Analysis of phototactic responses in Spodoptera frugiperda using Helicoverpa armigera as control

doi:10.1016/S2095-3119(19)62863-7

摘要/Abstract

摘要：

诱虫灯在现代农业的害虫预测预报和防治工作中得到广泛的应用。草地贪夜蛾于2018年底经云南迁飞入侵中国，严重威胁我国农作物的安全生产。为明确诱虫灯对草地贪夜蛾成虫的诱集效率，我们首先通过转录组测序确定其视蛋白基因的种类和数量。聚类分析表明，与其它夜蛾科昆虫类似，草地贪夜蛾表达4个视蛋白基因。但是草地贪夜蛾视蛋白基因的表达量显著低于棉铃虫中相对应的基因。趋光行为研究表明，棉铃虫和草地贪夜蛾成虫均具有显著正趋光性，其中草地贪夜蛾雌、雄成虫飞向光源的速度均显著高于棉铃虫，这可能是由于草地贪夜蛾飞行速度高于棉铃虫所致。然而，诱虫灯结果表明草地贪夜蛾的上灯率显著低于棉铃虫，这与视蛋白基因在两种昆虫中的表达水平一致。综上所述，本研究表明草地贪夜蛾成虫具有趋光性，诱虫灯可用于该虫的预测预报及防治工作，但诱集效率低于棉铃虫。

Abstract:

Light traps are widely utilized to monitor and manage insect pest populations. In late 2018, the fall armyworm (FAW), Spodoptera frugiperda, invaded China through Yunnan Province representing a huge threat to grain production. To estimate the efficiency of light traps on FAW moths, we first identified the opsin genes from FAW by using the transcriptome. Phylogenetic analysis indicated that the four opsins of FAW were clustered with those of other Noctuidae species. The expressed levels of opsins in S. frugiperda were lower than in Helicoverpa armigera, suggesting a different phototactic response between the two species. Then, we determined the phototactic behavior of FAW using H. armigera as a control, which is widely monitored and managed using light traps in China. Our results indicated that the two moths species showed significantly different phototactic behavior and both female and male FAW displayed faster flight-to-light speed than H. armigera. This may be due to a faster flight capacity in FAW compared to H. armigera. However, the capture rate of both female and male of S. frugiperda was significantly lower than that of H. armigera, which was consistent with the expression levels of opsins. These results support the positive phototaxis of S. frugiperda moths and suggest light traps could be used for monitoring and managing the pests, but with a lower efficiency than H. armigera.

Key words: Spodoptera frugiperda , Helicoverpa armigera , light performance , opsin genes , light trap

. [J]. Journal of Integrative Agriculture, 2021, 20(3): 821-828.

LIU Ying-jie, ZHANG Dan-dan, YANG Li-yu, DONG Yong-hao, LIANG Ge-mei, Philip DONKERSLEY, REN Guang-wei, XU Peng-jun, WU Kong-ming . Analysis of phototactic responses in Spodoptera frugiperda using Helicoverpa armigera as control[J]. Journal of Integrative Agriculture, 2021, 20(3): 821-828.

