Article abstract

Journal of Agricultural and Crop Research

Research Article | Published October 2022 | Volume 10, Issue 7. pp. 113-130.

doi: https://doi.org/10.33495/jacr_v10i7.22.128

 

Influence of agricultural practices on Spodoptera frugiperda (JE Smith) infestation, natural enemies and biocontrol in maize

 



 

 

Sharif A. Boukari1*

Antonio A. C. Sinzogan1

Rachidatou Sikirou2

Jean M. Deguenon1

Gbènakpon Aubin Y. G. Amagnidé2

Norliette Zossou3

Henri S. Totin Vodounon4

Aristide C. Adomou5

Adam Ahanchédé3

 

Email Author

 

1. Laboratoire d’Entomologie Agricole (LEAg), Faculté des Sciences Agronomiques (FSA), Université d’Abomey-Calavi (UAC), Abomey-Calavi, 01 BP 526 Cotonou, Benin.

2. Laboratoire de Défense des Cultures (LDC), Institut National des Recherches Agricoles du Bénin (INRAB), Abomey-Calavi, 01 BP 884 Cotonou, Benin.

3. Laboratoire de Biologie Végétale (LBV), Faculté des Sciences Agronomiques (FSA), Université d’Abomey-Calavi (UAC), Abomey-Calavi, 01 BP 526 Cotonou, Benin.

4. Laboratoire Pierre Pagney, Institut de Géographie, de l’Aménagement du Territoire et de l’Environnement (IGATE), Université d’Abomey-Calavi (UAC), Abomey-Calavi, 01 BP 526 Cotonou, Benin.

5. Département de Biologie Végétale, Faculté des Sciences et Techniques (FAST), Université d’Abomey-Calavi (UAC), Abomey-Calavi, 01 BP 526 Cotonou, Benin.


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Citation: Boukari SA, Sinzogan CAC, Sikirou R, Deguenon JM, Amagnidé GAY, Zossou N, Vodounon HST, Adomou AC, Ahanchédé A (2022). Influence of agricultural practices on Spodoptera frugiperda (JE Smith) infestation, natural enemies and biocontrol in maize. J. Agric. Crop Res. 10(7):113-130. doi: 10.33495/jacr_v10i7.22.128.

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 Abstract 


Maize (Zea mays L.) production in Africa is threatened by the recent invasion of the fall armyworm (FAW), Spodoptera frugiperda (JE Smith). The management of this pest is laborious and requires effective, sustainable and environmentally friendly control approaches. The present study investigated the natural enemies associated with S. frugiperda in maize fields through three climatic zones in Benin. Besides, the impact of different agricultural practices on its infestation and the performance of biocontrol agents were assessed. Larvae were collected from 67 maize fields and transferred to the laboratory, incubated and monitored for parasitoid emergence. The complex of natural enemies recorded in this study consisted of: entomopathogenic fungus Metarhizium sp., nematode Hexamermis sp. and parasitoids Chelonus bifoveolatus, Coccygidium luteum, Charops sp. and Drino quadrizonula. The results revealed that maize fields sown after soybean or cotton crops and those in which insecticides and herbicides were applied were associated with higher FAW infection rates by Metarhizium sp. The use of agricultural inputs led to lower FAW parasitism by Hexamermis sp. Regarding FAW infestation, the probability of high damage scores was higher in maize fields cultivated after fallow or cotton crops and in fields with mixed crops or those in which herbicides or relatively high fertilizer rates were applied. These findings provide several insights on the interaction between agricultural practices and FAW natural enemies that can be used for the implementation of an effective integrated management system for this pest in Benin or Africa.

Keywords  Fall armyworm   maize   infestation   agricultural practices   entomopathogenic fungi  

 nematodes   endoparasitoids   Benin 

 

 

Copyright © 2022 Author(s) retain the copyright of this article.

This article is published under the terms of the Creative Commons Attribution License 4.0

 

 

  References 

 

Abang AF, Nanga SN, Fotso Kuate A, Kouebou C, Suh C, Masso C, Saethre M-G, Fiaboe KKM (2021). Natural enemies of fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in different agro-ecologies. Insects, 12(6):509. https://doi.org/10.3390/insects 12060509.

Abrahams P, Beale T, Cock M, Corniani N, Day R, Godwin J, Murphy S, Richards G, Vos J (2017). Fall Armyworm Status. Impacts and control options in Africa: Preliminary Evidence Note. UKaid and CABI. Available online: https://www.invasive-species.org/wp-content/uploads/sites/2/2019/02/FAW-inception-report.pdf.

