The role of microorganisms in the ecology of bark beetles (Curculionidae, Scolytinae)

Balázs Balázs Gábor; Tuba Katalin; Lakatos Ferenc

Bulletin of Forestry Science / Volume 11 / Issue 2 / Pages 131-142
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Gábor Balázs Balázs, Katalin Tuba & Ferenc Lakatos

Correspondence

Correspondence: Balázs Balázs Gábor

Postal address: H-9400 Sopron, Bajcsy-Zsilinszky út 4.

e-mail: balazsbalazsg[at]gmail.com

Abstract

Some bark beetle species (Curculionidae, Scolytinae), especially in coniferous forests, are major factors for mass mortality of trees. Although bark beetle species usually do not attack healthy trees, they can colonize weakened or dying trees. Some species may have massive outbreaks, especially under defined abiotic conditions (like hot and dry weather or after wind and snow damage) and can have significant economic and ecological effect. Microorganisms associated with bark beetles such as fungi or bacteria play important roles in their colonization success, development, and gradation. This paper provides a review on the effects of microorganisms on the biology of bark beetles and interactions between bark beetles and their host plants. We present these interactions based on the holobiont theory, i.e., considering bark beetles and their associated microbiota as a whole.

Keywords: Scolytinae, microorganisms, symbioses, holobiont

References47

1.	Acuna R., Padilla B. E., Florez-Ramos C. P., Rubio J. D., Herrera J. C., Benavides P. et al. 2012: Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proceedings of the National Academy of Sciences of the United States of America 109: 4197–4202. DOI: 10.1073/pnas.1121190109
2.	Batra L. R. 1963: Ecology of ambrosia fungi and their dissemination by beetles. Transactions of the Kansas Academy of Science 66: 213–236. DOI: 10.2307/3626562
3.	Boone C., Keefover-Ring K., Mapes A. C., Adams A. S., Bohlmann J. & Raffa K. F. 2013: Bacteria associated with a treekilling insect reduce concentrations of plant defense compounds. Journal of Chemical Ecology 39: 1003–1006. DOI: 10.1007/s10886-013-0313-0
4.	Davis T. S. & Hofstetter R. W. 2011: Reciprocal interactions between the bark beetle-associated yeast Ogataea pini and host plant chemistry. Mycologia 103: 1201–1207. DOI: 10.3852/11-083
5.	de Bary A. 1879: Die Erscheinung der Symbiose: Vortrag. Strassburg, Verlag von Karl J. Trübner.
6.	de Beer Z. W., Duong T., Barnes I., Wingfield B. D. & Wingfield M. J. 2014: Redefining Ceratocystis and allied genera. Studies in Mycology 79: 187–219. DOI: 10.1016/j.simyco.2014.10.001
7.	DiGuistini S., Wang Y., Liao N. Y., Taylor G., Tanguay P., Feau N. et al. 2011: Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen. Proceedings of the National Academy of Sciences of the United States of America 108: 2504–2509. DOI: 10.1073/pnas.1011289108
8.	Douglas A. & Werren J. 2016: Holes in the Hologenome: Why host-microbe symbioses are not holobionts. mBio 7: e02099-15. DOI: 10.1128/mBio.02099-15
9.	Feijen F. A. A., Vos R. A., Nuytinck J. & Merckx V. S. F. T. 2018: Evolutionary dynamics of mycorrhizal symbiosis in land plant diversification. Scientific Reports 8: 10698. DOI: 10.1038/s41598-018-28920-x
10.	Frank A. B. 1877: Über die biologischen Verhältnisse des Thallus einiger Krustenflechten. Beiträge zur Biologie der Pflanzen 2: 123–200.
11.	García-Fraile P. 2018: Roles of bacteria in the bark beetle holobiont – how do they shape this forest pest? Annals of Applied Biology 172: 111–125. DOI: 10.1111/aab.12406
12.	Gilbert S. F., Sapp J. & Tauber A. I. 2012: A symbiotic view of life: We have never been individuals. The Quarterly Review of Biology 87: 325–341. DOI: 10.1086/668166
