Efek Non-Target Beauveria bassiana dan Metarhizium spp. terhadap Artropoda Predator: Meta-Analisis Efek Letal dan Subletal pada Berbagai Jalur Paparan
Non-Target Effects of Beauveria bassiana and Metarhizium spp. on Predatory Arthropods: A Meta-Analysis of Lethal and Sublethal Effects Across Exposure Pathways
DOI:
https://doi.org/10.25299/dp.2026.vol42(2).29309Keywords:
biological control, ecological risk, entomopathogenic fungi, Hedges' g, integrated pest management, natural enemyAbstract
Background: Entomopathogenic fungi (EPFs) such as Beauveria bassiana and Metarhizium spp. are widely used as biological control agents in integrated pest management (IPM), but their ecological risks to non-target predatory arthropods remain insufficiently understood; specifically, no quantitative synthesis has yet compared these effects across multiple exposure pathways and predator taxa simultaneously. Objective: This meta-analysis aimed to quantify and compare the lethal and sublethal effects of these two EPF species on predatory arthropods and to determine how exposure pathway and predator taxonomic group modulate the magnitude of ecological risk. Methods: Data were extracted from 27 laboratory studies published between 2015 and 2025, yielding 147 observations across more than 25 predator species representing six taxonomic orders (five with sufficient replication for pooled comparison). Effect sizes, expressed as log odds ratios and Hedges' g, were pooled using random-effects models, and mixed-effects moderator analyses compared EPF species, exposure pathway, and predator taxonomic order. Results: Both B. bassiana and Metarhizium spp. significantly increased predator mortality (pooled OR = 13.33) and reduced survival (OR = 7.665), with no significant difference in lethality between species. Developmental time was significantly prolonged and fecundity was significantly reduced, while longevity showed no significant overall effect, albeit based on limited data (k = 6). Exposure pathway was the strongest significant moderator of fecundity risk: direct application caused significantly greater fecundity reduction than soil or prey-mediated exposure, and Coleoptera showed the greatest susceptibility to developmental disruption among taxonomic orders based on the available data, with Coleoptera also being by far the most represented order (n = 67 observations). Conclusions: Exposure pathway, rather than EPF species identity, was the primary determinant of laboratory-observed lethal and sublethal effects on predatory arthropods, indicating that application method warrants priority attention in ecological risk assessment and in the design of EPF-based biological control strategies that seek to conserve predatory arthropods as key natural enemies, although field validation of these laboratory-based, worst-case-scenario estimates is still needed.
Downloads
References
Assadi, B. H., Chouikhi, S., Ettaib, R., M’hamdi, N. B., and Belkadhi, M. S. 2021. Effect of the native strain of the predator Nesidiocoris tenuis Reuter and the entomopathogenic fungi Beauveria bassiana and Lecanicillium muscarium against Bemisia tabaci (Genn.) under greenhouse conditions in Tunisia. Egyptian Journal of Biological Pest Control, 31, Article 47.
Atrchian, H., Mahdian, K., and Izadi, H. 2022. Sub-lethal effects of Metarhizium anisopliae on the life table parameters of the predatory coccinellid Menochilus sexmaculatus Fabricius. Journal of Applied Entomology, 146(9): 1136–1144.
Bayissa, W., Ekesi, S., Mohamed, S. A., Kaaya, G. P., Wagacha, J. M., Hanna, R., and Maniania, N. K. 2016. Interactions among vegetable-infesting aphids, the fungal pathogen Metarhizium anisopliae (Ascomycota: Hypocreales) and the predatory coccinellid Cheilomenes lunata (Coleoptera: Coccinellidae). Biocontrol Science and Technology, 26(2): 274–290.
Beemrote, A., Srinivasan, M. R., Ningombam, A., Singh, K. S., and Pravallika, P. 2025. Efficacy of soil-isolated entomopathogenic fungi from Manipur (N-E India) against Nilaparvata lugens Stål and their safety assessment on beneficial insects. Journal of Applied Entomology.