Acharjee P, Satpathi CR, Modak MK (2020). Long term studies on the role of parasitic nematode Hexamermis sp. in controlling brown plant hopper in farmer's rice field of West Bengal, India. India. Int. J. Cur. Res. Rev. 12(03):7-11. https://doi.org/10.31782/IJCRR.2020.12032.

Acheampong MA, Coombes CA, Moore SD, Hill MP (2020). Temperature tolerance and humidity requirements of select entomopathogenic fungal isolates for future use in citrus IPM programmes. J. Invertebr. Pathol. 174:107436. https://doi.org/10.1016/j.jip.2020.107436.

Agboton C, Onzo A, Ouessou FI, Goergen G, Vidal S, Tamò M (2014). Insect fauna associated with Anacardium occidentale (Sapindales: Anacardiaceae) in Benin, West Africa. J. Insect Sci. 14(1):12. https://doi.org/10.1093/jisesa/ieu091.

Agboyi LK, Goergen G, Beseh P, Mensah SA, Clottey VA, Glikpo R, Buddie A, Cafà G, Offord L, Day R, Rwomushana I, Kenis M (2020). Parasitoid Complex of Fall Armyworm, Spodoptera frugiperda, in Ghana and Benin. Insects, 11:68. https://doi.org/10.3390/insects11020068.

Agossou G, Gbehounou G, Zahm F, Agbossou EK (2019). Durabilité des exploitations agricoles de la basse vallée de l’Ouémé en République du Bénin. Agron. Africaine Sp. 31(2):125-145.

Ahissou BR, Sawadogo WM, Bonzi S, Baimey H, Somda I, Bokonon-Ganta AH, Verheggen FJ (2021). Natural enemies of the fall armyworm Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) in Burkina Faso. Tropicultura, 39(3):1881. https://doi.org/10.25518/2295-8010.1881.

Andrews KL (1980). The whorlworm, Spodoptera frugiperda, in Central America and neighboring areas. Fla. Entomol. 63(4):456-467.

Aniwanou CTS, Sinzogan AAC, Deguenon JM, Sikirou R, Stewart DA, Ahanchede A (2021). Bio-Efficacy of Diatomaceous Earth, Household Soaps, and Neem Oil against Spodoptera frugiperda (Lepidoptera: Noctuidae) Larvae in Benin. Insects, 12:18. https://doi.org/10.3390/insects12010018.

Baco MN, Abdoulaye T, Sanogo D, Langyintuo A (2011). Caractérisation des ménages producteurs de maïs en zone de savane sèche au Bénin. Rapport pays–Enquête-ménage–Benin, IITA, Ibadan, Nigeria, pp: 38. Available online: https://core.ac.uk/download/pdf/132689959.pdf (Accessed on 04 April, 2020).

Bala K, Sood AK, Pathania VS, Thakur S (2018). Effect of plant nutrition in insect pest management: A review. J. Pharmacogn. Phytochem. 7(4):2737-2742.

Baudron F, Zaman-Allah MA, Chaipa I, Chari N, Chinwada P (2019). Understanding the factors influencing fall armyworm (Spodoptera frugiperda J.E. Smith) damage in African smallholder maize fields and quantifying its impact on yield. A case study in Eastern Zimbabwe. Crop Prot. 120:141-150. https://doi.org/10.1016/j.cropro.2019.01.028.

Bednarek A, Gaugler R (1997). Compatibility of Soil Amendments with Entomopathogenic Nematodes. J. Nematol. 29(2): 220-227. https://www.ncbi.nlm.nih.gov/pmc/articles/ PMC2619768.

Bernardi D, Bernardi O, Horikoshi RJ, Salmeron E, Okuma DM, Farias JR, do Nascimento ARB, Omoto C (2017). Selection and characterization of Spodoptera frugiperda (Lepidoptera: Noctuidae) resistance to MON 89034 × TC1507 ×NK603 maize technology. Crop Protection 94:64-68. https://doi.org/10.1016/j.cropro.2016.11.026.

Bordat D, Goudegnon E (1991). Catalogue des principaux ravageurs des cultures maraîchères au Bénin. 1st Ed. CIRAD, Montpellier, France, pp. 15.

Bray JR, Curtis JT (1957). An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27: 325-349.

Campos-Herrera R, Jaffuel G, Chiriboga X, Blanco-Pérez R, Fesselet M, Půža V, Mascher F, Turlings TCJ (2015). Traditional and molecular detection methods reveal intense interguild competition and other multitrophic interactions associated with native entomopathogenic nematodes in Swiss tillage soils. Plant Soil, 389:237-255. https://doi.org/10.1007/s11104-014-2358-4.

