Abstract
Entomopathogenic fungi were collected from insects, belonging to orders Lepidoptera, Coleoptera, Hemiptera, Hymenoptera, and Diptera, with signs of infection. Single-spore colonies were identified based on morphological traits and ribosomal ITS sequences. The most commonly found fungi were Fusarium oxysporum Schlechtendal and Beauveria bassiana (Balsamo-Crivelli) Vuillemin. Isolation of Trichoderma atroviride Bisset, Aspergillus flavipes (Bainier and Sartory) Thom and Church, Aspergillus iizukae Sugiyama, Penicillium mallochii Rivera, Urb and Seifert, Penicillium adametzioides S. Abe ex G. Smith, and Mucor nidicola Madden, Stchigel, Guarro and Starks associated to insects is reported for the first time. Tests with B. bassiana isolates against Duponchelia fovealis Zeller (Lepidoptera: Crambidae), showed high larval mortality in vitro and in greenhouse, demonstrating its potential as biological control agent. Understanding the fungal microbiota from insects can provide promising isolates for use in integrated pest management programs. This is the first report characterizing the mycobiota in insects collected in strawberry crops, and evaluating the pathogenicity of B. bassiana against D. fovealis, a pest that causes severe losses to farmers.
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References
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267
Alves SB (1998) Microbial control of insects. Editora Fundação de Estudos Agrários Luiz de Queiroz, Piracicaba, 1163p (in Portuguese)
Araújo WL, Lima AOS, Azevedo JL, Marcon J, Kuklinsky-Sobral J, Lacava PT (2002) Manual: Isolation of endophytic microorganisms. Calq, Piracicaba (in Portuguese)
Asi MR, Bashir MH, Afzal M, Zia K, Akram M (2013) Potential of entomopathogenic fungi for biocontrol of Spodoptera litura Fabricius (Lepidoptera: Noctuidae). J Anim Plant Sci 23:913–918
Azevedo JL, Macheroni Jr. W, Pereira JO, Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotech 3. http://www.ejb.org/content/vol3/issue1/full/3/4. Accessed 12 Jul 2017
Badali H, Carvalho VO, Vicente VA, Attili-Angelis D, Kwiatkowski IB, Gerrits Van Den Ende AHG, de Hoog GS (2009) Cladophialophora saturnica sp. nov., a new opportunistic species of Chaetothyriales revealed using molecular data. Med Mycol 47:55–66
Barnett HC, Hunter BB (1972) Illustrated genera of imperfect fungi, 3rd edn. Burgess Publ, Minneapolis, p 241p
Berendsen RL, Pieterse CMJ, Bekker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:1360–1385
Bernardi D, Botton M, Nava DE, Zawadneak MAC (2015) Guide for identification and monitoring of pests and their natural enemies in strawberry. Embrapa, Brasília
Bonsignore CP, Vacante V (2010) Duponchelia fovealis Zeller. A new emergency for the strawberry? Prot colt 3:40–43 (in Italian)
Carvalho SP (2011) History and evolution of strawberry culture in Brazil in the last 50 years. Rev Hortic Bras 29, CD-ROM (in Portuguese)
Cohen E, Joseph T, Wassermann-Golan M (2001) Photostabilization of biocontrol agents by berberine. Int J Pest Manag 47:63–67
de Hoog GS, Guarro J, Gené J, Figueras MJ (2000) Atlas of clinical fungi. ASM, Utrecht
Edgington S, Segura H, De la Rosa W, Williams T (2000) Photoprotection of Beauveria bassiana: testing simple formulations for control of the coffee berry borer. Int J Pest Manag 46:169–176
Efil L, Özgür O, Efil F (2014) A new pest, Duponchelia fovealis Zeller, on strawberries in Turkey—damage, distribution and parasitoid. J Entomol Zool Stud 2:328–334
Fernandes EKK, Rangel DEN, Moraes AML, Bittencourt VREP, Roberts DW (2008) Cold activity of Beauveria and Metarhizium, and thermotolerance of Beauveria. J Invertebr Pathol 98:69–78
Fisher JJ, Rehner SA, Bruck DJ (2011) Diversity of rhizosphere associated entomopathogenic fungi of perennial herbs, shrubs and coniferous trees. J Invertebr Pathol 106:289–295
