Entomophagous Insects of The Invasive Fall Armyworm, Spodoptera frugiperda (Nixon) in African and Asian countries

and 16 larval parasitoids) have been recorded as well as 11 predator species. The most common egg parasitoid is Telenomus remus which is recorded in 8 countries of Africa as well as three countries of Asia (out of the 4 countries mentioned in Asia). The most common egg-larval parasitoid in Africa is Chelonus bifoveolatus as it is recorded in 8 countries whereas Ch. formosanus and Ch. nr blackburni are recorded in India (Asia). The most common larval parasitoids in Africa are Coccygidium luteum (7 countries), Cotesia icipe (6 countries) and Charops sp. (6 countries), whereas the most common one in India (Asia) is Campoletis chlorideae.


INTRODUCTION
The fall armyworm, Spodoptera frugiperdais (Nixon) is a highly destructive pest of cereals and is native to the tropical and subtropical regions of North, Central and South America (Kenis et al., 2019). It has been considered a risk to food security (Sagar et al., 2022). The insect is polyphagous with a host range of 353 plant species in 76 families (Montezano et al, 2018). It can cause 8.3 to 20.6 million tones losses in maize yield/year which represent 21 -53% of the total production (Day et al., 2020). However, Baudron et al. (2019) and Kumela et al. (2019) recorded 11.6% and 32 -47% yield losses, respectively.
As reported by Tending et al. (2019) the total life cycle of FAW averaged 25 days (22 -28 days) at 25 ºC. The female can deposit 1500 -2000 eggs during its life span which ranges from 7-10 days at 28 ºC . Abd Elmageed et al. (2021) reported that the incubation period of the egg, larval and pupal periods were found to be 3.47, 20.93, and 12.6 days, respectively, at 26 ºC and 55% R.H. whereas the total life cycle from egg to adult averaged 37.7 days.
The IPM of FAW has been carried out by agricultural control, chemical insecticides, sex attractants, bio-control agents (including parasitoids, predators and entomopathogens) as well as botanicals (Wan et al., 2021). The absence of diapause, the short generation time, the high fecundity and the resistance to at least 29 chemical insecticides including carbamates, organophosphorus and pyrethroids are the main factors that made S. frugiperda one of the most serious pests of crops mainly maize, rice and sorghum (Wan et al., 2021). In addition, S. frugiperda could develop resistance to Bt crops including corn and the first case of this resistance was observed in 2006 in Puerto Rico, USA after 3 years of planting Bt corn causing considerable losses of the yield that forced farmers to stop planting this crop (Abbas, 2016). Hence, the use of biological control agents seems to be a preferred method for its control providing high effectiveness as stated by Colmenarez et al., (2022).
S. frugiperda was first detected in the African continent starting from 2016 in West and Central Africa (Goergen et al., 2016, Ahissou et al.,2021a, Rwanda (Uzayisenga et al., 2018), Senegal (Brevault et al., 2018, in Sudan (Ebadi, 2022), in Egypt (Youssif, 2021;Rashed et al., 2022), and over 44 African countries (Abang et al., 2020). The insect was also recorded in several countries in Asia including India, China, Korea, Japan, Viet Nam and Sri Lanka Dao et al., 2020) as well as Syria, Jourdon and Israel (Pehlivan and Atakan, 2022). The insect successfully invaded Europe (Germany and the Netherlands, Agboyi et al.,2021, Jindal et al., 2021, Sun et al., 2021and Turkey, (Pehlivan and Atakan, 2022 as well as Australia (Apirajkamol et al. 2022). Early et al. (2018) stated that the environmental requirements for this pest to establish itself permanently are present in large parts of Africa and Asia. S. frugiperda was recorded to have the potential to cause losses in maize yield reaching 8 -20 tons per year equal to 13 billion USD per year in 12 African countries (Day et al., 2020). Ahissou et al.(2021b) claimed that Africa may be more appropriate for FAW biological control than North America for two reasons: 1. small-scale production of maize and other crops often closely cultivated, 2. chemical insecticides were rarely used in maize crops before the arrival of FAW in Africa. Both reasons probably make natural enemies easier to protect the crop.
(2019) could obtain T. chilonis from eggs of FAW collected from maize fields in Kenya.

