Improvement of Soilborne Pests Control with Agronomical Practices Exploiting the Interaction of Entomophagous Fungi

  • E. MalusáEmail author
  • L. Canfora
  • F. Pinzari
  • M. Tartanus
  • B. H. Łabanowska


The application of biological control agents (BCAs) is considered as an effective alternative for pest control. However, factors such as the formulation of the product, whose quality can affect the inoculant viability and persistence in soil, the stabilisation of the biocontrol effect under field conditions and the influence of agronomical practices as well as of the environmental conditions (weather and soil) are hampering a wider use of BCAs. After a brief review of these factors, we present some results concerning agronomical and ecological aspects from a case study carried out using different entomopathogenic fungi on organic strawberry plantations, which underline the possibility of improving BCAs efficacy, particularly when integrated into a more general strategy of pest control.


Biocontrol Pests Entomophagous fungi Soilborne Agronomy 



The work was supported by a grant from the Polish Ministry of Agriculture and Rural Development ‘Organic fruit production – Definition of good practices of plant protection against pests and diseases in organic crops’, nr. HORre-029-31-29/14(103).


  1. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512. doi: 10.1074/jbc.M112.433300 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bale JS, van Lenteren JC, Bigler F (2008) Biological control and sustainable food production. Phil Trans R Soc B 363:761–776. doi: 10.1098/rstb.2007.2182 CrossRefPubMedGoogle Scholar
  3. Baverstock J, Roy HE, Pell JK (2010) Entomopathogenic fungi and insect behaviour: from unsuspecting hosts to targeted vectors. Bio Control 55:89–102. doi: 10.1007/s10526-009-9238-5 Google Scholar
  4. Berg G, Zachow C, Müller H, Philipps J, Tilcher R (2013) Next-generation bio-products sowing the seeds of success for sustainable agriculture. Agronomy 3:648–656. doi: 10.3390/agronomy3040648 CrossRefGoogle Scholar
  5. Bochner BR (2011) Phenomics and phenotype microarrays: applications complementing metagenomics. In: de Bruijn FJ (ed) Handbook of molecular microbial ecology I: metagenomics and complementary approaches. Wiley, Hoboken, pp 533–540CrossRefGoogle Scholar
  6. Boldo JT, Junges A, Amaral KB, Staats CC, Vainstein MH, Schrank A (2009) Endochitinase CHI2 of the biocontrol fungus Metarhizium anisopliae affects its virulence toward the cotton stainer bug Dysdercus peruvianus. Curr Genet 55:551–560CrossRefPubMedGoogle Scholar
  7. Bordenstein SR, Theis KR (2015) Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13(8):e1002226. doi: 10.1371/journal.pbio.1002226 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Borglin S, Joyner D, DeAngelis KM, Khudyakov J, D’Haeseleer P, Joachimiak MP, Hazen T (2012) Application of phenotypic microarrays to environmental microbiology. Curr Opin Biotechnol 23:41–48CrossRefPubMedGoogle Scholar
  9. Bruck DJ (2010) Fungal entomopathogens in the rhizosphere. BioControl 55:103–112. doi: 10.1007/s10526-009-9236-7 CrossRefGoogle Scholar
  10. Canfora L, Malusà E, Salvati L, Renzi G, Petrarulo M, Benedetti A (2015) Short-term impact of two liquid organic fertilizers on Solanum lycopersicum L. rhizosphere Eubacteria and Archaea diversity. Appl Soil Ecol 88:50–59. doi: 10.1016/j.apsoil.2014.11.017 CrossRefGoogle Scholar
  11. Canfora L, Malusà E, Tkaczuk C, Tartanus M, Łabanowska BH, Pinzari F (2016) Development of a method for detection and quantification of B. brongniartii and B. bassiana in soil. Sci Rep 6:22933. doi: 10.1038/srep22933 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chandler D, Heale JB, Gillespie AT (1993) Competitive interaction between strains of Verticillium lecanii on two insect hosts. Ann Appl Biol 122:435–440CrossRefGoogle Scholar
  13. Cory JS, Ericsson JD (2010) Fungal entomopathogens in a tritrophic context. BioControl 55:75–88. doi: 10.1007/s10526-009-9247-4 CrossRefGoogle Scholar
