A comprehensive review of Chelonus s. str. Panzer (Hymenoptera: Braconidae: Cheloninae) with a special reference to the species associated with fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae)
Authors
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Department of Agriculture, Regional Field Office-IVA-CALABARZON, Regional Crop Protection Center, Marawoy, Lipa City, Batangas ,PH
ORLANDO A. CALCETAS -
Philippine Rice Research Institute, Maligaya, Science City Muñoz, Nueva Ecija 3119 ,PHRAVINDRA CHANDRA JOSHI
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Biodiversity Centre/Biological Control Centre for Africa, International Institute of Tropical Agriculture (IITA-Benin), 08- 01000 Cotonou ,BJGEORG GOERGEN
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ICAR-National Bureau of Agricultural Insect Resources, P.B. No. 2491, H.A. Farm Post, Bellary Road, Hebbal, Bengaluru – 560024, Karnataka ,INRICHA VARSHNEY
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Former Professor, Department of Entomology, Tamil Nadu Agricultural University, Coimbatore -641003, Tamil Nadu ,INM. S. VENUGOPAL
DOI:
https://doi.org/10.18311/jbc/2024/43637Keywords:
Fall armyworm, natural enemies, parasitoid, waspAbstract
The genus Chelonus s. str. (Chelonus) Panzer (Hymenoptera: Braconidae: Cheloninae) is reviewed with particular focus on species associated with fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae). Additionally, information on the biology and various mass-rearing techniques of the enumerated species are furnished, underlining their significance in biological control and integrated pest management strategies.
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Copyright (c) 2024 Orlando Adona A. Calcetas, Ravindra Chandra Joshi, Georg Goergen, Richa Varshney, M.S. Venugopal (Author)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Accepted 2024-06-14
Published 2023-06-28
References
Arambourg, Y., Pralavorio, R., and Chabot, B. 1970. The possibility of rearing Ageniaspis fuscicollis praysincola Silv. a parasite of Prays oleae Bern. (Lep. Hyponomeutidae) in a substitute host. Ann Zoo Ecol Anim, 2: 657-658. https://www.cabdirect.org/cabdirect/ abstract/19730503073
Agboyi, L. K., Goergen, G., Beseh, P., Mensah, S. A., Clottey, V. A., Glikpo, R., … Day, R. 2020. Parasitoid complex of fall armyworm, Spodoptera frugiperda, in Ghana and Benin. Insects, 11(2): 68. https://doi.org/10.3390/ insects11020068
Ahissou, B. R., Sawadogo, W.M., Bokonon-Ganta, A., Somda, I., and Verheggen, F. 2021. Integrated pest management options for the fall armyworm Spodoptera frugiperda in West Africa: Challenges and opportunities. A review. Biotechnol Agron Soc Environ, 25(3): 192-207. https:// doi.org/10.25518/1780-4507.19125
Amadou, L., Baoua, I., Ba, M. N., Karimoune, L., and Muniappan, R. 2018. Native parasitoids recruited by the invaded fall armyworm in Niger. Indian J Entomol, 80(4): 1253-1255. https://doi.org/10.5958/0974- 8172.2018.00338.3
Ashley, T. R. 1986. Geographical distributions and parasitization levels for parasitoids of the fall armyworm, Spodoptera frugiperda. Fla Entomol, 69(3): 516-524. https://doi.org/10.2307/3495384
Ashmead, W. H. 1904. Descriptions of new genera and species of Hymenoptera from the Philippines Islands. Proc US Nat Mus, 28(1387): 127-158. https://doi. org/10.5479/si.00963801.28-1387.127
Bahena, J. F., and Cortez, M. E. 2015. Gusano cogollero del maíz, Spodoptera frugiperda (Lepidoptera: Noctuidae). In: Arredondo BHC (ed), Casos de Control Biológico en México 2. Guadalajara, Jalisco, México: Biblioteca Básica de Agricultura, p. 181-250.
Baltazar, C. R. 1962. The genera of parasitic Hymenoptera in the Philippines, Part 1. Pac Insects, 4(4): 737-771. http://hbs.bishopmuseum.org/pi/pdf/4(4)-737.pdf
Baringbing, W.A. 1982. Laporan perjalanan dinas ke Nusa Tenggara Timur. Balai Penelitian Tanaman Industry, Bogor, Indonesia, Unpublished.