参考文献

Ali S, Masroor Z, Masroor M D. 2018. First record of the fall armyworm, Spodoptera frugiperda (JE Smith, 1797) (Lepidoptera: Noctuidae), an evil attack on paddy in Magadh, Bihar (India). International Journal of Emerging Technologies and Innovative Research, 5, 546–549.
Briscoe A D, Chittka L. 2001. The evolution of color vision in insects. Annual Review of Entomology, 46, 471–510.
Cutler D E, Bennett R R, Stevenson R D, White R H. 1995. Feeding behavior in the nocturnal moth Manduca sexta is mediated mainly by violet receptors, but where are they located in the retina? Journal of Experimental Biology, 198, 1909–1917.
Early R, González-Moreno P, Murphy S T, Day R. 2018. Forecasting the global extent of invasion of the cereal pest Spodoptera frugiperda, the fall armyworm. NeoBiota, 40, 25–50.
Feng H Q, Gould F, Huang Y X, Jiang Y Y, Wu K M. 2010. Modeling the population dynamics of cotton bollworm Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) over a wide area in northern China. Ecological Modelling, 221, 1819–1830.
Feng H Q, Wu K M, Cheng D F, Guo Y Y. 2004. Northward migration of Helicoverpa armigera (Lepidoptera: Noctuidae) and other moths in early summer observed with radar in northern China. Journal of Economic Entomology, 97, 1874–1883.
Feng H Q, Wu K M, Ni Y X, Cheng D F, Guo Y Y. 2005. Return migration of Helicoverpa armigera (Lepidoptera: Noctuidae) during autumn in northern China. Bulletin of Entomological Research, 95, 361–370.
Feng H Q, Wu X F, Wu B, Wu K M. 2009. Seasonal migration of Helicoverpa armigera (Lepidoptera: Noctuidae) over the Bohai Sea. Journal of Economic Entomology, 102, 95–104.
Futahashi R, Kawahara-Miki R, Kinoshita M, Yoshitake K, Yajima S, Arikawa K, Fukatsu T. 2015. Extraordinary diversity of visual opsin genes in dragonflies. Proceedings of the National Academy of Sciences of the United States of America, 112, E1247–E1256.
Goergen G, Kumar P L, Sankung S B, Togola A, Tamò M. 2016. First report of outbreaks of the fall armyworm Spodoptera frugiperda (JE Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. PLoS ONE, 11, e0165632.
van Grunsven R H A, Donners M, Boekee K, Tichelaar I, van Geffen K G, Groenendijk D, Berendse F, Veenendaal E M. 2014. Spectral composition of light sources and insect phototaxis, with an evaluation of existing spectral response models. Journal of Insect Conservation, 18, 225–231.
Hardke J T, Leonard B R, Huang F, Jackson R E. 2011. Damage and survivorship of fall armyworm (Lepidoptera: Noctuidae) on transgenic field corn expressing Bacillus thuringiensis Cry proteins. Crop Protection, 30, 168–172.
Henze M J, Oakley T H. 2015. The dynamic evolutionary history of pancrustacean eyes and opsins. Integrative and Comparative Biology, 55, 830–842.
Jackowska M, Bao R, Liu Z, McDonald E C, Cook T A, Friedrich M. 2007. Genomic and gene regulatory signatures of cryptozoic adaptation: Loss of blue sensitive photoreceptors through expansion of long wavelength-opsin expression in the red flour beetle Tribolium castaneum. Frontiers in Zoology, 4, 24.
Jiggins C D, Naisbit R E, Coe R L, Mallet J. 2001. Reproductive isolation caused by colour pattern mimicry. Nature, 411, 302–305.
Jing D P, Guo J F, Jiang Y Y, Zhao J Z, Sethi A, He K L, Wang Z Y. 2020. Initial detections and spread of invasive Spodoptera frugiperda in China and comparisons with other noctuid larvae in cornfield using molecular techniques. Insect Science, 27, 780–790.
Jing X F, Luo F, Zhu F, Huang Q Y, Lei C L. 2005. Effects of different light source and dark-adapted time on phototactic behavior of cotton bollworms (Helicoverpa armigera). Chinese Journal of Applied Ecology, 16, 586–588. (in Chinese)
Johansen N S, Vänninen I, Pinto D M, Nissinen A I, Shipp L. 2011. In the light of new greenhouse technologies: 2. Direct effects of artificial lighting on arthropods and integrated pest management in greenhouse crops. Annals of Applied Biology, 159, 1–27.
Kalleshwaraswamy C M, Asokan R, Swamy H M M, Maruthi M S, Pavithra H B, Hegde K, Navi S, Prabhu S T, Goergen G. 2018. First report of the fall armyworm, Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae), an alien invasive pest on maize in India. Pest Management in Horticultural Ecosystems, 24, 23–29.
Kelber A. 1999. Ovipositing butterflies use a red receptor to see green. Journal of Experimental Biology, 202, 2619–2630.
Kim K N, Huang Q Y, Lei C L. 2019. Advances in insect phototaxis and application to pest management: A review. Pest Management Science, 75, 3135–3143.
Kim K N, Song H S, Li C S, Huang Q Y, Lei C L. 2018. Effect of several factors on the phototactic response of the oriental armyworm, Mythimna separata (Lepidoptera: Noctuidae). Journal of Asia-Pacific Entomology, 21, 952–957.
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.
Land M F. 1997. Visual acuity in insects. Annual Review of Entomology, 42, 147–177.
Li B, Dewey C N. 2011. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12, 323.
Liu Y J, Yan S, Shen Z J, Li Z, Zhang X F, Liu X M, Zhang Q W, Liu X X. 2018. The expression of three opsin genes and phototactic behavior of Spodoptera exigua (Lepidoptera: Noctuidae): Evidence for visual function of opsin in phototaxis. Insect Biochemistry and Molecular Biology, 96, 27–35.