Caniço A, Mexia A, Santos L (2020). First report of native parasitoids of fall armyworm Spodoptera frugiperda smith (Lepidoptera: Noctuidae) in Mozambique. Insects, 11(9):615. https://doi.org/10.3390/insects110 90615.

Caniço A, Mexia A, Santos L (2021). Farmers’ knowledge, perception and management practices of fall armyworm (Spodoptera frugiperda Smith) in Manica province, Mozambique. NeoBiota, 68:127-143. https://doi.org/10.3897/neobiota.68.62844.

Carvalho RA, Omoto C, Field LM, Williamson MS, Bass C (2013). Investigating the molecular mechanisms of organophosphate and pyrethroid resistance in the Fall Armyworm Spodoptera frugiperda. PLoS One, 8:e62268. https://doi.org/10.1371/journal.pone.0062268.

Christensen RHB (2019) Ordinal-Regression Models for Ordinal Data. R package Version 2019.12-10, 2019. Available online: https://CRAN.R-project.org/package=ordinal.
Cook DR, Leonard BR, Gore J (2004). Field and laboratory performance of novel insecticides against armyworms (Lepidoptera: Noctuidae). Fla. Entomol. 87-433-439.

Costa VHD, Soares MA, Rodríguez FAD, Zanuncio JC, Silva IM, Valicente FH (2015). Nomuraea rileyi (Hypocreales: Clavicipitaceae) in Helicoverpa armigera (Lepidoptera: Noctuidae) larvae in Brazil. Fla. Entomol. 98(2):796-798. https://doi.org/10.1653/024.098.0263.

Crotty FV, Fychan R, Sanderson R, Rhymes JR, Bourdin F, Scullion J, Marley CL (2016). Understanding the legacy effect of previous forage crop and tillage management on soil biology, after conversion to an arable crop rotation. Soil Biol. Biochem. 103:241-252. https://doi.org/10.1016/j.soilbio.2016.08.018.

Cruz-Martínez H, Ruiz-Vega J, Cortés-Martínez C, Rosas-Diaz J (2017). Formulation of entomopathogenic nematodes for crop pest control – A review. Plant Prot. Sci. 53(1):15-24. https://doi.org/10.17221/35/2016-PPS.

Dajoz R (1971). Précis d’écologie. 1st Ed. Dunod, Paris, p. 434.

Dassou AG, Idohou R, Azandémè-Hounmalon GY, Sabi-Sabi A, Houndété J, Silvie P, Dansi A (2021). Fall armyworm, Spodoptera frugiperda (J.E. Smith) in maize cropping systems in Benin: abundance, damage, predatory ants and potential control. Int. J. Trop. Insect Sci. 41:2627-2636. https://doi.org/10.1007/s42690-021-00443-5.

Davis FM, Ng SS, Williams WP (1992). Visual rating scales for screening whorl-stage corn for resistance to fall armyworm. Technical Bulletin N° 186; Mississippi Agricultural and Forestry Research Experiment Station, Mississippi State, MS, USA. Available online: http://www.nal.usda.gov/ (Accessed on 15 October, 2019).

Day R, Abrahams P, Bateman M, Beale T, Clottey V, Cock M, Colmenarez Y, Corniani N, Early R, Godwin J, Gomez J, Gonzalez Moreno P, Murphy ST, Oppong-Mensah B, Phiri N, Pratt C, Silvestri S, Witt A (2017). Fall Armyworm: Impacts and Implications for Africa. Outlooks on Pest Manag. 28(5):196-201. https://doi.org/10.1564/v28_oct_02.

Djenontin JA, Wennink B, Dagbenongbakin G, Ouinkoun G (2002). Pratiques de gestion de fertilité dans les exploitations agricoles du Nord-Bénin. Proceedings of the “Savanes africaines : des espaces en mutation, des acteurs face à de nouveaux défis”, May 27-31, Prasac and Cirad, Garoua, Cameroun, pp. 1-9.

Durocher-Granger L, Mfune T, Musesha M, Lowry A, Reynolds L, Buddie L, Cafà G, Offord L, Chipabika G, Dicke M, 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.

Firake DM, Behere GT (2020). Natural mortality of invasive fall armyworm Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) in maize agroecosystems of northeast India. Biol. Control, 148:104303. https://doi.org/10.1016/j.biocontrol.2020.104303.