  14. de Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256CrossRefGoogle Scholar
  15. De Hoog GS (1972) The genera Beauveria, Isaria, Tritirachium and Acrodontium gen. nov. Stud Mycol 1:1–41Google Scholar
  16. DeBach P (1964) Biological control of insect pests and weeds. Chapman &Hall, LondonGoogle Scholar
  17. Dolci P, Guglielmo F, Secchi F, Ozino OI (2006) Persistence and efficacy of Beauveria brongniartii strains applied as biocontrol agents against Melolontha melolontha in the Valley of Aosta (northwest Italy). J Appl Microbiol 100:1063–1072. doi: 10.1111/j.1365-2672.2006.02808.x CrossRefPubMedGoogle Scholar
  18. Engel P, Moran NA (2013) The gut microbiota of insects – diversity in structure and function. FEMS Microbiol Rev 37:699–735. doi: 10.1111/1574-6976.12025 CrossRefPubMedGoogle Scholar
  19. Fan Y, Fang W, Guo S, Pei X, Zhang Y, Xiao Y, Li D, Jin K, Bidochka MJ, Pei Y (2007) Increased insect virulence in Beauveria bassiana strains overexpressing an engineered chitinase. Appl Environ Microbiol 73:295–302CrossRefPubMedGoogle Scholar
  20. Fang W, Leng B, Xiao Y, Jin K, Ma J, Fan Y, Feng J, Yang X, Zhang Y, Pei Y (2005) Cloning of Beauveria bassiana gene Bbchit1 and its application to improve fungal strain virulence. Appl Environ Microbiol 71:363–370CrossRefPubMedPubMedCentralGoogle Scholar
  21. Ghikas DV, Kouvelis VN, Typas MA (2010) Phylogenetic and biogeographic implications inferred by mitochondrial intergenic region analyses and ITS1-5.8S-ITS2 of the entomopathogenic fungi Beauveria bassiana and B. brongniartii. BMC Microbiol 10:174CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gupta SC, Leathers TD, El-Sayed GN, Ignoffo CM (1994) Relationships among enzyme activities and virulence parameters in Beauveria bassiana infections of Galleria mellonella and Trichoplusia ni. J Invertebr Pathol 64:13–17CrossRefGoogle Scholar
  23. Hallsworth JE, Magan N (1994) Effect of carbohydrate type and concentration on polyols and trehalose in conidia of three entomopathogenic fungi. Microbiol-SGM 140:2705–2713CrossRefGoogle Scholar
  24. Hirsch PR, Mauchline TH, Clark IM (2010) Culture independent molecular techniques for soil microbial ecology. Soil Biol Biochem 42(6):878–887CrossRefGoogle Scholar
  25. Hirsh J, Galidevara S, Strohmeier S, Devi KU, Reineke A (2013) Effects on diversity of soil fungal community and fate of an artificially applied Beauveria bassiana strain assessed through pyrosequencing. Microb Ecol 66:608–620CrossRefGoogle Scholar
  26. Hsiao WF, Khachatourians GG (1997) The role of extracellular enzymes in the virulence of the entomopathogenic fungus, Verticillium lecanii, to oat-bird cherry aphid, Ropalosiphum padi (Homoptera: Aphididae). Chin J Entomol 17:227–236Google Scholar
  27. Inglis GD, Johnson DL, Cheng KJ, Goettel MS (1997) Use of pathogen combinations to overcome constraints of temperature on entomopathogenic Hyphomycetes against grasshoppers. Biol Control 8:143–152CrossRefGoogle Scholar
  28. Inglis GD, Duke GM, Kawchuk LM, Goettel MS (1999) Influence of oscillating temperatures on the competitive infection and colonization of the migratory grasshopper by Beauveria bassiana and Metarhizium flavoviride. BioControl 14:111–120Google Scholar
  29. Jaber LR, Enkerli J (2016) Fungal entomopathogens as endophytes: can they promote plant growth? Biocontrol Sci Tech. doi: 10.1080/09583157.2016.1243227
  30. Jackson MA, Dunlap CA, Jaronski ST (2010) Ecological considerations in producing and formulating fungal entomopathogens for use in insect biocontrol. BioControl 55:129–145. doi: 10.1007/s10526-009-9240-y CrossRefGoogle Scholar
  31. Jaronski ST (2007) Soil ecology of the entomopathogenic ascomycetes: a critical examination of what we (think) we know. In: Maniana K, Ekesi S (eds) Use of entomopathogenic fungi in biological pest management. Research Sign Posts, Trivandrum, pp 91–144Google Scholar
