Efficacy of native entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin (Hypocreales: Cordycipitaceae) against Helicoverpa armigera (Hübner, 1808) (Lepidoptera: Noctuidae)

Year 2024, , 451 - 475, 21.01.2025

Abdurrahman Sami Koca

https://doi.org/10.16970/entoted.1595065

Abstract

Helicoverpa armigera (Hübner, 1808) (Lepidoptera: Noctuidae) is a significant agricultural pest with resistance to conventional synthetic insecticides. The present study, conducted in 2024 at Bolu Abant Izzet Baysal University, Biological Control Laboratory, investigated the pathogenicity of Beauveria bassiana (Balsamo) Vuillemin (Hypocreales: Cordycipitaceae) against six larval stages of H. armigera. Three conidial concentrations (1×10⁶, 1×10⁷, and 1×10⁸ conidia ml⁻¹) were evaluated. This study analyzed the effects of varying spore concentrations of B. bassiana on the mortality of H. armigera larvae, considering days post-application, dose, and larval stage. Lethal concentrations (LC50 and LC90) and lethal time values (LT50 and LT90) were calculated using probit analysis. Mortality increased with dose and was highest in early instars, particularly at 1×10⁸ conidia ml⁻¹, where LT₅₀ and LT₉₀ values for first instars were 4.05 and 8.10 days, respectively. Older instars exhibited lower mortality rates. LC₅₀ and LC₉₀ decreased with increasing concentrations, achieving 100% mortality in the first and second instars across all doses. Third instars displayed dose-dependent mortality, with LC₅₀ and LC₉₀ values of 6.88×10⁸ and 1.94×10⁴ conidia ml⁻¹, respectively. Higher spore concentrations reduced LT₅₀ and LT₉₀, enhancing mortality rates in younger larvae. These findings underscore the efficacy of B. bassiana against early larval stages, emphasizing the importance of application timing for effective biological control and its potential role in integrated pest management strategies.

Keywords

Beauveria bassiana, biological control, biopesticide, entomopathogenic fungus, Helicoverpa armigera

Thanks

The author would like to thank Prof. Dr. Göksel Özer (Bolu Abant Izzet Baysal University, Türkiye) for their help in the identification of the entomopathogenic fungus and prepare fungal suspensions.

Yerel entomopatojen fungus Beauveria bassiana (Balsamo) Vuillemin (Hypocreales: Cordycipitaceae)’nın Helicoverpa armigera (Hübner, 1808) (Lepidoptera: Noctuidae) üzerindeki etkinliği

Abstract

Helicoverpa armigera (Hübner, 1808) (Lepidoptera: Noctuidae), sentetik insektisitlere karşı direnç geliştirmiş önemli bir tarımsal zararlıdır. Bu çalışmada, entomopatojenik fungus Beauveria bassiana (Balsamo) Vuillemin (Hypocreales: Cordycipitaceae)’ın H. armigera’nın altı larva dönemine karşı etkinliği 2024 yılında Bolu Abant Izzet Baysal Üniversitesi, Biyolojik Mücadele Laboratuvarı’nda incelenmiştir. Üç farklı konidiyal konsantrasyon (1×106, 1×10⁷ ve 1×10⁸ konidi ml⁻¹) kullanılarak ölüm oranları değerlendirilmiştir. Uygulama sonrası günler, doz ve larva dönemleri göz önünde bulundurularak, B. bassiana’nın farklı spor konsantrasyonlarının etkileri analiz edilmiştir. Probit analizi ile öldürücü konsantrasyonlar (LC₅₀ ve LC₉₀) ve öldürücü zaman değerleri (LT₅₀ ve LT₉₀) hesaplanmıştır. Ölüm oranlarının, artan dozlarla yükseldiği ve özellikle genç larva dönemlerinde belirgin olup, özellikle birinci larva döneminde 1×10⁸ konidi ml⁻¹ konsantrasyonunda, LT₅₀ ve LT₉₀ değerleri sırasıyla 4,05 ve 8,10 gün olarak kaydedilmiştir. Daha ileri dönemlerde ise ölüm oranlarının düştüğü tespit edilmiştir. LC₅₀ ve LC₉₀ değerleri, artan konsantrasyonlarla azalarak birinci ve ikinci dönem larvalarda tüm dozlarda %100 ölüm sağlamıştır. Üçüncü dönem larvalar doz-bağımlı bir tepki göstermiş ve LC₅₀ ile LC₉₀ değerleri sırasıyla 6.88×10⁸ ve 1.94×10⁴ konidi ml⁻¹ olarak bulunmuştur. Daha yüksek spor konsantrasyonları, LT₅₀ ve LT₉₀ sürelerini kısaltarak özellikle genç larvalarda ölüm oranlarını artırmıştır. Bu bulgular, B. bassiana’nın genç larva dönemlerine karşı etkinliğini, etkili biyolojik mücadele için uygulama zamanlamasının önemini ve entegre zararlı yönetimi stratejilerinde potansiyel rolünü vurgulamaktadır.

