Eur. J. Entomol. 102 (4): 561-576, 2005 | DOI: 10.14411/eje.2005.081

Winter climates and coldhardiness in terrestrial insects

William J. TURNOCK, Paul G. FIELDS*
Cereal Research Centre, Agriculture and Agri-Food Canada, 195 Dafoe Rd, Winnipeg, MB, Canada R3T 2M9

Overwintering insects must avoid injury and death from the freezing of tissues and from metabolic disruptions associated with exposure to low, non-freezing temperatures. The winter climates of the world are classified in relation to insect overwintering on the basis of their minimum temperatures and the duration of the winter (when temperatures are below the thermal range for activity and development). Outside the Tropical Wet zone, the severity of exposure to cold (temperature, snowfall, duration of exposure, predictability, variability) can vary from a few days at 0°C to months below -20°C with extremes as low as -60°C. The severity of the temperature exposure may be ameliorated by the selection by insects of overwintering sites (exposed, partly-exposed, protected). The relationships among overwintering habitats, the minimum winter temperature in climatic zones, and the supercooling points (SCP) of over 350 terrestrial insects from published reports were examined. Variability in the SCP among insects within each climatic zone and habitat was wide. Among the freeze-susceptible species that overwintered in exposed or partly-protected habitats the SCP and the cold severity of climate were correlated. This was not the case for insects that overwintered in protected habitats. The SCP's of freeze-tolerant insects were generally higher than the freeze-susceptible insects, and the SCP's were not tightly linked with the cold severity of climatic zone. Insects, both freeze-susceptible and freeze-tolerant, overwintering in exposed habitats had lower SCP's than insects from habitats that offered some protection from ambient temperatures. Thirty-eight species had reports of SCP's for different geographical locations. Although there were occasionally differences in the SCP's, there was no consistent pattern of insects having lower SCP's when overwintering in colder habitats. The incidence of freeze-tolerance was higher in boreal and polar climatic zones than in climatic zones with warmer winters. Holometabola insects had a higher incidence of freeze-tolerance than hemimetabola insects. Suggestions for future research directions are outlined.

Keywords: Winter climates, snow-cover, overwintering, terrestrial insects, winter climatic zones, freeze-tolerance, freeze-susceptibility, non-freezing mortality, supercooling point, coldhardiness

Received: February 11, 2005; Revised: June 14, 2005; Accepted: June 14, 2005; Published: November 3, 2005  Show citation

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TURNOCK, W.J., & FIELDS, P.G. (2005). Winter climates and coldhardiness in terrestrial insects. EJE102(4), 561-576. doi: 10.14411/eje.2005.081
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References

  1. BAILEY W.G., OKE T.R. & ROUSE W.R. 1997: The Surface Climates of Canada. McGill-Queens Univ. Press, Montreal & Kingston, 484 pp Go to original source...
  2. BALE J.S. 1987: Insect cold hardiness: freezing and supercooling - an ecophysiological perspective. J. Insect Physiol. 33: 899-908 Go to original source...
  3. BALE J.S. 1991: Insects at low temperature: a predictable relationship? Func. Ecol. 5: 291-298 Go to original source...
  4. BALE J.S. 1993: Classes of insect coldhardiness. Func. Ecol. 7: 751-753
  5. BALE J.S. 1996: Insect cold hardiness: a matter of life and death. Eur. J. Entomol. 93: 369-382
  6. BALE J.S., HARRINGTON R. & CLOUGH M.S. 1988: Low temperature mortality of the peach-potato aphid Myzus persicae. Ecol. Entomol. 13: 121-129 Go to original source...
  7. BARNES B. & HODSON A.C. 1956: Low temperature tolerance of the European corn borer in relation to winter survival in Minnesota. J. Econ. Entomol. 49: 19-24 Go to original source...
