Survey of entomopathogenic nematodes and fungi in agricultural areas

https://doi.org/10.17221/7/2019-PPSCitation:Dzięgielewska M., Adamska I. (2020): Survey of entomopathogenic nematodes and fungi in agricultural areas. Plant Protect. Sci., 56: 214-225.
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In 2016-2018, in north-western Poland, field studies were carried out on the coexistence of various taxonomic groups, such as soil nematodes and fungi, including beneficial species that comprise the environment’s natural resistance to pests in agrocenoses. The research aimed to find a connection between select biotic and abiotic factors in the chosen crops which could have practical applications in plant protection. Entomopathogenic nematodes Steinernema feltiae Filipiev, 1934 and entomopathogenic fungi Cordyceps fumosorosea and Metarhizium anisopliae (Metschn.) Sorokin were found to be present in all studied agrocenoses; however, they showed clear preferences for some types of crops or soil. The research shows that the effectiveness of the biological methods of plant protection depends on the selection of the right biopreparations, which strengthen the local populations of the beneficial organisms present in specific agriculture areas.

References:
Abate B.A., Wingfield M.J., Slippers B., Hurley B.P. (2017): Commercialisation of entomopathogenic nematodes: should import regulations be revised? Biocontrol Science and Technology, 27: 149–168. https://doi.org/10.1080/09583157.2016.1278200
 
Abd-Elgawad M.M.M. (2019): Towards optimization of entomopathogenic nematodes for more service in the biological control of insect pests. Egyptian Journal of Biological Pest Control, 29: 77. doi:10.1186/s41938-019-0181-1 https://doi.org/10.1186/s41938-019-0181-1
 
Acosta−Martinez V., Mikha M.M., Vigil M.F. (2007): Microbial communities and enzyme activities in soils under alternative crop rotations compared to wheat−fallow for the Central Great Plains. Applied Soil Ecology, 37: 41−52. https://doi.org/10.1016/j.apsoil.2007.03.009
 
Anbesse S.A., Adge B.J., Gebru W.M. (2008): 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, 10: 701–709. https://doi.org/10.1163/156854108785787217
 
Ansari M.A., Evans M., Butt T.M. (2009): Identification of pathogenic strains of entomopathogenic nematodes and fungi for wireworm control. Crop Protection, 28: 269–272. https://doi.org/10.1016/j.cropro.2008.11.003
 
Ansari M.A., Shah F.A., Tirry L., Moens M. (2006): Field trials against Hoplia philanthus (Coleoptera: Scarabaeidae) with a combination of an entomopathogenic nematode and the fungus Metarhizium anisopliae CLO 53. Biolcontrol, 39: 453–459. https://doi.org/10.1016/j.biocontrol.2006.07.004
 
Ansari M.A., Tirry L., Moens M. (2005): Antagonism between entomopathogenic fungi and bacterial symbionts of entomopathogenic nematodes. Biocontrol, 50: 465–475. https://doi.org/10.1007/s10526-004-5524-4
 
Barbercheck M.E., Kaya H.K. (1990): Interactions between Beauveria bassiana and the entomogenous nematodes, Steinernema feltiae and Heterorhabditis heliothidis. Journal of Invertebrate Pathology, 55: 225–234.  https://doi.org/10.1016/0022-2011(90)90058-E
 
Barelli L., Moonjely S., Behie S.W., Bidochka M.J. (2016): Fungi with multifunctional lifestyles: endophytic insect pathogenic fungi. Plant Molecular Biology, 90: 657–664.  https://doi.org/10.1007/s11103-015-0413-z
 
Bayat F., Mirlohi A., Khodambashi M. (2009): Effects of endophytic fungi on some drought tolerance mechanisms of tall fescue in a hydroponics culture. Russian Journal of Plant Physiology, 56: 510–516.  https://doi.org/10.1134/S1021443709040104
 
Bedding R.A., Akhurst R. (1975): A simple technique for the detection of insect parasitic rhabditid nematodes in soil. Nematologica, 21: 109–110.  https://doi.org/10.1163/187529275X00419
 
Behie S.W., Jones S.J., Bidochka M.J. (2015): Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecology, 13: 112–119.  https://doi.org/10.1016/j.funeco.2014.08.001
 
Benvenuti C., Barzanti G.P., Marianelli L., Sabbatini Peverieri G., Paoli F., Bosio G., Venanzio D., Giacometto E., Roversi P.F. (2019): A new device for auto-disseminating entomopathogenic fungi against Popillia japonica: a study case. Bulletin of Insectology, 72: 219–225.
 
