Effects of Entomopathogenic Fungi on Natural Enemies: A Systematic Review of Their Use in Biological Control
Keywords:
Integrated pest management, mortality, predator, parasitoid, sublethal effectAbstract
This review evaluates the potential negative impacts of entomopathogenic fungi (EPF) on natural enemies, a key component of sustainable pest management. Literature from Scopus and PubMed, covering 12 countries, 13 EPF species, and 33 natural enemy species, was classified according to the International Organization for Biological Control (IOBC) scale. EPF often caused lethal effects, such as Lecanicillium muscarium killing the parasitoid Diaeretiella rapae, as well as sublethal effects, including reduced reproduction, shortened longevity, decreased survival rates, and prolonged development. These outcomes varied depending on specific EPF–natural enemy interactions. The findings highlight the need for more field-based and long-term studies to ensure EPF applications do not compromise the ecological role of natural enemies in Integrated Pest Management (IPM).
Downloads
Metrics
References
Abbas, M.S.T. 2020. Interactions between entomopathogenic fungi and entomophagous insects. Advances in Entomology, 8(3): 130–146.
Akbari, S., Mirfakhraie, S., Aramideh, S. & Safaralizadeh, M.H. 2020. Effect of fungal isolates and imidacloprid on cabbage aphid Brevicoryne brassicae and its parasitoid Diaeretiella rapae. Zemdirbyste, 107(3): 255–262.
Alharbi, W., Sandhu, S.K., Areshi, M., Alotaibi, A., Alfaidi, M., Al-Qadhi, G. & Morozov, A.Y. 2022. Revisiting implementation of multiple natural enemies in pest management. Scientific Reports, 12(1): 11897.
Araujo, E.S., Poltronieri, A.S., Poitevin, C.G., Mirás-Avalos, J.M., Zawadneak, M.A.C. & Pimentel, I.C. 2020. Compatibility between entomopathogenic fungi and egg parasitoids (Trichogrammatidae): a laboratory study for their combined use to control Duponchelia fovealis. Insects, 11(9): 630.
Atrchian, H., Mahdian, K. & 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.
Avery, P.B., George, J., Markle, L., Martini, X., Rowley, A.L., Meagher, R.L., Barger, R.E., Duren, E.B., Dawson, J.S. & Cave, R.D. 2022. Choice behavior of the generalist pentatomid predator Podisus maculiventris when offered lepidopteran larvae infected with an entomopathogenic fungus. BioControl, 67: 201–211.
Bamisile, B.S., Siddiqui, J.A., Akutse, K.S., Aguila, L.C.R. & Xu, Y. 2021. General limitations to endophytic entomopathogenic fungi use as plant growth promoters, pests and pathogens biocontrol agents. Plants, 10(10): 2119.
Battisti, L., Warmling, J.V., De Freitas Vieira, C., De Oliveira, D.H.R., De Lima, Y.R.A., De Freitas Bueno, A., Potrich, M., Schmaltz, L.E., Mazaro, S.M., Lopes, I.O.N. & Bueno, A.D.F. 2022. Selectivity of Metarhizium anisopliae and Beauveria bassiana to adults of Telenomus podisi (Hymenoptera: Scelionidae). Semina: Ciencias Agrarias, 43(2): 727–738.
Behie, S.W. & Bidochka, M.J. 2014. Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: an additional branch of the soil nitrogen cycle. Applied and Environmental Microbiology, 80(5): 1553–1560.
Betsi, P.C. & Perdikis, D.C. 2023. Lethal and sub-lethal effects of organic-production-approved insecticides and fungicides on the predator Macrolophus pygmaeus (Rambur) (Hemiptera: Miridae). Insects, 14(11): 866.
Bihal, R., Al-Khayri, J.M., Banu, A.N., Kudesia, N., Ahmed, F.K., Sarkar, R., Arora, A. & Abd-Elsalam, K.A. 2023. Entomopathogenic fungi: an eco-friendly synthesis of sustainable nanoparticles and their nanopesticide properties. Microorganisms, 11(6): 1617.
Butt, T.M., Coates, C.J., Dubovskiy, I.M. & Ratcliffe, N.A. 2016. Entomopathogenic fungi: new insights into host-pathogen interactions. Advances in Genetics, 94: 1–58.
Colinet, H., Boivin, G. & Hance, T. 2007. Manipulation of parasitoid size using the temperature-size rule: fitness consequences. Oecologia, 152(3): 425–433.
