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Climate change favours a destructive agricultural pest in temperate regions: late spring cold matters

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Abstract

Global climate change has profound consequences on survival and reproduction of arthropods. In particular, in temperate regions changes in spring temperatures have a major impact on crop pest population dynamics, but the mechanisms remain elusive. By analysing empirical data of Helicoverpa armigera moth populations from three sites over 12–13 years in northwestern China, and running modelling (DYMEX software), we intended to clarify how the late spring cold (LSC) events affect the populations of this destructive pest species. We then explored the relationships between LSC parameters and moth population dynamics using model simulations. Our results highlight the importance of LSC in driving H. armigera population dynamics. Of the LSC parameters tested, the duration of LSC measured as the maximum continuous days with a minimum temperature lower than 10 °C (MCDL) was a key factor influencing the population abundance of the spring and summer generations. Furthermore, the model showed that the timing of the LSC event had a major effect on how the MCDL influenced each generation. The timing with respect to the eclosion of the overwintering generation was critical, and it determined the variation in the abundance of the first and subsequent generations. Our findings imply that the abundance of H. armigera will increase as the frequency and duration of LSC events decrease under global spring warming. Incorporating the duration and timing of LSC events into decision-making should improve forecasting H. armigera abundance and other insect species under global climate change and better inform pest management.

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References

  • An J, Choi S (2013) The role of winter weather in the population dynamics of spring moths in the southwest Korean peninsula. J Asia-Pac Entomol 16:49–53

    Article  Google Scholar 

  • Bale JS, Hayward SAL (2010) Insect overwintering in a changing climate. J Exp Biol 213:980–994

    Article  PubMed  CAS  Google Scholar 

  • Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lem4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Core Team R (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Dell D, Sparks TH, Dennis RL (2005) Climate change and the effect of increasing spring temperatures on emergence dates of the butterfly Apatura iris (Lepidoptera: Nymphalidae). Eur J Entomol 102:161–167

    Article  Google Scholar 

  • Dong L-L, Li Q-Q, Ding Y-H (2015) Spatial and temporal characteristics of air temperature over China in spring under the background of global warming. Meteorol Mon 41:1177–1189

    Google Scholar 

  • Forrest JRK (2016) Complex responses of insect phenology to climate change. Curr Opin Insect Sci 17:49–54

    Article  PubMed  Google Scholar 

  • Gu S-M, Zalucki MP, Zhang B, Liu Y-J et al (2017) Simulation modelling the population dynamics of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) using DYMEX. Plant Prot 43:17–28

    Google Scholar 

  • Hallett RH, Goodfellow SA, Weiss RM, Olfert O (2009) MidgEmerge, a new predictive tool, indicates the presence of multiple emergence phenotypes of the overwintered generation of swede midge. Entomol Exp Appl 130:81–97

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 5:346–363

    Article  Google Scholar 

  • Huang J (2015) 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

    Article  PubMed  Google Scholar 

  • Huang J, Li J (2017) Spring phenology of cotton bollworm affects wheat yield. Ecol Evol 7:1078–1090

    Article  PubMed  PubMed Central  Google Scholar 

  • Ju RT, Gao L, Wei SJ, Li B (2017) Spring warming increases the abundance of an invasive specialist insect: links to phenology and life history. Sci Rep UK 7:14805

    Article  CAS  Google Scholar 

  • Keenan TF (2015) Phenology: Spring greening in a warming world. Nature 526:48–49

    Article  PubMed  CAS  Google Scholar 

  • Kim Y, Kimball JS, Zhang K, McDonald KC (2012) Satellite detection of increasing Northern Hemisphere non-frozen seasons from 1979 to 2008: implications for regional vegetation growth. Remote Sens Environ 121:472–487

    Article  Google Scholar 

  • Kriticos DJ, Ota N, Hutchison WD, Beddow JM et al (2015) The potential distribution of invading Helicoverpa armigera in North America: is it just a matter of time? PLoS ONE. https://doi.org/10.1371/journal.pone.0119618