Fite T, Damte T, Tefera T, Negeri M (2020). Hymenopteran and dipteran larval parasitoid species of the cotton bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) in chickpea growing districts of Ethiopia. Biocontrol Sci. Technol. 31(5): 541–545. https://doi.org/10.1080/09583157.2020.1859096.

Fronza E, Specht A, Heinzen H, Monteiro de Barros N (2017). Metarhizium (Nomuraea) rileyi as biological control agent. Biocontrol Sci. Technol. 27(11):1243-1264. https://doi.org/10.1080/09583157.2017.1391175.

Fuchs B, Saikkonen K, Helander M (2021). Glyphosate-modulated biosynthesis driving plant defense and species interactions. Trends Plant Sci. 26(4):312-323. https://doi.org/10.1016/j.tplants.2020.11.004.

Ginting S, Nadrawat Zarkani A, Sumarni T (2020). Natural incidence of entomopathogenic fungus Nomuraea rileyi on Spodoptera frugiperda infesting corn in Bengkulu. J. HPT Tropika, 20(2):85-91. https://doi.org/10.23960/j.hptt.22085-91.

Giraudo M, Hilliou F, Fricaux T, Audant P, Feyereisen R, Le Goff G (2014). Cytochrome P450s from the fall armyworm (Spodoptera frugiperda): responses to plant allelochemicals and pesticides. Insect Mol. Biol. 24(1):115-128. https://doi.org/10.1111/imb.12140.

Goergen G, Kumar PL, Sankung SB, Togola A, Tamò M (2016). First report of outbreaks of the fall armyworm, Spodoptera frugiperda (J E Smith) (Lepidoptera Noctuidae) a new alien invasive pest in West and Central Africa. PloS ONE, 11(10): e0165632. https://doi.org/10.1371/journal.pone.0165632.

Grant JA, Villani MG (2003). Soil moisture effects on entomopathogenic nematodes. Environ. Entomol. 32(1): 80-87. https://doi.org/10.1603/0046-225X-32.1.80.

Harker K, O'Donovan J (2013). Recent Weed Control, Weed Management, and Integrated Weed Management. Weed Technol. 27(1): 1-11. https://doi.org/10.1614/WT-D-12-00109.1.

Harrison RD, Thierfelder C, Baudron F, Chinwada P, Midega C, Schaffner U, Van Den Berg J (2019). Agro-ecological options for fall armyworm (Spodoptera frugiperda JE Smith) management: providing low-cost, smallholder friendly solutions to an invasive pest. J. Environ. Manage. 243:318-330. https://doi.org/10.1016/j.jenvman.2019.05.011.

Hay-Roe MM, Meagher RL, Nagoshi NR, Newman Y (2016). Distributional patterns of fall armyworm parasitoids in a corn field and a pasture field in Florida. Biol. Control, 96: 48-56. https://doi.org/10.1016/j.biocontrol.2016.02.003.

 Heard MS, Clark SJ, Rothery P, Perry JN, Bohan DA, Brooks DR, Champion GT, Dewar AM, Hawes C, Haughton AJ, May MJ, Scott RJ, Stuart RS, Squire GR, Firbank LG (2006). Effects of successive seasons of genetically modified herbicide-tolerant maize cropping on weeds and invertebrates. Ann. Appl. Biol. 149(3):249-254. https://doi.org/10.1111/j.1744-7348.2006.00091.

Hominick WM, Croft SL, Kuzoe FAS (1982). Description of parasitic stages of Hexamermis glossinae (Nematoda: Mermithidae) from Glossina in West Africa, with observations on the host-parasite association. Can. J. Zool. 60:3370-3376.

Houngbo S, Zannou A, Aoudji A, Sossou HC, Sinzogan A, Sikirou R, Zossou E, Vodounon HST, Adomou A, Ahanchédé A (2020). Farmers’ knowledge and management practices of fall armyworm, Spodoptera frugiperda (J.E. Smith) in Benin, West Africa. Agriculture, 10:430. https://doi.org/10.3390/agriculture10100430.

Hruska AJ (2019). Fall armyworm (Spodoptera frugiperda) management by smallholders. CAB Rev. 14:043. https://doi.org/10.1079/PAVSNNR201914043.

Huesing JE, Prasanna BM, McGrath D, Chinwada P, Jepson P, Capinera JL (2018). Integrated pest management of fall armyworm in Africa: an introduction. In: Fall Armyworm in Africa: A Guide for Integrated Pest Management, Prasanna BM, Huesing JE, Eddy R and Peschke VM (Eds.), CIMMYT, Mexico CDMX, pp. 1-10.

