Entomopathogenic fungi and entomopathogenic nematodes are globally distributed soil organisms capable of infecting and killing a vast variety of insects. Therefore, these organisms are frequently used as biocontrol agents in insect pest management. Both entomopathogenic fungi and nematodes share the soil environment and thus can infest and compete for the same insect host; however, natural co-infections are rarely found due to the cryptic soil environment. Our current knowledge on their interactions within hosts mainly comes from laboratory experiments. Because of the recent trend of combining biocontrol agents to increase their efficacy, many studies have focused on the co-application of different species of EPF and EPNs against various insect pests with variable outcomes ranging from synergistic effects and additive effects to antagonism. In addition, the effect on the development and reproduction of each pathogen varies from normal reproduction to exclusion, and generally the outcomes of the interactions are dependent on pathogen and host species, pathogen doses, and the timing of infection. The present review aims to summarize the current knowledge on the interactions of entomopathogenic fungi and nematodes within an insect host and to estimate the possible effects of the interactions on natural pathogen populations and on their use in biocontrol.

Biology Centre of the Czech Academy of Sciences Institute of Entomology Branišovská 31 37005 České Budějovice Czech Republic

Department of Soil Plant and Food Sciences University of Bari Aldo Moro Via G Amendola 165 a 70126 Bari Italy

Zobrazit více v PubMed

Poinar G.O. Nematodes for Biological Control of Insects. CRC Press; Boca Raton, FL, USA: 2018.

Poinar G.O., Jr. Taxonomy and Biology of Steinernematidae and Heterorhabditidae. Entomopathog. Nematodes Biol. Control. 1990;54:1–42.

Gaugler R. Entomopathogenic Nematology. CABI Publishing; Wallingford, UK: 2002.

Quesada-Moraga E., Yousef-Naef M., Garrido-Jurado I. Biopesticides for Sustainable Agriculture. Burleigh Dodds Science Publishing; Cambridge, UK: 2020. Advances in the Use of Entomopathogenic Fungi as Biopesticides in Suppressing Crop Pests; pp. 63–98.

Barbercheck M.E., Kaya H.K. Competitive Interactions between Entomopathogenic Nematodes and Beauveria Bassiana (Deuteromycotina: Hyphomycetes) in Soilborne Larvae of Spodoptera Exigua (Lepidoptera: Noctuidae) Environ. Entomol. 1991;20:707–712. doi: 10.1093/ee/20.2.707. DOI

Ansari M., Tirry L., Moens M. Interaction between Metarhizium Anisopliae CLO 53 and Entomopathogenic Nematodes for the Control of Hoplia Philanthus. Biol. Control. 2004;31:172–180. doi: 10.1016/j.biocontrol.2004.04.002. DOI

Shapiro-Ilan D.I., Jackson M., Reilly C.C., Hotchkiss M.W. Effects of Combining an Entomopathogenic Fungi or Bacterium with Entomopathogenic Nematodes on Mortality of Curculio Caryae (Coleoptera: Curculionidae) Biol. Control. 2004;30:119–126. doi: 10.1016/j.biocontrol.2003.09.014. DOI

Ansari M., Shah F., Butt T. Combined Use of Entomopathogenic Nematodes and Metarhizium Anisopliae as a New Approach for Black Vine Weevil, Otiorhynchus Sulcatus, Control. Entomol. Exp. Et Appl. 2008;129:340–347. doi: 10.1111/j.1570-7458.2008.00783.x. DOI

Tarasco E., Santiago Alvarez C., Triggiani O., Quesada Moraga E. Laboratory Studies on the Competition for Insect Haemocoel between Beauveria Bassiana and Steinernema Ichnusae Recovered in the Same Ecological Niche. Biocontrol Sci. Technol. 2011;21:693–704. doi: 10.1080/09583157.2011.570428. DOI

El Khoury Y., Noujeim E., Ravlić J., Oreste M., Addante R., Nemer N., Tarasco E. The Effect of Entomopathogenic Nematodes and Fungi against Four Xylophagous Pests. Biocontrol Sci. Technol. 2020;30:983–995. doi: 10.1080/09583157.2020.1781059. DOI

Goettel M.S., Poprawski T., Vandenberg J., Li Z., Roberts D.W. Safety to Nontarget Invertebrates of Fungal Biocontrol Agents. In: Laird M., Lacey L., Davidson E., editors. Safety of Microbial Insecticides. CRC Press; Boca Raton, FL, USA: 1990.

