Flight activity promotes reproductive processes in the fall armyworm, Spodoptera frugiperda

doi:10.1016/S2095-3119(20)63204-X

摘要/Abstract

摘要：

草地贪夜蛾属鳞翅目夜蛾科，自2016年以来相继入侵非洲和亚洲多地，对世界粮食生产安全构成严重威胁。远距离迁飞和较强的生殖能力是其种群快速扩张的生物学基础，但目前对其飞行与生殖间的相互关系研究较少。本文利用飞行磨吊飞模拟草地贪夜蛾的飞行活动，研究了草地贪夜蛾飞行后对其生殖活动的影响。结果表明与对照组（未飞行）相比，1-3日龄草地贪夜蛾飞行10 h后产卵前期均显著缩短，产卵同步性显著增强，产卵量、产卵历期和交配率等生殖参数没有显著差异；2日龄草地贪夜蛾飞行时间超过2.5 h后，与对照相比产卵前期显著缩短，产卵同步性显著增强，产卵量、产卵历期、交配率等生殖参数没有显著差异。另外，通过解剖雌、雄蛾的生殖系统发现，1日龄草地贪夜蛾经历5 h吊飞处理后，卵巢和精巢的发育速度明显加快。这些结果表明合适的飞行活动显著促进草地贪夜蛾的生殖进程，这增加了我们对其迁飞生物学与区域暴发关系的相关认识，有助于阐明草地贪夜蛾的爆发机制以及预测其发生为害趋势。

Abstract:

The fall armyworm (FAW), Spodoptera frugiperda (Lepidoptera: Noctuidae), has invaded many countries in Africa and Asia since 2016, posing a major threat to world food security. Long-distance migration and strong reproductive ability form the biological basis of its rapid population expansion, but the relationship between the flight and reproduction of FAW has not been studied in depth. Here, an empirical assessment of this relationship in an invasive FAW population in China found that 1–3-day-old adults which had undergone 10-h tethered flights had a significantly shorter pre-oviposition period and greater oviposition synchronization, but did not show any differences in fecundity, oviposition period, mating percentage or other reproductive variables. Further studies on moths after 1.25–15-h tethered flights indicated that the reproductive process of adults could be fully triggered by flight activity longer than 2.5 h. Dissection of the reproductive organs also showed that tethered flight promoted ovarian and testicular development of FAW. These results show that appropriate moth flight activity significantly speeds up the reproductive process of FAW, which increases our knowledge on its migratory biology in relation to regional outbreaks.

Key words: flight , reproduction , migration , invasion biology , movement ecology

. [J]. Journal of Integrative Agriculture, 2021, 20(3): 727-735.

GE Shi-shuai, HE Wei, HE Li-mei, YAN Ran, ZHANG Hao-wen, WU Kong-ming. Flight activity promotes reproductive processes in the fall armyworm, Spodoptera frugiperda[J]. Journal of Integrative Agriculture, 2021, 20(3): 727-735.

