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Effects of soil temperature and snow cover on the mortality of overwintering pupae of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

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Abstract

Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) is one of the most damaging insect pests in the world. However, little is known about the effects of snow cover and soil temperature on the overwintering pupae of H. armigera. A field experiment was conducted from November 2, 2012 to April 24, 2013 at the agrometeorological experimental station in Wulanwusu, China. Overwintering pupae were embedded into the soil at depths of 5, 10, and 15 cm in the following four treatments: without snow cover, snow cover, and increased temperatures from 600 and 1200 W infrared lights. The results showed that snow cover and rising temperatures could all markedly increase soil temperatures, which was helpful in improving the survival of the overwintering pupae of H. armigera. The mortality of overwintering pupae (MOP) at a depth of 15 cm was the highest, and the MOP at a depth of 5 cm followed. The lower accumulated temperature (≤0 °C) (AT ≤ °C) led to the higher MOP, and the lower diurnal soil temperature range (DSTR) likely led to the lower MOP. After snowmelt, the MOPs at the depths of 5 and 10 cm increased as the soil temperature increased, especially in April. The AT of the soil (≤0 °C) was the factor with the strongest effect on MOP. The soil moisture content was not a major factor affecting the MOP in this semiarid region because precipitation was 45 mm over the entire experimental period. With climate warming, the MOP will likely decrease, and the overwintering boundary air temperatures of H. armigera should be expanded due to higher soil temperatures and increased snow cover.

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References

  • Asahina E (1969) Frost resistance in insects. Adv Insect Physiol 6:1–49

    Article  Google Scholar 

  • Ayres MP, Lombardero MJ (2000) Assessing the consequences of global change for forest disturbance from herbivores and pathogens. Sci Total Environ 262:263–286

    Article  CAS  Google Scholar 

  • Beck SD (1983) Insect thermoperiodism. Annu Rev Entomol 28:91–108

    Article  Google Scholar 

  • Beltrami H (2001) On the relationship between ground temperature histories and meteorological records: a report on the Pomquet station. Glob Planet Chang 29:327–348

    Article  Google Scholar 

  • Bokhorst S, Phoenix GK, Bjerke JW, Callaghan TV, Huyer-Brugman F, Berg MP (2012) Extreme winter warming events more negatively impact small rather than large soil fauna: shift in community composition explained by traits not taxa. Glob Chang Biol 18:1152–1162

    Article  Google Scholar 

  • Brooks PD, McKnight D, Elder K (2004) Carbon limitation of soil respiration under winter snowpacks: potential feedbacks between growing season and winter carbon fluxes. Glob Chang Biol 11:231–238

    Article  Google Scholar 

  • Chen FJ, Zhai BP, Zhang XX (2003) Effects of soil moisture during pupal stage on population development of cotton bollworm, Helicoverpa armigera (Hübner). Acta Ecol Sin 23:112–121

    Google Scholar 

  • CMA (2003) Specification of surface air observation. China Meteorological Press, Beijing

    Google Scholar 

  • Danks HV (2000) Dehydration in dormant insects. J Insect Physiol 46:837–852

    Article  CAS  Google Scholar 

  • Decker KLM, Wang D, Waite C, Scherbatskoy T (2003) Snow removal and ambient air temperature effects on forest soil temperatures in northern Vermont. Soil Sci Soc Am J 67:1234–1243

    Article  CAS  Google Scholar 

  • Denlinger DL, Lee RE (2010) Insect low temperature biology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Eger JE Jr, Witz JA, Hartstack AW, Sterling WL Jr (1982) Survival of pupae of Heliothis virescens and Heliothis zea (Lepidoptera: Noctuidae) at low temperatures. Can Entomol 114:289–301

    Article  Google Scholar 

  • Eger JE Jr, Sterling WL, Hartstack AW Jr (1983) Winter survival of Heliothis virescens and Heliothis zea (Lepidoptera: Noctuidae) in College Station, Texas. Environ Entomol 12:970–975