13.	Guerrero R., Margulis L. & Berlanga M. 2013: Symbiogenesis: the holobiont as a unit of evolution. International Microbiology 16: 133–143. DOI: 10.2436/20.1501.01.188
14.	Harrington T. C. 2005: Ecology and evolution of mycophagous bark beetles and their fungal partners. In: Vega F. E. & Blackwell M. (eds.): Ecological and evolutionary advances in insect-fungal associations. Oxford University Press, Oxford, 257–291.
15.	Hofstetter R. W., Dinkins-Bookwalter J., Davis T. S. & Klepzig K. D. 2015: Symbiotic associations of bark beetles. In: Vega F. E. & Hofstetter R. W. (eds.): Bark beetles: biology and ecology of native and invasive species. Academic Press, London, 209–245. DOI: 10.1016/b978-0-12-417156-5.00006-x
16.	Hulcr J., Adams A. S., Raffa K. F., Hofstetter R. W., Klepzig K. D. & Currie C. R. 2011: Presence and diversity of Streptomyces in Dendroctonus and sympatric beetle galleries across North America. Molecular Ecology 61: 759–768. DOI: 10.1007/s00248-010-9797-0
17.	Hunt D . W. A. & Borden J. H. 1990: Conversion of verbenols to verbenone by yeasts isolated from Dendroctonus ponderosae (Coleoptera: Scolytidae). Journal of Chemical Ecology 16: 1385–1397. DOI: 10.1007/BF01021034
18.	Janson, E. M., Stireman J. O., Singer M. S. & Abbot P. 2008: Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification. Evolution 62: 997–1012. DOI: 10.1111/j.1558-5646.2008.00348.x
19.	Joy J. B. 2012: Symbiosis catalyses niche expansion and diversification. Proceedings of the Royal Society B: Biological Sciences 280: 2820. DOI: 10.1098/rspb.2012.2820
20.	Kirisits T. 2004: Fungal associates of European bark beetles with special emphasis on the ophiostomatoid fungi. 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. Springer, Dordrecht, 181–236. DOI: 10.1007/1-4020-2241-7_10
21.	Kirisits T. 2010: Fungi isolated from Picea abies infested by the bark beetle Ips typographus in the Białowieza forest in north-eastern Poland. Forest Pathology 40: 100–110. DOI: 10.1111/j.1439-0329.2009.00613.x
22.	Kirkendall L. R., Biedermann P. H. W. & Jordal B. H. 2015: Evolution and diversity of bark and ambrosia beetles. In: Vega F. E. & Hofstetter R. W. (eds.): Bark beetles: biology and ecology of native and invasive species. Academic Press, London, 85–156. DOI: 10.1016/B978-0-12-417156-5.00003-4
23.	Krokene P. 2015: Conifer defense and resistance to bark beetles. In: Vega F. E. & Hofstetter R. W. (eds.): Bark beetles: biology and ecology of native and invasive species. Academic Press, London, 177–207. DOI: 10.1016/B978-0-12-417156-5.00005-8
24.	Lah L., Haridas S., Bohlmann J. & Breuil C. 2013: The cytochromes P450 of Grosmannia clavigera: Genome organization, phylogeny, and expression in response to pine host chemicals. Fungal Genetics and Biology 50: 72–81. DOI: 10.1016/j.fgb.2012.10.002
25.	Leufven A., Bergstrom G. & Falsen E. 1984: Interconversion of verbenols and verbenone by identified yeasts associated from the spruce bark beetle Ips typographus. Journal of Chemical Ecology 10: 1349–1361. DOI: 10.1007/BF00988116
26.	Lévieux J., Cassier P., Guillaumin D. & Roques A. 1991: Structures implicated in the transportation of pathogenic fungi by the European bark beetle, Ips sexdentatus Boerner: ultrastructure of a mycangium. The Canadian Entomologist 123: 245–254. DOI: 10.4039/Ent123245-2
27.	Margulis L. 1970: Origin of eukaryotic cells: Evidence and research implications for a theory of the origin and evolution of microbial, plant and animal cells on the precambrian Earth. Yale University Press, New Heaven.
28.	Margulis L, & Fester R 1991: Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. MIT Press, Boston.
