J. For. Sci., 2020, 66(10):420-435 | DOI: 10.17221/123/2020-JFS

Entomopathogenic fungi of the genus Beauveria and their pathogenicity to Ips typographus (Coleoptera: Curculionidae) in the Vitosha National Park, BulgariaOriginal Paper

Marek Barta ORCID...*,1, Danail Takov2, Daniela Pilarska2,3, Danail Doychev4, Miriam Kádasi Horáková1
1 Institute of Forest Ecology, Slovak Academy of Sciences, Nitra, Slovak Republic
2 Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Sofia, Bulgaria
3 Department of Natural Sciences, New Bulgarian University, Sofia, Bulgaria
4 University of Forestry, Sofia, Bulgaria

Ips typographus is a serious pest for forestry in Eurasia. Effective control is difficult due to its cryptic habits and insect pathogenic microorganisms, including entomopathogenic fungi that are believed to be a promising alternative to the traditional control measures of this pest. In 2018, diversity of entomopathogenic fungi of the genus Beauveria was studied in populations of I. typographus in the Vitosha National Park, Bulgaria. Two species, B. bassiana and B. caledonica, were identified and 33 in vitro strains were obtained. Phylogenetic positions of the strains were evaluated according to phylogenetic inferences based on ITS and TEF-1α. Pathogenicity of the strains against bark beetles was tested in laboratory. All strains were pathogenic, although there was some variability in the efficacy of B. bassiana strains. Virulence of the five most pathogenic strains (four B. bassiana strains and one B. caledonica strain) was compared with the commercial mycoinsecticide Boverol® and highly-virulent B. bassiana strain ARSEF 12957 isolated from I. typographus in Slovakia. The strain from Boverol® was least virulent and the Slovak strain ARSEF 12957 was more efficient than the Bulgarian strains, but the difference was not significant. The laboratory experiments suggest that the Bulgarian strains have a potential for the control of bark beetle adults.

Keywords: Beauveria; bark beetles; natural fungal infection; spruce forests; virulence

Published: October 31, 2020  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Barta M, Takov D, Pilarska D, Doychev D, Horáková MK. Entomopathogenic fungi of the genus Beauveria and their pathogenicity to Ips typographus (Coleoptera: Curculionidae) in the Vitosha National Park, Bulgaria. J. For. Sci.. 2020;66(10):420-435. doi: 10.17221/123/2020-JFS.
Download citation

References

  1. Agrawal Y., Mual P., Shenoy B.D. (2014): Multi-gene genealogies reveal cryptic species Beauveria rudraprayagi sp. nov. from India. Mycosphere, 5: 719-736. Go to original source...
  2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. (1997): Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25: 3389-3402. Go to original source... Go to PubMed...
  3. Ariyawansa H.A., Hyde K.D., Jayasiri S.C., Buyck B., Chethana K.W.T. (2015): Fungal diversity notes 111-252-taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers, 75: 27-274. Go to original source...
  4. Barta M., Kádasi Horáková M., Georgieva M., Mirchev P., Zaemdzhikova G., Pilarska D., Takov D., Todorov M., Hubenov Z., Pilarski P., Georgiev G. (2020): Entomopathogenic fungi (Ascomycota: Hypocreales) as natural antagonists of the pine processionary moth, Thaumetopoea pityocampa (Lepidoptera: Notodontidae), in Bulgaria. Acta Zoologica Bulgarica, Supplement 15: 89-96.
  5. Barta M., Kautmanová I., Čičková H., Ferenčík J., Florián Š., Novotný J., Kozánek M. (2018a): 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. Go to original source...
  6. Barta M., Kautmanová I., Čičková H., Ferenčík J., Florián Š., Novotný J., Kozánek M. (2018b): The potential of Beauveria bassiana inoculum formulated into a polymeric matrix for a microbial control of spruce bark beetle. Biocontrol Science and Technology, 28: 718-735. Go to original source...