B.The Recorded Entomophagous Insects of FAW in Asian Countries:
According to literature, the survey of natural enemies of S. frugiperda in Asia has been carried out in only 4 countries up till now; India, China, Nipal and Indonesia. a.Parasitoids (Table 2): Jindal et al. (2021) reported that FAW larvae were collected during 2019 and 2020 from maize crops in India but no parasitoids could be observed in 2019. However, 2 parasitoid species could be obtained during 2020: Campoletis sp. and Chelonus formosonus Sonan. Parasitism rates were found to be 21.92 and 16.33% by the two species, respectively. A survey of natural enemies of S. frugiperda in South India in 2018 revealed the occurrence of 5 larval parasitoids: Coccogidium melleum, Eriborus sp., Odontepyris sp., Campoletis chlorideae Uchida and Exorista sorbillans. The first 3 species were recorded for the firsttime parasitizing S. frugiperda. The average parasitism by C. chlorideae was 2-3% whereas the other parasitoids showed negligible parasitism (Sharanabasappa et al. (2019).
A survey of the natural enemies complex in maize fields in North India showed 80.46% larval mortality of S. frugiperda. The egg-larval parasitoid, Chelonus nr. blackburni was the predominant parasitoid causing 49.24% larval mortality followed by Ch. formosanus. The survey also revealed the occurrence of the ichneumonid parasitoid, Temeluca sp. for the first time parasitizing FAW larvae in the fields (Sagar et al.,2022). A survey was conducted during 2019 -2020 at different locations in Tamil Nadu (India) for the natural enemies of S. frugiperda in maize fields (Anandhi and Saminathan, 2021). They obtained 4 parasitoid species namely: Peribeae sp. (Dipt.:Tachinidae), Euplectrus sp. nr. Xanthocephalus Girault and Temelucha sp. (Ichneumonidae) and the braconid, Microplitis domolitor Wilkenson for the first time in Tamil Nadu. , in a survey of FAW natural enemies in India, could obtain the egg parasitoids, Telenomus sp. and Trichogramma sp.; the larval parasitoids, Glyptapanteles creatonoti (Vier.), Campoletis chlorideae Uchida and an unidentified ichneomonid larval-pupal parasitoid. The parasitoid Coccygidium transcaspicum (Kokujev) (Hymenoptera: Braconidae) was obtained from fall armyworm S. frugiperda in maize fields in South India in 2019. It was the first report of C. transcaspicum as a parasitoid of S. frugiperda across the globe as mentioned by Gupta et al. (2020). Mallapur et al. (2022) carried out a survey of natural enemies of S. frugiperda in different maize fields in India, during 2019 and 2020 and obtained 2 parasitoids, Campoletes chloridae and Chelonus formosanus. Liao et al. (2019), in China, reported that 36 egg masses of FAW were collected from maize fields in 3 sites in China in 2019 out of which 11 egg masses (30.6%) were found to be parasitized by Tel. remus. Megaselia scalaris Loew (Dipt.: Phoridae) was reported as a parasitoid of S. frugiperda larvae and pupae for the first time in China as reported by Tang et al. (2021. In Indonesia, a survey of egg parasitoids of S. frugiperda was carried out in 3 different corn fields by placing 323 egg masses (8-h-old) of S. frugiperda on the plants for 24 h. The results showed that two egg parasitoids could be obtained, Telenomus sp. and Trichogramma sp. with percent parasitism ranging from 55.7-100% by Telenomus sp. and 0.0 -44% by Trichogramma sp. (Wahyuningsih et al., 2022). Also, Supeno et al. (2021), in Indonesia, recorded 3 larval parasitoids on S. frugiperda; Apanteles sp. (Hym.: Braconidae), Eriborus sp. (Hym.: Ichneumonidae) and Exorista sp. (Dipt.: Tachinidae). The average total rate of parasitism by the 3 parasitoids was 2.16%. The levels of parasitoids dominance were 67% (Tachinidae), 22% (Braconidae) and 11% (Ichneumonidae). b.Predators (Table 3): Sharanabasappa et al. (2019) recorded 3 predator species associated with FAW in maize fields in South India in 2018. The predators were Forficula sp., Harmonia octomaculata and Coccinella transvirsalis.  obtained the dermapteran predator, Forficula sp. associated with S. frugiperda in maize fields in Tamil Nadu. In addition, Shylesha and Sravika (2018) reported that nymphs and adults of Eocanthecona furcellata (Wolf) and Andrallus spinidens (Fabr.) (Hemiptera: Pentatomidae) were found to associate with S. frugiperda in maize fields in India. Also, Keerthy et al. (2020) reported E.furcellata as an important predator of S.frugiperda in maize fields in India. The pentatomids, Arma chinesis (Fallou) (Tang et al.,2019a) and Picromorus lewisi Scott (Tang et al., 2019b) were recorded as predators of S. frugiperda in maize fields in China. Also, Abbas et al. (2022), in China, reported the earwig, Doru luteipes (Scudder) as a predator of S. frugiperda in maize fields. Zeng et al. (2021) reported the anthocorid, Orius similis Zeng (Hem.: Anthocoridae) as a native predator of S. frugiperda in China.

