Cold tolerance and trehalose accumulation in overwintering larvae of the codling moth, Cydia pomonella (Lepidoptera: Tortricidae)

European Journal of Entomology

Volumn 104, Issue 3, 2007, Pages 385-392

  Khani, Abbas ^a   Moharramipour, Saeid ^a   Barzegar, Mohsen ^a  

^a TARBIAT MODARES UNIVERSITY   (Iran)

Author keywords

Acclimation; Cold hardiness; Cydia pomonella; Diapause; Overwintering; Supercooling point; Tortricidae; Trehalose

Indexed keywords

ACCLIMATION; COLD TOLERANCE; DIAPAUSE; LARVA; MOTH; OVERWINTERING; PHENOLOGY; SUPERCOOLING; SURVIVAL;

CYDIA POMONELLA; LEPIDOPTERA; TORTRICIDAE;

EID: 34848901033     PISSN: 12105759     EISSN: 18028829     Source Type: Journal    
DOI: 10.14411/eje.2007.057     Document Type: Article

References (74)

1. AKRAMI F. 1984: Diapause of codling moth in east Azerbaijan. Appl. Entomol. Phytopathol. 52: 1-6.
2. BALE J.S. 1993: Classes of insect cold hardiness. Funct. Ecol. 7: 751-753.
3. BARNES M.M. 1991: Tortricids in porne and stone fruits. In Van Der Geest L.P.S. & Evenhuis H.H. (eds): Tortricid Pests, Their Biology Natural Enemies and Control. Elsevier, Amsterdam, pp. 313-327.
4. BERANKOVÁ J., BARTÁK M. & KOCOUREK F. 1988: Variability in spring emergence of the overwintering generation of codling moth Cydia pomonella (L.). Acta Entomol. Bohemoslov. 85: 274-282.
5. BLOCK W. 1991: To freeze or not to freeze? Invertebrate survival of sub-zero temperatures. Funct. Ecol. 5: 284-290.
6. BLOEM S., CARPENTER J.E. & DORN S. 2006: Mobility of mass-reared diapaused and nondiapaused Cydia pomonella (Lepidoptera: Tortricidae): Effect of different constant temperatures and lengths of cold storage. J. Econ. Entomol. 99: 707-713.
7. COULSON S.J. & BALE J.S. 1996: Supercooling and survival of the beech leaf mining weevil Rhynchaenus fagi L. (Coleoptera: Curculionidae). J. Insect Physiol. 42: 617-623.
8. DANKS H.V. 2006: Insect adaptations to cold and changing environments. Can. Entomol. 138: 1-23.
9. DENLINGER D.L. 1991: Relationship between cold hardiness and diapause. In Lee R.E. Denlinger D.L. (eds): Insects at Low Temperature. Chapman & Hall, New York, pp. 174-198.
10. DINIZ-MENDES L., BERNARDES E., DE ARAUJO P.S., PANEK A.D. & PASCHOALIN V.M. 1999: Preservation of frozen yeast cells by trehalose. Biotechnol. Bioeng. 65: 572-578.
11. DORN S., SCHUMACHER P., ABIVARDI C. & MEYHÖFER R. 1999: Global and regional pest insects and their antagonists in orchards: spatial dynamics. Agric. Ecosyst. Environ. 73: 111-118.
12. FIELDS P.G. 1992: The control of stored-product insects and mites with extreme temperatures. J. Stored Prod. Res. 28: 89-118.
13. GEIER P.W. 1963: Wintering and spring emergence of codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), in south-castern Australia. Aust. J. Zool. 11: 431-435.
14. GILLOOLY J.F., BROWN J.H., WEST G.B., SAVAGE V.M. & CHARNOV E.L. 2001: Effects of size and temperature on metabolic rate. Science 293: 2249-2251.
15. GLEN D.M. & BRAIN P. 1982: Pheromone-trap catch in relation to the phenology of codling moth (Cydia pomonella). Ann. Appl. Biol. 101: 429-440.
16. GLENN P.A. 1922: Relation of temperature to development of the codling-moth. J. Econ. Entomol. 15: 193-198.