Jepson PC, Murray K, Bach O, Kachigamba D, Ndeithi F, Miano JK, McCracken T, Onyango D, Nthenga I, Agboka K, Byantwala S, De Groote H (2018). Pesticide Hazard and Risk Management and Compatibility with IPM. In: Fall Armyworm in Africa: A Guide for Integrated Pest Management, Prasanna BM, Huesing JE, Eddy R and Peschke VM (Eds.), CIMMYT, Mexico CDMX, pp. 29-44.

Kasoma C, Shimelis H, Laing M, Shayanowako AIT, Mathew I (2020). Screening of inbred lines of tropical maize for resistance to fall armyworm, and for yield and yield-related traits. Crop Prot. 136:105218. https://doi.org/10.1016/j.cropro.2020.105218.

Kenis M, du Plessis H, Van den Berg J, Ba MN, Goergen G, Kwadjo KE, Baoua I, Tefera T, Buddie A, Cafà G, Offord L, Rwomushana I, Polaszek A (2019). Telenomus remus, a candidate parasitoid for the biological control of Spodoptera frugiperda in Africa, is already present on the Continent. Insects, 10(4):92. https://doi.org/10.3390/insects10040092.

Kfir R (1997). Parasitoids of Plutella xylostella (Lepidoptera: Plutellidae) in South Africa: An annotated list. Entomophaga, 42:517-523. https://doi.org/10.1007/BF0276981.

Kolombar TM, Gugosyan YA, Brygadyrenko VV (2020). Impact of mineral fertilizers, growth stimulators, pH regulators vitamins and pigment supplements on the vitality of entomopathogenic nematodes of Steinernematidae and Heterorhabditidae families. Regul. Mech. Biosyst. 11(2):323-329. https://doi.org/10.15421/022049.

Kumela T, Simiyu J, Sisay B, Likhayo P, Mendesil E, Gohole L, Tefera T (2018). Farmers' knowledge, perceptions, and management practices of the new invasive pest, fall armyworm (Spodoptera frugiperda) in Ethiopia and Kenya. Int. J. Pest Manag. 65(1): 1-9. https://doi.org/10.1080/09670874.2017.1423129.

Lacey LA, Unruh TR (1998). Entomopathogenic nematodes for control of codling moth, Cydia pomonella (Lepidoptera: Tortricidae): Effect of nematode species concentration, temperature and humidity. Biol. Control, 13(3): 190-197. https://doi.org/10.1006/bcon.1998.0658.

Landis DA, Wratten SD, Gurr GM (2000). Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 45: 175–201. https://doi.org/10.1146/annurev.ento.45.1.175.

López MA, Martínez-Castillo AM, García-Gutiérrez C, Cortez-Mondaca E, Escobedo-Bonilla CM (2018). Parasitoids and Entomopathogens Associated with Fall Armyworm, Spodoptera frugiperda, in Northern Sinaloa. Southwest. Entomol. 43(4):867-881. https://doi.org/10.3958/059.043.0405.

Madl M, Van Achterberg C (2014). A catalogue of the Braconidae (Hymenoptera: Ichneumonoidea) of the Malagasy subregion. Linz. Biol. Beitr. 46(1):5-220.

Mama Sambo S. Togbé DR, Sinzogan AAC, Adomou A, Bokonon-Ganta HA, Karlsson MF (2019). Habitat factors associated with Fopius caudatus parasitism and population level of its host, Ceratitis Cosyra. Entomol. Exp. Appl. 168(1):28-40. https://doi.org/10.1111/eea.12858.

Mazzilli SR, Ernst OR, Pereira de Mello V, Pérez CA (2016). Yield losses on wheat crops associated to the previous winter crop: Impact of agronomic practices based on on-farm analysis. Eur. J. Agron. 75:99-104. https://doi.org/10.1016/j.eja.2016.01.007.

Meagher RL, Jr Nuessly GS, Nagoshi RN, Hay-Roe MM (2016). Parasitoids attacking fall armyworm (Lepidoptera: Noctuidae) in sweet corn habitats. Biol. Control, 95:66-72. https://doi.org/10.1016/j.biocontrol.2016.01.006.

Mensah S, Houehanou TD, Sogbohossou EA, Assogbadjo AE, Glèlè Kakai R (2014). Effect of human disturbance and climatic variability on the population structure of Afzelia africana Sm. ex pers. (Fabaceae–Caesalpinioideae) at country broad-scale (Bénin, West Africa). S. Afr. J. Bot. 95:165-173. https://doi.org/10.1016/j.sajb.2014.09.008.

