Eur. J. Entomol. 115: 198-207, 2018 | DOI: 10.14411/eje.2018.018

Cold hardiness of larvae of Dendrolimus tabulaeformis (Lepidoptera: Lasiocampidae) at different stages during the overwintering periodOriginal article

Yuying SHAO1, Yuqian FENG1, Bin TIAN1, Tao WANG2, Yinghao HE3, Shixiang ZONG1,*
1 Beijing Key Laboratory for Forest Pest Control, Beijing Forestry University, Beijing 100083, P. R. China; e-mails: zongsx@126.com, 1102671261@qq.com, fengyuqian1988@163.com, 363872410@qq.com
2 Mentougou Forestry Station, Beijing 102300, P. R. China; e-mail: 952330814@qq.com
3 School of Science, Beijing Forestry University, Beijing 100083, P. R. China; e-mail: 18811302553@163.com

The Chinese pine caterpillar Dendrolimus tabulaeformis is an important destructive leaf borer in boreal coniferous forests in China. This species overwinters in the larval stage. Changes in supercooling capacity and physiological-biochemical parameters of D. tabulaeformis larvae from a natural population were evaluated at different stages during the overwintering period. Cold hardiness of overwintering larvae collected in January was significantly greater than that of larvae collected in other months. January larvae survived for 15 days at -10°C and for approximately 2 days at -15°C. By contrast, larvae collected in September survived for no more than 4 h at -5°C and those in November and March no more than 1 day at -15°C. Supercooling point gradually decreased from -5.9 ± 0.3°C in September to a minimum of -14.1 ± 1.0°C in November, then gradually increased to the original value with the advent of spring. Water content gradually decreased from September to November, remained at approximately 74.5% until March and then gradually increased to levels similar to those in September. The lipid content gradually decreased from September to November, remained stable at approximately 3.2% until March and then gradually increased to levels similar to those in September. Glycogen content increased to a peak in November and then decreased. The concentrations of several metabolites showed significant seasonal changes. The most prominent metabolite was trehalose with a seasonal maximum in November. Glucose levels were highest in January and then gradually decreased until in May they were at levels similar to those in September. Glycerol levels remained relatively stable during winter but increased significantly in May. This study indicates that D. tabulaeformis is a freeze-avoidant insect. Larvae increase their supercooling capacity by regulating physiological-biochemical parameters during overwintering. Our results provide the basis for further research into the mechanism of cold hardiness in this species.

Keywords: Lepidoptera, Lasiocampidae, Dendrolimus tabulaeformis, larvae, supercooling point, cryoprotectants, cold hardiness

Received: May 30, 2017; Revised: March 29, 2018; Accepted: March 29, 2018; Published online: May 2, 2018  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
SHAO, Y., FENG, Y., TIAN, B., WANG, T., HE, Y., & ZONG, S. (2018). Cold hardiness of larvae of Dendrolimus tabulaeformis (Lepidoptera: Lasiocampidae) at different stages during the overwintering period. EJE, 115, Article 198-207. https://doi.org/10.14411/eje.2018.018
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Andreadis S.S. & Athanassiou C.G. 2017: A review of insect cold hardiness and its potential in stored product insect control. - Crop. Prot. 91: 93-99. Go to original source...
    2. Bale J.S. 1996: Insect 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. (B) 357: 849-862. Go to original source...
    4. Behm C.A. 1997: The role of trehaelos in the physiology of nematodes. - Int. J. Parasitol. 27: 215-229. Go to original source...
    5. Chen C.P. & Denlinger D.L. 1990: Activation of phosphorylase in response to cold and heat stress in the flesh fly, Sarcophaga crassipalpis. - J. Insect Physiol. 36: 549-554. Go to original source...
    6. Chen Y.J., Sun X.L., Zhang W.G., Mou Z.Z. & Guo G.Z. 2005: Relationship between variation of water, lipid and glycerin in over-wintering Diaphania pyloalis Walker larvae and cold-hardiness. - Sci. Sericult. 31: 111-116.
    7. Chen H., Liang G.M., Zou L.Y., Guo F., Wu K.M. & Guo Y.Y. 2010: Research progresses in the cold hardiness of insects. - Plant Prot. 36: 18-24.
    8. Crosthwaite J.C., Sobek S., Lyons D.B., Bernards M.A. & Sinclair B.J. 2011: The overwintering physiology of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae). - J. Insect Physiol. 57: 166-173. Go to original source...
