Occurrence of soil-inhabiting entomopathogenic fungi within a conventional and organic farm and their virulence against Spodoptera litura
##plugins.themes.bootstrap3.article.sidebar##
Issue
Section
Articles
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
##plugins.themes.bootstrap3.article.main##
AMINUDIN AFANDHI
♥
FERY ABDUL CHOLIQ
https://orcid.org/0000-0002-7545-1987
ITO FERNANDO
https://orcid.org/0000-0001-6776-4847
YOSEP MINAR ALBERT NANDUS MARPAUNG
YOGO SETIAWAN
Abstract
Abstract. Afandhi A, Choliq FA, Fernando I, Marpaung YMAN, Setiawan Y. 2022. Occurrence of soil-inhabiting entomopathogenic fungi within a conventional and organic farm and their virulence against Spodoptera litura. Biodiversitas 23: 1172-1180. Naturally occurring entomopathogenic fungi (EPF) are important components in agroecosystems as they serve as biocontrol agents of insect and mite pests. However, some cultivation practices may have deleterious effects on EPF. In this study, the occurrence of soil-inhabiting EPF was investigated between a conventional and organic farm. EPF was baited using Tenebrio molitor larvae, and their virulence was tested against Spodoptera litura larvae. The results showed a higher occurrence of EPF in the organic farm than the conventional farm, with Aspergillus sp., Beauveria sp., and Gliocladium sp. were exclusively found in organic soils. Among the twenty-five EPF isolates obtained, only four isolates were avirulent against S. litura larvae. Isolates belonging to Beauveria, Metarhizium, and Paecilomyces genera caused high mortality of S. litura larvae ranging from 40 to 65%. There was a significant positive relationship between the conidial viability of EPF and larval mortality. Since virulent isolates were found in conventional soils, efforts in preserving EPF prevalence are needed through the implementation of appropriate cultivation practices. The synthetic agrochemicals exclusion, organic fertilizers application, and crop rotation practiced in the organic farm should be integrated into any other agroecosystems as a form of conservation biological control strategies to strengthen the pest control service provided by EPF.
##plugins.themes.bootstrap3.article.details##
References
Afandhi A, Widjayanti T, Emi AAL, Tarno H, Afiyanti M, Handoko RNS. 2019. Endophytic fungi Beauveria bassiana Balsamo accelerates growth of common bean (Phaseolus vulgaris L.). Chem Biol Technol Agric 6: 11. DOI: 10.1186/s40538-019-0148-1
Ali-Shtayeh MS, Mara’I ABBM, Jamous RM. 2002. Distribution, occurrence and characterization of entomopathogenic fungi in agricultural soi in the Palestinian area. Mycopathologia 156: 235-244. DOI: 10.1023/a:1023339103522
Aw KMS, Hue SM. 2017. Mode of infection of Metarhizium spp. fungus and their potential as biological control agents. J Fungi 3(2): 30. DOI: 10.3390/jof3020030
Ayudya DR, Herlinda S, Suwandi S. 2019. Insecticidal activity of culture filtrates from liquid medium of Beauveria bassiana isolates from South Sumatra (Indonesia) wetland soil against larvae of Spodoptera litura. Biodiversitas 20(8): 2101-2109. DOI: 10.13057/biodiv/d200802
Barnett L, Hunter BB. 1987. Illustrated Genera of Imperfect Fungi, 4th edn. MacMillan Publishing, New York.