C.Laboratory and Field Studies on Parasitoids and Predators of S. frugiperda:
In Zambia, Sun et al. (2021) reported that the efficiency of the egg parasitoids, T. mwanzai and Trichogrammatoidea lutea, emerged from eggs of FAW in Zambia as compared to 3 species of Trichogramma native to China under laboratory conditions. The 3 species were T.ostriniae, T.leucaniae and T.japonicum. The results showed that Trichogrammatoidea was the best performing on FAW eggs among the 5 species and caused the highest rate of parasitism. Mohamed et al. (2021), in Kenya, found that C. icipe females accepted the 1 st instar than the and 2 nd instar larvae of S. frugiperda with parasitism levels of more than 60%, followed by the 3 rd instar, while the 4 th instar was the least accepted for oviposition. The 5 th and 6 th instars and pupal stages were not accepted for oviposition. In Kenya, over 140.000 wasps of each of Tel.remus and T. chilonis that parasitize FAW eggs; and 5000 wasps of C. icipe that parasitizes early larval instars of FAW have been released in maize fields in 5 counties. The initial post-release assessments revealed that rates of parasitism in FAW in the fields increased by 55, 50 and 38% for T. chilonis, Tel.remus and C. icipe , respectively (Anonymous, 2021).
Three releases (of 15,000 individuals, each) of Tel. remus were applied in maize plots of 0.5 ha in the major and minor rainy seasons of 2020, and compared to non-release control plots as well as to insecticide-treated plots in Ghana (Agboyi et al. (2021). No parasitism in egg masses was observed before the first release. Parasitism in egg masses after release reached 33% in the release plot of the major rainy season compared to 72 -100% in the minor rainy season and during which pest densities were much lower. However, no significant differences in egg parasitism were found among the release plots, the no-release control plots and the insecticide-treated plots. Similarly, no significant decrease in larval numbers or plant damage was found between the 3 treatments as well as no significant differences in cob damage or yield were noticed among the 3 treatments. The authors claimed that the lack of any significant differences between the 3 treatments might be attributed to the parasitoid dispersal during the 5 weeks of observation. The authors also mentioned that Tel. remus is able to parasitize the whole egg mass of S. frugiperda whereas Trichogramma spp. tend to parasitize only part of the egg mass. This is due to that the egg masses often consist of several layers and the female moth covers egg masses with scales that provide a barrier for Trichogramma females but not to Tel. remus. Similarly, Laminou et al. (2020), in Niger, reported that the egg parasitoids, Tel. remus and Trichogrammatoidea sp. were assessed in the laboratory for parasitizing egg masses of FAW. Tel.remus parasitized an average of 75% of the eggs, compared to 25% for Trichogrammatoidea sp. Tel.remus was able to parasitize egg masses that were fully covered with scales while, Trichogrammatoidea sp. parasitized only uncovered egg masses. In addition, releases of Tel.remus in sorghum fields caused up to 64% parasitism in FAW eggs. In this respect, in Egypt, we have never obtained Trichogramma from thousands of egg masses (which are covered with scales) of the cotton leaf worm, Spodoptera littoralis (Boisd) collected from the fields. Interestingly, we could obtain T.evanescens from 4 egg masses of S.littoralis (uncovered with scales) collected from a sugar cane field adjacent to a cotton field (Personal information). T.evanescens is an efficient egg parasitoid of the sugar cane borer, Chilo agamemnon (Bles.) in Egypt. Shen et al. (2023) obtained the egg-larval parasitoid, Ch. bifoveolatus from larvae of S. frugiperda in Zambia. The laboratory studies revealed that the female parasitoid could accept FAW eggs at 0.0, 1 and 2-day old and completed development successfully. The rates of parasitism, pupal rate and emergence rate for the parasitoid at the tested ages of eggs were higher than 90%, 75% and 82%, respectively. Sharanabasappa et al. (2021) reported Megaselia scalaris as a parasitoid of S. fugiperda for the first time in India. In the laboratory, the female was found to deposit the eggs on the 6 th larval instar or the pre-pupa and the adults emerge from the pre-pupa or the pupa. Evaluation of the efficiency of the egg parasitoids T. chilonis, T.dendrolimi and T.pretiosum for the control of S.frugiperda in maize fields in China was carried out by Yang et al. (2022). Release of Trichogramma wasps was done in cages (2x2x2 m) containing 20-25 maize plants each. 100 FAW eggs and 100 wasps were released in each cage 5 times at about 8 days intervals and rates of parasitism were assessed 48 h post-release. The results showed rates of parasitism ranged from 10.6 -24.5, 17.9 -31.4 and 16.6 -30.2% by T. chilonis, T.dendrolimi and T.pretiosum, respectively. However, there were no significant differences among the 5 releases. Also in Indonesia, Sari et al.
