Koinobiont Parasitism and Biology of Braconid Parasitoids on Invasive Fall Armyworm Spodptera frugiperda (J.E. smith) in controlled condtions

Koinobiont Parasitism and Biology of Braconid Parasitoids on Invasive Fall Armyworm Spodptera frugiperda (J.E. smith) in controlled condtions | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Koinobiont Parasitism and Biology of Braconid Parasitoids on Invasive Fall Armyworm Spodptera frugiperda (J.E. smith) in controlled condtions Amit Kumar, S. Ramesh Babu, Devendra Jain, Manoj Kumar, Vikram Singh This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-8776953/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted 10 You are reading this latest preprint version Abstract Background The Fall Armyworm highly destructive insect pests across the world. The native parastoid species such as Chelonus spp. is prominent natural enemy of this pest. The natural control of Spodoptera frugiperda may achieved by parasitods be able to strong tool. Results This study compared the life cycles and effectiveness of two parasitoid wasps, Chelonus formosanus and Chelonus blackburni , in a laboratory conditions. The key developmental durations for Chelonus formosanus and Chelonus blackburni were as follows an incubation period of 24.27 and 24.64 hours, a total larval period of 17.55 and 18.55 days and a pupal period of 10.27 and 11.09 days, respectively. This resulted in a total development time of 27.82 days for Chelonus formosanus and 29.65 days for Chelonus blackburni . Adult females laid approximately 192 and 199 eggs on Spodoptera frugiperda eggs and lived for about 6.0 and 6.6 days, respectively. Adult males lived for roughly 4.2 and 4.6 days, respectively. The parasitism potential was also evaluated. Following exposure, 66.2% of hosts parasitized by Chelonus formosanus and 59.6% parasitized by Chelonus blackburni reached the pupation stage. The successful emergence rate of adult wasps from these pupae was 63.8% for Chelonus formosanus and 52.4% for Chelonus blackburni . Conclusion The results indicate that Chelonus formosanus demonstrated greater effectiveness as a biological control agent against S. frugiperda under the tested conditions. Parasitism potential Chelonus formosanus Chelonus blackburni Life cycle Spodoptera frugiperda Background The Fall Armyworm (FAW), Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), is a highly polyphagous, dreaded insect pest native to tropical and subtropical areas of the Americas. The FAW reported to feed on more than 350 plant species belonging to 76 plant families (Montezano et al., 2018 ). Due to its massive migratory habit, it causes threat in Africa and Asia and it was first reported in Africa in 2016 (Goergen et al., 2016 ). In India, FAW was first reported on maize during May 2018 (Sharanabasappa et al ., 2018) from the state of Karnataka. Indian maize fields are at present under the frightful attack of the invasive pest Fall Armyworm. In Rajasthan, FAW was detected for the first time in early 2019 from the Southern region of the state on Rabi maize, which was confirmed by the morphological and molecular method (Babu et al., 2019 ). FAW larvae attack occurs in vegetative stages (leaves, stem, and branches) and reproductive stages (tasselling, silking, cob formation and senescence) of maize. According to Day et al. ( 2017 ), if S. Frugiperda is not controlled, maize yield losses could range from 8.3 to 20.6 million tonnes per year. The urgent need for biological control of the FAW arises from its devastating impact on crop yields and the severe limitations of sole reliance on chemical insecticides, which include rising resistance, environmental harm, and high costs for small-hold farmers (Ghafar et al., 2025 ). This makes the development of accessible, alternative strategies a critical priority. Consequently, the importance of biological control is paramount, as it provides a sustainable and ecologically balanced solution by leveraging native natural enemies to suppress pest populations in the long term. This approach is a cornerstone of Integrated Pest Management, ensuring economic viability and environmental health while safeguarding food security (Sutil et al., 2025 ). In India, a diverse array of natural enemies of S. frugiperda has been documented across the country. These include egg and larval parasitoids, as well as predators that have adapted to attack this invasive pest (Gupta et al., 2020 ). Key larval parasitoids identified include Chelonus spp., Bracon brevicornis, Campoletis chlorideae , and Cotesia spp., while the egg parasitoid Telenomus remus has shown significant potential. This indigenous guild of natural enemies plays a crucial role in naturally suppressing FAW and forms a sustainable foundation for developing conservation biological control strategies within Integrated Pest Management (IPM) programs for the country (Kafle and Joshi, 2025 ). Various species within the Cheloninae subfamily (Hymenoptera) serve as efficient natural enemies of economically significant crop pests, such as the fall armyworm (FAW). For example, Chelonus blackbruni and Chelonus formasonas a solitary egg-larval endoparasitoid in which a single parasitoid grub develops within and eventually emerges from each infected host larva demonstrated high rates of parasitism against FAW in maize fields in India (Kumar et al. 2025 ). In this study we investigated the effectiveness of mass-producing C. blackbruni and C. formasonas using the host S. frugiperda . The initial phase of the research measured the parasitism rate and development duration of these braconids when exposed to FAW eggs at different stages of maturity. The findings from our study can help inform the development of biocontrol strategies that utilize mass-produced native Chelonus parasitoids to manage FAW in regions where this invasive pest is prevalent. Methods FAW rearing The S. frugiperda larvae were collected from Fall Armyworm rearing laboratory, Department of Entomology, Rajasthan College of Agriculture, MPUAT, Udaipur. Larvae were maintained individually to avoid cannibalism. Later, larvae were taken to the insectary to be reared using an artificialdiet under controlled conditions of temperature (26 ± 2°C), relativehumidity (75 ± 5%), and a photoperiod of 12:12 h (light/dark) (Amer et al. , 2025). The pupae were kept in glass cagesuntil adult emergence. Ten adults (5 females and 5 males) were placein Kraft paper bags for mating and oviposition.Adults were feed a 10% honey solution dispensed on cotton wool, and was kept under the conditions described