Possibilities of native endophytic fungi as entomopathogenic biocontrol agents at a local scale: the case of deciduous and non-deciduous Mediterranean forest trees

Álvaro Benito-Delgado , Sergio Diez-Hermano , Julio Javier Diez

Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) : 26

PDF
Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) : 26 DOI: 10.1007/s11676-024-01815-6
Original Paper

Possibilities of native endophytic fungi as entomopathogenic biocontrol agents at a local scale: the case of deciduous and non-deciduous Mediterranean forest trees

Author information +
History +
PDF

Abstract

Tree endophytic fungi play an important role in reducing insect herbivory, either by repelling them or killing them directly. Identifying which fungi show such activity could lead to new environmentally friendly pesticides. In this study, the Mediterranean basin climate conditions are projected to harshen in the next decades, will increase vulnerability of tree species to pest invasions. Endophytic fungi were isolated from wood and leaves of Quercus pyrenaica, Q. ilex and Q. suber and tested for virulence against adults of the mealworm beetle, Tenebrio molitor L. using a direct contact method. Only 3 of 111 sporulating isolates had entomopathogenic activity, all identified as Lecanicillium lecanii. The pathogenicity of L. lecanii on T. molitor resulted in a median lethal time (TL50) of 14–16 d. Compared with commercial products, L. lecanii caused faster insect death than the nematode Steinernema carpocapsae and nuclear polyhedrosis virus (no effect on T. molitor survival), and slower than Beauveria bassiana (TL50 = 5), Beauveria pseudobassiana (TL50 = 8d) and Bacillus thuriengensis (80% mortality first day after inoculation). Mortality was also accelerated under water stress, reducing TL50 by an additional 33%. Remarkably, water stress alone had a comparable effect on mortality to that of L. lecanii isolates. This study confirms T. molitor as a good model insect for pathogenicity testing and agrees with management policies proposed in the EU Green Deal.

Graphical abstract

Cite this article

Download citation ▾
Álvaro Benito-Delgado, Sergio Diez-Hermano, Julio Javier Diez. Possibilities of native endophytic fungi as entomopathogenic biocontrol agents at a local scale: the case of deciduous and non-deciduous Mediterranean forest trees. Journal of Forestry Research, 2025, 36(1): 26 DOI:10.1007/s11676-024-01815-6

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Abalo M, Scorsetti AC, Vianna MF, Russo ML, De Abajo JM, Alberto S. Field evaluation of entomopathogenic fungi formulations against Rachiplusia nu (Lepidoptera: Noctuidae) in soybean crop J Plant Prot Res, 2023, 62(4): 403-410.

[2]

Alali S, Mereghetti V, Faoro F, Bocchi S, Al Azmeh F, Montagna M. Thermotolerant isolates of Beauveria bassiana as potential control agent of insect pest in subtropical climates PLoS ONE, 2019, 14(2): e0211457.

[3]

Alfina T, Haneda NF. Entomopathogenic fungi as biological agents in forest plant pest control: a systematic review IOP Conf Ser: Earth Environ Sci, 2022, 959(1): 012013.

[4]

Arthurs S, Dara SK. Microbial biopesticides for invertebrate pests and their markets in the United States J Invertebr Pathol, 2019, 165: 13-21.

[5]

Bamisile BS, Siddiqui JA, Akutse KS, Ramos Aguila LC, Xu YJ. General limitations to endophytic entomopathogenic fungi use as plant growth promoters, pests and pathogens biocontrol agents Plants (Basel), 2021, 10(10): 2119.

[6]

Busby PE, Ridout M, Newcombe G. Fungal endophytes: modifiers of plant disease Plant Mol Biol, 2016, 90(6): 645-655.

[7]

Cheraghi A, Habibpour B, Mossadegh MS, Sharififard M. Horizontal transmission of the entomopathogen fungus Metarhizium anisopliae in Microcerotermes diversus groups Insects, 2012, 3(3): 709-718.

[8]

Cory JS, Ericsson JD. Fungal entomopathogens in a tritrophic context Biocontrol, 2010, 55(1): 75-88.

[9]

Deruytter D, Coudron CL, Claeys J. The influence of wet feed distribution on the density, growth rate and growth variability of Tenebrio molitor J Insects Food Feed, 2021, 7(2): 141-149.

[10]

Devi KU, Sridevi V, Mohan CM, Padmavathi J. Effect of high temperature and water stress on in vitro germination and growth in isolates of the entomopathogenic fungus Beauveria bassiana (Bals.) Vuillemin J Invertebr Pathol, 2005, 88(3): 181-189.

[11]

Diez-Hermano S, Poveda J, Benito Á, Peix Á, Martín-Pinto P, Diez JJ. Soil mycobiome and forest endophytic fungi: is there a relationship between them? For Ecol Manag, 2024, 562: 121924.

[12]

Dunham B (2015) Products and trends in biopesticides. In: DunhamTrimmer, pp 1–23. https://dunhamtrimmer.com/wp-content/uploads/2015/01/Products-and-Trends.pdf

[13]

Eski A, Murat Gezgin M. Susceptibility of different life stages of Tenebrio molitor (Coleoptera: Tenebrionidae) to indigenous entomopathogenic fungi J Stored Prod Res, 2022, 98: 102008.

