¹Manguilibè Tchao,¹ Agbéko Kodjo Tounou,
¹Komi Agboka, ¹Gnon Tchein,
¹Tchegueni Matotiloa, ^1,2Atama Gnamkoulamba,
³Komla Sanda

¹Laboratoire de Recherche sur les Agroressources et Santé Environnementale (LARASE), Ecole Supérieure d’Agronomie (ESA),Université de Lomé (UL)

^1,2Institut National de Formation Agricole (INFA) de Tové

³Université de Kara

The fall armyworm Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) is an important maize pests that threaten food security in sub-Saharan Africa. In order to evaluate the diversity of natural enemies and especially their effectiveness for a sustainable management of this pest in Africa, a literature review was carried out. It consisted in exploiting 35 scientific publications from the most highly rated journals, over the period 2015-2020 relating to the inventory of the natural enemies of S. frugiperda and their effectiveness in the world in general and more particularly in Africa. It emerges from this study that there is a large diversity of natural enemies of S. frugiperda in the world. In total, 66 species of natural enemies belonging to 21 families in 10 orders have been recorded. Parasitoids have been the most studied 43 (64.18%) and the most used in the control of S. frugiperda, followed by predators 13 (19.40%) and entomopathogens (13.42%). In Africa, 24 of the 67 species have been recorded in 9 countries. Parasitoids were also created with a rate of 26.86% or 75.00% at the African level. The main most effective parasitoids were Telenomus remus (Hymenoptera: Scelionidae), Chelonus insularis Cresson (Hymenoptera: Braconidae) and Cotesia marginiventris Cresson (Hymenoptera: Braconidae) with parasitism rates varying between 0.85 and 9.90% depending on the environments. In view of the results, since these species have been listed in Africa, they seem to be real candidates for future programs for the sustainable management of this caterpillar. Research is underway in Togo and probably in the rest of the countries of the continent for a better knowledge and development of these natural enemies.

Corn, S. frugiperda, natural enemies, efficacy.

1) Adam, S., Edorh, P. A., Totin, H., Koumoulou, L., Amoussou E., Aklikokou, K. and Boko, M. 2010. Pesticides et métaux lourds dans l’eau de boisson, les sols et les sédiments de la ceinture cotonnière de Gogounou, Kandi et Banikoara (Benin). International Journal of Biological and Chemical Sciences, 4: 1170-1179.

2) Alain, K., Sawadogo, W., Nianogo J., Millogo-Rasolodimby, J., 2009. Usage des intrants chimiques dans un agrosystème tropical: diagnostic du risque de pollution environnementale dans la région cotonnière de l’est du Burkina Faso, Biotechnologie, Agronomie, Société et Environement, 4: 499-507.

3) Kostandini, G. and La Rovere R. 2015. Ex-ante welfareanalysis of technological change: the case of nitrogen efficient maize for African soils. Canadian Journal of Agriculture Economics, 64: 147-168.

4) Day, R., Abrahams, P., Bateman, M., Beale, T., Clotte, V., Cock M., Colmenarez, Y., Corniani, N., Early, R., Godwin, J. and al. 2017. Fall armyworm: impacts and implications for Africa. Outlooks on Pest Management, 28:196-201.

5) FAO. 2016. Guidelines on Highly Hazardous Pesticides. International Code of Conduct on Pesticide Management. Rome, Italy.

6) Wilmar, R-C., Julio C. R., Leopolodo C-L., Alfredo, C. and Edi A. M. 2016. Attraction, Feeding Preference, and Performance of Spodoptera frugiperda Larvae (Lepidoptera: Noctuidae) Reared on Two Varieties of Maize. Environmental Entomology, 45: 384-389. doi:10.1093/ee/nvv229.

7) Riggin, T. M., Espelie K. E., Wiseman, B. R. and Isenhour D. J. 1993. Distribution of fall armyworm (Lepidoptera: Noctuidae) parasitoids on five corn genotypes in South Georgia. Florida Entomologist, 76: 292–302.

8) Rios-Velasco, C., Gallegos-Morales, G., Cambero-Campos, J., Cerna-Chávez, E., Del Rincón-Castro, M. C. and Valenzuela-García R. 2011. Natural enemies of the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in Coahuila, México. Florida Entomologist, 94: 723–726.

9) Hogg, D. B., Anderson, R. E. and Pitre H. N. 1982. Early-season parasitization of fall armyworm (Lepidoptera: Noctuidae) larvae in Mississippi. Florida Entomologist, 65: 584–585.

10) Meagher, R. L., Nuessly, G., Nagoshi, R. N. and Hay-Roe, M. M. 2016. Parasitoids attacking fall armyworm (Lepidoptera: Noctuidae) in sweet corn habitats. Biological Control, 95: 66–72.