17. GOTO M., LI Y.P., KAYABA S., OUTANI S. & SUZUKI K. 2001: Cold hardiness in summer and winter diapause and post-diapause pupae of the cabbage armyworm, Mamestra brassicae L. under temperature acclimation. J. Insect Physiol. 47: 709-714.
18. GOTTWALD R. 1996: Prognose der phänologie wichtiger schadorganismen im apfelbau mit hilfe von temperatursummen. Ges. Pflanzen 48: 140-146.
19. HAGLEY E.A.C. 1970: The distribution and survival of overwintering codling moth larvae in southern Ontario. Proc. Entomol. Soc. Ont. 100: 40-47.
20. HAGSTRUM D.W. & FLINN P.W. 1994: Survival of Rhyzopertha dominica (Coleoptera: Bostrichidae) in stored wheat under fall and winter temperature conditions. Environ. Entomol. 23: 391-395.
21. HAYAKAWA Y. & CHINO H. 1981: Temperature-dependent inter-conversion between glycogen and trehalose in diapausing pupae of Philosamia cynthia ricini and pryeri. Insect Biochem. 11: 43-47.
22. HOLMAN G.M., NACHMAN R.J. & WRIGHT M.S. 1990: Insect neuropeptides. Annu. Rev. Entomol. 35: 201-217.
23. HOWELL J.F. & NEVEN L.G. 2000: Physiological development time and zero development temperature of the codling moth (Lepidoptera: Tortricidae). Environ. Entomol. 29: 766-772.
24. HOWELL J.F. & SCHMIDT R.S. 2002: Codling moth (Lepidoptera: Tortricidae): Development at constant and at orchard temperatures. J. Agri. Urban Entomol. 19: 15-23.
25. JONES S.R. & KUNZ S.E. 1997: Importance of supercooling points in the overwintering of the horn fly and stable fly (Diptera: Muscidae). J. Medical Entomol. 34: 426-429.
26. KANDROR O., DELEON A. & GOLDBERG A.L. 2002: Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc. Natl. Acad. Sci. USA 99: 9727-9732.
27. KONO Y., TAKAHASI M., MATSUSHITA K., NISHINA M., KAMEDA Y. & HORI E. 1994: Inhibition of flight in Periplaneta americana (Linn.) by a trehalase inhibitor, validoxylamine A. J. Insect Physiol. 40: 455-461.
28. KOŠŤÁL V. & ŠIMEK P. 1995: Dynamics of cold hardiness, supercooling and cryoprotectants in diapausing and non-diapausing pupae of the cabbage root fly, Delia radicum L. J. Insect Physiol. 41: 627-634.
29. KOŠŤÁL V. & ŠIMEK P. 1996: Biochemistry and physiology of aestivolhibernation in the adult apple blossom weevil Anthonomus pomorum (Coleoptera: Curcutionidae). J. Insect Physiol. 42: 727-733.
30. KOŠŤÁL V., ŠLACHTA M. & ŠINEK P. 2001: Cryoprotective role of polyols independent of the increase in supercooling capacity in diapausing adults of Pyrrhocoris apterus (Heteroptera: Insecta). Comp. Biochem. Physiol. (B) 130: 365-374.
31. KUHRT U., SAMIETZ J. & DORN S. 2005: Thermoregulation behaviour in codling moth larvae. Physiol. Entomol. 30: 54-61.
32. KUHRT U., SAMIETZ J. & DORN S. 2006: Thermal response in adult codling moth. Physiol. Entomol. 31: 80-88.
33. LEE R.E. 1991: Principles of insect low temperature tolerance. In Lee R.E. & Denlinger D.L. (eds): Insects at Low Temperature. Chapman & Hall, New York, pp. 17-46.
34. LESLIE S.B., ISRAELI E., LIGHTHART B., CROWE J.H. & CROWE L.M. 1995: Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl. Environ. Microbiol. 61: 3592-3597.
35. MINDER I.F., DASH A.V. & CHESNEK S.I. 1984: Seasonal changes in the resistance to cold and the content of glycogen, glycerin and reducing sugars in the body of hibernating larvae of the codling moth (Laspeyresia pomonella). Zool. Zh. 63: 1355-1362 [in Russian, English abstr.].
