Book contents
- Frontmatter
- Contents
- List of contributors
- Preface
- PART I PHYSIOLOGICAL AND MOLECULAR RESPONSES
- 1 A primer on insect cold-tolerance
- 2 Rapid cold-hardening: Ecological significance and underpinning mechanisms
- 3 Antifreeze and ice-nucleator proteins
- 4 Genomics, proteomics and metabolomics: Finding the other players in insect cold-tolerance
- 5 Cell structural modifications in insects at low temperatures
- 6 Oxygen: Stress and adaptation in cold-hardy insects
- 7 Interactions between cold, desiccation and environmental toxins
- PART II ECOLOGICAL AND EVOLUTIONARY RESPONSES
- PART III PRACTICAL APPLICATIONS
- Index
- References
1 - A primer on insect cold-tolerance
from PART I - PHYSIOLOGICAL AND MOLECULAR RESPONSES
Published online by Cambridge University Press: 04 May 2010
Book contents
- Frontmatter
- Contents
- List of contributors
- Preface
- PART I PHYSIOLOGICAL AND MOLECULAR RESPONSES
- 1 A primer on insect cold-tolerance
- 2 Rapid cold-hardening: Ecological significance and underpinning mechanisms
- 3 Antifreeze and ice-nucleator proteins
- 4 Genomics, proteomics and metabolomics: Finding the other players in insect cold-tolerance
- 5 Cell structural modifications in insects at low temperatures
- 6 Oxygen: Stress and adaptation in cold-hardy insects
- 7 Interactions between cold, desiccation and environmental toxins
- PART II ECOLOGICAL AND EVOLUTIONARY RESPONSES
- PART III PRACTICAL APPLICATIONS
- Index
- References
Summary
Introduction
Low temperature affects insects differently based on the severity of the cold and the duration of exposure. Life stage and acclimation state also have a major impact on an insect's response to low temperature. Many temperate and polar insects enhance their cold-tolerance seasonally in preparation for winter, as short, cool days in autumn trigger cold acclimatization, as well as entry into the metabolic depression of diapause. However, insects also have the capacity to make significant and rapid adjustments to even slight changes in environmental temperature, as would occur on a summer's day.
This introductory chapter seeks to provide a short primer on the physiology of insect cold-tolerance that will be useful to students and others new to the area of study. This overview of basic concepts in insect cold-tolerance intends to provide a context for later chapters providing in-depth reviews of specific areas. Specifically, this primer focuses on regulation of supercooling and ice nucleation, and basic adaptations promoting cold-tolerance. Suggestions for conducting and clearly reporting experimental results on insect cold-tolerance are also included. Since this volume is intended to update and complement our previous book, Insects at Low Temperature (Lee and Denlinger, 1991), this synoptic chapter will emphasize articles published during the past 20 years and topics not covered elsewhere in this volume.
Types of insect cold-tolerance
Chilling and cold are relative terms; consequently, the temperature ranges they represent vary depending on the species in question.
