Baseline toxicity and ovicidal action of different insecticides on new invasive insect pest into India: Fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae)

doi:10.21203/rs.3.rs-4859930/v1

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Baseline toxicity and ovicidal action of different insecticides on new invasive insect pest into India: Fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae)

https://doi.org/10.21203/rs.3.rs-4859930/v1

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Fall armyworm (Spodoptera frugiperda) (J.E. Smith) is a recent and invasive destructive insect pest of corn and other major crops of India; if left uncontrolled, it can destroy a crop totally. The pest carries history of resistance to many insecticides from its nativity and spread across the globe. It is likely to bear and /or develop resistance to a range of insecticides presently being used for its management in India, a possibility that has to be monitored regularly. The egg, being the first stage of the pest’s life cycle, is ideal for controlling its proliferation, and assessing the toxicity of different pesticides to eggs and larvae, and resistance, if any, to the pesticides is important for baseline studies. Accordingly, the present study assessed with common pesticides. In terms of their larvicidal action 72 h after application, chlorantraniliprole was found to be the most toxic, followed, in that order, by emamectin benzoate, flubendiamide, spinetoram, Spinosad, and azadirachtin. That order changed when the insecticides were tested for ovicidal action: thiodicarb was the most toxic, followed by spinetoram. Mortality was the highest in 3-day-old eggs, higher than that recorded in 1- or 2-day-old eggs and higher at the recommended doses than at half the recommended doses. Such differences in the target – larvae or eggs – are crucial to devising effective strategies for controlling insect pests. The strategies will be even more effective if the mechanism of action of the newer insecticides is elucidated.

Fall Armyworm

Maize

Toxicity

Ovicidal

The fall armyworm (FAW) (SN, family: order) originated in the South America and spread to Africa; in Africa, the pest was first noticed in 2016 and, within a short period, spread to more than 40 countries (Cook et al.2017; Day et al. 2017). Since 2016, FAW has resulted in extensive losses to maize in Africa, estimated at up to $5.50 million dollars annually in the top ten maize-producing countries and has been declared a serious threat to food security of the African continent (Anon. 2017). Recently, FAW has been detected in Asia as well (Abrahams et al. 2017; Day et al. 2017). In India, FAW on maize was recorded for the first time in Shivamogga district in Karnataka during May-June 2018 (Sharanabasappa et al. 2018) and the extent of damage to kharif maize in Karnataka was estimated at 6–100% (Mallapur et al. 2018). Another estimate put the potential reduction in maize yield at 45% (Hruska and Gladstone, 1988). Left uncontrolled, the figure can be as high as 100% in the tropics (Blanco et al. 2016). Controlling the pest is also rendered difficult because FAW lays its eggs within the host plants, and the behaviour of its larvae is such that it reduces the possibility of direct exposure to most of the insecticides. Clusters of 10–500 eggs are deposited throughout the plant canopy, especially on the underside of leaves or inside whorls. Groups of first-instar larvae are usually seen close to the spot where the eggs were deposited, but later-instar larvae scatter themselves among nearby plants (Ali et al.1989, Ali et al. 1990).

An array of management strategies, mostly centred on insecticides, has been proposed to manage FAW. Synthetic insecticides have proved less effective because FAW has developed resistance to them and lately even transgenic crops with Bt-proteins have been infested (Yu., 1982; Giraudo et al. 2014; Flagel et al., 2018). Resistance to carbaryl was first reported in Tifton, Georgia, USA (Young and McMillian, 1979). Data on dose–mortality provide baseline data not only for future monitoring of resistance to pesticides (Cook et al. 2004) but also for effective management of pests in the field. In the case of FAW, such data are available mostly for older insecticides.

One effective strategy in managing pests is to target their eggs, although only a few studies have compared the relative susceptibilities of eggs and adults to pesticides. Eggs also offer a convenient unit for study; represent a significant proportion of pest population; and, when laid in mass, offer an easy target. However, the susceptibility of insect eggs to insecticides changes during embryonic development and with the age of the eggs (Salkeld and Potter, 1953).