    Article  Google Scholar 

  • Field A (2000) Discovering statistics using SPSS for Windows. Sage, London

    Google Scholar 

  • Fitt GP (1989) The ecology of heliothis in relation to agroecosystems. Annu Rev Entomol 34:17–52

    Article  Google Scholar 

  • Goodrich LE (1982) The influence of snow cover on the ground thermal regime. Can Geotech J 19:421–432

    Article  Google Scholar 

  • Groffman PM, Driscoll CT, Fahey TJ, Hardy JP, Fitzhugh RD, Tierney GL (2001) Colder soils in a warmer world: a snow manipulation study in a northern hardwood forest ecosystem. Biogeochemistry 56:135–150

    Article  CAS  Google Scholar 

  • Guo YY (1995) Integration prevention and control for Helicoverpa armigera. Golden Shield Publishing House, Beijing, pp 16–25

    Google Scholar 

  • Han EN, Bause E (1998) Timing of diapause initiation, metabolic changes and overwintering survival of the spruce budworm Choristoneura fumiferana. Ecol Entomol 23:160–167

    Article  Google Scholar 

  • Hodkova M, Socha R (1995) Effect of temperature on photoperiodic response in a selected nondiapause strain of Pyrrhocoris apterus (Heteroptera). Physiol Entomol 20:303–308

    Article  Google Scholar 

  • Huang J, Li J (2015) Effects of climate change on overwintering pupae of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Int J Biometeorol 59:877–888

    Article  Google Scholar 

  • IPCC (2013) Climate change 2013. In: Stocker T, Dahe Q, Plattner GK (eds) The physical science basis: contribution of Working Group I to the 5th Assessment Report of the IPCC. IPCC, Stockholm

    Google Scholar 

  • Isard SA, Schaetzl RJ, Andresen JA (2007) Soils cool as climate warms in the great lakes region: 1951–2000. Ann Assoc Am Geogr 97:467–476

    Article  Google Scholar 

  • Jackson T, Mansfield K, Saafi M, Colman T, Romine P (2008) Measuring soil temperature and moisture using wireless MEMS sensors. Measurement 41:381–390

    Article  Google Scholar 

  • Koštál V, Yanagimoto M, Bastl J (2006) Chilling-injury and disturbance of ion homeostasis in the coxal muscle of the tropical cockroach (Nauphoeta cinerea). Comp Biochem Physiol B143:171–179

    Google Scholar 

  • Kreyling J, Henry HAL (2011) Vanishing winters in Germany: soil frost dynamics and snow cover trends, and ecological implications. Clim Res 46:269–276

    Article  Google Scholar 

  • Land WH Jr, Ford W, Park JW, Mathur R, Hotchkiss N, Heine J, Eschrich S, Qiao X, Yeatman T (2011) Partial least squares (PLS) applied to medical bioinformatics. Procedia Comput Sci 6:273–278

    Article  Google Scholar 

  • Leather SR, Walters KFA, Bale JS (1993) The ecology of insect overwintering. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Li C, Xie BY (1981) Effects of temperature and photoperiod on diapause of cotton bollworm, Helicoverpa armigera. Entomol Knowl 18:58–61

    CAS  Google Scholar 

  • Liu ZD, Gong PY, Wu KJ, Wei W, Sun JH, Li DM (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

    Article  CAS  Google Scholar 

  • Liu Z, Sun Y, Jia WM, Li BC (2010) Study on forecast of occurrence degree and emergence period for cotton bollworm on drip irrigation condition of north Xinjiang. Xinjiang Agric Sci 47(2):420–423

    Google Scholar 

  • Lu ZZ, Wang L, Zhang QH, Gong ZZ, Ding H (2006) Relationships between overwintering Agrotis segetum population and snow. Chin J Ecol 25(12):1532–1534

    Google Scholar 

  • Mackiewicz MC (2012) A new approach to quantifying soil temperature responses to changing air temperature and snow cover. Polar Sci 6:226–236