Hajek A.E., Butler L. Nontarget Effects of Biological Control. Springer; Berlin/Heidelberg, Germany: 2000. Predicting the Host Range of Entomopathogenic Fungi; pp. 263–276.

Uma Devi K., Padmavathi J., Uma Maheswara Rao C., Khan A.A.P., Mohan M.C. A Study of Host Specificity in the Entomopathogenic Fungus Beauveria Bassiana (Hypocreales, Clavicipitaceae) Biocontrol Sci. Technol. 2008;18:975–989. doi: 10.1080/09583150802450451. DOI

Georgis R. Present and Future Prospects for Entomopathogenic Nematode Products. Biocontrol Sci. Technol. 1992;2:83–99. doi: 10.1080/09583159209355222. DOI

Kaya H.K., Gaugler R. Entomopathogenic Nematodes. Annu. Rev. Entomol. 1993;38:181–206. doi: 10.1146/annurev.en.38.010193.001145. DOI

Mideo N. Parasite Adaptations to Within-Host Competition. Trends Parasitol. 2009;25:261–268. doi: 10.1016/j.pt.2009.03.001. PubMed DOI

Barbercheck M.E., Kaya H.K. Effect of Host Condition and Soil Texture on Host Finding by the Entomogenous Nematodes Heterorhabditis Bacteriophora (Rhabditida: Heterorhabditidae) and Steinernema Carpocapsae (Rhabditida: Steinernematidae) Environ. Entomol. 1991;20:582–589. doi: 10.1093/ee/20.2.582. DOI

Hussein H.M., Skoková Habuštová O., Půža V., Zemek R. Laboratory Evaluation of Isaria Fumosorosea CCM 8367 and Steinernema Feltiae Ustinov against Immature Stages of the Colorado Potato Beetle. PLoS ONE. 2016;11:e0152399. doi: 10.1371/journal.pone.0152399. PubMed DOI PMC

Barberchek M.E., Kaya H.K. Interactions between Beauveria Bassiana and the Entomogenous Nematodes, Steinernema Feltiae and Heterorhabditis Heliothidis. J. Invertebr. Pathol. 1990;55:225–234. doi: 10.1016/0022-2011(90)90058-E. DOI

Li J., Chen G., Wu H., Webster J.M. Identification of Two Pigments and a Hydroxystilbene Antibiotic from Photorhabdus Luminescens. Appl. Environ. Microbiol. 1995;61:4329–4333. doi: 10.1128/aem.61.12.4329-4333.1995. PubMed DOI PMC

Gualtieri M., Aumelas A., Thaler J.-O. Identification of a New Antimicrobial Lysine-Rich Cyclolipopeptide Family from Xenorhabdus Nematophila. J. Antibiot. 2009;62:295–302. doi: 10.1038/ja.2009.31. PubMed DOI

Böszörményi E., Érsek T., Fodor A., Fodor A., Földes L.S., Hevesi M., Hogan J., Katona Z., Klein M., Kormány A. Isolation and Activity of Xenorhabdus Antimicrobial Compounds against the Plant Pathogens Erwinia Amylovora and Phytophthora Nicotianae. J. Appl. Microbiol. 2009;107:746–759. doi: 10.1111/j.1365-2672.2009.04249.x. PubMed DOI

Hazir S., Shapiro-Ilan D.I., Bock C.H., Leite L.G. Trans-Cinnamic Acid and Xenorhabdus Szentirmaii Metabolites Synergize the Potency of Some Commercial Fungicides. J. Invertebr. Pathol. 2017;145:1–8. doi: 10.1016/j.jip.2017.03.007. PubMed DOI