above. S. frugiperda eggmasses deposited in Kraft paper bags were collected daily (Jindal et al. 2022 ). Parasitoids culture The neonates of S. frugiperda hatched from eggs were reared on the maize leaves at 27 ± 2 o C and 65 ± 2 relative humidity. The cocoons of Chelonus blackbruni collected from parasitized FAW larvae were kept for the adult emergence. Parasitoids were subjected to further multiplication. The adult pair of Chelonus blackburni was taken after 24 hours and exposed to the laboratory-reared FAW eggs for parasitism in test tubes and jars. Neonates of FAW hatched from parasitized eggs were reared on the artificial diet. Adult longevity and developmental period were calculated. The parasitism rate and emergence rate were calculated with the following formulae (Gupta et al. , 2019). Pupation rate = (Number of cocoons/total number of parasitoid larvae) × 100% Emergence rate = (Number of parasitoids/total number of cocoons) × 100% Statistical analysis The data of the developmental period of Chelonus spp. along with parasitism potential were analyzed with mean ± S.E. along with range. Results The life cycle study of Chelonus formosanus and Chelonus blackburni in laboratory conditions revealed that the incubation period of C. formosanus and C.blackburni were 24.27 ± 24.27 and 24.64 ± 1.87, respectively. The larval period of the first instar grub was recorded as 2.55 ± 0.26 and 2.82 ± 0.24 days. The second instar grubs last for 3.09 ± 0.22 and 3.27 ± 0.15 days, while the third instar grubs last for 3.36 ± 0.21 and 3.27 ± 0.29 days. The fourth instar grubs of parasitoids lasted for 3.82 ± 0.19 and 4.18 ± 0.19. Whereas, the fifth instar grubs lasted for 4.73 ± 0.29 and 5.00 ± 0.24, respectively. The total larval periodwas 17.55 and 18.55 days for C. formosanus and C.blackburni , respectively. While the pupal period was 10.27 ± 0.68 and 11.09 days for C. formosanus and C.blackburni , respectively. The total developmental periods of both braconids were 27.82 and 29.65, respectively. The C. formosanus laid 192.18 ± 7.56 eggs while the female of C.blackburni laid 198.73 ± 13.09 eggs on S. frugiperda eggs. The female wasps of C. formosanus last for 6.02 ± 0.64 days and 6.55 ± 0.43 days for C.blackburni. While the male wasps of C. formosanus last 4.18 ± 0.34 days and C.blackburni last for 4.64 ± 0.50 days. (Table 1 & 2 ) In terms of parasitism potential of Chelonus spp. was evaluated and found that 66.17 ± 1.80 and 59.61 ± 1.32 pupation percent for C. formosanus and C.blackburni , respectively. While the emergence rate was 63.84 ± 1.57 and 52.44 ± 0.57 per cent for C. formosanus and C.blackburni , respectively. The results of the present investigation showed that C. formosanus was more effective against S. Frugiperda (Table 3 ). Table 1 Life cycle of Chelonus formosanus on fall armyworm S. frugiperda in laboratory conditions Biological parametres Duration Mean ± S.E. (Range) Incubation period (hours) 24.27 ± 24.27 (14–32) Larval period (days) Ist instar 2.55 ± 0.26 (1–4) 2nd instar 3.09 ± 0.22 (2–4) 3rd instar 3.36 ± 0.21(2–4) 4th instar 3.82 ± 0.19 (3–5) 5th instar 4.73 ± 0.29 (4–6) Total larval period (days) 17.55 (16–20) Pupal period (days) 10.27 ± 0.68 (7–13) Total developmental period (days) 27.82 (24–32) Fecundity (eggs female − 1 ) 192.18 ± 7.56 (148–216) Female adult longevity (days) 6.02 ± 0.64 (4–6) Male adult longevity (days) 4.18 ± 0.34 (3–6) Data represent mean ± S.E. Table 2 Life cycle of Chelonus blackburni on fall armyworm S. frugiperda in laboratory conditions Biological parametres Duration Mean ± S.E. (Range) Incubation period (hours) 24.64 ± 1.87 (15–36) Larval period (days) Ist instar 2.82 ± 0.24 (2–4) 2nd instar 3.27 ± 0.15 (3–4) 3rd instar 3.27 ± 0.29 (2–4) 4th instar 4.18 ± 0.19(3–5) 5th instar 5.00 ± 0.24(4–6) Total larval period (days) 18.55(16–21) Pupal period (days) 11.09 ± 0.82(7–15) Total developmental period (days) 29.65(26–34) Fecundity (eggs female − 1 ) 198.73 ± 13.09 (119–245) Female adult longevity (days) 6.55 ± 0.43(4–9) Male adult longevity (days) 4.64 ± 0.50 (3–7) Data represent mean ± S.E. Table 3 Parasitism potential of Chelonus formasonas and Chelonus blackburni on FAW in laboratory conditions Particulars Chelonus formasonas Chelonus blackburni Pupation rate (%) 66.17 ± 1.80 (51.85-75.00) 59.61 ± 1.32 (47.62–71.43) Emergence rate (%) 63.84 ± 1.57 (54.55–76.47) 52.44 ± 0.57 (30.00-70.59) Data represent mean ± S.E. Discussion The Chelonus formosanus laid 192.18 ± 7.56 eggs, while the C.blackburni laid 198.73 ± 13.09 eggs in S. frugiperda eggs. The parasitism potential of the species was evaluated, with C. formosanus showing a higher effectiveness in parasitising S. frugiperda . Our results for the biology and parasitism potential of braconids agree with those of Shen et al. ( 2023 ) investigated the parasitism suitability of C. bifoveolatus on 0- to 2-day FAW eggs in laboratory conditions. Results showed that C. bifoveolatus successfully developed on all FAW eggs, with significant differences in egg-larva developmental duration. The parasitism, pupation, emergence, and female rates were generally high, suggesting C. bifoveolatus as a potential biological control agent against FAW in Africa. As FAW hosts age, parasitism by Trichogramma mwanzai and Trichogrammatoidea lutea reduces dramatically (Sun et al., 2021 ). T. dendrolimi parasitized Mythimna separata (Walker) eggs, with similar results (Hou et al., 2018 ). However, the parasitoid wasp Chelonus bifoveolatus can successfully develop on eggs of its natural host, the FAW, and the factitious host Corcyra cephalonica , with parasitism possible even on older eggs. While rearing on FAW resulted in faster population growth, rearing on C. cephalonica still produced wasps with substantial pest suppression potential, capable of parasitizing over 1,500 FAW eggs per individual in a life time. This confirms the suitability of C. cephalonica as a reliable host for mass-rearing this wasp for biocontrol programs (Shen et al. 2025 ; Kaur et al., 2025 ). Similarly, Agboyi et al. ( 2020 ) also reported that theten species were found parasitizing the pest, including two egg parasitoids, one egg–larval, five larval and two larval–pupal parasitoids. The two most abundant parasitoids in both countries were two Braconidae: the egg-larval parasitoid Chelonus bifoveolatus and the larval parasitoid Coccygidum luteum. Similarly, Singh et al. ( 2022 ) also reported that two species of egg parasitoids, two species of egg-larval and five species of larval parasitoids against S. frugiperda from farmers’ fields of Southern Rajasthan. Conclusions The