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Low temperature triggers physiological and behavioral shifts in adult oriental armyworm, Mythimna separata

Published online by Cambridge University Press:  13 January 2022

Fang Wang  and
Weixiang Lv Open the ORCID record for Weixiang Lv [Opens in a new window]
Fang Wang
Affiliation:
Key Laboratory of Southwest China Wildlife Resources Conservation, China West Normal University, Nanchong, China
Weixiang Lv*
Affiliation:
Key Laboratory of Southwest China Wildlife Resources Conservation, China West Normal University, Nanchong, China
*
Author for correspondence: Weixiang Lv, Email: [email protected]
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Abstract

Migratory insects display diverse behavioral strategies in response to external environmental shifts, via energy allocation of migration-reproduction trade-offs. However, how migratory insects distribute energy between migration and reproduction as an adaptive strategy to confront temporary low temperatures remains unclear. Here, we used Mythimna separata, a migratory cereal crop pest, to explore the effects of low temperature on reproductive performance, behavior, and energy allocation. We found that the influence of low temperatures on reproduction was not absolutely negative, but instead depended on the intensity, duration, and age of exposure to low temperature. Exposure to 6°C for 24 h significantly accelerated the onset of oviposition and ovarian development, and increased the synchrony of egg-laying and lifetime fecundity in 1-day-old adults compared to the control, while female's flight capacity decreased significantly on the first and second day after moths were exposed to 6°C. Furthermore, the abdominal and total triglycerides levels of females decreased significantly from exposure to low temperature, but their thoracic triglyceride content was significantly higher than the control on the third and fourth day. These results indicated that low temperatures induced M. separata to reduce energy investment for the development of flight system. This resulted in the shifting of moths from being migrants to residents during the environmental sensitive period (first day post-emergence). This expands our understanding of the adaptive strategy employed by migratory insects to deal with low temperatures and aids in the management of this pest species in China.

Keywords

Energy trade-offlow temperaturemigrationMythimna separatareproductiontriglyceride
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 4 , August 2022 , pp. 546 - 556
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Arrese, EL and Soulages, JL (2010) Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology 55, 207–225.CrossRefGoogle ScholarPubMed
Auerswald, L and Gäde, G (2000) Metabolic changes in the African fruit beetle, Pachnoda sinuata, during starvation. Journal of Insect Physiology 46, 343–351.CrossRefGoogle ScholarPubMed
Bertuso, AG, Morooka, S and Tojo, S (2002) Sensitive periods for wing development and precocious metamorphosis after precocene treatment of the brown planthopper, Nilaparvata lugens. Journal of Insect Physiology 48, 221–229.CrossRefGoogle ScholarPubMed
Chapman, JW, Reynolds, DR and Wilson, K (2015) Long-range seasonal migration in insects: mechanisms, evolutionary drivers and ecological consequences. Ecology Letters 18, 287–302.CrossRefGoogle ScholarPubMed
Chen, Q, Zhang, YD, Qi, XH, Xu, YW, Hou, YH, Fan, ZY, Shen, HL, Liu, D, Shi, XK, Li, SM, Du, Y and Wu, YQ (2019 a) The effects of climate warming on the migratory status of early summer populations of Mythimna separata (Walker) moths: a case–study of enhanced corn damage in central–northern China, 1980–2016. Ecology & Evolution 9, 12332–12123.CrossRefGoogle ScholarPubMed
Chen, YY, Zhang, W, Ma, G and Ma, CS (2019 b) More stressful event does not always depress subsequent life performance. Journal of Integrative Agriculture 18, 2321–2329.CrossRefGoogle Scholar
Cheng, YX, Luo, LZ, Jiang, XF and Sappington, TW (2012) Synchronized oviposition triggered by migratory flight intensifies larval outbreaks of beet webworm. PLoS ONE 7, e31562.CrossRefGoogle ScholarPubMed
Coombs, M, del Socorro, AP, Fitt, GP and Gregg, PC (1993) The reproductive maturity and mating status of Helicoverpa armigera, H. punctigera and Mythimna convecta (Lepidoptera: Noctuidae) collected in tower-mounted light traps in northern New South Wales, Australia. Bulletin of Entomological Research 83, 529–534.CrossRefGoogle Scholar