It was against this background that the present study sought to assess the baseline toxicity and the larvicidal and ovicidal action of different insecticides against the fall armyworm, Spodoptera frugiperda.

Spodoptera frugiperda was reared on maize leaves (hybrid DMH 119) in the laboratory at the Department of Entomology, College of Agriculture, Dharwad (Karnataka, India) from egg masses and caterpillars of FAW collected from a field of maize from the Main Agricultural Research Station, Dharwad. A fresh crop of maize was grown under insecticide-free conditions, used as a food for rearing of the host throughout the experiment. The egg masses were incubated, and the emerging neonates were fed on maize leaves up to pupation. The pupae were collected and kept in an emergence cage (36 cm × 36 cm × 36 cm), and the adults were given a 10% solution of honey as food. Fresh leaves of maize were provided for oviposition. One or two egg masses along with leaf bits were placed in Petri dishes (10 cm in diameter and 1.5 cm deep) for hatching. The neonate larvae emerging from the egg masses within the Petri dishes were kept separately in well-aerated plastic containers (25 cm × 9 cm × 10 cm) and reared on fresh and tender leaves of maize, which were replaced daily. The larvae were moved to larger containers (32 cm × 25 cm × 10 cm) to avoid overcrowding and to promote uniform growth and development. The rearing containers were sterilized with 0.01% sodium hypochlorite. The caterpillars were reared up to the 3rd-instar stage and then collected for the toxicity assays as and when required, and those that remained were used for further multiplication.

Preparation of insecticidal solutions:

All the test products used for the study were procured from the market. The insecticide formulations were diluted to achieve the required concentration using distilled water, and further serial dilution were achieved using Pearson’s square formula (Pearson, 1857).

Bioassay for larvicidal action:

Each test dose (2µL) was applied on the thoracic region of the 3rd-instar larvae placed in a Petri dish using a Hamilton topical micro applicator (Paramasivam and Selvi, 2017). First, the appropriate dosage range of each insecticide to get mortality between 20 and 80% was determined through pilot studies, following which each insecticide was tested at each of the six concentrations. Each concentration (treatment) was tested on 20 larvae and the test was replicated three times. A dose of 2µL of distilled water applied the same way served as a control. The larvae were considered dead if they appeared malformed, shrunk, and inactive. Mortality was recorded 24 h, 48 h, and 72 h after the treatment and its values were corrected using the formula developed by Abbot (1925):

Corrected mortality (%)	=	Mortality in treatment (%) – Mortality in control (%)	× 100
		100 – Mortality in control (%)

The data were then subjected to probit analysis (Abbott, 1925) for calculating LC₅₀ and LC₉₅ for each insecticide (lethal concentrations at which 50% and 95% of the treated population are killed, respectively).

Bioassay for ovicidal action

Egg masses required for the experiment were collected from the oviposition cages and sprayed with 0.01% sodium hypochlorite to eliminate any fungal infection before treating the eggs with the insecticides. The insecticide solutions were prepared using commercial-grade insecticides and diluted using distilled water to achieve the recommended concentrations and also 50% of the recommended concentrations. The details of the insecticides and the dosage used for treating the eggs of different ages are furnished in Table 1.

The eggs,1-, 2-, or 3-day-old, along with pieces of maize leaves, were placed in Petri dishes (100 mm in diameter) the base of which was lined with a filter paper to maintain moisture. Sufficient number of eggs were used for each treatment, and all treatments were replicated three times. The eggs were sprayed with the insecticidal solutions using a Potters precision spray tower (Burkard Manufacturing Co Ltd, Rickmansworth, Herts, England) or with distilled water. After the treatment, the Petri dishes were air-dried for 30 min and mortality was recorded 24 h, 48 h, and 72 h later. Eggs that appeared discoloured, shrunk, or deformed (flattened) were considered as dead eggs (Fig. 1). Egg mortality was calculated as before and the values were subjected to angular transformation before statistical analysis.

The analysis was carried out using Mstat (C), SPSS ver. 2.0, and Microsoft Excel, and the standard procedures for agricultural statistics (Gomez and Gomez, 1976) were consulted throughout the experiment.

