Virulence of entomopathogenic fungi in larvae of Lepidoptera: Noctuidae

Loureiro, Elisângela de S.; Dias, Pamella M.; Pessoa, Luis G. A.; Amaral, Tatiana S. do; Pessoa, Marcelo B.; Gregori, Gabriella S. de; Rodrigues, Andressa S.; Godoy, Maurício S. de

doi:10.1590/1983-21252024v3712375rc

Brasil

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Scientific Article • Rev. Caatinga 37 • 2024 • https://doi.org/10.1590/1983-21252024v3712375rc linkcopy

Virulence of entomopathogenic fungi in larvae of Lepidoptera: Noctuidae

Virulência de fungos entomopatogênicos sobre larvas de Lepidoptera: Noctuidae

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Currently, agricultural cropping systems have adopted integrated pest management (IPM) as a successful model for pest control. The use of entomopathogenic fungi in IPM has increased because of their great potential for reducing arthropod pest populations without causing harm to human health and ecosystems. Beauveria bassiana and Metarhizium anisopliae stand out among the most used fungi in biological control, with many isolates commercialized worldwide. Helicoverpa armigera is an agriculturally important pest in Brazil and worldwide, causing damage to several crops. In this context, the objective of this study was to evaluate the biological control potential of Beauveria bassiana, Metarhizium anisopliae, and M. rileyi on H. armigera. The results indicated that the entomopathogenic fungi B. bassiana (strain ESALQ PL63), M. anisopliae (strain ESALQ E9), and M. rileyi (strain UFMS 03), applied using different methods (direct application and dry film) and concentrations (1 × 10⁷, 1 × 10⁸, and 1 × 10⁹ conidia mL^-1), resulted in low mortality and no virulence in first-, third-, and fifth-instar larvae of H. armigera. The death of all individuals subjected to treatment with B. bassiana (strain ESALQ PL63) was confirmed by conidiogenesis. Considering the importance of H. armigera as an agricultural pest and the biodiversity of entomopathogenic fungi in Brazil, further investigations on the virulence of fungal strains are necessary to improve the integrated management of lepidopteran pests through microbial control, explore the potential of new strains, and understand the relationships between microorganisms and host defense mechanisms.

Keywords Biological control; Beauveria; Metarhizium; Helicoverpa. Pest management.

Source of variation	DF	3 DAA	6 DAA	9 DAA	12 DAA
Product (P)	3	0.50 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.52 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.62 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.75 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
Application method (A)	1	0.89 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.88 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.75 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
Concentration (C)	3	0.95 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.82 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.99 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.98 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
A×P	3	0.88 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.93 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.99 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.94 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
A×C	3	0.99 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.99 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
P×C	9	0.95 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.99 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.99 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.98 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
A×P×C	9	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.99 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
Residue	580	62.36	0.07	0.06	0.06

Product (P)	3 DAA	6 DAA	9 DAA	12 DAA
Control	0.03± 0.03 a	0.03±0.03 a	0.03±0.03 a	0.03±0.03 a
B. bassiana	0.09±0.02 a	0.09±0.02 a	0.08±0.02 a	0.07±0.02 a
M. anisopliae	0.07±0.02 a	0.07±0.01 a	0.06±0.02 a	0.06±0.02 a
M. rileyi	0.08±0.02 a	0.08±0.02 a	0.06±0.02 a	0.07±0.02 a
Application method (A)	3 DAA	6 DAA	9 DAA	12 DAA
Direct	0.08±0.01 a	0.08±0.01 a	0.06±0.01 a	0.07±0.01 a
Dry Film	0.08±0.01 a	0.08±0.01 a	0.07±0.01 a	0.06±0.01 a
Concentration (C)	3 DAA	6 DAA	9 DAA	12 DAA
10⁷ conidia mL^-1	0.09±0.02 a	0.08±0.02 a	0.07±0.02 a	0.06±0.02 a
10⁸ conidia mL^-1	0.09±0.02 a	0.07±0.02 a	0.06±0.02 a	0.06±0.02 a
10⁹ conidia mL^-1	0.08±0.02 a	0.10±0.02 a	0.07±0.02 a	0.07±0.02 a

