Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-15T10:52:48.888Z Has data issue: false hasContentIssue false
  • English
  • Français

Insect adaptations to cold and changing environments1

Published online by Cambridge University Press:  02 April 2012

H.V. Danks
H.V. Danks
Affiliation:
Biological Survey of Canada (Terrestrial Arthropods), Canadian Museum of Nature, P.O. Box 3443, Station D, Ottawa, Ontario, Canada K1P 6P4 (e-mail: hdanks@mus-nature.ca)
Get access Rights & Permissions [Opens in a new window]

Abstract

A review of insect adaptations for resistance to cold and for life-cycle timing reveals the complexity of the adaptations and their relationships to features of the environment. Cold hardiness is a complex and dynamic state that differs widely among species. Surviving cold depends on habitat choice, relationships with ice and water, and synthesis of a variety of cryoprotectant molecules. Many aspects are time-dependent and are integrated with other factors such as taxonomic affinity, resource availability, natural enemies, and diapause. Timing adaptations reflect the fact that all environments change over many different time frames, from days to thousands of years. Environments differ in severity and in the extent, nature, variability, and predictability of change, as well as in how reliably cues indicate probable conditions in the future. These differences are reflected by a wide range of insect life-cycle systems, life-cycle delays, levels of responsiveness to various environmental signals, genetic systems, and circadian responses. In particular, the degree of environmental change, its predictability on different time frames, and whether it can be monitored effectively dictate the balance between fixed and flexible timing responses. These same environmental features have to be characterized to understand cold hardiness, but this has not yet been done. Therefore, the following key questions must be answered in order to put cold hardiness into the necessary ecological context: How much do conditions change? How consistent is the change? How reliable are environmental signals?

Résumé

La présente rétrospective des adaptations pour la résistance au froid et l'ajustement temporel des cycles biologiques illustre la complexité des adaptations et leurs relations aux caractéristiques du milieu. La résistance au froid est un état dynamique et complexe qui varie considérablement d'une espèce à l'autre. La survie au froid dépend du choix de l'habitat, des relations avec la glace et l'eau et de la synthèse d'une gamme de molécules cryoprotectrices. Plusieurs des aspects sont reliés au temps et sont aussi intégrés à d'autres facteurs, tels que l'affinité taxonomique, la disponibilité des ressources, les ennemis naturels et la diapause. Les adaptations d'ajustement temporel sont reliées au fait que tous les milieux changent à des échelles temporelles multiples, allant de jours à plusieurs millénaires. Les milieux différent entre eux quant à la rigueur et à l'étendue, la nature, la variabilité et la prévisibilité du changement; de plus, les indices des conditions futures probables y sont plus ou moins fiables. Ces différences se reflètent dans les systèmes de cycles biologiques des insectes, les délais dans les cycles biologiques, les degrés de réaction aux divers signaux environnementaux, les systèmes génétiques et les réponses circadiennes. En particulier, le degré de changement environnemental, sa prévisibilité aux différentes échelles temporelles et la possibilité d'en faire un suivi efficace déterminent l'équilibre entre un ajustement temporel fixe et un flexible. Ces mêmes caractéristiques de l'environnement doivent être définies de manière à pouvoir comprendre la résistance au froid, mais ce n'est pas encore fait. Pour replacer la résistance au froid dans son contexte écologique obligé, les questions essentielles à poser sont donc: quelle est l'importance du changement de conditions? ce changement est-il uniforme? les signaux de l'environnement sont-ils fiables?

[Traduit par la Rédaction]

Type
Articles
Information
The Canadian Entomologist , Volume 138 , Issue 1: Adaptations and Constraints: a Symposium in Honour of Richard Ring / Adaptations et contraintes : un symposium en l'honneur de Richard Ring , February 2006 , pp. 1 - 23
Copyright
Copyright © Entomological Society of Canada 2006

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.)

References

Aitchison, C.W. 1979. Winter-active subnivean invertebrates in Southern Canada. I. Collembola; II. Coleoptera; III. Acari; IV. Diptera and Hymenoptera. Pedobiologia, 19: 113–120; 121–128; 153–160; 176–182.CrossRefGoogle Scholar
Aitchison, C.W. 1989. The ecology of winter-active collembolans and spiders. Aquilo Ser Zoologica, 24: 83–89.Google Scholar
Aoki, T. 1999. Larval development, emergence and seasonal regulation in Asiagomphus pryeri (Selys) (Odonata: Gomphidae). Hydrobiologia, 394: 179–192.Google Scholar
Bale, J.S. 1987. Insect cold hardiness: freezing and supercooling — an ecophysiological perspective. Journal of Insect Physiology, 33: 899–908.CrossRefGoogle Scholar
Bale, J.S. 1993. Classes of insect cold hardiness. Functional Ecology, 7: 751–753.Google Scholar
