Electrophysiological and olfactory behavioural responses of mature Stilpnotia candida to a mixture of volatiles from Populus×beijingensis

Abstract

This study examined the EAG (Electroantennogram) responses of Stilpnotia candida to a mix of host plant volatiles and to provide a foundation for the development of plant-derived attractants. During the peak period of adult eclosion, gas chromatography–mass spectrometry analyzed and identified the volatiles emitted by Populus ×  beijingensis found in Xizang. Based on the preliminary EAG experiments and the GC‒MS results, a blending scheme was developed. EAG and Y-tube-olfactometry were employed to measure the electrophysiological and behavioural responses of unmated males and females 24 h after eclosion 10 blends of volatiles derived from five host plants. The GC–MS analysis revealed 22 volatile compounds from Populus ×  beijingensis leaves, composed of esters, hydrocarbons, terpenoids, alcohols, phenols, and ether. The results indicated that all 10 blending schemes produced EAG responses in mature S. candida. The concentration thresholds were between 1 and 10 μg·μL^‒1, above the optimal concentration, and a corresponding decrease in EAG was observed. According to intergroup comparisons, mature S. candida had more pronounced EAG responses. Under different concentrations, there were significant differences in the EAG from male and female S. candida to each blending scheme. Behavioural response tests indicated that schemes 2, 7, and 8 exhibited significantly greater attractiveness to adult S. candida. The combined results from the EAG and behavioral response experiments demonstrated that unmated male and female adult S. candida have varying degrees of sensitivity to the volatile compounds from the 10 blending schemes specific to Xizangan Populus ×  beijingensis. Schemes 2, 7, and 8 showed robust EAG responses and attractive behavioural responses to both male and female adult S. candida.

Keywords

Stilpnotia candida / Host volatiles / Gas chromatography-mass spectrometry / Electroantennogram / Y-tube-olfactometer

References

[1] Alzamora RM, Apiolaza L, Ruiz C, Lanfranco D. Site, tree and silvicultural factors influencing the infestation of xylophagous insects on Nothofagus Forests. J for Res, 2020, 9(2): 1-7

[2] Andersson MN, Larsson MC, Schlyter F. Specificity and redundancy in the olfactory system of the bark beetle Ips typographus: single-cell responses to ecologically relevant odors. J Insect Physiol, 2009, 55(6): 556-567

[3] Beck JJ, Smith L, Baig N. An overview of plant volatile metabolomics, sample treatment and reporting considerations with emphasis on mechanical damage and biological control of weeds. Phytochem Anal, 2014, 25(4): 331-341

[4] Bi YG, Wang ZG, Lu F, Yan AH. Tentacle potentials and behavioural responses of Morus alba to five plant-derived volatile compounds and their mixtures. Silkworm Science, 2017, 43(01): 32-38

[5] Bo B, Zheng XS, Xu HX, Ruan YM, ZX LV, Zhu PY. Tentacle potential responses of adult rice stem borer (Borrelia australis) to plant volatiles. J Appl Entomol, 2022, 59(05): 988-996

[6] Bruce TJA, Wadhams LJ, Woodcock CM. Insect host location: a volatile situation. Trends Plant Sci, 2005, 10(6): 269-274

[7] Chen LH, Chen XL, Bei JX, Xu XL. Cloning and expression analysis of the common odour receptor gene GmolOR20 in the pear psyllid. Journal of Entomology, 2019, 62(04): 418-427

[8] Chi DF, Li XC, Xiao F, Yu J, Qian JJ, Pei YQ, Xie X. Effects of plant volatiles on the EAG response and behaviour of Saperda populnea L. (Coleoptera: Cerambycidae). Asian J Chem, 2013, 25(4): 1783-1789

[9] Cotazo-Calambas KM, Niño-Castro A, Valencia-Giraldo SM, Gómez-Díaz JS, Montoya-Lerma J. Behavioral response of the leaf-cutting ant Atta cephalotes (Hymenoptera: Formicidae) to Trichoderma sp. J Insect Behav, 2022, 35(4): 92-102

[10] Despland E. Role of olfactory and visual cues in the attraction/repulsion responses to conspecifics by gregarious and solitarious desert locusts. J Insect Behav, 2001, 14(1): 35-46

[11] Dicke M, Loreto F. Induced plant volatiles: from genes to climate change. Trends Plant Sci, 2010, 15(3): 115-117

