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Entomopathogenic nematodes as an effective and sustainable alternative to control the fall armyworm in Africa

2024-04-16, Fallet, Patrick, Didace Bazagwira, Livio Ruzzante, Geraldine Ingabire, Sacha Levivier, Bustos Segura, Carlos, Joelle Kajuga, Stefan Toepfer, Turlings, Ted, Joann Whalen

The recent invasion of the fall armyworm (FAW), a voracious pest, into Africa and Asia has resulted in unprecedented increases in insecticide applications, especially in maize cultivation. The health and environmental hazards posed by these chemicals have prompted a call for alternative control practices. Entomopathogenic nematodes are highly lethal to the FAWs, but their application aboveground has been challenging. In this study, we report on season-long field trials with an innocuous biodegradable gel made from carboxymethyl cellulose containing local nematodes that we specifically developed to target the FAW. In several Rwandan maize fields with distinct climatic conditions and natural infestation rates, we compared armyworm presence and damage in control plots and plots that were treated with either our nematode gel formulation, a commercial liquid nematode formulation, or the commonly used contact insecticide cypermethrin. The treatments were applied to the whorl of each plant, which was repeated three to four times, at 2-week intervals, starting when the plants were still seedlings. Although all three treatments reduced leaf damage, only the gel formulation decreased caterpillar infestation by about 50% and yielded an additional ton of maize per hectare compared with untreated plots. Importantly, we believe that the use of nematodes can be cost-effective, since we used nematode doses across the whole season that were at least 3-fold lower than their normal application against belowground pests. The overall results imply that precisely formulated and easy-to-apply nematodes can be a highly effective, affordable, and sustainable alternative to insecticides for FAW control.

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A novel strategy to control the fall armyworm with entomopathogenic nematodes