Cimen H., Touray M., Gulsen S.H., Erincik O., Wenski S.L., Bode H.B., Shapiro-Ilan D., Hazir S. Antifungal Activity of Different Xenorhabdus and Photorhabdus Species against Various Fungal Phytopathogens and Identification of the Antifungal Compounds from X. Szentirmaii. Appl. Microbiol. Biotechnol. 2021;105:5517–5528. doi: 10.1007/s00253-021-11435-3. PubMed DOI

Chen G., Dunphy G., Webster J. Antifungal Activity of Two Xenorhabdus Species and Photorhabdus Luminescens, Bacteria Associated with the Nematodes Steinernema Species and Heterorhabditis Megidis. Biol. Control. 1994;4:157–162. doi: 10.1006/bcon.1994.1025. DOI

Ansari M.A., Tirry L., Moens M. Antagonism between Entomopathogenic Fungi and Bacterial Symbionts of Entomopathogenic Nematodes. BioControl. 2005;50:465–475. doi: 10.1007/s10526-004-5524-4. DOI

Acevedo J.P.M., Samuels R.I., Machado I.R., Dolinski C. Interactions between Isolates of the Entomopathogenic Fungus Metarhizium Anisopliae and the Entomopathogenic Nematode Heterorhabditis Bacteriophora JPM4 during Infection of the Sugar Cane Borer Diatraea Saccharalis (Lepidoptera: Pyralidae) J. Invertebr. Pathol. 2007;96:187–192. doi: 10.1016/j.jip.2007.04.003. PubMed DOI

Kershaw M., Moorhouse E., Bateman R., Reynolds S., Charnley A. The Role of Destruxins in the Pathogenicity of Metarhizium Anisopliae for Three Species of Insect. J. Invertebr. Pathol. 1999;74:213–223. doi: 10.1006/jipa.1999.4884. PubMed DOI

Castrillo L.A., Roberts D.W., Vandenberg J.D. The Fungal Past, Present, and Future: Germination, Ramification, and Reproduction. J. Invertebr. Pathol. 2005;89:46–56. doi: 10.1016/j.jip.2005.06.005. PubMed DOI

Vey A., Hoagland R.E., Butt T.M. 12 Toxic Metabolites of Fungal Biocontrol Agents. Fungi Biocontrol Agents. 2001:311. doi: 10.1079/9780851993560.0311. DOI

Hummadi E.H., Dearden A., Generalovic T., Clunie B., Harrott A., Cetin Y., Demirbek M., Khoja S., Eastwood D., Dudley E. Volatile Organic Compounds of Metarhizium Brunneum Influence the Efficacy of Entomopathogenic Nematodes in Insect Control. Biol. Control. 2021;155:104527. doi: 10.1016/j.biocontrol.2020.104527. PubMed DOI PMC

KAYA H.K. Entomopathogenic Nematology. Volume 189. CABI; Wallingford, UK: 2002. Natural Enemies and Other. DOI

Shaurub E.-S.H., Reyad N.F., Abdel-Wahab H.A., Ahmed S.H. Mortality and Nematode Production in Spodoptera Littoralis Larvae in Relation to Dual Infection with Steinernema Riobrave, Heterorhabditis Bacteriophora, and Beauveria Bassiana, and the Host Plant. Biol. Control. 2016;103:86–94. doi: 10.1016/j.biocontrol.2016.08.007. DOI

Wu S., Youngman R.R., Kok L.T., Laub C.A., Pfeiffer D.G. Interaction between Entomopathogenic Nematodes and Entomopathogenic Fungi Applied to Third Instar Southern Masked Chafer White Grubs, Cyclocephala Lurida (Coleoptera: Scarabaeidae), under Laboratory and Greenhouse Conditions. Biol. Control. 2014;76:65–73. doi: 10.1016/j.biocontrol.2014.05.002. DOI

Gaugler R., Wang Y., Campbell J.F. Aggressive and Evasive Behaviors in Popillia Japonica (Coleoptera: Scarabaeidae) Larvae: Defenses against Entomopathogenic Nematode Attack. J. Invertebr. Pathol. 1994;64:193–199. doi: 10.1016/S0022-2011(94)90150-3. DOI

