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Effects of climate change on overwintering pupae of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

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Abstract

Climate change significantly affects insects’ behaviors. Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) is one of the most serious insect pests in the world. Much is known about the survival of the overwintering population and spring emergence of H. armigera. However, little is known about the effects of climate change on overwintering and spring emergence of H. armigera. This study investigated the effects of changes of air and soil temperatures and precipitation on overwintering pupae of H. armigera by analyzing historical data from Magaiti County in northwest China using statistical methods. The results showed that during the period of 1989–2006, the climate warming advanced the first-appearance date of overwintering pupae eclosion (FD) and end date of overwintering pupae eclosion (ED) by 1.276 and 0.193 days per year, respectively; the duration between the FD and ED (DFEPE) was prolonged by 1.09 days per year, which resulted in more eclosion of overwintering pupae. For a 1 °C increase in the maximum air temperature (T max) in winter, the FD became earlier by 3.234 days. Precipitation in winter delayed the FD and ED and produced little relative influence on DFEPE. A 1-mm increase of precipitation in winter delayed the FD and ED by 0.850 and 0.494 days, respectively. Mean air temperature (T mean) in March, with a 41.3 % relative influence, precipitation in winter, with a 49.0 % relative influence, and T mean in March, with a 37.5 % relative influence, were the major affecting factors on FD, ED, and DFEPE, respectively. T max in February with a 53.0 % relative influence was the major affecting factor on the mortality of overwintering pupae (MOP). Increased soil temperatures in October and November and autumn and air temperatures in winter could decrease the MOP, though the relative influences were lower than T max in February. Increased precipitation in winter increased the MOP, but the relative influence was only 4.2 % because of little precipitation. T mean in October had the greatest influence on the pre-wintering density of pupae (PDP). Increasing soil temperatures in October, November, and autumn increased PDP. A higher PDP increased overwintering survival and advanced FD and prolonged DFEPE. The overwintering boundary air temperatures of H. armigera should be expanded due to higher soil temperature and snow covering. Thus, climate warming helped to enhance the survival of overwintering pupae.

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References

  • 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 

  • Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, Butterfield J, Buse A, Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press MC, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Chang Biol 8(1):1–16

    Article  Google Scholar 

  • Bai ZG, Shen CL, Ma ZF (2004) Characteristic and applied technology of Jiaduo new type monitoring and predicting lamp for pests. China Plant Prot 24(12):32–33

    Google Scholar 

  • Caron RE, Bradley JR, Pleasants RH, Rabb RL, Stinner RE (1978) Overwintering survival of Heliothis zea produced on late-planted field corn in North Carolina. Environ Entomol 7:193–196

    Article  Google Scholar 

  • Carrillo MA, Heimpel GE, Moon RD, Cannon CA, Hutchison WD (2005) Cold hardiness of Habrobracon hebetor (Say) (Hymenoptera: Braconidae), a parasitoid of pyralid moths. J Insect Physiol 51:759–768

    Article  CAS  Google Scholar 

  • Cheng SL (1988) Agricultural meteorology and regionalization in Hebei province. Meteorological Publishing House, Beijing

    Google Scholar 

  • Danilevskii AS (1965) Photoperiodism and seasonal development of insects. Oliver & Boyd, London.

  • Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci U S A 105(18):6668–6672

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Duffield S (2004) Evaluation of the risk of overwintering Helicoverpa spp. pupae under irrigated summer crops in south-eastern Australia and the potential for area-wide management. Ann Appl Biol 144:17–26

    Article  Google Scholar 

  • Duffield SJ, Dillon ML (2005) The emergence and control of overwintering Helicoverpa armigera pupae in southern New South Wales. Aust J Entomol 44:316–320

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Feng DQ (2006) Reconsideration on photoperiod theory of insect diapause. Entomol East China 15(3):215–220

    CAS  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Fitt GP, Daly JC (1990) Abundance of overwintering pupae and the spring generation of Helicoverpa spp. (Lepidoptera: Noctuidae) in northern New South Wales, Australia: implications for pest management. J Econ Entomol 83:1827–1836

    Article  Google Scholar 

  • Franco A, Hill J, Kitschke C, Collingham Y, Roy DB (2006) Impacts of climate warming and habitat loss on extinctions at species’ low-latitude range boundaries. Global Chang Biol 12(8):l545–l1553

    Article  Google Scholar 

  • Fye RE (1978) Pupation preferences of bollworms, tobacco budworms, and beet armyworms and impact on mortality resulting from cultivation of irrigated cotton. J Econ Entomol 71:570–572

