 158:661–671.Google Scholar
Kukal, O. and T. E. Dawson. 1989. Temperature and food quality influences on feeding behavior, assimilation efficiency and growth rate of arctic woolly-bear caterpillars. Oecologia
Lee, R. E., C. -P. Chen, M. H. Meacham, and D. L. Denlinger. 1987. Ontogenetic patterns of cold-hardiness and glycerol production in Sarcophaga crassipalpis. J. Insect Physiol.
MacLean, S. F. and T. S. Jensen. 1986. Food plant selection by insect herbivores in Alaskan arctic tundra: the role of plant life form. Oikos
May, L. M. 1979. Insect thermoregulation. Annu. Rev. Entomol.
McEvoy, P. B. 1984. Increase in respiratory rate during feeding in larvae of the cinnabar moth Tyria jacobaese. Physiol. Entomol.
Meyer, S. G. E. 1980. Studies on anaerobic glucose and glutamate metabolism in larvae of Callitroga macellaria. Insect Biochem.
Meyer, S. G. E. 1978. Effects of heat, cold, anaerobiosis and inhibitors on metabolite concentrations in larvae of Callitroga macellaria. Insect Biochem.
Miller, L. K. 1982. Cold-hardiness strategies of some adult and immature insects overwintering in interior Alaska. Comp. Biochem. Physiol.
Montgomery, M.E. 1982. Life-cycle nitrogen budget for the gypsy moth, Lymantria dispar
, reared on artificial diet. J. Insect Physiol.
Price, P. W., C. E. Bouton, P. Gross, B. A. McPherson, J. N. Thompson, and A. E. Weiss. 1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst.
Price, P. W., H. Roininen, and J. Tahvanainen. 1987a. Plant age and attack by the bud galler, Euura mucronata. Oecologia
Price, P. W., H. Roininen, and J. Tahvanainen. 1987b. Why does the budgalling sawfly, Euura mucronata
attack long shoots? Oecologia
Regal, P. J. 1967. Voluntary hypothermia in reptiles. Science
Rosenthal, G. A. and D. H. Janzen. 1979. Herbivores: Their Interaction with Secondary Plant Metabolites
. Academic Press, New York.Google Scholar
Schaefer, J., K. J. Dramer, J. R. Garbow, G. S. Jacob, E. O. Stejskal, T. L. Hopkins, and R. D. Speirs. 1987. Aromatic cross-links in insect cuticle: detection by solid-state 13-C and 15-N NMR. Science
Scholander, P. F., W. Flagg, R. J. Hoch, and L. Irving. 1953. Climatic adaptation in arctic and tropical poikilotherms. Physiol. Zool.
Scholander, P. F., W. Flagg, R. J. Hoch, and L. Irving. 1954. Studies on the physiology of frozen plants and animals in the arctic. J. Cell. Comp. Physiol.
Scriber, J. M. and F. Slansky, Jr. 1981. The nutritional ecology of immature insects. Annu. Rev. Entomol.
Slansky, F. Jr. and J. M. Scriber. 1985. Food consumption and utilization. In Comprehensive Insect Physiology
, Vol. 4, eds. G. A. Kerkut and L. I. Gilbert, pp. 87–163. Pergamon Press, Oxford.Google Scholar
Sømme, L. 1974. Anaerobiosis in some alpine Coleóptera. Norsk. Entomol. Tidsskr.
Sømme, L. 1964. Effects of glycerol on cold-hardiness in insects. Can. J. Zool.
Storey, K. B. 1983. Metabolism and bound water in overwintering insects. Cryobiol.
Storey, K. B. and J. M. Storey. 1988. Freeze tolerance in animals. Physiol. Rev.
Storey, K. B., M. Micelli, K. W. Butler, I. C. P. Smith, and R. Deslauriers. 1984. 31-P NMR studies of the freezing tolerant larvae of the gall fly, Eurosta solidaginis. Eur. J. Biochem.
Svoboda, J. and B. Freedman, eds. 1989. Ecology of a High Arctic Lowland Oasis, Alexandria Fiord
), Ellesmere Island, N.W.T., Canada.
University of Toronto Press, Toronto.Google Scholar
Tauber, M. J., C. A. Tauber, and S. Masaki. 1986. Seasonal Adaptations of Insects
. Oxford University Press, New York.Google Scholar
Tsumuki, H. and K. Kanehisa. 1981. The fate of 14-C glycerol in the rice stem borer, Chilo suppressalis
Walker (Lepidoptera: Pyralidae). Appl. Entomol. Zool.
Wyatt, G. R. and G. F. Kalf. 1958. Organic components of insect hemolymph. Proceedings of the 10th International Congress on Entomology
, Vol. 2, p. 33.Google Scholar
Wyatt, G. R. and W. L. Meyer. 1959. The chemistry of insect hemolymph III. Glycerol. J. Gen. Physiol.
Yancey, P. H., M. E. Clark, S. C. Hank, R. D. Bowlus, and G. N. Somero. 1982. Living with water Stress: evolution of osmolyte systems. Science
Yi, S., C. Yin, and J. H. Nordin. 1987. The chilling induced biosynthesis and secretion of glycerol by Ostrinia nubilalis
larval fat bodies in vitro. J. Insect Physiol.
Zachariassen, K. E. 1985. Physiology of cold tolerance in insects. Phys. Rev.
Zachariassen, K. E., ed. 1982. Special section: Cold-hardiness in Poikilothermic animals. Comp. Biochem. Physiol.
Zachariassen, K. E. 1979. The mechanism of the cryoprotective effect of gylcerol in beetles tolerant to freezing. J. Insect Physiol.
Ziegler, R. and K. Roth. 1985. 13-C NMR spectroscopy of larvae of Manduca sexta in vivo. Nature