  32. Jaronski ST (2010) Ecological factors in the inundative use of fungal entomopathogens. BioControl 55:159–185. doi: 10.1007/s10526-009-9248-3 CrossRefGoogle Scholar
  33. Kabaluk T, Goettel M, Ericsson J, Erlandson M, Vernon B, Jaronski ST, Mackenzie K, Cosgrove L (2007) Promise versus performance: working toward the use of Metarhizium anisopliae as a biological control for wireworms. Bull IOBC/WPRS 30(7):69–76Google Scholar
  34. Kim JJ, Xie L, Han JH, Lee SY (2014) Influence of additives on the yield and pathogenicity of conidia produced by solid state cultivation of an Isaria javanica isolate. Mycobiology 42(4):346–352. doi: 10.5941/MYCO.2014.42.4.346 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Łabanowska BH, Bednarek H (2011) Efficacy of Beauveria brongniartii as Melocont in the control of the European cockchafer (Melolontha melolontha). IOBC/wprs Bull 66:179–182Google Scholar
  36. Łabanowska BH, Olszak RW (2003) The soil pests and their chemical and biological control on strawberry plantations in Poland. IOBC wprs Bull 26(2):93–99Google Scholar
  37. Li DC (2006) Review of fungal chitinases. Mycopathologia 161:345–360CrossRefGoogle Scholar
  38. Loesch A, Hutwimmer S, Strasser H (2010) Carbon utilization pattern as a potential quality control criterion for virulence of Beauveria brongniartii. J Invertebr Pathol 104:58–65Google Scholar
  39. Malusá E, Pinzari F, Canfora L (2016) Efficacy of biofertilizers: challenges to improve crop production. In: Singh DP, Singh HB, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity – vol. 2: functional applications. Springer, New Delhi, pp 17–40. doi: 10.1007/978-81-322-2644-4_2 CrossRefGoogle Scholar
  40. Mayerhofer J, Enkerli J, Zelger R, Strasser H (2015) Biological control of the European cockchafer: persistence of Beauveria brongniartii after long-term applications in the Euroregion Tyrol. BioControl 60:617–629CrossRefGoogle Scholar
  41. Mazid S, Rajkhowa RC, Kalita JC (2011) A review on the use of biopesticides in insect pest management. Int J Sci Adv Technol 1(7):169–178Google Scholar
  42. Meszka B, Sobiczewski P,. Bryk H, Chałańska A, Ślusarski Cz, Ciesielska J, Malusà E (2014) Effect of active steam disinfection on soil microorganisms and strawberry plants health and yield. In: Proceedings of XVI international conference on organic fruit growing, Hohenheim, Germany, pp 258–259Google Scholar
  43. Miller M, Palojärvi A, Rangger A, Reeslev M, Kjøller A (1998) The use of flurogenic substrates to measure fungal presence and activity in soil. Appl Environ Microbiol 64:613–617PubMedPubMedCentralGoogle Scholar
  44. Pereira RM, Stimac JL, Alves SB (1993) Soil antagonism affecting the dose response of workers of the red imported fire ant, Solenopsis invicta, to Beauveria bassiana conidia. J Invertebr Pathol 61:156–161CrossRefGoogle Scholar
  45. Pinzari F, Ceci A, Abu-Samra N, Canfora L, Maggi O, Persiani AM (2016) Phenotype MicroArray™ system in the study of fungal functional diversity and catabolic versatility. Res Microbiol. ISSN 0923-2508,
  46. Read AF, Taylor LH (2001) The ecology of genetically diverse infections. Science 292:1099–1102CrossRefPubMedGoogle Scholar
  47. Rodrıguez-Gomez D, Loera O, Saucedo-Castaneda G, Viniegra-Gonzalez G (2009) Substrate influence on physiology and virulence of Beauveria bassiana acting on larvae and adults of Tenebrio molitor. World J Microbiol Biotechnol 25:513–518CrossRefGoogle Scholar
  48. Sahai AS, Manocha MS (1993) Chitinases of fungi and plants: their involvement in morphogenesis and host-parasite interaction. FEMS Microbiol Rev 11:317–338CrossRefGoogle Scholar
  49. Schreiter S, Ding GC, Grosch R, Kropf S, Antweiler K, Smalla K (2014) Soil type-dependent effects of a potential biocontrol inoculant on indigenous bacterial communities in the rhizosphere of field-grown lettuce. FEMS Microbiol Ecol 90(3):718–730. doi: 10.1111/1574-6941.12430 CrossRefPubMedGoogle Scholar
  50. Schwarzenbach K, Enkerli J, Widmer F (2009) Effects of biological and chemical insect control agents on fungal community structures in soil microcosms. Appl Soil Ecol 42:54–62CrossRefGoogle Scholar