demonstrated efficacy and site-specific presence of dominant parasitoids like Chelonus spp. permit their prioritization for mass rearing and conservation biological control programs. Future work should also focus on integrating these types of native parasitoids and investigate the synergistic effects of combining multiple, proven parasitoid species for more resilient and sustainable management of fall armyworm. Declarations Acknowledgements Author contribution Competing Interests The authors declare no competing interests. Funding This study received no funding from any source or agent. Author Contribution Amit Kumar and S. Ramesh Babu conducted the study and collected the data during the course of investigation. Amit Kumar, Devendra Jain and Vikram Singh wrote the manuscript. S. Ramesh Babu and Manoj Kumar helped to prepare the manuscript along with technical assitance and shared their experience about FAW and its biological control. Acknowledgement The corresponding author whould like to thank Dr. S. Ramesh Babu, Head of department, for his understanding and generous suppport along the course of the study, as well as the planning this investigation for destructive FAW in Southern Rajasthan region where maize and sorghum are prominent crops. Data Availability No datasets were generated or analyzed during the present investigation. References Agboyi LK, Goergen G, Beseh P, Mensah SA, Clottey VA, Glikpo R, Kenis M (2020) Parasitoid complex of fall armyworm, Spodoptera frugiperda , in Ghana and Benin. Insects 11:68 Babu SR, Kalyan RK, Joshi S, Balai CM, Mahla MK, Rokadia P (2019) Report of an exotic invasive pest the fall armyworm, Spodoptera frugiperda (JE Smith) on maize in Southern Rajasthan. J entomol zool stud 7:1296–1300 Day R, Abrahams P, Bateman M, Beale T, Clottey V, Cock M, Witt A (2017) Fall armyworm: impacts and implications for Africa. Out pest manage 28:196–201 Ghafar MA, Ramzan M, Haq IU, Akhtar MR, Panhwar WA, Abbas D, Wang L (2025) Sustainable biological control methods for managing fall armyworm ( Spodoptera frugiperda ) in maize cultivation. Biol Sci Tech 35:1088–1123 Goergen G, Kumar PL, Sankung SB, 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 Gupta A, Lalitha Y, Varshney R, Shylesha AN, Van Achterberg C (2020) Chelonus formosanus Sonan (Hymenoptera: Braconidae) an egg-larval parasitoid of the invasive pest Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) amenable to laboratory mass production in India. J Entomol Zool Stu 8:1521–1524 Hou YY, Yang XB, Zang LS, Zhang C, Monticelli LS, Desneux N (2018) Effect of oriental armyworm Mythimna separata egg age on the parasitism and host suitability for five Trichogramma species. J Pest Sci 91:1181–1189 Jindal J, Sharma KP, Shera PS, Cheema HK (2022) Native Parasitoids of Fall Army Worm Spodoptera frugiperda (JE Smith) in Maize. Indian J Entomol e21049 Kafle L, Joshi RC (2025) Fall armyworm threatens Asian rice security: A review of sustainable management strategies. CABI Rev 20:0017 Kaur M, Bhullar M, Kaur R (2025) Invasive pest and diseases in Indian agriculture: Management and case studies. Rev Plant Stu 12:16–25 Kumar A, Babu SR, Singh B, KK, Shruti (2025) First Report on Brachymeria Spp as a Hyperparasitoid of Charops Bicolor from Southern Rajasthan, India. Indian J Entomol 594–596 Montezano DG, Sosa-Gómez DR, Specht A, Roque-Specht VF, Sousa-Silva JC, Paula-Moraes SD, Hunt TE (2018) Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. Afr entomol 26:286–300 Sharanabasappa S, Kalleshwaraswamy CM, Poorani J, Maruthi MS, Pavithra HB, Diraviam J (2019) Natural enemies of Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae), a recent invasive pest on maize in South India. Fla Entomol 102:619–623 Shen Z, Chen YM, Huang M, Tariq H, Tang LD, Wei J, Zang LS (2025) Mass rearing of Chelonus parasitoids with the alternative host Corcyra cephalonica : a promising biocontrol option against fall armyworm Spodoptera frugiperda . Pest Manage Sci 81:7710–7721 Shen Z, Zang ZY, Dai P, Xu W, Nkunika PO, Zang LS (2023) Identification of Chelonus Sp. from Zambia and its performance on different aged eggs of Spodoptera frugiperda . Insects 14:61 Singh B, Babu SR, Dhabhai SK, Kavipriya J, Kumar A (2022) Parasitoid complex of the fall Armyworm, Spodoptera frugiperda (J.E. Smith) in Maize of Southern Rajasthan. Third National Symposium Entomology (2022): Innovation and Enterepreneurship 8–10 December 2022, Hyderabad, India. p. 78 Sun JW, Hu HY, Nkunika POY, Dai P, Xu W, Bao HP, Desneux N, Zang LS (2021) Performance of two Trichogrammatid species from Zambia on fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae). Insects 12:859 Sutil WP, de Bueno F, Roswadoski A, Iasczczaki L, Carneiro RS, Colmenarez GS (2025) YC Improving Telenomus remus (Hymenoptera: Scelionidae) Adoption: Contribution of Different Egg Parasitoid Densities, Fed Adults, and Their Storage for Successful Biological Control of Spodoptera frugiperda (Lepidoptera: Noctuidae). Insects 16: 1032 Additional Declarations No competing interests reported. Cite Share Download PDF Status: Under Review Version 1 posted Editorial decision: Revision requested 01 May, 2026 Reviews received at journal 01 May, 2026 Reviewers agreed at journal 21 Apr, 2026 Reviewers agreed at journal 09 Mar, 2026 Reviews received at journal 05 Mar, 2026 Reviewers agreed at journal 27 Feb, 2026 Reviewers invited by journal 27 Feb, 2026 Editor assigned by journal 13 Feb, 2026 Submission checks completed at journal 13 Feb, 2026 First submitted to journal 03 Feb, 2026 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-8776953","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":598226114,"identity":"d8674104-d145-4cf6-9235-edfd64f78c89","order_by":0,"name":"Amit Kumar","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA8klEQVRIiWNgGAWjYFACxgYwxcbefPDBBzCDsJZGoB4DBj6eY8mGM0BamImzxoBBTiLHTJoHxCekhX/a4fYHH3f8kWOTyDE2tvm1TZ6PmYHxw8cc3Fokbic2Ns48Y2DMxvOs8HFu323DNmYGZsmZ2/BYA9TSzNtmkNjGnrzZOLfnNiNQCxszLx4t8iAtf0FaGBLMpC17btsT1GIA0sII0sKRYibN8ON2IkEthkAtM3vbjIF+AQZyb8Pt5DZmxma8fpG7nf7gw882OTn5dmBU/vhz23Y+kPHhIz7vowDGNjDZQKx6EPhDiuJRMApGwSgYKQAA9gBTgyKDVDsAAAAASUVORK5CYII=","orcid":"","institution":"Rajasthan College of Agriculture, Maharana Pratap University of Agriculture and Technology","correspondingAuthor":true,"prefix":"","firstName":"Amit","middleName":"","lastName":"Kumar","suffix":""},{"id":598226116,"identity":"3508421e-f384-4160-b2f2-b4b77ce81c91","order_by":1,"name":"S. Ramesh Babu","email":"","orcid":"","institution":"Rajasthan College of Agriculture, Maharana Pratap University of Agriculture and