Eur. J. Entomol. 105 (4): 599-606, 2008 | 10.14411/eje.2008.080

The effect of temperature on the diapause and cold hardiness of Dendrolimus tabulaeformis (Lepidoptera: Lasiocampidae)

Ju-Ping ZENG1,2, Feng GE*,1, Jian-Wei SU1, Yong WANG3
1 State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, P.R. China
2 Graduate University, Chinese Academy of Sciences, Beijing 100049, P.R. China
3 Hunan Agricultural University, Changsha 410128, P.R. China

Pine caterpillar, Dendrolimus tabulaeformis Tsai et Liu, is a major pine pest in North China. The larvae enter diapause in the third or fourth instar before winter. Supercooling points (SCP) and cold hardiness of the diapausing larvae were investigated and compared in non-acclimated, acclimated and de-acclimated larvae. A bimodal frequency distribution was observed with a break point of -14C in the SCP. Larvae in the low group (LG, SCP <= -14C) were more cold tolerant with lower lethal temperatures than those in the high group (HG, SCP > -14C). This bimodality occurred in three patterns, LG (> 60% of individuals in LG), LG-HG (< 60% of individuals in LG and HG) and HG (> 60% of individuals in HG), in response to cold acclimation and de-acclimation. The cold hardiness was ranked as: LG > LG-HG > HG pattern. Cold hardiness was enhanced by an increase in concentrations of trehalose, galactose, glucose and mannose in the haemolymph as well as by decrease in metabolism after cold acclimation, but was lost after de-acclimation. Loss of cold hardiness was correlated with decrease in sugars and increase in metabolic rate. In conclusion, the species is a chill tolerant insect, adopting the strategy of depressing SCP through accumulation of low molecular weight sugars in the haemolymph, concomitant with metabolic depression.

Keywords: Dendrolimus tabulaeformis, acclimation, de-acclimation, cold hardiness, supercooling point, low molecular weight sugars