Bale, J.S. 1996. Insect cold hardiness: a matter of life and death. European Journal of Entomology, 93: 369–382.Google Scholar
Bale, J.S. 2002. Insects and low t emperatures: from molecular biology to distributions and abundance. Philosophical Transactions of the Royal Society of London, B: Biological Sciences, 357: 849–862.CrossRefGoogle Scholar
Bale, J.S., Hansen, T.N., and Baust, J.G. 1989. Effect of cooling rate on the survival of larvae, pupariation, and adult emergence of the gall fly Eurosta solidaginis. Cryobiology, 26: 285–289.CrossRefGoogle Scholar
Bale, J.S., Block, W., and Worland, M.R. 2000. Thermal tolerance and acclimation response of the sub-Antarctic beetle Hydromedion sparsutum. Polar Biology, 23: 77–84.Google Scholar
Bale, J.S., Worland, M.R., and Block, W. 2001. Effects of summer frost exposures on the cold tolerance strategy of a sub-Antarctic beetle. Journal of Insect Physiology, 47: 1161–1167.CrossRefGoogle ScholarPubMed
Barrett, J. 1991. Anhydrobiotic nematodes. Agricultural Zoology Reviews, 4: 161–176.Google Scholar
Baust, J.G. 1982. Environmental triggers to cold hardening. Comparative Biochemistry and Physiology A, 73: 563–570.Google Scholar
Baust, J.G., and Lee, R.E. Jr., 1982. Environmental triggers to cryoprotectant modulation in separate populations of the gall fly Eurosta solidaginis (Fitch). Journal of Insect Physiology, 28: 431–436.Google Scholar
Baust, J.G., and Nishino, M. 1991. Freezing tolerance in the goldenrod gall fly (Eurosta solidaginis). In Insects at low temperature. Edited by Lee, R.E. Jr., and Denlinger, D.L.. Chapman and Hall, New York. pp. 260–275.CrossRefGoogle Scholar
Biron, D.-G., Brunel, E., Nenon, J.-P., Coderre, D., and Boivin, G. 1999. Etude préliminaire du déterminisme génétique contrôlant l'expression de l'émergence bimodale de Delia radicum (Diptera: Anthomyiidae). Annales de la Société Entomologique de France, 35 (Suppl.): 104–108.Google Scholar
Block, W. 1996. Cold or drought — the lesser of two evils for terrestrial arthropods? European Journal of Entomology, 93: 325–339.Google Scholar
Block, W. 2002. Interactions of water, ice nucleators and desiccation in invertebrate cold survival. European Journal of Entomology, 99: 259–266.Google Scholar
Block, W. 2003. Water or ice? The challenge for invertebrate cold survival. Science Progress, 86: 77–101.CrossRefGoogle ScholarPubMed
Brown, C.L., Bale, J.S., and Walters, K.F.A. 2004. Freezing induces a loss of freeze tolerance in an overwintering insect. Proceedings of the Royal Society Biological Sciences Series B, 271: 1507–1511.CrossRefGoogle Scholar
Brundin, L. 1966. Transantarctic relationships and their significance, as evidenced by chironomid midges, with a monograph of the subfamilies Podonominae and Aphroteniinae and the Austral Heptagyiae. Kungliga Svenska Vetenskapsakademiens Handlingar, 11: 7–472.Google Scholar
Campbell, A., and Mackauer, M. 1975. Thermal constants for development of the pea aphid (Homoptera: Aphididae) and some of its parasites. The Canadian Entomologist, 107: 419–423.Google Scholar
Campbell, I.C. 1986. Life histories of some Australian siphlonurid and oligoneuriid mayflies (Insecta: Ephemeroptera). Australian Journal of Marine and Freshwater Research, 37: 261–288.Google Scholar
Canard, M., and Grimal, A. 1993. Multiple action of photoperiod on diapause in the green lacewing Mallada picteti (McLachlan) (Neuroptera Chrysopidae). Bollettino dell'Istituto di Entomologia “Guido Grandi” della Universita degli Studi di Bologna, 47: 233–245.Google Scholar
Cannon, R.J.C., and Block, W. 1988. Cold tolerance of microarthropods. Biological Reviews of the Cambridge Philosophical Society, 63: 23–77.Google Scholar
Conradi-Larsen, E.-M., and Sømme, L. 1973 a. Anaerobiosis in the overwintering beetle, Pelophila borealis. Nature (London), 245: 388–390.CrossRefGoogle Scholar
Conradi-Larsen, E.-M., and Sømme, L. 1973 b. The overwintering of Pelophila borealis Payk. II. Aerobic and anaerobic metabolism. Norsk Entomologisk Tidsskrift, 20: 325–332.Google Scholar
Courtney, G.W. 1991. Life history patterns of Nearctic mountain midges (Diptera: Deuterophlebiidae). Journal of the North American Benthological Society, 10: 177–197.Google Scholar
Daley, M.E., Spyracopoulos, L., Jia, Z., Davies, P. L., and Sykes, B.D. 2002. Structure and dynamics of a ß-helical antifreeze protein. Biochemistry, 41: 5515–5525.CrossRefGoogle Scholar
Danks, H.V. 1971. Overwintering of some north temperate and arctic Chironomidae. II. Chironomid biology. The Canadian Entomologist, 103: 1875–1910.Google Scholar
Danks, H.V. 1978. Modes of seasonal adaptation in the insects. I. Winter survival. The Canadian Entomologist, 110: 1167–1205.Google Scholar
Danks, H.V. 1981. Arctic arthropods. A review of systematics and ecology with particular reference to North A merican fauna. Entomological Society of Canada, Ottawa, Ontario.Google Scholar
Danks, H.V. 1983. Extreme individuals in natural populations. Bulletin of the Entomological Society of America, 29: 41–46.Google Scholar
Danks, H.V. 1987. Insect dormancy: an ecological perspective. Biological Survey of Canada (Terrestrial Arthropods), Ottawa, Ontario.Google Scholar