  8. BAUST J.G. & EDWARDS J.S. 1979: Mechanisms of freezing tolerance in an Antarctic midge, Belgica antarctica. Physiol. Entomol. 4: 1-5 Go to original source...
  9. BAUST J.G. & LEE R.E. JR. 1981: Divergent mechanisms of frost-hardiness in two populations of the gall fly, Eurosta solidaginis. J. Insect Physiol. 27: 485-490 Go to original source...
  10. BAUST J.G. & MORRISSEY R.E. 1975: Supercooling phenomenon and water content independence in the overwintering beetle, Coleomegilla maculata. J. Insect Physiol. 21: 1751-1754 Go to original source...
  11. BAUST J.G., GRANDEE R., CONDON G. & MORRISSEY R.C. 1979: The diversity of strategies utilized by separate populations of gall insects. Physiol. Zool. 52: 572-580 Go to original source...
  12. BENNETT L.E. & LEE R.E. JR. 1989: Simulated winter to summer transition in diapausing adults of the lady beetle (Hippodamia convergens): supercooling point is not indicative of coldhardiness. Physiol. Entomol. 14: 361-367 Go to original source...
  13. BIRD J.M. & HODKINSON I.D. 1999: Species at the edge of their range: The significance of the thermal environment for the distribution of congeneric Craspedolepta species (Sternorrhyncha: Psylloidea) living on Chamerion angustifolium (Onagraceae). Eur. J. Entomol. 96: 103-109
  14. BLOCK W. 1982: Supercooling points of insects and mites on the Antarctic Peninsula. Ecol. Entomol. 7: 1-8 Go to original source...
  15. BROWN R.D. 2000: Northern hemisphere snowcover variability and change, 1915-1997. J. Climate 13: 2339-2355 Go to original source...
  16. CASAGRANDE R.A. & HAYNES D.L. 1976: A predictive model for cereal leaf beetle mortality from sub-freezing temperatures. Envir. Entomol. 5: 761-769 Go to original source...
  17. CLOUDSLEY-THOMPSON J.L. 1962: Microclimates and the distribution of terrestrial arthropods. Annu. Rev. Entomol. 7: 199-222 Go to original source...
  18. CLOUDSLEY-THOMPSON J.L. 1970: Terrestrial Invertebrates. In Whittow G.C. (ed.): Comparative Physiology of Thermoregu lation. Vol. I. Academic Press, New York & London, pp. 15-77
  19. DANKS H.V. 1978: Modes of seasonal adaptation in the insects. I. Winter survival. Can. Entomol. 110: 1167-1205 Go to original source...
  20. DANKS H.V. 1996: The wider integration of studies of insect coldhardiness. Eur. J. Entomol. 93: 383-403
  21. DANKS H.V., KUKAL O. & RING R.A. 1994: Insect cold-hardiness: insights from the Arctic. Arctic 47: 391-404 Go to original source...
  22. DENLINGER D.L., LEE R.E. JR., YOCUM G.D. & KUKAL O. 1992: Role of chilling in the acquisition of cold tolerance and the capacitation to express stress proteins in diapausing pharate larvae of the Gypsy Moth, Lymantria dispar. Arch. Insect Biochem. Physiol. 21: 271-280 Go to original source...
  23. DUMAN J.G. 1980: Factors involved in overwintering survival of the freeze tolerant beetle, Dendroides canadensis. J. Comp. Physiol. (B) 136: 53-59 Go to original source...
  24. DUMAN J.G. & MONTGOMERY S.L. 1991: Subzero temperature adaptions in arthropods from the summit of Mauna Kea, Hawaii. J. Exp. Zool. 259: 409-412 Go to original source...
  25. DYE D.G. 2002: Variability and trends in the annual snow-cover cycle in Northern Hemisphere land areas, 1972-2000. Hydrol. Processes 16: 3065-3077 Go to original source...
  26. FIELDS P.G. 1992: The control of stored-product insects and mites with extreme temperatures. J. Stored Prod. Res. 28: 89-118 Go to original source...