Technology","correspondingAuthor":false,"prefix":"","firstName":"S.","middleName":"Ramesh","lastName":"Babu","suffix":""},{"id":598226118,"identity":"2185aba2-17d1-42b2-9e17-44cd0539f2da","order_by":2,"name":"Devendra Jain","email":"","orcid":"","institution":"Rajasthan College of Agriculture, Maharana Pratap University of Agriculture and Technology","correspondingAuthor":false,"prefix":"","firstName":"Devendra","middleName":"","lastName":"Jain","suffix":""},{"id":598226120,"identity":"685ebc96-a0bc-404e-98e5-4ea64ca78504","order_by":3,"name":"Manoj Kumar","email":"","orcid":"","institution":"Post- Graduate College of Agriculture, Dr. Rajendra Prasad Central Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Manoj","middleName":"","lastName":"Kumar","suffix":""},{"id":598226122,"identity":"1edafe22-0aa4-425c-86ae-928f06d70b5e","order_by":4,"name":"Vikram Singh","email":"","orcid":"","institution":"Rajasthan College of Agriculture, Maharana Pratap University of Agriculture and Technology","correspondingAuthor":false,"prefix":"","firstName":"Vikram","middleName":"","lastName":"Singh","suffix":""}],"badges":[],"createdAt":"2026-02-03 14:11:14","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-8776953/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-8776953/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":103907212,"identity":"dad6f1d3-ae13-4877-8ca3-b02c35fab70a","added_by":"auto","created_at":"2026-03-04 11:12:14","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":755797,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-8776953/v1/9b6e8a13-5d75-44af-b3a2-dc433db042dd.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Koinobiont Parasitism and Biology of Braconid Parasitoids on Invasive Fall Armyworm Spodptera frugiperda (J.E. smith) in controlled condtions","fulltext":[{"header":"Background","content":"\u003cp\u003eThe Fall Armyworm (FAW), \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e (J.E. Smith) (Lepidoptera: Noctuidae), is a highly polyphagous, dreaded insect pest native to tropical and subtropical areas of the Americas. The FAW reported to feed on more than 350 plant species belonging to 76 plant families (Montezano et al., \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Due to its massive migratory habit, it causes threat in Africa and Asia and it was first reported in Africa in 2016 (Goergen et al., \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). In India, FAW was first reported on maize during May 2018 (Sharanabasappa \u003cem\u003eet al\u003c/em\u003e., 2018) from the state of Karnataka. Indian maize fields are at present under the frightful attack of the invasive pest Fall Armyworm. In Rajasthan, FAW was detected for the first time in early 2019 from the Southern region of the state on \u003cem\u003eRabi\u003c/em\u003e maize, which was confirmed by the morphological and molecular method (Babu et al., \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). FAW larvae attack occurs in vegetative stages (leaves, stem, and branches) and reproductive stages (tasselling, silking, cob formation and senescence) of maize. According to Day et al. (\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), if \u003cem\u003eS. Frugiperda\u003c/em\u003e is not controlled, maize yield losses could range from 8.3 to 20.6\u0026nbsp;million tonnes per year.\u003c/p\u003e \u003cp\u003eThe urgent need for biological control of the FAW arises from its devastating impact on crop yields and the severe limitations of sole reliance on chemical insecticides, which include rising resistance, environmental harm, and high costs for small-hold farmers (Ghafar et al., \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2025\u003c/span\u003e). This makes the development of accessible, alternative strategies a critical priority. Consequently, the importance of biological control is paramount, as it provides a sustainable and ecologically balanced solution by leveraging native natural enemies to suppress pest populations in the long term. This approach is a cornerstone of Integrated Pest Management, ensuring economic viability and environmental health while safeguarding food security (Sutil et al., \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2025\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIn India, a diverse array of natural enemies of \u003cem\u003eS. frugiperda\u003c/em\u003e has been documented across the country. These include egg and larval parasitoids, as well as predators that have adapted to attack this invasive pest (Gupta et al., \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Key larval parasitoids identified include \u003cem\u003eChelonus\u003c/em\u003e spp., \u003cem\u003eBracon brevicornis, Campoletis chlorideae\u003c/em\u003e, and \u003cem\u003eCotesia\u003c/em\u003e spp., while the egg parasitoid \u003cem\u003eTelenomus remus\u003c/em\u003e has shown significant potential. This indigenous guild of natural enemies plays a crucial role in naturally suppressing FAW and forms a sustainable foundation for developing conservation biological control strategies within Integrated Pest Management (IPM) programs for the country (Kafle and Joshi, \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2025\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eVarious species within the Cheloninae subfamily (Hymenoptera) serve as efficient natural enemies of economically significant crop pests, such as the fall armyworm (FAW).\u003c/p\u003e \u003cp\u003eFor example, \u003cem\u003eChelonus blackbruni\u003c/em\u003e and \u003cem\u003eChelonus formasonas\u003c/em\u003e a solitary egg-larval endoparasitoid in which a single parasitoid grub develops within and eventually emerges from each infected host larva demonstrated high rates of parasitism against FAW in maize fields in India (Kumar et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2025\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIn this study we investigated the effectiveness of mass-producing \u003cem\u003eC. blackbruni\u003c/em\u003e and \u003cem\u003eC. formasonas\u003c/em\u003e using the host \u003cem\u003eS. frugiperda\u003c/em\u003e. The initial phase of the research measured the parasitism rate and development duration of these braconids when exposed to FAW eggs at different stages of maturity.\u003c/p\u003e \u003cp\u003eThe findings from our study can help inform the development of biocontrol strategies that utilize mass-produced native \u003cem\u003eChelonus\u003c/em\u003e parasitoids to manage FAW in regions where this invasive pest is prevalent.