[12] Dötterl S, David A, Boland W, Silberbauer-Gottsberger I, Gottsberger G. Evidence for behavioral attractiveness of methoxylated aromatics in a dynastid scarab beetle-pollinated Araceae. J Chem Ecol, 2012, 38(12): 1539-1543

[13] Du YJ, Yan FS. Mechanism of plant volatile secondary substances in the relationship between phytophagous insects, parasitic plants and insect natural enemies. Acta Entomol Sin, 1994, 37(2): 233-250

[14] Du HT, Li Y, Zhu J, Liu F. Host-plant volatiles enhance the attraction of (Lepidoptera: Crambidae) to sex pheromone. Chemoecology, 2022, 32(3): 129-138

[15] Emilie D, Mallent M, Menut C, Chandre F, Martin T. Behavioral response of Bemisia tabaci(Hemiptera: Aleyrodidae) to 20 plant extracts. J Econ Entomol, 2015, 108(4): 1890-1901

[16] Faucheux MJ, Hamidi R, Mercadal M, Thomas M, Frérot B. Antennal sensilla of male and female of the nut weevil, Curculio nucumLinnaeus, 1758 (Coleoptera: Curculionidae). Annales De La Société Entomologique De France (n S), 2019, 55(5): 395-409

[17] Huang QT, Han XQ, Zhang GJ, Zhu-Salzman K, Cheng WN. Plant volatiles mediate host selection of Sitodiplosis mosellana (Diptera: Cecidomyiidae) among wheat varieties. J Agric Food Chem, 2022, 70(34): 10466-10475

[18] Hui Y. A preliminary study on the detection and reporting of Stilphotia candida Staudinger in Youyu county. Shanxi Forestry, 2014, 47(03): 47-48

[19] Jia XB. Risk analysis of Stilphotia candida Staudinger infestation in Shanzhou district. Henan for Sci Technol, 2017, 37(01): 41-43

[20] Jian NH, Zhao HL, Liu M. Driving force and potential of forest resource change: based on the results of the ninth national forest resources inventory. J for Grassl Policy, 2022, 2(3): 64-71

[21] Jie LL, Li WC. Morphological taxonomy of the Stilphotia candida Staudinger and analysis of its potential geographical distribution. J Jiangxi Agric Univ, 2018, 40(06): 1270-1275

[22] Jyothi KN, Prasuna AL, Sighamony S, Kumari BK, Prasad AR, Yadav JS. Electroantennogram responses of Apanteles obliquae (Hym., Braconidae) to various infochemicals. J Appl Entomol, 2002, 126(4): 175-181

[23] Kashiwagi GA, von Oppen S, Harburguer L, González-Audino P. The main component of the scent of Senecio madagascariensis flowers is an attractant for Aedes aegypti (L.) (Diptera: Culicidae) mosquitoes. Bull Entomol Res, 2022, 112(6): 837-846

[24] Katsoyannos BI, Hendrichs J. Food bait enhancement of fruit mimics to attract Mediterranean fruit fly females. J Appl Entomol, 1995, 119(1–5): 211-213

[25] Kausrud K, Okland B, Skarpaas O, Grégoire JC, Erbilgin N, Stenseth NC. Population dynamics in changing environments: the case of an eruptive forest pest species. Biol Rev Camb Philos Soc, 2012, 87(1): 34-51

[26] Knudsen JT, Eriksson R, Gershenzon J, Ståhl B. Diversity and distribution of floral scent. Bot Rev, 2006, 72(1): 1

[27] Kühnle A, Müller C. Relevance of visual and olfactory cues for host location in the mustard leaf beetle Phaedon cochleariae. Physiol Entomol, 2011, 36(168-76

[28] Landolt PJ, Phillips TW. Host plant influences on sex pheromone behavior of phytophagous insects. Annu Rev Entomol, 1997, 42: 371-391

[29] Li SG. Occurrence pattern and control measures of Stilphotia candida Staudinger. Mod Rural Sci Technol, 2015, 09: 26

[30] Li Q, Yao Y, He YT, Ma SY, Chu QW, Zhang S. The ecological adaptability of dominant poplar species to alpine environments in the Yarlung Zangbo River Basin. J Sichuan Univ (Natural Science Edition), 2023, 60(5): 203-211

