Skip to main content
Log in

Hypocrealean fungi associated with populations of Ips typographus in West Carpathians and selection of local Beauveria strains for effective bark beetle control

  • Original Article
  • Published:
Biologia Aims and scope Submit manuscript

Abstract

In Slovakia, a diversity of entomopathogenic fungi (Ascomycota, Hypocreales) associated with outbreaks of Ips typographus was studied in 81 localities and as many as 113 in vitro cultures of five entomopathogenic species were isolated from infected individuals: Beauveria bassiana (87 isolates), B. pseudobassiana (14 isolates), B. caledonica (6 isolates), Lecanicillium lecanii (4 isolates) and Isaria farinosa (2 isolates). B. pseudobassiana is recorded in natural populations of I. typographus for the first time. Biological properties of selected Beauveria isolates, including colony growth, biomass production, conidia yield and pathogenicity to I. typographus adults, were studied in a series of laboratory bioassays and much intra- and interspecific variability was detected. B. bassiana isolates produced biomass or conidia at significantly higher rate than B. pseudobassiana and B. caledonica isolates. Two B. bassiana isolates were selected as the most virulent to bark beetle adults, demonstrating a mean LC50 ranging from 0.72 to 2.05 × 106 conidia ml−1, and were qualified as promising candidates for biocontrol of I. typographus. Their virulence was significantly higher than that of the mycoinsecticides Boverol®, which was used as a reference strain in the virulence bioassays.

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
Fig. 3

Similar content being viewed by others

References

  • Agrawal Y, Mual P, Shenoy BD (2014) Multi-gene genealogies reveal cryptic species Beauveria rudraprayagi sp. nov. from India. Mycosphere 5:719–736

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. https://doi.org/10.1093/nar/25.17.3389

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ariyawansa HA, Hyde KD, Jayasiri SC et al (2015) Fungal diversity notes 111–252—taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 75:27–274. https://doi.org/10.1007/s13225-015-0346-5

    Article  Google Scholar 

  • Augustyniuk-Kram A, Kram KJ (2012) Entomopathogenic fungi as an important natural regulator of insect outbreaks in forests (Review). In: Blanco JA, Lo YH (eds) Forest ecosystems - more than just trees. InTech, Rijeka, pp 265–294

    Google Scholar 

  • Barta M (2010) Pathogenicity assessment of entomopathogenic fungi infecting Leptoglossus occidentalis (Heteroptera: Coreidae). Czech Mycol 62:67–78

    Google Scholar 

  • Bisset J, Widden P (1988) A new species of Beauveria isolated from Scottish moorland soil. Can J Bot 66:361–362

    Article  Google Scholar 

  • Bugeme DM, Maniania NK, Knapp M, Boga HI (2008) Effect of temperature on virulence of Beauveria bassiana and Metarhizium anisopliae isolates to Tetranychus evansi. Exp Appl Acarol 46:275–285. https://doi.org/10.1007/s10493-008-9179-1

    Article  PubMed  Google Scholar 

  • Chen MJ, Huang B, Li Z, Spatafora JW (2013) Morphological and genetic characterisation of Beauveria sinensis sp. nov. from China. Mycotaxon 124:301–308. https://doi.org/10.5248/124.301

    Article  Google Scholar 

  • Draganova S, Takov D, Doychev D (2007) Bioassays with isolates of Beauveria bassiana (Bals.) Vuill. and Paecilomyces farinosus (Holm.) Brown & Smith against Ips sexdentatus Boerner and Ips acuminatus Gyll. (Coleoptera: Scolytidae). Plant Sci 44:24–28

    Google Scholar 

  • Draganova S, Takov D, Doychev D (2010) Naturally-occurring entomopathogenic fungi on three bark beetle species (Coleoptera: Curculionidae) in Bulgaria. Pestic Phytomedicine (Belgrade) 25:59–63. https://doi.org/10.2298/PIF1001059D

    Article  Google Scholar 

  • Falťan V, Bánovský M, Blažek M (2011) Evaluation of land cover changes after extraordinary windstorm by using the land cover metrics: a case study on the high Tatras foothill. Aust Geogr 116:156–171