Baringbing, W. A., and Baringbing, B. 1984. Studies on Chelonus sp. a parasite of the coconut moth Batrachedra arenosella. Trop Pest Manag, 30(2): 207 p. https://doi. org/10.1080/09670878409370877
Belshaw, R., Fitton, M., Herniou, E., Gimeno, C., and Quicke, D. L. J. 1998. A phylogenetic reconstruction of the Ichneumonoidea (Hymenoptera) based on the D2 variable region of 28S ribosomal RNA. Syst Entomol, 23(2): 109-23. https://doi.org/10.1046/j.1365- 3113.1998.00046.x
Bernardi, D., Salmeron, E., Horikoshi, R. J., Bernardi, O., Dourado, P.M., Carvaletho, R. A. … Omoto, C. 2015. Cross-resistance between Cry1 proteins in fall armyworm (Spodoptera frugiperda) may affect the durability of current pyramided Bt maize hybrids in Brazil. PLoS ONE, 10(10): 140-130. https://doi. org/10.1371/journal.pone.0140130
Beyarslan, A. 2021. Taxonomic studies on Cheloninae (Hymenoptera, Braconidae) fauna of Northeastern Anatolia region (Ardahan, Erzurum, Iğdır, and Kars) of Turkey. Nat Somogy, 36: 111-124. https://doi. org/10.24394/natsom.2021.36.111
Biondi, A., Desneux, N., Siscaro, G., and Zappalà, L. 2012. Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: Selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere, 87(7): 803-812. https://doi. org/10.1016/j. chemosphere.2011.12.082
Calcetas, O. A., Joshi, R. C., Gupta, A., Ranjith, A. P., Madrid, M. A., and Fameronag, J. 2023. New record of CALCETAS et al. the egg-larval parasitoid, Chelonus formosanus Sonan of Fall Armyworm, Spodoptera frugiperda (J.E. Smith) in the Philippines. J Plant Prot, 7(2): 103-114.
Carrillo-Sánchez, J. L. 1985. Evolution of biological control in Mexico. Folia Entomol Mex, 65: 139-146.
Casmuz, A., Juarez, M. L., Socias, M. G., Murua, M. G., Prieto, S., Medina, S., … Gastaminzaet, G. 2010. Review of the host plants of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). Rev Soc Entomol Arg, 69(3-4): 209-231. https://www.biotaxa.org/RSEA/ article/view/28610
Chen, X. X., and van Achterberg, C. 1997. Revision of the subfamily Euphorinae (excluding the tribe Meteorini Cresson) (Hymenoptera: Braconidae) from China. Zool Verh, 313(1): 1-217. https://repository.naturalis.nl/ pub/317826
Chen, X. X., and van Achterberg, C. 2019. Systematics, phylogeny, and evolution of Braconid Wasps: 30 years of progress. Annu Rev Entomol, 64: 335-358
Chou, L. Y. 1981. A preliminary list of Braconidae (Hymenoptera) of Taiwan. J Agric Res China, 30(1): 71-88. (In Chinese)
Cock, M. J. W., Beseh, P. K., Buddie, A. G., Cafá, G., and Crozier, J. 2017. Molecular methods to detect Spodoptera frugiperda in Ghana, and implications for monitoring the spread of invasive species in developing countries. Sci Rep, 7(1): 4103. https://doi.org/10.1038/ s41598-017-04238-y
Collier, T., and van Steenwyk, R. 2004. A critical evaluation of augmentative biological control. Biol Control, 31(2): 245-256. https://www.cdfa.ca.gov/is/pdfs/Study/ BiologicalControl.pdf
Colmenarez, Y. Z., Babendreier, D., Wurst, F. R. F., Vásquez‑Freytez, C. L., and Bueno, A. D. F. 2022. The use of Telenomus remus (Nixon, 1937) (Hymenoptera: Scelionidae) in the management of Spodoptera spp.: potential, challenges and major benefits. CABI Agric Biosci, 3(5): 1-13. https://doi.org/10.1186/s43170-021- 00071-6
DeBach, P. 1964. Biological control of insect pests and weeds. Chapman and Hall Ltd, London 844 p.
De Saeger, H. 1948. Cardiochilinae et Sigalphinae (Hymenoptera Apocrita Fam. Braconidae). Exploration du Parc National Albert. Mission G.F. de Witte (1933- 1935). Fasc. 53. https://cd.chm-cbd.net/archives_rdc/ archives/publications/exploration-national-park-albert/ exploration-national-park-albert-first-series/missiong.- f.-de-witte-1933-1935/1948-fascicule-53- cardiochilinae-et-sigalphinae-hymenoptera-apocritafam./ copy-of-de-saeger_1948_complet.pdf
Dudarenko, G. P. 1974. Formation of the abdominal carapace in braconids (Hymenoptera, Braconidae). Entomol Rev, 53: 80-90.