[31] Loreto F, Schnitzler JP. Abiotic stresses and induced BVOCs. Trends Plant Sci, 2010, 15(3154-166

[32] Lou YG, Cheng JA. Pest-induced plant volatiles: basic properties, ecological functions and release mechanisms. J Ecol, 2000, 20(06): 1097-1106

[33] Luo YJ, Wang Y, Zhou Q, He J, Li X. Olfactory and behavioral responses of Papiliopolytes (Lepidoptera: Papilioidae) adults to volatiles form the branches and leaves of citrus. Acta Entomol Sin, 2023, 66(12): 1612-1625

[34] Ma ZG, Zhu JL, Sun ZQ, Liang J, Zhang ZX, Zhang LM, Sun LJ, Li WJ. The influences of biotic and abiotic factors on the occurrence and severity of poplar canker disease in Qingfeng county, China and the management implications. J Forestry Res, 2015, 26(4): 1025-1034

[35] Magsi FH, Luo ZX, Zhao YJ, Li ZQ, Cai XM, Bian L, Chen ZM. Electrophysiological and behavioral responses of Dasychira baibarana (Lepidoptera: Lymantriidae) to tea plant volatiles. Environ Entomol, 2021, 50(3): 589-598

[36] Mavridis K, Ilias A, Papapostolou KM, Varikou K, Michaelidou K, Tsagkarakou A, Vontas J. Molecular diagnostics for monitoring insecticide resistance in the western flower Thrips Frankliniella occidentalis. Pest Manag Sci, 2023, 79(4): 1615-1622

[37] Mills NJ, Beers EH, Shearer PW, Unruh TR, Amarasekare KG. Comparative analysis of pesticide effects on natural enemies in western orchards: a synthesis of laboratory bioassay data. Biol Contr, 2016, 102: 17-25

[38] Mobarak SH, Koner A, Debnath R, Barik A. The role of green gram plant volatile blends in the behavior of arctiid moth. Spilosoma Obliqua J Chem Ecol, 2022, 48(11–12): 802-816

[39] Neven L, Humble LM, Savard M, Noseworthy MK, Lavallée R, Gray M, Macquarrie CJK. Assessment of the systems approach for the phytosanitary treatment of wood infested with wood-boring insects. J Econ Entomol, 2020, 113(2): 679-694

[40] Niu YL, Qin JG, Lu B, Li XY, Deng QZ. Occurrence pattern and comprehensive control measures of the Stilphotia Candida Staudinger. Rural Sci Technol, 2022, 5: 34-36

[41] Panthawong A, Nararak J, Jhaiaun P, Sukkanon C, Chareonviriyaphap T. Synergistic behavioral response effect of mixtures of Andrographis paniculata, Cananga odorata, and Vetiveria zizanioides against Aedes aegypti (Diptera: Culicidae). InSects, 2023, 14(2): 155

[42] Pichersky E, Noel JP, Dudareva N. Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science, 2006, 311(5762808-811

[43] Raguso RA, Willis MA. Synergy between visual and olfactory cues in nectar feeding by naı̈ve hawkmoths. Manduca Sexta Anim Behav, 2002, 64(5): 685-695

[44] Ren LL (2014) Electrophysiological and behavioural responses of the pine ink skink and the natural enemy flower velvet parasitoid to several tree volatiles. Doctoral Thesis, Beijing Forestry University

[45] Runyon JB, Mescher MC, De Moraes CM. Volatile chemical cues guide host location and host selection by parasitic plants. Science, 2006, 313(5795): 1964-1967

[46] Skrylnik Y, Koshelyaeva Y, Meshkova V. Harmfulness of xylophagous insects for silver birch (Betula pendula Roth.) in the left-bank forest-steppe of Ukraine. Folia for Pol, 2019, 61(3): 159-173

[47] Strzyzewski I, Funderburk J, Martini X. Specificity of vectoring and non-vectoring flower Thrips species to pathogen-induced plant volatiles. J Pest Sci, 2023, 96(2): 441-449

[48] Tang XQ, Wang SZ, Lu J, Gao TT, Chen YQ. Tentacle potentials and behavioural responses of the fir tip borer to volatiles from spruce cones in Linzhi. For Sci Res, 2021, 34(06): 140-148(In Chinese)