Danks, H.V. 1991 a. Winter habitats and ecological adaptations for winter survival. In Insects at low temperature. Edited by Lee, R.E. Jr., and Denlinger, D.L.. Chapman and Hall, New York. pp. 231–259.Google Scholar
Danks, H.V. 1991 b. Life-cycle pathways and theanalysis of complex life cycles in insects. The Canadian Entomologist, 123: 23–40.Google Scholar
Danks, H.V. 1992 a. Long life cycles in insects. The Canadian Entomologist, 124: 167–187.Google Scholar
Danks, H.V. 1992 b. Arctic insects as indicators of environmental change. Arctic, 45: 159–166.Google Scholar
Danks, H.V. 1993. Patterns of diversity in the Canadian insect fauna. In Systematics and entomology: diversity, distribution, adaptation and application. Edited by Ball, G.E. and Danks, H.V.. Memoirs of the Entomological Society of Canada, 165: 51–74.Google Scholar
Danks, H.V. 1994. Diversity and integration of lifecycle controls in insects. In Insect life-cycle polymorphism: theory, evolution and ecological consequences for seasonality and diapause control. Edited by Danks, H.V.. Series Entomologica 52. Kluwer Academic Publishers, Dordrecht. pp. 5–40.Google Scholar
Danks, H.V. 1996. The wider integration of studies on insect cold-hardiness. European Journal of Entomology, 93: 383–403.Google Scholar
Danks, H.V. 1999. Life cycles in polar arthropods—flexible or programmed? European Journal of Entomology, 96: 83–102.Google Scholar
Danks, H.V. 2000 a. Dehydration in dormant insects. Journal of Insect Physiology, 46: 837–852.CrossRefGoogle ScholarPubMed
Danks, H.V. 2000 b. Insect cold hardiness: a Canadian perspective. CryoLetters, 21: 297–308.Google ScholarPubMed
Danks, H.V. 2001. The nature of dormancy responses in insects. Acta Societatis Zoologicae Bohemicae, 65: 169–179.Google Scholar
Danks, H.V. 2002 a. The range of insect dormancy responses. European Journal of Entomology, 99: 127–142.Google Scholar
Danks, H.V. 2002 b. Modification of adverse conditions by insects. Oikos, 99: 10–24.Google Scholar
Danks, H.V. 2003. Studying insect photoperiodism and rhythmicity: components, approaches and lessons. European Journal of Entomology, 100: 209–221.Google Scholar
Danks, H.V. 2004 a. Seasonal adaptations in arctic insects. Integrative and Comparative Biology, 44: 85–94.CrossRefGoogle ScholarPubMed
Danks, H.V. 2004 b. The roles of insect cocoons in cold conditions. European Journal of Entomology, 101: 433–437.Google Scholar
Danks, H.V. 2005 a. Key themes in the study of seasonal adaptations in insects. I. Patterns of cold hardiness. Applied Entomology and Zoology, 40: 199–211.CrossRefGoogle Scholar
Danks, H.V. 2005 b. How similar are daily and seasonal biological clocks. Journal of Insect Physiology, 51: 609–619.Google Scholar
Danks, H.V., and Foottit, R.G. 1989. Insects of the boreal zone of Canada. The Canadian Entomologist, 121: 626–677.Google Scholar
Danks, H.V., and Oliver, D.R. 1972. Diel periodicities of emergence of some high arctic Chironomidae (Diptera). The Canadian Entomologist, 104: 903–916.CrossRefGoogle Scholar
Denlinger, D.L. 1991. Relationship between cold hardiness and diapause. In Insects at low temperature. Edited by Lee, R.E. Jr., and Denlinger, D.L.. Chapman and Hall, New York. pp. 174–198.CrossRefGoogle Scholar
Denlinger, D.L., Rinehart, J.P., and Yocum, G.D. 2001. Stress proteins: a role in insect diapause? In Insect timing: circadian rhythmicity to seasonality. Edited by Denlinger, D.L., Giebultowicz, J.M., and Saunders, D.S.. Elsevier, Amsterdam. pp. 155–171.Google Scholar
Downes, J.A. 1965. Adaptations of insects in the arctic. Annual Review of Entomology, 10: 257–274.Google Scholar
Duman, J.G. 2001. Antifreeze and ice nucleator proteins in terrestrial arthropods. Annual Review of Physiology, 63: 327–357.CrossRefGoogle ScholarPubMed
Duman, J.G. 2002. The inhibition of ice nucleators by insect antifreeze proteins is enhanced by glycerol and citrate. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 172: 163–168.Google Scholar
Duman, J.G., and Serianni, A.S. 2002. The role of endogenous antifreeze protein enhancers in the hemolymph thermal hysteresis activity of t he beetle Dendroides canadensis. Journal of Insect Physiology, 48: 103–111.CrossRefGoogle Scholar
Duman, J.G., Wu, D. W., Xu, L., Tursman, D., and Olsen, T.M. 1991. Adaptations of insects to subzero temperatures. Quarterly Review of Biology, 66: 387–410.Google Scholar
Fields, P.G., and McNeil, J.N. 1986. Possible dual cold-hardiness strategies in Cisseps fulvicollis (Lepidoptera: Arctiidae). The Canadian Entomologist, 118: 1309–1311.Google Scholar
Fletcher, G.L., Hew, C.Y., and Davies, P.L. 2001. Antifreeze proteins of teleost fishes. Annual Review of Physiology, 63: 359–390.Google Scholar
Frank, S.A., and Slatkin, M. 1990. Evolution in a variable environment. American Naturalist, 136: 244–260.Google Scholar
Glitho, I.A., Lenga, A., Pierre, D., and Huignard, J. 1996. Changes in the responsiveness during two phases of diapause termination in Bruchidius atrolineatus Pic (Coleoptera: Bruchidae). Journal of Insect Physiology, 42: 953–960.Google Scholar
Goehring, L., and Oberhauser, K. S. 2002. Effects of photoperiod, temperature, and host plant age on induction of reproductive diapause and development time in Danaus plexippus. Ecological Entomology, 27: 674–685.Google Scholar