    9. Dai S.M., Cheng X.Y., Xiao Q.M. & Xie B.Y. 2006: Research progress in nematode cold tolerance. - Acta Ecol. Sin. 26: 3885-3890.
    10. Danks H.V. 1987: Insect Dormancy: An Ecological Perspective. Biological Survey of Canada Press, Ottawa, pp. 114-122.
    11. Danks H.V. 2006: Insect adaptations to cold and changing environments. - Can. Entomol. 138: 1-23. Go to original source...
    12. Denlinger D.L. 1991: Relationship between cold hardiness and diapause. In Lee R.E. et al. (eds): Insects at Low Temperature. Chapman & Hall, New York, London, pp. 174-198. Go to original source...
    13. Fan J.H., Xie Y.P., Xue J.L. & Li B.Z. 2008: A strain of parasitic Dendrolimus tabulaeformis toxin chemical constituents of Beauveria bassiana. - Acta Microbiol. Sin. 48: 596-601.
    14. Feng Y.Q., Wang J.L. & Zong S.X. 2014: Review of insect overwintering stages and cold-resistance strategies. - Chin. Agr. Sci. Bull. 30: 22-25.
    15. Feng Y.Q., Li W.B., Luo Y.Q., Wang T. & Zong S.X. 2015: Cold tolerance of Asias halodendri (Pallas) overwintering larvae. - Acta Agric. Bor.-Occid. Sin. 24: 175-180.
    16. Feng Y.Q., Xu L.L., Li W.B., Xu Z.C., Cao M., Wang J.L., Tao J. & Zong S.X. 2016: Seasonal changes in supercooling capacity and major cryoprotectants of overwintering Asian longhorned beetle (Anoplophora glabripennis) larvae. - Agr. For. Entomol. 18: 302-312. Go to original source...
    17. Folch J., Lees M. & Sloane Stanley G.H. 1957: A simple method for the isolation and purification of total lipids from animal tissues. - J. Biol. Chem. 226: 497-509. Go to original source...
    18. Han Z.J., Wang Y.C. & You Z.P. 1989: Cold-hardiness mechanism of terrestrial insects. - Chin. Bull. Entomol. 1: 39-42.
    19. Han R.D., Sun X.G., Xu Y.Y. & Zhang W.G. 2005: The biochemical mechanism of cold-hardiness in overwintering larva of Dendrolimus spectabilis Butler (Lepidoptera: Lasiocampidae). - Acta Entomol. Sin. 25: 1352-1356.
    20. Hao S.G. & Kang L. 2004: Supercooling capacity and cold hardiness of the eggs of the grasshopper Chorthippus fallax (Orthoptera: Acrididae). - Eur. J. Entomol. 101: 231-236. Go to original source...
    21. Holmstrup M. 1992: Cold hardiness strategy in cocoons of the lumbricid earthworm Dendrobaena octaedra (Savigny). - Comp. Biochem. Physiol. 102: 251-255. Go to original source...
    22. Jing X.H. & Kang L. 2002: Research progress in insect cold hardines. - Acta Entomol. Sin. 22: 2202-2207.
    23. Jing X.H. & Kang L. 2004: Overview and evaluation of research methodology for insect cold hardiness. - Chin. Bull. Entomol. 40: 7-10.
    24. Lee R.E. 1991: Principles of insect low temperature tolerance. In Lee R.E. & Denlinger D.L. (eds): Insect at Low Temperatures. Springer, New York, pp. 17-46. Go to original source...
    25. Lee R.E. 1989: Insect cold-hardiness: To freeze or not to freeze. - BioScience 39: 308-313. Go to original source...
    26. Lee R.E. 2010: A primer on insect cold tolerance. In Denlinger D.L. & Lee R.E. (eds): Low Temperature Biology of Insects. Cambridge University Press, Cambridge, pp. 3-34. Go to original source...
    27. Lee R.E. & Denlinger D.L. 1985: Cold tolerance in diapausing and non-diapausing stage of the flesh fly, Sarcophaga crassipalpis. - Physiol. Entomol. 10: 309-315. Go to original source...
    28. Li Y.J. 2008: The occurrence and control of major pests of Pinus tabulaeformis in Liaoning Province. - Liaoning For. Sci. Technol. 3: 57-59.
    29. Li X.P., Song L.W., Zhang H.H., Chen Y.Q., Zuo T.T., Wang J. & Sun W. 2012: Responses of Arma chinensis cold tolerance to rapid cold hardening and underlying physiological mechanisms. - Chin. J. Appl. Ecol. 23: 791-797.