Crespo, JG, Goller, F and Vickers, NJ (2012) Pheromone mediated modulation of pre-flight warm-up behavior in male moths. Journal of Experimental Biology 215, 2203–2209.CrossRefGoogle ScholarPubMed
Crespo, JG, Vickers, NJ and Goller, F (2014) Male moths optimally balance take-off thoracic temperature and warm-up duration to reach a pheromone source quickly. Animal Behaviour 98, 79–85.CrossRefGoogle Scholar
Cusson, M, McNeil, JN and Tobe, SS (1990) In vitro biosynthesis of juvenile hormone by corpora allata of Pseudaletia unipuncta virgin females as a function of age, environmental conditions, calling behaviour and ovarian development. Journal of Insect Physiology 36, 139–146.CrossRefGoogle Scholar
Dingle, H (2014) Migration: The Biology of Life on the Move, 2nd Edn. New York: Oxford University Press.CrossRefGoogle Scholar
Duan, JJ, Weber, DC and Dorn, S (1998) Flight behavior of pre- and post-diapause apple blossom weevils in relation to ambient temperature. Entomologia Experimentaliset Applicata 88, 97–99.CrossRefGoogle Scholar
Foerster, LA, Doetzer, AK and de Castro, LCF (2004) Emergence, longevity and fecundity of Trissolcus basalis and Telenomus podisi after cold storage in the pupal stage. Pesquisa Agropecuaria Brasileira 39, 841–845.CrossRefGoogle Scholar
Gruntenko, NE, Bownes, M, Terashima, J, Sukhanova, MZ and Raushenbach, IY (2003) Heat stress affects oogenesis differently in wild-type Drosophila virilis and a mutant with altered juvenile hormone and 20-hydroxyecdysone levels. Insect Molecular Biology 12, 393–404.CrossRefGoogle Scholar
Guo, JW, Li, WP, Zhang, J, Liu, XD, Zhai, BP and Gao, H (2019 a) Cnaphalocrocis medinalis moths decide to migrate when suffering nutrient shortage on the first day after emergence. Insects 10, 364.CrossRefGoogle ScholarPubMed
Guo, JW, Yang, F, Li, P, Liu, XD and Zhai, BP (2019 b) Female bias in an immigratory population of Cnaphalocrocis medinalis moths based on field surveys and laboratory tests. Scientific Reports 9, 18388.CrossRefGoogle Scholar
Jiang, XF (2018) Regularity of population occurrence and migration in the oriental armyworm, Mythimna separata (Walker). Journal of Integrative Agriculture 17, 1482–1505.CrossRefGoogle Scholar
Jiang, XF and Luo, LZ (2005) Comparison of behavioral and physiological characteristics between the emigrant and immigrant populations of the oriental armyworm, Mythimna separata (Walker). Acta Entomologica Sinica 48, 61–67.Google Scholar
Jiang, XF, Cai, B, Luo, LZ, Cao, YZ and Liu, YQ (2003) Influences of temperature and humidity synthesize on flight capacity in the moth s of oriental armyworm, Mythimna separata (Walker). Acta Ecologica Sinica 23, 738–743.Google Scholar
Jiang, YY, Qu, XF, Xia, B and Zeng, J (2009) Rules for investigation and forecast of the armyworm [Pseudaletia (Mythimna) separata Walker]. National Standard of the People's Republic of China, Standards Press of China, Beijing.Google Scholar
Jiang, XF, Luo, LZ and Sappington, TW (2010) Relationship of flight and reproduction in beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae), a migrant lacking the oogenesis-flight syndrome. Journal of Insect Physiology 56, 1631–1637.CrossRefGoogle ScholarPubMed
Jiang, XF, Luo, LZ, Zhang, L, Sappington, TW and Hu, Y (2011) Regulation of migration in Mythimna separata (Walker) in China: a review integrating environmental, physiological, hormonal, genetic, and molecular factors. Environmental Entomology 40, 516–533.CrossRefGoogle Scholar
Jiang, YY, Li, CG, Zeng, J and Liu, J (2014) Population dynamics of the armyworm in China: a review of the past 60 years’ research. Chinese Journal of Applied Entomology 51, 890–898.Google Scholar
Johnson, CG (1969) Migration and Dispersal of Insects by Flight. London: Methuen.Google Scholar
King, AM and MacRae, TH (2015) Insect heat shock proteins during stress and diapause. Annual Review of Entomology 60, 59–75.CrossRefGoogle ScholarPubMed
Kingsolver, JG, Higgins, JK and Augustine, KE (2015) Fluctuating temperatures and ectotherm growth: distinguishing non-linear and time-dependent effects. Journal of Experimental Biology 218, 2218–2225.Google ScholarPubMed
Klockmann, M, Günter, F and Fischer, K (2017) Heat resistance throughout ontogeny: body size constrains thermal tolerance. Global Change Biology 23, 686–696.CrossRefGoogle ScholarPubMed