Baseline toxicity of insecticides to fall armyworm larvae

Although the insecticides varied in their level of toxicity over time – the results 24 h after the treatment are shown in Table 2; after 48 h, in Table 3; and after 72 h, in Table 4 – chlorantraniliprole was the most toxic irrespective of the time elapsed after treatment: its LC₅₀ value was 0.17 ppm after 24 h, 0.14 ppm after 48 h, and 0.08 ppm after 72 h.

All the tested insecticides proved toxic except fipronil and azadirachtin at lower concentrations. Chlorantraniliprole, the most toxic, had a potency ratio of 13.3 followed by emamectin benzoate (potency ratio of 8.75) 72 h after the treatment (Fig.2). The next in order of toxicity were flubendiamide, spinetoram, and Spinosad (Fig. 2). Thiamethoxam 12.5% + lambda cyhalothrin 9.5% showed no particular advantage in terms of toxicity. Chlorantraniliprole belongs to the diamide group, which is the most recent addition to the groups of insecticides and shows specific target-site activity. The members of this group show a favourable toxicological profile and have proved highly effective against a wide spectrum of insect pests. Diamide insecticides are known to bind to ryanodine receptors in muscle cells, which causes the channels to open and release Ca⁺² ions, thereby depleting the level of calcium in the cells; the depletion in turn causes paralysis and, eventually, proves fatal (Cordova et al., 2006). On exposure to insecticides of the diamide group, the insects cease to feed. Flubendiamide, a member of the diamide group, is effective against a majority of lepidopteran pests whereas chlorantraniliprole targets stem borers, leaf folders, the diamond back moth, the cotton boll worm (Helicoverpa armigera), cotton leaf worm (Spodoptera litura), S. frugiperda, and many species of termites in addition to other lepidopterans (Teixeira and Andaloro, 2013). The present findings confirm those of Deshmukh et al. (2020) who evaluated the toxicity of insecticides to 2nd-instar larvae of S. frugiperda using the leaf dip method and observed that emamectin benzoate 5 SG was the most toxic, followed by chlorantraniliprole18.5 SC and spinetoram 11.7 SC. These findings show clearly that S. frugiperda, despite its recent appearance in Karnataka, is susceptible to a range of doses of different compounds. Hardke et al. (2011)also found spinetoram (0.066 µg/mL) and chlorantraniliprole (0.068 µg/mL) to be the most toxic to S. frugiperda when incorporated into its diet. Belay et al. (2012) studied the susceptibility of 3rd-instar larvae of FAW to chlorantraniliprole, flubendiamide, Spinosad, indoxacarb, and fenvalerate, all administered using a small hand sprayer; they reported more than 80% mortality 96 h after the application. Temple et al. (2009) found chlorantraniliprole to be toxic to the bollworm, Helicoverpa zea (Boddie), S. frugiperda, and Heliothis virescens. Sharma and Pathania (2014) reported that 5th-instar larvae of S. litura were highly susceptible to emamectin benzoate and indoxicarb administered as a leaf dip or as a topical application; Su et al. (2012) reported that in China, S.litura was susceptible to chlorantraniliprole 18.5 SC (LC₅₀was 4.20 µg a.i./mL) incorporated into the diet; and Karuppaiah et al. (2017)found that chlorantraniliprole 18.5% SC at doses of 1–4 ppm (LC₅₀) and emamectin benzoate 5% SG at doses of 1–3 ppm (LC₅₀) were the most effective formulations to control field populations of S. litura ²⁹.

The low toxicity of azadirachtin observed in the present study is consistent with the findings of Silva et al. (2015) who evaluated the toxicity of aqueous extracts of neem leaf and neem seed cake to S. frugiperda. However, azadirachtin at10 000 ppm was appreciably toxic in the present study, more so than the untreated control. Because neem acts through multiple pathways, it could still be considered a component of integrated pest management.

