Eur. J. Entomol. 101 (3): 445-458, 2004 | DOI: 10.14411/eje.2004.064

Photoperiod, diapause and cold-hardiness

Magdalena HODKOVA, Ivo HODEK
Institute of Entomology, Academy of Sciences, Ceske Budejovice, CZ-370 05 Czech Republic; e-mail: hodkova@entu.cas.cz

Great progress has recently been made in cryobiology. One field, however, has been neglected: the temporal sequence of the effects of photoperiod and temperature, and their relative importance in cold hardening. This is relevant to the question of importance of diapause in cold-hardiness. Denlinger (1991) outlined the categories of such relations and stressed a great need for further detailed research. A survey of studies done over the past decade revealed many gaps in the evidence and the ambiguous nature of the data on the photoperiodic regulation of cold-hardiness. We hope that this review will stimulate further research in this field. Among several directions where research is most needed we have stressed (1) simultaneous recording of changes in survival and dynamics of suspected cryoprotectants (stressed also by Danks, 1996), (2) checking the regulation of different phases of cold hardening, and (3) discrimination between direct and indirect (mediated via neuroendocrine system) effects of environmental cues on cold hardening.

Keywords: Photoperiod, temperature, diapause, cold-hardiness, hormones, survival, supercooling, cryoprotectants, Pyrrhocoris apterus

Received: January 9, 2004; Revised: April 20, 2004; Accepted: May 10, 2004; Published: September 20, 2004  Show citation

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HODKOVA, M., & HODEK, I. (2004). Photoperiod, diapause and cold-hardiness. EJE, 101(3), 445-458. doi: 10.14411/eje.2004.064
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    References

    1. Anchordoguy T.J., Rudolph A.S., Carpenter J.F. & Crowe J.H. 1988: Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 24: 324-331 Go to original source...
    2. Ansart A., Vernon P. & Daguzan J. 2001: Photoperiod is the main cue that triggers supercooling ability in the land snail, Helix aspersa (Gastropoda: Helicidae). Cryobiology 42: 266-273 Go to original source...
    3. Ansart A. & Vernon P. 2003: Cold hardiness in molluscs. Acta Oecol. 24: 95-102 Go to original source...
    4. Bale J.S. 1996: Insect cold hardiness: A matter of life and death. Eur. J. Entomol. 93: 369-382
    5. Bale J.S. 2002: Insects and low temperatures: from molecular biology to distributions and abundance. Phil. Trans. R. Soc. Lond. (B) 357: 849-862 Go to original source...
    6. Broufas G.D. & Koveos D.S. 2001: Cold hardiness characteristics in a strain of the predatory mite Euseius (Amblyseius) finlandicus (Acari: Phytoseidae) from northern Greece. Ann. Entomol. Soc. Am. 94: 82-90 Go to original source...
    7. Carpenter J.F. & Crowe J.H. 1988: The mechanism of cryoprotection of proteins by solutes. Cryobiology 25: 244-255 Go to original source...
    8. Chippendale G.M. 1977: Hormonal regulation of larval diapause. Annu. Rev. Entomol. 22: 121-138 Go to original source...
    9. Danks H.V. 1978: Modes of seasonal adaptation in the insects I. Winter survival. Can. Entomol. 110: 1167-1205 Go to original source...
    10. Danks H.V. 1987: Insect Dormancy: an Ecological Perspective. Biol. Survey Canada, Ottawa, 439 pp
    11. Danks H.V. 1996: The wider integration of studies on insect cold-hardiness. Eur. J. Entomol. 93: 383-403
    12. Danks H.V. 2000: Insect cold hardiness: a Canadian perspective. CryoLetters 21: 297-308
    13. Denlinger D.L. 1991: Relationship between cold hardiness and diapause. In Lee Jr. R.E. & Denlinger D.L. (eds): Insects at Low Temperature. Chapman & Hall, New York, pp. 174-198 Go to original source...