\u003c/p\u003e"},{"header":"Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eFAW rearing\u003c/h2\u003e \u003cp\u003eThe \u003cem\u003eS. frugiperda\u003c/em\u003e larvae were collected from Fall Armyworm rearing laboratory, Department of Entomology, Rajasthan College of Agriculture, MPUAT, Udaipur. Larvae were maintained individually to avoid cannibalism. Later, larvae were taken to the insectary to be reared using an artificialdiet under controlled conditions of temperature (26\u0026thinsp;\u0026plusmn;\u0026thinsp;2\u0026deg;C), relativehumidity (75\u0026thinsp;\u0026plusmn;\u0026thinsp;5%), and a photoperiod of 12:12 h (light/dark) (Amer \u003cem\u003eet al.\u003c/em\u003e, 2025). The pupae were kept in glass cagesuntil adult emergence. Ten adults (5 females and 5 males) were placein Kraft paper bags for mating and oviposition.Adults were feed a 10% honey solution dispensed on cotton wool, and was kept under the conditions described above. \u003cem\u003eS. frugiperda\u003c/em\u003e eggmasses deposited in Kraft paper bags were collected daily (Jindal et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2022\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eParasitoids culture\u003c/h3\u003e\n\u003cp\u003eThe neonates of \u003cem\u003eS. frugiperda\u003c/em\u003e hatched from eggs were reared on the maize leaves at 27\u0026thinsp;\u0026plusmn;\u0026thinsp;2 \u003csup\u003eo\u003c/sup\u003eC and 65\u0026thinsp;\u0026plusmn;\u0026thinsp;2 relative humidity. The cocoons of \u003cem\u003eChelonus blackbruni\u003c/em\u003e collected from parasitized FAW larvae were kept for the adult emergence. Parasitoids were subjected to further multiplication. The adult pair of \u003cem\u003eChelonus blackburni\u003c/em\u003e was taken after 24 hours and exposed to the laboratory-reared FAW eggs for parasitism in test tubes and jars. Neonates of FAW hatched from parasitized eggs were reared on the artificial diet. Adult longevity and developmental period were calculated. The parasitism rate and emergence rate were calculated with the following formulae (Gupta \u003cem\u003eet al.\u003c/em\u003e, 2019).\u003c/p\u003e \u003cp\u003ePupation rate = (Number of cocoons/total number of parasitoid larvae) \u0026times; 100%\u003c/p\u003e \u003cp\u003eEmergence rate = (Number of parasitoids/total number of cocoons) \u0026times; 100%\u003c/p\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analysis\u003c/h2\u003e \u003cp\u003eThe data of the developmental period of \u003cem\u003eChelonus\u003c/em\u003e spp. along with parasitism potential were analyzed with mean\u0026thinsp;\u0026plusmn;\u0026thinsp;S.E. along with range.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cp\u003eThe life cycle study of \u003cem\u003eChelonus formosanus\u003c/em\u003e and \u003cem\u003eChelonus blackburni\u003c/em\u003e in laboratory conditions revealed that the incubation period of \u003cem\u003eC. formosanus\u003c/em\u003e and \u003cem\u003eC.blackburni\u003c/em\u003e were 24.27\u0026thinsp;\u0026plusmn;\u0026thinsp;24.27 and 24.64\u0026thinsp;\u0026plusmn;\u0026thinsp;1.87, respectively. The larval period of the first instar grub was recorded as 2.55\u0026thinsp;\u0026plusmn;\u0026thinsp;0.26 and 2.82\u0026thinsp;\u0026plusmn;\u0026thinsp;0.24 days. The second instar grubs last for 3.09\u0026thinsp;\u0026plusmn;\u0026thinsp;0.22 and 3.27\u0026thinsp;\u0026plusmn;\u0026thinsp;0.15 days, while the third instar grubs last for 3.36\u0026thinsp;\u0026plusmn;\u0026thinsp;0.21 and 3.27\u0026thinsp;\u0026plusmn;\u0026thinsp;0.29 days. The fourth instar grubs of parasitoids lasted for 3.82\u0026thinsp;\u0026plusmn;\u0026thinsp;0.19 and 4.18\u0026thinsp;\u0026plusmn;\u0026thinsp;0.19. Whereas, the fifth instar grubs lasted for 4.73\u0026thinsp;\u0026plusmn;\u0026thinsp;0.29 and 5.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.24, respectively. The total larval periodwas 17.55 and 18.55 days for \u003cem\u003eC. formosanus\u003c/em\u003e and \u003cem\u003eC.blackburni\u003c/em\u003e, respectively. While the pupal period was 10.27\u0026thinsp;\u0026plusmn;\u0026thinsp;0.68 and 11.09 days for \u003cem\u003eC. formosanus\u003c/em\u003e and \u003cem\u003eC.blackburni\u003c/em\u003e, respectively. The total developmental periods of both braconids were 27.82 and 29.65, respectively. The \u003cem\u003eC. formosanus\u003c/em\u003e laid 192.18\u0026thinsp;\u0026plusmn;\u0026thinsp;7.56 eggs while the female of \u003cem\u003eC.blackburni\u003c/em\u003e laid 198.73\u0026thinsp;\u0026plusmn;\u0026thinsp;13.09 eggs on\u003cem\u003eS. frugiperda\u003c/em\u003e eggs. The female wasps of \u003cem\u003eC. formosanus\u003c/em\u003e last for 6.02\u0026thinsp;\u0026plusmn;\u0026thinsp;0.64 days and 6.55\u0026thinsp;\u0026plusmn;\u0026thinsp;0.43 days for \u003cem\u003eC.blackburni.\u003c/em\u003e While the male wasps of \u003cem\u003eC. formosanus\u003c/em\u003elast 4.18\u0026thinsp;\u0026plusmn;\u0026thinsp;0.34 days and \u003cem\u003eC.blackburni\u003c/em\u003e last for 4.64\u0026thinsp;\u0026plusmn;\u0026thinsp;0.50 days. (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e \u0026amp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e )\u003c/p\u003e \u003cp\u003eIn terms of parasitism potential of \u003cem\u003eChelonus\u003c/em\u003e spp. was evaluated and found that 66.17\u0026thinsp;\u0026plusmn;\u0026thinsp;1.80 and 59.61\u0026thinsp;\u0026plusmn;\u0026thinsp;1.32 pupation percent for \u003cem\u003eC. formosanus\u003c/em\u003e and \u003cem\u003eC.blackburni\u003c/em\u003e, respectively. While the emergence rate was 63.84\u0026thinsp;\u0026plusmn;\u0026thinsp;1.57 and 52.44\u0026thinsp;\u0026plusmn;\u0026thinsp;0.57 per cent for \u003cem\u003eC. formosanus\u003c/em\u003e and \u003cem\u003eC.blackburni\u003c/em\u003e, respectively. The results of the present investigation showed that \u003cem\u003eC. formosanus\u003c/em\u003e was more effective against\u003cem\u003eS. Frugiperda\u003c/em\u003e (Table\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eLife cycle of \u003cem\u003eChelonus formosanus\u003c/em\u003e on fall armyworm \u003cem\u003eS. frugiperda\u003c/em\u003e in laboratory conditions\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBiological parametres\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eDuration Mean\u0026thinsp;\u0026plusmn;\u0026thinsp;S.E. (Range)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eIncubation period (hours)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e24.27\u0026thinsp;\u0026plusmn;\u0026thinsp;24.27 (14\u0026ndash;32)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e \u003cp\u003e\u003cb\u003eLarval