Durocher‑Granger, L., Mfune, T., Musesha, M., Lowry, A., Reynolds, K., Buddie, A., Kenis, M. 2021. Factors influencing the occurrence of fall armyworm parasitoids in Zambia. J Pest Sci, 94: 1133-1146. https://doi. org/10.1007/s10340-020-01320-9
Early, R., González-Moreno, P., Murphy, S. T., and Day, R. 2018. Forecasting the global extent of invasion of the cereal pest Spodoptera frugiperda, the fall armyworm. NeoBiota, 40: 25-50. https://neobiota.pensoft.net/ articles.php?id=28165
Fiedler, A. K., Landis, D. A., and Wratten, S. D. 2008. Maximizing ecosystem services from conservation biological control: The role of habitat management. Biol Control, 45(2): 254-271. https://doi.org/10.1016/j. biocontrol.2007.12.009
Firake, D. M., and Behere, G. T. 2020a. Natural mortality of invasive fall armyworm, Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) in maize agroecosystems of northeast India. Biol Control, 148: 104-303. https://doi.org/10.1016/j. biocontrol.2020.104303
Firake, D. M., and Behere, G. T. 2020b. Bioecological attributes and physiological indices of invasive fall armyworm, Spodoptera frugiperda (J. E. Smith) infesting ginger (Zingiber officinale Roscoe) plants in India. Crop Prot, 137: 105-233. https://doi.org/10.1016/j. cropro.2020.105233
Ghahari, N. S., Gadallah, N. S., Kittel, R. N., Shaw, S. R., and Quicke, D. L. J. 2022. Subfamily Cheloninae Foerster, 1863. 256-287. In: Gadallah NS, Ghahari H, SR Shaw (eds), Braconidae of the Middle East (Hymenoptera) Taxonomy, Distribution, Biology, and Biocontrol Benefits of Parasitoid Wasps. Academic Press, Elsevier Inc., United Kingdom.
Goergen, G., Kumar, P. L., Sankung, S. B., Togola, A., and Tamò, M. 2016. First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera: Noctuidae), a new alien invasive pest in A comprehensivereview of Chelonus s. str. Panzer (Hymenoptera: Braconidae: Cheloninae) focusing on species... West and Central Africa. PLoS ONE, 11(10). https://doi. org/10.1371/journal.pone.0165632
Gupta, A., Babu, S. R., and Kumar, M. S. 2019. Cotesia ruficrus (Haliday, 1834) (Hymenoptera: Braconidae) emerging as a common natural parasitoid of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) in Indian maize fields. J Biol Control, 33(3): 193-196. https://doi.org/10.18311/jbc/2019/24118
Gupta, A., Babu, S.R., and Kumar, M.S. 2019. Cotesia ruficrus (Haliday, 1834) (Hymenoptera: Braconidae) emerging as a common natural parasitoid of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) in Indian maize fields. Journal of Biological Control, 33(3): 193-196. https://doi.org/10.18311/jbc/2019/24118
Gupta, A., Lalitha, Y., Varshney, R., Shylesha, A.N., and van Achterberg, C. 2020a. Chelonus formosanus Sonan (Hymenoptera: Braconidae) an egg-larval parasitoid of the invasive pest Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) amenable to laboratory mass production in India. J Entomol Zool Stud, 8(1): 1521- 1524.
Gupta, A., Soujanya, P. L., van Achterberg, C., and Sekhar, J. C. 2020b. Coccygidium transcaspicum (Kokujev) (Hymenoptera: Braconidae) parasitizing larvae of invasive pest Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) in India. Zootaxa, 4750(2): 293-297.
Gutiérrez-Ramírez, A., Robles-Bermúdez, A., Cambero- Campos, J., Santillán-Ortega, C., Ortíz-Catón, M., Coronado-Blanco, J.M., and Campos-Figueroa, M. 2015. Parasitoides de Spodoptera frugiperda (Lepidoptera: Noctuidae) Encontrados en Nayarit, México, Southwest Entomol, 40(3): 555-564. https:// doi.org/10.3958/059.040.0314
Hafez, M., Tawfik, M. F. S., and Ibrahim, A. A. 1980. The immature stages of Chelonus inanitus (L.), a parasite of the cotton leafworm, Spodoptera littoralis (Boisduval) in Egypt (Hymenoptera: Braconidae). Dtsch Entomol Z, 27(1-3): 29-38. https://doi.org/10.1002/ mmnd.19800270104
Heimpel, G. E., and Mills, N. J. 2017. Biological control - ecology and applications. Cambridge University Press, Cambridge. https://doi.org/10.1017/9781139029117
Huber, J. T. 2009. Biodiversity of Hymenoptera 303-323. In: Footit RG, Adler PH (eds), Insect Biodiversity: Science and Society. Wiley-Blackwell, Blackwell Publishing Limited. https://doi.org/10.1002/9781444308211.ch12