  7. Barta M., Kautmanová I., Kozánek M., Čičková H. (2018c): Highly virulent strain of entomopathogenic fungus Beauveria bassiana DSM 32081 for use in biological control of spruce bark beetle. SK patent 5046-2015. Sept 3, 2018.
  8. Bisset J., Widden P. (1988): A new species of Beauveria isolated from Scottish moorland soil. Canadian Journal of Botany, 66: 361-362. Go to original source...
  9. Bustamante D.E., Oliva M., Leiva S., Mendoza J.E., Bobadilla L., Angulo G., Calderon M.S. (2019): Phylogeny and species delimitations in the entomopathogenic genus Beauveria (Hypocreales, Ascomycota), including the description of B. peruviensis sp. nov. MycoKeys, 58: 47-68. Go to original source... Go to PubMed...
  10. Chen M.J., Huang B., Li Z.Z., Spatafora J.W. (2013): Morphological and genetic characterisation of Beauveria sinensis sp. nov. from China. Mycotaxon, 124: 301-308. Go to original source...
  11. Chen W.H., Han Y.F., Liang Z.Q., Jin D.C. (2017): A new araneogenous fungus in the genus Beauveria from Guizhou, China. Phytotaxa, 302: 57-64. Go to original source...
  12. Chen W.H., Liu M., Huang Z.X., Yang G.M., Han Y.F., Liang J.D., Liang Z.Q. (2018): Beauveria majiangensis, a new entomopathogenic fungus from Guizhou, China. Phytotaxa, 333: 243-250. Go to original source...
  13. Chen Z.H., Chen K., Dai Y.D., Zheng Y., Wang Y.B., Yang X.N., Yu H., Yang Y.M., Xu, L. (2019): Beauveria species diversity in the Gaoligong Mountains of China. Mycological Progress, 18: 933-943. Go to original source...
  14. Cognato A.I. (2015): Biology, systematics, and evolution of Ips. In: Vega F.E., Hofstetter R.W. (eds): Bark beetles: biology and ecology of native and invasive species. San Diego, Elsevier: 351-370. Go to original source...
  15. de Faria M.R., Wraight S.P. (2007): Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biological Control, 43: 237-256. Go to original source...
  16. 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 Science, 44: 24-28.
  17. Draganova S., Takov D., Doychev D. (2010): Naturallyoccurring entomopathogenic fungi on three bark beetle species (Coleoptera: Curculionidae) in Bulgaria. Pesticidi i Fitomedicina (Belgrade), 25: 59-63. Go to original source...
  18. Draganova S.A., Doychev D.D., Pilarska D.K., Takov D.I. (2017): Bioassays of entomopathogenic fungi against xylophagous insects in Bulgaria: laboratory and field experiments. Acta Zoologica Bulgarica, 69: 411-419.
  19. Edgar R.C. (2004): MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic acids research, 32: 1792-1797. Go to original source... Go to PubMed...
  20. Finney D.J. (1971): Probit Analysis. 3rd ed. London, Cambridge University Press: 333.
  21. Galko J., Nikolov Ch., Rell S., Kunca A., Vakula J., Gubka A., Zúbrik M. (2014): Vývoj nových typov feromónových lapačov. [The development of new types of pheromone traps]. In: Kunca, A. (ed): Proceedings of the 23rd conference "Aktuálne problémy v ochrane lesa 2014", Nový Smokovec, Apr 23-24, 2014: 182-187. (in Slovak)
  22. Gardes M., Bruns T.D. (1993): ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology, 2: 113-118. Go to original source... Go to PubMed...
  23. Georgiev G., Mirchev P., Tsankov G., Rossnev B., Petkov P. (2006): Outbreak of Ips typographus (L.) (Coleoptera: Scolytidae) and drying of Norway spruce on Vitosha Mountain. In: Stampfer K. et al. (eds): Proceedings of the 39th International Symposium FORMEC 2006 - Forestry mechanization, Sofia, Sept 24-28, 2006: 218-220.
  24. Glare T.R., Reay S.D., Nelson T.L., Moore R. (2008): Beauveria caledonica is a naturally occurring pathogen of forest beetles. Mycological Research, 112: 352-360. Go to original source... Go to PubMed...