Lee, JH and Uhm, KB (1995) Migration of the oriental armyworm Mythimna separata in East Asia in relation to weather and climate. In Drake, VA and Gatehouse, AG (eds), Insect Migration. Cambridge, UK: Cambridge University Press, pp. 105–116.CrossRefGoogle Scholar
Levie, A, Vernon, P and Hance, T (2005) Consequences of acclimation on survival and reproductive capacities of cold-stored mummies of Aphidius rhopalosiphi (Hymenoptera: Aphidiinae). Journal of Economic Entomology 98, 704–708.CrossRefGoogle ScholarPubMed
Li, GB (1961) Regularity of occurrence and control strategy in the oriental armyworm Mythimna separata in China. In Luo, LZ (ed.), China Plant Protection Science. Beijing, China: Science Press, pp. 446–466.Google Scholar
Li, KB, Gao, XW, Luo, LZ, Yin, J and Cao, YZ (2005) Changes in the activities of four related enzymes during the flight of oriental armyworm, Mythimna separata (Walker). Acta Entomologica Sinica 48, 643–647.Google Scholar
Li, BL, Xu, XL, Ji, JY and Wu, JX (2018) Effects of constant and stage-specific-alternating temperature on the survival, development and reproduction of the oriental armyworm, Mythimna separata (Walker) (Lepidoptera: Noctuidae). Journal of Integrative Agriculture 17, 1545–1555.CrossRefGoogle Scholar
Liang, LN, Zhang, W, Ma, G, Hoffmann, A and Ma, CS (2014) A single hot event stimulates adult performance but reduces egg survival in the oriental fruit moth, Grapholitha molesta. PLoS ONE 9, e116339.CrossRefGoogle ScholarPubMed
Lorenz, MW (2007) Oogenesis flight syndrome in crickets: age dependent egg production, flight performance, and biochemical composition of the flight muscles in adult female Gryllus bimaculatus. Journal of Insect Physiology 53, 819–832.CrossRefGoogle ScholarPubMed
Luo, LZ, Li, GB, Cao, YZ and Hu, Y (1995) The influence of larval rearing density on flight capacity and fecundity of adult oriental armyworm, Mythimna separata (Walker). Acta Entomologica Sinica 38, 38–45.Google Scholar
Luo, LZ, Jiang, XF, Li, KB and Hu, Y (1999) Influences of flight on reproduction and longevity of the oriental armyworm, Mythimna separata (Walker). Acta Entomologica Sinica 2, 150–158.Google Scholar
Luo, LZ, Li, KB, Jiang, XF and Hu, Y (2001) Regulation of flight capacity and contents of energy substances by methoprene in the moths of Oriental armyworm, Mythimna separata (Walker). Acta Entomologica Sinica 8, 63–72.Google Scholar
Ma, CS, Ma, G and Pincebourde, S (2020) Survive a warming climate: insect responses to extreme high temperatures. Annual Review of Entomology 66, 8.1–8.22.Google ScholarPubMed
Murata, M and Tojo, S (2004) Flight capability and fatty acid level in triacylglycerol of long-distance migratory adults of the common cutworm. Spodoptera litura. Zoological Science 21, 181–188.CrossRefGoogle ScholarPubMed
Nakasuji, F and Nakano, A (1990) Flight activity and oviposition characteristics of the seasonal form of a migrant skipper, Parnara guttata (Lepidoptera: Hesperiidae). Researches on Population Ecology 32, 227–233.CrossRefGoogle Scholar
Nijhout, HF (1999) Control mechanisms of polyphenic development in insects. Bioscience 49, 181–192.CrossRefGoogle Scholar
Pineda, A, Dicke, MC, Pieterse, MJ and Pozo, MJ (2013) Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Functional Ecology 27, 574–586.CrossRefGoogle Scholar
Piyaphongkul, J, Pritchard, J and Bale, J (2012) Heat stress impedes development and lowers fecundity of the brown planthopper Nilaparvata lugens (Stl). PLoS ONE 7, e47413.CrossRefGoogle Scholar
Potter, KA, Davidowitz, G and Woods, HA (2011) Cross-stage consequences of egg temperature in the insect Manduca sexta. Functional Ecology 25, 548–556.CrossRefGoogle Scholar
Qin, JY, Zhang, L, Liu, YQ, Sappington, TW, Cheng, YX, Luo, LZ and Jiang, XF (2017) Population projection and development of the Mythimna loreyi as affected by temperature: application of an age-stage, two-sex life table. Journal of Economic Entomology 110, 1583–1591.CrossRefGoogle ScholarPubMed
Rankin, MA and Burchsted, JCA (1992) The cost of migration in insects. Annual Review of Entomology 1992, 533–559.CrossRefGoogle Scholar
Rhainds, M (2010) Female mating failures in insects. Entomologia Experimentalis Applicata 136, 211–226.CrossRefGoogle Scholar
