Skip to main content
Log in

Characterization of entomopathogenic fungi from vineyards in Argentina with potential as biological control agents against the European grapevine moth Lobesia botrana

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Biological control by entomopathogenic fungi is a possible alternative to chemical insecticides. As the grapevine moth Lobesia botrana (Lepidoptera: Tortricidae), recently introduced in Argentina, is now the major pest in most of the vineyards in the country despite quarantine regulations, native entomopathogenic fungi could be a preferable alternative to current synthetic insecticides. Thus, the aim of this study was to characterize native fungus strains isolated from 45 soil samples, using larvae of L. botrana as bait insect, and infected arthropods from the wine-growing region in the west of Argentina. Sixteen strains were identified, belonging to two species: four strains to Beauveria bassiana (Hypocreales: Cordycipitaceae) and 12 strains to Metarhizium robertsii (Hypocreales: Clavicipitaceae). Based on their physiological features, M. robertsii strains collected from the west region of Argentina seem to be the most tolerant to the high temperatures specific to this region. Therefore, being well adapted to Argentinean climate conditions, some of the native M. robertsii could be proposed as biological control agents against L. botrana.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Baskar K, Raj GA, Mohan PM, Lingathurai S, Ambrose T, Muthu C (2012) Larvicidal and growth inhibitory activities of entomopathogenic fungus, Beauveria bassiana against Asian Army worm, Spodoptera litura Fab. (Lepidoptera: Noctuidae). J Entomol 9(3):155–162

    Article  Google Scholar 

  • Bidochka MJ, Khachatourians GG (1991) The implication of metabolic acids produced by Beauveria bassiana in pathogenesis of the migratory grasshopper, Melanoplus sanguinipes. J Invertebr Pathol 58(1):106–117

    Article  CAS  Google Scholar 

  • Bidochka MJ, Small CL (2005) Phylogeography of Metarhizium, an insect pathogenic fungus. In: Vega FE, Blackwell M (eds) Insect-fungal associations: ecology and evolution. Oxford University Press, New York, pp 28–50

    Google Scholar 

  • Bidochka MJ, Kamp AM, Lavender TM, Dekoning J, Amritha de Croos JN (2001) Habitat association in two genetic groups of the insect-pathogenic fungus Metarhizium anisopliae: uncovering cryptic species? J Appl Environ Microbiol 67(3):1335–1342

    Article  CAS  Google Scholar 

  • Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae linage. Mycologia 101(4):512–530

    Article  CAS  PubMed  Google Scholar 

  • Boiteux J, Soto Vargas C, Pizzuolo P, Lucero G, Silva MF (2014) Phenolic characterization and antimicrobial activity of folk medicinal plant extracts for their applications in olive production. Electrophoresis 35:1709–1728

    Article  CAS  PubMed  Google Scholar 

  • Butt TM, Coates CJ, Dubovskiy IM, Ratcliffe NA (2016) Entomopathogenic fungi: new insights into host–pathogen interactions. Adv Genet 94:307–364

    Article  CAS  PubMed  Google Scholar 

  • Cozzi G, Somma S, Haidukowski M, Logrieco A (2013) Ochratoxin A management in vineyards by Lobesia botrana biocontrol. Toxins 5(1):49–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43(3):237–256

    Article  CAS  Google Scholar 

  • Delbac L, Thiéry D (2016) Damage to grape flowers and berries by Lobesia botrana larvae (Denis & Schiffernüller) (Lepidoptera: Tortricidae), and relation to larval age. Aust J Grape Wine Res 22(2):256–261

    Article  Google Scholar 

  • Denier D, Bulmer MS (2015) Variation in subterranean termite susceptibility to fatal infections by local Metarhizium soil isolates. Insect Soc 62(2):219–226

    Article  Google Scholar 

  • El Kichaoui AY, Bara’a A, El-Hindi MW (2017) Isolation, molecular identification and under lab evaluation of the entomopathogenic fungi M. anisopliae and B. bassiana against the red palm weevil R. ferrugineus in Gaza Strip. Adv Microbiol 7:109–124