Keywords

Beauveria bassiana, biyolojik mücadele, biyopestisit, entomopatojen fungus, Helicoverpa armigera

Thanks

The author would like to thank Prof. Dr. Göksel Özer (Bolu Abant Izzet Baysal University, Türkiye) for their help in the identification of the entomopathogenic fungus and prepare fungal suspensions.

References

• Abbott, W. S., 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18 (2): 265-267.
• Ahmad, M., M. Iqbal Arif & Z. Ahmad, 1999. Patterns of resistance to organophosphate insecticides in field populations of Helicoverpa armigera in Pakistan. Pesticide Science, 55 (6): 626-632.
• Ahmad, M., M. Iqbal Arif & Z. Ahmad, 2003. Susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to new chemistries in Pakistan. Crop Protection, 22 (3): 539-544.
• Altinok, H. H., M. A. Altinok & A. S. Koca, 2019. Modes of action of entomopathogenic fungi. Current Trends in Natural Sciences, 8 (16): 117-124.
• Alwaneen, W. S., M. Tahir, P. B. Avery, W. Wakil, N. G. Kavallieratos, N. Eleftheriadou & A. S. Aldawood, 2024. Initial evaluation of the entomopathogenic fungi Beauveria bassiana and Metarhizium robertsii, and the entomopathogenic nematode Heterorhabditis bacteriophora, individually and in combination against the noxious Helicoverpa armigera (Lepidoptera: Noctuidae). Agronomy, 14 (7): 1395.
• Armes, N. J., G. S. Bond & R. J. Cooter, 1992. The Laboratory Culture and Development of Helicoverpa armigera. Natural Resources Institute, 22 pp.
• Arnemann, J. A., W. J. James, T. K. Walsh, J. V. C. Guedes, G. Smagghe, E. Castiglioni & W. T. Tay, 2016. Mitochondrial DNA COI characterization of Helicoverpa armigera (Lepidoptera: Noctuidae) from Paraguay and Uruguay. Genetics and Molecular Research, 15 (2): 1-8.
• Bale, J. S., J. C. Van Lenteren & F. Bigler, 2008. Biological control and sustainable food production. Philosophical Transactions of the Royal Society B: Biological Sciences, 363 (1492): 761-776.
• Bidochka, M. J., J. E. Kasperski & G. A. Wild, 1998. Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats. Canadian Journal of Botany, 76 (7): 1198-1204.
• Bing, L. A. & L. C. Lewis, 1991. Suppression of Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae) by endophytic Beauveria bassiana (Balsamo) Vuillemin. Environmental Entomology, 20 (4): 1207-1211.
• Bosa, C. F., D. Chávez, L. Torres, A. París, L. Villamizar & A. Cotes, 2004. Evaluación de aislamientos nativos de Nomuraea rileyi para el control de Spodoptera frugiperda (Lepidoptera: Noctuidae). Revista Colombiana de Entomología, 30 (1): 93-97 (in Spanish abstract in Turkish).
• Castillo Lopez, D. & G. A. Sword, 2015. The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea). Biological Control, 89 (2015): 53-60.
• Cherry, A. J., A. Banito, D. Djegui & C. Lome, 2004. Suppression of the stem-borer Sesamia calamistis (Lepidoptera; Noctuidae) in maize following seed dressing, topical application and stem injection with African isolates of Beauveria bassiana. International Journal of Pest Management, 50 (1): 67-73.
