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Fungal Diversity Associated to the Olive Moth, Prays Oleae Bernard: A Survey for Potential Entomopathogenic Fungi

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Abstract

Olive production is one of the main agricultural activities in Portugal. In the region of Trás-os-Montes, this crop has been considerably affected by Prays oleae. In order to evaluate the diversity of fungi on Prays oleae population of Trás-os-Montes olive orchards, larvae and pupae of the three annual generations (phyllophagous, antophagous and carpophagous) were collected and evaluated for fungal growth on their surface. From the 3,828 larvae and pupae, a high percentage of individuals exhibited growth of a fungal agent (40.6%), particularly those from the phyllophagous generation. From all the moth generations, a total of 43 species from 24 genera were identified, but the diversity and abundance of fungal species differed between the three generations. Higher diversity was found in the carpophagous generation, followed by the antophagous and phyllophagous generations. The presence of fungi displaying entomopathogenic features was highest in the phyllophagous larvae and pupae, with Beauveria bassiana as the most abundant taxa. The first report of Beauveria bassiana presence on Prays oleae could open new strategies for the biocontrol of this major pest in olive groves since the use of an already adapted species increases the guarantee of success of a biocontrol approach. The identification of antagonistic fungi able to control agents that cause major olive diseases, such as Verticillium dahliae, will benefit future biological control approaches for limiting this increasingly spreading pathogen.

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References

  1. Alagesaboopathi C (1994) Biological control of damping-off disease of cotton seedling. Curr Sci 66:864–868

    Google Scholar 

  2. Amóra S, Bevilaqua C, Feijó F, Silva M, Pereira R, Silva S, Alves N, Freire F, Oliveira D (2009) Evaluation of the fungus Beauveria bassiana (Deuteromycotina: Hyphomycetes), a potential biological control agent of Lutzomyia longipalpis (Diptera, Psychodidae). Biol Control 50:329–335

    Article  Google Scholar 

  3. Aquino de Muro M, Elliot S, Moore D, Parker B, Skinner M, Reid W, El Bouhssni M (2005) Molecular characterisation of Beauveria bassiana isolates obtained from overwintering sites of sunn pests (Eurygaster and Aelia species). Mycol Res 109:294–306

    Article  PubMed  CAS  Google Scholar 

  4. Bourbos V, Skoundridakis M, Metzidakis I (1999) Alternaria alternata: a new disease of leafy cuttings of olive shoots. In: Metzidakis I, Voyiatzis D (eds), Proceedings 3rd International ISHS Symposium on Olive Growing. Acta Horticulturae 474:585–587

    Google Scholar 

  5. Charnley A, Collins S (2007) Entomopathogenic fungi and their role in pest control. In: Kubicek C, Druzhinina I (eds) The Mycota, Volume 4—Environmental and Microbial Relationships 2nd edn. Springer-Verlag Berlin Heidelberg, pp 159–187.

  6. Cuthbertson A, Walters K (2005) Pathogenicity of the entomopathogenic fungus, Lecanicillium muscarium, against the sweetpotato whitefly Bemisia tabaci under laboratory and glasshouse conditions. Mycopathologia 160:315–319

    Article  PubMed  Google Scholar 

  7. Dalzoto P, Glienke-Blanco C, Kava-Cordeiro V, Ribeiro J, Kitajima E, Azevedo J (2006) Horizontal transfer and hypovirulence associated with double-stranded RNA in Beauveria bassiana. Mycol Res 110:1475–1481

    Article  PubMed  CAS  Google Scholar 

  8. De Lucca A (2007) Harmful fungi in both agriculture and medicine. Rev Iberoamer Micol 24:3–13

    Article  Google Scholar 

  9. Devi K, Sridevi V, Mohan C, 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 88:181–189

    Article  PubMed  Google Scholar 

  10. Eken C, Hayat R (2009) Preliminary evaluation of Cladosporium cladosporioides (Fresen.) de Vries in laboratory conditions, as a potential candidate for biocontrol of Tetranychus urticae Koch. World J Microbiol Biotechnol 25:489–492

    Article  Google Scholar 

  11. European Union. Council Regulation (EC) No 834/2007 of 28 June 2007

  12. Fravel D, Olivain C, Alabouvette C (2002) Fusarium oxysporum and its biocontrol. New Phytol 157:493–502

    Article  Google Scholar 

  13. Fuguet R, Vey A (2004) Comparative analysis of the production of insecticidal and melanizing macromolecules by strains of Beauveria spp.: in vivo studies. J Invertebr Pathol 85:152–167