- Type
- Chapter
- Information
- Low Temperature Biology of Insects , pp. 3 - 34Publisher: Cambridge University PressPrint publication year: 2010
References
and (2003). Protective effect of intracellular ice during freezing?Cryobiology 46, 197–202.CrossRefGoogle ScholarPubMed
and (1996). Freeze-protection of overwintering monarch butterflies in Mexico: critical role of the forest as a blanket and an umbrella. Ecological Entomology 21, 107–116.CrossRefGoogle Scholar
(1982). Supercooled water. In Water: A Comprehensive Treatise, ed. , vol. 7. New York: Plenum Press, pp. 1–81.Google Scholar
and (1997). Modeling seasonal changes in intracellular freeze-tolerance of fat body cells of the gall fly Eurosta solidaginis (Diptera, Tephritidae). Journal of Experimental Biology 200, 185–192.Google Scholar
, , , , , , , , , and (2005). Comparative overwintering physiology of Alaska and Indiana populations of the beetle Cucujus clavipes (Fabricius): role of antifreeze proteins, polyols, dehydration and diapause. Journal of Experimental Biology 208, 4467–4477.CrossRefGoogle Scholar
, , , , , , and (2005). NMR relaxation studies on the hydrate layer of intrinsically unstructured proteins. Biophysical Journal 88, 2030–2037.CrossRefGoogle ScholarPubMed
, , , and (1999). Cellular and molecular biology of the aquaporin water channels. Annual Review of Biochemistry 68, 425–458.CrossRefGoogle ScholarPubMed
, , , , and (2002). Accumulation of dehydrin-like proteins in the mitochondria of cereals in response to cold, freezing, drought and ABA treatment. BMC Plant Biology 2, 5–12.CrossRefGoogle ScholarPubMed
, , , and (2008). Invertebrate aquaporins: a review. Journal of Comparative Physiology B 178, 935–955.CrossRefGoogle ScholarPubMed
, , , and (2000). Identification of ice-nucleating active Pseudomonas fluorescens strains for biological control of overwintering Colorado potato beetles (Coleoptera: Chrysomelidae). Journal of Economic Entomology 93, 226–233.CrossRefGoogle Scholar
, , , , and (2001). Field persistence of ice-nucleating bacteria in overwintering Colorado potato beetles. Biological Control 21, 11–18.CrossRefGoogle Scholar
and (1992). Reduction of cold injury in flies using an intermittent pulse of high temperature. Cryobiology 29, 138–143.CrossRefGoogle Scholar
and (2004). Insect Physiological Ecology: Mechanisms and Patterns. New York: Oxford University Press.CrossRefGoogle Scholar
, , and (2008). Physiological variation and phenotypic plasticity: a response to ‘Plasticity in arthropod cryotypes’ by Hawes and Bale. Journal of Experimental Biology 211, 3353–3357.CrossRefGoogle ScholarPubMed
and (2007). Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology 33, 50–152.CrossRefGoogle Scholar
, , and (2002). Ice structuring proteins: a new name for antifreeze proteins. CryoLetters 23, 89–92.Google ScholarPubMed
, , , , and (2007). Proteomic profiling of a parasitic wasp exposed to constant and fluctuating cold exposure. Insect Biochemistry and Molecular Biology 37, 1177–1188.CrossRefGoogle ScholarPubMed
, , , and (2006). The impact of fluctuating thermal regimes on the survival of a cold-exposed parasitic wasp, Aphidius colemani. Physiological Entomology 31, 234–240.CrossRefGoogle Scholar
, , , , , and (1998a). Long-term reduction of cold hardiness following ingestion of ice-nucleating bacteria in the Colorado potato beetle, Leptinotarsa decemlineata. Journal of Insect Physiology 44, 1173–1180.CrossRefGoogle Scholar
and (2005). Cryoprotection by urea in a terrestrially hibernating frog. Journal of Experimental Biology 208, 4079–4089.CrossRefGoogle Scholar
, , , and (1998b). Soil hydric characteristics and environmental ice nuclei influence supercooling capacity of hatchling turtles Chrysemys picta. Journal of Experimental Biology 201, 3105–3112.Google ScholarPubMed