Jaraleño-Teniente, J., Lomeli-Flores, J. R., and Rodríguez- Leyva, E. 2020. Egg parasitoids survey of Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) in maize and sorghum in Central Mexico. Insects, 11(3). https:// doi.org/10.3390/insects11030157
Jindal, J., Sharma, K. P., Shera, P. S., and Cheema, H. K. 2022. Native parasitoids of fall armyworm Spodoptera frugiperda (J.E. Smith) in maize. Ind J Ent, 84(4): 865- 867. https://doi.org/10.55446/IJE.2021.72
Jones, D. 1985. Endocrine interaction between host (Lepidoptera) and parasite (Cheloninae: Hymenoptera): Is the host or the parasite in control? Ann Entomol Soc Am, 78(2): 141-148. https://doi.org/10.1093/ aesa/78.2.141
Kaeslin, M., Wehrle, I., Grossniklaus-Bürgin, C., Wyler, T., Guggisberg, D., Sehittny, J. C., and Lanzrein, B. 2005. Stage-dependent strategies of host invasion in the egg-larval parasitoid Chelonus inanitus. J Insect Physiol, 51(3): 287-296. https://doi.org/10.1016/j. jinsphys.2004.11.015
Keerthi, M. C., Suroshe, S. S., Doddachowdappa, S., Shivakumara, K. T., Mahesha, H. S., Rana, V. S., ... Shakil, N. A. 2023. Bio-intensive tactics for the management of invasive fall armyworm for organic maize production. Plants, 12(3). https://www.mdpi. com/2223-7747/12/3/685
Kenis, M., Benelli, G., Biondi, A., Calatayud, P. A., Day, R., Desneux, N., … Wu, K. 2022. Invasiveness, biology, ecology, and management of the fall armyworm, Spodoptera frugiperda. Entomol Gen, 43(2): 187-241. https://doi.org/10.1127/entomologia/2022/1659
Khajeh, N., Rakhshani, E., Barahoel, H., and Armjomandinejad, A. 2020. Taxonomic study of the genus Chelonus Panzer (Hymenoptera, Braconidae, Cheloninae) in Sistan region. 21st Iranian Plant Protection Congress.
Kittel, R. N., and Austin, A. D. 2014. Synopsis of Australian chelonine wasps (Hymenoptera: Braconidae: Cheloninae) with description of two new genera. Aust J Entomol., 53(2): 183-202. http://dx.doi.org/10.1111/ aen.12070
Kittel, R. N., Austin, A. D., and Klopfstein, S. 2016. Molecular and morphological phylogenetics of chelonine parasitoid wasps (Hymenoptera: Braconidae), with a critical assessment of divergence time estimations. Mol Phylogenetics Evol, 101: 224-41. https://doi. org/10.1016/j.ympev.2016.05.016 CALCETAS et al.
Koffi, D., Kyerematen, R., Eziah, V. Y., Agboka, K., Adom, M., Goergen, G., and Meagher Jr., R. L. 2020. Natural enemies of the fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) in Ghana. Fla Entomol, 103(1): 85-90. https://doi. org/10.1653/024.103.0414
Legner, E. F., and Thompson, S. N. 1977. Effects of the parental host on host selection, reproductive potential, survival, and fecundity of the egg-larval parasitoid, Chelonus sp. near curvimaculatus, reared on Pectinophora gossypiella and Phthorimaea operculella. Entomophaga, 22: 75-84. https://doi.org/10.1007/ BF02372992
Li, F., Wang, L., Lü, B., Cao, F., Pan, X., Yuan, L., and Wu, S. 2019. The report of Chelonus munakatae parasitizing fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in Hainan, China. Chinese J Biol Control, 35(6): 992-996. https://doi.org/10.16409/j.cnki.2095- 039x.2019.06.003
Li, T. H., Bueno, A. D. F., Desneux, N., Zhang, L., Wang, Z., Dong, H., Zang, L. S. 2023. Current status of the biological control of the fall armyworm Spodoptera frugiperda by egg parasitoids. J Pest Sci, 96: 1345- 1363. https://doi.org/10.1007/s10340-023-01639-z
Liu, J. F., Zhao, H. Y., Song, Y. F., Yu, Y. C., and Yang, M. F. 2022. A chromosome-level genome assembly of the parasitic wasp Chelonus formosanus Sonan, 1932 (Hymenoptera: Braconidae). Genome Biol Evol, 14(1): 1-6. https://doi.org/10.1093/gbe/evac006
Madl, M., and van Achterberg, C. 2014. A catalogue of the Braconidae (Hymenoptera: Ichneumonoidea) of the Malagasy subregion. Linzer Biologische Beitraege, 46(1): 5-220. https://zenodo.org/records/4507364
McComb, C. W., 1968. A revision of the Chelonus subgenus Microchelonus in North America, North of Mexico: (Hymenoptera: Braconidae). Uni Maryland, Agri Experi Stat, Bull, A-149(1967): 1-148.