    Article  PubMed  CAS  Google Scholar 

  14. Konstantopoulou M, Mazomenos B (2005) Evaluation of Beauveria bassiana and B. brongniartii strains and four wild-type fungal species against adults of Bactrocera oleae and Ceratitis capitata. BioControl 50:293–305

    Article  Google Scholar 

  15. Lacey L, Frutos R, Kaya H, Vail P (2001) Insect pathogens as biological control agents: do they have a future? Biol Control 21:230–248

    Article  Google Scholar 

  16. Logrieco A, Bottalico A, Mulé G, Moretti M, Perrone G (2003) Epidemiology of toxigenic fungi and their associated mycotoxins for some Mediterranean crops. Eur J Plant Pathol 109:645–667

    Article  CAS  Google Scholar 

  17. Mahmoud M (2009) Pathogenicity of three commercial products of entomopathogenic fungi, Beauveria bassiana, Metarhizum anisopilae and Lecanicillium lecanii against adults of olive fly, Bactrocera oleae (Gmelin) (Diptera: Tephritidae) in the laboratory. Plant Protect Sci 45:98–102

    Google Scholar 

  18. Malavolta C, Delrio G, Boller EF (2002) Guidelines for integrated production of olives. IOBC Technical Guideline III, 1st Edition, 25 (4), pp. 1–8.

  19. Mander U, Mikk M, Külvik M (1999) Ecological and low intensity agriculture as contributors to landscape and biological diversity. Landsc Urban Plann 46:169–177

    Article  Google Scholar 

  20. Marannino P, Santiago-Álvarez C, Lillo E, Quesada-Moraga E (2006) A new bioassay method reveals pathogenicity of Metarhizium anisopliae and Beauveria bassiana against early stages of Capnodis tenebrionis (Coleoptera; Buprestidae). J Invertebr Pathol 93:210–213

    Article  PubMed  Google Scholar 

  21. Maroco J (2003) Análise Estatística, com utilização do SPSS. Edições Sílabo, Lisboa, 822 pp

    Google Scholar 

  22. Maurer P, Couteaudieri Y, Girard P, Bridge P, Riba G (1997) Genetic diversity of Beauveria bassiana and relatedness to host insect range. Mycol Res 101:159–164

    Article  Google Scholar 

  23. Medrela-Kuder E (2010) Seasonal variations in the occurrence of culturable airborne fungi in outdoor and indoor air in Craców. Int Biodeterior Biodegrad 52:203–205

    Article  Google Scholar 

  24. Mercado-Blanco J, Rodríguez-Jurado D, Hervás A, Jiménez-Díaz R (2004) Suppression of Verticillium wilt in olive planting stocks by root-associated fluorescent Pseudomonas spp. Biol Control 30:474–486

    Article  Google Scholar 

  25. 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 

  26. Murad A, Laumann R, Mehta A, Noronha E, Franco O (2007) Screening and secretomic analysis of entomopathogenic Beauveria bassiana isolates in response to cowpea weevil (Callosobruchus maculatus) exoskeleton. Comp Biochem Physiol C 145:333–338

    Article  Google Scholar 

  27. Ordentlich A, Nachmias I (1990) Integrated control of Verticillium dahliae in potato by Trichoderma harzianum and captan. Crop Prot 9:363–366

    Article  CAS  Google Scholar 

  28. Pandey R, Arora D, Dubey R (1993) Antagonistic interactions between fungal pathogens and phylloplane fungi of guava. Mycopathologia 124:31–39

    Article  Google Scholar 

  29. Pathan A, Devi K, Vogel H, Reineke A (2007) Analysis of differential gene expression in the generalist entomopathogenic fungus Beauveria bassiana (Bals.) Vuillemin grown on different insect cuticular extracts and synthetic medium through cDNA-AFLPs. Fungal Genet Biol 44:1231–1241

    Article  PubMed  CAS  Google Scholar 

  30. Paterson R (2008) Cordyceps—A traditional Chinese medicine and another fungal therapeutic biofactory? Phytochemistry 69:1469–1495

    Article  PubMed  CAS  Google Scholar 

  31. Pereira J, Bento A, Cabanas E, Torres L, Herz A, Hassan A (2004) Ants as predators of the egg parasitoid Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae) applied for biological control of the olive moth, Prays oleae (Lepidoptera: Plutellidae) in Portugal. Biocontrol Sci Technol 14:653–664

