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Morphological, Molecular Identification and Virulence of Entomopathogenic Fungi Isolated From Dendroctonus micans (Kugelann,1794) (Coleoptera: Curculionidae)

Year 2024, Volume: 28 Issue: 2, 381 - 391, 30.04.2024
https://doi.org/10.16984/saufenbilder.1382917

Abstract

In this study, to determine an effective fungal agent against Dendroctonus micans (Kugelann, 1794) (Coleoptera: Curculionidae), which causes significant economic losses in forested areas, Picea orientalis (L.) Link in Artvin between 2021-2022. Dendroctonus micans larvae and adults were collected from the trees, and 18 fungi were isolated from larvae and adult insects. Morphological (infection type, colony morphology, spore form) and molecular (ITS1-5.8S ITS2 gene region) characterization determined that the isolates were Metarhizium anisopliae (Metschn.) Sorokin, 1883 (Hypocreales: Clavicipitaceae), M. robertsii, M. pinghaense and Clonostachys rosea Samuels & Rossman, 1999 (Hypocreales: Bionectriaceae). Isolates M. robertsii (OZM4) and M. pinhaense (OZM9) have been isolated from this pest for the first time. As a result of insecticidal activity tests performed on D. micans larvae and adults of 1x107spore/ml spore suspension, the larvae, M. anisopliae (OZM2), showed a mortality rate of 92% within 7 days and adults mortality was determined 100% at the end of the experiment, and mycosis rates were found to be consistent with mortality rates. These results show that isolates with high virulence are promising in microbial and integrated control applications against important forest pests.

Ethical Statement

This study does not require ethics committee permission or any special permission.

Supporting Institution

The authors has no received any financial support for the research, authorship or publication of this study.

Thanks

We thank the Trabzon Regional Directorate of Forestry for their support in the making of this study.