Mamahit, J. M. E., and Kolondam, B. J. 2023. A review on fall armyworm (Spodoptera frugiperda) insecticide resistance. Int J Res Rev, 10(5): 146-151. http://dx.doi. org/10.52403/ijrr.20230519
Mitsch, W. J. 1998. Ecological engineering — The 7-year itch. Ecol Eng, 10(2): 119-138. http://dx.doi.org/10.1016/ S0925-8574(98)00009-3
Mitsch, W. J. 2012. What is ecological engineering? Ecol Eng, 45: 5-12. https://doi.org/10.1016/j.ecoleng.2012.04.013
Molina-Ochoa, J., Carpenter, J. E., Heinrichs, E. A., and Foster, J. E. 2003. Parasitoids and parasites of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas and Caribbean Basin: an Inventory. Fla Entomol, 86(3): 254-289. https://doi.org/10.1653/0015- 4040(2003)086[0254:PAPOSF]2.0.CO;2
Montezano, D. G., Specht, A., Sosa-Gómez, D. R., Roque- Specht, V. F., Sousa-Silva, J. C., Paula-Moraes, S. V., … Hunt, T. E. 2018. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. Afr Ent, 26(2): 286-300. https://doi.org/10.4001/003.026.0286
Morgan, A. C., and Crumb, S. E. 1914. The tobacco split worm. Series: Bull U.S. Depart Agri Washington, D. C., USA. 59: 1-7. https://doi.org/10.5962/bhl.title.64426
Nagarkatti, S., and Singh, S. P. 1989. Importation and establishment of new natural enemies of Heliothis spp. (Lepidoptera: Noctuidae) into India, In: King EG, Jackson RD (eds), Proc Workshop on Biol Control Heliothis: Increasing the Effectiveness of Natural Enemies, Far Eastern Regional Research Office, United States Department of Agriculture, New Delhi, India, 375-385.
Nonveiller, G. 1984. Catalogue des insectes du Cameroun d’intérêt agricole, Belgrad, 1984. Bull Société Entomol France, 91(3-4).
Ngangambe, M. H., and Mwatawala, M. 2020. Effects of Entomopathogenic Fungi (EPFs) and cropping systems on parasitoids of fall armyworm (Spodoptera frugiperda) on maize in eastern central, Tanzania. Bio Sci Tech, 30(5): 418-430. https://doi.org/10.1080/0958 3157.2020.1726878
Otim, M. H., Aropet, S. A., Opio, M., Kanyesigye, D., Opolot, H. N., and Tay, T. W. 2021. Parasitoid distribution and parasitism of the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in different maize producing regions of Uganda. Insects, 12(2). https://doi. org/10.3390/insects12020121
Özmen, D. 2004. Biological relations between Chelonus oculator Panzer (Hymenoptera: Braconidae) and its host Spodoptera littoralis (Boisduval) and Ephestia kuehniella Zeller and investigation of the effects of Aldicarb on the parasitoid by radioisotope tracer technique [Unpublished doctoral dissertation] Ankara University, Graduate School of Natural and Applied Sciences Department of Plant Protection.
Papp, J. 1995. Revision of C. Wesmael’s Chelonus species (Hymenoptera Braconidae Cheloninae). Bull l’Institut Royal Sci Naturelles Belgique, 65: 115-134.
Pair, S. D., and Gross Jr., H. R. 1984. Field mortality of pupae of the fall armyworm, Spodoptera frugiperda (J.E. Smith), by predators and a newly discovered parasitoid, Diapetimorpha introita. J Georgia Entomol Soc, 19(1): 22-26. https://agris.fao.org/search/en/records/6473620e 08fd68d5460483ac
Parrella, M. P., Heinz, K. M., and Nunney, L. 1992. Biological control through augmentative releases of natural enemies: A strategy whose time has come. Amer Ento, 38(3): 172-180. https://doi.org/10.1093/ae/38.3.172
Pawar, A. D., Prasad, J., Asre, R., and Singh, R. 1983. Introduction of exotic parasitoid, Chelonus blackburni Cameron in India for the control of cotton bollworms. Ind J Ent, 45: 436-439.
Perier, J. D., Haseeb, M., Kanga, L. H. B., Meagher, R. L., and Legaspi, J. C. 2022. Intraguild Interactions of three biological control agents of the fall armyworm Spodoptera frugiperda (JE Smith) in Florida. Insects, 13(9). https://doi.org/10.3390/insects13090815
Plant Health Australia. 2020. Fall armyworm continuity plan for the Australian Grains Industry, Version 1 (November 2020). https://www.planthealthaustralia. com.au/wp-content/uploads/2020/11/Fall-Armworm- Continuity-Plan-2.pdf
Prasanna, B. M., Huesing, J. E., Eddy, R., and Peschke, V. M. 2018. Fall armyworm in Africa: A guide for integrated pest management. CIMMYT, Mexico.