    Google Scholar 

  • Ferenčík J (2016) Lykožrút smrekový vo Vysokých Tatrách [European spruce bark beetle in Tatra Mts]. In: Zouhar V (ed) Proceedings of conference Karpatské lesy, Bunč, Czech Republic, pp 101–114

  • Fernandes EK, Angelo IC, Rangel DE et al (2011) An intensive search for promising fungal biological control agents of ticks, particularly Rhipicephalus microplus. Vet Parasitol 182:307–318. https://doi.org/10.1016/j.vetpar.2011.05.046

    Article  PubMed  Google Scholar 

  • Finney DJ (1971) Probit analysis. Cambridge University Press, London

    Google Scholar 

  • Fleischer P Jr, Fleischer P, Ferenčík J, Hlaváč P, Kozánek M (2016) Elevated bark temperature in unremoved stumps after disturbances facilitates multi-voltinism in Ips typographus population in a mountainous forest. Lesn Cas For J 62:15–22. https://doi.org/10.1515/forj-2016-0002

    Google Scholar 

  • Fora CG, Banu CM, Chisăliţă I, Moatăr MM, Oltean I (2014) Parasitoids and predators of Ips typographus (L.) in unmanaged and managed spruce forests in Natural Park Apuseni, Romania. Not Bot Horti Agrobo 42:270–274. https://doi.org/10.15835/nbha4219430

    Google Scholar 

  • Glare TR, Reay SD, Nelson TL, Moore R (2008) Beauveria caledonica is a naturally occurring pathogen of forest beetles. Mycol Res 112:352–360. https://doi.org/10.1016/j.mycres.2007.10.015

    Article  CAS  PubMed  Google Scholar 

  • Goettel MS, Poprawski TJ, Vandenberg JD, Li Z, Roberts DW (1990) Safety to non-target invertebrates of fungal biocontrol agents. In: Laird M, Lacey LA, Davidson EW (eds) Safety of microbial insecticides. CRC Press, Boca Raton, pp 209–231

    Google Scholar 

  • Grodzki W, Kosibowicz M (2015) An attempt to use the fungus Beauveria bassiana (Bals.) Vuill. In forest protection against the bark beetle Ips typographus (L.) in the field. Forest Res Pap 76:5–17. https://doi.org/10.1515/frp-2015-0001

    Google Scholar 

  • Hallet S, Gregoire JC, Coremans-Pelseneer J (1994) Prospects in the use of the entomopathogenous fungus Beauveria bassiana (Bals.) Vuill. (Deuteromycetes: Hyphomycetes) to control the spruce bark beetle Ips typographus L. (Coleoptera: Scolytidae). Meded Fak Landbouwwet R U Gent 59:379–383

    Google Scholar 

  • Herrmann F, Wegensteiner R (2010) Infecting Ips typographus (Coleoptera, Curculionidae) with Beauveria bassiana, Metarhizium anisopliae or Isaria fumosorosea (Ascomycota). IOBC/wprs Bull 66:209–212

    Google Scholar 

  • Hilszczański J, Gibb H, Bystrowski C (2007) Insect natural enemies of Ips typographus (L.) (Coleoptera, Scolytinae) in managed and unmanaged stands of mixed lowland forest in Poland. J Pest Sci 80:99–107. https://doi.org/10.1007/s10340-006-0160-7

    Article  Google Scholar 

  • Humber RA (2012) Identification of entomopathogenic fungi. In: Lacey LA (ed) Manual of techniques in invertebrate pathology. Academic Press, Amsterdam, pp 151–187

    Chapter  Google Scholar 

  • Imoulan A, Wu HJ, Lu WL et al (2016) Beauveria medogensis sp. nov., a new fungus of the entomopathogenic genus from China. J Invertebr Pathol 139:74–81. https://doi.org/10.1016/j.jip.2016.07.006

    Article  CAS  PubMed  Google Scholar 

  • Jakuš R, Blaženec M (2011) Treatment of bark beetle attacked trees with entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin. Folia Forest Polonica, ser A 53:150–155

    Google Scholar 

  • Kaplan EL, Meier P (1958) Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457–481

    Article  Google Scholar 

  • Kautz M, Dworschak K, Gruppe A, Schopf R (2011) Quantifying spatio-temporal dispersion of bark beetle infestations in epidemic and non-epidemic conditions. Forest Ecol Manag 262:598–608. https://doi.org/10.1016/j.foreco.2011.04.023

    Article  Google Scholar 

  • Kirschner R (2001) Diversity of filamentous fungi in bark beetle galleries in central Europe. In: Misra JK, Horn BW (eds) Trichomycetes and other fungal groups: Robert W. Lichtwardt Commemoration Volume. Science Publishers Inc., Enfield, pp. 175–196.

