Abstract
Melocont® Pilzgerste, a commercial product based on the entomopathogenic fungus Beauveria brongniartii (Sacc.) Petch (Ascomycota: Hypocreales) strain BIPESCO 2, was applied at different rates and time points over a period of 24 years in East-, North- and South Tyrol (Austria and Italy) to control the European cockchafer (Melolontha melolontha L. and M. hippocastani F.). Beauveria spp. density was assessed and Beauveria spp. isolates were characterized at species and genotype level using Bloc intergenic region sequence and simple sequence repeat marker analyses. BIPESCO 2 was detected at 41 % of the treated sites, predominantly at sites where the fungus was applied at least once during the four years prior to sampling. At one site BIPESCO 2 was detected 15 years after the last treatment. Results showed that applications should be repeated to achieve good persistence of the biological control agent, and it indicated that despite intensive applications diverse populations of B. brongniartii or Beauveria spp. consortia can coexist in these habitats.
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Bruvo R, Michiels NK, D’Souza TG, Schulenburg H (2004) A simple method for calculation of microsatellite genotype distances irrespective of ploidy level. Mol Ecol 13:2101–2106
Bulmer MG (1977) Periodical insects. Am Nat 111:1099–1117
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
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1997
Enkerli J, Widmer F (2010) Molecular ecology of fungal entomopathogens: molecular genetic tools and their applications in population and fate studies. BioControl 55:17–37
Enkerli J, Widmer F, Gessler C, Keller S (2001) Strain-specific microsatellite markers in the entomopathogenic fungus Beauveria brongniartii. Mycol Res 105:1079–1087
Enkerli J, Widmer F, Keller S (2004) Long-term field persistence of Beauveria brongniartii strains applied as biocontrol agents against European cockchafer larvae in Switzerland. Biol Control 29:115–123
Faber W (1961) Ergebnisse zehnjähriger erhebungen über die Flugjahre des Maikäfers (Melolontha melolontha und Melolontha hippocastani) in Österreich. Pflanzenschutzberichte 27:101–146
Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256
Fornallaz C (1992) Microbial control of the May beetle Melolontha melolontha L. with the fungus Beauveria brongniartii (Sacc.) Petch: Demecological aspects of various control methods. PhD Thesis, ETH Zürich, CH
Goble TA (2012) Towards the development of a mycoinsecticide to control white grubs (Coleoptera, Scarabaeidae) in South African sugarcane. PhD thesis, Rhodes University, ZA
Goble TA, Costet L, Robene I, Nibouche S, Rutherford RS, Conong DE, Hill MP (2012) Beauveria brongniartii on white grubs attacking sugarcane in South Africa. J Invertebr Pathol 111:225–236
Hughes JB, Hellmann JJ (2005) The application of rarefaction techniques to molecular inventories of microbial diversity. Method Enzymol 397:292–308
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro NH (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132
Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281
Kang S, Mills AL (2006) The effect of sample size in studies of soil microbial community structure. J Microbial Methods 66:242–250
Keller S, Zimmermann G (2005) Scarabs and other soil pests in Europe, situation, perspective and control strategies. IOBC/WPRS Bull 28:9–12
Keller S, Kessler P, Jensen DB, Schweizer C (2002) How many spores of Beauveria brongniartii are needed to control Melolontha melolontha? IOBC/WPRS Bull 25:59–64
Keller S, Kessler P, Schweizer C (2003) Distribution of insect pathogenic soil fungi in Switzerland with special reference to Beauveria brongniartii and Metarhizium anisopliae. BioControl 48:307–319
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. J Invertebr Path 84:15–23
Kessler P, Enkerli J, Schweizer C, Keller S (2004) Survival of Beauveria brongniartii in the soil after application as a biocontrol agent against the European cockchafer Melolontha melolontha. BioControl 49:563–581