29.	Morales-Jimenez J., de Leon A.V.P., García-Domínguez A., Martínez-Romero E., Zuniga G. & Hernandez-Rodríguez C. 2013: Nitrogenfixing and uricolytic bacteria associated with the gut of Dendroctonus rhizophagus and Dendroctonus valens (Curculionidae: Scolytinae). Microbial Ecology 66: 200–210. DOI: 10.1007/s00248-013-0206-3
30.	Mushegian A. A.; Ebert D. 2016: Rethinking „mutualism” in diverse host‐symbiont communities. BioEssays 38: 100–108. DOI: 10.1002/bies.201500074
31.	Raffa K. F., Grégoire J. C. & Lindgren B. S. 2015: Natural history and ecology of bark beetles. In: Vega F. E. & Hofstetter R. W. (eds.): Bark beetles: biology and ecology of native and invasive species. Academic Press, London, 1–40. DOI: 10.1016/B978-0-12-417156-5.00001-0
32.	Scott J. J., Dong-Chan O., Yuceer M. C., Klepzig K. D., Clardy J. & Currie C. R. 2008: Bacterial protection of beetle-fungus mutualism. Science 322: 63. DOI: 10.1126/science.1160423
33.	Six D. L. 2003: Bark beetle-fungus symbioses. In: Bourtzis K. & Miller T. A. (eds.): Insect symbiosis. contemporary topics in entomology series. CRC Press, Boca Raton, London, New York, Washington D.C., 97–114. DOI: 10.1201/9780203009918-12
34.	Six D. L. 2012: Ecological and evolutionary determinants of bark beetle-fungus symbioses. Insects 3: 339–366. DOI: 10.3390/insects3010339
35.	Six D. L. 2013: The bark beetle holobiont: why microbes matter. Journal of Chemical Ecology 39: 989–1002. DOI: 10.1007/s10886-013-0318-8
36.	Six D. L. 2019: A major symbiont shift supports a major niche shift in a clade of tree‐killing bark beetles. Ecological Entomology 45: 190–201. DOI: 10.1111/een.12786
37.	Six D. L., James J. & Elser J. J. 2020: Mutualism is not restricted to tree‐killing bark beetles and fungi: the ecological stoichiometry of secondary bark beetles, fungi, and a scavenger. Ecological Entomology 45: 1134–1145. DOI: 10.1111/een.12897
38.	Six D. L. & Wingfield M. J. 2011: The role of phytopathogenicity in bark beetle-fungus symbioses: a challenge to the classic paradigm. Annual Reviev of Entomology 56: 255–272. DOI: 10.1146/annurev-ento-120709-144839
39.	Sprent J. I. 2005: Nitrogen in soils symbiotic fixation. In: Hillel D. (ed.): Encyclopedia of soils in the environment. Elsevier, Amsterdam, 46–56. DOI: 10.1016/B0-12-348530-4/00457-4
40.	Strullu-Derrein C., Selosse M. A., Kenrick P. & Martin F. M. 2018: The origin and evolution of mycorrhizal symbioses: from paleomycology to phylogenomics. New Phytologist 220: 1012–1030. DOI: 10.1111/nph.15076
41.	Vega F. E. & Biedermann P. H. W. 2020: On interactions, associations, mycetangia, mutualists and symbiotes in insect. fungus symbioses. Fungal Ecology 44: 100909. DOI: 10.1016/j.funeco.2019.100909
42.	Wadke N., Kandasamy D., Vogel H., Lah L., Wingfield B. D., Paetz C. et al. 2016: The bark-beetle-associated fungus, Endoconidiophora polonica, utilizes the phenolic defense compounds of its host as a carbon source. Plant Physiology 171: 914–931. DOI: 10.1104/pp.15.01916
43.	Yamaoka Y. 2017: Taxonomy and pathogenicity of ophiostomatoid fungi associated with bark beetle infesting conifers in Japan, with special reference to those related to subalpine conifers. Myoscience 58: 221–235. DOI: 10.1016/j.myc.2017.03.001
44.	Zilber-Rosenberg I. & Rosenberg E. 2008: Role of microorganisms in the evolution of animals and plants. FEMS Microbiology Reviews 32: 723–735. DOI: 10.1111/j.1574-6976.2008.00123.x
45.	Zipfel R. D., de Beer Z. W., Jacobs K., Wingfield B. D., Wingfield M. J. 2006: Multigene phylogenies define Ceratocystiopsis and Grosmannia distinct from Ophiostoma. Studies in Mycology 55: 75–97. DOI: 10.3114/sim.55.1.75
46.	Zook D. 1998: A new symbiosis language. Symbiosis News 1: 1–3.
47.	Zook D. 2015: Symbiosis-Evolution’s co-author. In: Gontier N. (ed.): Reticulate Evolution. Cham, Switzerland. Springer, 41–80. DOI: 10.1007/978-3-319-16345-1_2