Received: March 10, 2008; Accepted: May 27, 2008; Published: October 24, 2008

Download citation

References

  1. BALE J.S. 1991: Insects at low temperature: a predictable relationship? Funct. Ecol. 5: 291-298 Go to original source...
  2. BALE J.S. 1996: Insects cold hardiness: a matter of life and death. Eur. J. Entomol. 93: 369-382
  3. 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...
  4. BALE J.S. & PULLIN A.S. 1991: Opportunities and risks in the overwintering strategy of a wall-dwelling species of Hypogastrura (Collembola). CryoLetters 12: 155-162
  5. BARSON G. 1974: Some effects of freezing temperatures on overwintering larvae of the large elm bark beetle (Scolytus scolytus). Ann. Appl. Biol. 78: 219-224 Go to original source...
  6. BAUST J.G. & ROJAS R.R. 1985: Insect cold hardiness: facts and fancy. J. Insect Physiol. 31: 755-759 Go to original source...
  7. BLOCK W. 1990: Cold tolerance of insects and other arthropods. Phil. Trans. R. Soc. Lond. (B) 326: 613-633 Go to original source...
  8. BLOCK W. & SOMME L. 1982: Cold hardiness of terrestrial mites at Signy Island, Maritime Antarctic. Oikos 38: 157-167 Go to original source...
  9. CANNON R.J.C. & BLOCK W. 1988: Cold tolerance of microarthropods. Biol. Rev. 63: 23-77 Go to original source...
  10. CHEN C.J. 1990: Integrated Management of Pine Caterpillars in China. China Forestry Publishing House, Beijing, 401 pp. [in Chinese]
  11. CHEN B. & KANG L. 2005: Can greenhouses eliminate the development of cold resistance of the leaf-miners? Oecologia 144: 187-195 Go to original source...
  12. CHEN C.P., DENLINGER D.L. & LEE JR. R.E. 1987: Cold-shock injury and rapid cold hardening in the flesh fly Sarcophaga crassipalpis. Physiol. Zool. 60: 297-304 Go to original source...
  13. CHOWN S.L. & NICOLSON S.W. 2004: Insect Physiological Ecology. Mechanisms and Patterns. Oxford University Press, Oxford, 254 pp
  14. DANIEL S.H. & SMITH R.H. 1994: Functional anatomy of the egg pore in Callosobruchus maculates: a trade-off between gas exchange and protective functions? Physiol. Entomol. 19: 30-38 Go to original source...
  15. DENLINGER D.L. 1985: Hormonal control of diapause. In Kerkut G.A. & Gilbert L.T. (eds): Comprehensive Insect Physiology Biochemistry and Pharmacology. Vol. 8. Pergamon Press, Oxford, pp. 353-412
  16. DENLINGER D.L. 1991: Relationship between cold hardiness and diapause. In Lee Jr. R.E. & Denlinger D.L. (eds): Insects at Low Temperature. Chapman and Hall, New York, pp. 174-198
  17. FIELDS P.G., FLEURAT-LESSARD F., LAVENSEAU L., FEBVAY G., PEYPELUT L. & BONNOT G. 1998: The effect of cold acclimation and deacclimation on cold tolerance, trehalose and free amino acid levels in Sitophilus granaries and Cryptolestes ferugineus (Coleoptera). J. Insect Physiol. 44: 955-965 Go to original source...
  18. GAO F., GE F., LIU X.H. & SONG Y. 2008: Impact of insecticides on the structure and productivity of insect pest and natural enemy communities associated with intercropping in cotton agroecosystems. Int. J. Pest. Manag. 54: 103-114 Go to original source...
  19. GIA F.Y. & LI Z.L. 1991: A study on the photoperiodic diapause of Dendrolimus spp. Forest Res. 4: 69-71 [in Chinese, English abstr.]
  20. GILSON W.E. 1963: Differential respirometer of simplified and improved design. Science 141: 531-532 Go to original source...
  21. GOTO M., SEKINE Y., OUTA H., HUJIKURA M. & SUZUKI K. 2001: Relationship between cold hardiness and diapause, and between glycerol and free amino acid contents in overwintering larvae of the oriental corn borer, Ostrinia furnacalis. J. Insect Physiol. 47: 157-165 Go to original source...
  22. GUEDES R.N., SMITH R.H. & GUEDES N.M. 2003: Host suitability, respiration rate and the outcome of larval competition in strains of the cowpea weevil, Callosobruchus maculatus. Physiol. Entomol. 28: 298-305. Go to original source...
  23. HAN R.D., GE F., YARDIM E.N. & HE Z. 2005: The effect of low temperatures on diapause and non-diapause larvae of the pine caterpillar, Dendrolimus tabulaeformis Tsai et Liu (Lepidoptera: Lasiocampidae). Japan. J. Appl. Entomol. Zool. 40: 429-435 Go to original source...
  24. HOFMANN A.A. 1995: Acclimation: increasing survival at a cost. TREE 10: 1-2
  25. HOLMSTRUP M., BAYLEY M. & RAMLOV H. 2002: Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable Arctic invertebrates. Proc. Natl. Acad. Sci. 99: 5716-5720 Go to original source...
  26. HOU T.Q. 1987: The Pine Caterpillars in China. Science Press, Beijing, 311 pp. [in Chinese]
  27. HUANG L.L., XUE F.S., WANG G.H., HAN R.D. & GE F. 2005: Photoperiodic response of diapause induction in the pine caterpillar, Dendrolimus punctatus. Entomol. Exp. Appl. 117: 127-133 Go to original source...