  27. FIELDS P.G. & MCNEIL J.N. 1986: Possible dual cold-hardiness strategies in Cisseps fulvicollis (Lepidoptera: Arctiidae). Can. Entomol. 118: 1309-1311 Go to original source...
  28. FIELDS P.G. & MCNEIL J.N. 1988: The cold-hardiness of Ctenucha virginica (Lepidoptera: Arctiidae) larvae, a freezingtolerant species. J. Insect Physiol. 34: 269-277 Go to original source...
  29. FRENCH H.M. & SLAYMAKER O. 1993: Canada's Cold Environments. McGill-Queens Univ. Press, Montreal & Kingston, 340 pp Go to original source...
  30. GEHRKEN U. 1984: Winter survival of an adult bark beetle Ips acuminatus. J. Insect Physiol. 30: 421-429 Go to original source...
  31. GEHRKEN U. 1992: Inoculative freezing and thermal hysteresis in the adult beetles Ips acuminatus and Rhagium inquisitor. J. Insect Physiol. 38: 519-524 Go to original source...
  32. GEHRKEN U. & SOUTHON T.E. 1997: Effect of temperature on coldhardiness and tissue ice formation in the adult Chrysomelid beetle Melasoma collaris L. J. Insect Physiol. 43: 587-593 Go to original source...
  33. GEIGER R. 1950: The Climate near the Ground. Harvard University Press, Cambridge, USA, 482 pp
  34. GREEN G.W. 1962: Low winter temperatures and the European pine shoot moth, Rhyacionia buoliana (Schiff.) in Ontario. Can. Entomol. 94: 314-336 Go to original source...
  35. GRODY N.C. & BASIST A.N. 1996: Global identification of snowcover using SSM/I measurements. Trans. Geosci. Remote Sensing 34(1): 237-249 Go to original source...
  36. GRUBOR-LAJSIC G., BLOCK W., PALANACKI V. & GLUMAC S. 1991: Cold hardiness parameters of overwintering diapause larvae of Ostrinia nubilalis in Vojvodina, Yugoslavia. Cryo-Letters 12: 177-182
  37. HANEC W. & BECK S.D. 1960: Cold hardiness in the European corn borer, Pyrausta nubilalis (Huebn.). J. Insect Physiol. 5: 169-180 Go to original source...
  38. HANSEN T. & MERIVEE E. 1971: Cold hardiness of the cabbage butterflies Pieris brassicae L. and Pieris rapae L. Eesti NSV Tead. Akad. Toim. Biol. 20: 298-303 Go to original source...
  39. HODKOVA M. & HODEK I. 1994: Control of diapause and supercooling by the retrocerebral complex in Pyrrhocoris apterus. Entomol. Exp. Appl. 70: 237-245 Go to original source...
  40. JING X.H. & KANG L. 2003: Geographical variation in egg coldhardiness: a study on the adaptation strategies of the migratory locust, Locusta migratoria L. Ecol. Entomol. 28: 151-158 Go to original source...
  41. JOHNSON S.L. & LEE R.E. JR. 1990: Regulation of supercooling and nucleation in a freeze intolerant beetle (Tenebrio molitor). Cryobiology 27: 562-568 Go to original source...
  42. KALUSHKOV P. & NEDVED O. 2000: Coldhardiness of Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae) from central and southern Europe. Eur. J. Entomol. 97: 149-153 Go to original source...
  43. KING J.C. & TURNER J. 1997: Antarctic Meteorology and Climatology. Cambridge University Press, 425 pp Go to original source...
  44. KLOK C.J. & CHOWN S.L. 1997: Critical thermal limits, temperature tolerance and water balance of a sub-antarctic caterpillar, Pringleophaga marioni (Lepidoptera: Tineidae). J. Insect Physiol 43: 685-694 Go to original source...