Berry R.E., Liu J., Reed G. (1997): Comparison of endemic and exotic entomopathogenic nematode species for control of Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 90: 1528–1533. https://doi.org/10.1093/jee/90.6.1528
 
Bidochka M.J., Kasperski J.E., Wild G.A.M. (1998): Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats. Canadian Journal of Botany, 76: 1198–1204.  https://doi.org/10.1139/b98-115
 
Borcard D., Gillet F., Legendre P. (2018): Spatial analysis of ecological data. In: Numerical Ecology with R. Use R! Cham, Springer: 299–367.
 
Bouamama N., Vidal C., Fargues J. (2010): Effects of fluctuating moisture and temperature regimes on the persistence of quiescent conidia of Isaria fumosorosea. Journal of Invertebrate Pathology, 105: 139–144. https://doi.org/10.1016/j.jip.2010.05.014
 
Branine M., Bazzicalupo A., Branco S. (2019): Biology and applications of endophytic insect-pathogenic fungi. PLoS Pathogens, 15(7): e1007831. doi:10.1371/journal.ppat.1007831 https://doi.org/10.1371/journal.ppat.1007831
 
Bruck D.J., Lewis L.C. (2002): Rainfall and crop residue effects on soil dispersion and Beauveria bassiana spread to corn. Applied Soil Ecology, 20: 183–190.  https://doi.org/10.1016/S0929-1393(02)00022-7
 
Chandler D. (2009): Understanding the evolution and function of entomopathogenic fungi. Avalilable at http://www2.warwick.ac.uk/fac/sci/lifesci/research/entomopathogenicfungi/understanding_the_evolution_and_function_of_entomopathogenic_fungi.pdf
 
Chandler D., Hay D., Reid A.P. (1997): Sampling and occurrence of entomopathogenic fungi and nematodes in UK soils. Applied Soil Ecology, 5: 133–141.  https://doi.org/10.1016/S0929-1393(96)00144-8
 
Clifton E.H., Jaronski S.T., Hodgson E.W., Gassmann A.J. (2015): Abundance of soilborne entomopathogenic fungi in organic and conventional fields in the Midwestern USA with an emphasis on the effect of herbicides and fungicides on fungal persistence. PLoS ONE, 10(7): e0133613. doi:10.1371/journal.pone.0133613 https://doi.org/10.1371/journal.pone.0133613
 
Cruz-Martínez H., Ruiz-Vega J., Matadamas-Ortíz P.T., Cortés-Martínez C.I., Rosas-Diaz, J. (2017): Formulation of entomopathogenic nematodes for crop pest control –
 
a review. Plant Protection Science, 53: 15–24.
 
Cuthbertson A.G.S., Walters K.F.A., Northing P., Luo W. (2007): Efficacy of the entomopathogenic nematode, Steinernema feltiae, against sweetpotato whitefly Bemisia tabaci (Homoptera: Aleyrodidae) under laboratory and glasshouse conditions. Bulletin of Entomological Research, 97: 9–14. https://doi.org/10.1017/S0007485307004701
 
De Nardo E.A.B., Grewal P.S. (2003): Compatibility of Steinernema feltiae (Nematoda: Steinernematidae) with pesticides and plant growth regulators used in glasshouse plant production. Biocontrol Science and Technology, 13: 441–448. https://doi.org/10.1080/0958315031000124495
 
Dzięgielewska M. (2012): Occurrence of entomopathogenic nematodes of the family Steinernematidae and Heterorhabditidae in orchards chemically protected and unprotected. Progress in Plant Protection, 52: 415–420.
 
Dzięgielewska M., Erlichowski T. (2011): Entomopathogenic nematodes (Steinernematidae, Heterorhabditidae) and larvae of Elateridae aggregations in various agrocenosis. Progress in Plant Protection, 51: 1750–1756.
 