, , , , and (1997). Influence of soil hydric parameters on the winter cold hardiness of a burrowing beetle, Leptinotarsa decemlineata (Say). Journal of Comparative Physiology B 167, 169–176.CrossRefGoogle Scholar
, , and (1998). The role of vitrification in anhydrobiosis. Annual Review of Physiology 60, 73–103.CrossRefGoogle ScholarPubMed
(2002). Lessons from nature: the role of sugars in anhydrobiosis. Comparative Biochemistry and Physiology A – Molecular and Integrative Physiology 131, 505–513.CrossRefGoogle ScholarPubMed
, , , , , , , , and (2008). Effects of temperature on physiology and reproductive success of a montane leaf beetle: implications for persistence of native populations enduring climate change. Physiological and Biochemical Zoology 81, 718–732.CrossRefGoogle ScholarPubMed
(1971). Overwintering of some north temperate and arctic Chironomidae. II. Chironomid biology. Canadian Entomologist 103, 1875–1910.CrossRefGoogle Scholar
(2000). Dehydration in dormant insects. Journal of Insect Physiology 46, 837–852.CrossRefGoogle ScholarPubMed
(2007). How aquatic insects live in cold climates. Canadian Entomologist 139, 443–471.CrossRefGoogle Scholar
and (2001). Intracellular freezing, viability, and composition of fat body cells from freeze-intolerant larvae of Sarcophaga crassipalpis. Archives of Insect Biochemistry and Physiology 48, 199–205.CrossRefGoogle ScholarPubMed
and (1998). Physiology of cold sensitivity. In Temperature Sensitivity in Insects and Application in Integrated Pest Management, ed. , and . Boulder: Westview Press, pp. 55–95.Google Scholar
(2001). Antifreeze and ice nucleator proteins in terrestrial arthropods. Annual Review of Physiology 63, 327–357.CrossRefGoogle ScholarPubMed
(2002). The inhibition of ice nucleators by insect antifreeze proteins is enhanced by glycerol and citrate. Journal of Comparative Physiology B 172, 163–168.Google ScholarPubMed
, , , , and (2004). Antifreeze proteins in Alaskan insects and spiders. Journal of Insect Physiology 50, 259–266.CrossRefGoogle ScholarPubMed
(1993). Structural motifs in LEA proteins of higher plants. In Response of Plants to Cellular Dehydration during Environmental Stress, ed. and . Rockville, MD: American Society of Plant Physiologists, pp. 91–103.Google Scholar
, , , and (2003). Artificial expression of aquaporin-3 improves the survival of mouse oocytes after cryopreservation. Biology of Reproduction 68, 87–94.CrossRefGoogle ScholarPubMed
, , and (1997). Temporal accumulation and ultrastructural localization of dehydrins in Zea mays. Physiologia Plantarum 101, 545–555.CrossRefGoogle Scholar
, , , , and (2008). Cryoprotective dehydration and the resistance to inoculative freezing in the Antarctic midge, Belgica antarctica. Journal of Experimental Biology 211, 524–530.CrossRefGoogle ScholarPubMed
(1990). The cold-hardiness of Cryptolestes ferrugineus and the use of ice nucleation-active bacteria as a cold-synergist. Proceedings of the Fifth International Working Conference on Stored-Product Protection, pp. 1183–1191.Google Scholar
(1993). Reduction of cold tolerance of stored-product insects by ice-nucleating-active bacteria. Environmental Entomology 22, 470–476.CrossRefGoogle Scholar
and (1997). Inoculative freezing and the problem of winter survival for freshwater macroinvertebrates. Journal of the North American Benthological Society 16, 635–650.CrossRefGoogle Scholar
and (2007). p38 MAP kinase is a likely component of the signal transduction pathway triggering rapid cold-hardening in the flesh fly, Sarcophaga crassipalpis. Journal of Experimental Biology 210, 3295–3300.CrossRefGoogle Scholar
and (1992). Supercooling in a freeze-tolerant cranefly larva, Tipula sp. Journal of Insect Physiology 38, 131–137.CrossRefGoogle Scholar