[14]

European Council of the European Union (2020) European Green Deal. https://www.consilium.europa.eu/en/policies/green-deal/

[15]

Faye A, Dalpé Y, Ndungu-Magiroi K, Jefwa J, Ndoye I, Diouf M, Lesueur D. Evaluation of commercial arbuscular mycorrhizal inoculants Can J Plant Sci, 2013, 93(6): 1201-1208.

[16]

Ganassi S, Domenico CD, Altomare C, Samuels GJ, Grazioso P, Cillo PD, Pietrantonio L, De Cristofaro A. Potential of fungi of the genus Trichoderma for biocontrol of Philaenus spumarius, the insect vector for the quarantine bacterium Xylella fastidosa Pest Manag Sci, 2023, 79(2): 719-728.

[17]

Ganley RJ, Newcombe G. Fungal endophytes in seeds and needles of Pinus monticola Mycol Res, 2006, 110(Pt 3): 318-327.

[18]

Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts Mol Ecol, 1993, 2(2): 113-118.

[19]

Gómez-Vidal S, Lopez-Llorca LV, Jansson HB, Salinas J. Endophytic colonization of date palm (Phoenix dactylifera L.) leaves by entomopathogenic fungi Micron, 2006, 37(7): 624-632.

[20]

Güerri-Agulló B, Gómez-Vidal S, Asensio L, Barranco P, Lopez-Llorca LV. Infection of the red palm weevil (Rhynchophorus ferrugineus) by the entomopathogenic fungus Beauveria bassiana: a SEM study Microsc Res Tech, 2010, 73(7): 714-725.

[21]

Gurr GM, Reynolds OL, Johnson AC, Desneux N, Zalucki MP, Furlong MJ, Li ZY, Akutse KS, et al. (2018) Landscape ecology and expanding range of biocontrol agent taxa enhance prospects for diamondback moth management. A review. In: Agronomy for sustainable development (Vol. 38, Issue 23). Springer-Verlag France. https://doi.org/10.1007/s13593-018-0500-z

[22]

Hajek AE, Elkinton JS, Witcosky JJ. Introduction and spread of the fungal pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) along the leading edge of gypsy moth (Lepidoptera: Lymantriidae) spread Environ Entomol, 1996, 25(5): 1235-1247.

[23]

Hansen LL, Ramløv H, Westh P. Metabolic activity and water vapour absorption in the mealworm Tenebrio molitor L. (Coleoptera, Tenebrionidae): real-time measurements by two-channel microcalorimetry J Exp Biol, 2004, 207(Pt 3): 545-552.

[24]

Hansen LL, Westh P, Wright JC, Ramløv H. Metabolic changes associated with active water vapour absorption in the mealworm Tenebrio molitor L. (Coleoptera, Tenebrionidae): a microcalorimetric study J Insect Physiol, 2006, 52(3): 291-299.

[25]

Hesketh H, Roy HE, Eilenberg J, Pell JK, Hails RS. Challenges in modelling complexity of fungal entomopathogens in semi-natural populations of insects Biocontrol, 2010, 55(1): 55-73.

[26]

Inglis GD, Enkerli J, Goettel MS (2012) Laboratory techniques used for entomopathogenic fungi. In: Manual of techniques in invertebrate pathology. Academic Press, pp 189–253. https://doi.org/10.1016/b978-0-12-386899-2.00007-5

[27]

Jaber LR, Ownley BH. Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Contr, 2018, 116: 36-45.

[28]

Jamunarani GS, Ramanagouda SH, Venkateshalu B, Jayappa J, Raghavendra G, Rudresh DL, Kulkarni MS, Naika Mahantesha BN, Gopali JB. Isolation and evaluation of indigenous endophytic entomopathogenic fungus, Beauveria bassiana UHSB-END1 (Hypocreales: Cordycipitaceae), against Spodoptera litura Fabricius Egypt J Biol Pest Contr, 2022, 32(1): 120.

[29]

Karaborklu S, Altin N, Karabörklü S, Keskin Y. Native entomopathogenic fungi isolated from Duzce, Turkey and their virulence on the mealworm beetle [Tenebrio molitor L. (Coleoptera: Tenebrionidae)] Philipp Agric Sci, 2019, 102(1): 82-89

[30]

Kassambara A, Kosinski M, Biecek P (2021) survminer: Drawing Survival Curves using ‘ggplot2’. R package version 0.4.9. https://CRAN.R-project.org/package=survminer

[31]

Kim JC, Lee MR, Kim S, Lee SJ, Park SE, Nai YS, Lee GS, Shin TY, Kim JS. Tenebrio molitor-mediated entomopathogenic fungal library construction for pest management J Asia Pac Entomol, 2018, 21(1): 196-204.

[32]

Kim JC, Lee MR, Kim S, Lee SJ, Park SE, Baek S, Gasmi L, Shin TY, Kim JS. Long-term storage stability of Beauveria bassiana ERL836 granules as fungal biopesticide J Asia Pac Entomol, 2019, 22(2): 537-542.