Insecticides with hitherto undeployed modes of action are preferred because pest populations are yet to develop resistance to such insecticides; however, they are hard to find. The resistance to synthetic insecticides as demonstrated by FAW is due to their target sites being insensitive as well as due to metabolic resistance (Yu et al., 2003), the latter being the major mechanism of resistance mediated by families of enzymes that can detoxify insecticides. Such families of enzymes include the P450s, cytochromes, glutathione-S-transferases, and carboxylesterases. Metabolic resistance is one of the most common mechanisms of defence in herbivorous insects because they coevolve with plants, the defence by metabolizing using enzymes being a xenobiotic response. These enzymes can sequester or detoxify toxic molecules by interrupting the chain that results in toxicity or by decreasing its harmful effect: the enzymes convert the toxic compounds into non-toxic compounds or into compounds that more easily excreted by the insect (Després et al., 2007). However, such studies that seek to identify the exact mechanism of resistance need baseline data—and the present experiment was meant to obtain such data on the susceptibility to insecticides in current use against FAW and to develop ways to monitor new insecticides as a prelude to developing effective strategies to control pests.

Toxicity of insecticides to eggs

The effect of applying insecticides to the eggs that were 1, 2, or 3 days old was assessed as a function of time, namely 24 h, 48 h, and 72 h after application, and the results are given in Table 5, Table 6, and Table 7, respectively.

Thiodicarb 75 WP (T₁) proved the most toxic to eggs, with 69.2% mortality irrespective of the age of the eggs or of the concentration of the insecticide, whereas azadirachtin at 10 000 ppm was the least toxic. Also, the level of mortality increased with the age of the eggs. The recommended dose led to significantly higher mortality (16.8% on average) than that achieved when the dose was halved (10.3% on average).

The interaction studies between insecticides and their concentrations showed the marked effect of concentration. Thiodicarb, for example, resulted in 82.8% mortality at the recommended concentration; at the half the recommended concentration, the mortality dwindled to 7.8%. A similar marked decrease was seen with other insecticides as well. Azadirachtin, probably because it’s recommended concentration itself was very low (10 000 ppm), showed zero mortality at half of that concentration.

Thiodicarb proved the most potent ovicide among the six insecticides tested. This was expected because thiodicarb belongs to the carbamate group, and the ovicidal actions of its members are well known, especially against several species of Lepidoptera (Samy, 1964). However, fenoxycarb, also a member of the carbamate group, disrupts the embryonic development of FAW eggs by reducing eclosion(Gardner, 1991), which may explain why the ovicidal action of carbamate insecticides against FAW.

Clavijo and Notz (1995) also noted the effectiveness of thiodicarb 75 WP as an ovicide against H. zea and S. frugiperda, as did Natikar and Balikai (2015) who recorded 88.4% egg mortality in S. litura; RajaReddy and Divakar (1998) with chlorpyrifos against the same species; Purnachandra et al. (2000) with thiodicarb against S. litura and S. exigua; and Ahmed et al. (2001) with thiodicarb against S. Litura (95.6% mortality). Gonzales and Allen (1986) also noticed the superiority of thiodicarb as an ovicide against Heliothissp., Spodoptera sp., and Pseudoplasia includes, as did Mala et al. (1991) and Barbar et al. (2012) against H. armigera. Meantime, Thiodicarb and profenphos have also proved to be better insecticides to manage pink bollowrms of cotton.

Pampapathy (1998) recorded 88.4% egg mortality in H. armigera following thiodicarb application, and Abou-Taleb (2010) working on S.littoralis, and Singh et al. (1982), Ahmed et al. (1990), Mala et al. (1991), and Ramesh and Khan (1996) working on H. armigera also reported methomyl as an ovicide. Both methomyl and thiodicarb belong to the carbamate group and their ovicidal action on different species of Lepidoptera is well documented, findings that are consistent with the ovicidal action of thiodicarb on FAW observed in the present experiment.

However, Zidan et al. (1987) found thiodicarb to be less toxic to S. littoralis and Sharma et al. (1996) and Pachori and Sharma (1996) found methomyl less toxic than profenophos: it is possible that the susceptibility of eggs to an insecticide changes during embryonic development; that and the difference between species can together account for the discrepancy between the findings.