Rao, B. N., and Patel, R. C. 1974. Bionomics of Chelonus formosanus Sonan, an egg larval parasite of Spodoptera litura (F). Ind J Ent, 36(2): 103-109.
Rechav, Y. 1975. Biological and ecological studies of the parasitoid Chelonus inanitus (L.) (Hym.: Braconidae) in Israel. I. Distribution, abundance and parasitism in natural host populations. Entomoph, 20(4): 365-371.
Rechav, Y., and Orion, T. 1975. The development of the immature stages of Chelonus inanitus. Ann Entomol Soc Am, 68(3): 457-462. https://doi.org/10.1093/ aesa/68.3.457
Rechav. Y. 1978. Biological and ecological studies of the parasitoid Chelonus inanitus (L.) (Hym.: Braconidae) in Israel. IV. Oviposition, host preferences, and sex ratio. Entomoph, 23(1): 95-102. https://link.springer.com/ article/10.1007/BF02371997
Sagar, D., Suroshe, S. S., Keerthi, M. C., Poorani, J., Gupta, A., and Chandel, R. K. 2022. Native parasitoid complex of the invasive fall armyworm, Spodoptera frugiperda (JE Smith) from Northern India. Int J Trop Insect Sci, 42: 2773-2778. https://doi.org/10.1007/s42690-022-00743-4
Seymour, P. R., Roberts, H., and Davis, M. E. 1985. Insects and other invertebrates found in plant material imported into England and Wales, 1984. Reference Book, Ministry of Agriculture, Fisheries and Food, UK No. 442/84.
Shankar, G., and Adachi, Y. 2019. First report of the occurrence of fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) on Ginger (Zingiber officinale) in Haveri district, Karnataka. India J Entomol Zool Stud, 7(5): 78-80.
Sharkey, M. J., Janzen, D. H., Hallwachs, W., Chapman, E. G., Smith, M. A., Dapkey, T., … Burns, J. M. 2021. Minimalist revision and description of 403 new species in 11 subfamilies of Costa Rican braconid parasitoid wasps, including host records for 219 species. ZooKeys, 1013: 1-665. https://doi.org/10.3897/ zookeys.1013.55600
Sharanabasappa, K. C. M., Poorani, J., Maruthi, M. S., Pavithra, H. B., and Diraviam, J. 2019. Natural enemies of Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), a recent invasive pest on maize in South India. Fla Entomol, 102(3): 619-623. https://doi. org10.1653/024.102.0335
Sharanowski, B. J., Dowling, A. P. G., and Sharkey, M. J. 2011. Molecular phylogenetics of Braconidae (Hymenoptera: Ichneumonoidea), based on multiple nuclear genes, and implications for classification. Systematic Entomology, 36(3): 549-572.
Shaw, M. R., and Huddleston, T. 1991. Classification and biology of braconid wasps (Hymenoptera: Braconidae). Royal Ent Soc London, British Museum (Natural History) at The Natural History Museum, London 1-130.
Shaw, S. R. 1997. Subfamily Cheloninae. In: Wharton RA, Marsh PM, Sharkey MJ (eds), Identification Manual of the New World Genera of the Family Braconidae Hymenoptera vol. 1: 192-201. Washington, DC, USA.
Shen, Z., Zang, Z. -Y., Dai, P., Xu, W., Nkunika, P. O. Y., and Zang, L. S. 2023. Identification of Chelonus sp. from Zambia and its performance on different aged eggs of Spodoptera frugiperda. Insects, 14(1): 61. https://doi. org/10.3390/insects14010061
Shenefelt, R. D. 1973. Braconidae 6. Cheloninae. In: van Der VJ and Shenefelt RD (eds), Hymenopterorum Catalogus (nova editio) Pars, 10: 813-936. CALCETAS et al.
Shi, M., Chen, X. X., and van Achterberg, C. 2005. Phylogenetic relationships among the Braconidae (Hymenoptera: Ichneumonoidea) inferred from partial 16S rDNA, 28S rDNA D2, 18S rDNA gene sequences, and morphological characters. Mol Phylogenetics Evol, 37(1): 104-116. https://doi.org/10.1016/j. ympev.2005.03.035
Sisay, B., Simiyu, J., Mendesil, E., Likhayo, P., Ayalew, G., Mohamed, S., and Tefera, T. 2019. Fall armyworm, Spodoptera frugiperda infestations in East Africa: Assessment of damage and parasitism. Insects, 10(7). https://doi.org/10.3390/insects10070195
Sonan, J. 1932. Notes on some Braconidae and Ichneumonidae from Formosa, with descriptions of 18 new species. Trans Nat Hist Soc Formosa, 22: 66-87.