Wang Y., Campbell J.F., Gaugler R. Infection of Entomopathogenic Nematodes Steinernema Glaseri and Heterorhabditis Bacteriophora against Popillia Japonica (Coleoptera: Scarabaeidae) Larvae. J. Invertebr. Pathol. 1995;66:178–184. doi: 10.1006/jipa.1995.1081. DOI

Ansari M., Shah F., Tirry L., Moens M. Field Trials against Hoplia Philanthus (Coleoptera: Scarabaeidae) with a Combination of an Entomopathogenic Nematode and the Fungus Metarhizium Anisopliae CLO 53. Biol. Control. 2006;39:453–459. doi: 10.1016/j.biocontrol.2006.07.004. DOI

Srivastava C., Mohan L., Sharma P., Maurya P. A Review on Prospectives of Synergistic Approach in Insect Pest Management. J. Entomol. Res. 2011;35:255–266.

Jacques R., Morris O. Microbial Control of Insect Pests and Plant Diseases, 1970–1980. HD Burges; New York, NY, USA: 1981. Compatibility of Pathogens with Other Methods of Pest Control and with Different Crops.

Ericsson J.D., Todd Kabaluk J., Goettel M.S., Myers J.H. Spinosad Interacts Synergistically with the Insect Pathogen Metarhizium Anisopliae against the Exotic Wireworms Agriotes Lineatus and Agriotes Obscurus (Coleoptera: Elateridae) J. Econ. Entomol. 2007;100:31–38. doi: 10.1603/0022-0493(2007)100[31:SISWTI]2.0.CO;2. PubMed DOI

Shah F.A., Ansari M., Prasad M., Butt T. Evaluation of Black Vine Weevil (Otiorhynchus Sulcatus) Control Strategies Using Metarhizium Anisopliae with Sublethal Doses of Insecticides in Disparate Horticultural Growing Media. Biol. Control. 2007;40:246–252. doi: 10.1016/j.biocontrol.2006.10.005. DOI

Guetsky R., Shtienberg D., Elad Y., Dinoor A. Combining Biocontrol Agents to Reduce the Variability of Biological Control. Phytopathology. 2001;91:621–627. doi: 10.1094/PHYTO.2001.91.7.621. PubMed DOI

Otsuki H., Yano S. Functionally Different Predators Break down Antipredator Defenses of Spider Mites. Entomol. Exp. Et Appl. 2014;151:27–33. doi: 10.1111/eea.12164. DOI

Choo H.Y., Kaya H.K., Huh J., Lee D.W., Kim H.H., Lee S.M., Choo Y.M. Entomopathogenic Nematodes (Steinernema Spp. and Heterorhabditis Bacteriophora) and a Fungus Beauveria Brongniartii for Biological Control of the White Grubs, Ectinohoplia Rufipes and Exomala Orientalis, in Korean Golf Courses. Biocontrol. 2002;47:177–192. doi: 10.1023/A:1014559729607. DOI

Anbesse S.A., Adge B.J., Gebru W.M. Laboratory Screening for Virulent Entomopathogenic Nematodes (Heterorhabditis Bacteriophora and Steinernema Yirgalemense) and Fungi (Metarhizium Anisopliae and Beauveria Bassiana) and Assessment of Possible Synergistic Effects of Combined Use against Grubs of the Barley Chafer Coptognathus Curtipennis. Nematology. 2008;10:701–709.