参考文献

Baudron F, Zaman-Allah M A, Chaipa I, Chari N, Chinwada P. 2019. Understanding the factors influencing fall armyworm (Spodoptera frugiperda JE Smith) damage in African smallholder maize fields and quantifying its impact on yield. A case study in Eastern Zimbabwe. Crop Protection, 120, 141–150.
Bertram S M. 2007. Positive relationship between signaling time and flight capability in the Texas field cricket, Gryllus texensis. Ethology, 113, 875–880.
Boggs C L. 2010. Reproductive strategies of female butterflies: Variation in the constraints on fecundity. Ecological Entomology, 11, 7–15.
Cheng Y X, Luo L Z, Jiang X F, Sappington T W. 2012. Synchronized oviposition triggered by migratory flight intensifies larval outbreaks of beet webworm. PLoS ONE, 7, e31562.
Cui G F, Sun R R, Veeran S, Shu B S, Yuan H Q, Zhong G H. 2019. Combined transcriptomic and proteomic analysis of harmine on Spodoptera frugiperda Sf9 cells to reveal the potential resistance mechanism. Journal of Proteomics, 211, 103573.
Dingle H. 1996. Migration: The Biology of Life on the Move. Oxford University, New York.
Dingle H, Drake V A. 2007. What is migration? BioScience, 57, 113–121.
Dyakonova V, Krushinsky A. 2008. Previous motor experience enhances courtship behavior in male cricket Gryllus bimaculatus. Journal of Insect Behavior, 21, 172–180.
Fang M, Yao L, Li X M, Tang Q F. 2019. Influence of different nutrition supplement in adult stage on reproductive capacity of Spodoptera frugiperda. Plant Protection, 46, 193–195. (in Chinese)
Fu X W, Chang H, He L M, Zhao S Y, Wu K M. 2017. Flight performance of Macdunnoughia crassisigna (Lepidoptera: Noctuidae). Bulletin of Entomological Research, 107, 715–723.
Ge S S, He L M, He W, Xu R B, Sun X T, Wu K M. 2019. Determination on moth flight capacity of Spodoptera frugiperda. Plant Protection, 45, 28–33. (in Chinese)
Gibbs M, Dyck H V. 2010. Butterfly flight activity affects reproductive performance and longevity relative to landscape structure. Oecologia, 163, 341–350.
Goergen G, Kumar P L, Sankung S B, Togola A, Tamò M. 2016. First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. PLoS ONE, 11, e165632.
Guerra P A, Pollack G S. 2007. A life history trade-off between flight ability and reproductive behavior in male field Crickets (Gryllus texensis). Journal of Insect Behavior, 20, 377–387.
Guerra P A, Pollack G S. 2009. Flight behaviour attenuates the trade-off between flight capability and reproduction in a wing polymorphic cricket. Biology Letters, 5, 229–231.
Guo J L, Fu X W, Wu X, Zhao X C, Wu K M. 2015. Annual migration of Agrotis segetum (Lepidoptera: Noctuidae): Observed on a small isolated island in northern China. PLoS ONE, 10, e0131639.
He L M, Fu X W, Huang Y X, Shen X J, Sun X T, Wu K M. 2018. Seasonal patterns of Scotogramma trifolii Rottemberg (Lepidoptera: Noctuidae) migration across the Bohai Strait in northern China. Crop Protection, 106, 34–41.
He W, Zhao S Y, Ge S S, Jiang Y Y, Zhao X C, Wu K M. 2019. Population prediction method using sexual trapping for Spodoptera frugiperda. Plant Protection, 45, 48–53. (in Chinese)
IPPC (International Plant Protection Convention). 2019. First Detection Report of the Fall Armyworm Spodaptera Frugiperda (Lepidoptera: Noctuidae) on Maize in Myanmar. Food and Agriculture Organization, Rome.
Jiang X F, Luo L Z, Sappington T W. 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.
Jiang Y Y, Liu J, Xie M C, Li Y H, Yang J J, Zhang M L, Qiu K. 2019. Observation on law of diffusion damage of Spodoptera frugiperda in China in 2019. Plant Protection, 6, 10–19. (in Chinese)
Jindra M, Palli S R, Riddiford L M. 2013. The juvenile hormone signaling pathway in insect development. Annual Review of Entomology, 58, 181–204.
Johnson C G. 1969. Migration and Dispersal of Insects by Flight. Methuen, London. p. 763.
Karlsson B, Johansson A. 2008. Seasonal polyphenism and developmental trade-offs between flight ability and egg laying in a pierid butterfly. Proceedings of the Royal Society (B: Biological Sciences), 275, 2131–2136.
Kumela T, Simiyu J, Sisay B, Likhayo P, Mendesil E, Gohole L, Tefera T. 2018. Farmers’ knowledge, perceptions, and management practices of the new invasive pest, fall armyworm (Spodoptera frugiperda) in Ethiopia and Kenya. International Journal of Pest Management, 65, 1–9.
Li K B, Cao Y Z, Luo L Z, Gao X W, Yin J, Hu Y. 2005. Influences of flight on energetic reserves and juvenile hormone synthesis by corpora allata of the oriental armyworm, Mythimna separata (Walker). Acta Entomologica Sinica, 48, 155–160. (in Chinese)
Li K B, Luo L Z, Cao Y Z, Hu Y. 2001. Study on the relationship between degenerating flight muscle and reproduction in the oriental armyworm, Mythimna separata (Walker). Chinese Science Abstracts, 7, 662–664. (in Chinese)
Liang G M, Tan W J, Guo Y Y. 1999. Improvement of artificial rearing technique of Helicoverpa armigera. Plant Protection, 25, 15–17. (in Chinese)
Liu W, Li Y, Zhu L, Zhu F, Lei C L, Wang X P. 2016. Juvenile hormone facilitates the antagonism between adult reproduction and diapause through the methoprene-tolerant gene in the female Colaphellus bowringi. Insect Biochemistry and Molecular Biology, 74, 50–60.