Collinge, D.B., Jensen, D.F., Rabiey, M., Sarrocco, S., Shaw, M.W. & Shaw, R.H. 2022. Biological control of plant diseases – what has been achieved and what is the direction? Plant Pathology, 71: 1024–1047.
Corallo, A.B., Pechi, E., Bettucci, L. & 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): 15.
Cordeiro, E.M.G., Correˆa, A.S. & Guedes, R.N.C. 2014. Insecticide-mediated shift in ecological dominance between two competing species of grain beetles. Plos One, 9(6): e100990.
de Azevedo, A.G.C., Stuart, R.M. & Sigsgaard, L. 2018. Presence of a generalist entomopathogenic fungus influences the oviposition behaviour of an aphid-specific predator. BioControl, 63(5): 655–664.
Dias, P.M., Loureiro, E.D.S., Pessoa, L.G.A., Devoz, G.L.R., Barbosa Junior, G.B., Werner, A.M., Navarrete, A.A., Barbosa, J.C., Batista Filho, A. & de Alcântara Neves, P.M.O.J. 2020. Selectivity of entomopathogenic fungi to Chrysoperla externa (Neuroptera: Chrysopidae). Insects, 11(10): 716.
Domingues, M.M., Becchi, L.K., Velozo, S.G.M., de Souza, A.R., Barbosa, L.R., Soares, M.A., Serrão, J.E., Zanuncio, J.C., Wilcken, C.F. & Soliman, E.P. 2020. Selectivity of mycoinsecticides and a pyrethroid to the egg parasitoid Cleruchoides noackae (Hymenoptera: Mymaridae). Scientific Reports, 10(1): 14617.
Evans, E.W. 2009. Lady beetles as predators of insects other than Hemiptera. Biological Control, 51(2): 255–267.
FAO. 2021. Climate change fans spread of pests and threatens plants and crops, new FAO study. FAO publications catalogue 2022. https://www.fao.org/newsroom/detail/Climate-change-fans-spread-of-pests-and-threatens-plants-and-crops-new-FAO-study/en [3 October 2024].
Fazeli-Dinan, M., Talaei-Hassanloui, R. & Goettel, M. 2016. Virulence of the entomopathogenic fungus Lecanicillium longisporum against the greenhouse whitefly, Trialeurodes vaporariorum and its parasitoid Encarsia formosa. International Journal of Pest Management, 62(3): 251–260.
Fergani, Y.A., Refaei, E.A.E., Faiz, N.M. & Hamama, H.M. 2023. Evaluation of chlorpyrifos and Beauveria bassiana as a strategy in the Egyptian sugar beet fields: impact on Spodoptera littoralis (Boisduval) and its associated predators populations and the sugar beetroot yield. Egyptian Journal of Biological Pest Control, 33(1): 105.
Forbes, A.A., Bagley, R.K., Beer, M.A., Hippee, A.C. & Widmayer, H.A. 2018. Quantifying the unquantifiable: why Hymenoptera, not Coleoptera, is the most speciose animal order. BMC Ecology, 18(1): 21.
Frago, E. & Zytynska, S. 2023. Impact of herbivore symbionts on parasitoid foraging behaviour. Current Opinion in Insect Science, 56: 101027.
García-Espinoza, F., Yousef-Yousef, M., García del Rosal, M.J., Cuenca-Medina, M. & Quesada-Moraga, E. 2024. Greenhouse melon crop protection and production through the compatible use of a parasitoid with endophytic entomopathogenic ascomycetes. Journal of Pest Science, 97: 1899–1912.
Garner, A.J., Samanta, D., Weaver, M.M. & Horton, B.P. 2024. Changes to tropical cyclone trajectories in Southeast Asia under a warming climate. npj Climate and Atmospheric Science, 7(1): 156.
Gaston, K.J. 1991. The magnitude of global insect species richness. Conservation Biology, 5(3): 283–296.
González-Mas, N., Cuenca-Medina, M., Gutiérrez-Sánchez, F. & Quesada-Moraga, E. 2019. Bottom-up effects of endophytic Beauveria bassiana on multitrophic interactions between the cotton aphid, Aphis gossypii, and its natural enemies in melon. Journal of Pest Science, 92(3): 1271–1281.