Ansari M., Shah F., Butt T. The Entomopathogenic Nematode Steinernema Kraussei and Metarhizium Anisopliae Work Synergistically in Controlling Overwintering Larvae of the Black Vine Weevil, Otiorhynchus Sulcatus, in Strawberry Growbags. Biocontrol Sci. Technol. 2010;20:99–105. doi: 10.1080/09583150903420031. DOI

Batalla-Carrera L., Morton A., Santamaria S., García-del-Pino F. Isolation and Virulence of Entomopathogenic Fungi against Larvae of Hazelnut Weevil Curculio Nucum (Coleoptera, Curculionidae) and the Effects of Combining Metarhizium Anisopliae with Entomopathogenic Nematodes in the Laboratory. Biocontrol Sci. Technol. 2013;23:101–125. doi: 10.1080/09583157.2012.741681. DOI

Wakil W., Yasin M., Shapiro-Ilan D. Effects of Single and Combined Applications of Entomopathogenic Fungi and Nematodes against Rhynchophorus Ferrugineus (Olivier) Sci. Rep. 2017;7:5971. doi: 10.1038/s41598-017-05615-3. PubMed DOI PMC

Williams C.D., Dillon A.B., Harvey C.D., Hennessy R., Mc Namara L., Griffin C.T. Control of a Major Pest of Forestry, Hylobius Abietis, with Entomopathogenic Nematodes and Fungi Using Eradicant and Prophylactic Strategies. For. Ecol. Manag. 2013;305:212–222. doi: 10.1016/j.foreco.2013.05.055. DOI

Mc Namara L., Kapranas A., Williams C.D., O’Tuama P., Kavanagh K., Griffin C.T. Efficacy of Entomopathogenic Fungi against Large Pine Weevil, Hylobius Abietis, and Their Additive Effects When Combined with Entomopathogenic Nematodes. J. Pest Sci. 2018;91:1407–1419. doi: 10.1007/s10340-018-0994-9. DOI

Uzun Yiğit A., Göze Özdemir F.G., Demirözer O., Nayır T. Efficacy of Single and Combined Applications of Entomopathogenic Fungi and Nematodes against the Pupae of Colorado Potato Beetle (Leptinotarsa Decemlineata [Say]),(Coleoptera: Chrysomelidae) Egypt. J. Biol. Pest Control. 2022;32:81. doi: 10.1186/s41938-022-00578-8. DOI

Correa-Cuadros J., Sáenz-Aponte A., Rodríguez-Bocanegra M. In Vitro Interaction of Metarhizium Anisopliae Ma9236 and Beauveria Bassiana Bb9205 with Heterorhabditis Bacteriophora HNI0100 for the Control of Plutella Xylostella. SpringerPlus. 2016;5:2068. doi: 10.1186/s40064-016-3745-5. PubMed DOI PMC

Sáenz-Aponte A., Correa-Cuadros J., Rodríguez-Bocanegra M. Foliar Application of Entomopathogenic Nematodes and Fungi for the Management of the Diamond Back Moth in Greenhouse and Field. Biol. Control. 2020;142:104163. doi: 10.1016/j.biocontrol.2019.104163. DOI

Prinsloo S., Hill M.P., Moore S.D., Malan A.P., Coombes C.A. Interaction between an Entomopathogenic Fungus and Entomopathogenic Nematodes for Increased Mortality of Thaumatotibia Leucotreta (Lepidoptera: Tortricidae) Biocontrol Sci. Technol. 2022;32:1194–1207. doi: 10.1080/09583157.2022.2099528. DOI

Usman M., Gulzar S., Wakil W., Wu S., Piñero J.C., Leskey T.C., Nixon L.J., Oliveira-Hofman C., Toews M.D., Shapiro-Ilan D. Virulence of Entomopathogenic Fungi to Rhagoletis Pomonella (Diptera: Tephritidae) and Interactions with Entomopathogenic Nematodes. J. Econ. Entomol. 2020;113:2627–2633. doi: 10.1093/jee/toaa209. PubMed DOI

Wakil W., Usman M., Piñero J.C., Wu S., Toews M.D., Shapiro-Ilan D.I. Combined Application of Entomopathogenic Nematodes and Fungi against Fruit Flies, Bactrocera Zonata and B. Dorsalis (Diptera: Tephritidae): Laboratory Cups to Field Study. Pest Manag. Sci. 2022;78:2779–2791. doi: 10.1002/ps.6899. PubMed DOI

Gulzar S., Wakil W., Shapiro-Ilan D.I. Combined Effect of Entomopathogens against Thrips Tabaci Lindeman (Thysanoptera: Thripidae): Laboratory, Greenhouse and Field Trials. Insects. 2021;12:456. doi: 10.3390/insects12050456. PubMed DOI PMC