Franco MC, Baptista MC (2010) Duponchelia fovealis Zeller—new pest in Portugal. Frut Legum Flores 110:34–35 (in Portuguese)
Gabarty A, Salem HM, Fouda MA, Abas AA, Ibrahim AA (2014) Pathogencity induced by the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in Agrotis ipsilon (Hufn.). J Radiat Res Appl Sci 7:95–100
Gunde-Cinerman N, Zalar P, Jeram S (1998) Mycoflora of cave cricket Troglophilus neglectus cadavers. Mycopathol 141:111–114
Haddad ML, Vendramim JD (2000) Comparison of percentage data with cases of extreme values of 0 and 100%. An Soc Entomol Bras 29:835–837 (in Portuguese with English summary)
Henderson CF, Tilton EW (1995) Test with acaricides against the brown wheat mite. J Econ Entomol 43:157–161
Houbraken M, Bauweraerts I, Fevery D, Labeke MCV, Spanoghe P (2016) Pesticide knowledge and practice among horticultural workers in the Lam Dong region, Vietnam: a case study of chrysanthemum and strawberries. Sci Total Environ 550:1001–1009
Jaronski ST (2007) Soil ecology of the entomopathogenic Ascomycetes: a critical examination of what we (think) we know. In: Ekesi S, Maniania NK (eds) Use of entomopathogenic fungi in biological pest management. Research Signpost, Thiruvananthapuram, pp 315–322
Krieg A, Gröner A, Huber J, Zimmermann G (1981) Inactivation of certain insect pathogens by ultraviolet radiation. Z Pflanzenkr Pflanzenschutz 88:38–48
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Leland JE, Behle RW (2005) Coating Beauveria bassiana with lignin for protection from solar radiation and effects on pathogenicity to Lygus lineolaris (Heteroptera: Miridae). Biocontrol Sci Technol 15:309–320
Matyjaszcyk E (2015) Products containing microorganisms as a tool in integrated pest management and the rules of their market placement in the European Union. Pest Manag Sci 71:1201–1206
Moshi AP, Matoju I (2017) The status of research on and application of biopesticides in Tanzania. Crop Prot 92:16–28
Nelder JA, Baker RJ (1972) Generalized linear models. Wiley, New Jersey
Oliveira RC, Neves PMOJ, Alves LFA (2004) Entomopathogenic fungi selection to control Oligonychus yothersis (McGregor) (Acari: Tetranychidae) in Paraguay tea crops (Ilex paraguariensis St. Hill.). Neotrop Entomol 33:347–351
Oshita D, Jardim ICSF (2012) Strawberry: Food, environmental and sanitary concerns, monitored by modern liquid chromatography. Sci Chromatogr 4:52–76 (in Portuguese with English summary)
Pires LM, Marques EJ, Oliveira JV, Alves SB (2010) Selection of isolates of entomopathogenic fungi for controlling Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) and their compatibility with insecticides used in tomato crop. Neotrop Entomol 39:977–984
Robertson JL, Russell RM, Preisler HK, Savin NE (2007) Bioassays with arthropods, 2nd edn. CRC Press, Boca Raton
Rondot Y, Reineke A (2016) Endophytic Beauveria bassiana in grapevine Vitis vinifera (L.) reduces infestation with piercing-sucking insects. Biol Control. https://doi.org/10.1016/j.biocontrol.2016.10.006
Rossman AY, Palm ME, Spielman LJ (1987) A literature guide for the identification of plant pathogenic fungi. APS Press, St Paul
Shakeri J, Foster HA (2007) Proteolytic activity and antibiotic production by Trichoderma harzianum in relation to pathogenicity to insects. Enzym Microb Technol 40:961–968
Shapiro SS, Wilk MB (1965) An analysis of variance test for normality. Biom 52:591–611
Silva VCA, Barros R, Marques JE, Torres JB (2003) Susceptibiliy of Plutella xylostella (L.) (Lepidoptera: Plutellidae) to the fungi Beauveria bassiana (Bals.) Vuill. and Metarhizium anisopliae (Metsch.) Sorok. Neotrop Entomol 32:653–658
Sun BD, Liu XZ (2008) Occurrence and diversity of insect-associated fungi in natural soils in China. Appl Soil Ecol 39:100–108