Lv W X, Jiang X F, Zhang L, Luo L Z. 2014. Effect of different tethered flight durations on the reproduction and adult longevity of Mythimna separata (Lepidoptera: Noctuidae). Chinese Journal of Applied Entomology, 51, 914–921. (in Chinese)
Montezano D. 2018. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomology, 26, 286–300.
Morales-Ramos J. 1996. Significance of adult nutrition and oviposition experience on longevity and attainment of full fecundity of Catolaccus grandis (Hymenoptera: Pteromalidae). Annals of the Entomological Society of America, 89, 555–563.
Murua G, Molina-ochoa J, Coviella C. 2006. Population dynamics of the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) and its parasitoids in northwestern Argentina. Florida Entomologist, 89, 175–182.
Nagoshi R N, Meagher R L, Flanders K, Gore J, Jackson R, Lopez J, Armstrong J S, Buntin G D, Sansone C, Leonard B R. 2008. Using haplotypes to monitor the migration of fall armyworm (Lepidoptera: Noctuidae) corn-strain populations from Texas and Florida. Journal of Economic Entomology, 101, 742–749.
Polilov A A. 2011. Thoracic musculature of Sericoderus lateralis (Coleoptera, Corylophidae): Miniaturization effects and flight muscle degeneration related to development of reproductive system. Entomological Review, 91, 735–742.
Ramalho S R, Bezerra C D S, de Oliveira D G L, Lima L S, Neto S M, de Oliveira C F R, Verbisck N V, Macedo M L R. 2018. Novel Peptidase Kunitz inhibitor from Platypodium elegans seeds is active against Spodoptera frugiperda larvae. Journal of Agricultural and Food Chemistry, 66, 1349–1358.
Rankin M A, Burchsted J C A. 1992. The cost of migration in insects. Annual Review of Entomology, 37, 533–559.
Rivero-Borja M, Guzmán-Franco A W, Rodríguez-Leyva E, Santillan-Ortega C, Perez-Panduro A. 2018. Interaction of Beauveria bassiana and Metarhizium anisopliae with chlorpyrifos ethyl and spinosad in Spodoptera frugiperda larvae. Pest Management Science, 74, 2047–2052.
Sharanabasappa D, Kalleshwaraswamy C M, Asokan R, Swamy M, Maruthi M S, Pavithra H B, Hegde K, Navi S, Prabhu S T, Goergen G. 2018. First report of the fall armyworm, Spodaptera frugiperda (J E Smith) (Lepidoptera: Noctuidae), an alien invasive pest on maize in India. Pest Management in Horticultural Ecosystem, 24, 23–29.
Sparks A N. 1979. A review of the biology of the fall Armyworm. The Florida Entomologist, 62, 82–87.
Sparks A N, Jackson R D, Carpentar J E, Muller R A. 1986. Insects captured in light traps in the Gulf of Mexico. Annals of the Entomological Society of America, 79, 132–139.
Sun X X, Hu C X, Jia H R, Wu Q L, Shen X J, Zhao S Y, Jiang Y Y, Wu K M. 2021. Case study on the first immigration of fall armyworm, Spodoptera frugiperda invading into China. Journal of Integrative Agriculture, 20, 664–672.
Tambo J A, Day R K, Lamontagne-Godwin J, Silvestri S, Beseh P K, Oppong-Mensah B, Phiri N A, Matimelo M. 2020. Tackling fall armyworm (Spodoptera frugiperda) outbreak in Africa: an analysis of farmers’ control actions. International Journal of Pest Management, 66, 298–310.
Velde L V, Dyck H V. 2013. Lipid economy, flight activity and reproductive behaviour in the speckled wood butterfly: on the energetic cost of territory holding. Oikos, 122, 555–562.
Westbrook J K, Nagoshi R N, Meagher R L, Fleischer S J, Jairam S. 2016. Modeling seasonal migration of fall armyworm moths. International Journal of Biometeorology, 60, 255–267.
Wolf W W, Westbrook J K, Raulston J R, Pair S D, Lingren P D. 1995. Radar observations of orientation of noctuids migrating from corn fields in the Lower Rio Grande Valley. Southwestern Entomologist Supplement (USA), 18, 45–61.
Wu Q L, He L M, Shen X J, Jiang Y Y, Liu J, Wu K M. 2019a. Estimation of the potential infestation area of newly-invaded fall armyworm Spodoptera frugiperda in the Yangtze River Valley of China. Insects, 10, 298.
Wu Q L, Jiang Y Y, Hu G, Wu K M. 2019b. Analysis on spring and summer migration routes of fall armyworm (Spodoptera frugiperda) from tropical and southern subtropical zones of China. Plant Protection, 45, 1–9. (in Chinese)
Wu X, Fu X W, Guo J L, Zhao X C, Wu K M. 2015. Annual migration of cabbage moth, Mamestra brassicae L. (Lepidoptera: Noctuidae), over the sea in northern China. PLoS ONE, 10, e0132904.
Zera A J. 2007. Endocrine analysis in evolutionary-developmental studies of insect polymorphism: hormone manipulation versus direct measurement of hormonal regulators. Evolution and Development, 9, 499–513.
Zhang L, Pan P, Sappington T W, Lv W X, Luo L Z, Jiang X F. 2015. Accelerated and synchronized oviposition induced by flight of young females may intensify larval outbreaks of the rice leaf roller. PLoS ONE, 10, e0121821.
Zhao S Y, Yang X M, He W, Zhang H W, Jiang Y Y, Wu K M. 2019. Ovarian development gradation and reproduction potential prediction in Spodoptera frugiperda. Plant Protection, 45, 28–34. (in Chinese)
Zhao X Y, Fu X W, Ali A, Wilson K, Wu K M. 2016. Is Heliothis viriplaca (Lepidoptera: Noctuidae) a long-distance migrant? Bulletin of Entomological Research, 106, 1–9.