period (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"1\" nameend=\"c3\" namest=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eIst instar\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e2.55\u0026thinsp;\u0026plusmn;\u0026thinsp;0.26 (1\u0026ndash;4)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003e2nd instar\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e3.09\u0026thinsp;\u0026plusmn;\u0026thinsp;0.22 (2\u0026ndash;4)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003e3rd instar\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e3.36\u0026thinsp;\u0026plusmn;\u0026thinsp;0.21(2\u0026ndash;4)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003e4th instar\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e3.82\u0026thinsp;\u0026plusmn;\u0026thinsp;0.19 (3\u0026ndash;5)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003e5th instar\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e4.73\u0026thinsp;\u0026plusmn;\u0026thinsp;0.29 (4\u0026ndash;6)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eTotal larval period (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e17.55 (16\u0026ndash;20)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003ePupal period (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e10.27\u0026thinsp;\u0026plusmn;\u0026thinsp;0.68 (7\u0026ndash;13)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eTotal developmental period (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e27.82 (24\u0026ndash;32)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eFecundity (eggs female\u003c/b\u003e\u003csup\u003e\u003cb\u003e\u0026minus;\u0026thinsp;1\u003c/b\u003e\u003c/sup\u003e\u003cb\u003e)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e192.18\u0026thinsp;\u0026plusmn;\u0026thinsp;7.56 (148\u0026ndash;216)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eFemale adult longevity (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e6.02\u0026thinsp;\u0026plusmn;\u0026thinsp;0.64 (4\u0026ndash;6)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eMale adult longevity (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e4.18\u0026thinsp;\u0026plusmn;\u0026thinsp;0.34 (3\u0026ndash;6)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eData represent mean\u0026thinsp;\u0026plusmn;\u0026thinsp;S.E.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eLife cycle of \u003cem\u003eChelonus blackburni\u003c/em\u003e on fall armyworm \u003cem\u003eS. frugiperda in\u003c/em\u003e laboratory conditions\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"2\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBiological parametres\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eDuration Mean\u0026thinsp;\u0026plusmn;\u0026thinsp;S.E. (Range)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eIncubation period (hours)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e24.64\u0026thinsp;\u0026plusmn;\u0026thinsp;1.87 (15\u0026ndash;36)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eLarval period (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eIst instar\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2.82\u0026thinsp;\u0026plusmn;\u0026thinsp;0.24 (2\u0026ndash;4)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003e2nd instar\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3.27\u0026thinsp;\u0026plusmn;\u0026thinsp;0.15 (3\u0026ndash;4)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003e3rd instar\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3.27\u0026thinsp;\u0026plusmn;\u0026thinsp;0.29 (2\u0026ndash;4)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003e4th instar\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e4.18\u0026thinsp;\u0026plusmn;\u0026thinsp;0.19(3\u0026ndash;5)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003e5th instar\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.24(4\u0026ndash;6)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eTotal larval period (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e18.55(16\u0026ndash;21)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003ePupal period (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e11.09\u0026thinsp;\u0026plusmn;\u0026thinsp;0.82(7\u0026ndash;15)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eTotal developmental period (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e29.65(26\u0026ndash;34)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eFecundity (eggs female\u003c/b\u003e\u003csup\u003e\u003cb\u003e\u0026minus;\u0026thinsp;1\u003c/b\u003e\u003c/sup\u003e\u003cb\u003e)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e198.73\u0026thinsp;\u0026plusmn;\u0026thinsp;13.09 (119\u0026ndash;245)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eFemale adult longevity (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e6.55\u0026thinsp;\u0026plusmn;\u0026thinsp;0.43(4\u0026ndash;9)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eMale adult longevity (days)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e4.64\u0026thinsp;\u0026plusmn;\u0026thinsp;0.50 (3\u0026ndash;7)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eData represent mean\u0026thinsp;\u0026plusmn;\u0026thinsp;S.E.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab3\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 3\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eParasitism potential of \u003cem\u003eChelonus\u003c/em\u003e formasonas and \u003cem\u003eChelonus blackburni\u003c/em\u003e on FAW in laboratory conditions\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eParticulars\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cem\u003eChelonus formasonas\u003c/em\u003e\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cem\u003eChelonus blackburni\u003c/em\u003e\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003ePupation rate (%)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e66.17\u0026thinsp;\u0026plusmn;\u0026thinsp;1.80\u003c/p\u003e \u003cp\u003e(51.85-75.00)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e59.61\u0026thinsp;\u0026plusmn;\u0026thinsp;1.32\u003c/p\u003e \u003cp\u003e(47.62\u0026ndash;71.43)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eEmergence rate (%)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e63.84\u0026thinsp;\u0026plusmn;\u0026thinsp;1.57\u003c/p\u003e \u003cp\u003e(54.55\u0026ndash;76.47)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e52.44\u0026thinsp;\u0026plusmn;\u0026thinsp;0.57\u003c/p\u003e \u003cp\u003e(30.00-70.59)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eData represent mean\u0026thinsp;\u0026plusmn;\u0026thinsp;S.E.