Potential of adjuvants and an entomopathogenic fungus for the management of Helicoverpa armigeraAbstract
Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) is a polyphagous species that feeds on crops of high economic importance in Brazil. Biological control, a component of Integrated Pest Management (IPM), employs parasitoids, predators, and entomopathogenic fungi to control agricultural pests as a strategy to reduce insecticide use and promote more sustainable practices. Adjuvants and activators, including vegetable oils, mineral oils, and fusel oil, can enhance the efficacy and toxicity of bioinsecticides. Thus, the objective of this study was to evaluate the effects of different adjuvants and the entomopathogenic fungus Metarhizium rileyi on Helicoverpa armigera larvae. The treatments consisted of sterile distilled water, fusel oil, and commercial adjuvants (Aureo®, Nimbus®, and Protac®) at different concentrations, in addition to the application of M. rileyi (1×109 conidia mL-1). Two milliliters of each treatment was applied to each replicate using a Potter spray tower. Cumulative daily mortality percentage and efficacy were calculated using Abbott's formula. All data were subjected to analysis of variance (F-test), and the means were compared using the Scott–Knott test at a 5% significance level. The adjuvants Nimbus® and Aureo® at all tested concentrations, and fusel oil at 1.5%, resulted in larval mortality rates exceeding 80% by day 6 post-application. Regarding efficacy, except for fusel oil at the lowest concentration, the other treatments showed values above 80%. Therefore, efficacy was considered more relevant than cumulative mortality, as it accounts for mortality and more accurately reflects treatment effectiveness.
Keywords:
defoliators; Noctuidae; biological control; chemical control
Resumo
Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) é uma espécie polífaga que se alimenta de culturas de grande importância econômica no Brasil. O controle biológico, componente do Manejo Integrado de Pragas (MIP), utiliza parasitoides, predadores e fungos entomopatogênicos no controle de pragas agrícolas, configurando uma estratégia para reduzir o uso de inseticidas e promover práticas mais sustentáveis. Adjuvantes e ativadores, incluindo óleos vegetais, minerais e óleo fusel, podem potencializar a eficiência e a toxicidade de bioinseticidas. Assim, o objetivo deste estudo foi avaliar os efeitos de diferentes adjuvantes e do fungo entomopatogênico Metarhizium rileyi sobre lagartas de H. armigera. Os tratamentos foram compostos por água destilada esterilizada, óleo fusel e adjuvantes comerciais (Aureo®, Nimbus® e Protac®) em diferentes concentrações, além da aplicação de M. rileyi (1×109 conídios mL−1). Dois mililitros de cada tratamento foram aplicados por repetição com o auxílio de uma torre de Potter. As porcentagens de mortalidade diária acumulada e de eficiência foram calculadas pela fórmula de Abbott. Todos os dados foram submetidos à análise de variância (teste F), e as médias comparadas pelo teste de Scott-Knott a 5% de probabilidade. Os adjuvantes Nimbus® e Aureo®, em todas as concentrações testadas, e o óleo fusel (1,5%) proporcionaram mortalidade superior a 80% das lagartas seis dias após a aplicação. Em relação à eficiência, exceto o óleo fusel na menor concentração, os demais tratamentos apresentaram valores acima de 80%. Portanto, a eficiência foi considerada mais relevante que a mortalidade acumulada, pois desconta a mortalidade da testemunha e reflete com maior precisão a efetividade dos tratamentos.
Palavras-chave:
lagarta desfolhadora; Noctuidae; controle biológico; controle químico
1. Introduction
Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) is a polyphagous species that feeds on cultivated and wild plants across multiple botanical families of major economic importance, including Asteraceae, Fabaceae, Malvaceae, Poaceae, and Solanaceae (Pogue, 2004; Perini et al., 2016; Pinto et al., 2017; Dourado et al., 2021).
In Brazil, H. armigera was classified as a quarantine pest until 2013, when its presence was first reported in crops in the states of Goiás, Mato Grosso, and Bahia, leading to increased insecticide use for its control in subsequent years and the reestablishment of H. armigera populations in agricultural systems (Specht et al., 2021). H. armigera is likely distributed throughout Brazil due to its high dispersal capacity, which allows it to travel up to 1,000 km in flight, and its adaptability to adverse environmental conditions (Silva et al., 2020).
