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Entomopathogenic fungi disrupt the feeding behavior of Euschistus heros in soybean

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Abstract

This study evaluated the effects of the entomopathogenic fungi on the feeding behavior of the Neotropical brown stink bug, Euschistus heros, using electropenetrography (AC-DC) technology. Twenty females per treatment were reared under controlled conditions and exposed to soybean pods treated with fungal suspensions (2 µL on the pronotum with 5 × 106 and 6.15 × 108 conidia mL− 1 for Cordyceps javanica and Metarhizium anisopliae, respectively), chemical insecticide (Thiamethoxam + Lambda-cyhalothrin, 0.025/100 mL), and aqueous solution of Polysorbate 80 (0.01% v/v) (control). Response variables associated with count and duration of feeding behavior over 72 h of recording were modelled using GAMLSS (generalized additive models for location, scale, and shape) to assess the statistical significance of treatments and for pairwise comparisons of means (p < 0.05). The fungal treatments and chemical insecticide significantly reduced the frequency and duration of feeding events, especially stylet penetration and seed ingestion, compared to untreated controls. Additionally, insects treated with fungi spent more time in non-feeding behavior, indicating disrupted feeding behavior. Both fungi also shortened the duration of the final feeding probe by about 13 h. Furthermore, electropenetrography enables assessment of pest–plant interactions and biocontrol efficacy beyond mortality.

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Data availability

The raw datasets generated during the current study are available in the Zenodo repository at: [https://doi.org/10.5281/zenodo.16572536](https:/doi.org/10.5281/zenodo.16572536).

References

  1. Sosa-Gómez, D. R. et al. Prevalence, damage, management and insecticide resistance of stink bug populations (Hemiptera: Pentatomidae) in commodity crops. Agric. Entomol. 22, 99–118 (2020).

    Google Scholar 

  2. Lucini, T. & Panizzi, A. R. Electropenetrography (EPG): a breakthrough tool unveiling stink bug (Pentatomidae) feeding on plants. Neotropic Entomol. 47, 6–18 (2018).

    Google Scholar 

  3. Hickmann, F., Cordeiro, E. M. G., Aurelio, M. S. L., Saldanha, A. V. & Corrêa, A. S. Host preference and survivorship of Euschistus Heros strains on cotton and soybean. Entomol. Exp. Appl. 171, 564–571 (2023).

    Google Scholar 

  4. Moscardi, F. et al. Soja Manejo Integrado De Insetos E Outros Artrópodes-praga in 213–334 (Embrapa Soja, 2012).

  5. Silva, R. A. et al. Temporal variation and Spatial distribution of Euschistus Heros (Hemiptera: Pentatomidae) during the soybean grain formation period. Res. Soc. Dev. 11, e6411931102 (2022).

    Google Scholar 

  6. Tessmer, M. A. et al. Histology of damage caused by Euschistus Heros (F.) nymphs in soybean pods and seeds. Neotrop. Entomol. 51, 112–121 (2022).

    Google Scholar 

  7. Ecco, M. et al. Stink bug control at different stages of soybean development. Arq. Inst. Biol. 87, e1132018 (2020).

    Google Scholar 

  8. Woodcock, B. A. et al. Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356, 1393–1395 (2017).

    Google Scholar 

  9. Tibola, C. M., Silva, L., Sgubin, F. & Omoto, C. Monitoring resistance of Euschistus Heros (Fabricius) (Hemiptera: Pentatomidae) to insecticides by using encapsulated artificial diet bioassay. Insects 12, 559 (2021).

    Google Scholar 

  10. van Lenteren, J. C., Bolckmans, K., Köhl, J., Ravensberg, W. J. & Urbaneja, A. Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63, 39–59 (2018).

    Google Scholar 

  11. Gielen, R., Meister, H., Tammaru, T. & Põldmaa, K. Fungi recorded on folivorous lepidoptera: high diversity despite moderate prevalence. J. Fungi. 7, 25 (2021).

    Google Scholar 

  12. Alfina, T. & Haneda, N. F. Entomopathogenic fungi as biological agents in forest plant pest control: A systematic review. IOP Conf. Ser. Earth Environ. Sci. 959 https://doi.org/10.1088/1755-1315/959/1/012013 (2022).

