Ecological Mechanism Underlying the Repellence of Cnaphalocrocis medinalis Egg-deposited Rice Plant on the Subsequent Adult Oviposition

doi:10.16409/j.cnki.2095-039x.2024.07.023

Abstract

Abstract: Oviposition behavior is a critical process for insects to ensure the continuation of their population, and location of the suitable host plants is of key important for reproductive success of insects. Oviposition on host plants can activate the plant's defense mechanisms against insects. This defense mechanism can not only directly impede the development of insect eggs, but also make the plant to prepare for defense against subsequent larval attacks. In this study, we explored that the impact of Cnaphalocrocis medinalis (RLF) egg-deposited rice plants on oviposition preference of the subsequent adults, and their response to volatile compounds induced by egg deposition. The greenhouse experiments revealed that rice plants with egg deposition for 4 days exhibited a significant repellent effect on RLF females, regardless of whether the eggs were removed or not. Moreover, compared to the healthy plants, RLF eggs laid on rice plants that had undergone 4 days of egg deposition displayed a prolonged hatching periods and reduced hatching rates. GC-MS analysis showed that healthy rice plants and plants with eggs deposition for 4 days released the same kinds of 22 volatile compounds. However, there were 6 volatiles showing significantly different in amount between the two treated rice plants. Among the 6 compounds, except for styrene, the release amounts of 5 other volatiles (decanal, dodecane, tridecane, tetradecane, and nonanal) significantly decreased by the plants with egg deposition. The function of the volatile compounds was tested and the results indicated that tetradecane with the highest release rate exhibited a significant attraction to RLF female oviposition, while decanal displayed a marked repellent effect on RLF females. The other 4 volatiles showed no significant effect on the oviposition behavior of the pest. This may suggest that the RLF females prefer to lay eggs on healthy rice plants may be due to the ecological effects of reduced tetradecane release from egg-deposited rice plants, or due to the integrated regulation of RLF female behavior by multiple rice volatiles, including decanal. These findings enhance our understanding of the host plant selection mechanism of RLF and provide valuable insights for the development of ecological management strategies for control of this pest.

Key words: Cnaphalocrocis medinalis, eggs deposition, rice volatiles, oviposition preference

CLC Number:

S476

XING Jingyuan, TIAN Zhiqiang, YAO Chengcheng, HU Xiaoyun, CHU Dong, LI Yunhe. Ecological Mechanism Underlying the Repellence of Cnaphalocrocis medinalis Egg-deposited Rice Plant on the Subsequent Adult Oviposition[J]. Chinese Journal of Biological Control, 2025, 41(2): 299-308.