Bruck DJ. 2004. Natural occurrence of entomopathogens in Pacific Northwest nursery soils and their virulence to the black vine weevil, Otiorhynchus sulcatus (F.) (Coleoptera Curculionidae). J Environ Entomol 33: 1335-1343. DOI: 10.1603/0046-225X-33.5.1335
Brunner-Mendoza C, Reyes-Montes MR, Moonjely S, Bidochka MJ, Toriello C. 2019. A review on the genus Metarhizium as an entomopathogenic microbial biocontrol agent with emphasis on its use and utility in Mexico. Biocontrol Sci Technol 29(1): 83-102. DOI: 10.1080/09583157.2018.1531111
Butt TM, Coates CJ, Dubovskiy IM, Ratcliffe NA. 2016. Entomopathogenic fungi: new insights into host-pathogen interactions. Adv Genet 94: 307-364. DOI: 10.1016/bs.adgen.2016.01.006
Clifton EH, Jaronski ST, Hodgson EW, Gassmann AJ. 2015. Abundance of soil-borne 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
D'Alessandro CP, Padin S, Urrutia MI, López Lastra CC. 2011. Interaction of fungicides with the entomopathogenic fungus Isaria fumosorosea. Biocontrol Sci Technol 21(2): 189-197. DOI: 10.1080/09583157.2010.536200
Dara SK. 2019. Non-entomopathogenic roles of entomopathogenic fungi in promoting plant health and growth. Insects 10(9): 277. DOI: 10.3390/insects10090277
Domsch KH, Gams W, Anderson TH. 2007. Compendium of Soil Fungi, 2nd edn. IHW-Verlag and Verlagsbuchhandlung, Eching. DOI: 10.1111/j.1365-2389.2008.01052_1.x
Dromph KM. 2003. Collembolans as vectors of entomopathogenic fungi. Pedobiologia 47(3): 245-256. DOI: 10.1078/0031-4056-00188
Faria M, Lopes RB, Souza DA, Wraight SP. 2015. Conidial vigor vs. viability as predictors of virulence of entomopathogenic fungi. J Invertebr Pathol 125: 68-72. DOI: 10.1016/j.jip.2014.12.012
Faria MR, Wraight SP. 2007. Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 47(3): 237–256. DOI: 10.1016/j.biocontrol.2007.08.001
Goble TA, Dames JF, Hill MP, Moore SD 2010. The effects of farming system, habitat type and bait type of the isolation of entomopathogenic fungi from citrus soils in the Eastern Cape Orovince, South Africa. BioControl 55: 399-412. DOI: 10.1007/s10526-009-9259-0
Goettel MS, Eilenberg J, Glare TR. 2010. Entomopathogenic Fungi and their Role in Regulation of Insect Populations. In: Gilbert LI, Gill SS (eds.). Insect Control Biological and Synthetic Agents. Elsevier, London.
Hallsworth JE, Magan N. 1999. Water and temperature relations of growth of the entomogenous fungi Beauveria bassiana, Metarhizium anisopliae, and Paecilomyces farinosus. J Invertebr Pathol 74(3): 261-266. DOI: 10.1006/jipa.1999.4883
Harith-Fadzilah N, Ghani IA, Hassan M. 2021. Omics-based approach in characterizing mechanisms of entomopathogenic fungi pathogenicity: a case example of Beauveria bassiana. J King Saud Univ Sci 33: 101332. DOI: 10.1016/j.jksus.2020.101332
Jenkins NE, Grzywacz D. 2000. Quality control of fungal and viral biocontrol agents – assurance of product performance. Biocontrol Sci Technol 10(6): 753-777. DOI: 10.1080/09583150020011717
Klingen I, Eilenberg J, Meadow R. 2002. Effects of farming systems, field margins and bait insect on the occurrence of insect pathogenic fungi in soils. Agric Ecosyst Environ 91(1-3): 191-198. DOI: 10.1016/S0167-8809(01)00227-4
Klingen I, Haukeland S. 2006. The Soil as Reservoir for Natural Enemies of Pest Insects and Mites with Emphasis on Fungi and Nematodes. In: Eilenberg J, Hokkanen HMT (eds.). Ecological and Societal Approach to Biological Control. Springer, Dordrecht.
Li Z, Alves SB, Roberts DW, Fan M, Jr Delalibera I, Tang J, Lopes RB, Faria M, Rangel DEN. 2010. Biological control of insects in Brazil and China: history, current programs and reasons for their successes using entomopathogenic fungi. Biocontrol Sci Technol 20(2): 117-136. DOI: 10.1080/09583150903431665
Loria R, Galaini S, Roberts DW. 1983. Survival of inoculum of the entomopathogenic fungus Beauveria bassiana as influenced by fungicides. Environ Entomol 12: 1724–1726. DOI: 10.1093/ee/12.6.1724
Majchrowicz I, Poprawski TJ. 1993. Effects in vitro of nine fungicides on growth of entomopathogenic fungi. Biocontrol Sci Technol 3(3): 321-336. DOI: 10.1080/09583159309355287
Medo J, Cagá? L. 2011. Factors affecting the occurrence of entomopathogenic fungi in soils of Slovakia as revealed using two methods. Biol. Control 59: 200-208. DOI: 10.1016/j.biocontrol.2011.07.020
Meyling NV, Eilenberg J. 2006. Occurrence and distribution of soil borne entomopathogenic fungi within a single organic agroecosystem. Agric Ecosyst Environ 113: 336-341. DOI: 10.1016/j.agee.2005.10.011
Meyling NV, Lübeck M, Buckley EP, Eilenberg J, Rehner SA. 2009. Community composition, host range and genetic structure of the fungal entomopathogen Beauveria in adjoining agricultural and seminatural habitats. Mol Ecol 18: 1282–1293. DOI: 10.1111/j.1365-294X.2009.04095.x