  13. Jiang, W. et al. Effects of the entomopathogenic fungus Metarhizium anisopliae on the mortality and immune response of Locusta migratoria. Insects 11, 36 (2020).

    Google Scholar 

  14. Resquín-Romero, G. et al. Virulence of Metarhizium brunneum (Ascomycota: Hypocreales) strains against stink Bugs Euschistus Heros and Dichelops furcatus (Hemiptera: Pentatomidae). J. Econ. Entomol. 113, 2540–2545 (2020).

    Google Scholar 

  15. Walker, G. P., Fereres, A. & Tjallingii, W. F. Guidelines for conducting, analyzing, and interpreting electrical penetration graph (EPG) experiments on herbivorous piercing–sucking insects. Entomol. Exp. Appl. 172, 564–580 (2024).

    Google Scholar 

  16. Backus, E. A., Cervantes, F. A., Guedes, R. N. C., Li, A. Y. & Wayadande, A. C. AC–DC electropenetrography for in-depth studies of feeding and oviposition behaviors. Ann. Entomol. Soc. Am. 112, 236–248 (2019).

    Google Scholar 

  17. Coutinho, W. B. G., Silva, F. C., Barrigossi, J. A. F., Almeida, A. C. S. & Jesus, F. G. Silicon applications in rice plants alter the stylet probing behaviors of Glyphepomis spinosa (Hemiptera: Pentatomidae). J. Insect Sci. 24, 23 (2024).

    Google Scholar 

  18. de Almeida, A. C. Can Metarhizium anisopliae reduce the feeding of the Neotropical brown stink bug, Euschistus Heros (Fabricius, 1798), and its damage to soybean seeds? J. Fungi. 11, 247 (2025).

    Google Scholar 

  19. Maluta, N., Castro, T. & Spotti Lopes, J. R. DC-electrical penetration graph waveforms for Dalbulus Maidis (Hemiptera: Cicadellidae) and the effects of entomopathogenic fungi on its probing behavior. Sci. Rep. 13, 22033 (2023).

    Google Scholar 

  20. Ministério da Agricultura e Pecuária (MAPA). AGROFIT — Sistema de Agrotóxicos Fitossanitários. Ministério da Agricultura e Pecuária (2025). https://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons

  21. Lucini, T. & Panizzi, A. R. Waveform characterization of the soybean stem feeder Edessa meditabunda: overcoming the challenge of wiring pentatomids for EPG. Entomol. Exp. Appl. 158, 118–132 (2016).

    Google Scholar 

  22. Cervantes, F. A. et al. Correlation of electropenetrography waveforms from Lygus lineolaris (Hemiptera: Miridae) feeding on cotton squares with chemical evidence of inducible tannins. J. Econ. Entomol. 110, 2068–2075 (2017).

    Google Scholar 

  23. Lucini, T. & Panizzi, A. R. Electropenetrography monitoring of the Neotropical brown-stink bug (Hemiptera: Pentatomidae) on soybean pods: an electrical penetration Graph-histology analysis. J. Insect Sci. 18, 5 (2018).

    Google Scholar 

  24. Silva, A. R., Almeida, A. C. S., Jesus, F. G. & Barrigossi, J. A. F. INFEST: an R web application to perform statistical analysis of insect feeding behavior data from EPG systems. J. Econ. Entomol. https://doi.org/10.1093/jee/toaf232 (2025).

    Google Scholar 

  25. Rigby, R. A. & Stasinopoulos, D. M. Generalized additive models for location, scale and shape. Appl. Statist. 54, 507–554 (2005).

    Google Scholar 

  26. Oliveira, G. P. et al. Alternatives for simulating and modeling simplified insect feeding eletropenetrography discrete data. Acta Sci. Agron. 47, e71591 (2025).

  27. Arias-Chavarría, L. D. et al. Evaluation of the viability of microencapsulated Trichoderma longibrachiatum conidia as a strategy to prolong the shelf life of the fungus as a biological control agent. Front. Chem. 15, 12:1473217 (2025).