Laengle T, Strasser H (2010) Developing a risk indicator to comparatively assess environmental risks posed by microbial and conventional pest control agents. Biocontrol Sci Technol 20:659–681
Laengle T, Pernfuss B, Seger C, Strasser H (2005) Field efficacy evaluation of Beauveria brongniartii against Melolontha melolontha in potato cultures. Sydowia 57:54–93
Manter DK, Weir TL, Vivanco JM (2010) Negative effects of sample pooling on PCR-based estimates of soil microbial richness and community structure. Appl Environ Microb 76:2086–2090
Meyling NV, Eilenberg J (2007) Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biol Control 43:145–155
Meyling NV, Pilz C, Keller S, Widmer F, Enkerli J (2012) Diversity of Beauveria spp. isolates from pollen beetles Meligethes aeneus in Switzerland. J Invertebr Path 109:76–82
Pötsch EM, Strasser H, Berger HK (1997) Was Sie über tierische Schädlinge am Grünland wissen sollten. Der Fortschrittliche Landwirt 6:29–37
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. Cited 02 Dec 2014
Rehner SA, Posada F, Buckley EP, Infante F, Castillo A, Vega FE (2006) Phylogenetic origins of African and neotropical Beauveria bassiana s.l. pathogens of the coffee berry borer, Hypothenemus hampei. J Invertebr Pathol 93:11–21
Rehner SA, Minnis AM, Sung GH, Luangsa-Ard J, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073
Scheepmaker JWA, Butt TM (2010) Natural and released inoculum levels of entomopathogenic fungal biocontrol agents in soil in relation to risk assessment and in accordance with EU regulations. Biocontrol Sci Technol 20:503–552
Schwarzenbach K, Enkerli J, Widmer F (2007a) Objective criteria to assess representativity of soil fungal community profiles. J Microbiol Methods 68:358–366
Schwarzenbach K, Widmer F, Enkerli J (2007b) Cultivation-independent analysis of fungal genotypes in soil by using simple sequence repeat markers. Appl Environ Microbiol 73:6519–6525
Srivastava CN, Maurya P, Sharma P, Mohan L (2009) Prospective role of insecticides of fungal origin: review. Entomol Res 39:341–355
Strasser H, Enkerli J (2001) Biological control of Melolontha melolontha with Melocont®-Pilzgerste based on Beauveria brongniartii: long term study in pastures from 1994-2000. In: 34rd Annual Meeting of the Society for Invertebrate Pathology, Noordwijkerhout, NL, pp 71
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2724–2729
Zimmermann G (2007) Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Sci Technol 17:553–596
Acknowledgments
We would like to thank Dipl.-Ing. Dr. Andreas Koutny, Ing. Mag. FH Peter Frank (Agricultural chamber Tirol), P. A. Peter Neulichedl (Research Centre for Agriculture and Forestry) and students of Innsbruck University, Austria for support with collecting soil samples. We are grateful to Andy Lutz (Agroscope) for support with the genetic analyses, Roland Kölliker (Agroscope) for statistical advice and Franco Widmer (Agroscope) for providing critical discussions and comments on the manuscript. The quality of the manuscript was further improved by the valuable input and recommendations of two anonymous reviewers. This project was funded by the Tyrolean Regional Government (BEAUMON, Grant Agreement No. LWSJF 0109/736) and by the European Community’s Seventh Framework Programme Grant INBIOSOIL (FP7_ENV.2011.3.1.9, Agreement No. 282767). This project was conducted at the Institute of Microbiology in Innsbruck, Austria, and at the Institute for Sustainability Sciences at Agroscope, Switzerland.
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Mayerhofer, J., Enkerli, J., Zelger, R. et al. Biological control of the European cockchafer: persistence of Beauveria brongniartii after long-term applications in the Euroregion Tyrol. BioControl 60, 617–629 (2015). https://doi.org/10.1007/s10526-015-9671-6
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DOI: https://doi.org/10.1007/s10526-015-9671-6