36. MIYAZAKI S., KAYUKAWA T., CHEN B., NOMURA M. & ISHIKAWA Y. 2006: Enhancement of cold hardiness by acclimation is stage-specific in the non-diapausing pupae of onion maggot Delia antiqua (piptera: Anthomyiidae). Eur. J. Entomol. 103: 691-694.
37. MOFFITT H.R. & ALBANO D. 1972: Effects of commercial fruit storage on stages of the codling moth. J. Econ. Entomol. 65: 770-773.
38. NAEEMULLAH M., TANAKA K., TSUMUKI H. & TAKEDA M. 1999: Relationship of cold tolerance to developmental determination in the Indian meal moth, Plodia interpunctella (Lepidoptera: Phycitidae). Appl. Entomol. Zool. 34: 267-276.
39. NEEDHAM G.R., JAWORSKI D.C., CHEN C.-P. & LEE R.E.JR. 1996: Cold hardiness of a laboratory reared colony of lone star ticks (Acari: Ixodidae). J. Med. Entomol. 33: 706-710.
40. NEVEN L.G. 1994: Combined heat treatments and cold storage effects on mortality of fifth-instar codling moth (Lepidoptera: Tortricidae). J. Econ. Entomol. 87: 1262-1265.
41. NEVEN L.G. 1999: Cold hardiness adaptations of codling moth, Cydia pomonella. Cryobiology 38: 43-50.
42. NEVEN L.G., FERGUSON H.J. & KNIGHT A. 2000: Sub-zero cooling synchronizes post-diapause development of codling moth, cydia pomonella. Cryo-Letters 21: 203-214.
43. NEWCOMER E.J. 1920: Winterkilling of codling moth larvae. J. Econ. Entomol. 13: 441-442.
44. NEWCOMER E.J. 1936: Effect of cold storage on eggs and young larvae of codling moth. J. Econ. Entomol. 29: 1123-1125.
45. 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.
46. NORDIN J.H., CUI, Z. & YIN C.M. 1984: Cold-induced glycerol accumulation by Ostrinia nubilalis larvae is developmentally regulated. J. Insect Physiol. 30: 563-566.
47. PELLERIN-MENDES C., MILLION L., MARCHAND-ARVIER M., LABRUDE P. & VIGNERON C. 1997: In vitro study of the protective effect of trehalose and dextran during freezing of human red blood cells in liquid nitrogen. Cryobiology 35: 173-186.
48. PIO C.J. & BAUST J.G. 1988: Effects of temperature cycling on cryoprotectant profiles in the goldenrod gall fly, Eurosta solidaginis (Fitch). J. Insect Physiol. 34: 767-771.
49. RAJABI G., BEHESHTI N.D., AKRAMI F., BAYATASSADI H., DICKLER E. & DAVOUD Z. 1978: Codling moth in Iran. An abstract of results obtained during the years 1975, 1976 and 1977. Appl. Entomol. Phytopathol. 46: 1-54.
50. RAUDONIS L. 2002: Effects of temperature on egg laying activity of codling moth (Cydia pomonella L.). Sodininkyste ir Darzininkyste 21: 165-173.
51. RICRARDSON J.C., JORGESEN C.D. & CROFT B.A. 1982: Embryogenesis of the codling moth, Laspeyresia pomonella: Use in validating phenology models. Ann. Entomol. Soc. Am. 75: 201-209.
52. RIEDL H. & CROFT B.A. 1978: The effects of photoperiodic and effective temperatures on the seasonal phenology of the codling moth (Lepidoptera: Tortricidae). Can. Entomol. 110: 455-470.
53. RING R.A. & DANKS H.V. 1998: The role of trehalose in cold-hardiness and desiccation. Cryo-Letters 19: 275-282.
54. ROJAS R.R., CHARLET L.D. & LEOPOLD R.A. 1991: Biochemistry and physiology of overwintering in the mature larva of the red sunflower seed weevil, Smicronyx fulvus Leconte (Coleoptera: Curculionidae). J. Insect Physiol. 37: 489-496.