Meyling NV, Thorup-Kristensen K, Eilenberg J. 2011. Below- and aboveground abundance and distribution of fungal entomopathogens in experimental conventional and organic cropping systems. Biol Control 59: 180–186. DOI: 10.1016/j. biocontrol.2011.07.017
Mie A, Andersen HR, Gunnarsson S, Kahl J, Kesse-Guyot E, Rembia?kowska E, Quaglio G, Grandjean P. 2017. Human health implications of organic food and organic agriculture: a comprehensive review. Environ Health 16: 111. DOI: 10.1186/s12940-017-0315-4
Moreno-Gavíra A, Huertas V, Diánez F, Sánchez-Montesinos B, Santos M. 2020. Paecilomyces and its importance in the biological control of agricultural pests and diseases. Plants 9(12): 1746. DOI: 10.3390/plants9121746
Nguyen HC, Tran TVA, Nguyen QL, Nguyen NN, Nguyen MK, Nguyen NTT, Su CH, Lin KH. 2017. New;y isolated Paecilomyces javanicus as novel biocontrol agents for Plutella xylostella and Spodoptera litura. Not Bot Horti Agrobo 45: 280-286. DOI: 10.15835/nbha45110726
Niu X, Xie W, Zhang J, Hu Q. 2019. Biodiversity of entomopathogenic fungi in the soils of South China. Microoganisms 7: 311. DOI: 10.3390/microorganisms7090311
Pell JK, Hannam JJ, Steinkraus DC. 2010. Conservation biological control using fungal entomopathogens. BioControl 55: 187-198. DOI: 10.1007/s10526-009-9245-6
Puspitarini RD, Afandhi A, Fernando I. 2021a. Evaluation of indigenous fungal entomopathogens and aqueous leaf extract of Annona muricata against Polyphagotarsonemus latus infesting Jatropha curcas in Indonesia. Biodiversitas 22(7): 2648-2655. DOI: 10.13057/biodiv/d220713
Puspitarini RD, Fernando I, Sianturi YPPA, Rachmawati R. 2021b. Compatibility of Jatropha curcas seed extract and entomopathogenic fungus Akanthomyces lecanii against the citrus red mite Panonychus citri. Biocontrol Sci Technol. DOI: 10.1080/09583157.2021.1993134
Quesada-Moraga E, Navas-Cortés JA, Maranhao EAA, Ortiz-Urquiza A, Santiago-Álvarez C. 2007. Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils. Mycol Res 111(8): 947-966. DOI: 10.1016/j.mycres.2007.06.006
R Core Team. 2020. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
Ramos Y, Portal O, Lysøe E., Meyling NV, Klingen I. 2017. Diversity and abundance of Beauveria bassiana in soils, stink bugs and plant tissues of common bean from organic and conventional fields. J Invertebr Pathol 150: 114–120. DOI: 10.1016/j.jip.2017.10.003.
Sánchez-Peña SR, Lara SJ, Medina RF. 2011. Occurrence of entomopathogenic fungi from agricultural and natural ecosystems in Saltillo, Mexico, and their virulence towards thrips and whiteflies. J Insect Sci 11: 1-10. DOI: 10.1673/031.011.010110.1673/031.011.0101
Shah FA, Ansari MA, Watkins J, Phelps Z, Cross J, Butt TM. 2009. Influence of commercial fungicides on the germination, growth and virulence of four species of entomopathogenic fungi. Biocontrol Sci Technol 19(7): 743-753. DOI: 10.1080/09583150903100807
Sharma L, Oliveira I, Gonçalves F, Raimundo F, Singh RK, Torres L, Marques G. 2021. Effect of soil chemical properties on the occurrence and distribution of entomopathogenic fungi in Portuguese grapevine fields. Pathogens 10: 137. DOI: 10.3390/pathogens10020137
Sharma L, Oliveira I, Torres L, Marques G. 2018. Entomopathogenic fungi in Portuguese vineyards soils: suggesting a ‘Galleria-Tenebrio-bait method’ as bait-insects Galleria and Tenebrio significantly underestimate the respective recoveries of Metarhizium (roberstii) and Beauveria (bassiana). MycoKeys 38: 1-23. DOI: 10.3897/mycokeys.38.26790
Uzman D, Pliester J, Leyer I, Entling MH, Reineke A. 2019. Drivers of entomopathogenic fungi presence in organic and conventional vineyard soils. Appl Soil Ecol 133: 89-97. DOI: 10.1016/j.apsoil.2018.09.004
Teja KNP, Rahman SJ. 2016. Characterisation and evaluation of Metarhizium anisopliae (Metsch.) Sorokin strains for their temperature tolerance. Mycology 7(4): 171-179. DOI: 10.1080/21501203.2016.1247116
Tkaczuk C, Król A, Majchrowska-Safaryan A, Nicewicz ?. 2014. The occurrence of entomopathogenic fungi in soils from fields cultivated in a conventional and organic system. J Ecol Eng 15(4): 137-144. DOI: 10.12911/22998993.1125468
Todorova SI, Coderre D, Duchesne RM, Côté JC. 1998. Compatibility of Beauveria bassiana with selected fungicides and herbicides. Environ Entomol 27(2): 427-433. DOI: 10.1093/ee/27.2.427
Vänninen I. 1995. Distribution and occurrence of four entomopathogenic fungi in Finland: effect of geographical location, habitat type and soil type. Mycol Res 100(1): 93-101. DOI: 10.1016/S0953-7562(96)80106-7
Vänninen I, Tyni-Juslin J, Hokkanen H. Persistence of augmented Metarhizium anisopliae and Beauveria bassiana in Finnish agricultural soil. Biocontrol 45: 201-222. DOI: 10.1023/A:1009998919531
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: 149-159. DOI: 10.1016/j.funeco.2009.05.001.