[49] Thia JA, Korhonen PK, Young ND, Gasser RB, Umina PA, Yang Q, Edwards O, Walsh T, Hoffmann AA. The redlegged earth mite draft genome provides new insights into pesticide resistance evolution and demography in its invasive Australian range. J Evol Biol, 2023, 36(2): 381-398

[50] Tooker JF, Crumrin AL, Hanks LM. Plant volatiles are behavioral cues for adult females of the gall wasp Antistrophus rufus. Chemoecology, 2005, 15(2): 85-88

[51] Triana MF, França PHB, Queiroz AFO, Santos JM, Goulart HF, Santana AEG. Morphological, chemical and electrophysiological investigations of Telchin licus (Lepidoptera: Castniidae). PLoS ONE, 2020, 15(4 e0231689

[52] Tyagi S, Ram Keval (2020) Understanding and utilizing resistance to insects in plants. In book: Advances in Agricultural Entomology (pp.91–115), Edition: Vol-12. Publisher: AkiNik Publications. https://doi.org/10.22271/ed.book.1061

[53] Völkl W, Sullivan DJ. Foraging behaviour, host plant and host location in the aphid hyperparasitoid Euneura augarus. Entomologia Exp Applicata, 2000, 97(1): 47-56

[54] Wang X, Xu ZH, Tang SY, Cheke RA. Cumulative effects of incorrect use of pesticides can lead to catastrophic outbreaks of pests. Chaos Soliton Fract, 2017, 100: 7-19

[55] Wang Q, Xu P, Sanchez S, Duran P, Andreazza F, Isaacs R, Dong K. Behavioral and physiological responses of Drosophila melanogaster and D. suzukii to volatiles from plant essential oils. Pest Manag Sci, 2021, 77(8): 3698-3705

[56] Yang YF. Research on the technical application of applying ring coating to prevent and control Stilphotia candida Staudinger pests in forests. Modern Horticulture, 2020, 43(16): 5-6

[57] Yang H, Yang W, Liang XY, Yang MF, Yang CP, Zhu TH, Wu XL. The EAG and behavioral responses of (Coleoptera: Cerambycidae) to the composition of volatiles. J Kansas Entomol Soc, 2011, 84(3): 217-231

[58] Zhang Y. Comparative study of secondary metabolites in different strains of poplar trees. For Sci Technol, 2013, 5(05): 12-14

[59] Zhang YR, Wang R, Yu LF, Lu PF, Luo YQ. Identification of Caragana plant volatiles, overlapping profiles, and olfactory attraction to Chlorophorus caragana in the laboratory. J Plant Interact, 2015, 10(1): 41-50

[60] Zhang JC, Liu JJ, Gao F, Chen M, Jiang YS, Zhao HT, Ma WH. Electrophysiological and behavioral responses of Apis mellifera and Bombusterrestris to melon flower volatiles. InSects, 2022, 13(11): 973

[61] Zhang LX, Ren Y, Meng FL, Bao HB, Xing F, Tian CM. Verification of the protective effects of poplar phenolic compounds against poplar anthracnose. Phytopathology, 2022, 112(102198-2206

[62] Zhao R, Wang HH, Gao J, Zhang YJ, Li X, Zhou JJ, Liang P, Gao XW, Gu SH. Plant volatile compound methyl benzoate is highly effective against Spodoptera frugiperda and safe to non-target organisms as an eco-friendly botanical-insecticide. Ecotoxicol Environ Saf, 2022, 245: 114101

[63] Zhong GJ, Gao XY, Shen JM, He MY, Liang KY, Zhang JW, Pan YY, Su XN, Zhang YP, Hu LM. Ligand binding properties of odorant binding protein BdorOBP2 to methyl eugenol analogues of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). J Environ Entomol, 2024, 46(2): 480-488(In Chinese)

[64] Zhou QY, Cheng X, Wang SS, Liu SR, Wei CL. Effects of chemical insecticide imidacloprid on the release of C₆ green leaf volatiles in tea plants (Camellia sinensis). Sci Rep-Uk, 2019, 9(11-6

[65] Zhuo ZH, Jin YW, Xu DP, Liao WK. Electroantennogram responses of (Hope) to the selected volatile components of host plants. Tratt and Thunb Glob Ecol Conserv, 2022, 33: 1986-1998(In Chinese)

RIGHTS & PERMISSIONS

Northeast Forestry University