    Article  CAS  Google Scholar 

  • Fargues J, Maniania N, Delmas J, Smits N (1992) Influence de la temperature sur la croissance in vitro d´hyphomycètes entompathogènes. Agronomie, EDP Sciences 12(7):557–564

    Article  Google Scholar 

  • Ferreira A, Bastos MMSM, Aguiar A (2003) Criaçao de traça da uva Lobesia botrana. In: Actas do VI encontro nacional de proteçao integrada, Castelo Branco-Portugal, 83–88

  • Goble TA, Dames JF, Hill MP (2010) The effects of farming system, habitat type and bait type on the isolation of entomopathogenic fungi from citrus soils in the Eastern Cape Province, South Africa. BioControl 55(3):399–412

    Article  Google Scholar 

  • Humber RA (2012) Identification of entomopathogenic fungi. In: Lacey LA (ed) Manual of techniques in invertebrate pathology, 2nd edn. Academic Press (Elsevier), London, pp 151–186

    Chapter  Google Scholar 

  • Inglis GD, Enkerli J, Goettel MS (2012) Laboratory techniques used for entomopathogenic fungi: hypocreales. In: Lacey LA (ed) Manual of techniques in invertebrate pathology, 2nd edn. Academic Press (Elsevier), London, pp 189–251

    Chapter  Google Scholar 

  • 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 SignPosts, Trivandrum, pp 91–143

    Google Scholar 

  • Jaronski ST (2009) Ecological factor in the inundative use of fungal entomopathogens. BioControl 55(1):159–185

    Article  Google Scholar 

  • Keller S, Kessler P, Schweizer C (2003) Distribution of insect pathogenic soil fungi in Switzerland with special reference to Beauveria brongniartii and Metharhizium anisopliae. BioControl 48(3):307–319

    Article  Google Scholar 

  • Kepler RM, Ugine TA, Maul JE, Cavigelli MA, Rehner SA (2015) Community composition and population genetics of insect pathogenic fungi in the genus Metarhizium from soils of a long-term agricultural research system. Environ Microbiol 17(8):2791–2804

    Article  PubMed  Google Scholar 

  • Klingen I, Eilenberg J, Meadow R (2002) Effects of farming system, field margins and bait insect on the occurrence of insect pathogenic fungi in soils. Agric Ecosyst Environ 91:191–198

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Langeron M, Vanbreuseghem R (1952) Présis de mycologie. Masson et Cie (eds) Paris

  • Meyling N (2007) Methods for isolation of entomopathogenic fungi from soil environment. Laboratory manual. Department of Ecology, Faculty of Life Science, University of Copenhagen. http://orgprints.org/11200. Accessed 15 Oct 2013

  • Meyling N, 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

    Article  Google Scholar 

  • Meyling N, Lübeck M, Bucley 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(6):1282–1293

    Article  CAS  PubMed  Google Scholar 

  • Nishi O, Hasegawa K, Iiyama K, Yasunaga-Aoki C, Shimizu S (2011) Phylogenetic analysis of the Metarhizium spp. isolated from soil in Japan. Appl Entomol Zool 46:301–309

    Article  Google Scholar 

  • Nishi O, Iiyama K, Yasunaga-Aoki C, Shimizu S (2013) Comparison of the germination rates of Metarhizium spp. conidia from Japan at high and low temperatures. Lett Appl Microbiol 57(6):554–560

    Article  CAS  PubMed  Google Scholar 

  • Oda H, Hatakeyama Y, Yamamoto Y, Enomoto K, Shigano T, Iwano H (2014) Phylogenetic relationships among strains of the entomopathogenic fungus Beauveria bassiana (Hypocreales: Clavicipitaceae) isolated from Japan. Appl Entomol Zool 49(2):213–221

    Article  Google Scholar 

  • Quesada-Moraga E, Navas-Cortés JA, Maranhao EA, 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

    Article  PubMed  Google Scholar 

  • Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-alpha sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97(1):84–98