WHO. 2016. Test Procedures for Insecticide Resistance Monitoring in Malaria Vector Mosquitoes, 2nd edn. World Health Organization. Available at https://apps.who.int/iris/bitstream/handle/10665/250677/9789241511575-eng.pdf
Yang H, Qin CS, Chen YM, Zhang GY, Dong LH, Wan SQ. 2019. Persistence of Metarhizium (Hypocreales: Clavicipitaceae) and Beauveria bassiana (Hypocreales: Cavicipitaceae) in tobacco soils and potential as biocontrol agents of Spodoptera litura (Lepidoptera: Noctuidae). Environ Entomol 48(1): 147-155. DOI: 10.1093/ee/nvy161
Most read articles by the same author(s)
- ABDUL LATIEF ABADI, FERY ABDUL CHOLIQ, MUTHIA OKTAVIANITA, NOVIA ARINATA, MOCHAMMAD SYAMSUL HADI, YOGO SETIAWAN , Screening of soil fungi as bioremediation fungicide and its effect on growth of potato plants , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 3 (2022)
- RETNO DYAH PUSPITARINI, ALDY PURWANTORO, VANADYA DECEMBRY ALODYA PRADIFTA, FAIZ NASHIRUDDIN MUHAMMAD, ITO FERNANDO, Abundance of arthropod pests and their natural enemies on cassava fields implementing different agroecosystem management , Biodiversitas Journal of Biological Diversity: Vol. 25 No. 9 (2024)
- YOGO SETIAWAN, FADEL MUHAMMAD HAMDOEN, FAIZ NASHIRUDDIN MUHAMMAD, KUNIHIKO HATA, HAGUS TARNO, JIANGUO WANG, Species composition of Bactrocera fruit flies (Diptera: Tephritidae) and their parasitoids on horticultural commodities in Batu City and Malang District, East Java, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 25 No. 1 (2024)
- TITA WIDJAYANTI, RESTU RIZKYTA KUSUMA, LUQMAN QURATA AINI, CINDY DIAH AYU FITRIANI, ANTOK WAHYU SEKTIONO, MOCHAMMAD SYAMSUL HADI, YOGO SETIAWAN, Screening of phyllospheric and endophytic bacteria as biocontrol agents of Xanthomonas oryzae pv. oryzae , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 4 (2023)
- HAGUS TARNO, EVY OCTAVIA, TOTO HIMAWAN, YOGO SETIAWAN, Detection of fruit flies (Diptera: Tephritidae) using cue-lure and methyl eugenol in Depok City and Bogor District, West Java, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 8 (2022)
- WIWIN WINDRIYANTI, NONI RAHMADHINI, ITO FERNANDO, RAMADHANI MAHENDRA KUSUMA, Arthropods discovered on refugio flowering plants in Mangifera indica plantation , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 9 (2023)
- ITO FERNANDO, FAIZ NASHIRUDDIN MUHAMMAD, RAHMAT FURQONI, M. BAYU MARIO, RETNO DYAH PUSPITARINI, IRISA TRIANTI, MUHAMMAD AKHID SYIB’LI, AKHMAD RIZALI, Local and landscape effects on the abundance and diversity of soil arthropods in citrus orchards of Malang and Batu, East Java, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 25 No. 10 (2024)