Mesmin X, Cortesero A-M, Daniel L, Plantegenest M, Faloya V, Le Raleca A (2020). Influence of soil tillage on natural regulation of the cabbage root fly Delia radicum in brassicaceous crops. Agric. Ecosyst. Environ. 293:106834. https://doi.org/10.1016/j.agee.2020.106834.

Midega CAO, Pittchar JO, Pickett JA, Hailu GW, Khan ZR (2018). A climate-adapted push-pull system effectively controls fall armyworm, Spodoptera frugiperda (J. E. Smith), in maize in East Africa. Crop Prot. 105:10-15. https://doi.org/10.1016/j.cropro.2017.11.003.

Millar LC, Barbercheck ME (2002). Effects of tillage practices on entomopathogenic nematodes in a corn agroecosystem. Biol. Control 25(1): 1-11. https://doi.org/10.1016/S1049-9644(02)00042-7.

Miraldo LL, Bernardi O, Horikoshi JR, Amaral SAF, Bernardi D, Omoto C (2016). Functional dominance of different aged larvae of Bt-resistant Spodoptera frugiperda (Lepidoptera: Noctuidae) on transgenic maize expressing Vip3Aa20 protein. Crop Prot. 88:65-71. https://doi.org/10.1016/j.cropro.2016.06.004.

Mochi DA, Monteiro AC, Barbosa JC (2005). Action of Pesticides to Metarhizium anisopliae in Soil. Neotrop. Entomol. 34(6):961-971.

Mochiah MB, Baidoo PK, Owusu-Akyaw M (2011). Influence of different nutrient applications on insect populations and damage. J. Appl. Biosci. 38:2564-2572.

Mongkolsamrit S, Khonsanit A, Thanakitpipattana D, Tasanathai K, Noisripoom W, Lamlertthon S, Himaman W, Houbraken J, Samson RA, Luangsa-ard J (2020). Revisiting Metarhizium and the description of new species from Thailand. Stud. Mycol. 95:171-251. https://doi.org/10.1016/j.simyco.2020.04.001.

Mutamiswa R, Chidawanyika F, Nyamukondiwa C (2017). Dominance of spotted stem borer Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) over indigenous stem borer species in Africa's changing climates: ecological and thermal biology perspectives. Agric. For. Entomol. 19(4):344-356. https://doi.org/10.1111/afe.12217.

Ngangambe MH, Mwatawala MW (2020). Effects of entomopathogenic fungi (EPFs) and cropping systems on parasitoids of fall armyworm (Spodoptera frugiperda) on maize in eastern central, Tanzania. Biocontrol Sci. Technol. 30(5):418-430.

Ogunfunmilayo AO, Kazeem SA, Idoko JE, Adebayo RA, Fayemi EY, Adedibu OB, Oloyede-Kamiyo QO, Nwogwugwu JO, Akinbode OA, Salihu S, Offord LC, Buddie AG, Ofuya TI (2021). Occurrence of natural enemies of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) in Nigeria. PLoS ONE, 16(7):e0254328. https://doi.org/10.1371/journal.pone.0254328.

Okada H, Harada H (2007). Effects of tillage and fertilizer on nematode communities in a Japanese soybean field. Appl. Soil Ecol. 35(3): 582-598. https://doi.org/10.1016/j.apsoil.2006.09.008.

Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019). Vegan: Community Ecology Package. R package Version 2.5-5, 2019. Available online: https://CRAN.R-project.org/package=vegan (accessed on 15 October 2021).

Otim MH, Adumo Aropet S, Opio M, Kanyesigye D, Nakelet Opolot H, Tek Tay W (2021). Parasitoid distribution and parasitism of the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in different maize producing regions of Uganda. Insects, 12(2):121. https://doi.org/10.3390/insects12020121.

Patient D, Nchiwan N, Koehler H (2019). Abundance and Diversity of Insect Pests on Maize, Cowpea and Okra in a Comparative Experiment Testing Effects of Intercropping and Insecticide in the Cameroonian Guinean Savannah and Sudano Sahelian Agro-ecological Zones. J. Exp. Agric. Int. 29(6):1-20. https://doi.org/10.9734/JEAI/2019/4567.

R Core Team (2021). A Language and Environment for Statistical Computing Version 4.1.1. Available online: http://www.R-project.org/ (Accessed on 10 October 2021).