, , , and (1991). Inoculative freezing in overwintering tenebrionid beetle, Bolitophagus reticulatus Panz. Journal of Insect Physiology 37, 683–687.CrossRefGoogle Scholar
and (1998). Introduction: temperature sensitivity and integrated pest management. In Temperature Sensitivity in Insects and Application in Integrated Pest Management, ed. and . Boulder: Westview Press, pp. 1–5.Google Scholar
and (2007). Plasticity in arthropod cryotypes. Journal of Experimental Biology 210, 2585–2592.CrossRefGoogle ScholarPubMed
(1993). The Hot-Blooded Insects: Strategies and Mechanisms of Thermoregulation. Cambridge, MA: Harvard University Press.Google Scholar
, , and (1985). A novel method of natural cryoprotection. Plant Physiology 79, 41–56.CrossRefGoogle ScholarPubMed
(1995). Polyol accumulation in earthworm cocoons induced by dehydration. Comparative Biochemistry and Physiology A 111, 251–255.CrossRefGoogle Scholar
, , and (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
, , and (1999). Cryoprotective and osmotic responses to cold acclimation and freezing in freeze-tolerant and freeze-intolerant earthworms. Journal of Comparative Physiology B 169, 207–214.CrossRefGoogle Scholar
and (1998). Dehydration and cold hardiness in the Arctic collembolan Onychiurus arcticus Tullberg 1876. Journal of Comparative Physiology B 168, 197–203.CrossRefGoogle Scholar
and (1994). Dehydration of earthworm cocoons exposed to cold: a novel cold hardiness mechanism. Journal of Comparative Physiology B 164, 312–315.CrossRefGoogle Scholar
, , and (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
and (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
, , and (2007). Effects of diapause and cold-acclimation on the avoidance of freezing injury in fat body tissue of the rice stem borer, Chilo suppressalis Walker. Journal of Insect Physiology 53, 685–690.CrossRefGoogle ScholarPubMed
, , , , and (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
, , , and (2008). Climate change and outbreaks of geometrids Operophtera brumata and Epirrita autumnata in subarctic birch forest: evidence of a recent outbreak range expansion. Journal of Animal Ecology 77, 257–264.CrossRefGoogle ScholarPubMed
, , and (1991a). INA bacteria isolated from diamondback moth, Plutella xylostella L. pupae (Lepidoptera: Yponomeutidae). Japanese Journal of Applied Entomology and Zoology 35, 7–11.CrossRefGoogle Scholar
, , , and (1991b). Erwinia herbicola: ice nucleation active bacteria isolated from diamondback moth, Plutella xylostella L. pupae. Japanese Journal of Applied Entomology and Zoology 35, 247–251.CrossRefGoogle Scholar
, , , and (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
and (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.CrossRefGoogle Scholar
, , , , , , , and (2006). Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochemical and Biophysical Research Communications 348, 56–61.CrossRefGoogle Scholar
, , , , , , , and (2007). Trehalose transporter 1, a facilitated and high-capacity trehalose transporter allows exogenous trehalose uptake into cells. Proceedings of the National Academy of Sciences, USA 104, 11585–11590.CrossRefGoogle ScholarPubMed
(1984). A novel cold-tolerant insect found in a Himalayan glacier. Nature 310, 225–227.CrossRefGoogle Scholar
, , and (2001). Cryoprotective role of polyols independent of the increase in supercooling capacity in diapausing adults of Pyrrhocoris apterus (Heteroptera: Insecta). Comparative Biochemistry and Physiology Part B 130, 365–374.CrossRefGoogle Scholar
, , and (2004). On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in adults of Pyrrhocoris apterus. Journal of Experimental Biology 207, 1509–1521.CrossRefGoogle ScholarPubMed