  45. KOPPEN W. 1931: Grundriss der Klimakunde. De Gruyter, Berlin, 380 pp Go to original source...
  46. KOPVILLEM H. & KUUSIK A. 1971: On the cold-hardiness of overwintering eggs of the European pine sawfly, Neodiprion sertifer (Geoffr.) and its parasite Achrysocharella ruforum (Krausse). Eesti NSV Tead. Akad. Toim. Biol. 20: 291-297 Go to original source...
  47. KOSTAL V. 1993: Cold-hardiness and supercooling capacity in diapausing and nondiapausing stages of the cabbage root fly Delia radicum. Cryobiology 30: 524-531 Go to original source...
  48. LAMB R.J., TURNOCK W.J. & HAYHOE H.N. 1985: Winter survival and outbreaks of Bertha armyworm, Mamestra configurata (Lepidoptera: Noctuidae), on canola. Can. Entomol. 117: 727-736 Go to original source...
  49. LARSEN K.H., LEE R.E. JR. & NAULT L.R. 1993: Influence of developmental conditions on coldhardiness of adult Dalbulus leafhoppers: implications for overwintering. Entomol. Exp. Appl. 67: 99-108 Go to original source...
  50. LEE R.E. JR. 1980: Physiological adaptations of Coccinellidae to supranivean and subnivean hibernacula. J. Insect Physiol. 26: 138-138 Go to original source...
  51. LEE R.E. JR. 1989: Insect cold-hardiness: to freeze or not to freeze. Bioscience 39: 308-313 Go to original source...
  52. LOZINA-LOZINSKII L.K. 1974: Studies in Cryo-Biology. John Wiley, New York, 259 pp
  53. MACPHEE A.W. 1964: Cold-hardiness, habitat, and winter survival of some orchard arthropods in Nova Scotia. Can. Entomol. 96: 617-625 Go to original source...
  54. MADRID F.J. & STEWART R.K. 1981: Ecological significance of coldhardiness and winter mortality of eggs of the Gypsy Moth Lymantria dispar L., in Quebec. Envir. Entomol. 10: 586-589 Go to original source...
  55. MERIVEE E. 1978: Cold-Hardiness in Insects. Acad. Sci. Estonian SSR, Tallin, 188 pp. (in Estonian, English abstr.)
  56. MILLER L.K. 1969: Freezing tolerance in an adult insect. Science 166: 105-106 Go to original source...
  57. MILLER L.K. 1982: Coldhardiness strategies of some adult and immature insects overwintering in Interior Alaska. Comp. Biochem. Physiol. (A) 73: 595-604 Go to original source...
  58. NEDVED O. 1993: Comparison of coldhardiness in two ladybird beetles (Coleoptera: Coccinellidae) with contrasting hibernation behavior. Eur. J. Entomol. 90: 465-470
  59. NEDVED O. 1998: Modelling the relationship between cold injury and accumulated degree days in terrestrial arthropods. CryoLetters 19: 267-274
  60. NEDVED O. 2000a: Chill tolerance in the tropical beetle Stenotarsus rotundus. Cryo-Letters 21: 25-30
  61. NEDVED O. 2000b: Snow White and the seven dwarfs: a multivariate approach to classification of cold tolerance. CryoLetters 21: 339-0348.
  62. NEDVED O., LAVY D. & VERHOEF H.A. 1998: Modelling the timetemperature relationship in cold injury and effect of hightemperature interruptions on survival in a chill-sensitive collembolan. Func. Ecol. 12: 816-824 Go to original source...
  63. O'DOHERTY R. & BALE J.S. 1985: Factors affecting coldhardiness of the peach-potato aphid Myzus persicae. Ann. Appl. Biol. 106: 219-228 Go to original source...
  64. OHYAMA Y. & ASAHINA E. 1972: Frost resistance in adult insects. J. Insect Physiol. 18: 267-282 Go to original source...