Goto, S.G., and Kimura, M.T. 1998. Heat- and cold- shock responses and temperature adaptations in subtropical and temperate species of Drosophila. Journal of Insect Physiology, 44: 1233–1239.CrossRefGoogle ScholarPubMed
Greenslade, P. 1981. Survival of Collembola in arid environments: observations in south Australia and the Sudan. Journal of Arid Environments, 4: 219–228.CrossRefGoogle Scholar
Grodhaus, G. 1971. Sporadic parthogenesis in three species of Chironomus (Diptera). The Canadian Entomologist, 103: 338–340.Google Scholar
Hadley, N.F. 1994. Water relations of terrestrial arthropods. Academic Press, New York.Google Scholar
Hairston, N.G. Jr., and De Stasio, B.T. Jr., 1988. Rate of evolution slow ed by a dormant propagule pool. Nature (London), 336: 239–242.Google Scholar
Hanski, I. 1988. Four kinds of extra long diapause in insects: a review of theory and observations. Annales Zoologici Fennici, 25: 37–53.Google Scholar
Hinton, H.E. 1960. A fly larva that tolerates dehydration and temperatures from –270 °C to +102 °C. Nature (London), 188: 336–337.Google Scholar
Hodek, I. 1981. Le rôle des signaux de l'environnement et des processus endogènes dans la régulation de la reproduction par la diapause imaginale. Bulletin de la Société Zoologique de France, 106: 317–325.Google Scholar
Hodek, I. 1983. Role of environmental factors and endogenous mechanisms in the seasonality of re-production in insects diapausing as adults. In Diapause and life cycle strategies in insects. Edited by Brown, V.K. and Hodek, I.. Series Entomologica. Vol. 23. Dr. W. Junk, The Hague. pp. 9–33.Google Scholar
Hodek, I., and Hodková, M. 1992. Regulation of postdiapause reproduction by recurrent photoperiodic response. In Advances in regulation of insect reproduction. Edited by Bennettová, B., Gelbč, I., and Soldán, T.. Institute of Entomology, Czech Academy of Sciences, Ceske Budejovice. pp. 119–124.Google Scholar
Hodkinson, I.D., Webb, H.R., Bale, J.S., Block, W., Coulson, S.J., and Strathdee, A.T. 1998. Global change and arctic ecosystems: conclusions and predictions from experiments w ith t errestrial invertebrates on Spitsbergen. Arctic and Alpine Research, 30: 306–313.Google Scholar
Hodková, M., and Hodek, I. 1994. Control of diapause and supercooling by the retrocerebral complex in Pyrrhocoris apterus. Entomologia Experimentalis et Applicata, 70: 237–245.Google Scholar
Hodková, M., and Hodek, I. 2004. Photoperiod, diapause and cold-hardiness. European Journal of Entomology, 101: 445–458.Google Scholar
Holmstrup, M. 1992. Cold hardiness strategy in co-coons of the lumbricid earthworm Dendrobaena octaedra (Savigny). Comparative Biochemistry and Physiology A, 102: 49–54.Google Scholar
Holmstrup, M., and Sømme, L. 1998. Dehydration and cold hardiness in the Arctic collembolan Onychiurus arcticus Tullberg 1876. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 168: 197–203.Google Scholar
Holmstrup, M., and Zachariassen, K.E. 1996. Physiology of cold hardiness in earthworms. Comparative Biochemistry and Physiology A, 115: 91–101.Google 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 of the United States of America, 99: 5716–5720.Google Scholar
Horwath, K.L., and Duman, J.G. 1984. Yearly variations in the overwintering mechanisms of the cold-hardy beetle Dendroides canadensis. Physiological Zoology, 57: 40–45.Google Scholar
Hynes, H.B.N., and Hynes, M.E. 1975. The life history of many of the stoneflies (Plecoptera) of southeastern mainland Australia. Australian Journal of Marine and Freshwater Research, 26: 113–153.Google Scholar
Ingrisch, S. 1986. The plurennial life cycles of the European Tettigoniidae (Insecta: Orthoptera). I. The effect of temperature on embryonic development and hatching. Oecologia (Berlin), 70: 606–616.CrossRefGoogle Scholar
Iriarte, P. F., and Hasson, E.A. 2000. The role of the use of different host plants in the maintenance of the inversion polymorphism in the cactophilic Drosophila buzzatii. Evolution, 54: 1295–1302.Google Scholar
Irwin, J.T., and Lee, R.E. Jr., 2000. Mild winter temperatures reduce survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae). Journal of Insect Physiology, 46: 655–661.Google Scholar
Irwin, J.T., and Lee, R.E. Jr., 2003. Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos, 100: 71–78.Google Scholar
Itô, Y. 1998. Role of escape from predators in periodical cicada (Homoptera: Cicadidae) cycles. Annals of t he Entomological Society of America, 91: 493–496.Google Scholar
Jia, F.-Y., Greenfield, M.D., and Collins, R.D. 2000. Genetic variance of sexually selected traits in waxmoths: maintenance by genotype × environment interaction. Evolution, 54: 953–967.Google Scholar
Joanisse, D.R., and Storey, K.B. 1996. Oxidative stress and antioxidants in overwintering larvae of cold-hardy goldenrod gall insects. Journal of Experimental Biology, 199: 1483–1491.Google Scholar
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
Kalushkov, P., Hodková, M., Nedvěd, O., and Hodek, I. 2001. Effect of thermoperiod on diapause intensity in Pyrrhocoris apterus (Heteroptera Pyrrhocoridae). Journal of Insect Physiology, 47: 55–61.Google Scholar