  51. Schwieger F, Tebbe CC (2000) Effect of field inoculation with Sinorhizobium meliloti L33 on the composition of bacterial communities in rhizospheres of a target plant (Medicago sativa) and a non-target plant (Chenopodium album) – linking of 16S rRNA gene-based single-strand conformation polymorphism community profiles to the diversity of cultivated bacteria. Appl Environ Microbiol 66(8):3556–3565CrossRefPubMedPubMedCentralGoogle Scholar
  52. Seidl V (2008) Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions. Fungal Biol Rev 22:36–42CrossRefGoogle Scholar
  53. Sparling GP (1997) Soil microbial biomass, activity and nutrient cycling as indicators of soil health. In: Pankhurst CE, Double BM, Gupta VVSR (eds) Biological indicators of soil health. CAB International, Wallingford, pp 97–119Google Scholar
  54. Srikanth J, Santhalakshmi G (2012) Effect of media additives on the production of Beauveria brongniartii, an entomopathogenic fungus of Holotrichia serrata. Sugar Tech 14:284–290CrossRefGoogle Scholar
  55. St Leger RJ, Cooper RM, Charnley K (1986) Cuticle-degrading enzymes of entomopathogenic fungi: regulation of production of chitinolytic enzymes. J Gen Microbiol 132:1509–1517Google Scholar
  56. St Leger RJ, Allee LL, May B, Staples RC, Roberts DW (1992) World-wide distribution of genetic variation among isolates of Beauveria spp. Mycol Res 96:1007–1015CrossRefGoogle Scholar
  57. Stern VM, Smith RF, van den Bosch R, Hagen KS (1959) The integration of chemical and biological control of the spotted alfalfa aphid. Integr Control Concept Hilgardia 29:81–101CrossRefGoogle Scholar
  58. Tartanus M, Łabanowska BH, Malusá E Tkaczuk C, Chałanska A (2016) Holistic approach for an effective control of white grub of European cockchafer (Melolontha melolontha) in organic strawberry plantations in Poland. Proceedings of XVII International Conference on Organic Fruit Growing, Hohenheim, Germany, pp 293–294Google Scholar
  59. Tesi R, Gelsomino A, Baldi A, Lenzi A, Peruzzi A (2007) Soil disinfection with steam alone or combined with CaO in a greenhouse radish crop. Adv Hortic Sci 21:75–82Google Scholar
  60. Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. Biomed Res Int 863240.  10.1155/2013/863240
  61. Triolo E, Materazzi A, Luvisi A (2004) Exothermic reactions and steam for the management of soil-borne pathogens: five years of research. Adv Hortic Sci 2:89–94Google Scholar
  62. Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzón A, Ownley BH, Pell JK, Rangel DEN, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159CrossRefGoogle Scholar
  63. Vidal S (2015) Entomopathogenic fungi as endophytes:plant–endophyte–herbivore interactions and prospects for use in biological control. Curr Sci 108:1–9Google Scholar
  64. Watrous J, Roach P, Alexandrov T, Heath BS, Yang JY, Kersten RD, van der Voortg M, Poglianoh K, Grossi H, Raaijmakersg JM, Moorec BS, Laskind J, Bandeirac N, Dorresteina PC (2012) Mass spectral molecular networking of living microbial colonies. PNAS 109:E1743–E1752. doi: 10.1073/pnas.1203689109 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Xu J, Baldwin D, Kindrachuk C, Hegedus DD (2006) Serine proteases and metalloproteases associated with pathogenesis but not host specificity in the Entomophthoralean fungus Zoophthora radicans. Can J Microbiol 52:550–559CrossRefPubMedGoogle Scholar
  66. Yao H, He Z, Wilson Campbell MJCD (2000) Microbial biomass and community structure in a sequence of soils with increasing fertility and changing land use. Microb Ecol 40:223–237PubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • E. Malusá
    • 1
    Email author
  • L. Canfora
    • 2
  • F. Pinzari
    • 2
  • M. Tartanus
    • 1
  • B. H. Łabanowska
    • 1
  1. 1.Research Institute of HorticultureSkierniewicePoland
  2. 2.CREA-Research Center Agriculture and EnvironmentRomeItaly

Personalised recommendations