Rinehart, JP, Yocum, GD and Denlinger, DL (2000) Thermotolerance and rapid cold hardening ameliorate the negative effects of brief exposures to high or low temperatures on fecundity in the flesh fly, Sarcophaga crassipalpis. Physiology Entomology 25, 330–336.CrossRefGoogle Scholar
Sappington, TW (2018) Migratory flight of insect pests within a year-round distribution: European corn borer as a case study. Journal of Integrative Agriculture 17, 1485–1505.CrossRefGoogle Scholar
Sharma, HC and Davies, JC (1983) The oriental armyworm, Mythimna separata (Wlk.) distribution, biology and control: a literature review. Miscellaneous report No 59. Wrights Lane, London: Overseas Development Administration.Google Scholar
Shirai, Y (2006) Flight activity, reproduction, and adult nutrition of the beet webworm, Spoladea recurvalis (Lepidoptera: Pyralidae). Applied Entomology and Zoology 41, 405–414.CrossRefGoogle Scholar
Tezze, AA and Botto, EN (2004) Effect of cold storage on the quality of Trichogramma nerudai (Hymenoptera: Trichogrammatidae). Biological Control 30, 11–16.CrossRefGoogle Scholar
Thornhill, R and Alcock, J (1983) The Evolution of Insect Mating Systems. Cambridge, MA: Harvard University Press.CrossRefGoogle Scholar
Turnock, WJ and Fields, PG (2005) Winter climates and coldhardiness in terrestrial insects. European Journal of Entomology 102, 561–576.CrossRefGoogle Scholar
Wang, FY, Zhang, XX and Zhai, BP (2010) Flight and re-migration capacity of the rice leaf folder moth, Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Crambidae). Acta Entomologica Sinica 53, 1265–1272.Google Scholar
Yu, JZ, Chi, H and Chen, BH (2013) Comparison of the life tables and predation rates of Harmonia dimidiata (F.) (Coleoptera: Coccinellidae) fed on Aphis gossypii Glover (Hemiptera: Aphididae) at different temperatures. Biological Control 64, 1–9.CrossRefGoogle Scholar
Zeng, J, Jiang, YY and Liu, J (2013) Analysis of the armyworm outbreak in 2012 and suggestions of monitoring and forecasting. Journal of Plant Protection 39, 117–121.Google Scholar
Zhang, ZT and Li, GB (1985) A study on the flight characteristics of the oriental armyworm, Mythimna separata (Walker). Acta Phytotaxonomica Sinica 12, 93–100.Google Scholar
Zhang, L, Luo, LZ, Jiang, XF and Hu, Y (2006) Influences of starvation on the first day after emergence on ovarian development and flight potential in adults of the oriental armyworm, Mythimna separata (Walker) (Lepidopterea: Noctuidae). Acta Entomologica Sinica 49, 895–902.Google Scholar
Zhang, L, Luo, LZ and Jiang, XF (2008 a) Starvation influences allatotropin gene expression and juvenile hormone titer in the female adult oriental armyworm, Mythimna separata. Archives of Insect Biochemistry Physiology 68, 63–70.CrossRefGoogle ScholarPubMed
Zhang, L, Jiang, XF and Luo, LZ (2008 b) Determination of sensitive stage for switching migrant oriental armyworms into residents. Environmental Entomology 37, 1389–1395.CrossRefGoogle ScholarPubMed
Zhang, L, Pan, P, Sappington, TW, Lu, WX, Luo, LZ and Jiang, XF (2015 a) Accelerated and synchronized oviposition induced by flight of young females may intensify larval outbreaks of the rice leaf roller. PLoS ONE 10, e0121821.CrossRefGoogle ScholarPubMed
Zhang, W, Rudolf, V and Ma, CS (2015 b) Stage-specific heat effects: timing and duration of heat waves alter demographic rates of a global insect pest. Oecologia 179, 947–57.CrossRefGoogle ScholarPubMed
Zhang, L, Cheng, LL, Chapman, JW, Sappington, TW, Liu, JJ, Cheng, YX and Jiang, XF (2020) Juvenile hormone regulates the shift from migrants to residents in adult oriental armyworm, Mythimna separata. Scientific Reports 10, 11626.CrossRefGoogle ScholarPubMed
Zhao, XC, Feng, HQ, Wu, B, Wu, XF, Liu, ZF, Wu, KM and McNeil, JN (2009) Does the onset of sexual maturation terminate the expression of migratory behaviour in moths? A study of the oriental armyworm, Mythimna separata. Journal of Insect Physiology 55, 1039–1043.CrossRefGoogle ScholarPubMed
Zhao, F, Hoffmann, AA, Xing, K and Ma, CS (2017) Life stages of an aphid living under similar thermal conditions differ in thermal performance. Journal of Insect Physiology 99, 1–7.CrossRefGoogle ScholarPubMed
Zhou, Z, Guo, J, Chen, H and Wan, F (2010) Effects of temperature on survival, development, longevity, and fecundity of Ophraella communa (Coleoptera: Chrysomelidae), a potential biological control agent against Ambrosia artemiiifolia (Asterales: Asteraceae). Environmental Entomology 39, 1021–1027.CrossRefGoogle ScholarPubMed