    14. Denlinger D.L. 2002: Regulation of diapause. Annu. Rev. Entomol. 47: 93-122 Go to original source...
    15. Drobnis E.Z., Crowe L.M., Berger T., Anchordoguy T.J., Overstreet J.W. & Crowe J.H. 1993: Cold shock damage is due to lipid phase transition in cell membranes: A demonstration using sperm as model. J. Exper. Zool. 265: 432-437 Go to original source...
    16. Goto S.G. & Kimura M.T. 1998: Heat- and cold-shock responses and temperature adaptation in subtropical and temperate species of Drosophila. J. Insect Physiol. 44: 1233-1239 Go to original source...
    17. Goto S.G. & Kimura M.T. 2004: Heat-shock-responsive genes are not involved in the adult diapause of Drosophila triauraria. Gene 326: 117-122 Go to original source...
    18. Goto M., Takahashi K. & Suzuki C. 1993a: Ecological study on the barnyard grass stem borer, Enosima leucotaeniella (Lepidoptera: Pyralidae) VIII. Seasonal changes of carbohydrate contents in overwintering larvae. Appl. Entomol. Zool. 28: 417-421 Go to original source...
    19. Goto M., Takahashi K. & Suzuki C. 1993b: Ecological study on the barnyard grass stem borer, Enosima leucotaeniella (Lepidoptera: Pyralidae) IX. Effect of temperature on carbohydrate contents in diapausing and early post-diapausing larvae. Appl. Entomol. Zool. 28: 433-437 Go to original source...
    20. Goto S.G., Yoshida K.M. & Kimura M.T. 1998: Accumulation of Hsp 70 mRNA under environmental stresses in diapausing and nondiapausing adults of Drosophila triauraria. J. Insect Physiol. 44: 1009-1015 Go to original source...
    21. Hamilton M.D., Rojas R.R. & Baust J.G. 1986: Juvenile hormone: Modulation of cryoprotectant synthesis in Eurosta solidaginis by a component of the endocrine system. J. Insect Physiol. 32: 971-979 Go to original source...
    22. Hanc Z. & Nedved O. 1999: Chill injury at alternating temperatures in Orchesella cincta (Collembola: Entomobryidae) and Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). Eur. J. Entomol. 96: 165-168
    23. Hart A.J. & Bale J.S. 1998: Factors affecting the freeze tolerance of the hoverfly Syrphus ribesii (Diptera: Syrphidae). J. Insect Physiol. 44: 21-29 Go to original source...
    24. Hazel J.R. 1997: Thermal adaptations in biological membranes: Beyond homeoviscous adaptation. In Bittar E.E. & Willis J.S. (eds): Advances in Molecular and Cell Biology: Thermobiology. Vol. 19. Jai Press, London, pp. 57-101 Go to original source...
    25. 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...
    26. Hodkova M. & Hodek I. 1997: Temperature regulation of supercooling and gut nucleation in relation to diapause of Pyrrhocoris apterus (Heteroptera). Cryobiology 34: 70-79 Go to original source...
    27. Hodkova M., Berkova P. & Zahradnickova H. 2002: Photoperiodic regulation of the phospholipid molecular species composition in thoracic muscles and fat body of Pyrrhocoris apterus (Heteroptera) via an endocrine gland, corpus allatum. J. Insect Physiol. 48: 1009-1019 Go to original source...
    28. Hodkova M., Simek P., Zahradnickova H. & Novakova O. 1999: Seasonal changes in the phospholipid composition in thoracic muscles of a heteropteran, Pyrrhocoris apterus. Insect Biochem. Molec. Biol. 29: 367-376 Go to original source...
    29. Hodkova M., Somme L., Hanzal R., Brunnhofer V. & Hodek I. 1992: The effect of allatectomy and photoperiod on the supercooling point in Pyrrhocoris apterus adults. Physiol. Entomol. 17: 165-168 Go to original source...
    30. Hoffmann A.A., Sorensen J.G. & Loeschke V. 2003: Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J. Therm. Biol. 28: 175-216 Go to original source...
    31. Horwath K.L. & Duman J.G. 1983: Preparatory adaptations for winter survival in the cold hardy beetles, Dendroides canadensis and D. concolor. J. Comp. Physiol. 151: 225-232 Go to original source...