    Article  PubMed  PubMed Central  Google Scholar 

  • Leather SR (1994) The effect of temperature on oviposition, fecundity and egg hatch in the pine beauty moth, Panolis flammea (Lepidoptera: Noctuidae). B Entomol Res 84:515–520

    Article  Google Scholar 

  • Li C, Li S-Q, Guo B-F (1987) Studies on the temperature threshold of cotton bollworm development in varying temperature. Acta Entomol Sin 30:253–258

    Google Scholar 

  • Li Z-Y, Zalucki MP, Yonow T, Kriticos DJ et al (2016) Population dynamics and management of diamondback moth (Plutella xylostella) in China: the relative contributions of climate, natural enemies and cropping patterns. B Entomol Res 106:197–214

    Article  CAS  Google Scholar 

  • Lu Z-Z, Baker G (2013) Spatial and temporal dynamics of Helicoverpa armigera (Lepidoptera, Noctuidae) in contrasting agricultural landscape in northwestern China. Int J Pest Manag 59:25–34

    Article  Google Scholar 

  • Lu Z-Z, Zalucki MP, Perkins LE, Wang D-Y et al (2013) Towards a resistance management strategy for Helicoverpa armigera in Bt-cotton in Northwestern China: an assessment of potential refuge crops. J Pest Sci 5:695–703

    Article  Google Scholar 

  • Magiafoglou A, Hoffmann AA (2003) Cross-generation effects due to cold exposure in Drosophila serrata. Funct Ecol 5:664–672

    Article  Google Scholar 

  • Maywald GF, Sutherst RW, Zalucki MP (1998) DYMEX—general modelling in entomology. In: 6th Australian applied entomological research conference. Univ Queensland, Brisbane, Australia. Pest management—future challenges, vols 1 and 2, proceedings. A325–A325

  • Meiners T, Barbara R, Elisabeth O (2006) Oviposition at low temperatures—late season negatively affects the leaf beetle Galeruca tanaceti (Coleoptera: Galerucinae) but not its specialised egg parasitoid Oomyzus galerucivorus (Hymenoptera: Eulophidae). Eur J Entomol 103:765–770

    Article  Google Scholar 

  • Miao W, Guo Z-Y, Lu Z-Z et al (2006) Estimation of generations of Helicoverpa armigera (Hübner) and Aphis gossypii (Glover) in Xinjiang Based on single sine model. Xinjiang Agr Sci 43:186–188

    Google Scholar 

  • Mironidis GK (2014) Development, survivorship and reproduction of Helicovpera armigera (Lepidoptera: Noctuidae) under fluctuating temperatures. B Entomol Res 104:751–764

    Article  Google Scholar 

  • Mironidis GK, Soultani MS (2008) Development, survivorship and reproduction of Helicovpera armigera (Lepidoptera: Noctuidae) under constant and alternating temperatures. Environ Entomol 37:16–28

    Article  PubMed  CAS  Google Scholar 

  • Mockett RJ, Matsumoto Y (2014) Effect of prolonged coldness on survival and fertility of Drosophila melanogaster. PLoS ONE. https://doi.org/10.1371/journal.pone.0092228

    Article  PubMed  PubMed Central  Google Scholar 

  • Morin X, Ameglio T, Ahas R, Kurzbesson C et al (2007) Variation in cold hardiness and carbohydrate concentration from dormancy induction to bud burst among provenances of three European oak species. Tree Physiol 27:817–825

    Article  PubMed  CAS  Google Scholar 

  • Noor-ul-Ane M, Ali Mirhosseini M, Crickmore N, Saeed S et al (2017) Temperature-dependent development of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) and its larval parasitoid, Habrobracon hebetor (Say) (Hymenoptera: Braconidae): implications for species interactions. B Entomol Res 108:295–304