Hassan, S.A., Bigler, F., Bogenschütz, H., Boller, E., Brun, J., Calis, J.N.M., Chiverton, P., Coremans-Pelseneer, J., Duso, C., Grove, A., Heimbach, U., Helyer, N., Hokkanen, H., Lewis, G.B., Mansour, F., Moreth, L., Polgar, L., Samsoe-Petersen, L., Sauphanor, B., Staubli, A., Sterk, G., Vainio, A., van de Veire, M., Viggiani, G. & Vogt, H. 1991. Results of the fifth joint pesticide testing programme carried out by the IOBC/WPRS-Working Group "Pesticides and beneficial organisms." Entomophaga, 36(1): 55–60.
Heimpel, G.E. 2019. Linking parasitoid nectar feeding and dispersal in conservation biological control. Biological Control, 132: 36–41.
Heviefo, G.A., Nyamador, S.W., Datinon, B.D., Glitho, I.A. & Tamò, M. 2020. Comparative efficacy of endophytic versus foliar application of the entomopathogenic fungus Beauveria bassiana against the crucifer diamondback moth larvae for sustainable cabbage protection. International Journal of Biological and Chemical Sciences, 14(4): 1448–1458.
Jarrahi, A. & Safavi, S.A. 2016a. Effects of pupal treatment with Proteus® and Metarhizium anisopliae sensu lato on functional response of Habrobracon hebetor parasitising Helicoverpa armigera in an enclosed experiment system. Biocontrol Science and Technology, 26(2): 206–216.
Jarrahi, A. & Safavi, S.A. 2016b. Sublethal effects of Metarhizium anisopliae on life table parameters of Habrobracon hebetor parasitizing Helicoverpa armigera larvae at different time intervals. BioControl, 61(2): 167–175.
José Da Silva, R., Fernandes Martins, I.C., De Conte Carvalho De Alencar, J., Da Silva, K.P., Cividanes, F.J., Duarte, R.T., Agostini, L.T., Silva, R.J., Polanczyk, R.A. & Pratissoli, D. 2017. The effect of the entomopathogenic fungus Lecanicillium longisporum (Petch) Zare & Gams (Hypocreales: Cordycipitacea) on the aphid parasitoid Diaeretiella rapae McIntoch (Hymenoptera: Braconidae, Aphidiinae). Entomologia Generalis, 36(3): 219–229.
Kaczmarek, A. & Boguś, M.I. 2021. Fungi of entomopathogenic potential in Chytridiomycota and Blastocladiomycota, and in fungal allies of the Oomycota and microsporidia. IMA Fungus, 12(1): 29.
Kaya, H.K. & Vega, F.E. 2012. Scope and basic principles of insect pathology. In: Insect Pathology. F.E. Vega & H.K. Kaya (Eds.). Academic Press, San Diego. pp. 1-12.
Khan, S., Guo, L., Maimaiti, Y., Mijit, M. & Qiu, D. 2012. Entomopathogenic fungi as microbial biocontrol agent. Molecular Plant Breeding, 3(7): 63–79.
Leppla, N.C., Lebeck, L.M. & Johnson, M.W. 2024. Status and trends of biological control research, extension, and education in the United States. Annals of the Entomological Society of America, 117(3): 149–161.
Li, X.L., Zhang, J.J., Li, D.D., Cai, X.Y., Qi, Y.X. & Lu, Y.Y. 2024. Toxicity of Beauveria bassiana to Bactrocera dorsalis and effects on its natural predators. Frontiers in Microbiology, 15: 1362089.
Lilly, D.G., Latham, S.L., Webb, C.E. & Doggett, S.L. 2016. Cuticle thickening in a pyrethroid-resistant strain of the common bed bug, Cimex lectularius L. (Hemiptera: Cimicidae). Plos One, 11(4): e0153302.
Liu, J.F., Zhang, Z.Q., Beggs, J.R. & Wei, X.Y. 2019. Influence of pathogenic fungi on the life history and predation rate of mites attacking a psyllid pest. Ecotoxicology and Environmental Safety, 183: 109585.
Mama Sambo, S., Akutse, K.S., du Plessis, H., Aigbedion-Atalor, P.O., Mohamed, S.A. & Ndlela, S. 2022. Interactions between the entomopathogenic fungus Metarhizium anisopliae ICIPE 20 and the endoparasitoid Dolichogenidea gelechiidivoris, and implications for combined biocontrol of Tuta absoluta. Biology, 11(9): 1323.