Kelty, J.D., and Lee, R.E. Jr., 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.Google Scholar
Kemp, D. J. 2000. The basis of life-history plasticity in the tropical butterfly Hypolimnas bolina (L.) (Lepidoptera: Nymphalidae). Australian Journal of Zoology, 48: 67–78.Google Scholar
Khaldey, Ye. L. 1977. The biology, phenology and photoperiodic reaction of Forficula tomis (Dermaptera, Forficulidae.) Entomological Review, 56 (4): 6–12. Translation of Entomologicheskoye Obozreniye, 56: 721–730.Google Scholar
Kimura, M.T. 1990. Quantitative response to photoperiod during reproductive diapause in the Drosophila auraria species-complex. Journal of Insect Physiology, 36: 147–152.Google Scholar
Knight, J.D., Bale, J.S., Franks, F., Mathias, S.F., and Baust, J.G. 1986. Insect cold hardiness: supercooling points and pre-freeze mortality. CryoLetters, 7: 194–203.Google Scholar
Knülle, W. 1987. Genetic variability and ecological adaptability of hypopus formation in a stored product mite. Experimental and Applied A carology, 3: 21–32.Google Scholar
Knülle, W. 1991. Genetic and environmental determinants of hypopus duration in the stored-product mite Lepidoglyphus destructor. Experimental and Applied Acarology, 10: 231–258.Google Scholar
Košt'ál, V., and Hodek, I. 1997. Photoperiodism and control of summer diapause in the Mediterranean tiger moth Cymbalophora pudica. Journal of Insect Physiology, 43: 767–777.Google Scholar
Košt'ál, V., Shimada, K., and Hayakawa, Y. 2000. Induction and development of winter larval diapause in a drosophilid fly, Chymomyza costata. Journal of Insect Physiology, 46: 417–428.Google Scholar
Košt'ál, V., Berková, P., and Simek, P. 2003. Remodelling of membrane phospholipids during transition to diapause and cold-acclimation in the larvae of Chymomyza costata (Drosophilidae). Comparative Biochemistry and Physiology B, 135: 407–419.Google Scholar
Kukal, O., Serianni, A.S., and Duman, J.G. 1988. Glycerol metabolism in a freeze-tolerant arctic insect: an in vivo 13C NMR study. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 158: 175–183.Google Scholar
Kukal, O., Duman, J.G., and Serianni, A. S. 1989. Cold-induced mitochondrial degradation and cryoprotectant synthesis in freeze-tolerant arctic caterpillars. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 158: 661–671.Google Scholar
Lafontaine, J.D., and Wood, D.M. 1997. Butterflies and moths (Lepidoptera) of the Yukon. In Insects of the Yukon. Edited by Danks, H.V. and Downes, J.A.. Biological Survey of Canada (Terrestrial Arthropods), Ottawa, Ontario. pp. 723–785.Google Scholar
Lankinen, P., and Riihimaa, A. 1997. Effects of temperature on weak circadian eclosion rhythmicity in Chymomyza costata (Diptera: Drosophilidae). Journal of Insect Physiology, 43: 251–260.Google Scholar
Lavenseau, L., and Hilal, A. 1990. Regulation des cycles saisonniers chez la sesamie (lepidoptère, Noctuidae). In Régulation des cycles s aisonniers chez les invertébrés. Edited by Ferron, P., Missonnier, J., and Mauchamp, B.. Institut National de la Recherche Agronomique, Paris. pp. 243–246.Google Scholar
Layne, J.R. Jr., and Kuharsky, D.K. 2000. Triggering of cryoprotectant synthesis in the woolly bear caterpillar (Pyrrharctia isabella Lepidoptera: Arctiidae). Journal of Experimental Zoology, 286: 367–371.Google Scholar
Lee, R.E. Jr., 1991. Principles of insect low temperature tolerance. In Insects at low temperature. Edited by Lee, R.E. Jr., and Denlinger, D.L.. Chapman and Hall, New York. pp. 17–46.Google Scholar
Lee, R.E. Jr., and Costanzo, J.P. 1998. Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Annual Review of Physiology, 60: 55–72.Google Scholar
Lee, R.E. Jr., and Denlinger, D. L. (Editors). 1991. Insects at low temperature. Chapman and Hall, New York.Google Scholar
Lee, R.E. Jr., Warren, G.J., and Gusta, L.V. (Editors). 1995. Biological ice nucleation and its applications. American Phytopathological Society, St. Paul, Minnesota.Google 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.Google Scholar
Li, N., Andorfer, C.A., and Duman, J.G. 1998. Enhancement of insect antifreeze protein activity by solutes of low molecular mass. Journal of Experimental Biology, 201: 2243–2251.CrossRefGoogle ScholarPubMed
Lloyd, M., and Dybas, H.S. 1966. The periodical cicada problem. I. Population ecology; II. Evolution. Evolution, 20: 133–139; 466–505.Google Scholar
Luker, L.A., Hatle, J.D., and Juliano, S.A. 2002. Reproductive responses to photoperiod by a south Florida population of t he grasshopper Romalea microptera (Orthoptera: Romaleidae). Environmental Entomology, 31: 702–707.Google Scholar
Madura, J.D., Baran, K., and Wierzbicki, A. 2000. Molecular recognition and binding of thermal hysteresis proteins to ice. Journal of Molecular Recognition, 13: 101–113.Google Scholar
Masaki, S. 2002. Ecophysiological consequences of variability in diapause intensity. European Journal of Entomology, 99: 143–154.Google Scholar
Matsumoto, M., Saito, S., and Ohmine, I. 2002. Molecular dynamics simulation of the ice nucleation and growth process leading to water freezing. Nature (London), 416: 409–413.Google Scholar