  25. Grégoire J.C., Evans H.F. (2004): Damage and control of Bawbilt organisms - an overview. In: Lieutier F., Day K.R., Battisti A., Grégoire J.C., Evans H.F. (eds): Bark and Wood Boring Insects in Living Trees in Europe, A Synthesis. Dordrecht, Kluwer Academic Publishers: 19-37. Go to original source...
  26. 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 Research Papers, 76: 5-17. Go to original source...
  27. Herrmann F., Wegensteiner R. (2010): Infecting Ips typographus (Coleoptera, Curculionidae) with Beauveria bassiana, Metarhizium anisopliae or Isaria fumosorosea (Ascomycota). IOBC/WPRS Bulletin, 66: 209-212.
  28. Humber R.A. (2012): Identification of entomopathogenic fungi. In: Lacey L.A. (ed.): Manual of Techniques in Invertebrate Pathology. Amsterdam, Academic Press: 151-187. Go to original source...
  29. Jakuš R., Blaženec M. (2011): Treatment of bark beetle attacked trees with entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin. Folia Forestalia Polonica, series A, 53: 150-155.
  30. Kausrud K., Økland B., Skarpaas O., Grégoire J.C., Erbilgin N., Stenseth N.C. (2012): Population dynamics in changing environments: the case of an eruptive forest pest species. Biological Reviews, 87: 34-51. Go to original source... Go to PubMed...
  31. Kepler R.M., Luangsa-ard J.J., Hywel-Jones N.L., Quandt C.A., Sung G.H., Rehner S.A., Aime M.C., Henkel T.W., Sanjuan T., Zare R., Chen M.J., Li Z.Z., Rossman A.Y., Spatafora J.W., Shrestha B. (2017): A phylogeneticallybased nomenclature for Cordycipitaceae (Hypocreales). IMA Fungus, 8: 335-353. Go to original source... Go to PubMed...
  32. Khonsanit A., Luangsa-ard J.J., Thanakitpipattana D., Noisripoom W., Chaitika T., Kobmoo N. (2020): Cryptic diversity of the genus Beauveria with a new species from Thailand. Mycological Progress, 19: 291-315. Go to original source...
  33. Kirschner R. (2001): Diversity of filamentous fungi in bark beetle galleries in central Europe. In: Misra J.K., Horn B.W. (eds): Trichomycetes and Other Fungal Groups. Enfield, Science Publishers: 175-196.
  34. 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). Turkish Journal of Agriculture and Forestry, 40: 241-248. Go to original source...
  35. Kreutz J., Vaupel O., Zimmermann G. (2004a): Efficacy of Beauveria bassiana (Bals.) Vuill. against the spruce bark beetle, Ips typographus L., in the laboratory under various conditions. Journal of Applied Entomology, 128: 384-389. Go to original source...
  36. Kreutz J., Zimmermann G., Vaupel, O. (2004b): 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 Science and Technology, 14: 837-848. Go to original source...
  37. Kumar S., Stecher G., Li M., Knyaz C., Tamura K. (2018): MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35: 1547-1549. Go to original source... Go to PubMed...
  38. Lacey L.A., Grzywacz D., Shapiro-Ilan D.I., Frutos R., Brownbridge M., Goettel M.S. (2015): Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology, 132: 1-41. Go to original source... Go to PubMed...
  39. Landa Z., Horňák P., Osborne L.S., 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.
  40. Medo J., Michalko J., Medová J., Cagáň Ľ. (2016): Phylogenetic structure and habitat associations of Beauveria species isolated from soils in Slovakia. Journal of Invertebrate Pathology, 140: 46-50. Go to original source... Go to PubMed...
  41. Modlinger R., Novotný P. (2015): Quantification of time delay between damages caused by windstorms and by Ips typographus. Central European Forestry Journal, 61: 221-231. Go to original source...