References

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  • [2] S. Seybold, D. Huber, J. Lee, A. Graves, J. Bohlmann, ‘‘Pine monoterpenes and pine bark beetles: a marriage of convenience for defense and chemical communication,’’ Phytochemistry Reviews, vol. 5, pp. 143-178, 2006.
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  • [4] F. Armendáriz-Toledano, A. Niño, B. T. Sullivan, L. R. Kirkendall, G. Zúñiga, ‘‘A new species of bark beetle, Dendroctonus mesoamericanus sp. nov. (Curculionidae: Scolytinae), in southern Mexico and Central America,’’ Annals of the Entomological Society of America, vol. 108, no. 3, pp. 403-414, 2015.
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  • [7] J. D. Reeve, F. E. Anderson, S. T. Kelley, ‘‘Ancestral state reconstruction for Dendroctonus bark beetles: evolution of a tree killer,’’ Environmental Entomology, vol. 41, no. 3, pp. 723-730, 2012.
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  • [18] M. Yaman, Ö. Ertürk, İ. Aslan, ‘‘Isolation of some pathogenic bacteria from the great spruce bark beetle, Dendroctonus micans and its specific predator, Rhizophagus grandis,’’ Folia Microbiologica, vol. 55, pp. 35-38, 2010.
  • [19] S. Kocacevik, A. Sevim, M. Eroglu, Z. Demirbag, I. Demir, ‘‘Molecular characterization, virulence and horizontal transmission of Beauveria pseudobassiana from Dendroctonus micans (Kug.) (Coleoptera: Curculionidae),’’ Journal of Applied Entomology, vol. 139, no. 5, pp. 381-389, 2015.
  • [20] B. Lovett, R. J. St Leger, ‘‘The insect pathogens,’’ Microbiology Spectrum, vol. 5, no. 2, pp.10-1128, 2017.
  • [21] L. A. Lacey, D. Grzywacz, D. I. Shapiro-Ilan, R. Frutos, M. Brownbridge, M. S. Goettel, ‘‘Insect pathogens as biological control agents: back to the future,’’ Journal of Invertebrate Pathology, vol. 132, pp. 1-41, 2015.
  • [22] M. S. Ali-Shtayeh, A. B. B. Marai, R. M. Jamous, ‘‘Distribution, occurrence and characterization of entomopathogenic fungi in agricultural soil in the Palestinian area,’’ Mycopathologia, vol. 156, no.3, pp. 235-244, 2003.
  • [23] R. A. Humber, ‘‘Fungi: identification,’’ İNManual of techniques in insect pathology, Academic Press, 1997, pp. 153-185.
  • [24] J. L. Harris, ‘‘Modified method for fungal slide cultures,’’ Journal of Clinical Microbiology, vol. 24, no. 3, pp. 460-461, 1986.
  • [25] T. J. T. White, S. Bruns, J. Taylor, “Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics,’’ in PCR Protocols: A Guide to Methods and Applications, M. A. Innis, D. H. Gelfand, J. J. Sninsky, T. J. White. Academic Press, San Diego,1990, pp. 482.
  • [26] K. Tamura, G. Stecher, D. Peterson, A. Filipski, S. Kumar, ‘‘MEGA6: molecular evolutionary genetics analysis version 6.0.,’’ Molecular Biology and Evolution, vol. 30, no. 12, pp. 2725-2729, 2013.
  • [27] W. S. Abbott, ‘‘A method of computing the effectiveness of an insecticide,’’ Journal of Economic Entomology, vol. 18, pp. 265-267, 1925.
  • [28] C. L. Du, B. Yang, J. H. Wu, S. Ali, ‘‘Identification and virulence characterization of two Akanthomyces attenuatus isolates against Megalurothrips usitatus (Thysanoptera: Thripidae),’’ Insects, vol.10, no. 6, pp. 168, 2019.
  • [29] N. Tangthirasunun, S. Poeaim, K. Soytong, P. Sommartya, S. Popoonsak, ‘‘Variation in morphology and ribosomal DNA among isolates of Metarhizium anisopliae from Thailand,’’ Journal of Agricultural Technology, vol. 6, no. 2, pp. 317-329, 2010.