Maelzer D A, Zalucki M P. 1999. Analysis of long-term light-trap data for Helicoverpa spp. (Lepidoptera: Noctuidae) in Australia: The effect of climate and crop host plants. Bulletin of Entomological Research, 89, 455–463.
Mallapur C P, Naik A K, Hagari S, Prabhu S T, Patil P K. 2018. Status of alien pest fall armyworm, Spodoptera frugiperda (J E Smith) on maize in northern Karnataka. Journal of Entomology and Zoology Studies, 6, 432–436.
Merlin C, Gegear R J, Reppert S M. 2009. Antennal circadian clocks coordinate sun compass orientation in migratory monarch butterflies. Science, 325, 1700–1704.
Montezano D G, Specht A, Sosa-Gomez D R, Roque-Specht V F, Sousa-Silva J C, Paula-Moraes S V, Peterson J A, Hunt T E. 2018. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomology, 26, 286–300.
Nagoshi R N, Meagher R L. 2008. Review of fall armyworm (Lepidoptera: Noctuidae) genetic complexity and migration. Florida Entomologist, 91, 546–554.
Nagoshi R N, Silvie P, Meagher R L. 2007. Comparison of haplotype frequencies differentiate fall armyworm (Lepidoptera: Noctuidae) corn-strain populations from Florida and Brazil. Journal of Economic Entomology, 100, 954–961.
Oh M S, Lee C H, Lee S G, Lee H. 2011. Evaluation of high power light emitting diodes (HPLEDs) as potential attractants for adult Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). Journal of the Korean Society for Applied Biological Chemistry, 54, 416–422.
Omoto C, Bernardi O, Salmeron E, Sorgatto R J, Dourado P M, Crivellari A, Carvalho R A, Willse A, Martinelli S, Head G P. 2016. Field-evolved resistance to Cry1Ab maize by Spodoptera frugiperda in Brazil. Pest Management Science, 72, 1727–1736.
Otim M H, Tay W T, Walsh T K, Kanyesigye D, Adumo S, Abongosi J, Ochen S, Sserumaga J, Alibu S, Abalo G, Asea G, Agona A. 2018. Detection of sister-species in invasive populations of the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) from Uganda. PLoS ONE, 13, e0194571.
Park J H, Lee H S. 2017. Phototactic behavioral response of agricultural insects and stored-product insects to light-emitting diodes (LEDs). Applied Biological Chemistry, 60, 137–144.
Peitsch D, Fietz A, Hertel H, de Souza J, Ventura D F, Menzel R. 1992. The spectral input systems of hymenopteran insects and their receptor-based colour vision. Journal of Comparative Physiology (A: Sensory, Neural, and Behavioral Physiology), 170, 23–40.
Pogue M G. 2002. A world revision of the genus Spodoptera Guenée: (Lepidoptera: Noctuidae). Memoirs of the American Entomological Society, 43, 1–20.
Salcedo E, Huber A, Henrich S, Chadwell L V, Chou W H , Paulsen R, Britt S G. 1999. Blue-and green-absorbing visual pigments of Drosophila: Ectopic expression and physiological characterization of the R8 photoreceptor cell-specific Rh5 and Rh6 rhodopsins. Journal of Neuroscience, 19, 10716–10726.
Sharkey C R, Fujimoto M S, Lord N P, Shin S, McKenna D D, Suvorov A, Martin G J, Bybee S M. 2017. Overcoming the loss of blue sensitivity through opsin duplication in the largest animal group, beetles. Scientific Reports, 7, 8.
Sparks A N. 1979. A review of the biology of the fall armyworm. Florida Entomologist, 62, 82–87.
Stokstad E. 2017. New crop pest takes Africa at lightning speed. Science, 356, 473–474.
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.
Terakita A. 2005. The opsins. Genome Biology, 6, 213.
Tokushima Y, Uehara T, Yamaguchi T, Arikawa K, Kainoh Y, Shimoda M. 2016. Broadband photoreceptors are involved in violet light preference in the parasitoid fly Exorista Japonica. PLoS ONE, 11, e0160441.
Wang L, Chen K W, Lu Y Y. 2019. Long-distance spreading speed and trend predication of fall armyworm, Spodoptera frugiperda, in China. Journal of Environmental Entomology, 41, 683–694. (in Chinese)
Weiss M R. 2001. Vision and learning in some neglected pollinators: beetles, flies, moths and butterflies. In: Chittka L, Thomson J D, eds., Cognitive Ecology of Pollination: Animal Behavior and Floral Evolution. Cambridge University Press, Cambridge. pp. 106–126.
Wu K M, Lu Y H, Feng H Q, Jiang Y Y, Zhao J Z. 2008. Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science, 321, 1676–1678.
Xu P J, Feuda R, Lu B, Xiao H J, Graham R I, Wu K M. 2016. Functional opsin retrogene in nocturnal moth. Mobile DNA, 7, 18.
Xu P J, Lu B, Xiao H J, Fu X W, Murphy R W, Wu K M. 2013. The evolution and expression of the moth visual opsin family. PLoS ONE, 8, e78140.
Yan S, Zhu J L, Zhu W L, Zhang X F, Li Z, Liu X X, Zhang Q W. 2014. The expression of three opsin genes from the compound eye of Helicoverpa armigera (Lepidoptera: Noctuidae) is regulated by a circadian clock, light conditions and nutritional status. PLoS ONE, 9, e111683.
Zalucki M P, Daglish G, Firempong S, Twine P. 1986. The biology and ecology of Heliothis armigera (Hübner) and Heliothis punctigera Wallengren (Lepidoptera, Noctuidae) in Australia - what do we know. Australian Journal of Zoology, 34, 779–814.
Zheng L X, Zheng Y, Wu W J, Fu Y G. 2014. Field evaluation of different wavelengths light-emitting diodes as attractants for adult Aleurodicus dispersus Russell (Hemiptera: Aleyrodidae). Neotropical Entomology, 43, 409–414.