Susceptibility of fall armyworm Spodoptera frugiperda (JE Smith) to microbial and botanical bioinsecticides and control failure likelihood estimation

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INTRODUCTION
The fall armyworm Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) is one of the most important polyphagous pests of maize and other important economic crops, in tropical and subtropical regions of the Americas.It was first reported on the African continent in 2016 (Goergen et al., 2016).Favorable climatic conditions, year-round availability of host plants, high reproductive capacity, and dispersal of adults have allowed the fall armyworm to establish itself permanently in Africa (Montezano et al., 2018;Prasanna et al., 2018).
The fall armyworm is currently managed mainly by the application of chemical insecticides (Kansiime et al., 2019;Houngbo et al., 2020).Their widespread and sometimes indiscriminate use in the Americas has resulted in high levels of resistance in fall armyworm populations to the major classes of insecticides such as carbamates, organochlorines, organophosphates and pyrethroids (Gutiérrez-Moreno et al., 2019).Not surprisingly, treatment failures have been reported by farmers as has already been the case in Mexico and Puerto Rico (Gutiérrez-Moreno et al., 2019).
Research and development of alternatives are high on the agenda for sustainable management of this pest in West Africa (Prasanna et al., 2018;Harrison et al., 2019).Bioinsecticides have the advantage of being less toxic to non-target organisms and human health (Bateman et al., 2018;Sisay et al., 2019).On one hand, plant extracts have demonstrated some potential insecticidal activities against the fall armyworm in field and laboratory conditions (Sisay et al., 2019;Phambala et al., 2020).On the other hand, a recent analysis of national pesticide and biopesticide lists from 19 African countries identified 29 biopesticides that could be approved for use in fall armyworm management (Bateman et al., 2018), subject to their efficacy being proven against this new pest.In this study, we evaluated the susceptibility of fall armyworm collected in Burkina Faso to seven bioinsecticides available on the West African market.

Insect collection and rearing.
A starter colony of fall armyworm was established from a maize field located in Nasso (11°13'11''N, 4°26'11''W), Houet province in Burkina Faso.Approximately 600 fourth-instar larvae were collected in November 2020.Larvae were reared in the laboratory on maize leaves as described by Ahissou et al. (2021a).The F1 generation was used for all bioassays.
Insecticide assay.Bioassays were conducted according to the adapted IRAC 020 protocol, by leaf dipping using first, second and third instar F1 larvae (http:// www.irac-online.org/).The first and second stages were used for plant extract-based bioinsecticides that were less toxic.They were performed as described by Ahissou et al. (2021a) and mortality was assessed after 72 h for all bioinsecticides except for spinetoram and spinosad (48 h).Each insecticide was tested using at least five concentrations, after dilution with distilled water containing Triton X-100 (0.2 g .l -1 ).Non-treated maize leaves were collected, washed with tap water and dried.Then, they were immersed for 10 seconds in the insecticide solution and left to dry for 1 h.Control leaves were treated only with a solution of Triton in water.Leaves were placed in individual Petri dishes (9 cm in diameter) containing blotting paper.A total of 40 larvae were individually exposed to each concentration of each tested product.

Statistical analysis.
Percentage mortality data were corrected for control mortality (Abbott, 1925) and subjected to probit analysis (Finney, 1971) using SPSS software, to calculate slope values, lethal concentrations (LC 50 ; LC 80 ), and fiducial limits (95%).Control failure likelihood (CFL) was calculated by multiplying the achieved mortality percentage by 100, dividing the product by the minimum required efficacy (e.g.70%) and subtracting the result from 100 (Guedes, 2017).Additionally, an ANOVA was performed to compare mortality rates between different concentrations of a bioinsecticide (Tukey's test, p < 0.05).

RESULTS
The observed control mortality rate was found to be less than 3% and was used to correct mortality.For the seven bioinsecticides tested, the theoretical values were not significantly different from the observed values, so the Probit model was considered appropriate (Tables 1  and 2).The LC 50 and LC 80 values and their confidence intervals and CFL are presented in table 1.
Spinetoram and spinosad were the most toxic of the insecticides tested with LC 80 values of 85.3 µg .l -1 and 437.9 µg .l -1 respectively.These values are 99% lower than recommended by the manufacturer.
Bacillus thuringiensis LC 50 and LC 80 values increased significantly with the developmental stage of the fall armyworm, as the confidence intervals did not overlap.Lethal concentration values were 5.6 to 10.6 times higher than the manufacturer's recommended dose, so the CFL is very high (74.3-100%).
Plant extract-based insecticides tested were less toxic to the fall armyworm larvae.Lethal concentrations values were 6 to 23 times higher than the manufacturers' recommended concentrations, meaning that the CFL is high.
For each bioinsecticide, the observed mortality rates were always affected by the tested concentrations (p < 0.0001) (Table 2).

DISCUSSION
Our study was conducted to identify low toxicity molecules effective against the fall armyworm in West Africa.Spinetoram (LC 80 = 85.3 µg .l -1 ) and spinosad (LC 80 = 437.9µg .l -1 ) insecticides have the best efficacy profiles against fall armyworm at concentrations significantly lower than manufacturers' recommendations.The high slope values (7.26 to 27.03) mean that a small increase in insecticide concentration is sufficient to significantly increase larval mortality, suggesting that the fall armyworm population is very sensitive to these molecules.At the recommended dose very limited treatment failure should be observed.Similar results were obtained in Brazil, China, Mexico and Puerto Rico (Gutiérrez-Moreno et al., 2019;Lira et al., 2020).With CFL close to zero, both spinosyns are more effective than chemical insecticides such as abamectin (CFL = 66%), deltamethrin (CFL = 80%), and lambda-cyhalothrin (CFL = 96%) (Ahissou et al., 2021a) which are widely used against this pest in West Africa (Kansiime et al., 2019;Ahissou et al., 2021b).
For the plant extract-based insecticides tested, the required LC 80 values were much higher than the manufacturers' recommended concentrations with better results on smaller larvae.However, it is interesting to note that the leaves treated with the botanical insecticides were not consumed by the larvae.Azadirachtin and C. procera are powerful food deterrents and insect growth regulators (Seigler, 1998;Isman, 2006).Their use should be recommended -as it is the case of azadirachtin in China (Zhao et al., 2020) -in fall armyworm IPM programs in combination with other compatible methods.

CONCLUSIONS
In conclusion, we recommend extending to farmers these results, which show that some bioinsecticides are very effective and could play an important role in IPM programs against fall armyworm.Apart from superior insecticidal activity relative to some chemical insecticides, such bioinsecticides have the advantage of being less toxic to non-target organisms.