Integrated Pest Management (IPM) combines control strategies to improve the effectiveness of agricultural technologies while promoting environmental sustainability and reducing costs (Oliveira et al., 2022; Bueno et al., 2025). In this context, biological control is a key component of IPM programs, employing parasitoids, predators, and entomopathogenic microorganisms to manage agricultural pests, thereby reducing insecticide application costs and supporting sustainable profitable production (Fontes et al., 2020; Parra, 2023).
Microbial control agents include entomopathogenic fungi, which exhibit high genetic variability, the ability to infect hosts at different developmental stages, penetration through the integument, and production of propagules with high dispersal capacity (Loeblein et al., 2022). Metarhizium rileyi (Farlow) Samson is an entomopathogenic fungus recognized as a natural control agent of lepidopteran pests in several economically important crops (Loureiro et al., 2020; Montecalvo and Navasero, 2024). The first record of an epizootic caused by M. rileyi on H. armigera populations in Brazil occurred in cotton crops in 2015 (Costa et al., 2015).
Adjuvants are substances added to agrochemical formulations to improve the solubilization and dispersion of active ingredients, improving deposition, adhesion, and retention of the spray solution, thereby potentially intensifying the efficacy of bioinsecticides and pesticides against target organisms (Costa et al., 2003; Reinbacher et al., 2023; Loureiro et al., 2025). Activators formulated with vegetable or mineral oils are primarily used to enhance the biological activity of agrochemicals and bioinsecticides, increasing absorption rates and improving efficacy (Buteler and Stadler, 2011). Mineral oils are widely used to control pests such as mites, scale insects, leaf-mining larvae, and psyllids (Raypuriya et al., 2019; Conceschi et al., 2024). Fusel oil is a byproduct of ethanol distillation that contains higher alcohols such as isoamyl alcohol, which is harmful to human health and potentially toxic to insects (Massa et al., 2023).
Recent studies have demonstrated the feasibility of combining entomopathogenic fungi with oils, both as adjuvants in formulations (Cowles et al., 2000; Loeblein et al., 2022) and as synergists in pest management (Arnosti et al., 2019; Raypuriya et al., 2019). However, there remains a gap in research evaluating the effects of these products on entomopathogenic fungi. Most studies focused on oils as adjuvants in entomopathogen formulations rather than as adjuvants in spray solutions. In this context, the objective of this study was to evaluate the effects of different adjuvants and the entomopathogenic fungus Metarhizium rileyi on Helicoverpa armigera larvae to support the development of more sustainable pest management strategies.
2. Material and Methods
2.1. Acquisition of adjuvants and entomopathogenic fungus
The adjuvants used were commercial formulations, and fusel oil was obtained from sugarcane mill byproducts provided by IACO Agrícola S/A. Spray solutions of the adjuvants were prepared at concentrations of 0.5%, 1.0%, and 1.5%. The concentrations used for the adjuvants were based on the methodology described for fusel oil as an herbicide (Azania et al., 2010). The concentration of the mineral oil–based adjuvant followed that used for insect control (Raypuriya et al., 2019). As the M. rileyi isolate UFMS 03 has no commercial formulation, this entomopathogen was produced in the laboratory (Loureiro et al., 2019).
2.2. Mass rearing of Helicoverpa armigera
The rearing was initiated with larvae and eggs of H. armigera at different developmental stages, along with egg masses collected from a soybean field at the Experimental Campus of the Federal University of Mato Grosso do Sul, Chapadão do Sul, MS, Brazil (18°47'39"S, 52°37'22"W; 800 m altitude), where no chemical pesticides had been applied.
Additional insect collections were performed in the same area at different times and incorporated into the colony to maintain vigor and increase the genetic variability of the population. In the laboratory, the insects were maintained at a temperature of 25 ± 1 °C, 70% ± 10% relative humidity, and a 12-hour photoperiod in a controlled environment room.
Insects were reared and fed on a modified artificial diet based on white beans. After pupation, pupae were separated by sex, and following adult emergence, eight pairs were placed in each rearing unit. Adults were fed a diet consisting of two parts brewer's yeast and one part honey, which was heated and applied to the adult feeder. Rearing units were constructed from PVC tubes (23 cm in height, 10 cm in diameter), internally lined with white sulfite paper as an oviposition substrate, sealed at the upper end with voile fabric, and supported at the lower end by an expanded polystyrene base lined with paper towel (Ribeiro, 2017).
Egg masses were removed from the rearing units and stored in plastic containers. Following hatching, larvae were individually placed in Petri dishes and fed the artificial diet until they reached 1-7 mm in length.
2.3. Application of adjuvants and Metarhizium rileyi on larvae
The bioassay was conducted using larvae measuring 1–7 mm in length, individually placed in Petri dishes and fed an artificial diet.