    32. Ito K. & Nakata T. 1998: Diapause and survival in winter in two species of predatory bugs, Orius sauteri and O. minutus. Entomol. Exp. Appl. 89: 271-276 Go to original source...
    33. Kimura M.T., Awasaki T., Ohtsu T. & Shimada K. 1992: Seasonal changes in glycogen and trehalose content in relation to winter survival of four temperate species of Drosophila. J. Insect Physiol. 38: 871-875 Go to original source...
    34. Kostal V. & Simek P. 2000: Overwintering strategy in Pyrrhocoris apterus (Heteroptera): the relations between life-cycle, chill tolerance and physiological adjustments. J. Insect Physiol. 46: 1321-1329 Go to original source...
    35. Kostal V. & Slachta M. 2001: Variation in cold hardiness during overwintering in Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). Acta Soc. Zool. Bohem. 65: 239-245
    36. Kostal V., Slachta M. & Simek P. 2001: Cryoprotective role of polyols independent of the increase in supercooling capacity in diapausing adults of Pyrrhocoris apterus (Heteroptera). Comp. Bioch. Physiol. (B) 130: 365-374 Go to original source...
    37. Kostal V., Berkova P. & Simek P. 2003: Remodelling of membrane phospholipids during transition to diapause and cold-acclimation in the larvae of Chymomyza costata (Drosophilidae). Comp. Bioch. Physiol. (B) 135: 407-419 Go to original source...
    38. Langer A. & Hance T. 2000: Overwintering strategies and cold hardiness of two aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae). J. Insect Physiol. 46: 671-676 Go to original source...
    39. Lee R.E. Jr., Chen C.-P., Meacham M.H. & Denlinger D.L. 1987: Ontogenetic patterns of cold-hardiness and glycerol production in Sarcophaga crassipalpis. J. Insect Physiol. 33: 587-592 Go to original source...
    40. Lee R.E. Jr., Denlinger D.L. & Chen C.P. 1988: Insect cold-hardiness and diapause: Regulatory relationships. In Sehnal F., Zabza A. & Denlinger D.L. (eds): Endocrinological Frontiers in Insect Ecology. Wroclaw Tech. Univ., Wroclaw, pp. 243-262
    41. Lefevere K.S., Koopmanschap A.B. & De Kort C.A.D. 1989: Changes in the concentrations of metabolites in haemolymph during and after diapause in female Colorado potato beetle, Leptinotarsa decemlineata. J. Insect Physiol. 35: 121-128 Go to original source...
    42. Leopold R.A. 1991: Cryopreservation of insect germplasm: cells, tissues and organisms. In Lee Jr.R.E. & Denlinger D.L. (eds): Insects at Low Temperature. Chapman & Hall, New York, pp. 174-198 Go to original source...
    43. Lewis R.N.A.H., Mannock D.A., McElhaney R.N., Turne D.C. & Gruner S.M. 1989: Effect of fatty acyl chain length and structure on the lamellar gel to liquid-crystalline and lamellar to reverse hexagonal phase transition of aqueous phosphatidyletanolamine dispersions. Biochemistry 28: 541-548 Go to original source...
    44. Merivee E. 1978: Cold-Hardiness in Insects. Acad. Sci. Estonian SSR. Tallin, 178 pp. (In Estonian, with 23 pp. of English summary.) Milonas P.G. & Savopoulou-Soultani M. 1999: Cold hardiness in diapause and non-diapause larvae of the summer fruit tortrix, Adoxophyes orana (Lepidoptera: Tortricidae). Eur. J. Entomol. 96: 183-187
    45. Moreau R., Oliver D., Gordoux L. & Dutrieu J. 1981: Carbohydrate metabolism in Pieris brassicae L. (Lepidoptera: variations during normal and diapausing development. Comp. Biochem. Physiol. (B) 68: 95-99 Go to original source...