Dzięgielewska M., Skwiercz A. (2018): The influence of selected abiotic factors on the occurrence of entomopathogenic nematodes (Steinernematidae, Heterorhabditidae) in soil. Polish Journal of Soil Science, 51: 11–21.  https://doi.org/10.17951/pjss.2018.51.1.11
 
Ehlers R.V., Sulistyanto D., Marini J. (1996): Control of scarabaeid larvae in golf course turf with Heterorhabditis megidis and H. bacteriophora. In: Smits P.H. (ed.): IOBC/WPRS Bulletin, 19: 84–85.
 
Eilenberg J., Hajek A., Lomer C. (2001): Suggestions for unifying the terminology in biological control. Biocontrol, 46: 387–400.  https://doi.org/10.1023/A:1014193329979
 
El-Borai F.E., Campos-Herrera R., Stuart R.J., Duncan L.W. (2011): Substrate modulation, group effects and the behavioral responses of entomopathogenic nematodes to nematophagous fungi. Journal of Invertebrate Pathology, 106: 347–356.  https://doi.org/10.1016/j.jip.2010.12.001
 
Fisher J.J., Rehner S.S, Bruck D.J. (2011): Diversity of rhizosphere associated entomopathogenic fungi of perennial herbs, shrubs and coniferous trees. Journal of Intervebrate Pathology, 106: 289–295. https://doi.org/10.1016/j.jip.2010.11.001
 
Gürlek S., Sevim A., Sezgin F.M., Sevim E. (2018): Isolation and characterization of Beauveria and Metarhizium spp. from walnut fields and their pathogenicity against the codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae). Egyptian Journal of Biological Pest Control, 28: 50. doi:10.1186/s41938-018-0055-y https://doi.org/10.1186/s41938-018-0055-y
 
Helmberger M.S., Shields E.J., Wickings K.G. (2017): Ecology of belowground biological control: Entomopathogenic nematode interactions with soil biota. Applied Soil Ecology, 121: 201–213.  https://doi.org/10.1016/j.apsoil.2017.10.013
 
Hominick W.M., Briscoe B.R., Pino F.G., Heng J., Hunt D.J., Kozodoy E., Mráček Z., Nguyen K.B., Reid A.P., Spiridonov S., Stock P., Sturhan D., Waturu C., Yoshida M. (1997): Biosystematics of entomopathogenic nematodes: current status, protocols and definitions. Journal of Helminthology, 71: 271–298.  https://doi.org/10.1017/S0022149X00016096
 
Hominick W.M., Reid A.P., Briscoe B.R. (1995): Prevalence and habitat specificity of steinernematid and heterorhabditid nematodes isolated during soil surveys of the UK and the Netherlands. Journal of Helminthology, 69: 27–32. https://doi.org/10.1017/S0022149X00013791
 
Humber R.A. (2012): Identification of entomopathogenic fungi. In: Lacey L.A. (ed.): Manual of techniques in invertebrate pathology. Cambridge, Academic Press: 151–182.
 
Hunt D. (2007): Introduction. In: Nguyen K.B., Hunt D.J. (eds): Entomopathogenic nematode: systematics, phylogeny and bactrial symbionts. Nematology Monographs and Perspectives, Vol 5. Leiden-Boston, Brill: 611–692.
 
IUSS Working Group WRB (2015): World Reference Base for soil resources 2014. International soil classification system for naming soils and creating legends for soil maps. Update 2015. World Soil Resources Report No. 106. Rome, FAO: 203.
 
Jaber L.R., Ownley B.H. (2018): Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biological Control, 116: 36–45. https://doi.org/10.1016/j.biocontrol.2017.01.018
 
Jagodič A., Trdan S., Laznik Ž. (2019): Entomopathogenic nematodes: can we use the current knowledge on belowground multitrophic interactions in future plant protection programmes? – Review. Plant Protection Science, 55: 243–254.  https://doi.org/10.17221/24/2019-PPS
 
Jarmuł-Pietraszczyk J., Kamionek M., Kania I. (2011): Occurrence of entomopathogenic fungi in selected parks and urban forests of the Warsaw District Ursynow. Ecological Chemistry and Engineering A, 18: 1571–1574.
 