  42. Mudrončeková S., Mazán M., Nemcovic M., Salamon I. (2013): Entomopathogenic fungus species Beauveria bassiana (Bals.) and Metarhizium anisopliae (Metsch.) used as mycoinsecticide effective in biological control of Ips typographus (L.). The Journal of Microbiology, Biotechnology and Food Sciences, 2: 2469.
  43. Netherer S., Matthews B., Katzensteiner K., Blackwell E., Henschke P., Hietz P., Pennerstorfer J., Rosner S., Kikuta S., Schume H., Schopf A. (2015): Do water-limiting conditions predispose Norway spruce to bark beetle attack? New Phytologist, 205: 1128-1141. Go to original source... Go to PubMed...
  44. Nikolov C., Konopka B., Kajba M., Galko J., Kunca A., Jansky L. (2014): Post-disaster forest management and bark beetle outbreak in Tatra National Park, Slovakia. Mountain Research and Development, 34: 326-335. Go to original source...
  45. 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 Ecology and Management, 363: 63-73. Go to original source...
  46. Panayotov M., Bebi P., Tsvetanov N., Alexandrov N., Laranjeiro L., Kulakowski D. (2015): The disturbance regime of Norway spruce forests in Bulgaria. Canadian Journal of Forest Research, 45: 1143-1153. Go to original source...
  47. Panayotov M., Georgiev D. (2012): Dynamics in the Ips typographus outbreak following the 2001 windthrow in Bistrishko branishte Reserve, Bulgaria. Silva Balcanica, 1: 38-48.
  48. Rehner S.A., Buckley E.P.A (2005): Beauveria phylogeny inferred from ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia, 97: 84-98. Go to original source... Go to PubMed...
  49. Rehner S.A., Posada F., Buckley E.P., Infante F., Castillo A., Vega F.E. (2006): Phylogenetic origins of African and Neotropical Beauveria bassiana s. l. pathogens of the coffee berry borer, Hypothenemus hampei. Journal of Invertebrate Pathology, 93: 11-21. Go to original source... Go to PubMed...
  50. Rehner S.A., Minnis A.M., Sung G.H., Luangsa-ard J.J., Devotto L., Humber R.A. (2011): Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia, 103: 1055-1073. Go to original source... Go to PubMed...
  51. Robène-Soustrade I., Jouen E., Pastou D., Payet-Hoarau M., Goble T., Linderme D., Lefeuvre P., Calmès C., Reynaud B., Nibouche S., Costet L. (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. Go to original source... Go to PubMed...
  52. Rossnev B.G., Georgiev P., Mirchev G., Tsankov P., Petkov (2005): Influence of the wind throw in biosphere reserve Bistrishko branishte on the number of Ips typographus (L.) (Coleoptera: Scolytidae) and the condition of Picea abies L. (Karst.) plantations on Vitosha. Agricultural University - Plovdiv, Scientific Works, 50: 239-244. (in Russian with English abstract)
  53. Sanjuan T., Tabima J., Restrepo S., Laessøe T., Spatafora J.W., Franco-Molano A.E. (2014): Entomopathogens of Amazonian stick insects and locusts are members of the Beauveria species complex (Cordyceps sensu stricto). Mycologia, 106: 260-275. Go to original source... Go to PubMed...
  54. Stadelmann G., Bugmann H., Wermelinger B., Bigler C. (2014): Spatial interaction between storm damage and subsequent infestations by the European spruce bark beetle. Forest Ecology and Management, 318: 167-174. Go to original source...
  55. Sung G.H., Hywel-Jones N.L., Sung J.M., Luangsa-ard J.J., Shrestha B., Spatafora J.W. (2007): Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Studies in Mycology, 57: 5-59. Go to original source... Go to PubMed...
  56. Takov D., Pilarska D., Wegensteiner R. (2006): Entomopathogens in Ips typographus (Coleoptera: Scolytidae) from several spruce stands in Bulgaria. Acta Zoologica Bulgarica, 58: 409-420.
  57. Takov D., Doychev D., Wegensteiner R., Pilarska D. (2007): Study of bark beetle (Coleoptera, Scolytidae) pathogens from coniferous stands in Bulgaria. Acta Zoologica Bulgarica, 59: 87-96.