    Article  Google Scholar 

  • Ge F, Chen FJ, Parajulee MN, Yardim EN (2005) Quantification of diapausing fourth generation and suicidal fifth generation cotton bollworm, Helicoverpa armigera, in cotton and corn in northern China. Entomol Exp Appl 116:1–7

    Article  Google Scholar 

  • Graham HM, Fife LC (1972) Over-wintering of Heliothis spp. in the Lower Rio Grande valley, Texas. J Econ Entomol 65:708–711

    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 

  • 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

  • Kiritani K (2006) Predicting impacts of global warming on population dynamics and distribution of arthropods in Japan. Popul Ecol 48:5–12

    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 

  • Li C, Li SQ, Guo BF (1987) Studies of the temperature threshold of cotton bollworm development in varying temperature environments. Acta Entomol Sin 30(3):253–258

    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 

  • Li YP, Goto M, Ito S, Sato K, Sasaki Goto N (2001) Physiology of diapause and cold hardiness in the overwintering pupae of the fall webworm Hyphantria cunea (Lepidoptera: Arctiidae) in Japan. J Insect Physiol 47:1181–1187

    Article  CAS  Google Scholar 

  • Liu YF, Gu DX (1997) An analysis of occurrence trend of crop pests with warming climate in China. Nat Enemies Insects 19(2):93–96

    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 ZD, Gong PY, Heckel DG, Wei W, Sun JH, Li DM (2009) Effects of larval host plants on overwintering physiological dynamics and survival of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). J Insect Physiol 55:1–9

    Article  CAS  Google Scholar 

  • Lu ZQ, Xu YH (1998) The consideration with the incessant outbreak of the cotton bollworm, Helicoverpa armigera (Hübner). Entomol Knowl 35:132–136

    Google Scholar 

  • Lynch M, Gabriel W (1987) Environmental tolerance. Am Nat 129:283–303

    Article  Google Scholar 

  • Meng HL, Chang GS, Ren SZ (1962) A further studies on the cotton bollworm, Heliothis armigera (Hübner). Acta Entomol Sin 11(1):71–82

    Google Scholar 

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

    CAS  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 

  • Murray DAH (1991) Investigations into the development and survival of Heliothis spp. pupae in South-East Queensland. PhD Thesis, University of Queensland

  • 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 

  • Parmesan C (1996) Climate and species’ range. Nature 382:765–766

    Article  CAS  Google Scholar 

  • Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Global Chang Biol 13(9):1860–1872

    Article  Google Scholar 

  • Parmesan C, Ryrholm N, Stefanescu C, Hill JK, Thomas CD, Descimon H, Huntley B, Kaila L, Kullberg J, Tammaru T, Tennent WJ, Thomas JA, Warren M (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399(6736):579–583

    Article  CAS  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421(6918):37–42

    Article  CAS  Google Scholar 

  • Parajulee MN, Rummel DR, Arnold MD, Carroll SC (2004) Long-term seasonal abundance of Helicoverpa zea and Heliothis virescens (Lepidoptera: Noctuidae) moths in the Texas High Plains. J Econ Entomol 97:668–677

    Article  CAS  Google Scholar 

  • Parencia CR Jr (1964) Winter survival of the bollworm in central Texas. J Econ Entomol 57:757–758

    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 

  • Satake A, Ohgushi T, Urano S, Uehimura K (2006) Modeling population dynamics of a tea pest with temperature-dependent development: predicting emergence timing and potential damage. Ecol Res 21(1):l07–l16

    Article  Google Scholar 

  • Sheng CF (1993) The imperfect fifth generation cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) occurring in the north Northern China in 1992. Entomol Knowl 30:47

    Google Scholar 

  • Shimizu K, Shimizu K, Fujisaki K (2006) Timing of diapause induction and overwintering success in the cotton bollworm Helicoverpa armigera (Hb.) (Lepidoptera: Noctuidae) under outdoor conditions in temperate Japan. Appl Entomol Zool 41(1):151–159

    Article  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 

  • Stadelbacher EA, Pfrimmer TR (1972) Winter survival of the bollworm at Stoneville, Mississippi. J Econ Entomol 65:1030–1034

    Google Scholar 

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

    Google Scholar 

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

  • Uvarov BP (1931) Insect and Climate. Trans Entomol Soc, London, p 1–232

  • Westgarth-Smith AR, Leroy SAG, Collins PEF, Harrington R (2007) Temporal variations in English populations of a forest insect pest, the green spruce aphid (Elatobium abietinum), associated with the North Atlantic Oscillation and global warming. Quatern Int 173:153–160