  • [30] B. J. Bentz, A. M. Jönsson, ‘’Modeling Bark Beetle Responses to Climate Change, 533-53,’’ in Reviews the Modeling Approach to The Bark Beetle Dynamics Under A Climate Change Scenario. ed., F. E. Vega, R. W. Hofstetter. San Diego, Academic Press, 2015, pp. 533-53 pp.
  • [31] K.F. Raffa, B. H. Aukema, B. J. Bent, A. L. Carroll, J. A. Hicke, M. G. Turner, W. H. Romme, ‘‘Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions,’’ Bioscience, vol. 58, no. 6, pp. 501-517, 2008.
  • [32] C. I. Fraser, O. Brahy, P. Mardulyn, L. Dohet, F. Mayer F, J. C. Grégoire, ‘‘Flying the nest: male dispersal and multiple paternity enables extrafamilial matings for the invasive bark beetle Dendroctonus micans,’’ Heredity, vol. 113, no. 4, pp. 327-333, 2014.
  • [33] F. Mayer, F. B. Piel, A. Cassel‐Lundhagen, N. Kirichenko, L. Grumiau, B. Økland, P. Mardulyn, ‘‘Comparative multilocus phylogeography of two Palaearctic spruce bark beetles: influence of contrasting ecological strategies on genetic variation,’’ Molecular Ecology, vol. 24, no. 6, pp. 1292-1310, 2015.
  • [34] J. Kreutz, O. Vaupel, G. Zimmermann, ‘‘Efficacy of Beauveria bassiana (Bals.) Vuill. against the spruce bark beetle, Ips typographus L, in the laboratory under various conditions,’’ Journal of Applied Entomology, vol. 128, pp. 384–389, 2004.
  • [35] S. A. Draganova, D. D. Doychev, D. K. Pilarska, D. I. Takov, ‘‘Bioassays of entomopathogenic fungi against xylophagous insects in Bulgaria: laboratory and field experiments,’’ Acta Zoologica Bulgarica, vol. 69, no. 3, pp. 411-419, 2017.
  • [36] Y. A. Batta, ‘’Biocontrol of almond bark beetle (Scolytus amygdali Geurin-Meneville, Coleoptera: Scolytidae) using Beauveria bassiana (Bals.) Vuill. (Deuteromycotina: Hyphomycetes),’’Journal of Apply Microbiology, vol. 103, pp. 1406–1414, 2007.
  • [37] S. Keller, C. Epper, B. Wermelinger, ‘‘Metarhizium anisopliae as a New Pathogen of the Spruce Bark Beetle Ips typographus,’’ Mitteilungen der Schweizerischen Entomologischen Gesellschaft, vol. 77, pp. 121 – 123, 2004.
  • [38] F. Ihara, M. Toyama, T. Sato, ‘‘Pathogenicity of Metarhizium anisopliae to the chestnut weevil larvae under laboratory and field conditions,’’ Applied Entomology and Zoology, vol. 38, no. 4, pp. 461-465, 2003.
  • [39] P. Marannino, C. Santiago-Álvarez, E. de Lillo, E. Quesada-Moraga, ‘‘A new bioassay method reveals pathogenicity of Metarhizium anisopliae and Beauveria bassiana against early stages of Capnodis tenebrionis (Coleoptera; Buprestidae),’’ Journal of Invertebrate Pathology, vol. 93, no. 3, pp. 210-213, 2006.
  • [40] G. E. Moore, ‘‘Mortality factors caused by path- bacteria and fungi of the southern pine beetle in North Carolina,’’ Journal of Invertebrate Pathology, vol. 17, pp. 28-37, 1971.
  • [41] G. S. Pabst, P. P. Sikorowski, ‘‘Susceptibility of southern pine beetle (Dendroctonus frontalis) on oligidic medium to Paecilomyces viridis and also Beauveria bassiana, and Metarhizium anisopliae,’’ Journal of Georgia Entomology Socienty, vol. 15, pp.235-241, 1980.
  • [42] D. Takov, M. Barta, T. Toshova, D. Doychev, D. Pilarska, ‘‘On the Pathogenicity of Metarhizium pemphigi against Ips typographus L,’’ Proceedings of the Bulgarian Academy of Sciences, vol. 75, no. 4, pp. 554-560, 2022.
Year 2024, Volume: 28 Issue: 2, 381 - 391, 30.04.2024
https://doi.org/10.16984/saufenbilder.1382917