    30. Li Y. 2013: Biology characteristic and prevention of Chinese pine larva aculeata. - Mod. Agric. Sci. Technol. 21: 165-167.
    31. Li M. 2014: Comprehensive prevention and control technology of Dendrolimus. - Mod. Agr. Sci. Technol. 24: 21.
    32. Li Y.P. & Gong H. 2000: Insect cryobiology: II. Ice core material (ice core protein) and the frost resistance of insect. - Chin. Bull. Entomol. 37: 250-254.
    33. Liu K.W. 2012: Sex Pheromone Identification of Chinese Pine Moth Dendrolimus tabulaeformis and the Release Rates of Pine Caterpillar Moths Pheromones from Dispensers. M.Sc. Thesis, Shandong Agricultural University, Shandong.
    34. Liu S.H. 2006: The harms of Dendrolimus tabulaeformis and preventing methods. - Sci-Tech. Inform. Dev. Econ. 16: 285-286.
    35. Liu Y.Q. 1963: A general survey of the geographical distribution of Dendrolimus germar in the eastern portion of China. - Acta Ecol. Sin. 12: 345-353.
    36. Liu Z., Gong P., Wu K., Wei W., Sun J. & Li D. 2007: Effects of larval host plants on over-wintering preparedness and survival of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). - J. Insect Physiol. 53: 1016-1026. Go to original source...
    37. Liu H., Yin H.J., Cheng X.J., Lin B., Zhao C.Z. & Yin C.Y. 2010: Problems and strategies of sustainable regeneration of plantation ecosystem in China. - World For. Res. 23: 71-75.
    38. Ma R.Y., Hao S.G., Kong W.N., Sun J.H. & Kang L. 2006: Cold hardiness as a factor for assessing the potential distribution of the Japanese pine sawyer Monochamus alternatus (Coleoptera: Cerambycidae) in China. - Ann. For. Sci. 63: 449-456. Go to original source...
    39. Ouyang F. & Ge F. 2014: Determination and analysis of antifreeze and cold resistance of insects. - J. Appl. Entomol. 51: 1646-1652.
    40. Ouyang F., Liu Z.D., Yin J., Su J., Wang C. & Ge F. 2011: Effect of transgenic Bt cotton on overwintering characteristics and survival of Helicoverpa armigera. - J. Insect Physiol. 57: 153-160. Go to original source...
    41. Qin J.M., Luo S.D., He S.Y. & Wu J. 2015: Researching in characters and functions of trehalose and trehalose enzymes in insects. - J. Environ. Entomol. 37: 163-169.
    42. Rozsypal J., Koštál V., Zahradníčková H. & Šimek P. 2013: Overwintering strategy and mechanisms of cold tolerance in the codling moth (Cydia pomonella). - Plos One 8(4): e61745, 11 pp. Go to original source...
    43. Saeidi F., Moharramipour S. & Barzegar M. 2012: Seasonal patterns of cold hardiness and cryoprotectant profiles in Brevicoryne brassicae (Hemiptera: Aphididae). - Environ. Entomol. 41: 1638-1643. Go to original source...
    44. 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...
    45. Sinclair B.J., Alvarado L.E.C. & Ferguson L.V. 2015: An invitation to measure insect cold tolerance: methods, approaches, and workflow. - J. Therm. Biol. 53: 180-197. Go to original source...
    46. Sømme L. 1982. Supercooling and winter survival in terrestrial arthropods. - Comp. Biochem. Physiol. (A) 73: 519-543. Go to original source...
    47. Stephen R.M., Chen C.P. & Virginia K.W. 2001: Cold tolerance and proline metabolic gene expression in Drosophila melanogaster. - J. Insect Physiol. 47: 393-400. Go to original source...
    48. Storey K.B. & Storey J.M. 1991: Biochemistry of cryoprotectants. In Lee R.E. & Denlinger D.L. (eds): Insect at Low Temperatures. Chapman and Hall, New York, pp. 64-93. Go to original source...
    49. Sun X.G., Mao X.H. & Li S.T. 2001: The cold tolerance mechanism of insects and its research development. - J. Shandong Agr. Univ. 32: 393-396.
    50. Tang W.G. 2012: Study on biological characteristics and comprehensive prevention and control technology of Dendrolimus tabulaeformis. - J. Shanxi Agr. Sci. 58: 47-49.