  58. Takov D., Doychev D., Linde A., Draganova S., Pilarska D. (2011): Pathogens of bark beetles (Coleoptera: Curculionidae) in Bulgarian forests. Phytoparasitica, 39: 343-352. Go to original source...
  59. Takov D., Doychev D., Linde A., Draganova, S., Pilarska D. (2012): Pathogens of bark beetles (Curculionidae: Scolytinae) and other beetles in Bulgaria. Biologia, 67: 966-972. Go to original source...
  60. Tamura K., Nei, M. (1993): Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10: 512-526. Go to PubMed...
  61. Vakula J., Sitková Z., Galko J., Gubka A., Zúbrik M., Kunca A., Rell S. (2014): Impact of irrigation on the gallery parameters of spruce bark beetle (Ips typographus L., Coleoptera: Curculionidae, Scolytinae). Forestry Journal, 60: 61-67. Go to original source...
  62. Vakula J., Zúbrik M., Galko J., Gubka A., Kunca A., Nikolov C., Bošeľa M. (2015): Influence of selected factors on bark beetle outbreak dynamics in the Western Carpathians. Forestry Journal, 61: 149-156. Go to original source...
  63. Vakula J., Kunca A., Barta M., Lalík M., Galko J., Gubka A., Zúbrik M., Rell S., Nikolov C. (2019): Vertical transmission of the Beauveria bassiana between the double-spined bark beetle Ips duplicatus. In: Duduman M.L., Lupaștean D., Horodnic S.A., Palaghianu C. (eds): Recent Changes in Forest Insects and Pathogens Significance - IUFRO Meeting WP 7.03.10 "Methodology of forest insect and disease survey in Central Europe", Suceava, Sept 16-20, 2019: 87.
  64. 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). Anzeiger für Schädlingskunde Pflanzenschutz Umweltschutz, 69: 175-179. (in German with English abstract) Go to original source...
  65. Vega F.E., Kaya H.K. (2012): Insect Pathology. 2nd ed. San Diego, Academic Press: 508.
  66. Wang Y., Tang D.X., Duan D.E., Wang Y.B., Yu, H. (2020): Morphology, molecular characterization, and virulence of Beauveria pseudobassiana isolated from different hosts. Journal of Invertebrate Pathology, 172: 107333. Go to original source... Go to PubMed...
  67. Wegensteiner R. (1996): Laboratory evaluation of Beauveria bassiana (Bals.) Vuill. against the bark beetle, Ips typographus (L.) (Coleoptera, Scolytidae). IOBC/WPRS Bulletin, 19: 186-189
  68. Wegensteiner R. (2007): Pathogens in bark beetles. In: Lieutier F., Day K.R., Battisti A., Grégoire J.C., Evans H.F. (eds): Bark and Wood Boring Insects in Living Trees in Europe, A Synthesis. Dordrecht, Springer: 291-313. Go to original source...
  69. Wegensteiner R., Tkaczuk C., Bałazy S., Griesser S., Rouffaud M.A., Stradner A., Steinwender B.M., Hager H., Papierok B. (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 Protozoologica, 54: 219-232.
  70. Wegensteiner R., Wermelinger B., Herrmann M. (2015b): Natural enemies of bark beetles: predators, parasitoids, pathogens, and nematodes. In: Vega F.E., Hofstetter R.W. (eds): Bark Beetles - Biology and Ecology of Native and Invasive Species. London, Academic Press: 247-304. Go to original source...
  71. Wermelinger B. (2004): Ecology and management of the spruce bark beetle Ips typographus - a review of recent research. Forest Ecology and Management, 202: 67-82. Go to original source...
  72. Zhang S.L., He L.M., Chen X., Huang B. (2012): Beauveria lii sp. nov. isolated from Henosepilachna vigintioctopunctata. Mycotaxon, 121: 199-206. Go to original source...
  73. Zimmermann G. (2007): Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Science and Technology, 17: 553-596. Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.