Acuna R., Padilla B. E., Florez-Ramos C. P., Rubio J. D., Herrera J. C., Benavides P. et al. 2012: Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proceedings of the National Academy of Sciences of the United States of America 109: 4197–4202. DOI: 10.1073/pnas.1121190109

Batra L. R. 1963: Ecology of ambrosia fungi and their dissemination by beetles. Transactions of the Kansas Academy of Science 66: 213–236. DOI: 10.2307/3626562

Boone C., Keefover-Ring K., Mapes A. C., Adams A. S., Bohlmann J. & Raffa K. F. 2013: Bacteria associated with a treekilling insect reduce concentrations of plant defense compounds. Journal of Chemical Ecology 39: 1003–1006. DOI: 10.1007/s10886-013-0313-0

Davis T. S. & Hofstetter R. W. 2011: Reciprocal interactions between the bark beetle-associated yeast Ogataea pini and host plant chemistry. Mycologia 103: 1201–1207. DOI: 10.3852/11-083

de Bary A. 1879: Die Erscheinung der Symbiose: Vortrag. Strassburg, Verlag von Karl J. Trübner.

de Beer Z. W., Duong T., Barnes I., Wingfield B. D. & Wingfield M. J. 2014: Redefining Ceratocystis and allied genera. Studies in Mycology 79: 187–219. DOI: 10.1016/j.simyco.2014.10.001

DiGuistini S., Wang Y., Liao N. Y., Taylor G., Tanguay P., Feau N. et al. 2011: Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen. Proceedings of the National Academy of Sciences of the United States of America 108: 2504–2509. DOI: 10.1073/pnas.1011289108

Douglas A. & Werren J. 2016: Holes in the Hologenome: Why host-microbe symbioses are not holobionts. mBio 7: e02099-15. DOI: 10.1128/mBio.02099-15

Feijen F. A. A., Vos R. A., Nuytinck J. & Merckx V. S. F. T. 2018: Evolutionary dynamics of mycorrhizal symbiosis in land plant diversification. Scientific Reports 8: 10698. DOI: 10.1038/s41598-018-28920-x

Frank A. B. 1877: Über die biologischen Verhältnisse des Thallus einiger Krustenflechten. Beiträge zur Biologie der Pflanzen 2: 123–200.

García-Fraile P. 2018: Roles of bacteria in the bark beetle holobiont – how do they shape this forest pest? Annals of Applied Biology 172: 111–125. DOI: 10.1111/aab.12406

Gilbert S. F., Sapp J. & Tauber A. I. 2012: A symbiotic view of life: We have never been individuals. The Quarterly Review of Biology 87: 325–341. DOI: 10.1086/668166

Guerrero R., Margulis L. & Berlanga M. 2013: Symbiogenesis: the holobiont as a unit of evolution. International Microbiology 16: 133–143. DOI: 10.2436/20.1501.01.188

Harrington T. C. 2005: Ecology and evolution of mycophagous bark beetles and their fungal partners. In: Vega F. E. & Blackwell M. (eds.): Ecological and evolutionary advances in insect-fungal associations. Oxford University Press, Oxford, 257–291.