Biryol, S., Araz Sayın, N., Aktürk, R., Bilgin, L., İşık, S., Soydinç, A., Topkara, E. F., Yanar, O., Ayvaz, S., Turna, H., and Demir, I. 2025. Target and non-target impact of oil-based Beauveria bassiana formulation in controlling forest insect pests. Journal of Pest Science, 98(4): 2129–2144.
Borenstein, M., Hedges, L. V., Higgins, J. P. T., and Rothstein, H. R. 2009. Introduction to meta-analysis. John Wiley & Sons.
Bruck, D. J. 2010. Fungal entomopathogens in the rhizosphere. BioControl, 55: 103–112.
Corallo, A. B., Pechi, E., Bettucci, L., and Tiscornia, S. 2021. Biological control of the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae) by entomopathogenic fungi and their side effects on natural enemies. Egyptian Journal of Biological Pest Control, 31(1): 1–9.
de Azevedo, A. G. C., Eilenberg, J., Steinwender, B. M., and Sigsgaard, L. 2019. Non-target effects of Metarhizium brunneum (BIPESCO 5/F 52) in soil show that this fungus varies between being compatible with, or moderately harmful to, four predatory arthropods. Biological Control, 131: 18–24.
de Azevedo, A. G. C., Stuart, R. M., and Sigsgaard, L. 2018. Presence of a generalist entomopathogenic fungus influences the oviposition behaviour of an aphid-specific predator. BioControl, 63(5): 655–664.
de Faria, M. R., and Wraight, S. P. 2007. Mycoinsecticides and mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biological Control, 43(3): 237–256.
Dias, P. M., de Souza Loureiro, E., Pessoa, L. G. A., Devoz, G. L. R., Barbosa Junior, G. B., Werner, A. M., Navarrete, A. A., and Teodoro, P. E. 2020. Selectivity of entomopathogenic fungi to Chrysoperla externa (Neuroptera: Chrysopidae). Insects, 11(10): 716.
Dogan, Y. O., Hazir, S., Yildiz, A., Butt, T. M., and Cakmak, I. 2017. Evaluation of entomopathogenic fungi for the control of Tetranychus urticae (Acari: Tetranychidae) and the effect of Metarhizium brunneum on the predatory mites (Acari: Phytoseiidae). Biological Control, 111: 6–12.
Egger, M., Davey Smith, G., Schneider, M., and Minder, C. 1997. Bias in meta-analysis detected by a simple, graphical test. BMJ, 315(7109): 629–634.
Eilenberg, J., Hajek, A., and Lomer, C. 2001. Suggestions for unifying the terminology in biological control. BioControl, 46: 387–400.
Fincham, W. N. W., Dunn, A. M., Brown, L. E., Hesketh, H., and Roy, H. E. 2019. Invasion success of a widespread invasive predator may be explained by a high predatory efficacy but may be influenced by pathogen infection. Biological Invasions, 21(12): 3545–3560.
Furlong, M. J., and Pell, J. K. 2005. Interactions between entomopathogenic fungi and other arthropod natural enemies. In F. E. Vega and M. Blackwell (Eds.), Insect-fungal associations: Ecology and evolution (pp. 51–73). Oxford University Press.
Goettel, M. S., Eilenberg, J., and Glare, T. 2010. Entomopathogenic fungi and their role in regulation of insect populations. In Insect control (pp. 387–431). Academic Press.
Haelewaters, D., Hiller, T., Kemp, E. A., van Wielink, P. S., Shapiro-Ilan, D. I., Aime, M. C., Nedvěd, O., Pfister, D. H., and Cottrell, T. E. 2020. Mortality of native and invasive ladybirds co-infected by ectoparasitic and entomopathogenic fungi. PeerJ, 8, Article e10110.
Hajek, A. E., and St. Leger, R. J. 1994. Interactions between fungal pathogens and insect hosts. Annual Review of Entomology, 39: 293–322.