Source of variation	DF	3 DAA	6 DAA	9 DAA	12 DAA
Product (P)	3	0.43 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.50 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.62 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.70 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
Application method (A)	1	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.87 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
Concentration (C)	3	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.97 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.98 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.94 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
P×A	3	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.98 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.98 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
P×C	9	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
A×C	3	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
P×A×C	9	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
Residue	580	0.08	0.07	0.06	0.06

Product (P)	3 DAA	6 DAA	9 DAA	12 DAA
Control	0.03±0.00 a	0.03±0.00 a	0.03±0.00 a	0.03±0.00 a
B. bassiana	0.10±0.00 a	0.09±0.00 a	0.08±0.00 a	0.07±0.00 a
M. anisopliae	0.10±0.00 a	0.07±0.00 a	0.06±0.00 a	0.07±0.00 a
M. rileyi	0.10±0. 00 a	0.08±0.00 a	0.06±0.00 a	0.07±0. 00 a
Application method (A)	3 DAA	6 DAA	9 DAA	12 DAA
Direct	0.09±0.00 a	0.08±0.00 a	0.06±0.00 a	0.07±0.00 a
Dry film	0.09±0. 00 a	0.08±0.00 a	0.07±0.00 a	0.07±0. 00 a
Concentration (C)	3 DAA	6 DAA	9 DAA	12 DAA
10⁷ conidia mL^-1	0.10±0.00 a	0.08±0.00 a	0.03±0.00 a	0.07±0.00 a
10⁸ conidia mL^-1	0.10±0.00 a	0.08±0.00 a	0.07±0.00 a	0.06±0.00 a
10⁹ conidia mL^-1	0.10±0.00 a	0.09±0.00 a	0.06±0.00 a	0.08±0.00 a

Source of variation	DF	3 DAA	6 DAA	9 DAA	12 DAA
Products (P)	3	0.54 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.23 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.27 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.35 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
Application method (A)	1	0.63 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.76 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.76 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.87 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
Concentration (C)	3	0.94 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.80 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.89 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.93 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
P×A	3	0.98 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.88 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.94 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.85 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
P×C	9	0.99 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.99 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.99 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
A×C	3	0.98 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	0.95 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
P×A×C	9	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.	1.00 ^ns ns Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.
Residue	580	0.06	0.07	0.07	0.06

Product (P)	3 DAA	6 DAA	9 DAA	12 DAA
Control	0.03±0.00 a	0.03±0.00 a	0.03±0.00 a	0.03±0.00 a
B. bassiana	0.08±0.00 a	0.10±0.00 a	0.10±0.00 a	0.09±0.00 a
M. anisopliae	0.07±0.00 a	0.08±0.00 a	0.07±0.00 a	0.05±0.00 a
M. rileyi	0.06±0. 00 a	0.06±0.00 a	0.06±0.00 a	0.07±0.00 a
Application method (A)	3 DAA	6 DAA	9 DAA	12 DAA
Direct	0.07±0.00 a	0.08±0.00 a	0.08±0.00 a	0.06±0.00 a
Dry film	0.06±0.00 a	0.07±0.00 a	0.07±0.00 a	0.07±0.00 a
Concentration (C)	3 DAA	6 DAA	9 DAA	12 DAA
10⁷ conidia mL^-1	0.08±0.00 a	0.06±0.00 a	0.07±0.00 a	0.07±0.00 a
10⁸ conidia mL^-1	0.08±0.00 a	0.09±0.00 a	0.09±0.00 a	0.08±0.00 a
10⁹ conidia mL^-1	0.07±0.00 a	0.08±0.00 a	0.08±0.00 a	0.06±0.00 a

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[TFN1] ^*
Significant at a 5% level by the F test;

[TFN2] ^ns
Not significant. DF = degrees of freedom. Bioassay conducted under laboratory conditions: air temperature of 25±1 °C, relative air humidity of 70±10%, and 12-hour photoperiod.