Sonan, J. 1937. Studies on the tobacco caterpillar, Prodenia litura FAB., in Formosa. Gov. Formosa, Centr. Inst., Div. Agri Bull, 70. (In Japanese)
Subramaniam, S. 2022. Identifying potential parasitoids of the fall armyworm, Spodoptera frugiperda, and the risk to Australian horticulture. Final Report to Queensland Department of Agriculture and Fisheries. Tamil Nadu Agricultural University (TNAU). 2023. Mass production of Chelonus blackburni. https://agritech. tnau.ac.in/crop_protection/crop_prot_bio_mass_ parasitoids5.html
Tang, Y., and Marsh, P. M. 1994. A taxonomic study of the genus Ascogaster in China” (Hymenoptera: Braconidae: Cheloninae). J Hymenopt Res, 3: 279-302.
Tang, P., Wang, Z., …Wu, Q.. 2019. The natural enemies of the fall armyworm Spodoptera frugiperda and their application in biological control programs. Chinese Journal of Applied Entomology, 56: 370-381.
Tendeng, E., Labou, B., Diatte, M., Djiba, S., and Diarra, K. 2019. The fall armyworm Spodoptera frugiperda (JE Smith), a new pest of maize in Africa: Biology and first native natural enemies detected. Internat J Biol Chem Sci, 13(2): 1011-1026. https://doi.org/10.4314/ijbcs. v13i2.35
Trisyono, Y. A., Suputa-Aryuwandari. V. E. F., Hartaman, M., and Jumari, J. 2019. Occurrence of heavy infestation by the fall armyworm Spodoptera frugiperda, a new alien invasive pest, in corn in Lampung Indonesia. J Perlindun Tanam Indonesia, 23(1): 156-160.
Jaraleño-Teniente, J., Lomeli-Flores, J. R., Rodríguez-Leyva, E., Bujanos-Muñiz, R., and Rodríguez-Rodríguez, S. E. 2020. Egg parasitoids survey of Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) in maize and sorghum in Central Mexico. Insects, 11(3). https://doi. org/10.3390/insects11030157
Tobias, V. I. 2000. Subfamily Cheloninae. In: Lehr PA. (ed.), Key to the insects of the Russian Far East, Vol. IV. Neuropteroidea, Mecoptera, Hymenoptera, Vol. IV (pp. 426-571), Dal’nauka, Vladivostok.
Tobias, V. I. 2011. A new subgenus of the genus Microchelonus Szépligeti and a new species of the genus Chelonus Panzer (Hymenoptera: Braconidae) from Central Asia. Russ Entomol J, 20(3): 327-330.
Valdez, E. M., Joshi, R. C., Rillon, G. S., Donayre, D. K. M., Martin, E. C., dela Cruz, K. B., … Annamalai, S. 2023a. Rice: A new host of fall armyworm Spodoptera frugiperda (J.E. Smith) and its strains in the Philippines. Insect Environ, 26(2): 129-36.
Valdez, E. M., Rillon, G. S., Joshi, R. C., dela Cruz, K. B., Donayre, D. K. M., Martin, E. C., … Annamalai, S. 2023b. Fall armyworm, Spodoptera frugiperda (J.E. Smith) damage on rice in the Philippines. Asia Pacific J Sustain Agri, Food Energy, 11(2): 37-46.
Valdez, E. M., Joshi, R. C., Rillon, G. S., dela Cruz, K. B., Donayre, D. K. M., Martin, E. C., … Annamalai, S. 2024. Novel records of parasitoids targeting fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), in rice-corn-based cropping systems in the Philippines. J Biol Control, 38(1): 82-86. https://doi. org/10.18311/jbc/2024/36513
van Achterberg, C. 1976. A preliminary key to the subfamilies of the subfamilies of the Braconidae (Hymenoptera). Tijdschrift voor Entomologie, 119: 33-78. https://www. biodiversitylibrary.org/part/66809
van Achterberg, C., and Polaszek, A. 1996. The parasites of cereal stemborers (Lepidoptera: Cossidae, Crambidae, Noctuidae, Pyralidae) in Africa, belong to the family Braconidae (Hymenoptera: Ichneumonoidea). Zoolog Verhand, 304(1): 1-123. https://repository.naturalis.nl/ pub/317822
Van den Berg, H., Waage, J. K., and Cock, M. J. W. 1988. Natural enemies of Helicoverpa armigera in Africa: A review. CAB Internat.