Higgins, J. P. T., and Thompson, S. G. 2002. Quantifying heterogeneity in a meta-analysis. Statistics in Medicine, 21(11): 1539–1558.
Inglis, G. D., Goettel, M. S., Butt, T. M., and Strasser, H. 2001. Use of hyphomycetous fungi for managing insect pests. In T. M. Butt, C. Jackson, and N. Magan (Eds.), Fungi as biocontrol agents: Progress, problems and potential (pp. 23–69). CABI.
Klingen, I., and Haukeland, S. 2006. The soil as a reservoir for natural enemies of pest insects and mites with emphasis on fungi and nematodes. In J. Eilenberg and H. M. T. Hokkanen (Eds.), An ecological and societal approach to biological control (pp. 145–211). Springer.
Koricheva, J., Gurevitch, J., and Mengersen, K. (Eds.). 2013. Handbook of meta-analysis in ecology and evolution. Princeton University Press.
Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M., and Goettel, M. S. 2015. Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology, 132: 1–41.
Li, X. L., Zhang, J. J., Li, D. D., Cai, X. Y., Qi, Y. X., and Lu, Y. Y. 2024. Toxicity of Beauveria bassiana to Bactrocera dorsalis and effects on its natural predators. Frontiers in Microbiology, 15, Article 1362089.
Matos, G., Chen, Y., Doyle, V. P., Rehner, S. A., and Diaz, R. 2022. Will the application of biocontrol fungi disrupt predation of Acanthococcus lagerstroemiae by coccinellids? Journal of Invertebrate Pathology, 193, Article 107789.
Meyling, N. V., and Eilenberg, J. 2006. Occurrence and distribution of soil-borne entomopathogenic fungi within a single organic agroecosystem. Agriculture, Ecosystems & Environment, 113(1–4): 336–341.
Midthassel, A., Leather, S. R., Wright, D. J., and Baxter, I. H. 2016. Compatibility of Amblyseius swirskii with Beauveria bassiana: Two potentially complimentary biocontrol agents. BioControl, 61(4): 437–447.
Mitina, G. V., Pazyuk, I. M., Choglokova, A. A., and Cherepanova, M. A. 2024. Pathogenicity of fungi of the genus Lecanicillium sensu lato against the predatory bug Orius laevigatus Fieber (Heteroptera, Anthocoridae) and effectiveness of dissemination of fungal spores by the predator against the peach aphid Myzus persicae (Sulzer) (Hemiptera, Aphididae). Entomological Review, 104(9): 525–535.
Mohamed, G. S. 2019. The virulence of the entomopathogenic fungi on the predatory species, Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) under laboratory conditions. Egyptian Journal of Biological Pest Control, 29, Article 23.
Morda, C., Nuvoli, M. T., and Ruiu, L. 2024. Safety of the entomopathogenic fungus Beauveria bassiana for wild and laboratory-reared Chrysoperla lucasina strains. Insects, 15(8): 576.
Page, M. J., McKenzie, J. E., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., Shamseer, L., Tetzlaff, J. M., Akl, E. A., Brennan, S. E., Chou, R., Glanville, J., Grimshaw, J. M., Hróbjartsson, A., Lalu, M. M., Li, T., Loder, E. W., Mayo-Wilson, E., McDonald, S., … Moher, D. 2021. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ, 372, Article n71.
Portilla, M., Luttrell, R., Snodgrass, G., Zhu, Y. C., and Riddick, E. 2017. Lethality of the entomogenous fungus Beauveria bassiana strain NI8 on Lygus lineolaris (Hemiptera: Miridae) and its possible impact on beneficial arthropods. Journal of Entomological Science, 52(4): 352–369.
Ríos-Moreno, A., Quesada-Moraga, E., and Garrido-Jurado, I. 2018. Treatments with Metarhizium brunneum BIPESCO5 and EAMa 01/58-Su strains (Ascomycota: Hypocreales) are low risk for the generalist predator Chrysoperla carnea. Journal of Pest Science, 91: 385–394.