Meidell, E.-M. 1983. Diapause, aerobic and anaerobic metabolism in alpine, adult Melasoma collaris (Coleoptera). Oikos, 41: 239–244.Google Scholar
Meier, P., and Zettel, J. 1997. Cold hardiness in Entomobrya nivalis (Collembola, Entomobryidae): annual cycle of polyols and antifreeze proteins, and antifreeze triggering by temperature and photoperiod. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 167: 297–304.Google Scholar
Miller, K. 1982. Cold-hardiness strategies of some adult and immature insects overwintering in interior Alaska. Comparative Biochemistry and Physiology A, 73: 595–604.Google Scholar
Miller, L.K. 1978. Physiological studies of arctic animals. Comparative Biochemistry and Physiology A, 59: 327–334.Google Scholar
Miller, L.K., and Smith, J.S. 1975. Production of threitol and sorbitol by an adult insect: association with freezing tolerance. Nature (London), 258: 519–520.Google Scholar
Miller, L.K., and Werner, R. 1987. Extreme super- cooling as an overwintering strategy in three species of willow gall insects from interior Alaska. Oikos, 49: 253–260.CrossRefGoogle Scholar
Moreira, G.R.P., and Peckarsky, B.L. 1994. Multiple developmental pathways of Agnetina capitata (Plecoptera: Perlidae) in a t emperate forest stream. Journal of the North American Benthological Society, 13: 19–29.Google Scholar
Morimoto, R.I., Tissieres, A., and Georgopoulos, C. (Editors). 1994. Biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.Google Scholar
Morissey, R.E., and Baust, J.G. 1976. The ontogeny of cold t olerance in the gall fly Eurosta solidaginis. Journal of Insect Physiology, 22: 431–437.CrossRefGoogle Scholar
Mousseau, T. A., and Dingle, H. 1991. Maternal effects in insect life histories. Annual Review of Entomology, 36: 511–534.Google Scholar
Nakamura, K., and Numata, H. 2000. Photoperiodic control of the intensity of diapause and diapause development in the bean bug, Riptortus clavatus (Heteroptera: Alydidae). European Journal of Entomology, 97: 19–23.Google Scholar
Neal, J.W. Jr., Chittams, J.L., and Bentz, J.-A. 1997. Spring emergence by larvae of the eastern tent caterpillar (Lepidoptera: Lasiocampidae): a hedge against high-risk conditions. Annals of the Entomological Society of America, 90: 596–603.Google Scholar
Nedvěd, O. 2000. Snow white and the seven dwarfs: a multivariate approach to classification of cold tolerance. CryoLetters, 21: 339–348.Google Scholar
Nelson, D.E., and Lee, R.E. Jr., 2004. Cuticular lipids and desiccation resistance in overwintering larvae of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae). Comparative Biochemistry and Physiology B, 138: 313–320.CrossRefGoogle Scholar
Nishizuka, M., Azuma, A., and Masaki, S. 1998. Diapause response to photoperiod and temperature in Lepisma saccharina Linnaeus (Thysanura: Lepismatidae). Entomological Science, 1: 7–14.Google Scholar
Niva, C.C., and Becker, M. 1998. Embryonic external morphogenesis of Rhammatocerus conspersus (Bruner) (Orthoptera: Acrididae: Gomphocerinae) and determination of the diapausing embryonic stage. Anais da Sociedade Entomologica do Brasil, 27: 577–583.Google Scholar
Norling, U. 1976. Seasonal regulation in Leucorrhinia dubia (van der Linden) (Anisoptera: Libellulidae). Odonatologica, 5: 245–263.Google Scholar
Parry, W.H. 1986. The overwintering strategy of Aphidecta obliterata in Scottish coniferous forests. In Ecology of Aphidophaga. Edited by Hodek, I.. Academia, Prague; Dr. W. Junk, Dordrecht. pp. 179–184.Google Scholar
Pullin, A.S. 1994. Evolution of cold hardiness strategies in insects. CryoLetters, 15: 6–7.Google Scholar
Pullin, A.S., and Bale, J.S. 1989. Influence of diapause and temperature on cryoprotectant synthesis and cold hardiness in pupae of Pieris brassicae. Comparative Biochemistry and Physiology A, 94: 499–503.Google Scholar
Ramløv, H., Wharton, D.A., and Wilson, P. W. 1996. Recrystallization in a freezing tolerant Antarctic nematode, Panagrolaimus davidi, and an alpine weta, Hemideina maori (Orthoptera; Stenopelmatidae). Cryobiology, 33: 607–613.Google Scholar
Ricci, C. 2001. Dormancy patterns in rotifers. Hydrobiologia, 446/447: 1–11.Google Scholar
Ring, R.A. 1977. Cold-hardiness of the bark beetle, Scolytus ratzeburgi Jans. (Col., Scolytidae). Norwegian Journal of Entomology, 24: 125–136.Google Scholar
Ring, R.A. 1981. The physiology and biochemistry of cold tolerance in arctic insects. Journal of Thermal Biology, 6: 219–229.Google Scholar
Ring, R.A. 1982. Freezing-tolerant insects with low supercooling points. Comparative Biochemistry and Physiology A, 73: 605–612.Google Scholar
Ring, R.A. 1983. Cold tolerance in Canadian arctic insects. In Plant, animal, and microbial adaptations to terrestrial environments. Edited by Margaris, N.S., Arianoutsou-Faraggitaki, M., and Reiter, R.J.. Plenum, New York. pp. 17–29.Google Scholar
Ring, R.A., and Danks, H.V. 1994. Desiccation and cryoprotection: overlapping adaptations. CryoLetters, 15: 181–190.Google Scholar
Ring, R.A., and Danks, H.V. 1998. The role of trehalose in cold-hardiness and desiccation. CryoLetters, 19: 275–282.Google Scholar
Ring, R.A., and Tesar, D. 1981. Adaptations to cold in Canadian Arctic insects. Cryobiology, 18: 199–211.Google Scholar