, , , and (2007). Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of ion homeostasis. Comparative Biochemistry and Physiology, Part A 147, 231–238.CrossRefGoogle ScholarPubMed
, , and (2006). Chilling-injury and disturbance of ion homeostasis in the coxal muscle of the tropical cockroach (Nauphoeta cinerea). Comparative Biochemistry and Physiology B 143, 173–179.CrossRefGoogle Scholar
, , and (2007). Sperm production and mating potential of males after a cold shock on pupae of the parasitoid wasp Dinarmus basalis. Journal of Insect Physiology 53, 1008–1015.CrossRefGoogle ScholarPubMed
(2001). Physiological Plant Ecology: Ecophysiology and Stress Physiology of Functional Groups, 4th edn. New York: Springer.Google Scholar
and (1994). Cold tolerance including rapid cold-hardening and inoculative freezing in migrant monarch butterflies in Ohio. Journal of Insect Physiology 40, 859–864.CrossRefGoogle Scholar
, , and (1990). Inoculation triggers at high subzero temperatures in a freeze-tolerant frog (Rana sylvatica) and insect (Eurosta solidaginis). Canadian Journal of Zoology 68, 506–510.CrossRefGoogle Scholar
, , , and (1995a). Isolation of ice-nucleating active bacteria from the freeze tolerant frog, Rana sylvatica. Cryobiology 32, 358–365.CrossRefGoogle ScholarPubMed
(1989). Insect cold-hardiness: to freeze or not to freeze. BioScience 39, 308–313.CrossRefGoogle Scholar
(1991). Principles of insect low temperature tolerance. In Insects at Low Temperature, ed. and . New York and London: Chapman and Hall, pp. 17–46.CrossRefGoogle Scholar
, , , , and (2001). Using ice-nucleating bacteria to reduce winter survival of Colorado potato beetles: development of a novel strategy for biological control. In Insect Timing: Circadian Rhythmicity to Seasonality, ed. , and . Amsterdam: Elsevier, pp. 213–227.CrossRefGoogle Scholar
and (1998). Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Annual Review of Physiology 60, 55–72.CrossRefGoogle ScholarPubMed
, , , , and (1994). Ice-nucleating active bacteria reduce the cold-hardiness of the freeze-intolerant Colorado potato beetle (Coleoptera, Chrysomelidae). Journal of Economic Entomology 87, 377–381.CrossRefGoogle Scholar
, , , and (2006). Rapid cold-hardening increases membrane fluidity and cold tolerance of insect cells. Cryobiology 52, 459–463.CrossRefGoogle ScholarPubMed
, , and (1993a). Insect cold-hardiness and ice nucleating active microorganisms including their potential use for biological control. Journal of Insect Physiology 39, 1–12.CrossRefGoogle Scholar
, , and (1995b). Biological control of insect pests using ice-nucleating microorganisms. In Biological Ice Nucleations and its Applications, ed. , and . St. Paul: APS Press, pp. 257–269.Google Scholar
and (1985). Effect of temperature and duration of exposure on tissue ice formation in the gall fly, Eurosta solidaginis (Diptera, Tephritidae). CryoLetters 6, 24–34.Google Scholar
, , , and (1993b). Survival of intracellular freezing, lipid coalescence and osmotic fragility in fat-body cells of the freeze-tolerant gall fly Eurosta solidaginis. Journal of Insect Physiology 39, 445–450.CrossRefGoogle Scholar
, , , , and (1996). Anatomic site of application of ice-nucleating active bacteria affects supercooling in the Colorado potato beetle (Coleoptera: Chrysomelidae). Environmental Entomology 25, 465–469.CrossRefGoogle Scholar
, , , and (1992). Ice-nucleating active bacteria decrease the cold-hardiness of stored grain insects. Journal of Economic Entomology 85, 371–374.CrossRefGoogle Scholar
, , , , and (1991). Isolation of ice nucleating active bacteria from insects. Journal of Experimental Zoology 257, 124–127.CrossRefGoogle Scholar
, , and (eds.) (1995c). Biological Ice Nucleation and its Applications. St. Paul: APS Press.