Sun BD, Yu H, Chen AJ, Liu XZ (2008) Insect-associated fungi in soils of field crops and orchards. Crop Prot 27:1421–1426
Svedese VM, Lima EAL, Porto ALF (2013) Horizontal transmission and effects of the temperature in pathogenicity of Beauveria bassiana against Diatraea saccharalis (Lepidoptera: Crambidae). Braz Arch Biol Technol 56:413–419
Tefera T, Pringle K (2003) Germination, radial growth, and sporulation of Beauveria bassiana and Metarhizium anisopliae isolates and their virulence to Chilo partellus (Lepidoptera: Pyralidae) at different temperatures. Biocontrol Sci Technol 13:699–704
Trizelia, Nurdin F (2010) Virulence of entomopathogenic fungus Beauveria bassiana isolates to Crocidolomia pavonana F (Lepidoptera: Crambidae). Agrivita 32:254–260
Tuininga AR, Miller JL, Morath SU, Daniels TJ, Falco RC, Marchese M, Sahabi S, Rosa D, Stafford KC III (2009) Isolation of entomopatogenic fungi from soils and Ixodes scapularis (Acari: Ixodidae) ticks: prevalence and methods. J Med Entomol 46:557–565
Valero-Jiménez CA, Wiegers H, Zwaan BJ, Koenraadt CJM, van Kan JAL (2016) Genes involved in virulence of the entomopathogenic fungus Beauveria bassiana. J Invertebr Pathol 133:41–49
Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzón A, Ownley BH, Pell JK, Rangel EN, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159
Vu VH, Hong SI, Kim K (2007) Selection of entomopathogenic fungi for aphid control. J Biosci Bioeng 104:498–505
Wang D, Deng J, Pei Y, Li T, Jin Z, Liang L, Wang W, Li L, Dong X (2017) Identification and virulence characterization of entomopathogenic fungus Lecanicillium attenuatum against the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae). Appl Entomol Zool 52:511–518
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322
Wraight SP, Ramos ME, Avery PB, Jaronski ST, Vandenberg JD (2010) Comparative virulence of Beauveria bassiana isolates against lepidopteran pest of vegetables crops. J Invertebr Pathol 103:186–199
Zawadneak MAC, Gonçalves RB, Pimentel IC, Schuber JM, Santos B, Poltronieri AS, Solis MA (2016) First record of Duponchelia fovealis (Lepidoptera: Crambidae) in South America. Idesia 34:91–95
Zawadneak MAC, Gonçalves RB, Poltronieri AS, Santos B, Bischoff AM, Borba AM, Pimentel IC (2017) Biological parameters of Duponchelia fovealis (Lepidoptera: Crambidae) reared in the laboratory on two diets. Eur J Entomol 114:291–294
Zimmermann G (1982) Effect of high temperatures and artificial sunlight on the viability of conidia of Metarhizium anisopliae. J Invertebr Pathol 40:36–40
Zimmermann G (2007a) Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Sci Technol 17:553–596
Zimmermann G (2007b) Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Sci Technol 17:879–920
Acknowledgements
We wish to express our deepest appreciation for the financial support received from National Council for Scientific and Technological Development (CNPq). We thank the National Council for the Improvement of Higher Education (CAPES), and Federal University of Parana. We are also grateful to Novozymes BioAg for providing Bovemax® and Methamax®, especially Dr. Maria Silvia Pereira Leite, and the staff of the Laboratory of Microbiology and Molecular Biology and Laboratory of Entomology Prof. Angelo Moreira da Costa Lima.
Funding
This study was supported by National Council for Scientific and Technological Development (CNPq) under Grant 38-2013.
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Poitevin, C.G., Porsani, M.V., Poltronieri, A.S. et al. Fungi isolated from insects in strawberry crops act as potential biological control agents of Duponchelia fovealis (Lepidoptera: Crambidae). Appl Entomol Zool 53, 323–331 (2018). https://doi.org/10.1007/s13355-018-0561-0
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DOI: https://doi.org/10.1007/s13355-018-0561-0