Reboredo GR, Camino NB (2019). A new species of Hexamermis Steiner, 1924 (Nematoda, Mermithidae) parasitizing Epilachna paenulata (Germar, 1824) (Coleopera Coccinellidae) in Argentina. Rev. Peru. Biol. 26(1):021-026. https://doi.org/10.15381/rpb.v26i1.15906.

Reddy PP (2017). Agro-ecological Approaches to Pest Management for Sustainable Agriculture. 1st Ed. Springer Nature Singapore Pte Ltd., Gateway East, Singapore, pp. 339. https://doi.org/10.1007/978-981-10-4325-3.

Riggin TM, Wiseman BR, Isenhour DJ, Espelie KE (1992). Incidence of fall armyworm (Lepidoptera: Noctuidae) parasitoids on resistant and susceptible corn genotypes. Environ. Entomol. 21(4):888-895. https://doi.org/10.1093/ee/21.4.888.

Ríos-Velasco C, Cerna-Chavez E, Sánchez-Peña S, Gallegos-Morales G (2010). Natural epizootic of the entomopathogenic fungus Nomuraea rileyi (Farlow) Samson infecting Spodoptera frugiperda (Lepidoptera: Noctuidae) in Coahuila México. J. Res. Lepid. 43:7-8.

Rivero‐Borja M, Guzmán‐Franco AW, Rodríguez‐Leyva E, Santillán‐Ortega C, Pérez‐Panduro A (2018). Interaction of Beauveria bassiana and Metarhizium anisopliae with chlorpyrifos ethyl and spinosad in Spodoptera frugiperda larvae. Pest Manag. Sci. 74(9):2047-2052. https://doi.org/10.1002/ps.4884.

Robertson IAD (1973). Notes on the Insect Parasites of Some Lepidopteran Pests in Tanzania. E. Afr. agric. For. J. 39(1):82-93. https://doi.org/10.1080/00128325.1973.11662621.

Rowen EK Tooker J F (2020). Fertilizing corn with manure decreases caterpillar performance but increases slug Damage. Environ. Entomol. 49(1):141-150. https://doi.org/10.1093/ee/nvz145.

Ruiz-Nájera RE, Ruiz-Estudillo RA, Sánchez-Yanez JM, Molina-Ochoa J, Skoda SR, Coutiño-Ruiz R, Foster JE (2013). Occurrence of entomopathogenic fungi and parasitic nematodes on Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae collected in central Chiapas, México. Fla Entomol. 96(2):498-503. https://doi.org/10.1653/024.096.0215.

Rusch A, Bommarco R, Ekbom B (2017). Conservation biological control in agricultural landscapes. In: Insect-Plant Interactions in a Crop Protection Perspective, Sauvion N, Thiéry D and Calatayud PA (Eds.), Advances in Botanical Research, Academic Press, London, UK, pp. 333-360. https://doi.org/10.1016/bs.abr.2016.11.001.

Schumacher V, Poehling H-M (2012). In vitro effect of pesticides on the germination vegetative growth, and conidial production of two strains of Metarhizium anisopliae. Fungal Biol. 116(1):121-132. https://doi.org/10.1016/j.funbio.2011.10.007.

Shah PA, Godonou I, Gbongboui C, Lomer CJ (1994). Natural levels of fungal infections in grasshoppers in Northern Benin. Biocontrol Sci. Technol. 4(3):331-341. https://doi.org/10.1080/09583159409355341.

Sharmila R, Shanmuga Priya M, Subramanian S, Poornima K, Pandiyan M (2018). Review on ecology of entomopathogenic nematodes. J. Entomol. Zool. Stud. 6(4):1086-1093.

Silva RA, da Quintela ED, Mascarin GM, Barrigossi JAF, Lião LM (2013). Compatibility of conventional agrochemicals used in rice crops with the entomopathogenic fungus Metarhizium anisopliae. Sci. Agric. 70(3):152-160. https://doi.org/10.1590/s0103-90162013000300003.

Smith DFQ, Camacho E, Thakur R, Barron AJ, Dong Y, Dimopoulos G, Broderick NA, Casadevall A (2021). Glyphosate inhibits melanization and increases susceptibility to infection in insects. PLoS Biol. 19(5):e3001182. https://doi.org/10.1371/journal.pbio.3001182.

Sisay B, Simiyu J, Malusi P, Likhayo P, Mendesil E, Elibariki N, Wakgari M, Ayalew G, Tefera T (2018). First report of the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), natural enemies from Africa and assessment of damage and pheromone lures. J. Appl. Entomol. 142(8):800-804. https://doi.org/10.1111/jen.12534.