    Google Scholar 

  28. Barelli, L., Behie, S. W., Hu, S. & Bidochka, M. J. Profiling Destruxin synthesis by specialist and generalist Metarhizium insect pathogens during coculture with plants. Appl. Environ. Microbiol. 88, e0247421 (2022).

    Google Scholar 

  29. Ardia, D. R., Gantz, J. E., Schneider, B. C. & Strebel, S. Costs of immunity in insects: an induced immune response increases metabolic rate and decreases antimicrobial activity. Funct. Ecol. 26, 732–739 (2012).

    Google Scholar 

  30. Gielen, R. et al. Entomopathogenic fungi as mortality agents in insect populations: A review. Ecol. Evolut. 14, e70666 (2024).

    Google Scholar 

  31. Singh, K. S. et al. The genome sequence of the Neotropical brown stink bug, Euschistus Heros provides insights into population structure, demographic history and signatures of adaptation. Insect Biochem. Mol. Biol. 152, 103890 (2023).

    Google Scholar 

  32. Miyashita, A., Lee, T. Y. M., McMillan, L. E., Easy, R. & Adamo, S. A. Immunity for nothing and the eggs for free: apparent lack of both physiological trade-offs and terminal reproductive investment in female crickets (Gryllus texensis). PLoS ONE 14, e0209957 (2019).

  33. Zhang, D., Qi, H. & Zhang, F. Parasitism by entomopathogenic fungi and insect host defense strategies. Microorganisms 13, 283 (2025).

    Google Scholar 

  34. Zambrano, N. D., Arteaga, W., Velasquez, J. & Chirinos, D. T. Side effects of lambda cyhalothrin and Thiamethoxam on insect pests and natural enemies associated with cotton. Sarhad J. Agric. 7, 1098–1106 (2021).

    Google Scholar 

  35. Wu, S., Youngman, R. R., Kok, L. T. & Laub, C. A. Sublethal effect of Beauveria Bassiana and Metarhizium brunneum (Hypocreales: Clavicipitaceae) on Cyclocephala lurida (Coleoptera: Scarabaeidae). J. Entomol. Sci. 51, 43–53 (2016).

    Google Scholar 

  36. Liu, D., Smagghe, G. & Liu, T. X. Interactions between entomopathogenic fungi and insects and prospects with glycans. J. Fungi. 9, 575 (2023).

    Google Scholar 

  37. Sánchez-Pérez, L., de Barranco-Florido, C., Rodríguez-Navarro, J. E. & Cervantes-Mayagoitia, S. Ramos-López, M. Á. Enzymes of entomopathogenic fungi, advances and insights. Adv. Enzyme Res. 2, 65–76 (2014).

    Google Scholar 

  38. Wang, H., Peng, H., Li, W., Cheng, P. & Gong, M. The toxins of Beauveria Bassiana and the strategies to improve their virulence to insects. Front. Microbiol. 12, 705343 (2021).

    Google Scholar 

  39. Qu, S. L., Li, S. S., Li, D. & Zhao, P. J. Metabolites and their bioactivities from the genus Cordyceps. Microorganisms 10, 1489 (2022).

    Google Scholar 

  40. Smid, H. M. & Vet, L. E. M. The complexity of learning, memory and neural processes in an evolutionary ecological context. Curr. Opin. Insect Sci. 15, 61–69 (2016).

    Google Scholar 

  41. Nanzer, S. L. L. et al. Assessment of entomopathogenic nematodes and their symbiotic bacteria to control the stink Bugs Euschistus Heros and Dichelops Melacanthus (Heteroptera: Pentatomidae) in the soybean-corn succession system. Turk. J. Zool. 45, 356–371 (2021).

    Google Scholar 

  42. Battisti, L. et al. Selectivity of Metarhizium anisopliae and Beauveria Bassiana to adults of Telenomus Podisi (Hymenoptera: Scelionidae). Semin Cienc. Agrar. 43, 727–738 (2022).