• Cherry, A. J., P. Abalo & K. Hell, 2005. A laboratory assessment of the potential of different strains of the entomopathogenic fungi Beauveria bassiana (Balsamo) Vuillemin and Metarhizium anisopliae (Metschnikoff) to control Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) in stored cowpea. Journal of Stored Products Research, 41 (3): 295-309.
• Christian, N., B. E. Sedio, X. Florez-Buitrago, L. A. Ramírez-Camejo, E. I. Rojas, L. C. Mejía, S. Palmedo, A. Rose, J. W. Schroeder & E. A. Herre, 2020. Host affinity of endophytic fungi and the potential for reciprocal interactions involving host secondary chemistry. American Journal of Botany, 107 (2): 219-228.
• Coates, B. S., R. L. Hellmich & L. C. Lewis, 2002. Allelic variation of a Beauveria bassiana (Ascomycota: Hypocreales) minisatellite is independent of host range and geographic origin. Genome, 45 (1): 125-132.
• Cunningham, J. P. & M. P. Zalucki, 2014. Understanding Heliothine (Lepidoptera: Heliothinae) pests: what is a host plant? Journal of Economic Entomology, 107 (3): 881-896.
• Darsouei, R., J. Karimi & L. L. Stelinski, 2024. Endophytic colonization of sugar beet by Beauveria varroae and Beauveria bassiana reduces performance and host preference in armyworm, Spodoptera littoralis. Crop Protection, 175 (2024): 106441 (1-14).
• Deans, C. & V. Krischik, 2023. The current state and future potential of microbial control of scarab pests. Applied Sciences, 13 (2): 766.
• Feng, H., X. Wu, B. Wu & K. Wu, 2009. Seasonal migration of Helicoverpa armigera (Lepidoptera: Noctuidae) over the Bohai sea. Journal of Economic Entomology, 102 (1): 95-104.
• Fitt, G. P., 1989. The ecology of Heliothis species in relation to agroecosystems. Annual Review of Entomology, 34 (1): 17-53.
• García-Estrada, C., E. Cat & I. Santamarta, 2016. “Beauveria bassiana as Biocontrol Agent: Formulation and Commercialization for Pest Management, 81-96” In: Agriculturally Important Microorganisms: Commercialization and Regulatory Requirements in Asia (Eds. H. R. Singh, B. K. Sarma & C. Keswani), Springer, 305 pp.
• Glass, N. L. & G. C. Donaldson, 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology, 61 (4): 1323-1330.
• Goettel, M. S. & T. Glare, 2010. “Entomopathogenic Fungi and Their Role in Regulation of Insect Populations, 387-419”. In: Insect Control: Biological and Synthetic Agents (Eds. L. I. Gilbert & S. S. Gill), Academic Press, 490 pp.
• Güney, İ. G., G. Özer, Ş. Türkölmez & S. Derviş 2022. Canker and leaf scorch on olive (Olea europaea L.) caused by Neoscytalidium dimidiatum in Turkey. Crop Protection, 157 (2022): 105985 (1-11).
• Hafez, M., F. N. Zaki, A. Moursy & M. Sabbour, 1997. Biological effects of the entomopathogenic fungus, Beauveria bassiana on the potato tuber moth Phthorimaea operculella (Seller). Anzeiger für Schädlingskunde, Pflanzenschutz, Umweltschutz, 70 (1): 158-159.
• Idrees, A., Z. A. Qadir, K. S. Akutse, A. Afzal, M. Hussain, W. Islam & J. Li, 2021. Effectiveness of entomopathogenic fungi on immature stages and feeding performance of Fall Armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae. Insects, 12 (11): 1044.
• Inglis, G. D., J. Enkerli & M. S. Goettel, 2012. “Laboratory Techniques Used for Entomopathogenic Fungi: Hypocreales, 189-253”. In: Manual of Techniques in Invertebrate Pathology (Eds. L. A. Lacey), Academic Press, 504 pp.