    51. Wang X.H. & Kang L. 2014: Molecular mechanisms of phase change in locusts. - Annu. Rev. Entomol. 59: 225-243. Go to original source...
    52. Wang Q.S. & Wang Y.Z. 2006: Study on the relationship between the damage of Dendrolimus tabulaeformis and stand three factors. - Protect. For. Sci. Technol. 2006(z1): 25-27.
    53. Wang P., Yu Y., Men X.Y., Zhang S.C., Zhang A.S., Zhang Y.Y. & Ling L.L. 2011: Dynamics of cold-resistant substances in overwintering cocooned and non-cocooned larvae of the peach fruit moth, Carposina niponensis Walsingham (Lepidoptera: Carposinidae). - Acta Entomol. Sin. 54: 279-285.
    54. Wharton D.A., Young S.R. & Barrett J. 1984: Cold tolerance in nematodes. - J. Comp. Physiol. (B) 154: 73-77. Go to original source...
    55. Williams C.M., Thomas R.H., Macmillan H.A., Marshall K.E. & Sinclair B.J. 2011: Triacylglyceride measurement in small quantities of homogenised insect tissue: comparisons and caveats. - J. Insect Physiol. 57: 160-1613. Go to original source...
    56. Xia R.X. & Xu L.H. 1993: Study on the super-cooling point of the overwintering larvae of three kinds of pine caterpillar. - Sci. Silva. Sin. 29: 186-189.
    57. Xia N.B., Tu Q.H. & Ma Z.S. 1989: A study on sampling techniques for Dendrolimus tabulaeformis larvae. - Acta Ecol. Sin. 9: 341-347.
    58. Xia N.B., Tu Q.H. & Zhang S.F. 1990: Study on the dynamic pattern of Dendrolimus tabulaeformis larvae. - Sci. Silva. Sin. 26: 322-328.
    59. Xue J.L., Niu X. & Xie Y.P. 2006: Changes of protein, esterase and PPO in Dentrolimus tabulaeformis infected by Beauveria bassiana. - Chin. J. Appl. Environ. Biol. 12: 814-818.
    60. Yuan Y.Y., Gao B.J., Li M., Yuan S.L. & Zhou G.N. 2008: The genetic diversity of Dendrolimus tabulaeformis in forests of different stand types. - Acta Ecol. Sin. 28: 2100-2106.
    61. Zachariassen K.E. 1985: Physiology of cold tolerance in insect. - Physiol. Rev. 65: 799-832. Go to original source...
    62. Zeng J.P., Ge F., Su J.W. & Wang Y. 2008: The effect of temperature on the diapause and cold hardiness of Dendrolimus tabulaeformis (Lepidoptera: Lasiocampidae). - Eur. J. Entomol. 105: 599-606. Go to original source...
    63. Zeng J.P., Ge F., Su J.W. & He Z. 2010: Researches on the occurrences of major forest insect pests of pine caterpillar Dendrolimus spp. in China. - Chin. Bull. Entomol. 47: 451-459.
    64. Zhang L.L. 2005: Study of Influence on Growth and Development of Dendrolimus tabulaeformis (Tsai et Liu). M.S. Thesis. Beijing Forestry University, Beijing.
    65. Zhang L.X. 2011: New progress in the study on spatial pattern of different instars population and sampling technique of Dendrolimus tabulaeformis. - Liaoning For. Sci. Technol. 6: 25-31.
    66. Zhang Y.L., Mu W., Chen Z.L., Han Z.R., Ma C. & Zhai R.H. 2007: Susceptibility and related physiological and biochemical mechanisms of Carposina niponensis Walsingham larvae on six insecticides before and after overwintering. - Chin. J. Appl. Ecol. 18: 1913-1916.
    67. Zhao L.J. 2003: Study on Water Consumption Characteristics of Main Plantation Tree Species and Technology of Drought Resistant for Afforestation in North China. M.S. Thesis, Beijing Forestry University, Beijing.
    68. Zhao J., Yu L.Y., Li M., Zheng F.Q., Zhang F. & Xu Y.Y. 2008: Seasonal variation in cold tolerance of the multicolored ladybeetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) adults. - Acta Entomol. Sin. 51: 1271-1278.
    69. Zhu J., Zhang X.F., Yang W.B. & Wang Z.M. 1995: Study on the damage mechanism and the influence to forest growth of Dendrolimus tabulaeformis. - Shaanxi For. Sci. Technol. 3: 36-39.

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content