    Google Scholar 

  • Kocaçevik S, Sevim A, Eroğlu M, Demirbağ Z, Demir I (2016) Virulence and horizontal transmission of Beauveria pseudobassiana S.A. Rehner & Humber in Ips sexdentatus and Ips typographus (Coleoptera: Curculionidae). Turk J Agric For 40:241–248. https://doi.org/10.3906/tar-1504-64

    Article  Google Scholar 

  • Kreutz J, Zimmermann G, Vaupel O (2004a) Horizontal transmission of the entomopathogenic fungus Beauveria bassiana among the spruce bark beetle, Ips typographus (Col., Scolytidae) in the laboratory and under field conditions. Biocontrol Sci Tech 14:837–848. https://doi.org/10.1080/788222844

    Article  Google Scholar 

  • Kreutz J, Vaupel O, Zimmermann G (2004b) Efficacy of Beauveria bassiana (Bals.) Vuill. Against the spruce bark beetle, Ips typographus L., in the laboratory under various conditions. J Appl Entomol 128:384–389. https://doi.org/10.1111/j.1439-0418.2004.00813.x

    Article  Google Scholar 

  • Kunca A, Zúbrik M (2006) Vetrová kalamita z 19. 11. 2004. In: National Forest Centre (ed). Lesmedium, Bratislava, p. 40. Available at: http://www.forestportal.sk/lesne-hospodarstvo/ochrana-lesa/Documents/Kunca_kalamita.pdf

  • Lacey LA, Grzywacz D, Shapiro-Ilan DI et al (2015) Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 132:1–41. https://doi.org/10.1016/j.jip.2015.07.009

    Article  CAS  PubMed  Google Scholar 

  • Landa Z, Horňák P, Osborne LS, Nováková A, Bursová E (2001) Entomogenous fungi associated with spruce bark beetle Ips typographus L. (Coleoptera, Scolytidae) in the bohemian Forest. Silva Gabreta 6:259–272

    Google Scholar 

  • Markova G (2000) Pathogenicity of several entomogenous fungi to some of the most serious forest insect pests in Europe. IOBC/wprs Bull 23:231–239

    Google Scholar 

  • Medo J, Michalko J, Medová J, Cagáň Ľ (2016) Phylogenetic structure and habitat associations of Beauveria species isolated from soils in Slovakia. J Invertebr Pathol 140:46–50. https://doi.org/10.1016/j.jip.2016.08.009

    Article  PubMed  Google Scholar 

  • Mudrončeková S, Mazáň M, Nemčovič M, Šalamon I (2013) Entomopathogenic fungus species Beauveria bassiana (Bals.) and Metarhizium anisopliae (Metsch.) used as mycoinsecticide effective in biological control of Ips typographus (L.) J Microbiol Biotechnol Food Sci 2:2469–2472

    Google Scholar 

  • Økland B, Bjørnstad ON (2006) A resource-depletion model of forest insect outbreaks. Ecology 87:283–290. https://doi.org/10.1890/05-0135

    Article  PubMed  Google Scholar 

  • Økland B, Netherer S, Marini L (2015) The Eurasian spruce bark beetle: the role of climate. In: Björkman C, Niemelä P (eds) Climate change and insect pests. CABI, Wallingford, pp 202–219. https://doi.org/10.1079/9781780643786.0202

    Chapter  Google Scholar 

  • Økland B, Nikolov C, Krokene P, Vakula J (2016) Transition from windfall- to patch-driven outbreak dynamics of the spruce bark beetle Ips typographus. Forest Ecol Manag 363:63–73. https://doi.org/10.1016/j.foreco.2015.12.007