Abstract

References

  • [1] D. L. Wood, ‘‘The role of pheromones, kairomones, and allomones in the host selection and colonization behavior of bark beetles,’’ Annual Review of Entomology, vol. 27, pp. 411-446, 1982.
  • [2] S. Seybold, D. Huber, J. Lee, A. Graves, J. Bohlmann, ‘‘Pine monoterpenes and pine bark beetles: a marriage of convenience for defense and chemical communication,’’ Phytochemistry Reviews, vol. 5, pp. 143-178, 2006.
  • [3] A. Martín, I. Etxebeste, G. Pérez, G. Álvarez, E. Sánchez, J. Pajares, ‘‘Modified pheromone traps help reduce bycatch of bark-beetle natural enemies,’’ Agricultural and Forest Entomology, vol. 15, no. 1, pp. 86-97, 2013.
  • [4] F. Armendáriz-Toledano, A. Niño, B. T. Sullivan, L. R. Kirkendall, G. Zúñiga, ‘‘A new species of bark beetle, Dendroctonus mesoamericanus sp. nov. (Curculionidae: Scolytinae), in southern Mexico and Central America,’’ Annals of the Entomological Society of America, vol. 108, no. 3, pp. 403-414, 2015.
  • [5] D. L. Six, R. Bracewell, ‘’Dendroctonus,’’ in Bark beetles: Biology and ecology of native and invasive species, Academic Press, ed., London: Vega FE, Hofstetter RW, 2017 pp. 305-350.
  • [6] A. Büyükterzi, G. E. Özcan, O. E. Sakici, ‘‘Variations in the attack pattern of Dendroctonus micans and the colonization rate of Rhizophagus grandis in Picea orientalis stands,’’ Biologia, vol. 77, no. 9, pp. 2475-2485, 2022.
  • [7] J. D. Reeve, F. E. Anderson, S. T. Kelley, ‘‘Ancestral state reconstruction for Dendroctonus bark beetles: evolution of a tree killer,’’ Environmental Entomology, vol. 41, no. 3, pp. 723-730, 2012.
  • [8] H. Alkan Akıncı, F. E. Bak, B. A. Çalışkan, ‘‘Some tree features affecting host selection by Dendroctonus micans (Kugelann) (Coleoptera: Curculionidae, Scolytinae): experimental results from Artvin spruce forests,’’ Artvin Çoruh University Journal of Forestry Faculty, vol. 19, no. 2, pp. 186-193, 2018.
  • [9] CABI, ‘‘Dendroctonus micans (great spruce bark beetle),’’ Feb. 16, 2021. [Online]. Available:https://www.cabi.org/isc/datasheet/18352.
  • [10] G. Rouault, J. N. Candau, F. Lieutier, L. M. Nageleisen, J. C. Martin, N. Warzée, ‘‘Effects of drought and heat on forest insect populations in relation to the 2003 drought in Western Europe,’’ Annals of Forest Science, vol. 63, no. 6, pp. 613-624, 2006.
  • [11] J. Hushaw, ‘‘Forest pests and climate change,’’ Apr. 1, 2021. [Online]. Available: https://www.manomet.org/wpcontent/uploads/old-files/Forest Pests-and-Climate Change_FullBulletin.pdf).
  • [12] D. Kulakowski, ‘‘Managing bark beetle outbreaks (Ips typographus, Dendroctonus spp.) in conservation areas in the 21st century,’’ Forest Research Papers, vol. 77, no. 4, pp. 352-357, 2016.
  • [13] B. Yuksel. ‘‘The Damaging Insect Species at Oriental Spruce Forests and Their Predators and Parasite Species. II. Eastern Black Sea Forestry Research Institute Technical Notes, Trabzon, Turkey, vol. 6, pp. 46, 1997.
  • [14] D. W. Langor, ‘‘Arthropods and nematodes co-occur with the eastern larch beetle, Dendroctonus simplex (Col.: Scolytidae), in Newfoundland,’’ Entomophaga, vol. 36, pp. 303-313, 1991.
  • [15] H. Yılmaz, K. Sezen, H. Kati, Z. Demirbag, ‘‘The first study on the bacterial flora of the European spruce bark beetle, Dendroctonus micans (Coleoptera: Scolytidae),’’ Biologia Bratislava, vol. 61, pp. 679-686, 2006.
  • [16] M. Yaman, R. Radek, ‘‘Pathogens and parasites of adults of the great spruce bark beetle, Dendroctonus micans (Kugelann) (Coleoptera: Curculionidae, Scolytinae) from Turkey,’’ Journal of Pest Science, vol. 81, pp. 91-97, 2008.
  • [17] A. Sevim, İ. Demir, E. Tanyeli, Z. Demirbag, ‘‘Screening of entomopathogenic fungi against the European spruce bark beetle, Dendroctonus micans (Coleoptera: Scolytidae),’’ Biocontrol Science and Technology, vol. 20, pp. 3-11, 2010.
  • [18] M. Yaman, Ö. Ertürk, İ. Aslan, ‘‘Isolation of some pathogenic bacteria from the great spruce bark beetle, Dendroctonus micans and its specific predator, Rhizophagus grandis,’’ Folia Microbiologica, vol. 55, pp. 35-38, 2010.
  • [19] S. Kocacevik, A. Sevim, M. Eroglu, Z. Demirbag, I. Demir, ‘‘Molecular characterization, virulence and horizontal transmission of Beauveria pseudobassiana from Dendroctonus micans (Kug.) (Coleoptera: Curculionidae),’’ Journal of Applied Entomology, vol. 139, no. 5, pp. 381-389, 2015.
  • [20] B. Lovett, R. J. St Leger, ‘‘The insect pathogens,’’ Microbiology Spectrum, vol. 5, no. 2, pp.10-1128, 2017.
  • [21] L. A. Lacey, D. Grzywacz, D. I. Shapiro-Ilan, R. Frutos, M. Brownbridge, M. S. Goettel, ‘‘Insect pathogens as biological control agents: back to the future,’’ Journal of Invertebrate Pathology, vol. 132, pp. 1-41, 2015.
  • [22] M. S. Ali-Shtayeh, A. B. B. Marai, R. M. Jamous, ‘‘Distribution, occurrence and characterization of entomopathogenic fungi in agricultural soil in the Palestinian area,’’ Mycopathologia, vol. 156, no.3, pp. 235-244, 2003.