    Article  Google Scholar 

  32. Quesada-Moraga E, Maranhao E, Valverde-García P, Santiago-Álvarez C (2006) Selection of Beauveria bassiana isolates for control of the whiteflies Bemisia tabaci and Trialeurodes vaporariorum on the basis of their virulence, thermal requirements, and toxicogenic activity. Biol Control 36:274–287

    Article  Google Scholar 

  33. Ramos P, Campos M, Ramos J (1998) Long-term study on the evaluation of yield and economic losses caused by Prays oleae Bern. in the olive crop of Granada (southern Spain). Crop Prot 17:645–647

    Article  Google Scholar 

  34. Rencher AC (1995) Methods of multivariate analysis. John Willey, New York, 708 pp

    Google Scholar 

  35. Roussos S, Zaouia N, Salih G, Tantaoui-Elaraki A, Lamrani K, Cheheb M, Hassouni H, Verh F, Perraud-Gaime I, Augur C, Ismaili-Alaoui M (2006) Characterization of filamentous fungi isolated from Moroccan olive and olive cake: toxinogenic potential of Aspergillus strains. Mol Nutr Food Res 50:500–506

    Article  PubMed  CAS  Google Scholar 

  36. Santoro P, Neves P, Alexandre T, Sartori D, Alves L, Fungaro M (2008) Selection of Beauveria bassiana isolates to control Alphitobius diaperinus. J Invertebr Pathol 97:83–90

    Article  PubMed  Google Scholar 

  37. Silva V, Barros R, Marques E, Torres J (2003) Suscetibilidade de Plutella xylostella (L.) (Lepidoptera: Plutellidae) aos Fungos Beauveria bassiana (Bals.) Vuill. e Metarhizium anisopliae (Metsch.) Sorok. Neotrop Entomol 32:653–658

    Google Scholar 

  38. Sun B, Yu H, Chen A, Liu X (2008) Insect-associated fungi in soils of field crops and orchards. Crop Prot 27:1421–1426

    Article  Google Scholar 

  39. Topbaş M, Tosun U, Çan G, Kaklikkaya N, Aydin F (2006) Identification and seasonal distribution of airborne fungi in urban outdoor air in an Eastern Black Sea Turkish town. Turk J Med Sci 31:31–36

    Google Scholar 

  40. Torres-Barragán A, Anaya A, Alatorre R, Toriello C (2004) Entomopathogenic fungi from ‘El Eden’ Ecological Reserve, Quintana Roo, Mexico. Mycopathologia 158:61–71

    Article  PubMed  Google Scholar 

  41. Vänninen I, Hokkanen H (1997) Efficacy of entomopathogenic fungi and nematodes against Argyrestthia conjugella (Lep: Yponomeutidae). Entomophaga 42:377–385

    Article  Google Scholar 

  42. Vega F, Goettel M, Blackwell M, Chandler D, Jackson M, Keller S, Koike M, Maniania N, Monzón A, Ownley B, Pell J, Rangel D, Roy H (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159

    Article  Google Scholar 

  43. Verma M, Brar S, Tyagi R, Surampalli R, Valéro J (2007) Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem Eng J 37:1–20

    Article  Google Scholar 

  44. Tj W, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Shinsky J, White Tj (eds) PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

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Acknowledgements

This work was supported by the Science and Technology Foundation (Fundação para a Ciência e Tecnologia—FCT) project PTDC/AGR-AAM/102600/2008 “entomopathogenic fungi associated to olive pests: isolation, characterization and selection for biological control”. The first author is grateful to the Science and Technology Foundation for the Ph.D. grant SFRH/BD/44265/2008.

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Authors and Affiliations

  1. CIMO/School of Agriculture, Polytechnic Institute of Bragança, Campus de Santa Apolónia, Apartado 1172, 5301-854, Bragança, Portugal

    Ivo Oliveira, José A. Pereira, Albino Bento & Paula Baptista

  2. Centre for Biodiversity Functional and Integrative Genomics (BioFIG), Plant Functional Biology Centre, University of Minho, Campus de Gualtar, 4710-057, Braga, Portugal

    Teresa Lino-Neto

Authors
  1. Ivo Oliveira
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  2. José A. Pereira
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  3. Teresa Lino-Neto
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  4. Albino Bento
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  5. Paula Baptista
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Correspondence to Paula Baptista.

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Oliveira, I., Pereira, J.A., Lino-Neto, T. et al. Fungal Diversity Associated to the Olive Moth, Prays Oleae Bernard: A Survey for Potential Entomopathogenic Fungi. Microb Ecol 63, 964–974 (2012). https://doi.org/10.1007/s00248-011-9955-z

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