    Article  Google Scholar 

  • Püntener W (1981) Manual for field trials in plant protection. Ciba-Geigy, Basle

    Google Scholar 

  • Ravensberg WJ (2011) Mass production and product development of a microbial pest control agent. In: Ravensberg WJ (ed) A roadmap to the successful development and commercialization of microbial pest control products for control of arthropods. Springer, New York, pp 59–127

    Chapter  Google Scholar 

  • Reddy KRK, PraveenKumar D, Reddy KRN (2013) Entomopathogenic fungi: a potential bioinsecticide. Kavaka 41:23–32

    Google Scholar 

  • Rehner SA, Buckley EP (2005) A Beauveria phylogeny inferred from ITS and EF1-a sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98. https://doi.org/10.1080/15572536.2006.11832842

    CAS  PubMed  Google Scholar 

  • Rehner SA, Minnis AM, Sung GH et al (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073. https://doi.org/10.3852/10-302

    Article  PubMed  Google Scholar 

  • Robène-Soustrade I, Jouen E, Pastou D et al (2015) Description and phylogenetic placement of Beauveria hoplocheli sp. nov. used in the biological control of the sugarcane white grub, Hoplochelus marginalis, on Reunion Island. Mycologia 107:1221–1232. https://doi.org/10.3852/14-344

    Article  PubMed  Google Scholar 

  • Seidl R, Müller J, Hothorn T et al (2015) Small beetle, large-scale drivers: how regional and landscape factors affect outbreaks of the European spruce bark beetle. J Appl Ecol 53:530–540. https://doi.org/10.1111/1365-2664.12540

    Article  PubMed Central  PubMed  Google Scholar 

  • Stadelmann G, Bugmann H, Wermelinger B, Bigler C (2014) Spatial interactions between storm damage and subsequent infestations by the European spruce bark beetle. Forest Ecol Manag 318:167–174. https://doi.org/10.1016/j.foreco.2014.01.022

    Article  Google Scholar 

  • Sujeetha JARP, Sahayaraj K (2014) Role of entomopathogenic fungus in pest management. In: Sahayaraj K (ed) Basic and applied aspects of biopesticides. Springer, New Delhi, pp 31–46

    Google Scholar 

  • Takov D, Doychev D, Linde A et al (2012) Pathogens of bark beetles (Curculionidae: Scolytinae) and other beetles in Bulgaria. Biologia 67:966–972. https://doi.org/10.2478/s11756-012-0086-x

    Article  Google Scholar 

  • Vakula J, Kunca A, Zúbrik M et al (2007) Distribution of two invasive pests in Slovakia since 1996. In: Evans H, Oszako T (eds) Alien invasive species and international trade. IUFRO UNIT, Jedlnia, pp 105–113

    Google Scholar 

  • Vakula J, Gubka A, Galko J, Varkonda Š (2012) Aplikácia entomopatogénov do populácií škodcov s využitím feromónových lapačov [Application of entomopathogenic fungi into pest populations using pheromone traps]. In: Kunca A (ed) Aktuálne problémy v ochrane lesa 2012. National Forest Centre, Zvolen, pp 92–96

    Google Scholar 

  • Vakula J, Gubka A, Galko J, Kunca A, Zúbrik M (2013) Podkôrny hmyz – pretrvávajúca hrozba smrečín Slovenska. Aké sú dôvody? [Bark beetles - the continuing threat of spruce forests of Slovakia. What are the reasons?] Les a Letokruhy 7–8:38–39

  • Vaupel O, Zimmermann G (1996) Orientierende Versuche zur Kombination von Pheromonfallen mit dem insektenpathogenen Pilz Beauveria bassiana (Bals.) Vuill. gegen die Borkenkäferart lps typographus L. (Col., Scolytidae) [Preliminary trials on the combination of pheromone traps with the entomopathogenic fungus Beauveria bassiana (Bals.) Vuill. against the bark beetle species Ips typographus L. (Col., Scolytidae)]. Anz Schadlingskd Pfl 69:175–179

    Article  Google Scholar 

  • Vega FE, Meyling NV, Luangsa-Ard JJ, Blackwell M (2012) Chapter 6 – Fungal Entomopathogens. In: Vega FE, Kaya HK (eds) Insect pathology. Academic Press, San Diego, pp 171–220. https://doi.org/10.1016/B978-0-12-384984-7.00006-3