Rivers, D.B., Antonelli, A. L., and Yoder, J.A. 2002. Bags of the bagworm Thyridopteryx ephemeraeformis (Lepidoptera: Psychidae) protect diapausing eggs from water loss and chilling injury. Annals of t he Entomological Society of America, 95: 481–486.Google Scholar
Ryan, R.B. 1975. Photoperiod effects on development of the larch casebearer, Coleophora laricella (Lepidoptera: Coleophoridae). The Canadian Entomologist, 107: 1305–1310.Google Scholar
Sabelis, M.W., and Janssen, A. 1994. Evolution of life-history patterns in the Phytoseiidae. In Mites: ecological and evolutionary analyses of life-history patterns. Edited by Houck, M.A.. Chapman and Hall, New York. pp. 70–98.Google Scholar
Sakagami, S.F., Tanno, K., Tsutsui, H., and Honma, K. 1985. The role of cocoons in overwintering of the soybean pod borer Leguminivora glycinivorella (Lepidoptera: Tortricidae). Journal of the Kansas Entomological Society, 58: 240–247.Google Scholar
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.Google Scholar
Sinclair, B.J. 1999. Insect cold tolerance: How many kinds of frozen? European Journal of Entomology, 96: 157–164.Google Scholar
Sinclair, B.J. 2001. Field ecology of freeze tolerance: interannual variation in cooling rates, freeze—thaw and thermal stress in the microhabitat of the alpine cockroach Celatoblatta quin-quemaculata. Oikos, 93: 286–293.CrossRefGoogle Scholar
Sinclair, B.J., and Chown, S.L. 2003. Rapid responses to high temperature and desiccation but not to low temperature in the freeze tolerant sub-Antarctic caterpillar Pringleophaga marioni (Lepidoptera, Tineidae). Journal of Insect Physiology, 49: 45–52.Google Scholar
Šlachta, M., Vambera, J., Zahradnĭčková, H., and Košt'ál, V. 2002. Entering diapause is a prerequisite for successful cold-acclimation in adult Graphosoma lineatum (Heteroptera: Pentatomidae). Journal of Insect Physiology, 48: 1031–1039.Google Scholar
Sømme, L. 1974 a. The overwintering of Pelophila borealis Payk. III. Freezing tolerance. Norsk Entomologisk Tidsskrift, 21: 131–134.Google Scholar
Sømme, L. 1974 b. Anaerobiosis in some alpine Coleoptera. Norsk Entomologisk Tidsskrift, 21: 155–158.Google Scholar
Sømme, L. 1996. Anhydrobiosis and cold tolerance in tardigrades. European Journal of Entomology, 93: 349–357.Google Scholar
Sømme, L. 1999. The physiology of cold hardiness in terrestrial arthropods. European Journal of Entomology, 96: 1–10.Google Scholar
Sømme, L., and Birkemoe, T. 1997. Cold tolerance and dehydration in Enchytraeidae from Svalbard. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 167: 264–269.Google Scholar
Soszynska, A., and Durska, E. 2002. Cold-adapted scuttle-flies species of Triphleba Rondani (Diptera: Phoridae). Annales Zoologici, 52: 279–283.Google Scholar
Spieth, H.R. 2002. Estivation and hibernation of Pieris brassicae (L.) in southern Spain: synchronization of two complex behavioral patterns. Population Ecology, 44: 273–280.Google Scholar
Stearns, S.C., and Kawecki, T.J. 1994. Fitness sensitivity and the canalization of life-history traits. Evolution, 48: 1438–1450.Google Scholar
Stevens, D.J., Hansell, M.H., Freel, J.A., and Monaghan, P. 1999. Developmental trade-offs in caddis flies: increased investment in larval defence alters adult resource allocation. Proceedings of the Royal Society Biological Sciences Series B, 266: 1049–1054.Google Scholar
Stevens, D.J., Hansell, M.H., and Monaghan, P. 2000. Developmental trade-offs and life histories: Strategic allocation of resources in caddis flies. Proceedings of the Royal Society Biological Sciences Series B, 267: 1511–1515.Google Scholar
Storey, K.B., and Storey, J.M. 1988. Freeze tolerance in animals. Physiological Reviews, 68: 27–84.Google Scholar
Storey, K.B., and Storey, J.M. 1992. Biochemical adaptations for winter survival in insects. Advances in Low-Temperature Biology, 1: 101–140.Google Scholar
Storey, K.B., Baust, J.G., and Beuscher, P. 1981. Determination of water “bound” by soluble subcellular components during low-temperature acclimation in the gall fly larva, Eurosta solidagensis. Cryobiology, 18: 315–321.Google Scholar
Storey, K.B., Churchill, T. A., and Joanisse, D.R. 1993. Freeze tolerance in hermit flower beetle (Osmoderma eremicola) larvae. Journal of Insect Physiology, 39: 737–742.Google Scholar
Strong-Gunderson, J.M., Lee, R.E. Jr., and Lee, M.R. 1989. Ice-nucleating bacteria promote transcuticular nucleation in insects. Cryobiology, 26: 551.Google Scholar
Tanaka, S. 1983. Seasonal control of nymphal diapause in the spring ground cricket, Pteronemobius nitidus (Orthoptera: Gryllidae). In Diapause and life cycle strategies in insects. Edited by Brown, V.K. and Hodek, I.. Series Entomologica. Vol. 23. Dr. W. Junk, The Hague. pp. 35–53.Google Scholar
Tanno, K. 1977. Ecological observation and frost-resistance in overwintering pre-pupae, Sciara sp. (Sciaridae). Low Temperature Science, Series B Biological Sciences, 35: 63–74.Google Scholar
Tillman, P.G., and Powell, J.E. 1991. Developmental time in relation to temperature for Microplitis croceipes, M. demolitor, Cotesia kazak (Hymenoptera: Braconidae), and Hyposoter didymator (Hymenoptera: Ichneumonidae), endoparasitoids of the t obacco budworm ( Lepidoptera: Noctuidae). Environmental Entomology, 20: 61–64.Google Scholar