The fungal suspension was prepared using sterilized distilled water with 0.01% (v/v) Tween 80®, to which conidia of M. rileyi (isolate UFMS 03) were added and standardized to a concentration of 1×109 conidia mL−1 using a Neubauer chamber. A volume of 2 mL of each adjuvant and fungal suspension was applied per replicate using a Potter spray tower at a pressure of 15 psi. After application, Petri dishes were sealed, wrapped with PVC film, and maintained in a climate-controlled room under a 12-hour photoperiod, at 25 ± 1 °C, and 70% ± 10% relative humidity.
The bioassay comprised fourteen treatments with 50 replicates each, totaling 700 larvae, arranged in a completely randomized experimental design. The treatments were as follows: T1 – sterilized distilled water; T2 – fusel oil (0.5%); T3 – fusel oil (1.0%); T4 – fusel oil (1.5%); T5 – Protac® (0.5%); T6 – Protac® (1.0%); T7 – Protac® (1.5%); T8 – Nimbus® (0.5%); T9 – Nimbus® (1.0%); T10 – Nimbus® (1.5%); T11 – Aureo® (0.5%); T12 – Aureo® (1.0%); T13 – Aureo® (1.5%); and T14 – M. rileyi (1 × 109 conidia mL−1), as summarized in Table 1. Adjuvant concentrations were applied according to the manufacturers' recommendation (AGROFIT, 2025).
Mortality was assessed every 24 hours up to 12 days after application. Insects treated with the entomopathogenic fungus that succumbed were individually transferred to 1.5 mL Eppendorf® microtubes sealed with hydrophilic cotton lightly moistened with sterilized distilled water to confirm mortality. The microtubes were maintained under a 12-hour photoperiod, at 25 ± 1 °C and 70 ± 10% relative humidity, to allow fungal growth and confirm insect mortality, following the methodology of Loureiro et al. (2024).
Cumulative daily mortality percentage and treatment efficacy were evaluated on days 6 and 12 post-application using Abbott's formula (Abbott, 1925). Data were subjected to analysis of variance (ANOVA; F-test), and means were compared using the Scott–Knott test at a 5% significance level.
3. Results
The treatment containing Metarhizium rileyi achieved 100% control efficacy against Helicoverpa armigera larvae (Table 2). The obtained data indicated that treatments with commercial adjuvants at the highest concentration (1.5%) exhibited the greatest control of H. armigera (Table 2). However, there was no significant difference among treatments, except for fusel oil at 0.5%.
Efficiency (EP) (%) six and twelve days after application of different treatments in Helicoverpa armigera caterpillars (25 ± 1 °C, 12h photoperiod and 70 ± 10% RH) (n = 50 caterpillars).
When analyzing each treatment individually, fusel oil exhibited the greatest variation in efficacy between days 6 and 12 (Table 2). In the treatment with fusel oil (0.5%), larvae developed to the pupal stage but died due to fissures and deformations induced by the treatment (Figure 1). In treatments that allowed pupal formation, some pupae failed to fully close their integument, resulting in hemolymph leakage, while others retained integument integrity but exhibited blister-like deformations (Figure 1).
Deformity in Helicoverpa armigera pupae after application of Fusel oil (0.5%). The red circles highlight the damage caused to the organism.
When assessing cumulative daily mortality, the M. rileyi treatment resulted in the highest mortality (24%) on the first day after application, reaching 100% by day 6 (Figure 2). Among the adjuvants tested, Nimbus® at 1.5% concentration resulted in the highest mortality on the first day after application (Figure 2). The adjuvants Nimbus® and Aureo® at all tested concentrations, and fusel oil at 1.5%, achieved larval mortality rates exceeding 80% by day 6 post-application (Figure 2), indicating insecticidal activity likely associated with oil content in their formulations (Loureiro et al., 2025).
Daily cumulative mortality (%) of Helicoverpa armigera subjected to different treatments (25 ± 1°C, 12h photoperiod and 70 ± 10% RH).
4. Discussion
The authors Loureiro et al. (2020) evaluated different strains of M. rileyi applied to H. armigera larvae and observed no significant mortality during the exposure period but reported a significant reduction in oviposition across all treatments compared to the control. Additionally, Faria et al. (2021) reported high virulence of M. rileyi (isolate CG381) against Spodoptera frugiperda under laboratory and greenhouse conditions, with mortalities exceeding 95%, and up to 59% under field conditions when applied in oily formulations directed to the corn whorl. For a phytosanitary product to be considered economically viable, it must achieve at least 80% efficacy against the pest (Tomquelski and Martins, 2007).