Johansson M., Stenberg B., Torstensson L. (1999): Microbiological and chemical changes in two arable soils after long-term sludge amendments. Biology and Fertility Soils, 30: 160–167.  https://doi.org/10.1007/s003740050603
 
Johnson S.N., Benefer C.M., Frew A., Griffiths B.S., Hartley S.E., Karley A.J., Rasmann S., Schumann M., Sonnemann I., Robert C.A. (2016): New frontiers in belowground ecology for plant protection from root-feeding insects. Applied Soil Ecology, 108: 96–107. https://doi.org/10.1016/j.apsoil.2016.07.017
 
Kaya H.A, Stock S.P. (1997): Techniques in insect nematology. In: Lacey L.A. (ed.): Manual of Techniques in Insect Pathology. San Diego, Academic Press: 281–324.
 
Kepler R.M., Ugine T.A., Maul J.E., Cavigelli M.A., Rehner S.A. (2015): Community composition and population genetics of insect pathogenic fungi in the genus Metarhizium from soils of a long-term agricultural research system. Environmental Microbiology, 17: 2791–2804. https://doi.org/10.1111/1462-2920.12778
 
Kergunteuil A., Bakhtiari M., Formenti L., Xiao Z., Defossez E., Rasmann S. (2016): Biological control beneath the feet: A review of crop protection against insect root herbivores. Insects 7 (4): 70. doi:10.3390/insects7040070 https://doi.org/10.3390/insects7040070
 
Kessler P., Matzke H., Keller S. (2003): The effect of application time and soil factors on the occurrence of Beauveria brongniartii applied as a biological control agent in soil. Journal of Invertebrate Pathology, 84: 15–23.  https://doi.org/10.1016/j.jip.2003.08.003
 
Keyser C.A., Thorup-Kristensen K., Meyling N.V. (2014): Metarhizium seed treatment mediates fungal dispersal via roots and induces infections in insects. Fungal Ecology, 11: 122–131.  https://doi.org/10.1016/j.funeco.2014.05.005
 
Klingen I., Eilenberg J., Meadow R. (2002): Effects of farming system, field margins and bait insect on the occurrence of insect pathogenic fungi in soils. Agriculture, Ecosystems and Environment, 91: 191–198.  https://doi.org/10.1016/S0167-8809(01)00227-4
 
Kolczarek R., Jankowski K. (2014): Occurrence of entomopathogenic fungi in soils from Festuca pratensis Huds. crop. Journal of Ecological Engineering, 15: 73–77.
 
Koppenhöfer A.M, Fuzy E.M. (2008): Attraction of four entomopathogenic nematodes to four white grub species. Journal of Invertebrate Pathology, 99: 227–234.  https://doi.org/10.1016/j.jip.2008.05.003
 
Koppenhöfer A.M., Fuzy E.M. (2004): Effect of white grub developmental stage on susceptibility to entomopathogenic nematodes. Journal of Economic Entomology, 97: 1842–1849. https://doi.org/10.1603/0022-0493-97.6.1842
 
Krebs C.J. (2009): Ecology: The Experimental Analysis of Distribution and Abundance. 6th Ed. San Francisco, Benjamin Cummings.
 
Kreft A., Skrzypek H. (2002): Insect infection by entomogenous nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in conditions of competition. Annales Universitatis Mariae Curie-Skłodowska Lublin – Polonia, Sectio C, 57: 39–52.
 
Kruitbos L.M., Heritage S., Hapca S., Wilson M.J. (2010): The influence of habitat quality on the foraging strategies of the entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis megidis. Parasitology, 137: 303–309.  https://doi.org/10.1017/S0031182009991326
 
Kuhar T., Speese J., Whalen J., Alvares J., Alokhin A., Ghidiu G., Spellman M. (2003): Current status of insecticidal control of wireworms in potatoes. Pesticide Outlook, 14: 265–267.  https://doi.org/10.1039/b314851n
 
Kuhlmann U., Burgt W.A.C.M. (1998): Possibilities for biological control of the western corn rootworm, Diabrotica virgifera virgifera LeConte, in Central Europe. Biocontrol News and Information, 19: 59–68.
 