2023, Fallet, Patrick, Turlings, Ted

La chenille légionnaire d'automne (Spodoptera frugiperda, Smith ; Lepidoptera : Noctuidae) est une espèce d'insecte originaire des Amériques connue pour être un ravageur agricole majeur. Elle peut se nourrir d'une grande variété de plantes, mais elle est particulièrement dévastatrice pour le maïs. L'invasion récente de la chenille légionnaire d'automne en Afrique et en Asie provoque des ravages considérables dans la culture du maïs, entraînant une augmentation importante de l'utilisation d'insecticides synthétiques nocifs, dont l'efficacité est souvent marginale. Cette efficacité limitée est principalement due au comportement alimentaire spécifique de ces chenilles. Elles se trouvent principalement cachées en profondeur dans les feuilles enroulées du maïs, ce qui en fait des cibles difficiles pour les insecticides de contact conventionnels. En outre, la chenille légionnaire d'automne a rapidement développée des résistances à une large gamme d'insecticides synthétiques ainsi qu'à certaines toxines de Bacillus thuringiensis (Bt) couramment utilisées contre les insectes nuisibles dans certaines régions du monde. Des solutions de lutte efficaces, sûres et durables sont primordiales pour garantir la sécurité alimentaire et préserver les organismes bénéfiques, tels que les pollinisateurs, ainsi que l'environnement. Plusieurs agents de contrôle biologique, tels que les nématodes entomopathogènes, peuvent être très efficaces contre des chenilles, mais leur application sur les feuilles des plantes est difficile. Les nématodes entomopathogènes sont des parasites qui ciblent spécifiquement les insectes. Ils peuplent les sols du monde entier et sont couramment utilisés comme agents de lutte biologique depuis des décennies, notamment parce qu'ils ont la capacité de localiser activement, d'infecter et de rapidement tuer des insectes. En tant qu'organismes du sol, les nématodes sont particulièrement sensibles aux conditions abiotiques aériennes, et notamment présentes sur le feuillage, telles que la dessiccation et le rayonnement UV. L'objectif de cette thèse est de relever ces défis en explorant de nouvelles solutions pour appliquer et protéger les nématodes entomopathogènes sur les feuilles de maïs, afin d'assurer un contrôle efficace et durable de la chenille légionnaire d'automne. Nous démontrons dans les chapitres 1 et 2 que des nématodes isolés localement représentent d'excellents candidats contre la chenille légionnaire d'automne. Ils offrent également l'avantage d'éviter le risque d'introduction d'espèces exotiques dans une région cible, associé à l'utilisation de nématodes commerciaux souvent non indigènes. Dans le chapitre 3, nous explorons différentes méthodes de formulation des nématodes pour une application foliaire. Une formulation développée lors ce travail à base de gel de carboxyméthylcellulose s’est avérée très efficace, tuant 100 % des chenilles en laboratoire et réduisant de manière significative l’infestation des plantes lors d'essais préliminaires sur le terrain au Rwanda. Dans le chapitre 4, nous évaluons, au long d'une saison complète de croissance du maïs au Rwanda, l’efficacité de nématodes formulés dans le gel. Les résultats démontrent que, formulés dans le gel, les nématodes ont systématiquement limité les dommages aux plantes. En outre, ce traitement a été nettement plus efficace pour réduire l'infestation des plantes que la cyperméthrine, un insecticide couramment utilisé, et a conduit à une augmentation du rendement par rapport aux plantes contrôles non traitées. Enfin, nous avons démontré au chapitre 5 que l'ajout de substances naturelles et facilement disponibles dans le gel prolongeait la survie et l'efficacité des nématodes exposés aux rayons UV, et ceci à un coût abordable. Cette avancée pourrait se traduire par une efficacité accrue des nématodes dans des conditions agricoles réelles et contribuer à étendre l'utilisation des nématodes contre les ravageurs foliaires. Cette thèse démontre le potentiel des nématodes entomopathogènes natifs, isolés localement, pour lutter contre la chenille légionnaire d'automne et représente une étape vers la gestion durable de ce ravageur dévastateur. ABSTRACT The fall armyworm (Spodoptera frugiperda, Smith; Lepidoptera: Noctuidae) is an insect species native to the Americas known to be a major agricultural pest. It can feed on a large variety of plants, but is particularly devastating to maize. The recent invasion of the fall armyworm in Africa and Asia has wreaked havoc in maize cultivation, leading to a tremendous increase in the use of harmful synthetic insecticides, which are often only marginally effective. This limited efficacy is mainly due to the specific feeding behaviour of the fall armyworm caterpillars, which are mostly found deep within the wrapped leaves of the maize whorl, making them difficult targets for conventional contact insecticides. In addition, the fall armyworm has rapidly developed resistances to a wide range of synthetic insecticides as well as to some Bacillus thuringiensis (Bt) toxins commonly employed against insect pests in some regions of the world. Effective, safe and sustainable control alternatives are desperately needed to ensure food security as well as to preserve beneficial organisms, such as pollinators, and the environment. Several biological control agents, such as entomopathogenic nematodes, can be quite effective in killing armyworms, but their application on plant leaves is challenging. Entomopathogenic nematodes are parasites that specifically target insects. They live in soils around the world and are commonly used as biological control agents for decades, notably because they have the ability to actively locate, infect and swiftly kill insects. As soil organisms, nematodes are particularly sensitive to the abiotic conditions found aboveground and on foliage, such as desiccation and UV radiation. The aim of this thesis is to address these challenges by exploring novel solutions to apply and protect entomopathogenic nematodes on maize leaves to ensure effective as well as sustainable control of the fall armyworm. We showed in Chapters 1 and 2 that locally isolated nematodes represent excellent candidates against the fall armyworm. They also offer the advantage of preventing the risk of introducing foreign species in a target country, associated with the use of often non-native commercially available nematodes. In Chapter 3, we explored different methods to formulate nematodes for aboveground application. We found a here-developed carboxymethyl cellulose gel formulation to be quite effective, killing 100% caterpillars in laboratory conditions and significantly reducing FAW infestations in preliminary field trials in Rwanda. In Chapter 4, we showed that throughout a full maize growing season in Rwanda, nematodes formulated in the gel consistently limited plant damage. In addition, the nematode-gel was significantly more effective than the commonly used insecticide cypermethrin in reducing armyworms infestation. This led to an increased grain yield as compared to untreated control plants. Lastly, we demonstrated in Chapter 5 that the addition of affordable, readily available, natural substances to the gel formulation prolonged the survival and effectiveness of nematodes exposed to UV radiation. This could translate into an increased efficacy of the nematode-gel formulation in realistic farming conditions as well as contribute to expanding the use of nematodes against aboveground pests. This thesis demonstrates the potential of locally isolated entomopathogenic nematodes for fall armyworm control and represents a step towards the sustainable management of this devastating pest.

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Comparative Screening of Mexican, Rwandan and Commercial Entomopathogenic Nematodes to Be Used against Invasive Fall Armyworm, Spodoptera frugiperda

2022-2-16, Fallet, Patrick, De Gianni, Lara, Machado, Ricardo A. R., Bruno, Pamela, Bernal, Julio S., Karangwa, Patrick, Kajuga, Joelle, Waweru, Bancy, Bazagwira, Didace, Degen, Thomas, Toepfer, Stefan, Turlings, Ted

The fall armyworm (FAW), Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) is an important pest of maize originating from the Americas. It recently invaded Africa and Asia, where it causes severe yield losses to maize. To fight this pest, tremendous quantities of synthetic insecticides are being used. As a safe and sustainable alternative, we explore the possibility to control FAW with entomopathogenic nematodes (EPN). We tested in the laboratory whether local EPNs, isolated in the invasive range of FAW, are as effective as EPNs from FAW native range or as commercially available EPNs. This work compared the virulence, killing speed and propagation capability of low doses of forty EPN strains, representing twelve species, after placing them with second-, third- and sixth-instar caterpillars as well as pupae. EPN isolated in the invasive range of FAW (Rwanda) were found to be as effective as commercial and EPNs from the native range of FAW (Mexico) at killing FAW caterpillars. In particular, the Rwandan Steinernema carpocapsae strain RW14-G-R3a-2 caused rapid 100% mortality of second- and third-instar and close to 75% of sixth-instar FAW caterpillars. EPN strains and concentrations used in this study were not effective in killing FAW pupae. Virulence varied greatly among EPN strains, underlining the importance of thorough EPN screenings. These findings will facilitate the development of local EPN-based biological control products for sustainable and environmentally friendly control of FAW in East Africa and beyond.