  65. OKE T.R. 1987: Boundary Layer Climates. 2nd ed. Methuen, London, 435 pp
  66. OLSEN T.M. & DUMAN J.G. 1997: Maintenance of the supercooled state in the gut fluid of overwintering pyrochroid beetle larvae, Dendroides canadensis: role of ice nucleators and antifreeze proteins. J. Comp. Physiol. (B) 167: 114-127 Go to original source...
  67. PANTYUKHOV G.A. 1964: The effect of low temperatures on different populations of the Brown-tail Moth Euproctis chrysorrhoea (L.) and the Gypsy Moth Lymantrria dispar (L.) (Lepidoptera: Orgyidae). Entomol. Rev. 43: 47-65
  68. PANTYUKHOV G.A. 1971: Coldhardiness in some species of Coccinellidae. In Maavara V. (ed.): Coldhardiness in Insects and Mites. Abstracts from a Symposium Held in Tartu (Estonian SSR) April 19 to 21, 1971. Academy of Sciences of the Estonian SSR, Tartu, pp. 103-108 (in Russian)
  69. PULLIN A.S. & BALE J.S. 1989: Influence of diapause and temperature on cryoprotectant synthesis and coldhardiness in pupae of Pieris brassicae. Comp. Biochem. Physiol. (A) 94: 499-503 Go to original source...
  70. PULLIN A.S., BALE J.S. & FONTAINE X.L.R. 1991: Physiological aspects of diapause and cold tolerance during overwintering in Pieris brassicae. Physiol. Entomol. 16: 447-556 Go to original source...
  71. RAMLOV H. 1999: Microclimate and variations in haemolymph composition in the freezing-tolerant New Zealand alpine weta Heimideina maori Hutton (Orthoptera: Stenopelmatidae). J. Comp. Physiol. (B) 169: 224-235 Go to original source...
  72. RAMLOV H. 2000: Aspects of natural cold tolerance in ectothermic animals. Human Reprod. 15 (Suppl. 5): 26-46 Go to original source...
  73. RENAULT D., SALIN C., VANNIER G. & VERNON P. 2002: Survival at low temperatures in insects: what is the significance of the supercooling point. Cryo-Letters 23: 217-228
  74. RICKARDS J., KELLEHER R.J. & STOREY K.B. 1987: Strategies of freeze avoidance in larvae of the goldenrod gall moth Epiblemma scudderiana: winter profiles of a natural population. J. Insect Physiol. 33: 443-450 Go to original source...
  75. RING R.A. 1982: Freezing-tolerant insects with low supercooling points. Comp. Biochem. Physiol. (A) 73: 605-612 Go to original source...
  76. RING R.A. & TESAR D. 1980: Coldhardiness of the Arctic beetle Pytho americanus Kirby, Coleoptera, Pythidae (Salpingidae). J. Insect Physiol. 26: 763-774 Go to original source...
  77. ROBERTS S.J., ARMBRUST E.J. & SELL D.K. 1972: Supercooling points of several species of Lepidoptera found on soybeans. Envir. Entomol. 1: 671-672 Go to original source...
  78. SAKAGAMI S.F., TANNO K., TSUTSUI H. & HONMA K. 1985: The role of cocoons in overwintering of the Soybean Pod Borer Leguminivora glycinivorella (Lepidoptera: Tortricidae). J. Kans. Entomol. Soc. 58: 240-247
  79. SALT R.W. 1959: Role of glycerol in the cold-hardening of Bracon cephi (Gahan). Can. J. Zool. 37: 59-69 Go to original source...
  80. SATVELD O. 1975: Overvintringsbiologien tilden skarptannete barkbillen Ips acuminatus Gyll. (Coleoptera: Scolytidae) med saerlig vekt pa kuldetoleranse . University of Oslo, 112 pp
  81. SHEL'DESHOVA G.G. 1967: Ecological factors determining distribution of the Codling Moth Laspeyresia pomonella L. (Lepidoptera, Tortricidae) in the northern and southern hemispheres. Entomol. Rev. 46: 349-360
  82. SHIMADA K., SAKAGAMI S.F., HONMA K. & TSUTSUI H. 1984: Seasonal changes of glycogen/trehalose contents, supercooling points, and survival rate in mature larvae of the overwintering Soybean Pod Borer Leguminivora glycinivorella. J. Insect Physiol. 30: 369-373 Go to original source...