[33]

Kouadio ANMS, Nandjui J, Krou SM, Séry DJM, Nelson PN, Zézé A. A native arbuscular mycorrhizal fungus inoculant outcompetes an exotic commercial species under two contrasting yam field conditions Rhizosphere, 2017, 4: 112-118.

[34]

Koziol L, Schultz PA, Parsons S, Bever JD. Native mycorrhizal fungi improve milkweed growth, latex, and establishment while some commercial fungi may inhibit them Ecosphere, 2022, 13(5): e4052.

[35]

Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS. Insect pathogens as biological control agents: back to the future J Invertebr Pathol, 2015, 132: 1-41.

[36]

Lacey LA (2017) Microbial control of insect and mite pests. From theory to practice LA Lacey (Ed) Amsterdam, Boston. Elsevier/Academic Press

[37]

Lazo J (2018) Application of spatial analysis techniques to conservation and restoration of Mediterranean Quercus under future climate change scenarios. https://doi.org/10.13140/RG.2.2.29801.13921

[38]

Lerche S, Meyer U, Sermann H, Buettner C. Dissemination of the entomopathogenic fungus Verticillium lecanii (Zimmermann) Viégas (Hyphomycetales: Moniliaceae) in a population of Frankliniella occidentalis (pergande, 1895) (Thysanoptera: Thripidae) Commun Agric Appl Biol Sci, 2004, 69(3): 195-200

[39]

Lovett B, St Leger RJ. Genetically engineering better fungal biopesticides Pest Manag Sci, 2018, 74(4): 781-789.

[40]

Maistrou S, Paris V, Jensen AB, Rolff J, Meyling NV, Zanchi C. A constitutively expressed antifungal peptide protects Tenebrio molitor during a natural infection by the entomopathogenic fungus Beauveria bassiana Dev Comp Immunol, 2018, 86: 26-33.

[41]

Mann AJ, Davis TS. Entomopathogenic fungi to control bark beetles: a review of ecological recommendations Pest Manag Sci, 2021, 77(9): 3841-3846.

[42]

Nicoletti R, Becchimanzi A. Endophytism of Lecanicillium and Akanthomyces Agriculture, 2020, 10(6): 205.

[43]

Picciotti U, Dalbon VA, Ciancio A, Colagiero M, Cozzi G, De Bellis L, Finetti-Sialer MM, Greco D, et al.. “Ectomosphere”: insects and microorganism interactions Microorganisms, 2023, 11(2): 440.

[44]

R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ .

[45]

Reay SD, Brownbridge M, Gicquel B, Cummings NJ, Nelson TL. Isolation and characterization of endophytic Beauveria spp. (Ascomycota: Hypocreales) from Pinus radiata in New Zealand forests Biol Contr, 2010, 54(1): 52-60.

[46]

Richardson K, Steffen W, Lucht W, Bendtsen J, Cornell SE, Donges JF, Drüke M, Fetzer I, et al.. Earth beyond six of nine planetary boundaries Sci Adv, 2023, 9(37): eadh2458.

[47]

Santamaría O, Smith DR, Stanosz GR. Interaction between Diplodia pinea and D. scrobiculata in red and jack pine seedlings Phytopathology, 2011, 101(3): 334-339.

[48]

Shah PA, Pell JK. Entomopathogenic fungi as biological control agents Appl Microbiol Biotechnol, 2003, 61(5–6): 413-423.

[49]

Shin TY, Lee MR, Kim JC, Nai YS, Kim JS. A new strategy using entomopathogenic fungi for the control of tree borer insects Entomol Res, 2022, 52(7): 327-333.

[50]

Therneau T (2022) A package for survival analysis in R. R package version 3.4–0. https://CRAN.R-project.org/package=survival

[51]

Urs KCD, Hopkins TL. Effect of moisture on growth rate and development of two strains of Tenebrio molitor L. (Coleoptera, Tenebrionidae) J Stored Prod Res, 1973, 8(4): 291-297.

[52]

Vega FE, Posada F, Catherine Aime M, Pava-Ripoll M, Infante F, Rehner SA. Entomopathogenic Fungal Endophytes Biol Contr, 2008, 46(1): 72-82.

[53]

Vega FE, Meyling NV, Luangsa-ard JJ, Blackwell M (2012) Fungal entomopathogens. In: Insect pathology. Academic Press, pp 171–220. https://doi.org/10.1016/b978-0-12-384984-7.00006-3

[54]

White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols. Academic press, pp 315–322. https://doi.org/10.1016/b978-0-12-372180-8.50042-1

[55]

Wraight SP, Carruthers RI (2003) Production, delivery, and use of mycoinsecticides for control of insect pests on field crops. In: Biopesticides. Humana Totowa, NJ, pp 233–270. https://doi.org/10.1385/0-89603-515-8:233

[56]

Zhang LL (2015) Colonization pattern of crop plants by endophytic fungi. University Goettingen Repository, Doctoral Thesis. https://doi.org/10.53846/goediss-5123

Funding

Universidad de Valladolid

RIGHTS & PERMISSIONS

The Author(s)

AI Summary AI Mindmap
PDF

301

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/