Hofstetter R. W., Dinkins-Bookwalter J., Davis T. S. & Klepzig K. D. 2015: Symbiotic associations of bark beetles. In: Vega F. E. & Hofstetter R. W. (eds.): Bark beetles: biology and ecology of native and invasive species. Academic Press, London, 209–245. DOI: 10.1016/b978-0-12-417156-5.00006-x

Hulcr J., Adams A. S., Raffa K. F., Hofstetter R. W., Klepzig K. D. & Currie C. R. 2011: Presence and diversity of Streptomyces in Dendroctonus and sympatric beetle galleries across North America. Molecular Ecology 61: 759–768. DOI: 10.1007/s00248-010-9797-0

Hunt D . W. A. & Borden J. H. 1990: Conversion of verbenols to verbenone by yeasts isolated from Dendroctonus ponderosae (Coleoptera: Scolytidae). Journal of Chemical Ecology 16: 1385–1397. DOI: 10.1007/BF01021034

Janson, E. M., Stireman J. O., Singer M. S. & Abbot P. 2008: Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification. Evolution 62: 997–1012. DOI: 10.1111/j.1558-5646.2008.00348.x

Joy J. B. 2012: Symbiosis catalyses niche expansion and diversification. Proceedings of the Royal Society B: Biological Sciences 280: 2820. DOI: 10.1098/rspb.2012.2820

Kirisits T. 2004: Fungal associates of European bark beetles with special emphasis on the ophiostomatoid fungi. 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. Springer, Dordrecht, 181–236. DOI: 10.1007/1-4020-2241-7_10

Kirisits T. 2010: Fungi isolated from Picea abies infested by the bark beetle Ips typographus in the Białowieza forest in north-eastern Poland. Forest Pathology 40: 100–110. DOI: 10.1111/j.1439-0329.2009.00613.x

Kirkendall L. R., Biedermann P. H. W. & Jordal B. H. 2015: Evolution and diversity of bark and ambrosia beetles. In: Vega F. E. & Hofstetter R. W. (eds.): Bark beetles: biology and ecology of native and invasive species. Academic Press, London, 85–156. DOI: 10.1016/B978-0-12-417156-5.00003-4

Krokene P. 2015: Conifer defense and resistance to bark beetles. In: Vega F. E. & Hofstetter R. W. (eds.): Bark beetles: biology and ecology of native and invasive species. Academic Press, London, 177–207. DOI: 10.1016/B978-0-12-417156-5.00005-8

Lah L., Haridas S., Bohlmann J. & Breuil C. 2013: The cytochromes P450 of Grosmannia clavigera: Genome organization, phylogeny, and expression in response to pine host chemicals. Fungal Genetics and Biology 50: 72–81. DOI: 10.1016/j.fgb.2012.10.002

Leufven A., Bergstrom G. & Falsen E. 1984: Interconversion of verbenols and verbenone by identified yeasts associated from the spruce bark beetle Ips typographus. Journal of Chemical Ecology 10: 1349–1361. DOI: 10.1007/BF00988116

Lévieux J., Cassier P., Guillaumin D. & Roques A. 1991: Structures implicated in the transportation of pathogenic fungi by the European bark beetle, Ips sexdentatus Boerner: ultrastructure of a mycangium. The Canadian Entomologist 123: 245–254. DOI: 10.4039/Ent123245-2

Margulis L. 1970: Origin of eukaryotic cells: Evidence and research implications for a theory of the origin and evolution of microbial, plant and animal cells on the precambrian Earth. Yale University Press, New Heaven.

Margulis L, & Fester R 1991: Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. MIT Press, Boston.

Morales-Jimenez J., de Leon A.V.P., García-Domínguez A., Martínez-Romero E., Zuniga G. & Hernandez-Rodríguez C. 2013: Nitrogenfixing and uricolytic bacteria associated with the gut of Dendroctonus rhizophagus and Dendroctonus valens (Curculionidae: Scolytinae). Microbial Ecology 66: 200–210. DOI: 10.1007/s00248-013-0206-3

Mushegian A. A.; Ebert D. 2016: Rethinking „mutualism” in diverse host‐symbiont communities. BioEssays 38: 100–108. DOI: 10.1002/bies.201500074

Raffa K. F., Grégoire J. C. & Lindgren B. S. 2015: Natural history and ecology of bark beetles. In: Vega F. E. & Hofstetter R. W. (eds.): Bark beetles: biology and ecology of native and invasive species. Academic Press, London, 1–40. DOI: 10.1016/B978-0-12-417156-5.00001-0