  83. SHINTANI Y. & ISHIKAWA Y. 1999: Geographic variation in coldhardiness of eggs and neonate larvae of the yellow-spotted longicorn beetle, Psacothea hilaris. Physiol. Entomol. 24: 158-164 Go to original source...
  84. SINCLAIR B.J. 1999: Insect cold tolerance: How many kinds of frozen? Eur. J. Entomol. 96: 157-164
  85. SINCLAIR B.J. 2001: Field ecology of cold tolerance: interannual variation in cooling rates, freeze-thaw and thermal stress in the microhabitat of the alpine cockroach Celatoblatta quinquemaculata. Oikos 93: 286-293 Go to original source...
  86. SINCLAIR B.J., ADDO-BEDIAKO A., CHOWN S.L. 2003: Climatic variability and the evolution of insect freeze tolerance. Biol. Rev. 78: 181-195 Go to original source...
  87. SOMME L. 1964: Effects of glycerol on cold-hardiness in insects. Can. J. Zool. 42: 87-101 Go to original source...
  88. SOMME L. 1965: Further observations on glycerol and coldhardiness in insects. Can. J. Zool. 43: 765-770 Go to original source...
  89. SOMME L. 1967: The effect of temperature and anoxia on haemolymph composition and supercooling in three overwintering insects. J. Insect Physiol. 13: 805-814 Go to original source...
  90. SOMME L. 1978: Nucleating agents in the haemolymph of third instar larvae of Eurosta solidaginis (Fitch) (Dipt., Tephritidae). Norw. J. Entomol. 25: 187-188
  91. SOMME L. 1982: Supercooling and winter survival in terrestrial arthropods. Comp. Biochem. Physiol. (A) 73: 519-543 Go to original source...
  92. SOMME L. 1999: The physiology of cold hardiness in terrestrial arthropods. Eur. J. Entomol. 96: 1-10
  93. SOMME L. & ZACHARIASSEN K.E. 1981: Adaptations to low temperatures in high altitude insects from Mount Kenya. Ecol. Entomol. 6: 199-204 Go to original source...
  94. STOREY K.B. & STOREY J.M. 1987: Freeze tolerance: constraining forces, adaptive mechanisms. Can. J. Zool. 66: 1122-1127 Go to original source...
  95. SULLIVAN C.R. 1965: Laboratory and field investigations on the ability of eggs of the European pine sawfly, Neodiprion sertifer (Geoffroy) to withstand low temperatures. Can. Entomol. 97: 978-993 Go to original source...
  96. SULLIVAN C.R. & WALLACE D.R. 1972: The potential northern dispersal of the Gypsy Moth, Porthetria dispar (Lepidoptera: Lymantriidae). Can. Entomol. 104: 1349-1345 Go to original source...
  97. TAUBER M.J., TAUBER C.A. & MASAKI S. 1986: Seasonal Adaptations of Insects. Oxford University Press, New York, 411 pp
  98. TENOW O. & NILSSEN A. 1990: Egg cold hardiness and topoclimatic limitations to outbreaks of Epirrita autumnata in northern Fennoscandia. J. Appl. Ecol. 27: 723-734 Go to original source...
  99. TREWARTHA G.T. & HORN L.H. 1980: An Introduction to Climate. McGraw-Hill, New York, 416 pp
  100. TRUCHAN J. & BUTCHER J.W. 1970: Coldhardiness of Dendrosoter protuberans. J. Econ. Entomol. 63: 328-330 Go to original source...