Kukla J., Whitfeld T., Cajthaml T., Baldrian P., Veselá-Šimáčková H., Novotný V., Frouz J. (2019): The effect of traditional slash-and-burn agriculture on soil organic matter, nutrient content, and microbiota in tropical ecosystems of Papua New Guinea. Land Degradation & Development, 30: 166–177.
 
Lacey L.A., Shapiro-Ilan D.I. (2008): Microbial control of insect pests in temperate orchard systems: potential for incorporation into IPM. Annual Review of Entomology, 53: 121–144.  https://doi.org/10.1146/annurev.ento.53.103106.093419
 
Lacey L.A., Grzywacz D., Shapiro-Ilan D.I., Frutos R., Brownbridge M., Goettel M.S. (2015): Insect pathogens as biological control agents: back to the future. Journal of Invertebrate Pathology, 132: 1–41. https://doi.org/10.1016/j.jip.2015.07.009
 
Labaude S., Griffin Ch.T. (2018): Transmission success of entomopathogenic nematodes used in pest control – https://doi.org/10.3390/insects9020072
 
a review. Insects, 9 (2): 72. doi:10.3390/insects9020072.  https://doi.org/10.3390/insects9020072
 
Leite L., Shapiro Ilan D.I., Hazir S. (2018): Survival of Steinernema feltiae in different formulation substrates: improved longevity in a mixture of gel and vermiculite. Biological Control, 126: 192–197. https://doi.org/10.1016/j.biocontrol.2018.05.013
 
Liao X., O’Brien T.R., Fang W., St. Leger R.J. (2014): The plant beneficial effects of Metarhizium species correlate with their association with roots. Applid Microbiology and Biotechnology, 98: 7089–7096. https://doi.org/10.1007/s00253-014-5788-2
 
Mäder P., Fliessbach A., Dubois D., Gunst L., Fried P., Niggli U. (2002): Soil fertility and biodiversity in organic farming. Science, 296: 1694–1697.  https://doi.org/10.1126/science.1071148
 
Magdoff F. (2001): Concept, components, and strategies of soil health in agroecosystems. Journal of Nematology, 33: 169–172.
 
Medo J., Cagáň L. (2011): Factors affecting the occurrence of entomopathogenic fungi in soils of Slovakia as revealed using two methods. Biological Control, 59: 200–208.  https://doi.org/10.1016/j.biocontrol.2011.07.020
 
Meng X., Hu J., Ouyang G. (2017): The isolation and identification of pathogenic fungi from Tessaratoma papillosa Drury (Hemiptera: Tessaratomidae). PeerJ, 5: e3888. doi: 10.7717/peerj.3888 https://doi.org/10.7717/peerj.3888
 
Meyling N.V., Eilenberg J. (2006): Occurrence and distribution of soil borne entomopathogenic fungi within a single organic agroecosystem. Agriculture, Ecosystems and Environment, 113: 336–341.  https://doi.org/10.1016/j.agee.2005.10.011
 
Miętkiewski R., Żurek M., Tkaczuk C., Bałazy S. (1991): Occurrence of entomopathogenic fungi in arable soil, forest soil and litter. Roczniki Nauk Rolniczych, 21: 61–68.
 
Morton A., Garcia-del-Pino F. (2017): Laboratory and field evaluation of entomopathogenic nematodes for control of Agriotes obscurus (L.) (Coleoptera: Elateridae). Journal of Applied Entomology, 141: 241–246.  https://doi.org/10.1111/jen.12343
 
Mráček Z. (1980): The use of Galleria traps for obtaining nematode parasites of insects in Czechoslovakia (Lepidoptera: Nematoda, Steinernematidae). Acta Entomologica Bohemoslovaca, 77: 378–382.
 
Mráček Z., Bečvář S. (2000): Insect aggregations and entomopathogenic nematode occurrence. Nematology, 2: 297–301.  https://doi.org/10.1163/156854100509169
 
Mráček Z., Bečvář S., Kindlmann P. (1999): Survey of entomopathogenic nematodes from the families (Nematoda: Rhabditida) in the Czech Republic. Folia Parasitologica, 46: 145–148.
 