  • [23] R. A. Humber, ‘‘Fungi: identification,’’ İNManual of techniques in insect pathology, Academic Press, 1997, pp. 153-185.
  • [24] J. L. Harris, ‘‘Modified method for fungal slide cultures,’’ Journal of Clinical Microbiology, vol. 24, no. 3, pp. 460-461, 1986.
  • [25] T. J. T. White, S. Bruns, J. Taylor, “Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics,’’ in PCR Protocols: A Guide to Methods and Applications, M. A. Innis, D. H. Gelfand, J. J. Sninsky, T. J. White. Academic Press, San Diego,1990, pp. 482.
  • [26] K. Tamura, G. Stecher, D. Peterson, A. Filipski, S. Kumar, ‘‘MEGA6: molecular evolutionary genetics analysis version 6.0.,’’ Molecular Biology and Evolution, vol. 30, no. 12, pp. 2725-2729, 2013.
  • [27] W. S. Abbott, ‘‘A method of computing the effectiveness of an insecticide,’’ Journal of Economic Entomology, vol. 18, pp. 265-267, 1925.
  • [28] C. L. Du, B. Yang, J. H. Wu, S. Ali, ‘‘Identification and virulence characterization of two Akanthomyces attenuatus isolates against Megalurothrips usitatus (Thysanoptera: Thripidae),’’ Insects, vol.10, no. 6, pp. 168, 2019.
  • [29] N. Tangthirasunun, S. Poeaim, K. Soytong, P. Sommartya, S. Popoonsak, ‘‘Variation in morphology and ribosomal DNA among isolates of Metarhizium anisopliae from Thailand,’’ Journal of Agricultural Technology, vol. 6, no. 2, pp. 317-329, 2010.
  • [30] B. J. Bentz, A. M. Jönsson, ‘’Modeling Bark Beetle Responses to Climate Change, 533-53,’’ in Reviews the Modeling Approach to The Bark Beetle Dynamics Under A Climate Change Scenario. ed., F. E. Vega, R. W. Hofstetter. San Diego, Academic Press, 2015, pp. 533-53 pp.
  • [31] K.F. Raffa, B. H. Aukema, B. J. Bent, A. L. Carroll, J. A. Hicke, M. G. Turner, W. H. Romme, ‘‘Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions,’’ Bioscience, vol. 58, no. 6, pp. 501-517, 2008.
  • [32] C. I. Fraser, O. Brahy, P. Mardulyn, L. Dohet, F. Mayer F, J. C. Grégoire, ‘‘Flying the nest: male dispersal and multiple paternity enables extrafamilial matings for the invasive bark beetle Dendroctonus micans,’’ Heredity, vol. 113, no. 4, pp. 327-333, 2014.
  • [33] F. Mayer, F. B. Piel, A. Cassel‐Lundhagen, N. Kirichenko, L. Grumiau, B. Økland, P. Mardulyn, ‘‘Comparative multilocus phylogeography of two Palaearctic spruce bark beetles: influence of contrasting ecological strategies on genetic variation,’’ Molecular Ecology, vol. 24, no. 6, pp. 1292-1310, 2015.
  • [34] J. Kreutz, O. Vaupel, G. Zimmermann, ‘‘Efficacy of Beauveria bassiana (Bals.) Vuill. against the spruce bark beetle, Ips typographus L, in the laboratory under various conditions,’’ Journal of Applied Entomology, vol. 128, pp. 384–389, 2004.
  • [35] S. A. Draganova, D. D. Doychev, D. K. Pilarska, D. I. Takov, ‘‘Bioassays of entomopathogenic fungi against xylophagous insects in Bulgaria: laboratory and field experiments,’’ Acta Zoologica Bulgarica, vol. 69, no. 3, pp. 411-419, 2017.
  • [36] Y. A. Batta, ‘’Biocontrol of almond bark beetle (Scolytus amygdali Geurin-Meneville, Coleoptera: Scolytidae) using Beauveria bassiana (Bals.) Vuill. (Deuteromycotina: Hyphomycetes),’’Journal of Apply Microbiology, vol. 103, pp. 1406–1414, 2007.
  • [37] S. Keller, C. Epper, B. Wermelinger, ‘‘Metarhizium anisopliae as a New Pathogen of the Spruce Bark Beetle Ips typographus,’’ Mitteilungen der Schweizerischen Entomologischen Gesellschaft, vol. 77, pp. 121 – 123, 2004.
  • [38] F. Ihara, M. Toyama, T. Sato, ‘‘Pathogenicity of Metarhizium anisopliae to the chestnut weevil larvae under laboratory and field conditions,’’ Applied Entomology and Zoology, vol. 38, no. 4, pp. 461-465, 2003.
  • [39] P. Marannino, C. Santiago-Álvarez, E. de Lillo, E. Quesada-Moraga, ‘‘A new bioassay method reveals pathogenicity of Metarhizium anisopliae and Beauveria bassiana against early stages of Capnodis tenebrionis (Coleoptera; Buprestidae),’’ Journal of Invertebrate Pathology, vol. 93, no. 3, pp. 210-213, 2006.
  • [40] G. E. Moore, ‘‘Mortality factors caused by path- bacteria and fungi of the southern pine beetle in North Carolina,’’ Journal of Invertebrate Pathology, vol. 17, pp. 28-37, 1971.
  • [41] G. S. Pabst, P. P. Sikorowski, ‘‘Susceptibility of southern pine beetle (Dendroctonus frontalis) on oligidic medium to Paecilomyces viridis and also Beauveria bassiana, and Metarhizium anisopliae,’’ Journal of Georgia Entomology Socienty, vol. 15, pp.235-241, 1980.
  • [42] D. Takov, M. Barta, T. Toshova, D. Doychev, D. Pilarska, ‘‘On the Pathogenicity of Metarhizium pemphigi against Ips typographus L,’’ Proceedings of the Bulgarian Academy of Sciences, vol. 75, no. 4, pp. 554-560, 2022.
There are 42 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section Research Articles
Authors