Sivakumar T, Jiji T, Naseema A (2020). Effect of pesticides used in banana agro-system on entomopathogenic fungus, Metarhizium majus Bisch, Rehner and Humber. Int. J. Trop. Insect Sci. 40:283-291. https://doi.org/10.1007/s42690-019-00080-z.

Sun B, Li F, He X, Cao FE, Bandason E, Shapiro-Ilan D, Ruan W, Wu S (2020). First report of Ovomermis sinensis (Nematoda: Mermithidae) parasitizing fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in China. J. Nematol. 52:e2020-50. https://doi.org/10.21307/jofnem-2020-050.

Tanyi CB, Nkongho RN, Okolle JN, Tening AS, Ngosong C (2020). Effect of intercropping beans with maize and botanical extract on fall armyworm (Spodoptera frugiperda) infestation. Int. J. Agron. 2020:4618190. https://doi.org/10.1155/2020/4618190.

Tendeng E, Labou B, Diatte M, Djiba S, Diarra K (2019). The fall armyworm Spodoptera frugiperda (J.E. Smith), a new pest of maize in Africa: Biology and first native natural enemies detected. Int. J. Biol. Chem. Sci. 13(2):1011-1026. https://doi.org/10.4314/ijbcs.v13i2.35.

Thomas R, Vaughn I, Lello J (2013). Data analysis with R statistical software: A guidebook for scientists. Eco-explore, Newport, UK, p. 149.

Togola A, Meseka S, Menkir A, Badu-Apraku B, Bouka O, Tamò M, Djouaka R (2018). Measurement of Pesticide Residues from Chemical Control of the Invasive Spodoptera frugiperda (Lepidoptera: Noctuidae) in a Maize Experimental Field in Mokwa, Nigeria. Int. J. Environ. Res. Public Health, 15(5):849. https://doi.org/10.3390/ijerph15050849.

Udayakumar A, Shivalingaswamy TM, Bakthavatsalam N (2020). Legume-based intercropping for the management of fall armyworm, Spodoptera frugiperda L. in maize. J. Plant Dis. Prot.128:775-779. https://doi.org/10.1007/s41348-0202-00401-2.

Van Huis A (1981). Integrated pest management in the small farmer’s maize crop in Nicaragua. PhD thesis, Mededelingen Land bouwhoge school Wageningen, Netherlands. https://library.wur.nl/WebQuery/wurpubs/fulltext/20654.

Visalakshi M, Kishore Varma P, Chandra Sekhar V, Bharathalaxmi M, Manisha BL, Upendhar S (2020). Studies on mycosis of Metarhizium (Nomuraea) rileyi on Spodoptera frugiperda infesting maize in Andhra Pradesh India. Egypt. J. Biol. Pest Control, 30:135. https://doi.org/10.1186/s41938-020-00335-9.

Volkmar C, Hussein ML-Al, Jany D, Hunold I, Richter L, Kreuter T, Wetzel T (2003). Ecological studies on epigeous arthropod populations of transgenic sugar beet at Friemar (Thuringia? Germany). Agric. Ecosyst. Environ. 95(1):37-47. https://doi.org/10.1016/S0167-8809(02)00166-4.

Wale M, Schulthess F, Kairu EW, Omwega CO (2007). Effect of cropping systems on cereal stem borers in the cool‐wet and semi‐arid ecozones of the Amhara region of Ethiopia. Agric. For. Entomol. 9(2):73-84. https://doi.org/10.1111/j.1461-9563.2007.00324.x.

Wheeler GS, Ashley TR, Andrews KL (1989). Larval parasitoids and pathogens of the fall armyworm in Honduran maize. Entomophaga, 34:331-340. https://doi.org/10.1007/BF02372472.

Wood SA, Karp DS, De Clerck F, Kremen C, Naeem S, Palm CA (2015). Functional traits in agriculture: agrobiodiversity and ecosystem services. Trends Ecol. Evol. 30(9):531-539. https://doi.org/10.1016/j.tree.2015.06.013.

Youssef MAM (2021). The first report to record the parasitoids of the fall armyworm, Spodoptera frugiperda in Egypt. Int. J. Agric. Sci. 3(2):52-57. https://doi.org/10.21608/svuijas.2021.65535.1086.

Yousef M, Quesada-Moraga E, Garrido-Jurado I (2015). Compatibility of herbicides used in olive orchards with a Metarhizium brunneum strain used for the control of preimaginal stages of tephritids in the soil. J. Insect Sci. 88:605-612. https://doi.org/10.1007/s10340-014-0632-0.