11) 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. Florida Entomologist, 86 254-289.

12) Beserra, E. B., Dias, C. T. and Parra, J. R. P. 2002. Distribution and natural parasitism of Spodoptera frugiperda (Lepidoptera: Noctuidae) eggs at different phenological stages of corn. Florida Entomologist, 85: 588–593.

13) Murúa, M. G., Molina-Ochoa, J. and Fidalgo, P. 2009. Natural distribution of parasitoids of larvae of the fall armyworm, Spodoptera frugiperda, in Argentina. Journal of Insect Science, 9: 20. doi: 10.1673/031.009.2001.

14) Nagoshi, R. N., Koffi D., Agboka K., Tounou K. A., Banerjee R., Jurat-Fuentes J. L et Meagher R. L., 2017. Comparative molecular analyses of invasive fall armyworm in Togo reveal strong similarities to populations from the eastern United States and the Greater Antilles. PLoS ONE, 12: 1-15. https://doi.org/10.1371/journal.pone.0181982.

15) Meagher, Jr. L. R., Agboka, K., Tounou, K. A., Koffi, D., Agbevohia, A. K., Amouze, R. T., Adjevi, M. K. and Nagoshi N. R. 2019. Comparison of pheromone trap design and lures for Spodoptera frugiperda in Togo and genetic characterization of moths caught. The Netherlands Entomological Society Entomologia Experimentalis et Applicata 1–10.

16) Koffi, D., Kyerematen R., Eziah V. Y., Agboka K. et Adom M. et al., 2020. Natural Enemies of the Fall Armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) in Ghana. Florida Entomologist, 103: 85-90.

17) Agboyi, L. K., Goergen G., Beseh P., Mensah S. A., Clottey V. A., Glikpo R., Buddie A., Cafà G., Oord L., Day R. , Ivan R. and Kenis M. 2019. Parasitoid Complex of Fall Armyworm, Spodoptera frugiperda, in Ghana and Benin. Insects, 10. doi:10.3390/insects10110410.

18) Tendeng, E., Labou, B., Diatte, M., Djiba S. and 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. International Journal of Biological and Chemistry Sciences, 13: 1011–1026.

19) Ordóñez-García, M., Rios-Velasco C., Berlanga-Reyes D. I., Acosta-Muñiz C. H., Salas-Marina M. A. and Cambero-Campos, O. J. 2015. Occurrence of natural enemies of Spodoptera frugiperda (Lepidoptera: Noctuidae) in Chihuahua, Mexico. Florida Entomologist, 98: 843–847.

20) López, M. A., Martínez-Castillo A. M., García-Gutiérrez C., Cortez-Mondaca E. and EscobedoBonilla C. M. 2018. Parasitoids and Entomopathogens Associated with Fall Armyworm, Spodoptera frugiperda, in Northern Sinaloa. Southwestern Entomologist, 43: 867-881.

21) Araiza, M. D. S. 2018. Natural Enemies of the Fall Armyworm1 and the Corn Earworm2 in Sorghum and Maize in Irapuato, Guanajuato, Mexico. Southwestern Entomologist, 43:715-722.

22) Jaraleño-Teniente, J., Lomeli-Flores J. R., Rodríguez-Leyva E., Bujanos-Muñiz R. and Rodríguez-Rodríguez E. S. 2020. Egg Parasitoids Survey of Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) in Maize and Sorghum in Central Mexico. Insects, 11, 157. doi:10.3390/insects11030157.

23) Ngangambe, M. H. et Mwatawala W. M. 2020. Effects of entomopathogenic fungi (EPFs) and cropping systems on parasitoids of fall armyworm (Spodoptera frugiperda) on maize in eastern central, Tanzania. Biocontrol Science and Technology, DOI: 10.1080/09583157.2020.1726878.

24) Firake, D.M. and Behere G. T. 2020. Natural mortality of invasive fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) in maize agroecosystems of northeast India. Biological Control, 148. doi:10.1016/j.biocontrol.2020.104303.

25) Sisay, B., Simiyu J., Malusi P., Likhayo P., Mendesil E., Elibariki N., Wakgari M., Ayalew G. and Tefera T. 2018. First report of the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), natural enemies from Africa. Journal of Applied Entomology, 142: 800-804.

26) Caniço, A., Mexia, A. and Santos L. 2020. First Report of Native Parasitoids of Fall Armyworm Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) in Mozambique. Insects, 11: 1-12. Doi:10.3390/insects11090615.

27) Ankita, G., Ramesh, B. S. 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: 193-196.

28) Shylesha, A. N., Jalali, S. K., Gupta, A., Varshney, R., Venkatesan, T., Shetty, P., Ojha, R., Ganiger, P. C., Navik, O., Subaharan, K., Bakthavatsalam, N. and Ballal, C. R. 2018. Studies on new invasive pest Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) and its natural enemies. Journal of Biological Control, 32: 145-151.