Manfrino, R.G. & Rocca, M. 2024. Susceptibility of Orius insidiosus to Beauveria bassiana, Akanthomyces muscarius, and Cordyceps fumosorosea and their effects on predator behavior. Entomologia Experimentalis et Applicata, 172(10): 902–909.
Martins, I.C.F., Silva, R.J., Alencar, J.R.D.C.C., Silva, K.P., Cividanes, F.J., Duarte, R.T., Agostini, L.T., Polanczyk, R.A. & Pratissoli, D. 2014. Interactions between the entomopathogenic fungi Beauveria bassiana (Ascomycota: Hypocreales) and the aphid parasitoid Diaeretiella rapae (Hymenoptera: Braconidae) on Myzus persicae (Hemiptera: Aphididae). Journal of Economic Entomology, 107(3): 933–938.
Mascarin, G.M. & Jaronski, S.T. 2016. The production and uses of Beauveria bassiana as a microbial insecticide. World Journal of Microbiology and Biotechnology, 32(11): 177.
Matos Franco, G., Chen, Y., Doyle, V.P., Rehner, S.A. & Diaz, R. 2022. Will the application of biocontrol fungi disrupt predation of Acanthococcus lagerstroemiae by coccinellids? Journal of Invertebrate Pathology, 193: 107789.
Memmott, J., Martinez, N.D. & Cohen, J.E. 2000. Predators, parasitoids and pathogens: species richness, trophic generality and body sizes in a natural food web. Journal of Animal Ecology, 69(1): 1-15.
Mesquita, A.L.M. & Lacey, L.A. 2001. Interactions among the entomopathogenic fungus, Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes), the parasitoid, Aphelinus asychis (Hymenoptera: Aphelinidae), and their aphid host. Biological Control, 22(1): 51–59.
Mezőfi, L., Markó, G., Nagy, C., Korányi, D. & Markó, V. 2020. Beyond polyphagy and opportunism: natural prey of hunting spiders in the canopy of apple trees. PeerJ, 8: e9334.
Miranda-Fuentes, P., Quesada-Moraga, E., Aldebis, H.K. & Yousef-Naef, M. 2020. Compatibility between the endoparasitoid Hyposoter didymator and the entomopathogenic fungus Metarhizium brunneum: a laboratory simulation for the simultaneous use to control Spodoptera littoralis. Pest Management Science, 76(3): 1060–1070.
Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., Antes, G., Atkins, D., Barbour, V., Barrowman, N., Berlin, J.A., Clark, J., Clarke, M., Cook, D., D'Amico, R., Deeks, J.J., Devereaux, P.J., Dickersin, K., Egger, M., Ernst, E., Gøtzsche, P.C., Grimshaw, J., Guyatt, G., Higgins, J., Ioannidis, J.P.A., Kleijnen, J., Lang, T., Magrini, N., McNamee, D., Moja, L., Mulrow, C., Napoli, M., Oxman, A., Pham, B., Rennie, D., Sampson, M., Schulz, K.F., Shekelle, P.G., Tovey, D. & Tugwell, P. 2009. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine, 6(7): e1000097.
Murdoch, W.W., Briggs, C.J. & Nisbet, R.M. 2003. Consumer-Resource Dynamics (MPB-36). Princeton University Press, Princeton. 456 pp.
Ningrum, R.W., Noni Rahmadhini & Windriyanti, W. 2024. Exploration and pathogenicity test of Beauveria bassiana against grayak caterpillars (Spodoptera litura F.). Jurnal Ilmu-Ilmu Pertanian Indonesia, 26(1): 54–60.
Ortiz-Urquiza, A. & Keyhani, N.O. 2013. Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects, 4(3): 357–374.
Pagac, A.A., Geden, C.J., Martin, G.P., Patterson, P.H. & Machtinger, E.T. 2023. Susceptibility of the adult house fly (Diptera: Muscidae) and 3 of its principal parasitoids (Hymenoptera: Pteromalidae) to the GHA strain of Beauveria bassiana and 4 isolates from field-collected muscid flies. Journal of Medical Entomology, 60(6): 1364–1373.
Panwar, N. & Szczepaniec, A. 2024. Endophytic entomopathogenic fungi as biological control agents of insect pests. Pest Management Science, 80(9): 4160–4172.
Peeters, C., Molet, M., Lin, C.C. & Billen, J. 2017. Evolution of cheaper workers in ants: a comparative study of exoskeleton thickness. Biological Journal of the Linnean Society, 121(3): 556-563.