55. ROJAS R.R., CHARLET L.D. & LEOPOLD R.A. 1994: Trehalose accumulation in the overwintering larva of the long-horned sunflower girdler, Dectes texanus. Cryo-Letters 15: 394-398.
56. RUDOLPH A.S. & GOINS B. 1991: The effect of hydration stress solutes on the phase behaviour of hydrated dipalmitoylpho-spatidylcholine. Biochim. Biophys. Acta 1066: 90-94.
57. SÆTHRE M.G. & HOFSVANG T. 2002: Effect of temperature on oviposition behavior, fecundity, and fertility in two northern european populations of the codling moth (Lepidoptera: Tortricidae). Environ. Entomol. 31: 804-815.
58. SAEB H. 1994: Bio-ecological investigations on codling moth in the Rasht region. J. Entomol. Soc. Iran 14: 17-18.
59. SATO H.A. 1964: Preliminary report on the response to temperature of the overwintering immature stage of Carpocapsa pomonella. Ann. Rept. Soc. Plant Prot. N. Japan 15: 113.
60. 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: 349-359.
61. SIEGLER E.H. 1946: Susceptibility of hibernating codling moth larvae to low temperatures, and the bound water content. J. Agr. Res. 72: 329-340.
62. SØMME L. 1968: The effect of acclimation and glycerol injection on mortality and pupation in larvae of Ephestia kuehniella after exposures at low temperatures. Entomol. Exp. Appl. 11: 143-148.
63. SØMME L. 1982: Supercooling and winter survival in terrestrial arthropods. Comp. Biochem. Physiol. (A) 73: 519-543.
64. SØMME L. 1999: The physiology of cold hardiness in terrestrial arthropods. Eur. J. Entomol. 96: 1-10.
65. STOREY J.M. & STOREY K.B. 1983: Regulation of cryoprotectant metabolism in the overwintering gall fly larvae, Eurosta solidaginis: temperature control of glycerol and sorbitol levels. J. Comp. Physiol. 149: 495-502.
66. STOREY K.B. & STOREY J.M. 1988: Freeze tolerance in animals. Physiol. Rev. 68: 27-84.
67. STOREY K.B. & STOREY J.M. 1991: Biochemistry of cryoprotectants. In Lee R.E. & Denlinger D.E. (eds): Insects at Low Temperature. Chapman & Hall, New York, pp. 64-93.
68. TOBA H.H. & MOFFITT H.R. 1991: Controlled-atmosphere cold storage as a quarantine treatment for nondiapausing codling moth (Lepidoptera: Tortricidae) larvae in apples. J. Econ. Entomol. 84: 1316-1319.
69. TSUMUKI H. 1990: Environmental adaptations of the rice stem borer Chilo suppressalis and the blue alfalfa aphid, Acyrthosiphon kondoi to seasonal fluctuations. In Hoshi M. & Yamashita O. (eds): Advances in Invertebrate Reproduction 5. Elsevier, Amsterdam, pp. 273-278.
70. YOKOYAMA V.Y. & MILLER G.T. 1989: Response of codling moth and oriental fruit moth (Lepidoptera, Tortricidae) immatures to low-temperature storage of stone fruits. J. Econ. Entomol. 82: 1152-1156.
71. YOTHERS M.A. & CARLSON F.W. 1941: Orchard observations of the emergence of codling moths from two year old larvae. J. Econ. Entomol. 34: 109-110.
72. ZACHARIASSEN K.E. 1985: Physiology of cold tolerance in insects. Physiol. Rev. 65: 799-832.
73. ZACHARIASSEN K.E., KRISTIANSEN E., PEDERSEN S.A. & HAMMEL H.T. 2004: Ice nucleation in solutions and freeze-avoiding insects-homogeneous or heterogeneous? Cryobiology 48: 309-321.
74. ZHOU X.L., ZHU H., ZHANG S.Z., ZHU F.M., CHEN G.M. & YAN L.X. 2006: Freeze-drying of humanIplatelets: influence of intracellular trehalose and extracellular protectants. Cryo-Letters 27: 43-50.