Scott J. J., Dong-Chan O., Yuceer M. C., Klepzig K. D., Clardy J. & Currie C. R. 2008: Bacterial protection of beetle-fungus mutualism. Science 322: 63. DOI: 10.1126/science.1160423

Six D. L. 2003: Bark beetle-fungus symbioses. In: Bourtzis K. & Miller T. A. (eds.): Insect symbiosis. contemporary topics in entomology series. CRC Press, Boca Raton, London, New York, Washington D.C., 97–114. DOI: 10.1201/9780203009918-12

Six D. L. 2012: Ecological and evolutionary determinants of bark beetle-fungus symbioses. Insects 3: 339–366. DOI: 10.3390/insects3010339

Six D. L. 2013: The bark beetle holobiont: why microbes matter. Journal of Chemical Ecology 39: 989–1002. DOI: 10.1007/s10886-013-0318-8

Six D. L. 2019: A major symbiont shift supports a major niche shift in a clade of tree‐killing bark beetles. Ecological Entomology 45: 190–201. DOI: 10.1111/een.12786

Six D. L., James J. & Elser J. J. 2020: Mutualism is not restricted to tree‐killing bark beetles and fungi: the ecological stoichiometry of secondary bark beetles, fungi, and a scavenger. Ecological Entomology 45: 1134–1145. DOI: 10.1111/een.12897

Six D. L. & Wingfield M. J. 2011: The role of phytopathogenicity in bark beetle-fungus symbioses: a challenge to the classic paradigm. Annual Reviev of Entomology 56: 255–272. DOI: 10.1146/annurev-ento-120709-144839

Sprent J. I. 2005: Nitrogen in soils symbiotic fixation. In: Hillel D. (ed.): Encyclopedia of soils in the environment. Elsevier, Amsterdam, 46–56. DOI: 10.1016/B0-12-348530-4/00457-4

Strullu-Derrein C., Selosse M. A., Kenrick P. & Martin F. M. 2018: The origin and evolution of mycorrhizal symbioses: from paleomycology to phylogenomics. New Phytologist 220: 1012–1030. DOI: 10.1111/nph.15076

Vega F. E. & Biedermann P. H. W. 2020: On interactions, associations, mycetangia, mutualists and symbiotes in insect. fungus symbioses. Fungal Ecology 44: 100909. DOI: 10.1016/j.funeco.2019.100909

Wadke N., Kandasamy D., Vogel H., Lah L., Wingfield B. D., Paetz C. et al. 2016: The bark-beetle-associated fungus, Endoconidiophora polonica, utilizes the phenolic defense compounds of its host as a carbon source. Plant Physiology 171: 914–931. DOI: 10.1104/pp.15.01916

Yamaoka Y. 2017: Taxonomy and pathogenicity of ophiostomatoid fungi associated with bark beetle infesting conifers in Japan, with special reference to those related to subalpine conifers. Myoscience 58: 221–235. DOI: 10.1016/j.myc.2017.03.001

Zilber-Rosenberg I. & Rosenberg E. 2008: Role of microorganisms in the evolution of animals and plants. FEMS Microbiology Reviews 32: 723–735. DOI: 10.1111/j.1574-6976.2008.00123.x

Zipfel R. D., de Beer Z. W., Jacobs K., Wingfield B. D., Wingfield M. J. 2006: Multigene phylogenies define Ceratocystiopsis and Grosmannia distinct from Ophiostoma. Studies in Mycology 55: 75–97. DOI: 10.3114/sim.55.1.75

Zook D. 1998: A new symbiosis language. Symbiosis News 1: 1–3.

Zook D. 2015: Symbiosis-Evolution’s co-author. In: Gontier N. (ed.): Reticulate Evolution. Cham, Switzerland. Springer, 41–80. DOI: 10.1007/978-3-319-16345-1_2

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Balázs, B. G., Tuba, K. & Lakatos, F. (2021): The role of microorganisms in the ecology of bark beetles (Curculionidae, Scolytinae). Bulletin of Forestry Science, 11(2): 131-142. (in Hungarian) DOI: 10.17164/EK.2021.005

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Volume 11, Issue 2
Pages: 131-142

DOI: 10.17164/EK.2021.005

First published:
13 September 2021

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