Many phytosanitary products include oils of both vegetable and mineral origin as insecticides, acaricides, fungicides, herbicides, or spreading adjuvants (Grewal and Joshi, 2022). However, some of these products may affect microorganisms such as entomopathogenic fungi, potentially altering vegetative growth, viability, and sporulation, or genetic composition, which can influence their virulence (Loureiro et al., 2023; Loureiro et al., 2025). Adjuvants can enhance the dispersion and solubilization of active ingredients, improving deposition, spreading, wetting, adhesion, and retention of entomopathogenic fungi conidia on the insect or plant surface (Costa et al., 2003).
Adjuvants are widely used to enhance the efficacy of phytosanitary products, reduce evaporation, foaming, volatilization, and spray drift, and improve the performance of application equipment. They also improve the efficacy of the active ingredient and provide properties such as photoprotection, feeding stimulation, and antievaporative effects (Green and Beestman, 2007). Therefore, evaluating the compatibility and performance of entomopathogenic fungi with adjuvants is essential to identify potential interferences and synergistic or additive effects in pest management. Different compounds should be incorporated into the spray solution to ensure adequate suspensibility and dispersion in the spray solution, as well as to enhance deposition, spreading, wetting, adhesion, retention, and efficacy on the target pest (Costa et al., 2003; Loureiro et al., 2023).
In addition to causing the larval mortality, recent studies have shown that M. rileyi can reduce egg production by 100% in the filial generation of H. armigera using isolates UFMS 02 and 03 (Loureiro et al., 2020). The mortality observed in this study can be attributed to the formation of the appressoria by entomopathogenic fungi, which involves hyphal swelling with high enzymatic activity (proteases, chitinases, and lipases), facilitating mechanical penetration of the fungus (Xiong et al., 2013) and potentially influencing the rate of colonization and subsequent insect mortality.
Oily emulsions adhere to the insect cuticle, wings, and other structures, leading to mortality (Baliota and Athanassiou, 2023; Seni, 2023). Oily substances can induce insect mortality through anoxia by obstructing spiracles and may also act as fumigants, causing nervous system impairment, narcosis, corrosion, cell rupture, and desiccation (Leong et al., 2012).
Therefore, additional studies on the use of adjuvants as insecticidal agents are essential to advance knowledge in integrated pest management, particularly given the importance of H. armigera as a pest that causes substantial agricultural losses and limited efficacy of currently registered chemical products for its control. The technological innovation of this study contributes to the social, environmental, and economic dimensions of the food production chain, aligning with the United Nations Sustainable Development Goals (SDGs).
5. Conclusions
Based on the data obtained in this study, the entomopathogenic fungus Metarhizium rileyi achieved 100% efficacy in controlling Helicoverpa armigera larvae. Mortality in the M. rileyi (isolate UFMS 03) treatment was confirmed by conidiogenesis on all dead larvae. The adjuvants Nimbus ® and Aureo® at all tested concentrations, and fusel oil at 1.5%, achieved larval mortality rates exceeding 80% by day 6 post-application. In terms of efficacy, all treatments, except for fusel oil at the lowest concentration, achieved rates above 80%. These results contribute to the United Nations Sustainable Development Goals (SDGs), particularly SDG 2 (Zero Hunger), SDG 3 (Good Health and Well-Being), SDG 12 (Responsible Consumption and Production), and SDG 13 (Climate Action), by promoting resilient and environmentally sustainable agricultural practices.
Acknowledgments
The authors would like to thank the National Council for Scientific and Technological Development (CNPq); the Universidade Federal de Mato Grosso do Sul (UFMS) in Chapadão do Sul, MS, Brazil; the Universidade Federal da Grande Dourados in Dourados, MS, Brazil, and the members of the LAMIP Research Group.
This study was financed in part by the Brazilian Coordination for the Improvement of Higher Education Personnel - Brazil (CAPES) - Finance Code 001, the Women in Science Program of the Federal University of Mato Grosso do Sul (UFMS); the Foundation for Support of Education, Science, and Technology Development of the State of Mato Grosso do Sul (FUNDECT), project funding agency (number 224/2022, 71/027.188/2022 and SIAFEM number 31970) and for granting a master's scholarship (number 90/2024, 83//003.581/2024).
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Data Availability Statement
The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.
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Edited by
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Editor:
Takako Matsumura Tundisi
The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.