, , and (1998). Post pupariation cold storage of three species of flies: increasing chilling tolerance by acclimation and recurrent recovery periods. Cryobiology 36, 213–224.CrossRefGoogle ScholarPubMed
(1980). Responses of Plants to Environmental Stresses, 2nd edn. New York: Academic Press, Inc.Google Scholar
(1983). The role of bacterial ice nucleation in frost injury to plants. Annual Review of Phytopathology 21, 363–384.CrossRefGoogle Scholar
(1953). The mechanism of the protective action of glycerol against haemolysis by freezing and thawing. Biochimica et Biophysica Acta 11, 28–36.CrossRefGoogle ScholarPubMed
(2004). Principles of cryobiology. In Life in the Frozen State, ed. , and . Boca Raton: CRC Press, pp. 3–66.CrossRefGoogle Scholar
and (2008). 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
(1968). Modified model for the mechanism of freezing injury in erythrocytes. Nature 218, 333–336.CrossRefGoogle ScholarPubMed
and (1991). Surviving the big chill: overwintering strategies of aquatic and terrestrial insects. American EntomologistSummer111–118.CrossRefGoogle Scholar
, , and (1994). Comparative ultrastructure of fat body cells of freeze-susceptible and freeze-tolerant Eurosta solidaginis larvae after chemical fixation and high pressure freezing. Journal of Insect Physiology 40, 155–164.CrossRefGoogle Scholar
, , and (1996). Fat body cells and calcium phosphate spherules induce ice nucleation in the freeze-tolerant larvae of the gall fly Eurosta solidaginis (Diptera, Tephritidae). Journal of Experimental Biology 199, 465–471.Google Scholar
, , , and (2004). The water to ice transition: implications for living cells. In Life in the Frozen State, ed. , and . Boca Raton: CRC Press, pp. 67–108.CrossRefGoogle Scholar
(2000). Snow White and the Seven Dwarfs: a multvariate approach to classification of cold tolerance. CryoLetters 21, 339–348.Google Scholar
and (1997). Freezing survival by isolated Malpighian tubules of the New Zealand alpine weta Hemideina maori. Journal of Experimental Biology 201, 227–236.Google Scholar
and (2003). Modeling current and future potential wintering distributions of eastern North American monarch butterflies. Proceedings of the National Academy of Sciences, USA 100, 14063–14068.CrossRefGoogle ScholarPubMed
, , , and (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
, , and (1991). Overwintering of freshwater benthic marcoinvertebrates. In Insects at Low Temperature, ed. and . New York: Chapman and Hall, pp. 360–375.CrossRefGoogle Scholar
, , , and (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
, , and (2007). Evidence for a novel cryoprotective protein from freeze-tolerant larvae of the goldenrod gall fly Eurosta solidaginis. Cryobiology 54, 125–128.CrossRefGoogle ScholarPubMed
, , , and (2007). Influence of soil moisture on egg cold hardiness in the migratory locust Locusta migratoria (Orthoptera: Acrididae). Physiological Entomology 32, 219–224.CrossRefGoogle Scholar
and (2000). Extreme resistance to desiccation in overwintering larvae of the gall fly Eurosta solidaginis (Diptera: Tephritidae). Journal of Experimental Biology 203, 983–789.Google Scholar
and (2007). Modeling cold tolerance in the mountain pine beetle, Dendroctonus ponderosae. Journal of Insect Physiology 53, 559–572.CrossRefGoogle ScholarPubMed
, , , and (2004). The importance of fluctuating thermal regimes for repairing chill injuries in the tropical beetle Alphitobius diaperinus (Coleoptera: Tenebrionidae) during exposure to low temperature. Physiological Entomology 29, 139–145.CrossRefGoogle Scholar
, , , , , and (2006). Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect. Proceedings of the National Academy of Sciences, USA 103, 14223–14227.CrossRefGoogle Scholar
, , , , , and (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