29) Sharanabasappa, Kalleshwaraswamy, C. M., Maruthi, M. S., Pavithra, H. B., Poorani, J. and Diraviam, J., 2019. Natural enemies of Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), a recent invasive pest on maize in South India. Florida Entomologist, 102: 618-623. doi:10.1653/024.102.0335.

30) Liao, Y., Yang, B., Xu, M., Lin, W., Wang, D., Chen, K. and Chen, H. 2019. First report of Telenomus remus parasitizing Spodoptera frugiperda and its natural parasitism in South China. Article in press.

31) Kenis, M., du Plessis, H., Van den Berg, J., Ba, M., Goergen, G., Kwadjo, K., Baoua, I., Tefera, T., Buddie, A., Cafà, G., Offord, L., Rwomushana, I. and 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, 92. doi:10.3390/insects10040092.

32) Sun, B., Li, F., He, X., Cao, F., Bandason, E., Shapiro-Ilan, D., Ruan, W. and Wu, S. 2020. First report of Ovomermis sinensis (Nematoda: Mermithidae) parasitizing fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in China. Journal of nematology, 52. e2020-50.

33) Rivero-Borja, M., Guzmán-Franco, A. W., Rodríguez-Leyva, E., Santillán-Ortega, C. and Pérez, P. A. 2018. Interaction of Beauveria bassiana and Metarhizium anisopliae with chlorpyrifos ethyl and spinosad in Spodoptera frugiperda larvae: Fungusinsecticide interactions. Pest Management Science, 74 : 2047-2052.

34) Gichuhi, J., Subramanian, S., Khamis, F. M., Van den Berg, J., du Plessis, H., Ekesi, S. and Herren, J. K. 2019. Diversity of fall armyworm, Spodoptera frugiperda and their gut bacterial community in Kenya. doi: https://doi.org/10.1101/664987.

35) Raghunandan, B. L., Patel, N. M., Dave, H. J. and Mehta, D. M. 2019. Natural occurrence of nucleopolyhedrovirus infecting fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) in Gujarat, India. Journal of Entomology and Zoology Studies, 7: 1040-1043.

36) Luis Pidre, M., Sabalette, K. B., Romanowski, V. and Ferrelli, M. L. 2018. Identification of an Argentinaan isolate of Spodoptera frugiperda granulovirus. Revista A rgentina de Microbiología, 51:381-385.

37) García-Banderas, D., Tamayo-Mejía, F., Pineda, S., de la Rosa, J. I. F., Lasa, R., Chavarrieta-Yá ñez, J. M., Gervasio-Rosas, E., Zamora-Avilés, N., Morales, S. I., Ramos-Ortiz, S.,Valle, J. and Martínez-Castillo, A. M. 2020. Biological characterization of two Spodoptera frugiperda nucleopolyhedrovirus isolates from Mexico and evaluation of one isolate in a small-scale field trial. Biological Control, 104316. https://doi.org/10.1016/j.biocontrol.2020.104316.

38) Figueiredo, M. L. C., Cruz, I., da Silva, R. B. and Foster, J. E. 2018. Biological control with Trichogramma pretiosum increases organic maize productivity by 19.4%. Agronomy for Sustainable Development, 35:1175–1183.

39) Bentivenha, J. P. F., Rodrigues, J. G., Lima, M. F., Marçon, P., Popham, H. J. R. and Omoto, C. 2018. Baseline Susceptibility of Spodoptera frugiperda (Lepidoptera: Noctuidae) to SfMNPV and Evaluation of Cross-Resistance to Major Insecticides and Bt Proteins. Journal of Economic Entomology, 20: 1–8.

40) de Lira, A. C., Mascarin, G. M. and Delalibera, J. Í. 2020. Microsclerotia production of Metarhizium spp. for dual role as plant biostimulant and control of Spodoptera frugiperda through corn seed coating, Fungal Biology, doi: https://doi.org/10.1016/j.funbio.2020.03.011.

41) Pomari-Fernandes, A., Bueno, A. F., De Bortoli, S. A. and Favetti, B. F. 2018. Dispersal capacity of the egg parasitoid Telenomus remus Nixon (Hymenoptera: Platygastridae) in maize and soybean crops. Biological Control, 126: 158–168.

42) Dasilva, C. S. B., Vieira, J. M., Loiácono, M., Margaría, C. and Parra, J. R. P. 2015. Evidence of exploitative competition among egg parasitoids of Spodoptera frugiperda (Lepidoptera: Noctuidae) in maize. Revista Colombiana de Entomología, 41: 184-186.

43) Moral, R. A., Demétrioa, C. G. B. HIndia, J. B., Godoy, A. W. C. and Fernandes, F. S. 2016. Parasitism-mediated prey selectivity in laboratory conditions and implications for biological control, Basic and Applied Ecology, article in press.