    Article  Google Scholar 

  • Marshall KE, Sinclair BJ (2012) The impacts of repeated cold exposure on insects. J Exp Biol 215:1607–1613

    Article  Google Scholar 

  • Mirondis GK, Stamopoulos DC, Savopoulou-Soultani M (2010) Over-wintering survival and spring emergence of Helicoverpa armigera (Lepidoptera: Noctuidae) in Northern Greece. Environ Entomol 39(4):1068–1084

    Article  Google Scholar 

  • Mironidis GK, Savopoulou-soultani M (2008) Development, survivorship, and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) under constant and alternating temperatures. Physiol Ecol 37(1):16–28

    CAS  Google Scholar 

  • Naes T, Martens H (1985) Comparison of prediction methods for multicollinearity data. Commun Stat Simul C 14:545–576

    Article  Google Scholar 

  • Nakai T, Takeda M (1995) Temperature and photoperiodic regulation of summer diapause and reproduction in Pyrrhalta humeralis (Coleoptera: Chrysomelidae). Appl Entomol Zool 30:295–301

    Google Scholar 

  • Ouyang F, Liu ZD, Yin J, Su JW, Wang CZ, Ge F (2011) Effects of transgenic Bt cotton on overwintering characteristics and survival of Helicoverpa armigera. J Insect Physiol 57:153–160

    Article  CAS  Google Scholar 

  • Ouyang F, Hui C, Ge S, Men XY, Zhao ZH, Shi PJ, Zhang YS, Li BL (2014) Weakening density dependence from climate change and agricultural intensification triggers pest outbreaks: a 37-year observation of cotton bollworms. Ecol Evol 4(17):3362–3374

    Article  Google Scholar 

  • Pan WW, Wei CZ, Ding Q, Fu J, Zhang YS (2009) Nitrogenous fertilizer recommendation model for cotton under mulch-drip irrigation. Plant Nutr Fert Sci 15(1):204–210

    CAS  Google Scholar 

  • Pauli JN, Zuckerberg B, Whiteman JP, Porter W (2013) The subnivium: a deteriorating seasonal refugium. Front Ecol Environ 11:260–267

    Article  Google Scholar 

  • Qi H, Song F (2003) A daily soil temperature dataset and soil temperature climatology of the contiguous United States. J Appl Meteorol Climatol 42:1139–1156

    Article  Google Scholar 

  • Rummel DR, Neece KC, Arnold MD, Lee BA (1986) Overwintering survival and spring emergence of Heliothis zea (Boddie) in the Texas southern high plain. Southwest Entomol 11:1–9

    Google Scholar 

  • Seyfried MS, Flerchinger GN, Murdock MD, Hanson CL, Van Vactor S (2001) Long term soil temperature database, Reynolds Creek Experimental Watershed, Idaho, United States. Water Resour Res 37:2843–2846

    Article  Google Scholar 

  • Sinclair BJ (2014) Linking energetics and overwintering in temperate insects. J Thermal Biol. doi:10.1016/j.jtherbio.2014.07.007i

    Google Scholar 

  • Slosser JE, Phillips JR, Herzog GA (1975) Overwintering survival and spring emergence of the bollworm in Arkansas. Environ Entomol 4:1015–1024

    Article  Google Scholar 

  • Sokratov SA, Barry RG (2001) Parameterization of an intra-seasonal variation in the thermo-insulation effect of snow cover on soil temperatures and energy balance. National Snow and Ice Data Center. http://www.breiling.org/snow/barrow.pdf

  • Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, New York

    Google Scholar 

  • Tenge AJ, Kaihura FBS, Lal R, Singh BR (1998) Diurnal soil temperature fluctuations for different erosional classes of an oxisol at Mlingano, Tanzania. Soil Till Res 49:211–217