and (1980). Cold-hardiness of the arctic beetle, Pytho americanus Kirby Coleoptera, Pythidae (Salpingidae). Journal of Insect Physiology 26, 763–774.CrossRefGoogle Scholar
and (1981). Adaptations to cold in Canadian Arctic insects. Cryobiology 18, 199–211.CrossRefGoogle ScholarPubMed
and (1996). Chilling injury in the housefly: evidence for the role of oxidative stress between pupariation and emergence. Cryobiology 33, 447–458.CrossRefGoogle Scholar
, , , , , , , and (2008). Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki. Proceedings of the National Academy of Sciences, USA 105, 5093–5098.CrossRefGoogle Scholar
(1961). Principles of insect cold-hardiness. Annual Review of Entomology 6, 55–74.CrossRefGoogle Scholar
, , , and (1953). Studies on the physiology of frozen plants and animals in the Arctic. Journal of Cellular Comparative Physiology 42, 1–56.CrossRefGoogle ScholarPubMed
and (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
(1999). Insect cold tolerance: how many kinds of frozen?European Journal of Entomology 96, 157–164.Google Scholar
, , and (2003). Climatic variability and the evolution of insect freeze tolerance. Biological Reviews 78, 181–195.CrossRefGoogle ScholarPubMed
and (1997). Avoidance of intracellular freezing by the freezing-tolerant New Zealand Alpine weta Hemideina maori (Orthoptera: Stenopelmatidae). Journal of Insect Physiology 43, 621–625.CrossRefGoogle Scholar
(1992). Adapting to water stress: convergence on common solutions. In Water and Life, ed. , , and . London: Springer-Verlag, pp. 3–18.CrossRefGoogle Scholar
(1982). Supercooling and winter survival in terrestrial arthropods. Comparative Biochemistry and Physiology 73A, 519–543.CrossRefGoogle Scholar
, , , and (1995). Effect of biological ice nucleators on insect supercooling capacity varies with anatomic site of application. Journal of Insect Physiology 41, 603–608.CrossRefGoogle Scholar
and (1989). Freeze/thaw-induced destabilization of the plasma membrane and the effects of cold acclimation. Journal of Bioenergetics and Biomembranes 21, 21–41.CrossRefGoogle ScholarPubMed
, , and (1981). Intermediary metabolism during low temperature acclimation in the overwintering gall fly larva, Eurosta solidaginis. Journal of Comparative Physiology B 144, 183–190.CrossRefGoogle Scholar
and (1988). Freeze tolerance in animals. Physiological Reviews 68, 27–84.CrossRefGoogle ScholarPubMed
and (1991). Biochemistry of cryoprotectants. In Insects at Low Temperature, ed. , and . New York and London: Chapman and Hall, pp. 64–93.CrossRefGoogle Scholar
and (1996). Natural freezing survival in animals. Annual Review of Ecology and Systematics 27, 365–386.CrossRefGoogle Scholar
, , , and (1990). Ingestion of ice-nucleating active bacteria increases the supercooling point of the lady beetle Hippodamia convergens. Journal of Insect Physiology 36, 153–157.CrossRefGoogle Scholar
and (2003). Transmission of ice-nucleating active bacteria from a prey reduces cold hardiness of a predator (Araneae: Theridiidae). Naturwissenschaften 90, 449–451.CrossRefGoogle Scholar
, , , , , and (2002). Aquaporin expression correlates with freeze tolerance in baker's yeast, and overexpression improves freeze tolerance in industrial strains. Applied and Environmental Microbiology 68, 5981–5989.CrossRefGoogle ScholarPubMed
, , and (2007). Vitrification in tissue preservation: new developments. In Life in the Frozen State, ed. , and . Boca Raton: CRC Press, pp. 603–642.Google Scholar
, , , , , and (2008). Rapid cold-hardening in larvae of the Antarctic midge, Belgica antarctica: cellular cold-sensing and a role for calcium. American Journal of Physiology 294, R1938–R1946.Google Scholar
, , , , and (2007). Impact of minimum winter temperatures on the population dynamics of Dendroctonus frontalis. Ecological Applications 17, 882–899.CrossRefGoogle ScholarPubMed