  28. KLOK C.J. & CHOWN S.L. 1998: Interactions between desiccation resistance, host-plant contact and the thermal biology of a leaf-dwelling sub-antarctic caterpillar, Embryonopsis halticella (Lepidoptera: Yponomeutidae). J. Insect Physiol. 44: 615-628 Go to original source...
  29. KLOK C.J., CHOWN S.L. & GASTON K.J. 2003: The geographic ranges structure of the holly leaf-miner. III. Cold hardiness physiology. Funct. Ecol. 17: 858-868 Go to original source...
  30. LEATHER S.R., WALTERS K.F.A. & BALE J. S. 1993: The Ecology of Insect Overwintering. Cambridge University Press, Cambridge, 255 pp
  31. LEE JR. R.E. 1989: Insect cold-hardiness: to freeze or not to freeze. BioScience 39: 308-313 Go to original source...
  32. LEE JR. R.E. 1991: Principles of insect low temperature tolerance. In Lee Jr. R.E. & Denlinger D.L. (eds): Insects at Low Temperature. Chapman and Hall, New York, 513 pp
  33. LEE JR. R.E. & DENLINGER D.L. 1991: Insects at Low Temperature. Chapman and Hall, New York, pp. 17-46
  34. LEE JR. R.E., CHEN C.P. & DENLINGER D.L. 1987: A rapid coldhardening process in insects. Science 238: 1415-1417 Go to original source...
  35. LEE JR. R.E., DAMODARAN K., YI S.X. & LORIGAN G.A. 2006: Rapid coldhardening increases membrane fluidity and cold tolerance of insect cells. Cryobiology 52: 459-463 Go to original source...
  36. LEINAAS H.P. & FJELLBERG A. 1985: Habitat structure and life history strategies of two partly sympatric and closely related, lichen feeding collembolan species. Oikos 44: 448-458 Go to original source...
  37. LEINAAS H.P. & SOMME L. 1984: Adaptations in Xenylla maritima and Anurophorus laricis (Collembola) to lichen habitats on alpine rocks. Oikos 43: 197-206 Go to original source...
  38. LI Z.L. & GIA F.Y. 1989: Photoperiodic reaction of the pine caterpillar Dendrolimus tabulaeformis Tsai et Liu. Acta Entomol. Sin. 32: 410-417 [in Chinese, English abstr.]
  39. LIU Q.S., ZHANG P. & FAN Z.Y. 2005: Analysis of carbohydrates by high performance anion exchange chromatography with pulsed amperometric detection (HPAE-PAD). Modern Sci. Instruments 1: 75-78 [in Chinese, English abstr.]
  40. PULLIN A.S. & BALE J.S. 1989: Effects of low temperature on diapausing Aglais urticae and Inachis io (Lepidoptera: Nymphalidae): Cold hardiness and overwintering survival. J. Insect Physiol. 35: 277-281 Go to original source...
  41. RICKARDS J., KELLEHER M.J. & STOREY K.B. 1987: Strategies of freeze avoidance in larvae of the goldenrod gall moth, Epiblema scudderiana: Winter profiles of a natural population. J. Insect Physiol. 33: 443-450 Go to original source...
  42. RING R.A. 1982: Freezing-tolerant insects with low supercooling points. Comp. Biochem. Phys. (A) 73: 605-612 Go to original source...
  43. SALT R.W. 1961: Principles of insect cold-hardiness. Annu. Rev. Entomol. 6: 55-74 Go to original source...
  44. SINCLAIR B.J., VERNON P., KLOK C.J. & CHOWN S.L. 2003a: Insects at low temperatures: an ecological perspective. Trends Ecol. Evol. 5: 257-262 Go to original source...
  45. SINCLAIR B.J., KLOK C.J., SCOTT M.B., TERBLANCHE J.S. & CHOWN S.L. 2003b: Diurnal variation in supercoling points of three species of Collembola from Cape Hallett, Antarctica. J. Insect Physiol. 49: 1049-1061 Go to original source...
  46. SOMME L. & BLOCK W. 1982: Cold hardiness of Collembola at Signy Island, Maritime Antarctic. Oikos 38: 168-176 Go to original source...
  47. SLACHTA M., VAMBERA J., ZAHRADNICKOVA H. & KOSTAL V. 2002: Entering diapause is a prerequisite for successful coldacclimation in adult Graphosoma lineatum (Heteroptera: Pentatomidae). J. Insect Physiol. 48: 1031-1039 Go to original source...
  48. SPICER J.I. & GASTON K.J. 1999: Physiological Diversity and its Ecological Implications. Blackwell, Oxford, 241 pp
  49. STOREY K.B. & STOREY J.M. 1988: Freeze tolerance in animals. Physiol. Rev. 68: 27-84
  50. TAUBER M.J., TAUBER C.A. & MASAKI S. 1986: Seasonal Adaptations of Insects. Oxford University Press, New York, 411 pp
  51. WANG X.H. & KANG L. 2005: Differences in egg thermotolerance between tropical and temperate populations of the migratory locust Locusta migratoria (Orthoptera: Acridiidae). J. Insect Physiol. 51: 1277-1285 Go to original source...
  52. WORLAND M.R. & BLOCK W. 1999: Ice-nucleating bacteria from the guts of two sub-Antarctic beetles, Hydromedion sparsutum and Perimylops antarcticus (Perimylopidae). Cryobiology 38: 60-67 Go to original source...
  53. WORLAND M.R. & CONVEY P. 2001: Rapid cold hardening in Antarctic microarthropods. Funct. Ecol. 15: 515-524 Go to original source...
  54. WORLAND M.R., LEINAAS H.P. & CHOWN S.L. 2006: Supercooling point frequency distributions in Collembola are affected by moulting. Funct. Ecol. 20: 323-329 Go to original source...
  55. ZHAO Y.X. & KANG L. 2000: Cold tolerance of the leafminer Liriomyza sativae (Dipt., Agromyzidae). J. Appl. Entomol. 124: 185-189 Go to original source...