References

[1] Hilker M, Meiners T. Plants and insect eggs: how do they affect each other?[J]. Phytochemistry, 2011, 72(13): 1612-1623.
[2] Jallow M F A, Zalucki M P. Within-and between-population variation in host-plant preference and specificity in Australian Helicoverpa armigera Hübner (Lepidoptera: Noctuidae)[J]. Australian Journal of Zoology, 1996, 44(5): 503-519.
[3] Holland J N, Buchanan A L, Loubeau R. Oviposition choice and larval survival of an obligately pollinating granivorous moth[J]. Evolutionary Ecology Research, 2004, 6(4): 607-618.
[4] Lu W, Wang Q, Tian M Y, et al. Host selection and colonization strategies with evidence for a female-produced oviposition attractant in a longhorn beetle[J]. Environmental Entomology, 2011, 40(6): 1487-1493.
[5] 陆宴辉, 张永军, 吴孔明. 植食性昆虫的寄主选择机理及行为调控策略[J]. 生态学报, 2008(10): 5113-5122.
[6] 唐宇翀, 周成理, 陈晓鸣. 植食性昆虫产卵行为生态学研究进展[J]. 林业科学研究, 2010, 23(5): 770-777.
[7] 张庆贺, 姬兰柱. 植食性昆虫产卵的化学生态学[J]. 生态学杂志, 1994, 13(6): 39-43.
[8] Allision J D, Borden J H, Seybold S J. A review of the chemical ecology of the Cerambycidae (Coleoptera)[J]. Chemoecology, 2004, 14(3): 123-150.
[9] 樊慧, 金幼菊, 李继泉, 等. 引诱植食性昆虫的植物挥发性信息化合物的研究进展[J]. 北京林业大学学报, 2004(3): 76-81.
[10] Erb M. Plant defenses against herbivory: closing the fitness gap[J]. Trends in Plant Science, 2017, 23(3): 187-194.
[11] Kessler A, Baldwin I T. Defensive function of herbivore-induced plant volatile emissions in nature[J]. Science, 2001, 291(5511): 2141-2144.
[12] Sun X L, Wang G C, Gao Y, et al. Volatiles emitted from tea plants infested by Ectropis obliqua larvae are attractive to conspecific moths[J]. Journal of Chemical Ecology, 2014, 40(10): 1080-1089.
[13] Fatouros N E, Lucas-Barbosa D, Weldegergis B T, et al. Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels[J]. PLoS ONE, 2012, 7(8): e43607.
[14] Bruce T J A, Midega C A O, Birkett M A, et al. Is quality more important than quantity? Insect behavioural responses to changes in a volatile blend after stemborer oviposition on an African grass[J]. Biology Letters, 2010, 6(3): 314-317.
[15] Hilker M, Fatouros N E. Resisting the onset of herbivore attack: plants perceive and respond to insect eggs[J]. Current Opinion in Plant Biology, 2016, 32: 9-16.
[16] Bandoly M, Hilker M, Steppuhn A. Oviposition by Spodoptera exigua on Nicotiana attenuata primes induced plant defence against larval herbivory[J]. The Plant Journal, 2015, 83(4): 661-672.
[17] Bandoly M, Grichnik R, Hilker M, et al. Priming of anti-herbivore defence in Nicotiana attenuata by insect oviposition: herbivore-specific effects[J]. Plant, Cell & Environment, 2016, 39(4): 848-859.
[18] Hilker M, Fatouros N E. Plant responses to insect egg deposition[J]. Annual Review of Entomology, 2015, 60: 493-515.
[19] Seino Y, Suzuki Y, Sogawa K. An ovicidal substance produced by rice plants in response to oviposition by the whitebacked planthopper, Sogatella furcifera Horváth (Homoptera: Delphacidae)[J]. Applied Entomology and Zoology, 1996, 31(4): 467-473.
[20] Suzuki Y, Sogawa K, Seino Y. Ovicidal reaction of rice plants against the whitebacked planthopper, Sogatella furclfera Horváth (Homoptera: Delphacidae)[J]. Applied Entomology and Zoology, 1996, 31(1): 111-118.
[21] Yamasaki M, Yoshimura A, Yasui H. Genetic basis of ovicidal response to whitebacked planthopper (Sogatella furcifera Horváth) in rice (Oryza sativa L.)[J]. Molecular Breeding, 2003, 12: 133-143.
[22] 罗绍岳. 水稻稻纵卷叶螟和稻飞虱的发生与防治措施[J]. 种子科技, 2023,41(24): 73-75,81.
[23] Hu X, Su S, Liu Q, et al. Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper[J]. eLife, 2020, 9: e55421.
[24] Liu Q, Hu X, Su S, et al. Cooperative herbivory between two important pests of rice[J]. Nature Communications, 2021, 12(1): 6772.
[25] 陈萍. 稻纵卷叶螟在水稻和玉米上的适合度与产卵选择[D]. 北京: 中国农业科学院, 2021.
[26] 张茂新, 凌冰, 庞雄飞. 非嗜食植物中的昆虫产卵驱避物及其利用[J]. 昆虫天敌, 2003(1): 28-36.
[27] 钦俊德, 王琛柱. 论昆虫与植物的相互作用和进化的关系[J]. 昆虫学报, 2001(3): 360-365.
[28] 邵瑞. 棉铃虫卵沉积诱导的番茄防御反应[D]. 武汉: 华中农业大学, 2023.
[29] Hamm J C, Stout M J, Riggio R M. Herbivore-and elicitor-induced resistance in rice to the rice water weevil (Lissorhoptrus oryzophilus Kuschel) in the laboratory and field[J]. Journal of Chemical Ecology, 2010, 36: 192-199.
[30] Li G, Ishikawa Y. Oviposition deterrents from the egg masses of the adzuki bean borer, Ostrinia scapulalis and Asian corn borer, O. furnacalis[J]. Entomologia Experimentalis et Applicata, 2005, 115(3): 401-407.
[31] Liu M, Yu H, Li G. Oviposition deterrents from eggs of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae): Chemical identification and analysis by electroantennogram[J]. Journal of Insect Physiology, 2008, 54(4): 656-662.
[32] Zhang X, Liu Y, Guo M, et al. A female-specific odorant receptor mediates oviposition deterrence in the moth Helicoverpa armigera[J]. Current Biology, 2024, 34(1): 1-11.
[33] Schott J, Fuchs B, Böttcher C, et al. Responses to larval herbivory in the phenylpropanoid pathway of Ulmus minor are boosted by prior insect egg deposition[J]. Planta, 2022, 255(1): 16.
[34] Bittner N, Hundacker J, Achotegui-Castells A, et al. Defense of Scots pine against sawfly eggs (Diprion pini) is primed by exposure to sawfly sex pheromones[J]. Proceedings of the National Academy of Sciences, 2019, 116(49): 24668-24675.
[35] Liu S, Zhao J, Hamada C, et al. Identification of attractants from plant essential oils for Cyrtorhinus lividipennis, an important predator of rice planthoppers[J]. Journal of Pest Science, 2019, 92(2): 769-780.
[36] 郭丽. 杨小舟蛾产卵对2 种黑杨派无性系的诱导抗性研究[D]. 北京: 中国林业科学研究院, 2019.
[37] Penaflor M F G V, Erb M, Robert C A M, et al. Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize[J]. Planta, 2011, 234: 207-215.
[38] 杨灯海. 草地贪夜蛾诱导的玉米挥发物对东方粘虫和亚洲玉米螟行为的影响[D]. 合肥: 安徽农业大学, 2023.
[39] 孙小旭, 张秀歌, 李祥, 等. 蓝桉叶片挥发物对棉铃虫产卵选择行为的影响[J]. 植物保护学报, 2018, 45(3): 576-584.