Al Mazra’awi M., Shipp J., Broadbent A., Kevan P. Dissemination of Beauveria Bassiana by Honey Bees (Hymenoptera: Apidae) for Control of Tarnished Plant Bug (Hemiptera: Miridae) on Canola. Environ. Entomol. 2006;35:1569–1577. doi: 10.1093/ee/35.6.1569. DOI

Kapongo J.P., Shipp L., Kevan P., Broadbent B. Optimal Concentration of Beauveria Bassiana Vectored by Bumble Bees in Relation to Pest and Bee Mortality in Greenhouse Tomato and Sweet Pepper. BioControl. 2008;53:797–812. doi: 10.1007/s10526-007-9142-9. DOI

Baverstock J., Roy H.E., Pell J.K. The Ecology of Fungal Entomopathogens. Springer; Berlin/Heidelberg, Germany: 2009. Entomopathogenic Fungi and Insect Behaviour: From Unsuspecting Hosts to Targeted Vectors; pp. 89–102.

Zhang Y.-X., Sun L., Lin G.-Y., Lin J.-Z., Chen X., Ji J., Zhang Z.-Q., Saito Y. A Novel Use of Predatory Mites for Dissemination of Fungal Pathogen for Insect Biocontrol: The Case of Amblyseius Swirskii and Neoseiulus Cucumeris (Phytoseiidae) as Vectors of Beauveria Bassiana against Diaphorina Citri (Psyllidae) Syst. Appl. Acarol. 2015;20:177–187.

Lin G., Tanguay A., Guertin C., Todorova S., Brodeur J. A New Method for Loading Predatory Mites with Entomopathogenic Fungi for Biological Control of Their Prey. Biol. Control. 2017;115:105–111. doi: 10.1016/j.biocontrol.2017.09.012. DOI

Nermuť J., Konopická J., Zemek R., Kopačka M., Bohatá A., Půža V. Dissemination of Isaria Fumosorosea Spores by Steinernema Feltiae and Heterorhabditis Bacteriophora. J. Fungi. 2020;6:359. doi: 10.3390/jof6040359. PubMed DOI PMC

Nermuť J., Hopfgartner M., Konopická J., Půža V. Enhancement of Spores’ Dissemination in the Combination of Entomopathogenic Nematodes and Fungus. J. Pest Sci. 2022 submitted.

Wilson M.J., Ehlers R.-U., Glazer I. Entomopathogenic Nematode Foraging Strategies–Is Steinernema Carpocapsae Really an Ambush Forager? Nematology. 2012;14:389–394. doi: 10.1163/156854111X617428. DOI

KOPPENHOFER A., GREWAL P. Nematodes as Biocontrol Agents. CABI; New York, NY, USA: 2005. Compatibility and Interactions with Agrochemicals and Other Biocontrol Agents. 147–166.

Půža V., Nermuť J., Konopická J., Skoková Habuštová O. Efficacy of the Applied Natural Enemies on the Survival of Colorado Potato Beetle Adults. Insects. 2021;12:1030. doi: 10.3390/insects12111030. PubMed DOI PMC

Zemek R., Konopická J., Jozová E., Skoková Habuštová O. Virulence of Beauveria Bassiana Strains Isolated from Cadavers of Colorado Potato Beetle, Leptinotarsa Decemlineata. Insects. 2021;12:1077. doi: 10.3390/insects12121077. PubMed DOI PMC

Půža V. Principles of Plant-Microbe Interactions. Springer; Berlin/Heidelberg, Germany: 2015. Control of Insect Pests by Entomopathogenic Nematodes; pp. 175–183.

Smits P.H. Post-Application Persistence of Entomopathogenic Nematodes. Biocontrol Sci. Technol. 1996;6:379–388. doi: 10.1080/09583159631352. DOI

Systematics and phylogeny of the entomopathogenic nematobacterial complexes Steinernema-Xenorhabdus and Heterorhabditis-Photorhabdus