Mráček Z., Bečvář S., Kindlmann P., Jersáková J. (2005): Habitat preference for entomopathogenic nematodes, their insect hosts and new faunistic records for the Czech Republic. Biological Control, 34: 27–37.  https://doi.org/10.1016/j.biocontrol.2005.03.023
 
Mudrončeková S., Mazáň M., Nemčovič M., Šalamon I. (2013): Entomopathogenic fungus species Beauveria bassiana (Bals.) and Metarhizium anisopliae (Metsch.) used as mycoinsecticide effective in biological control of Ips typographus (L.). Journal of Microbiology, Biotechnology and Food Sciences, 2: 2469–2472.
 
Nannipieri P., Ascher J., Ceccherini M.T., Landi L., Pietramellara G., Renella G. (2003): Microbial diversity and soil functions. European Journal of Soil Science, 54: 655–670.  https://doi.org/10.1046/j.1351-0754.2003.0556.x
 
Nelly N., Syahrawati M.Y., Hamid H., Habazar T., Gusnia D.N. (2019): Diversity and characterization of entomopathogenic fungi from rhizosphere of maize plants as potential biological control agents. Biodiversitas, 20: 1435–1441.  https://doi.org/10.13057/biodiv/d200536
 
Nguyen K.B. (2007): Methodology, morphology and identification. In: Nguyen K.B., D.J. Hunt (eds): Entomopathogenic Nematode: Systematics, Phylogeny and Bacterial Symbionts, 5. Nematology Monographs and Perspectives. Brill, Leiden: 59–119.
 
Nishi O., Iiyama K., Yasunaga-Aoki C., Shimizu S. (2013): Comparison of the germination rates of Metarhizium spp. conidia from Japan at high and low temperatures. Letters in Applied Microbiology, 57: 554–560. https://doi.org/10.1111/lam.12150
 
Nishi O., Iiyama K., Yasunaga-Aoki C., Shimizu S. (2017): Species associations and distributions of soil entomopathogenic fungi Metarhizium spp. in Japan. Mycology, 8: 308–317.  https://doi.org/10.1080/21501203.2017.1386244
 
Nishi O., Sato H. (2019): Isolation of Metarhizium spp. from rhizosphere soils of wild plants reflects fungal diversity in soil but not plant specificity. Mycology, 10: 22–31. https://doi.org/10.1080/21501203.2018.1524799
 
Popowska-Nowak E., Skrzecz I., Tumialis D., Pezowicz E., Samborska I., Góral K. (2016): Entomopathogenic fungi in the soils of forest plantations: towards the control of large pine weevil, Hylobius abietis. Baltic Forestry, 22: 8–15.
 
Půža V. (2015): Control of insect pests by entomopathogenic nematodes. In: Lugtenberg B. (ed.): Principles of Plant-Microbe Interactions. Cham, Springer Internationa Publishing AG: 175–183.
 
Půža V., Mráček Z., Nermu J. (2016): Novelties in pest control by entomopathogenic and mollusc-parasitic nematodes. In: Gill HK, Goyal G (eds): Integrated pest management (IPM): environmentally sound pest management. Intech Open: 71–102.
 
Quesada-Moraga E., Navas-Cortés J.A., Maranhao E.A.A., Ortiz-Urquiza A., Santiago-Álvarez C. (2007): Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils. Mycological Research, 111: 947–966. https://doi.org/10.1016/j.mycres.2007.06.006
 
Ramos Y., Portal O., Lysøe E., Meyling N.V., Klingen I. (2017): Diversity and abundance of Beauveria bassiana in soils, stink bugs and plant tissues of common bean from organic and conventional fields. Journal of Invertebrate Pathology, 150: 114–120.  https://doi.org/10.1016/j.jip.2017.10.003
 
Rasmann S., Turlings T.C.J. (2016): Root signals that mediate mutualistic interactions in the rhizosphere. Current Opinion in Plant Biology, 32: 62–68.  https://doi.org/10.1016/j.pbi.2016.06.017
 