44) Perier, J. D. 2018. Integration of two predaceous stinbugs and a larval parasitoid to manage the Fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). College of agricultural and food sciences in partial fulfillment of the requirement of the degree of Master in science in agricultural sciences, 66p.

45) Contreras-Cornejoa, H. A., del-Vala, E., Macías-Rodríguezc, L., Alarcónd, A., Carlos, E. González-Esquivela, C. E. and Larsena, J. 2018. Trichoderma atroviride, a maize root associated fungus, increases the parasitism rate of the fall armyworm Spodoptera frugiperda by its natural enemy Campoletis sonorensis. Soil Biology and Biochemistry, 122:196–202.

46) Hernandez-Trejo, A., Estrada-Drouaillet, B., López-Santillán, J. A., Rios-Velasco, C., Rodríguez-Herrera, R. and Osorio-Hernández, E. 2019. Effects of Native Entomopathogenic Fungal Strains and Neem Extract on Spodoptera frugiperda on Maize. Southwestern Entomologist, 44: 117-124.

47) Salazar-Mendoza, P., Rodriguez-Saona, C. and Fernandes, A. O. 2020. Release density, dispersal capacity, and optimal rearing conditions for Telenomus remus, an egg parasitoid of Spodoptera frugiperda, in maize. Biocontrol Science and Technology, DOI: 10.1080/09583157.2020.1776841.

48) Mallapur, C., Naik, A. K., Hagari, S. and Lingappa, S. 2018. Potentiality of Nomuraea rileyi (Farlow) Samson against the fall armyworm, Spodoptera frugiperda (J.E Smith) infesting maize. Journal of Entomology and Zoology Studies, 6.

49) Qing Xuan, X., Song, W., RenBin, T., Su, W., Fan, Z., Jiao, M., Shu, L. and Ning D. 2019. Study on the predation potential of Chrysopa pallens on Spodoptera frugiperda. Journal of Environmental Entomology, 41: 754-759.

50) Akutse, K. S., Kimemia, J. W., Ekesi, S., Khamis, F. M., Ombura, O. L. and Subramanian, S. 2019. Ovicidal effects of entomopathogenic fungal isolates on the invasive Fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Applied Entomology, 00: 1-9. https://doi.org/10.1111/jen.12634.

51) Ashley, T. R. 1979. Classification and distribution of fall armyworm parasites. Florida Entomologist, 62: 114–123.

52) Goergen, G., Kumar, P., Sankung, S., 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 West and Central Africa, PLoS ONE, 10: e0165632.

53) Varella, A. C., Menezes-Netto, C. A., Alonso, J. D., Caixeta, D. F., Peterson, R. K. D. and Fernandes, O. A. 2015. Mortality Dynamics of Spodoptera frugiperda (Lepidoptera: Noctuidae) Immatures in Maize. PLoS ONE, 10. doi:10.1371/journal. pone.0130437.

54) Polaszek, A. 1992. Cereal stem boers and their parasitoids in Africa. Proceedings of the Section Experimental and Applied Entomology of the Netherlands Entomological Society, 3:70-71.

55) Skovgård, H. and Päts P., 1996. Effects of intercropping on maize stemborers and their natural enemies. Bulletin of Entomological Research, 86: 599-607. doi:10.1017/s0007485300039407.

56) Polaszek, A. 1995. Cereal stem borers in Africa: Taxonomy and natural enemies. Handbook for training course held at ICIPE Nairobi, 15–28 October 1995.

57) Viteri, D. M., Linares, A. M. and Flores, L. 2018. Use of the entomopathogenic nematode Steinernema carpocapsae in combination with low-toxicity insecticides to control fall armyworm (Lepidoptera: Noctuidae) larvae. Florida Entomologist, 101:327–9.

58) FAO, 2018b. Gestion intégrée de la chenille légionnaire d’automne sur le maïs. Un guide pour les champs-écoles des producteurs en Afrique. Pesticides botaniques pour la gestion de la chenille légionnaire d’automne.

59) Vieira, N. F., Pomari-Fernandes, A., Lemes, A. A. F., Vacari, A. M, De Bortoli, S. A. and Bueno, A. F. 2017. Cost of Production of Telenomus remus (Hymenoptera: Platygastridae) Grown in Natural and Alternative Hosts. Journal of Economic Entomology, 110: 2724–2726.

Volume 05 Issue 07 July 2022

There is an Open Access article, distributed under the term of the Creative Commons Attribution – Non Commercial 4.0 International (CC BY-NC 4.0) (https://creativecommons.org/licenses/by-nc/4.0/), which permits remixing, adapting and building upon the work for non-commercial use, provided the original work is properly cited.