    Article  Google Scholar 

  • Wilson AGL, Lewis T, Cunningham RB (1979) Overwintering and spring emergence of Heliothis armigera (Lepidoptera: Noctuidae) in the Naomi Valley, New South Wales, Australia. B Entomol Res 69:97–110

    Article  Google Scholar 

  • Worland MR (2005) Factors that influence freezing in the sub-Antarctic springtail Tullbergia antarctica. J Insect Physiol 51:881–894

    Article  CAS  Google Scholar 

  • Wu KJ, Chen YP, Li MH (1978) Life tables for experimental populations of the cotton bollworm, Heliothis armigera (Hübner), at different temperatures. Acta Entomol Sin 21(4):385–392

    Google Scholar 

  • Wu KM, Chen DF, Xiu G, Zhai BP, Guo YY (2001) Radar observation of autumn migration of insects in Northern China. Acta Ecol Sin 21(11):1833–1838

    Google Scholar 

  • Wu KJ, Gong PY (1984) Respiratory metabolism of the cotton bollworm, Heliothis armigera (Hübner). Acta Entomol Sin 27(2):128–135

    Google Scholar 

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

    Google Scholar 

  • Wu KM, Guo YY (1996) Investigation on the migration and diapause in Helicoverpa armigera—diapause termination and emergence pattern in Helicoverpa armigera. Sci Agric Sin 29(1):15–20

    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 Phytophys Sin 24(2):142–146

    Google Scholar 

  • Wu KM, Guo YY (2000) On the cold hardiness of cotton bollworm populations from Xinjiang Uygur Autonomous Region. Acta Phytophys Sin 27(1):23–26

    Google Scholar 

  • Wu KM, Guo YY, Wei FJ, Sun FZ (1997) On the cold hardiness of cotton bollworm, Helicoverpa armigera (Hübner). Acta Ecol Sin 17(3):298–302

    Google Scholar 

  • Wu KM, Guo YY, Wu Y (2002) Ovarian development of adult females of cotton bollworm and its relation to migratory behavior around Bohai Bay of China. Acta Ecol Sin 22(7):1075–1078

    Google Scholar 

  • Wu KM, Lu YH, Feng HQ, Jiang YY, Zhao JZ (2008) Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 321(5896):1676–1678

    Article  CAS  Google Scholar 

  • Wu KM, Zhai BP, Feng HQ, Chen DF, Guo YY (2006) Radar observations on the migratory behavior of the second generation cotton bollworm moths in the north part of northern China. Acta Phytophyl Sin 33(2):163–167

    Google Scholar 

  • Ye LF, Fu X, Ge F (2011) Contribution of C3 and C4 host plants for the overwintering and 1st generation of Helicoverpa armigera (Hübner) in northern China. Acta Ecol Sin 31(2):449–454

    Google Scholar 

  • Zalucki MP, Furlong MJ (2005) Forecasting Helicoverpa populations in Australia: a comparison of regression based models and a bioclimatic based modelling approach. Insect Sci 12:45–56

    Article  Google Scholar 

  • Zhai BP (2004) Computing the day length for programming insect behavior. Entomol Knowl 41(2):178–184

    Google Scholar 

  • Zhang JH, Li YC (2000) Analysis of overwintering weather indexes of Helicoverpa armigera in Xinjiang. Meteorol Mon 14:50–52

    Google Scholar 

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

  • 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 XX, Zhen ZQ, Xie JY, Mi XY (1998) Preliminary studies on facultative migration of cotton bollworm in China. Plant Prot Technol Ext 18(3):3–5

    CAS  Google Scholar 

  • Zhen ZQ, Zhang XX, Xie JY, Mi XY (2000) Flight capacity and facultative migration of cotton bollworm. Chin J Appl Ecol 11(4):603–608

    Google Scholar 

  • Zhou XF, Applebaum SW, Coll M (2000) Overwintering and spring migration in the bollworm Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Israel. Environ Entomol 29:1289–1294

    Article  Google Scholar 

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Acknowledgments

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

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

    Jian Huang

  2. Xinjiang Plant Protection Station, Urumqi, 830006, China

    Jing Li

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Huang, J., Li, J. Effects of climate change on overwintering pupae of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Int J Biometeorol 59, 863–876 (2015). https://doi.org/10.1007/s00484-014-0903-8

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