Photoperiod, diapause and cold-hardiness

European Journal of Entomology

Volumn 101, Issue 3, 2004, Pages 445-458

  Hodkova, Magdalena ^a   Hodek, Ivo ^a  

^a INSTITUTE OF ENTOMOLOGY   (Czech Republic)

Author keywords

Cold hardiness; Cryoprotectants; Diapause; Hormones; Photoperiod; Pyrrhocoris apterus; Supercooling; Survival; Temperature

Indexed keywords

COLD TOLERANCE; CRYOBIOLOGY; DIAPAUSE; ENVIRONMENTAL CUE; PHOTOPERIOD; SURVIVAL;

HETEROPTERA; PYRRHOCORIDAE; PYRRHOCORIS APTERUS;

EID: 5644295743     PISSN: 12105759     EISSN: 18028829     Source Type: Journal    
DOI: 10.14411/eje.2004.064     Document Type: Article

References (83)

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.
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.
3. ANSART A. & VERNON P. 2003: Cold hardiness in molluscs. Acta Oecol. 24: 95-102.
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.
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.
7. CARPENTER J.F. & CROWE J.H. 1988: The mechanism of cryoprotection of proteins by solutes. Cryobiology 25: 244-255.
8. CHIPPENDALE G.M. 1977: Hormonal regulation of larval diapause. Annu. Rev. Entomol. 22: 121-138.
9. DANKS H.V. 1978: Modes of seasonal adaptation in the insects I. Winter survival. Can. Entomol. 110: 1167-1205.
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.
14. DENLINGER D.L. 2002: Regulation of diapause. Annu. Rev. Entomol. 47: 93-122.
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.
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.
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.
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.
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.
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.
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.
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.
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.
25. HODKOVA M. & HODEK I. 1994: Control of diapause and supercooling by the retrocerebral complex in Pyrrhocoris apterus. Entomol. Exp. Appl. 70: 237-245.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
40. LEE R.E. JR., DENLINGER D.L. & CHEN C.P. 1988: Insect coldhardiness 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.
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.
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.
44. MERIVEE E. 1978: Cold-Hardiness in Insects. Acad. Sci. Estonian SSR. Tallin, 178 pp. (In Estonian, with 23 pp. of English summary.)
45. 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. 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.
51. OHTSU T., KIMURA M.T. & KATAGIRI C. 1998: How Drosophila species acquire cold tolerance: Qualitative change of phospholipids. Eur. J. Biochem. 252: 608-611.
52. PULLIN A.S. 1992: Diapause metabolism and changes in carbohydrates related to cryoprotection in Pieris brassicae. J. Insect Physiol. 38: 319-327.
53. 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.
54. 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.
55. 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.
56. PULLIN A.S. & WOLDA H. 1993: Glycerol and glucose accumulation during diapause in a tropical beetle. Physiol. Entomol. 18: 75-78.
57. RAABE M. 1982: Insect Neurohormones. Plenum, New York & London, 352 pp.
58. RING R.A. & DANKS H.V. 1994: Desiccation and cryoprotection: overlapping adaptations. Cryo-Letters 15: 181-190.
59. RING R.A. & DANKS H.V. 1998: The role of trehalose in coldhardiness and desiccation. Cryo-Letters 19: 275-282.
60. 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.
61. ROJAS R.R., HAMILTON M.D. & BAUST J.G. 1987: Juvenile hormone modulation of insect cold hardening: Ice nucleating activity. Cryobiology 24: 465-472.
62. 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.
63. 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.
64. 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.
65. 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.
66. SLACHTA M., VAMBERA J., ZAHRADNICKOVA H. & KOSTAL V. 2002b: Entering diapause is a prerequisite for successful coldacclimation in adult Graphosoma lineatum (Heteroptera: Pentatomidae). J. Insect Physiol. 48: 1031-1039.
67. 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.
68. TANAKA K. 1996: Seasonal and latitudinal variation in supercooling ability of the house spider, Achaearanea tepidariorum (Araneae: Theridiidae). Func. Ecol. 10: 185-192.
69. TANAKA S. 2000: The role of moisture in the control of diapause, mating and aggregation in a tropical insect. Entomol Sci. 3: 147-155.
70. 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.
71. 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.
72. 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.
73. 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.
74. WATANABE M. & TANAKA K. 1998a: Adult diapause and cold hardiness in Aulacophora nigripennis (Coleoptera: Chrysomelidae). J. Insect Physiol. 44: 1103-1110.
75. 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.
76. 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.
77. 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.
78. WATANABE M. & TANAKA K. 2000: Hormonal control of diapause and overwintering traits in a leaf beetle, Aulacophora nigripennis. Physiol. Entomol. 25: 337-345.
79. 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.
80. 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.
81. 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.
82. ZACHARIASSEN K.E. 1985: Physiology of cold tolerance in insects. Physiol. Rev. 65: 799-832.
83. ZACHARIASSEN K.E. & LUNDHEIM R. 1992: The endocrine control of insect cold hardiness. Zool. Jb. Physiol. 96: 183-196.