van Huis, A. 1981. Integrated pest management in the small farmers’ maize crop in Nicaragua. Veenman and Zonen, Wageningen, The Netherlands. https://library.wur.nl/ WebQuery/wurpubs/74659
van Emden, H. F. 2002. Conservation biological control: From theory to practice. In: Van Driesche R (ed) Proc 1st Internat Symp Biol Control Arthropods, United States Depart Agricult Forest Service, Hawaii. USDA Forest Service, Morgantown, WV. 199-208.
van Lenteren, J. C. 2000. A greenhouse without pesticides: Fact or fantasy? Crop Prot, 19: 375-384. https://doi. org/10.1016/S0261-2194(00)00038-7
van Lenteren, J. C., Hale, A., Klapwijk, J. N., van Schelt, J., Steinberg, S. 2003. Guidelines for quality control of commercially produced natural enemies. Quality control and production of biological control agents: theory and testing procedures. CABI Publishing, Wallingford, p. 1-8. https://doi.org/10.1079/9780851996882.0265
Varshney, K. 1999. Taxonomic studies on Indian Cheloninae (Hymenoptera: Braconidae). [Unpublished doctoral dissertation]. Aligarh Muslim University, Aligarh, India. Watanabe, C. 1937. A contribution to the knowledge of the braconid fauna of the empire of Japan (Hymenoptera). J Facul Agricul, Hokkaido Imperial University, 42(1): 1-188.
Westbrook, J., Fleischer, S., Jairam, S., Meagher, R., and Nagoshi, R. 2019. Multigenerational migration of fall armyworm, a pest insect. Ecosph, 10(11): 12 p. https:// doi.org/10.1002/ecs2.2919
Wheeler, G. S., Ashley, T. R., and Andrews, K. L. 1989. Larval parasitoids and pathogens of the fall armyworm in Honduran maize. Entomoph, 34(3): 331-340. https:// doi.org/10.1007/bf02372472
Wharton, R. A. 1993. Bionomics of the Braconidae. Ann Rev Entomol, 38: 121-143. https://doi.org/10.1146/annurev. en.38.010193.001005
Yadav, D. N. 1980. Studies on the natural enemies of Heliothis armigera (Hübner) and its biological control using an egg-parasite, Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae). Gujarat Agricult University Res J, 6(1): 62-63. https://eurekamag.com/ research/000/991/000991435.php
Yousuf, M. and Ray, P. 2009. Record of Chelonus Panzer (Braconidae: Cheloninae) from Central India. J Biopest, 2(2): 145-149. http://www.jbiopest.com/users/lw8/ efiles/mohd_yousuf.pdf
Yu, D. S., van Achterberg, C., and Horstmann, K. 2013. Biological and taxonomical information: Ichneumonoidea 2012. Ottawa (Taxapad Interactive Catalogue), 304.
Yu, D. S., van Achterberg, C., and Horstmann, K. 2016. Taxapad 2016. Ichneumonoidea 2015. Database on flash-drive. 304. https://www.scienceopen. com/document?vid=55b95bf4-66fd-4cea-8b9b- 27b4dbefc056
Zang, L. -S., Shen, Z., and Li, T. H. 2022. A method of using rice moth eggs as a factious host for the production of Chelonus bifoveolatus. China patent 202210918583.0. Chinese.
Zenner, I., Álvarez, A., and Barreto, S. 2006. Influence of parasitism by Chelonus insularis Cresson (Hymenoptera: Braconidae) on the susceptibility of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) to insecticides. Neotro Entomol, 35(6): 818-822.
Zettel, H. 1990. Neue Phanerotoma - Arten von pazifischen Inseln (Hym. Braconidae). Dtsch Entomol Zt, 37(1-3) 45-69. https://doi.org/10.1002/mmnd.19900370116
Zhang, H. Y. 2008. Taxonomic study on genus Chelonus Panzer, 1806 (Hymenoptera: Braconidae: Cheloninae) from China [Doctoral dissertation, Zhejiang University].
Zhang, H. Y., Shi, M., He, J. -H., and Chen, X. -X. 2008. New species and records of the subgenus Microchelonus Szépligeti (Braconidae: Cheloninae) from China. Biologia, 63(1): 107-112. https://doi.org/10.2478/ s11756-008-0001-7
Zhou, J. -J., van Achterberg, K., Tang, P., and Chen, X. -X. 2022. A new subgenus of Chelonus Panzer, 1806 (Braconidae: Cheloninae) from China. Zootaxa, 5115(2): 288-294. https://doi.org/10.11646/zootaxa.5115.2.8
Zhou, J. -J., van Achterberg, K., Tang, P., Chen, X. -X.. 2024. A review of the subgenera Carinichelonus, Microchelonus, Parachelonus and Stylochelonus of the genus Chelonus Panzer (Braconidae: Cheloninae) with descriptions of twenty-one new species from China.