• Inglis, G. D., M. S. Goettel, T. M. Butt & H. Strasser, 2001. “Use of Hyphomycetous Fungi for Managing Insect Pests, 23-69”. In: Fungi as Biocontrol Agents: Progress, Problems and Potential (Eds. C. Jackson, N. Magan & T. M. Butt), Wallingford UK: CABI Publishing, 390 pp.
• Jaber, L. R. & B. H. Ownley, 2018. Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? BioControl, 116 (2018): 36-45.
• Jones, C. M., A. Papanicolaou, G. K. Mironidis, J. Vontas, Y. Yang, K. S. Lim & J. W. Chapman, 2015. Genomewide transcriptional signatures of migratory flight activity in a globally invasive insect pest. Molecular Ecology, 24 (9): 4901-4911.
• Kaçar, G., A. Butrón, D. Kontogiannatos, P. Han, M. F. G. Peñaflor, G. P. Farinós, F. Huang, W. D. Hutchison, B. H. S. de Souza, R. A. Malvar, A. Kourti, R. Ramirez-Romero, J. L. Smith, A. S. Koca, M. Pineda & K. Haddi, 2023. Recent trends in management strategies for two major maize borers: Ostrinia nubilalis and Sesamia nonagrioides. Journal of Pest Science, 96 (3): 879-901.
• Kakimoto, T., K. Fujisaki & T. Miyatake, 2003. Egg laying preference, larval dispersion, and cannibalism in Helicoverpa armigera (Lepidoptera: Noctuidae). Annals of the Entomological Society of America, 96 (6): 793-798.
• Koca, A. S. & G. Kaçar, 2024. Maize pests and their natural enemies in the north-west of Türkiye. KSU Tarım ve Doğa Dergisi, 27 (Suppl 1): 59-73.
• Kriticos, D. J., N. Ota, W. D. Hutchison, J. Beddow, T. Walsh, W. T. Tay, & M. P. Zalucki, 2015. The potential distribution of invading Helicoverpa armigera in North America: is it just a matter of time? PLoS One, 10 (3): e0119618.
• Lee, K. P. & K. Wilson, 2006. Melanism in a larval Lepidoptera: repeatability and heritability of a dynamic trait. Ecological Entomology, 31 (2): 196-205.
• Liu, Z., J. Scheirs & D. G. Heckel, 2010. Host plant flowering increases both adult oviposition preference and larval performance of a generalist herbivore. Environmental Entomology, 39 (2): 552-560.
• Mascarin, G. M. & S. T. Jaronski, 2016. The production and uses of Beauveria bassiana as a microbial insecticide. World Journal of Microbiology and Biotechnology, 32 (2016): 1-26.
• Meyling, N. V. & J. Eilenberg, 2007. Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. BioControl, 43 (2): 145-155.
• Michereff‐Filho, M., J. B. Torres, L. N. Andrade & M. U. C. Nunes, 2008. Effect of some biorational insecticides on Spodoptera eridania in organic cabbage. Pest Management Science, 64 (7): 761-767.
• Nguyen, N. T., C. Borgemeister, H. M. Poehling & G. Zimmermann, 2007. Laboratory investigations on the potential of entomopathogenic fungi for biocontrol of Helicoverpa armigera (Lepidoptera: Noctuidae) larvae and pupae. Biocontrol Science and Technology, 17 (8): 853-864.
• Queiroz-Santos, L., M. M. Casagrande & A. Specht, 2018. Morphological characterization of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae: Heliothinae). Neotropical Entomology, 47 (2018?): 517-542.