    46. Nedved O., Hodkova M., Brunnhofer V. & Hodek I. 1995: Simultaneous measurement of low temperature survival and supercooling in a sample of insects. Cryo-Letters 7: 108-112
    47. Nedved O. & Windsor D. 1994: Supercooling ability, fat and water contents in a diapausing tropical beetle, Stenotarsus rotundus (Coleoptera: Endomychidae). Eur. J. Entomol. 91: 307-312
    48. Nomura M. & Ishikawa Y. 2001: Dynamic changes in cold hardiness, high temperature tolerance and trehalose content in the onion maggot, Delia antiqua (Diptera: Anthomyiidae), associated with the summer and winter diapause. Appl. Entomol. Zool. 36: 443-449 Go to original source...
    49. Ohtsu T., Kimura M.T. & Hori S.H. 1995: The influence of eclosion timing on winter survival and triacylglycerol accumulation in four temperate species of Drosophila. Physiol. Entomol. 20: 248-252 Go to original source...
    50. Ohtsu T., Kimura M.T. & Katagiri C. 1998: How Drosophila species acquire cold tolerance: Qualitative change of phospholipids. Eur. J. Biochem. 252: 608-611 Go to original source...
    51. Pullin A.S. 1992: Diapause metabolism and changes in carbohydrates related to cryoprotection in Pieris brassicae. J. Insect Physiol. 38: 319-327 Go to original source...
    52. Pullin A.S. & Bale J.S. 1989a: Effects of ecdysone, juvenile hormone and haemolymph transfer on cryoprotectant metabolism in diapausing and non-diapausing pupae of Pieris brassicae. J. Insect Physiol. 35: 911-918 Go to original source...
    53. Pullin A.S. & Bale J.S. 1989b: Influence of diapause and temperature on cryoprotectant synthesis and cold hardiness in pupae of Pieris brassicae. Comp. Biochem. Physiol. (A) 94: 499-503 Go to original source...
    54. 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: 447-456 Go to original source...
    55. Pullin A.S. & Wolda H. 1993: Glycerol and glucose accumulation during diapause in a tropical beetle. Physiol. Entomol. 18: 75-78 Go to original source...
    56. Raabe M. 1982: Insect Neurohormones. Plenum, New York & London, 352 pp Go to original source...
    57. Ring R.A. & Danks H.V. 1994: Desiccation and cryoprotection: overlapping adaptations. Cryo-Letters 15: 181-190
    58. Ring R.A. & Danks H.V. 1998: The role of trehalose in cold-hardiness and desiccation. Cryo-Letters 19: 275-282
    59. Ring R.A. & Riegert P.W. 1991: Tribute to R.W. Salt. In Lee Jr. R.E. & Denlinger D.L. (eds): Insects at Low Temperature. Chapman & Hall, New York, pp. 3-16 Go to original source...
    60. Rojas R.R., Hamilton M.D. & Baust J.G. 1987: Juvenile hormone modulation of insect cold hardening: Ice nucleating activity. Cryobiology 24: 465-472 Go to original source...
    61. Rojas R.R., Charlet L.D. & Leopold R.A. 1994: Biochemistry and physiology of overwintering in the mature larva of the sunflower stem weevil, Cylindrocopturus adspersus (Coleoptera: Curculionidae) in the Northern Great Plains. J. Insect Physiol. 40: 201-205 Go to original source...
    62. Saunders D.S. & Hayward S.A.L. 1998: Geographical and diapause-related cold tolerance in the blow fly, Calliphora vicina. J. Insect Physiol. 44: 541-551 Go to original source...
    63. Shimada K. & Riihimaya A. 1990: Cold-induced freezing tolerance in diapausing and non-diapausing larvae of Chymomyza costata (Diptera: Drosophilidae) with accumulation of trehalose and proline. Cryo-Letters 11: 243-250
    64. Slachta M., Berkova P., Vambera J. & Kostal V. 2002a: Physiology of cold-acclimation in non-diapausing adults of Pyrrhocoris apterus (Heteroptera). Eur. J. Entomol. 99: 181-187 Go to original source...
    65. Slachta M., Vambera J., Zahradnickova H. & Kostal V. 2002b: Entering diapause is a prerequisite for successful cold-acclimation in adult Graphosoma lineatum (Heteroptera: Pentatomidae). J. Insect Physiol. 48: 1031-1039 Go to original source...