In the present experiment, spinetoram was the next best insecticide (Fig.3). Hassan (2009), recorded the lowest LC₅₀ value of 1.14 ±1.14% on 3-day-old eggs of S. littoralis treated with spinetoram, which is consistent with the present findings, whereas in another study (Abou-Taleb, 2010) both spinetoram and methomyl showed only low ovicidal activity against S.littoralis: the ovicidal action of spinoteram and its mechanism are yet to be elucidated, but it may be toxic to larvae and eggs.

The age of S. frugiperda eggs influenced their susceptibility to all the insecticides tested, because it may have changed during embryonic development. The effect (susceptibility) also depends on the insecticide and the insect species (Salkeld and Potter, 1953). In the present investigation, the susceptibility was directly proportional to the age of the egg (Fig. 2). The permeability of eggs, the number of layers, and their chemical and physical properties are important variables that govern the efficacy of an ovicide, and these variables may vary with the species of insects.

Hassan (2009), also reported that older eggs of S. liturawere more susceptible to indoxicarb and spinetoram: the lethal effect was attributed to the chemicals being absorbed into the chorion and its subsequent oral uptake as the neonate larvae feed through the chorion in the process of hatching. These results explain the efficacy of thiodicarb and spinetoram against 3-day-old eggs observed in the present experiment. Saleh et al. (2015) also found that emamectin benzoate more toxic to older eggs of S. litura, and Armer et al. (2012) observed a similar result with emamectin benzoate and pyridaly tested against the pink bollworm (Pectinophora gossypiella). Zidan et al. (1987) also noted that older eggs of S.littoralis were more susceptible than younger ones and Pachori and Sharma (1996) observed that hatching in 2- and 3-day-old eggs was inhibited more than that in 1- or 2-day-old eggs. However, Gardner (1991) obtained the opposite results with fenoxycarb against S. frugiperda: the percentage of eclosion was the lowest in 1-day-old eggs than that in 2- or 3-day-old eggs. Yet again, the contradictory results might be due to the difference in the insecticides and their target. The mechanism of the ovicidal action of thiodicarb against S. frugiperda is yet to be elucidated, and its susceptibility may differ with the age of eggs and with the insecticides.

In general, in the present experiment, egg mortality increased as the concentration of the insecticide increased. These observations are consistent with those made by Tysowsky and Gallo (1977), who tested permethrin (Ambush) against S. frugiperda and observed that lowest percentage hatchability in lower concentrations and reciprocal at high concentration. They suggest that egg masses of S. frugiperda are covered with scales: at lower concentrations, not enough of the active ingredient reaches the surface of eggs, making it less effective. Many other researchers (Haragreaves and Cooper, (1984); Sharma et al. (1996); Ramesh and Khan, (1996); Pachori and Sharma, (1996); and Pampapathy, (1998)) have also noted the marked ovicidal action at higher doses of different insecticides on the eggs of H. armigera.

Differences in the target – larvae or eggs – are crucial to devising effective strategies for controlling insect pests. Of the six insecticides tested against fall armyworm, thiodicarb was the most toxic to eggs, followed by spinetoram. Mortality was the highest in 3-day-old eggs, higher than that recorded in 1- or 2-day-old eggs and higher at the recommended doses than at half the recommended doses. Chlorantraniliprole was the most toxic to the larvae, followed, in that order, by emamectin benzoate, flubendiamide, spinetoram, Spinosad, and azadirachtin. Pesticides can be used even more effectively if the mechanism of action of the newer insecticides is elucidated.

Acknowledgement: Masedi O. Race acknowledge Government of India, ICAR New Delhi and Botswana for offering Indo Africa fellowship.

Authors’ Contributions

Masedi O. Race, executed the research and wrote the manuscript, Guruprasad G.S. and Udikeri S.S., conceived the idea and supervised the work revised and reviewed the manuscript.

Funding

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Availability of data and materials

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding authors.

Ethics approval and consent to participate

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Competing interests

The authors declare that they have no competing interests.

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Baseline toxicity and ovicidal action of different insecticides on new invasive insect pest into India: Fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae)

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Abstract

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Introduction

Materials and methods

Preparation of insecticidal solutions:

Bioassay for larvicidal action:

Bioassay for ovicidal action

Results and discussion

Conclusion

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References

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