    Article  Google Scholar 

  • Ouyang F, Hui C, Men X-Y, Zhang Y-S et al (2016) Early eclosion of overwintering cotton bollworm moths from warming temperature accentuates yield loss in wheat. Agr Ecosyst Environ 217:89–98

    Article  Google Scholar 

  • Piao S-L, Tan J-G, Chen A-P, Fu YH et al (2015) Leaf onset in the northern hemisphere triggered by daytime temperature. Nat Commun. https://doi.org/10.1038/ncomms7911

    Article  PubMed  PubMed Central  Google Scholar 

  • Reddy GVP, Shi P-J, Hui C, Ge F et al (2015) The seesaw effect of winter temperature change on the recruitment of cotton bollworms Helicoverpa armigera through mismatched phenology. Ecol Evol 5:5652–5661

    Article  PubMed  PubMed Central  Google Scholar 

  • Regniere J, Nealis VG (2018) Two side of a coin: host-plant synchrony fitness trade-offs in the population dynamics of the western spruce budworm. Insect Sci 25:117–126

    Article  PubMed  Google Scholar 

  • Rinehart JP, Yocum GD, West M, Kemp WP (2011) A fluctuating thermal regime improves survival of cold-mediated delayed emergence in developing megachile rotundata (Hymenoptera: Megachilidae). J Econ Entomol 104:1162–1166

    Article  PubMed  Google Scholar 

  • Roland J, Matter SF (2016) Pivotal effect of early-winter temperatures and snowfall on population growth of alpine Parnassius smintheus butterflies. Ecol Monogr 86:412–428

    Article  Google Scholar 

  • Satake A, Ohgushi T, Urano S, Uchimura K (2006) Modeling population dynamics of a tea pest with temperature-dependent development: predicting emergence timing and potential damage. Ecol Res 21:107–116

    Article  Google Scholar 

  • Sato Y, Sato S (2015) Spring temperature predicts the long-term molting phenology of two cicadas, Cryptotympana facialis and Graptopsaltria nigrofuscata (Hemiptera: Cicadidae). Annu Entomol Soc Am 108:494–500

    Article  Google Scholar 

  • Takeda K, Musolin DL, Fujisaki K (2010) Dissecting insect responses to climate warming: overwintering and post-diapause performance in the southern green stink bug, Nezara viridula, under simulated climate-change conditions. Physiol Entomol 35:343–353

    Article  Google Scholar 

  • Tay WT, Soria MF, Walsh T et al (2013) A brave new world for an old world pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS ONE. https://doi.org/10.1371/journal.pone.0080134

    Article  PubMed  PubMed Central  Google Scholar 

  • Uelmen JA, Lindroth RL, Tobin PC, Reich PB et al (2016) Effects of winter temperatures, spring degree-day accumulation, and insect population source on phonological synchrony between forest tent caterpillar and host trees. Forest Ecol Manag 362:241–250

    Article  Google Scholar 

  • Visser ME, Holleman LJM (2001) Warmer springs disrupt the synchrony of oak and winter moth phenology. Proc R Soc B Biol Sci 268:289–294

    Article  CAS  Google Scholar 

  • Wagenhoff E, Wagenhoff A, Blum R, Veit H et al (2014) Does the prediction of the time of egg hatch of Thaumetopoea processionea (Lepidoptera: Notodontidae) using a frost day/temperature sum model provide evidence of an increasing temporal mismatch between the time of egg hatch and that of budburst of Quercus robur due to recent global warming? Eur J Entomol 111:207–215

    Google Scholar 

  • Wang G-C, Song R-N, Bo Z-H, Wang X-L (2010) Analysis on causes for “Late Spring Clodness” in Dalian 2008. Meteorol Environ Res 1:61–63

    Google Scholar 

  • Wang T, Ottle C, Peng S-S, Janssens IA et al (2014) The influence of local spring temperature variance on temperature sensitivity of spring phenology. Glob Change Biol 20:1473–1480