Raya-Díaz S., Sánchez-Rodríguez A.R., Segura-Fernández J.M., del Campillo M.dC., Quesada-Moraga E. (2017): Entomopathogenic fungi-based mechanisms for improved Fe nutrition in sorghum plants grown on calcareous substrates. PLoS ONE, 12(10): e0185903. doi:10.1371/journal.pone.0185903 https://doi.org/10.1371/journal.pone.0185903
 
Rostislav Z., Konopická J., Půža V., Bohatá A., Hussein H. M., Habuštová O.S. (2017): Microbial and nematode control of the Colorado potato beetle. microbial and nematode control of invertebrate pests IOBC-WPRS Bulletin, 129: 157–161.
 
Sánchez-Rodríguez A.R., Barrón V., del Campillo M.C., Quesada-Moraga E. (2016): The entomopathogenic fungus Metarhizium brunneum: a tool for alleviating Fe chlorosis. Plant Soil, 406: 1–17. https://doi.org/10.1007/s11104-016-2887-0
 
Sasan R., Bidochka M. (2012): The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. American Journal of Botany, 99: 101–107.  https://doi.org/10.3732/ajb.1100136
 
Sevim A., Höfte M., Demirbağ Z. (2012): Genetic variability of Beauveria bassiana and Metarhizium anisopliae var. anisopliae isolates obtained from the Eastern Black Sea Region of Turkey. Turkish Journal of Biology, 36: 255–265.
 
Shapiro-Ilan D.I., Bruck D.J., Lacey L.A. (2012): Principles of epizootiology and microbialcontrol. In: Vega F.E., Kaya H.K. (eds): Insect Pathology, 2nd Ed. San Diego, Academic Press: 29–72.
 
Shapiro-Ilan D.I., Lewis E.E., Schliekelman P. (2014): Aggregative group behavior in insect parasitic nematode dispersal. International Journal of Parasitology, 44: 49–54.  https://doi.org/10.1016/j.ijpara.2013.10.002
 
Shapiro-Ilan D.I., Hazir S., Glazer I. (2017): Basic and applied research: entomopathogenic nematodes. In: Lacey L.A. (ed.): Microbial agents for control of insect pests: from discovery to commercial development and use. Amsterdam, Academic Press: 91–105.
 
Siebielec G., Smreczak B., Klimkowicz-Pawlas A., Kowalik M., Kaczyński R., Koza P., Ukalska-Jaruga A., Łysiak M., Wójtowicz U., Poręba L., Chabros E. (2017): Raport z III etapu realizacji zamówienia „Monitoring chemizmu gleb ornych w Polsce w latach 2015–2017”. Instytut Uprawy Nawożenia i Gleboznawstwa Państwowy Instytut Badawczy w Puławach: 190.
 
St. Leger R.J. (2008): Studies on adaptations of Metarhizium anisopliae to life in the soil. Journal of Invertebrate Pathology, 98: 271–276. https://doi.org/10.1016/j.jip.2008.01.007
 
Steinwender B.M., Enkerli J., Widmer F., Eilenberg J., Kristensen H.L., Bidochka M.J., Meyling N.V. 2015. Root isolations of Metarhizium spp. from crops reflect diversity in the soil and indicate no plant specificity. Journal of Invertebrate Pathology, 132: 142–148.  https://doi.org/10.1016/j.jip.2015.09.007
 
Stuart R.J, Barbercheck M.E., Parwinder S.G., Taylor R.A.J., Hoy C.W. (2006): Population biology of entomopathogenic nematodes: concepts, issues and models. Biological Control, 38: 80–102.  https://doi.org/10.1016/j.biocontrol.2005.09.019
 
Sturhan D. (1999): Prevalence and habitat specificity of entomopathogenic nematodes in Germany. In: Gwynn R.L., Smith P.H., Griffin C., Ehlers R.-U., Boemare N., Masson J.P. (eds): Entomopathogenic Nematodes: Aplication and Persistence of Entomopathogenic Nematodes. Proceeding of COST 819 Workshop, May 16–20, 1995, Todi, Italy: 123–132.
 