    Google Scholar 

  43. Bava, R. et al. Entomopathogenic fungi for pests and predators control in beekeeping. Vet. Sci. 9, 95 (2022).

    Google Scholar 

  44. Ebert, T. A., Backus, E. A. & Rogers, M. E. Handling artificially terminated events in electropenetrography data. J. Econ. Entomol. 111, 1987–1990 (2018).

    Google Scholar 

  45. Athanassiou, C. G., Kavallieratos, N. G., Rumbos, C. I. & Kontodimas, D. C. Influence of temperature and relative humidity on the insecticidal efficacy of Metarhizium anisopliae against larvae of Ephestia Kuehniella (Lepidoptera: Pyralidae) on wheat. J. Insect Sci. 17, 22 (2017).

    Google Scholar 

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Acknowledgements

The authors gratefully acknowledge the financial support provided by the National Council for Scientific and Technological Development (CNPq), [grant number: 309733/2021-9] and the Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG), [grant number: 1721]. We also thank the Instituto Federal Goiano and the Center of Excellence in Bioinputs (CEBIO) for their institutional support throughout this study.

Funding

This research was supported by the National Council for Scientific and Technological Development–CNPq [grant number: 309733/2021-9] and the Fundação de Amparo à Pesquisa do Estado de Goiás–Fapeg [grant number: 1721]. The research also received institutional support from Instituto Federal Goiano and the Center of Excellence in Bioinputs (CEBIO).

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Authors and Affiliations

  1. Departamento de Ciências Agrárias, Instituto Federal Goiano – Campus Rio Verde, Rio Verde-GO, Brazil

    Guilherme Pereira de Oliveira, Frederico Antonio Loureiro Soares & Pablo da Costa Gontijo

  2. Departamento de Agronomia, Instituto Federal Goiano – Campus Urutaí, Urutaí-GO, Brazil

    André Cirilo de Sousa Almeida & Kaylaine Aparecida Gomes de Souza

  3. Laboratório de Estatística e Geoprocessamento, Instituto Federal Goiano – Campus Urutaí, Urutaí-GO, Brazil

    Anderson Rodrigo da Silva

Authors

  1. Guilherme Pereira de Oliveira
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  2. Frederico Antonio Loureiro Soares
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  3. André Cirilo de Sousa Almeida
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  4. Kaylaine Aparecida Gomes de Souza
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  5. Pablo da Costa Gontijo
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Contributions

Mr. Guilherme Pereira Oliveira*, ORCID: 0000-0001-7440-6773. Conceptualization; Data curation; Formal analysis; Funding acquisition; Investigation; Methodology; Project administration; Resources; Software; Supervision; Validation; Visualization; Writing – original draft; Writing – review & editing. *Corresponding Author. Professor Frederico Antonio Loureiro Soares, ORCID: 0000-0002-4152-5087. Conceptualization; Formal analysis; Investigation; Methodology; Project administration; Resources; Supervision; Validation; Writing – review & editing. Professor André Cirilo de Sousa Almeida, ORCID: 0000-0001-9786-2990. Conceptualization; Data curation; Formal analysis; Methodology; Resources; Software; Supervision; Validation; Writing – review & editing. Ms. Kaylaine Aparecida Gomes de Souza, ORCID: 0009-0008-6124-4427. Data curation; Formal analysis; Investigation; Methodology; Software; Validation; Visualization. Professor Pablo da Costa Gontijo, ORCID: 0000-0001-8173-0539. Conceptualization; Data curation; Investigation; Methodology; Resources; Software; Writing – review & editing. Professor Anderson Rodrigo da Silva, ORCID: 0000-0003-2518-542X. Conceptualization; Data curation; Formal analysis; Project administration; Resources; Supervision; Writing – review & editing.

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Correspondence to
Guilherme Pereira de Oliveira.

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de Oliveira, G.P., Soares, F.A.L., Sousa Almeida, A.C.d. et al. Entomopathogenic fungi disrupt the feeding behavior of Euschistus heros in soybean.
Sci Rep (2025). https://doi.org/10.1038/s41598-025-31096-w

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  • DOI: https://doi.org/10.1038/s41598-025-31096-w

Keywords

  • Biological control

  • Cordyceps javanica

  • Metarhizium anisopliae
  • Electropenetrography
  • Integrated pest management

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