    Chapter  Google Scholar 

  • Vicentini S, Faria MR, Oliveira MRV (2001) Screening of Beauveria bassiana (Deuteromycotina: Hyphomycetes) isolates against nymphs of Bemisia tabaci (Genn.) biotype B (Hemiptera: Aleyrodidae) with description of a new bioassay method. Neotrop Entomol 30:97–103. https://doi.org/10.1590/S1519-566X2001000100015

    Article  Google Scholar 

  • Wegensteiner R (1992) Untersuchungen zur Wirkung von Beauveria-Arten auf Ips typographus (Col., Scolytidae) [Studies on the effect of Beauveria species on Ips typographus (Col., Scolytidae)]. Mitt Dtsch Ges Allg Angew Entomol 8:104–106

    Google Scholar 

  • Wegensteiner R (1996) Laboratory evaluation of Beauveria bassiana (Bals.) Vuill. against the bark beetle, Ips typographus (L.) (Coleoptera, Scolytidae). IOBC/wprs Bull 19:186–189

    Google Scholar 

  • Wegensteiner R (2007) Pathogens in bark beetles. In: Lieutier F, Day KR, Battisti A, Grégoire JC, Evans HF (eds) Bark and wood boring insects in living trees in Europe, a synthesis. Springer, Dordrecht, pp 291–313

    Google Scholar 

  • Wegensteiner R, Dedryver CA, Pierre JS (2010) The comparative prevalence and demographic impact of two pathogens in swarming Ips typographus adults: a quantitative analysis of long term trapping data. Agr Forest Entomol 12:49–57. https://doi.org/10.1111/j.1461-9563.2009.00449.x

    Article  Google Scholar 

  • Wegensteiner R, Tkaczuk C, Bałazy S et al (2015a) Occurrence of pathogens in populations of Ips typographus, Ips sexdentatus (Coleoptera, Curculionidae, Scolytinae) and Hylobius spp. (Coleoptera, Curculionidae, Curculioninae) from Austria, Poland and France. Acta Protozool 54:219–232

    Google Scholar 

  • Wegensteiner R, Wermelinger B, Herrmann M (2015b) Natural enemies of bark beetles: predators, parasitoids, pathogens, and nematodes. In: Vega FE, Hofstetter RW (eds) Bark beetles - biology and ecology of native and invasive species. Academic press, London, pp 247–304. https://doi.org/10.1016/B978-0-12-417156-5.00007-1

    Google Scholar 

  • Wermelinger B (2004) Ecology and management of the spruce bark beetle Ips typographus – a review of recent research. Forest Ecol Manag 202:67–82. https://doi.org/10.1016/j.foreco.2004.07.018

    Article  Google Scholar 

  • 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, San Diego, pp 315–322

    Google Scholar 

  • Zhang SL, He LM, Chen X, Hueng B (2012) Beauveria lii sp. nov. isolated from Henosepilachna vigintioctopunctata. Mycotaxon 121:199–206. https://doi.org/10.5248/121.199

    Article  Google Scholar 

  • Zimmermann G (2008) The entomopathogenic fungi Isaria farinosa (formerly Paecilomyces farinosus) and the Isaria fumosorosea species complex (formerly Paecilomyces fumosoroseus): biology, ecology and use in biological control. Biocontrol Sci Tech 18:865–901. https://doi.org/10.1080/09583150802471812

    Article  Google Scholar 

Download references

Acknowledgement

This research was funded by the Operational Program of Research and Development and co-financed with the European Fund for Regional Development (EFRD). Grant: ITMS 26220220087: The development of ecological methods to control chosen forest pests in vulnerable mountainous regions of Slovakia.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marek Barta.

Electronic supplementary material

Online Resource 1

(PDF 115 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barta, M., Kautmanová, I., Čičková, H. et al. Hypocrealean fungi associated with populations of Ips typographus in West Carpathians and selection of local Beauveria strains for effective bark beetle control. Biologia 73, 53–65 (2018). https://doi.org/10.2478/s11756-018-0005-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11756-018-0005-x

Keywords

Navigation