Sun B-D., Yu H., Chen A.J., Liu X-Z. (2008): Insect-associated fungi in soils of field crops and orchards. Crop Protection, 27: 1421–1426.  https://doi.org/10.1016/j.cropro.2008.07.010
 
Thiele-Bruhn S., Bloem J., de Vries F.T., Kalbitz K., Wagg C. (2012): Linking soil biodiversity and agricultural soil management. Current Opinion in Environmental Sustainability, 4: 523–528.  https://doi.org/10.1016/j.cosust.2012.06.004
 
Tkaczuk C., Król A., Majchrowska-Safaryan A., Nicewicz Ł. (2014): The occurrence of entomopathogenic fungi in soils from fields cultivated in a conventional and organic system. Journal of Ecological Engineering, 15: 137–144.
 
Tkaczuk C., Krzyczkowski T., Wegensteiner R. (2012): The occurrence of entomopathogenic fungi in soils from mid-field woodlots and adjacent small-scale arable fields. Acta Mycologica, 47: 191–202.  https://doi.org/10.5586/am.2012.024
 
Tkaczuk C., Renella G. (2003): Occurrence of entomopathogenic fungi in soils from Central Italy under different management. IOBC/WPRS Bulletin, 26: 85–89.
 
Toba H., Lindgren J., Turner J., Vail P. (1983): Susceptibility of the Colorado beetle and wireworms to Steinernema feltiae and S. glaseri. Journal of Invertebrate Pathology, 15: 597–601.
 
Trizelia Armon N., Jailani H. (2015): Keanekaragaman cendawan entomopatogen pada rizosfer berbagai tanaman sayuran (The diversity of entomopathogenic fungi on rhizosphere of various vegetable crops). Prosiding Seminar Nasional Masyarakat Biodiversitas Indonesia, 1: 998–1004.
 
Ulu T.C., Sadic B., Slsurluk I.A., Alsit T. (2015): Virulence of four entomopathogenic nematode species for plum sawfly, Hoplocampa flava L. (Hymenoptera: Tenthredinidae). Invertebrate Survival Journal, 12: 274–277.
 
Uzman D., Pliester J., Leyer I., Entling M.H., Reineke A. (2019): Drivers of entomopathogenic fungi presence in organic and conventional vineyard soils. Applied Soil Ecology, 133: 89–97.  https://doi.org/10.1016/j.apsoil.2018.09.004
 
Vega F.E. (2008): Insect pathology and fungal endophytes. Journal of Invertebrate Pathology, 98: 277–279. https://doi.org/10.1016/j.jip.2008.01.008
 
Vega F.E., Goettel M.S., Blackwell M.S., Chandler D., Jackson M.A., Keller S., Koike M., Maniania N.K., Monzon A., Ownley B.H., Pell J.K., Rangel D.E.N., Roy H.E. (2009): Fungal entomopathogens: new insights on their ecology. Fungal Ecology, 2: 149–159.  https://doi.org/10.1016/j.funeco.2009.05.001
 
Webster R. (2007): Analysis of variance, inference, multiple comparisons and sampling effects in soil research. European Journal of Soil Science, 58: 74–82.  https://doi.org/10.1111/j.1365-2389.2006.00801.x
 
White G.F. (1927): A method for obtaining infective nematode larvae from cultures. Since, 66: 302–303.  https://doi.org/10.1126/science.66.1709.302-a
 
Wu S., Youngman R.R., Kok L.T., Laub C.A., Pfeiffer D.G. (2014): 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. Biological Control, 76: 65–73.  https://doi.org/10.1016/j.biocontrol.2014.05.002
 
Wyrebek M., Huber C., Sasan R.K., Bidochka M.J. (2011): Three sympatrically occurring species of Metarhizium show plant rhizosphere specificity. Microbiology, 157: 2904–2911.  https://doi.org/10.1099/mic.0.051102-0
 
Zimmermann G. (1986): The 'Galleria bait method' for detection of entomopathogenic fungi in soil. Journal of Applied Entomology, 102: 213–215. https://doi.org/10.1111/j.1439-0418.1986.tb00912.x
 
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