Plouvier, W.N. & Wajnberg, E. 2018. Improving the efficiency of augmentative biological control with arthropod natural enemies: a modeling approach. Biological Control, 125: 121–130.
Quesada-Moraga, E., Garrido-Jurado, I., Yousef-Yousef, M. & González-Mas, N. 2022. Multitrophic interactions of entomopathogenic fungi in BioControl. BioControl, 67(5): 457–472.
Rajula, J., Pittarate, S., Suwannarach, N., Kumla, J., Ptaszynska, A.A., Thungrabeab, M., Mekchay, S. & Krutmuang, P. 2021. Evaluation of native entomopathogenic fungi for the control of fall armyworm (Spodoptera frugiperda) in Thailand: a sustainable way for eco-friendly agriculture. Journal of Fungi, 7(12): 1073.
Rajula, J., Rahman, A. & Krutmuang, P. 2020. Entomopathogenic fungi in Southeast Asia and Africa and their possible adoption in biological control. Biological Control, 151: 104399.
Ríos-Moreno, A., Garrido-Jurado, I., Resquín-Romero, G., Arroyo-Manzanares, N., Arce, L. & Quesada-Moraga, E. 2016. Destruxin A production by Metarhizium brunneum strains during transient endophytic colonisation of Solanum tuberosum. Biocontrol Science and Technology, 26(11): 1574–1585.
Sánchez-Bayo, F. 2021. Indirect effect of pesticides on insects and other arthropods. Toxics, 9(8): 177.
Sani, I., Jamian, S., Saad, N., Abdullah, S., Mohd Hata, E., Jalinas, J. & Ismail, S.I. 2023. Identification and virulence of entomopathogenic fungi, Isaria javanica and Purpureocillium lilacinum isolated from the whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) in Malaysia. Egyptian Journal of Biological Pest Control, 33(1): 14.
Savary, S., Willocquet, L., Pethybridge, S.J., Esker, P., McRoberts, N. & Nelson, A. 2019. The global burden of pathogens and pests on major food crops. Nature Ecology and Evolution, 3(3): 430–439.
Savi, P.J., de Moraes, G.J., Hountondji, F.C.C., Nansen, C. & de Andrade, D.J. 2024. Compatibility of synthetic and biological pesticides with a biocontrol agent Phytoseiulus longipes (Acari: Phytoseiidae). Experimental and Applied Acarology, 93(2): 273–295.
Shrestha, G., Enkegaard, A., Reddy, G.V.P., Skovgård, H. & Steenberg, T. 2017. Susceptibility of larvae and pupae of the aphid parasitoid Aphelinus abdominalis (Hymenoptera: Aphelinidae) to the entomopathogenic fungus Beauveria bassiana. Annals of the Entomological Society of America, 110(1): 121–127.
Stork, N.E. 1991. The composition of the arthropod fauna of Bornean lowland rain forest trees. Journal of Tropical Ecology, 7(2): 161–180.
Upadhyay, R.K., Mukerji, K.G. & Chamola, B.P. 2000. Biocontrol Potential and its Exploitation in Sustainable Agriculture. Kluwer Academic/Plenum Publishers, New York. 317 pp.
van Lenteren, J.C. 2012. IOBC Internet Book of Biological Control, version 6. IOBC Global, Wageningen. 435 pp.
Wu, Y., Fang, H., Liu, X., Michaud, J.P., Xu, H., Zhao, Z., Zhang, S., Liu, Y. & Peng, Y. 2022. Laboratory evaluation of the compatibility of Beauveria bassiana with the egg parasitoid Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae) for joint application against the oriental fruit moth Grapholita molesta (Lepidoptera: Tortricidae). Pest Management Science, 78(8): 3608–3619.
Zhang, Z., Lu, Y., Xu, W., Sui, L., Du, Q., Wang, Y., Zhao, Y., Jiang, T., Zhang, L. & Song, X. 2020. Influence of genetic diversity of seventeen Beauveria bassiana isolates from different hosts on virulence by comparative genomics. BMC Genomics, 21(1): 451.
Published
How to Cite
Issue
Section
Any reproduction of figures, tables and illustrations must obtain written permission from the Chief Editor (wicki@ukm.edu.my). No part of the journal may be reproduced without the editor’s permission