• Riaz, S., J. B. Johnson, M. Ahmad, G. P. Fitt & M. Naiker, 2021. A review on biological interactions and management of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Applied Entomology, 145 (6): 467-498.
• Russo, M. L., A. C. Scorestti, M. F. Vianna, N. Allegrucci, N. A. Ferreri, M. N. Cabello & S. A. Pelizza, 2019. Effects of endophytic Beauveria bassiana (Ascomycota: Hypocreales) on biological, reproductive parameters and food preference of the soybean pest Helicoverpa gelotopoeon. Journal of King Saud University-Science, 31 (4): 1077-1082.
• Sandhu, S. S., S. E. Unkles, R. C. Rajak & J. R. Kinghorn, 2001. Generation of benomyl resistant Beauveria bassiana strains and their infectivity against Helicoverpa armigera. Biocontrol Science and Technology, 11 (2): 245-250.
• Silva, A. C. L., G. A. Silva, P. H. Nogueira Abib, A. T. Carolino & R. L. Samuels, 2020. Endophytic colonization of tomato plants by the entomopathogenic fungus Beauveria bassiana for controlling the South American tomato pinworm, Tuta absoluta. CABI Agriculture and Bioscience, 1 (3): 1-9.
• Tahir, M., W. Wakil, A. Ali & S. T. Sahi, 2019. Pathogenicity of Beauveria bassiana and Metarhizium anisopliae isolates against larvae of the polyphagous pest Helicoverpa armigera. Entomologia Generalis, 38 (1): 225-242.
• Talekar, N. S., R. T. Opena & P. Hanson, 2006. Helicoverpa armigera management: a review of AVRDC's research on host plant resistance in tomato. Crop Protection, 25 (5): 461-467.
• Vandenberg, J. D., M. Ramos & J. A. Altre, 1998. Dose-response and age-and temperature-related susceptibility of the diamondback moth (Lepidoptera: Plutellidae) to two isolates of Beauveria bassiana (Hyphomycetes: Moniliaceae). Environmental Entomology, 27 (4): 1017-1021.
• Vega, F. E., M. S. Goettel, M. Blackwell, D. Chandler, M. A. Jackson, S. Keller & H. E. Roy, 2009. Fungal entomopathogens: new insights on their ecology. Fungal Ecology, 2 (4): 149-159.
• Wagner, B. L. & L. C. Lewis, 2000. Colonization of corn, Zea mays, by the entomopathogenic fungus Beauveria bassiana. Applied and Environmental Microbiology, 66 (8): 3468-3473.
• Walsh, T. K., D. G. Heckel, Y. Wu, S. Downes, K. H. J. Gordon & J. G. Oakeshott, 2022. Determinants of insecticide resistance evolution: comparative analysis among Heliothines. Annual Review of Entomology, 67 (1): 387-406.
• White, T. J., T. Bruns, S. J. W. T. Lee & Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications, 18 (1): 315-322.
• Wilson, K., S. C. Cotter, A. F. Reeson & J. K. Pell, 2001. Melanism and disease resistance in insects. Ecology Letters, 4 (6): 637-649.
• Younas, A., W. Wakil, Z. Khan, M. Shaaban & S. M. Prager, 2017. The efficacy of Beauveria bassiana, jasmonic acid and chlorantraniliprole on larval populations of Helicoverpa armigera in chickpea crop ecosystems. Pest Management Science, 73 (2): 418-424.
• Zalucki, M. P., G. Daglish, S. Firempong & P. Twine, 1986. The biology and ecology of Heliothis armigera (Hubner) and Heliothis punctigera Wallengren (Lepidoptera, Noctuidae) in Australia-What do we know. Australian Journal of Zoology, 34 (6): 779-814
• Zimmermann, G., 2007. Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Science and Technology, 17 (6): 553-596.