Rizwan, M., Atta, B., Arshad, M., Khan, R. R., Dageri, A., and Rizwan, M. 2021. Nondetrimental impact of two concomitant entomopathogenic fungi on life history parameters of a generalist predator, Coccinella septempunctata (Coleoptera: Coccinellidae). Scientific Reports, 11, Article 20699.
Rohatgi, A. 2022. WebPlotDigitizer (Version 4.6) [Computer software].
Roy, H. E., and Cottrell, T. E. 2008. Forgotten natural enemies: Interactions between coccinellids and insect-parasitic fungi. European Journal of Entomology, 105(3): 391–398.
Roy, H. E., Steinkraus, D. C., Eilenberg, J., Hajek, A. E., and Pell, J. K. 2006. Bizarre interactions and endgames: Entomopathogenic fungi and their arthropod hosts. Annual Review of Entomology, 51: 331–357.
Sahayaraj, K., Subash, N., Allingham, R. W., Kumar, V., Avery, P. B., Mehra, L. K., McKenzie, C. L., and Osborne, L. S. 2018. Lethal and sublethal effects of three microbial biocontrol agents on Spodoptera litura and its natural predator Rhynocoris kumarii. Insects, 9(3), Article 101.
Sayed, S. M., Elarrnaouty, S. A., AlOtaibi, S., and Salah, M. 2021. Pathogenicity and side effect of indigenous Beauveria bassiana on Coccinella undecimpunctata and Hippodamia variegata (Coleoptera: Coccinellidae). Insects, 12(1): 42.
Schmidt-Jeffris, R. A., Beers, E. H., and Sater, C. 2021. Meta-analysis and review of pesticide non-target effects on phytoseiids, key biological control agents. Pest Management Science, 77(11): 4848–4862.
Scorsetti, A. C., Vianna, F., Pelizza, S., Fogel, M. N., and Schneider, M. I. 2017. Interactions between the entomopathogenic fungus Beauveria bassiana and the Neotropical predator Eriopis connexa (Coleoptera: Coccinellidae): Implications in biological control of pest. Journal of Plant Protection Research, 57(4): 389–395.
Trizelia, Busniah, M., and Permadi, A. 2017. Pathogenicity of entomopathogenic fungus Metarhizium spp. against predators Menochilus sexmaculatus Fabricius (Coleoptera: Coccinellidae). Asian Journal of Agriculture, 1(1): 1–5.
Ullah, M. S., and Lim, U. T. 2017. Laboratory evaluation of the effect of Beauveria bassiana on the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae). Journal of Invertebrate Pathology, 148: 102–109.
Ullah, M. I., Altaf, N., Afzal, M., Arshad, M., Mehmood, N., Riaz, M., Majeed, S., Ali, S., and Abdullah, A. 2019. Effects of entomopathogenic fungi on the biology of Spodoptera litura (Lepidoptera: Noctuidae) and its reduviid predator, Rhynocoris marginatus (Heteroptera: Reduviidae). International Journal of Insect Science, 11: 1–7.
van Lenteren, J. C., Bolckmans, K., Köhl, J., Ravensberg, W. J., and Urbaneja, A. 2018. Biological control using invertebrates and microorganisms: Plenty of new opportunities. BioControl, 63(1): 39–59.
Viechtbauer, W. 2010. Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36(3): 1–48.
Wu, S., Gao, Y., Xu, X., Wang, E., Wang, Y., and Lei, Z. 2015. Feeding on Beauveria bassiana-treated Frankliniella occidentalis causes negative effects on the predatory mite Neoseiulus barkeri. Scientific Reports, 5, Article 12033.
Zilnik, G., Bergeron, P. E., Chuang, A., Diepenbrock, L., Hanel, A., Middleton, E., Moretti, E., and Schmidt-Jeffris, R. 2023. Meta-analysis of herbicide non-target effects on pest natural enemies. Insects, 14(10): 787.