    66. Tanaka K. 1995: Seasonal change in glycogen and inositol/sorbitol contents of the house spider, Achaearanea tepidariorum (Araneae: Theridiidae). Comp. Biochem. Physiol. (B) 110: 539-545 Go to original source...
    67. Tanaka K. 1996: Seasonal and latitudinal variation in supercooling ability of the house spider, Achaearanea tepidariorum (Araneae: Theridiidae). Func. Ecol. 10: 185-192 Go to original source...
    68. Tanaka S. 2000: The role of moisture in the control of diapause, mating and aggregation in a tropical insect. Entomol. Sci. 3: 147-155
    69. Tsumuki H. & Hirai M. 1999: Effects of JH and ecdysone on endogenous ice nucleus production in larvae of the rice stem borer, Chilo suppressalis (Lepidoptera: Pyralidae). Appl. Entomol. Zool. 34: 119-121 Go to original source...
    70. Tsumuki H. & Kanehisa K. 1980: Effect of low temperature on glycerol and trehalose concentration in haemolymph of the rice stem borer, Chilo suppressalis (Lepidoptera: Pyralidae). Jap. J. Appl. Entomol. Zool. 24: 189-193 Go to original source...
    71. Tsumuki H. & Kanehisa K. 1981: Effect of JH and ecdysone on glycerol and carbohydrate contents in diapausing larvae of the rice stem borer, Chilo suppressalis (Lepidoptera: Pyralidae). Appl. Entomol. Zool. 16: 7-15 Go to original source...
    72. Watanabe M. & Tanaka K. 1997: Photoperiodic control of adult diapause, cold hardiness and inositol accumulation in a beetle, Aulacophora nigripennis (Coleoptera: Chrysomelidae). Zool. Sci. 14: 233-237 Go to original source...
    73. Watanabe M. & Tanaka K. 1998a: Adult diapause and cold hardiness in Aulacophora nigripennis (Coleoptera: Chrysomelidae). J. Insect Physiol. 44: 1103-1110 Go to original source...
    74. Watanabe M. & Tanaka K. 1998b: Effect of juvenile hormone analogs on diapause termination and myo-inositol content in Aulacophora nigripennis adults (Coleoptera: Chrysomelidae). Appl. Entomol. Zool. 33: 259-262 Go to original source...
    75. Watanabe M. & Tanaka K. 1999a: Cold tolerance strategy of the freeze-intolerant chrysomelid, Aulacophora nigripennis (Coleoptera: Chrysomelidae), in warm temperate regions. Eur. J. Entomol. 96: 175-181
    76. Watanabe M. & Tanaka K. 1999b: Seasonal change of the thermal response in relation to myo-inositol metabolism in adults of Aulacophora nigripennis (Coleoptera: Chrysomelidae). J. Insect Physiol. 45: 167-172 Go to original source...
    77. Watanabe M. & Tanaka K. 2000: Hormonal control of diapause and overwintering traits in a leaf beetle, Aulacophora nigripennis. Physiol. Entomol. 25: 337-345 Go to original source...
    78. Xu L. & Duman J.G. 1991: Involvement of juvenile hormone in the induction of antifreeze protein production by the fat body of larvae of the beetle Dendroides canadensis. J. Exper. Zool. 258: 288-293 Go to original source...
    79. Xu L., Neven L.G. & Duman J.G. 1990: Hormonal control of hemolymph lipoprotein ice nucleators in overwintering freeze-susceptible larvae of the stag beetle Ceruchus piceus: adipokinetic hormone and juvenile hormone. J. Comp. Physiol. (B) 160: 51-59 Go to original source...
    80. Xu L., Duman J.G., Wu D.W. & Goodman W.G. 1992: A role for juvenile hormone in the induction of antifreeze protein production by the fat body in the beetle Tenebrio molitor. Comp. Biochem. Physiol. (B) 101: 105-109 Go to original source...
    81. Zachariassen K.E. 1985: Physiology of cold tolerance in insects. Physiol. Rev. 65: 799-832 Go to original source...
    82. Zachariassen K.E. & Lundheim R. 1992: The endocrine control of insect cold hardiness. Zool. Jb. Physiol. 96: 183-196

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