    Article  Google Scholar 

  • Tennenhaus M (1998) PLS regression methods. J Chemo 211–228

  • Thorn CE, Schlyter JPL, Darmondy RG, Dixon JC (1999) Statistical relationships between daily and monthly air and shallow-ground temperatures in Karkevagge, Swedish Lapland. Permafr Periglac Process 10:317–330

    Article  Google Scholar 

  • Trumbore SE, Chadwick OA, Amundson R (1996) Rapid exchange between soil carbon and atmospheric carbon dioxide driven by temperature change. Science 272:393–395

    Article  CAS  Google Scholar 

  • Williams CM, Henry HAL, Sinclair BJ (2014) Cold truths: how winter drives responses of terrestrial organisms to climate change. Biol Rev. doi:10.1111/brv.12105

    Google Scholar 

  • Wu ZJ (1992) Relative analysis of change rule between soil moisture content in fields and change of number during Helicoverpa armigera (Hübner) pupae stage. KunChong ZhiShi 29(2):77–79

    Google Scholar 

  • Wu KM, Guo YY (1995) Factors for diapause induced in cotton bollworm, Helicoverpa armigera (Hübner). Acta Phytophy Sin 22:331–336

    Google Scholar 

  • Wu KM, Guo YY (1997) The influences of soil moisture content on emergence and cold hardiness of different geographical populations of cotton bollworm. Acta Phytoph Sin 24(2):142–146

    Google Scholar 

  • Yang YT, Wang DH, Zhu MH (1998) Relation between soil moisture and emergence of cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) and the effect of soil moisture on the occurrence of next generation. Acta Gossypii Sin 10:210–215

    Google Scholar 

  • Yang YT, Wang DH, Zhu MH (2001) Effects of soil characteristics on the occurrence of Helicoverpa armigera (Hübner) and its regional division. Acta Ecol Sin 21:959–963

    Google Scholar 

  • Zalucki MP, Daglish G, Firempong S, Twine PH (1986) The biology and ecology of Heliothis armigera (Hübner) and H. punctigera Wallengren (Lepidoptera: Noctuidae) in Australia: what do we know? Aust J Zool 34:779–814

    Article  Google Scholar 

  • Zalucki MP, Murray DAH, Gregg PC, Fitt GP, Twine PH, Jones C (1994) Ecology of Helicoverpa armigera (Hübner) and H. punctigera (Wallengren) in the inland of Australia: larval sampling and host plant relationships during winter and spring. Aust J Zool 42:329–346

    Article  Google Scholar 

  • Zhang T (2005) Influence of the seasonal snow cover on the ground thermal regime: an overview. Rev Geophys 43. doi:10.1029/2004RG000157

  • Zhang XW, Zhang JB (2006) Xinjiang meteorology manual [M]. Meteorology Publishing, Beijing

    Google Scholar 

  • Zhang XX, Wang YC, Geng JG, Shen JL (1980) Study on the outbreak factors of cotton bollworm, Helicoverpa armigera (Hübner)—relationship between soil moisture and pupation emergence. Entomol Knowl 17:9–13

    Google Scholar 

  • Zhang YS, Wang S, Barr AG, Black TA (2008) Impact of snow cover on soil temperature and its simulation in a boreal aspen forest. Cold Reg Sci Technol 52:355–370

    Article  Google Scholar 

  • Zhu XG (1979) Relationship between climate and occurrence of Helicoverpa armigera (Hübner) in catchment area in Yangzi River. China Cotton 2:35–39

    Google Scholar 

Download references

Acknowledgments

The work was supported by the National Natural Science Foundation of China (41275119) and the Desert Foundation of IDM, CMA (Sqj2012010).

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  1. Institute of Desert and Meteorology, China Meteorological Administration, Urumqi, 830002, China

    Jian Huang

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Correspondence to Jian Huang.

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Huang, J. Effects of soil temperature and snow cover on the mortality of overwintering pupae of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Int J Biometeorol 60, 977–989 (2016). https://doi.org/10.1007/s00484-015-1090-y

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  • DOI: https://doi.org/10.1007/s00484-015-1090-y

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