Seda Biryol 0000-0003-0881-5004

Ali Soydinç 0000-0003-4208-2000

Sevda İşık 0000-0002-1032-1807

Early Pub Date April 24, 2024
Publication Date April 30, 2024
Submission Date October 31, 2023
Acceptance Date December 26, 2023
Published in Issue Year 2024 Volume: 28 Issue: 2

Cite

APA Biryol, S., Soydinç, A., & İşık, S. (2024). Morphological, Molecular Identification and Virulence of Entomopathogenic Fungi Isolated From Dendroctonus micans (Kugelann,1794) (Coleoptera: Curculionidae). Sakarya University Journal of Science, 28(2), 381-391. https://doi.org/10.16984/saufenbilder.1382917
AMA Biryol S, Soydinç A, İşık S. Morphological, Molecular Identification and Virulence of Entomopathogenic Fungi Isolated From Dendroctonus micans (Kugelann,1794) (Coleoptera: Curculionidae). SAUJS. April 2024;28(2):381-391. doi:10.16984/saufenbilder.1382917
Chicago Biryol, Seda, Ali Soydinç, and Sevda İşık. “Morphological, Molecular Identification and Virulence of Entomopathogenic Fungi Isolated From Dendroctonus Micans (Kugelann,1794) (Coleoptera: Curculionidae)”. Sakarya University Journal of Science 28, no. 2 (April 2024): 381-91. https://doi.org/10.16984/saufenbilder.1382917.
EndNote Biryol S, Soydinç A, İşık S (April 1, 2024) Morphological, Molecular Identification and Virulence of Entomopathogenic Fungi Isolated From Dendroctonus micans (Kugelann,1794) (Coleoptera: Curculionidae). Sakarya University Journal of Science 28 2 381–391.
IEEE S. Biryol, A. Soydinç, and S. İşık, “Morphological, Molecular Identification and Virulence of Entomopathogenic Fungi Isolated From Dendroctonus micans (Kugelann,1794) (Coleoptera: Curculionidae)”, SAUJS, vol. 28, no. 2, pp. 381–391, 2024, doi: 10.16984/saufenbilder.1382917.
ISNAD Biryol, Seda et al. “Morphological, Molecular Identification and Virulence of Entomopathogenic Fungi Isolated From Dendroctonus Micans (Kugelann,1794) (Coleoptera: Curculionidae)”. Sakarya University Journal of Science 28/2 (April 2024), 381-391. https://doi.org/10.16984/saufenbilder.1382917.
JAMA Biryol S, Soydinç A, İşık S. Morphological, Molecular Identification and Virulence of Entomopathogenic Fungi Isolated From Dendroctonus micans (Kugelann,1794) (Coleoptera: Curculionidae). SAUJS. 2024;28:381–391.
MLA Biryol, Seda et al. “Morphological, Molecular Identification and Virulence of Entomopathogenic Fungi Isolated From Dendroctonus Micans (Kugelann,1794) (Coleoptera: Curculionidae)”. Sakarya University Journal of Science, vol. 28, no. 2, 2024, pp. 381-9, doi:10.16984/saufenbilder.1382917.
Vancouver Biryol S, Soydinç A, İşık S. Morphological, Molecular Identification and Virulence of Entomopathogenic Fungi Isolated From Dendroctonus micans (Kugelann,1794) (Coleoptera: Curculionidae). SAUJS. 2024;28(2):381-9.