    CAS  PubMed  Google Scholar 

  • Rehner SA, Posada FJ, Buckley EP, Infante F, Castillo A, Vega FE (2006) Cryptic lineage diversification, mating potential and recombination in the mitotic insect pathogenic fungus Beauveria bassiana. J Invertebr Pathol 93:11–21

    Article  PubMed  Google Scholar 

  • Rehner SA, Minnis AM, Sung GH, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103(5):1055–1073

    Article  PubMed  Google Scholar 

  • Rezende JM, Riguetti-Zanardo AB, da Silva Lopez M, Delalibera I, Rehner SA (2015) Phylogenetic diversity of Brazilian Metarhizium associated with sugarcane agriculture. BioControl 60(4):495–505

    Article  Google Scholar 

  • Safavi SA, Kharrazi A, Rasoulian GR, Bandani AR (2010) Virulence of some isolates entomopathogenic fungus, Beauveria bassiana on Ostrinia nubilalis (Lepidoptera: Pyralidae). J Agric Sci Technol 12:13–21

    Google Scholar 

  • Sahayaraj K, Borgio F (2010) Virulence of entomopathogenic fungus Metarhizium anisopliae (Metsch.) Sorokin on seven insect pests. Indian J Agric Res 44(3):195–200

    Google Scholar 

  • Steinwender BM, Enkerli J, Widmer F, Eilenberg J, Thorup-Kristensen K, Meyling NV (2014) Molecular diversity of the entomopathogenic fungal Metarhizium community within an agroecosystem. J Invertebr Pathol 123:6–12

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: moleclar evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity for detection of Cryptosporidium parvum, E. coli K99, and rotavirus in calf feces. J Vet Diagn Invest 11:314–318

    Google Scholar 

  • Thompson SR, Brandenburg RL, Arends JJ (2006) Impact of moisture and UV degradation of Beauveria bassiana (Balsamo) Vuillemin conidial viability in turfgrass. Biol Control 39:401–407

    Article  Google Scholar 

  • Tsui CKM, Sivichai S, Berbee ML (2006) Molecular systematics of Helicoma, Helicomyces and Helicosporium and their teleomorphs inferred from rDNA sequences. Mycologia 98:94–104

    Article  CAS  PubMed  Google Scholar 

  • Uma Devi K, Sridevi V, Murali Mohan Ch, Padmavathi J (2005) 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 88:151–189

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Wraight SP, Ramos ME, Avery PB, Jaronski ST, Vandenberg JD (2010) Comparative virulence of Beauveria bassiana isolates against lepidopteran pests of vegetable crops. J Invertebr Pathol 103(3):186–199

    Article  CAS  PubMed  Google Scholar 

  • Zhang SL, He LM, Chen X, Huang B (2013) Beauveria lii sp. nov. isolated from Henosepilachna vigintioctopunctata. Mycotaxon 121(1):199–206

    Article  Google Scholar 

  • Zola ME, Pukkila PJ (1986) Inheritance of DNA methylation in Coprinus cinereus. Mol Cell Biol 6(1):195–200

    Article  Google Scholar 

Download references

Acknowledgements

We thank the following individuals for their cooperation, courtesy and help in the creation of this paper: Laura Torres Monteiro, Sylvie Richart Cervera, Pascale Roux, Laura García, María López Plantey, Jonathan Gaudin, Juliette Poidatz, Antonella Balloni, Andrés Riquelme, Josefina Zuin Segura and Aurélia Nivault. Additionally, we thank the following institutions for their financial cooperation: Coorporation Vitivinicola Argentina (COVIAR), Universidad Nacional de Cuyo (SeCTyP) and INRA-Bordeaux.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rodrigo López Plantey.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Nicolai Meyling

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

López Plantey, R., Papura, D., Couture, C. et al. Characterization of entomopathogenic fungi from vineyards in Argentina with potential as biological control agents against the European grapevine moth Lobesia botrana. BioControl 64, 501–511 (2019). https://doi.org/10.1007/s10526-019-09955-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-019-09955-z

Keywords

Navigation