\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eThe \u003cem\u003eChelonus formosanus\u003c/em\u003e laid 192.18\u0026thinsp;\u0026plusmn;\u0026thinsp;7.56 eggs, while the \u003cem\u003eC.blackburni\u003c/em\u003e laid 198.73\u0026thinsp;\u0026plusmn;\u0026thinsp;13.09 eggs in \u003cem\u003eS. frugiperda\u003c/em\u003e eggs. The parasitism potential of the species was evaluated, with \u003cem\u003eC. formosanus\u003c/em\u003eshowing a higher effectiveness in parasitising\u003cem\u003eS. frugiperda\u003c/em\u003e. Our results for the biology and parasitism potential of braconids agree with those of Shen et al. (\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2023\u003c/span\u003e) investigated the parasitism suitability of \u003cem\u003eC. bifoveolatus\u003c/em\u003e on 0- to 2-day FAW eggs in laboratory conditions. Results showed that \u003cem\u003eC. bifoveolatus\u003c/em\u003e successfully developed on all FAW eggs, with significant differences in egg-larva developmental duration. The parasitism, pupation, emergence, and female rates were generally high, suggesting \u003cem\u003eC. bifoveolatus\u003c/em\u003e as a potential biological control agent against FAW in Africa. As FAW hosts age, parasitism by \u003cem\u003eTrichogramma mwanzai\u003c/em\u003e and \u003cem\u003eTrichogrammatoidea lutea\u003c/em\u003e reduces dramatically (Sun et al., \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). \u003cem\u003eT. dendrolimi\u003c/em\u003e parasitized \u003cem\u003eMythimna separata\u003c/em\u003e (Walker) eggs, with similar results (Hou et al., \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). However, the parasitoid wasp \u003cem\u003eChelonus bifoveolatus\u003c/em\u003e can successfully develop on eggs of its natural host, the FAW, and the factitious host \u003cem\u003eCorcyra cephalonica\u003c/em\u003e, with parasitism possible even on older eggs. While rearing on FAW resulted in faster population growth, rearing on \u003cem\u003eC. cephalonica\u003c/em\u003e still produced wasps with substantial pest suppression potential, capable of parasitizing over 1,500 FAW eggs per individual in a life time. This confirms the suitability of \u003cem\u003eC. cephalonica\u003c/em\u003e as a reliable host for mass-rearing this wasp for biocontrol programs (Shen et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2025\u003c/span\u003e; Kaur et al., \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2025\u003c/span\u003e). Similarly, Agboyi et al. (\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2020\u003c/span\u003e) also reported that theten species were found parasitizing the pest, including two egg parasitoids, one egg\u0026ndash;larval, five larval and two larval\u0026ndash;pupal parasitoids. The two most abundant parasitoids in both countries were two Braconidae: the egg-larval parasitoid \u003cem\u003eChelonus bifoveolatus\u003c/em\u003e and the larval parasitoid \u003cem\u003eCoccygidum luteum.\u003c/em\u003e Similarly, Singh et al. (\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2022\u003c/span\u003e) also reported that two species of egg parasitoids, two species of egg-larval and five species of larval parasitoids against \u003cem\u003eS. frugiperda\u003c/em\u003efrom farmers\u0026rsquo; fields of Southern Rajasthan.\u003c/p\u003e"},{"header":"Conclusions","content":"\u003cp\u003eThe demonstrated efficacy and site-specific presence of dominant parasitoids like \u003cem\u003eChelonus\u003c/em\u003e spp. permit their prioritization for mass rearing and conservation biological control programs. Future work should also focus on integrating these types of native parasitoids and investigate the synergistic effects of combining multiple, proven parasitoid species for more resilient and sustainable management of fall armyworm.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthor contribution\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\u003cp\u003e \u003cstrong\u003eCompeting Interests\u003c/strong\u003e \u003cp\u003eThe authors declare no competing interests.\u003c/p\u003e \u003c/p\u003e\u003ch2\u003eFunding\u003c/h2\u003e \u003cp\u003eThis study received no funding from any source or agent.\u003c/p\u003e\u003ch2\u003eAuthor Contribution\u003c/h2\u003e\u003cp\u003eAmit Kumar and S. Ramesh Babu conducted the study and collected the data during the course of investigation. Amit Kumar, Devendra Jain and Vikram Singh wrote the manuscript. S. Ramesh Babu and Manoj Kumar helped to prepare the manuscript along with technical assitance and shared their experience about FAW and its biological control.\u003c/p\u003e\u003ch2\u003eAcknowledgement\u003c/h2\u003e\u003cp\u003eThe corresponding author whould like to thank Dr. S. Ramesh Babu, Head of department, for his understanding and generous suppport along the course of the study, as well as the planning this investigation for destructive FAW in Southern Rajasthan region where maize and sorghum are prominent crops.\u003c/p\u003e\u003ch2\u003eData Availability\u003c/h2\u003e\u003cp\u003eNo datasets were generated or analyzed during the present investigation.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eAgboyi LK, Goergen G, Beseh P, Mensah SA, Clottey VA, Glikpo R, Kenis M (2020) Parasitoid complex of fall armyworm, \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e, in Ghana and Benin. 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J Entomol Zool Stu 8:1521\u0026ndash;1524\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHou YY, Yang XB, Zang LS, Zhang C, Monticelli LS, Desneux N (2018) Effect of oriental armyworm \u003cem\u003eMythimna separata\u003c/em\u003e egg age on the parasitism and host suitability for five \u003cem\u003eTrichogramma\u003c/em\u003e species. J Pest Sci 91:1181\u0026ndash;1189\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJindal J, Sharma KP, Shera PS, Cheema HK (2022) Native Parasitoids of Fall Army Worm \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e (JE Smith) in Maize. Indian J Entomol e21049\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKafle L, Joshi RC (2025) Fall armyworm threatens Asian rice security: A review of sustainable management strategies. 