    Article  Google Scholar 

  • Wang C, Cao R-Y, Chen J, Rao Y-H et al (2015a) Temperature sensitivity of spring vegetation phenology correlates to within-spring warming speed over the Northern Hemisphere. Ecol Indic 50:62–68

    Article  Google Scholar 

  • Wang H-J, Ge Q-S, Rutishauser T, Dai Y-X et al (2015b) Parameterization of temperature sensitivity of spring phenology and its application in explaining diverse phenological responses to temperature change. Sci Rep UK. https://doi.org/10.1038/srep08833

    Article  Google Scholar 

  • Wu K-C, Chen Y-P, Li M-H (1980) Influence of temperature on the growth of laboratory population of the cotton bollworm, Helithis armigera (Hübner). Acta Entomol Sin 23:358–368

    Google Scholar 

  • Wu G, Chen F-J, Ge F (2006) Response of multiple generations of cotton bollworm Helicoverpa armigera Hübner, feeding on spring wheat, to elevated CO2. J Appl Entomol 130:2–9

    Article  Google Scholar 

  • Wu K-J, Gong P-Y, Ruan Y-M (2009) Estimating developmental rates of Helicoverpa armigera (Lepidoptera: Noctuidae) pupae at constant and alternating temperature by nonlinear models. Acta Entomol Sin 52:640–650

    Google Scholar 

  • Yonow T, Zalucki MP, Sutherst RW, Dominiak BC et al (2004) Modelling the population dynamics of the Queensland fruit fly, Bactrocera (Dacus) tryoni: a cohort-based approach incorporating the effects of weather. Ecol Model 173:9–30

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Zhang J, Ma J-H, Lu Y, Wang P-L et al (2013) Long-term dynamic change of Helicoverpa armigera (Hübner) population in Bt Cotton-growing areas in south Xinjiang. Arid Zone Res 30:520–526

    Google Scholar 

  • Zhang B, Peng Y, Zhao X-J, Hoffmann AA et al (2016) Emergence of the overwintering generation of peach fruit moth (Carposina sasakii) depends on diapause and spring soil temperatures. J Insect Physiol 86:32–39

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank local plant protection stations of agricultural department for their valuable fieldwork and collection of monitoring data. We thank anonymous reviewers for their valuable comments. This study was supported by the “International collaborative program of the Ministry of Scientific and Technology of the People’s Republic of China” (No. 2011DFA33170), the Thousand Youth Talents plan of China (Y772101001) and Main Service Project of Characteristic Institute, Chinese Academy of Sciences (TSS-2015-014-FW-1-4).

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Authors and Affiliations

  1. Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Ürümqi, 830011, China

    Shimin Gu, Peng Han & Zhaozhi Lu

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Shimin Gu & Peng Han

  3. State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Ürümqi, 830011, China

    Shimin Gu & Zhaozhi Lu

  4. CAS Research Center for Ecology and Environment of Central Asia, Chinese Academy of Sciences, Ürümqi, 830011, China

    Shimin Gu & Zhaozhi Lu

  5. Institute of Ecology, University of Innsbruck, 6020, Innsbruck, Austria

    Zhengpei Ye

  6. School of Biological Sciences, The University of Queensland, 4072, Brisbane, Australia

    Lynda E. Perkins & Myron P. Zalucki

  7. Plant Protection Station of Xinjiang Uyghur Autonomous Region, Ürümqi, 830049, China

    Jing Li & Huiqing Wang

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  1. Shimin Gu
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Correspondence to Zhaozhi Lu.

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Gu, S., Han, P., Ye, Z. et al. Climate change favours a destructive agricultural pest in temperate regions: late spring cold matters. J Pest Sci 91, 1191–1198 (2018). https://doi.org/10.1007/s10340-018-1011-z

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  • DOI: https://doi.org/10.1007/s10340-018-1011-z

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