  101. TSUTSUI H., TANNO K. & TORIKURA H. 1987: Coldhardiness of overwintering eggs in Celaena leucostigma and Amphipoea fucosa (Lepidoptera: Noctuidae). Jap. J. Appl. Entomol. Zool. 31: 261-263 Go to original source...
  102. TURNOCK W.J. 1993: Cold-hardiness of Lacanobia atlantica (Lepidoptera: Noctuidae), and a comparison with three other insect species that overwinter in the same habitat. Can. J. Zool. 71: 1710-1714 Go to original source...
  103. TURNOCK W.J. & BILODEAU R.J. 1992: Life history and coldhardiness of Athrycia cinerea (Dipt.: Tachinidae) in western Canada. Entomophaga 37: 353-362. Go to original source...
  104. TURNOCK W.J. & BODNARYK R.P. 1991: Latent cold injury and its conditional expression in the Bertha armyworm, Mamestra configurata (Noctuidae: Lepidoptera). Cryo-Letters 12: 377-384
  105. TURNOCK W.J. & BODNARYK R.P. 1993: The reversal of cold injury and its effect on the response to subsequent cold exposures. Cryo-Letters 14: 251-256
  106. TURNOCK W.J. & CARL K.P. 1995: Evaluation of the Palaearctic Eurithia consobrina (Diptera: Tachinidae) as a potential biocontrol agent for Mamestra configurata (Lepidoptera: Noctuidae) in Canada. Biocontrol Sci. Technol. 5: 55-67 Go to original source...
  107. TURNOCK W.J., LAMB R.J. & BODNARYK R.P. 1983: Effects of cold stress during diapause on the survival and development of Mamestra configurata (Lepidoptera: Noctuidae). Oecologia 56: 185-192 Go to original source...
  108. TURNOCK W.J., JONES T.H. & READER P.M. 1985: Effects of cold stress during diapause on the survival and development of Delia radicum (Diptera; Anthomyiidae) in England. Oecologia 67: 506-510 Go to original source...
  109. TURNOCK W.J., READER P.M. & BRACKEN G.K. 1990: A comparison of the coldhardiness of populations of Delia radicum (L.) (Diptera: Anthomyiidae) from southern England and the Canadian prairies. Can. J. Zool. 68: 830-835 Go to original source...
  110. TURNOCK W.J., BOIVIN G. & RING R.A. 1998: Interpopulation differences in the coldhardiness of Delia radicum (Diptera: Anthomyiidae). Can. Entomol. 130: 119-129 Go to original source...
  111. VAN DER LAAK S. 1982: Physiological adaptations to low temperature in freezing-tolerant Phyllodecta laticollis beetles. Comp. Biochem. Physiol. (A) 73: 613-620 Go to original source...
  112. VAN DER WOUDE & VERHOEF H.A. 1986: A comparative study of winter survival in two temperate Collembola. Ecol. Entomol. 11: 333-340 Go to original source...
  113. VERNON P., VANNIER G. & LUCE J.-M. 1996: Decouverte de larves tolerantes et intolerantes L la congelation dans une meme guilde de Cetoines (Coleopteres) en foret de Fountainebleau. Ecologie 27: 131-142
  114. WERNER R.A. 1978: Overwinter survival of spear-marked black moth, Pheumaptera hastata (Lepidoptera: Geometridae), pupae in interior Alaska. Can. Entomol. 110: 877-882 Go to original source...
  115. ZACHARIASSEN K.E. 1977: Effects of glycerol in freeze-tolerant Pytho depressus L. (Col., Pythidae). Norw. J. Entomol. 24: 25-29
  116. ZACHARIASSEN K.E. 1980: The role of polyols and nucleating agents in cold-hardy beetles. J. Comp. Physiol. 140: 227-234 Go to original source...
  117. ZACHARIASSEN K.E. & HAMMEL H.T. 1976: Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262: 285-287 Go to original source...

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