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Pest Manage Sci 81:7710\u0026ndash;7721\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eShen Z, Zang ZY, Dai P, Xu W, Nkunika PO, Zang LS (2023) Identification of \u003cem\u003eChelonus\u003c/em\u003e Sp. from Zambia and its performance on different aged eggs of \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e. Insects 14:61\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSingh B, Babu SR, Dhabhai SK, Kavipriya J, Kumar A (2022) Parasitoid complex of the fall Armyworm, \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e (J.E. Smith) in Maize of Southern Rajasthan. Third National Symposium Entomology (2022): Innovation and Enterepreneurship 8\u0026ndash;10 December 2022, Hyderabad, India. p. 78\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSun JW, Hu HY, Nkunika POY, Dai P, Xu W, Bao HP, Desneux N, Zang LS (2021) Performance of two Trichogrammatid species from Zambia on fall armyworm, \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e (J. E. Smith) (Lepidoptera: Noctuidae). Insects 12:859\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSutil WP, de Bueno F, Roswadoski A, Iasczczaki L, Carneiro RS, Colmenarez GS (2025) YC Improving \u003cem\u003eTelenomus remus\u003c/em\u003e (Hymenoptera: Scelionidae) Adoption: Contribution of Different Egg Parasitoid Densities, Fed Adults, and Their Storage for Successful Biological Control of \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e (Lepidoptera: Noctuidae). Insects 16: 1032\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"egyptian-journal-of-biological-pest-control","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"ebpc","sideBox":"Learn more about [Egyptian Journal of Biological Pest Control](http://ejbpc.springeropen.com)","snPcode":"41938","submissionUrl":"https://submission.springernature.com/new-submission/41938/3","title":"Egyptian Journal of Biological Pest Control","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Springer Open","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Parasitism potential, Chelonus formosanus, Chelonus blackburni, Life cycle, Spodoptera frugiperda","lastPublishedDoi":"10.21203/rs.3.rs-8776953/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-8776953/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eBackground\u003c/h2\u003e \u003cp\u003eThe Fall Armyworm highly destructive insect pests across the world. The native parastoid species such as \u003cem\u003eChelonus\u003c/em\u003e spp. is prominent natural enemy of this pest. The natural control of \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e may achieved by parasitods be able to strong tool.\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e \u003cp\u003eThis study compared the life cycles and effectiveness of two parasitoid wasps, \u003cem\u003eChelonus formosanus\u003c/em\u003e and \u003cem\u003eChelonus blackburni\u003c/em\u003e, in a laboratory conditions. The key developmental durations for \u003cem\u003eChelonus formosanus\u003c/em\u003e and \u003cem\u003eChelonus blackburni\u003c/em\u003e were as follows an incubation period of 24.27 and 24.64 hours, a total larval period of 17.55 and 18.55 days and a pupal period of 10.27 and 11.09 days, respectively. This resulted in a total development time of 27.82 days for \u003cem\u003eChelonus formosanus\u003c/em\u003e and 29.65 days for \u003cem\u003eChelonus blackburni\u003c/em\u003e. Adult females laid approximately 192 and 199 eggs on \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e eggs and lived for about 6.0 and 6.6 days, respectively. Adult males lived for roughly 4.2 and 4.6 days, respectively. The parasitism potential was also evaluated. Following exposure, 66.2% of hosts parasitized by \u003cem\u003eChelonus formosanus\u003c/em\u003e and 59.6% parasitized by \u003cem\u003eChelonus blackburni\u003c/em\u003e reached the pupation stage. The successful emergence rate of adult wasps from these pupae was 63.8% for \u003cem\u003eChelonus formosanus\u003c/em\u003e and 52.4% for \u003cem\u003eChelonus blackburni\u003c/em\u003e.\u003c/p\u003e\u003ch2\u003eConclusion\u003c/h2\u003e \u003cp\u003eThe results indicate that \u003cem\u003eChelonus formosanus\u003c/em\u003e demonstrated greater effectiveness as a biological control agent against \u003cem\u003eS. frugiperda\u003c/em\u003e under the tested conditions.\u003c/p\u003e","manuscriptTitle":"Koinobiont Parasitism and Biology of Braconid Parasitoids on Invasive Fall Armyworm Spodptera frugiperda (J.E. smith) in controlled condtions","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2026-03-04 11:11:04","doi":"10.21203/rs.3.rs-8776953/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2026-05-01T23:19:37+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-05-01T12:47:00+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"292254946134145881807232637461828669069","date":"2026-04-22T03:10:35+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"71484848064434505643646713074781757156","date":"2026-03-09T12:07:19+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-03-05T16:50:08+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"141810065060819336425796008287485073978","date":"2026-02-27T14:45:49+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2026-02-27T13:03:19+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2026-02-13T16:08:08+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2026-02-13T16:04:50+00:00","index":"","fulltext":""},{"type":"submitted","content":"Egyptian Journal of Biological Pest Control","date":"2026-02-03T13:31:43+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"egyptian-journal-of-biological-pest-control","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"ebpc","sideBox":"Learn more about [Egyptian Journal of Biological Pest Control](http://ejbpc.springeropen.com)","snPcode":"41938","submissionUrl":"https://submission.springernature.com/new-submission/41938/3","title":"Egyptian Journal of Biological Pest Control","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Springer Open","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"8340a583-112a-48ea-9317-431718c21f23","owner":[],"postedDate":"March 4th, 2026","published":true,"recentEditorialEvents":[{"type":"decision","content":"Revision requested","date":"2026-05-01T23:19:37+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-05-01T12:47:00+00:00","index":27,"fulltext":""}],"rejectedJournal":[],"revision":"","amendment":"","status":"under-review","subjectAreas":[],"tags":[],"updatedAt":"2026-05-11T10:09:59+00:00","versionOfRecord":[],"versionCreatedAt":"2026-03-04 11:11:04","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-8776953","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-8776953","identity":"rs-8776953","version":["v1"]},"buildId":"XKTyCvWXoU3ODBz1xrDgd","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}