, , , and (1992). An ice-nucleating active fungus isolated from the gut of the rice stem borer, Chilo suppressalis Walker (Lepidoptera: Pyralidae). Journal of Insect Physiology 38, 119–125.CrossRefGoogle Scholar
and (1993). The reversal of cold injury and its effect on the response to subsequent cold exposures. CryoLetters 14, 251–256.Google Scholar
and (2005). Winter climates and cold hardiness in terrestrial insects. European Journal of Entomology 102, 561–576.CrossRefGoogle Scholar
, , and (1994). Freeze tolerance adaptations in the centipede, Lithobius forficatus. Journal of Experimental Zoology 268, 347–353.CrossRefGoogle Scholar
, , , , and (2005). A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Science 308, 691–693.CrossRefGoogle Scholar
(1995). Principles of ice nucleation. In Biological Ice Nucleation and its Applications, ed. , and . St. Paul: APS Press, pp. 1–28.Google Scholar
and (2002). Evolution of freezing susceptibility and freezing tolerance in terrestial arthropods. Comptes Rendus Biologies 325, 1185–1190.CrossRefGoogle Scholar
, , , and (2002). To freeze or not to freeze? An evolutionary perspective on the cold-hardiness strategies of overwintering ectotherms. American Naturalist 160, 255–270.Google ScholarPubMed
, , , and (2009). Freeze tolerance in an Alaska stonefly. Journal of Experimental Biology 212, 305–312.CrossRefGoogle Scholar
and (1995). Survival of intracellular freezing by the antarctic nematode Panagrolaimus davidi. Journal of Experimental Biology 198, 1381–1387.Google ScholarPubMed
, , and (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
, , and (2003). Ice nucleation in nature: supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology 46, 88–98.CrossRefGoogle ScholarPubMed
, , and (1998). Partial desiccation induced by sub-zero temperatures as a component of the survival strategy of the Arctic collembolan Onychiurus arcticus (Tullberg). Journal of Insect Physiology 44, 211–219.CrossRefGoogle Scholar
, , and (2004). Intracellular freezing and survival in the freeze tolerant alpine cockroach Celatoblatta quinquemaculata. Journal of Insect Physiology 50, 225–232.CrossRefGoogle ScholarPubMed
(2005). Organic osmolytes as compatible, metabolic and counteracting cryoprotectants in high osmolarity and other stresses. Journal of Experimental Biology 208, 2819–2830.CrossRefGoogle Scholar
and (2004). In vivo and in vitro rapid cold hardening protects cells from cold-shock injury in the flesh fly. Journal of Comparative Physiology B 174, 611–615.CrossRefGoogle ScholarPubMed
and (2005). Changes in gut and Malpighian tubule transport during seasonal acclimatization and freezing in the gall fly Eurosta solidaginis. Journal of Experimental Biology 208, 1895–1904.CrossRefGoogle ScholarPubMed
, , and (2007). Rapid cold-hardening protects Drosophila melanogaster from cold-induced apoptosis. Apoptosis 12, 1183–1193.CrossRefGoogle ScholarPubMed
(1985). Physiology of cold tolerance in insects. Physiological Reviews 65, 799–832.CrossRefGoogle ScholarPubMed
(1991). The water relations of terrestrial arthropods. In Insects at Low Temperature, ed. and . New York and London: Chapman and Hall, pp. 47–63.CrossRefGoogle Scholar
(1992). Ice nucleating agents in cold-hardy insects. In Water and Life, ed. , and . Berlin: Springer-Verlag, pp. 261–281.CrossRefGoogle Scholar
and (1976). Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262, 285–287.CrossRefGoogle ScholarPubMed
and (1982). Antifreeze effect of thermal hysteresis agents protects highly supercooled insects. Nature 298, 865–867.CrossRefGoogle Scholar
, , , and (2004). Ice nucleation in solutions and freeze-avoiding insects: homogeneous or heterogeneous?Cryobiology 48, 309–321.CrossRefGoogle ScholarPubMed
- 160
- Cited by