(2020) exposed each of the egg masses of S. frugiperda to a mated female of Tel.remus in a tube for 24 h. The rates of parasitism averaged 69.4% (35/50 eggs), the survival rates of emerged adults averaged 60% and the % of females was 74%. Ghosh et al. (2022), in India, reported that 3 releases of the larval parasitoid, Bracon brevicornis (Wesm.) in maize fields at a rate of 4000 adults/ha at weekly intervals caused a 54% average reduction in infestation by S. frugiperda. Varshney et al. (2021), in India, designed a biocontrol-based integrated pest management (IPM) strategy for FAW in the field in the spring and autumn seasons (2018)(2019). This strategy comprised the installation of FAW pheromone traps, 4 releases of Trichogramma pretiosum Riley, 2 sprays of neem oil, one spray of each of Bacillus thuringiensis  and Metarhizium anisopliae . The results showed reductions of 76 and 71 % in egg masses and 80 and 74% in larval populations at 60 days after application in spring and autumn seasons, respectively. In addition, cob yield/acre was higher compared to farmers` practice (6 -7 sprays of emamectin benzoate 5% SG in spring and autumn seasons). Also, Muniappan (2023) suggested an IPM program for S. frugiperda in maize fields in South Asia that involved seed treatment by insecticides, the release of the egg parasitoids, T. pretiosum and Tel. remus, pheromone traps, and the release of the larval parasitoids, Bracon hebetor Say and B. brevicornis. Shylesha and Sravika (2018) found that nymphs and adults of Eocanthecona furcellata (Wolf) and Andrallus spinidens (Fabr.) (Hemiptera: Pentatomidae) were found preying on S. frugiperda effectively in maize fields in India. The authors mentioned that both species are being reared for potential an IPM program of FAW. Keerthy et al. (2020), in India, reported that the adult of E.furcellata was capable of feeding on 126, 88 and 69 2 nd , 4 th and 6 th larval instars of FAW in the laboratory during its lifetime in the laboratory. Also, Abbas et al. (2022), in China, reported the earwig, Doru luteipes (Scudder) as a predator of S. frugiperda in maize fields and both the nymph and adult were found to consume 8 -12 and 10 -21 S. frugiperda larvae daily, respectively, in the laboratory. Adults of Orius similis Zeng (Hem.: Anthocoridae) were found to prey on eggs and only 1 st instar larvae of S. frugiperda in the laboratory. The maximum daily consumption of females was 23.7 eggs or 26.2 larvae whereas the male consumed 22.5 eggs or 19.6 larvae (Zeng et al., 2021).  reported that 2 nd and 3 rd instar larvae of Eupeodes corolla (Dipt.: Syrphidae) preyed on 1 st and 2 nd instar larvae of FAW consuming a maximum of 54.5 and 83.3 larvae, respectively, over 24 h period. Interestingly, once Spodoptera larvae reached 3 rd instar, they exhibited aggressive behavior and equally preyed on surphid larvae. The 5 th and 6 th instar larvae consumed 16.4 -19,2, 6.0 -19.6 and 6.7-8.3 of 1 st , 2 nd and 3 rd instar E.corolla larvae/day, respectively.

Conclusion
A total of 48 and 24 parasitoids as well as 17 and 11 predators have been recorded, so far, as entomophagous insects of S. frugiperda in Africa and Asia, respectively. These different species of parasitoids and predators attacking the developmental stages of S. frugiperda can have a considerable role in the IPM strategy against this pest.