Townsend, G.D., and Pritchard, G. 1998. Larval growth and development of the stonefly Pteronarcys californica (Insecta: Plecoptera) in the Crowsnest River, Alberta. Canadian Journal of Zoology, 76: 2274–2280.Google Scholar
Turnock, W.J., and Boivin, G. 1997. Inter- and intra-population differences in the effects of temperature on postdiapause development of Delia radicum. Entomologia Experimentalis et Applicata, 84: 255–265.Google Scholar
Turnock, W. J., Reader, P.M., and Bracken, G.K. 1990. A comparison of the cold hardiness of populations of Delia radicum (L.) (Diptera: Anthomyiidae) from southern England and the Canadian prairies. Canadian Journal of Zoology, 68: 830–835.Google Scholar
Turnock, W. J., Boivin, G., and Ring, R.A. 1998. Interpopulation differences in the coldhardiness of Delia radicum (Diptera: Anthomyiidae). The Canadian Entomologist, 130: 119–129.Google Scholar
Vali, G. 1995. Principles of ice nucleation. In Biological ice nucleation and its applications. Edited by Lee, R.E. Jr., Warren, G.J., and Gusta, L.V.. American Phytopathological Society, St. Paul, Minnesota. pp. 1–28.Google Scholar
van der Woude, H.A., and Verhoef, H.A. 1988. Reproductive diapause and cold hardiness in temperate Collembola Orchesella cincta and Tomocerus minor. Journal of Insect Physiology, 34: 387–392.CrossRefGoogle Scholar
Vernon, P., and Vannier, G. 2002. Evolution of freezing susceptibility and freezing tolerance in terrestrial arthropods. Comptes Rendus Biologies, 325: 1185–1190.Google Scholar
Voituron, Y., Mouquet, N., de Mazancourt, C., and Clobert, J. 2002. To freeze or not to freeze? An evolutionary perspective on t he cold-hardiness strategies of overwintering ectotherms. American Naturalist, 160: 255–270.Google Scholar
Wassmer, G.T., and Page, T. L. 1993. Photoperiodic time measurement and a graded photoperiodic response in a cockroach. Journal of Biological Rhythms, 8: 47–56.Google Scholar
Watanabe, M., and Tanaka, K. 1998 a. A dult diapause and cold hardiness in Aulacophora nigripennis (Coleoptera: Chrysomelidae). Journal of Insect Physiology, 44: 1103–1110.Google Scholar
Watanabe, M., and Tanaka, K. 1998 b. Effect of juvenile hormone analogs on diapause termination and myoinositol content in Aulacophora nigripennis adults (Coleoptera: Chrysomelidae). Applied Entomology and Zoology, 33: 259–262.Google Scholar
Watanabe, M., and Tanaka, K. 1999. Cold tolerance strategy of the freeze-intolerant chrysomelid, Aulacophora nigripennis (Coleoptera: Chrysomelidae), in warm-temperate regions. European Journal of Entomology, 96: 175–181.Google Scholar
Wathen, B., Kuiper, M., Walker, V., and Jia, Z. 2003. A new model for simulating 3D crystal growth and its application to the study of antifreeze proteins. Journal of the American Chemical Society, 125: 729–737.Google Scholar
Williams, K.S., and Simon, C. 1995. The ecology, behavior, and evolution of periodical cicadas. Annual Review of Entomology, 40: 269–295.Google Scholar
Wilson, P. W., and Leader, J.P. 1995. Stabilization of supercooled fluids by thermal hysteresis proteins. Biophysical Journal, 68: 2098–2107.Google Scholar
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.Google Scholar
Wipking, W., and Mengelkoch, C. 1994. Control of alternate-year flight activities in high-alpine Ringlet butterflies (Erebia, Satyridae) and Burnet moths (Zygaena, Zygaenidae) from temperate environments. In Insect life-cycle polymorphism: theory, evolution and ecological consequences for seasonality and diapause control. Edited by Danks, H.V.. Series Entomologica 52. Kluwer Academic Publishers, Dordrecht. pp. 313–347.Google Scholar
Wolfe, J., Bryant, G., and Koster, K. L. 2002. What is ‘unfreezable water’, how unfreezable is it and how much is there? CryoLetters, 23: 157–166.Google Scholar
Worland, M.R., and Block, W. 2003. Desiccation stress at sub-zero temperatures in polar terrestrial arthropods. Journal of Insect Physiology, 49: 193–203.Google Scholar
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 t he Arctic collembolan Onychiurus arcticus (Tullberg). Journal of Insect Physiology, 44: 211–219.Google Scholar
Worland, M.R., Block, W., and Grubor-Lajsic, G. 2000. Survival of Heleomyza borealis (Diptera, Heleomyzidae) larvae down to –60 °C. Physiological Entomology, 25: 1–5.Google Scholar
Yoder, J.A., Denlinger, D.L., Dennis, M.W., and Kolattukudy, P.E. 1992. Enhancement of diapausing flesh fly puparia with additional hydrocarbons and evidence for alkane biosynthesis by a decarbonylation mechanism. Insect Biochemistry and Molecular Biology, 22: 237–243.Google Scholar
Zachariassen, K.E., and Hammel, H.T. 1976. Nucleating agents in the haemolymph of insects tolerant to freezing. Nature (London), 262: 285–287.Google Scholar
Zachariassen, K.E., K ristiansen, E., Pedersen, S.A., and Hammel, H.T. 2004. Ice nucleation in solutions and freeze-avoiding insects — homogeneous or heterogeneous? Cryobiology, 48: 309–321.Google Scholar
Zwick, P. 1996. Variable egg development of Dinocras spp. (Plecoptera, Perlidae) and the stonefly seed bank theory. Freshwater Biology, 35: 81–100.Google Scholar