Article

Article name THE CORE OF THE KOLOGRIV FOREST STATE NATURE RESERVE (RUSSIA) IS A HOTSPOT OF LICHEN BIODIVERSITY IN THE SOUTHERN TAIGA OF EASTERN EUROPE
Authors

Gennadii P. Urbanavichus, PhD, Leader Researcher of the Kola Science Centre RAS (184209, Russia, Murmansk Region, Apatity, Akademgorodok, 14a); Kologriv Forest State Nature Reserve (157440, Russia, Kostroma Region, Kologriv, Nekrasov Street, 48); iD ORCID: https://orcid.org/0000-0003-3222-5151; e-mail: g.urban@mail.ru
Irina N. Urbanavichene, PhD, Senior Researcher of the Komarov Botanical Institute of RAS (197376, Russia, St. Petersburg, Prof. Popov Street, 2); iD ORCID: https://orcid.org/0000-0002-5492-5215; e-mail: urbanavichene@gmail.com

Reference to article

Urbanavichus G.P., Urbanavichene I.N. 2022. The core of the Kologriv Forest State Nature Reserve (Russia) is a hotspot of lichen biodiversity in the southern taiga of Eastern Europe. Nature Conservation Research 7(3): 46–63. https://dx.doi.org/10.24189/ncr.2022.029

Electronic Supplement. Lichens and allied non-lichenised fungi of the core of the Kologriv Forest State Nature Reserve (Kostroma Region, Russia) (Link).

Section Research articles
DOI https://dx.doi.org/10.24189/ncr.2022.029
Abstract

In this study, we aim to evaluate the diversity of lichens and allied non-lichenised fungi, co-existing in dark-coniferous and broad-leaved forests of the southern taiga in the East European Plain. The Kologriv Forest State Nature Reserve (589 km2) was established in 2006 to preserve the last fragments of the unique primeval forests of the southern taiga. The territory of the Kologriv cluster of the Kologriv Forest State Nature Reserve (481 km2) is located in the north of the Kostroma Region (Russia). The main phorophytes in this cluster are Picea abies, Tilia cordata, Betula pubescens, and Abies sibirica. In our time-limited study (four days in May 2021), we selected a 10 000-m2 (hereinafter – 1-ha) plot (a presumed lichen diversity hotspot) in the primeval forest stand in the core of the Kologriv cluster of the Kologriv Forest State Nature Reserve (58.80164° N, 43.98533° E, at altitude ca. 200 m a.s.l.). For a detailed study of the species composition of lichens on this plot, all types of substrates were examined, including trunks and branch surface of various tree species under various conditions, dead and rotting wood of snags, stumps, and fallen logs. In addition, 22 points in various parts of the protected core were examined by the route method in May 2019 and May 2021. This detailed survey in the primeval forest in the core of the Kologriv Forest State Nature Reserve has revealed an unexpectedly high lichen diversity: 230 species recorded in a single 1-ha plot is equal to or much more than the number of species recorded in several Protected Areas of far larger sizes in European Russia. The number of species found on this plot is 73% of the one recorded in the whole protected core (316 species) and 58% of the lichen diversity known in the entire area of the Kologriv Forest State Nature Reserve (398 species). The genus Asterophoma is new for European Russia. The genera Bachmanniomyces and Bryostigma are new for the lichen flora of the middle belt of European Russia. There are 91 species listed for the first time for the lichen flora of the Kologriv Forest State Nature Reserve. Of them, 83 species are new to the Kostroma Region. Two species (Micarea synotheoides and Stigmidium exasperatum) are new to Russia. Rinodina macrospora was found for the first time in Europe. Three species, Asterophoma mazaediicola, Biatora veteranorum, and Biatoropsis minuta, are new to European Russia. 13 species were found for the first time in the middle belt of European Russia: Bachmanniomyces punctum, Bryostigma lapidicola, Heterocephalacria bachmannii, Lepra borealis, Micarea byssacea, M. melaeniza, M. nowakii, M. pseudomicrococca, M. pycnidiophora, Ochrolechia mahluensis, Scoliciosporum perpusillum, Skyttea gregaria, Stigmidium congestum, Trapeliopsis gelatinosa, Xylographa soralifera. Four threatened species (Leptogium burnetiae, Lobaria pulmonaria, Menegazzia terebrata and Nephromopsis laureri) are listed in the Red Data Book of the Russian Federation. We have made a comparison of the lichen flora diversity found in the core of the Kologriv Forest State Nature Reserve with previously obtained data in Western and Central Europe. The core of the Kologriv Forest State Nature Reserve meets the criteria of a hotspot of lichen biodiversity on the European level. We would like to emphasise the importance of finding such hotspots of lichen diversity by an inventory of the lichen flora in other Protected Areas.

Keywords

biodiversity, inventory, Kostroma Region, lichen flora, Micarea synotheoides, primeval forest, Rinodina macrospora, Stigmidium exasperatum, Usnea longissima, virgin forests

Artice information

Received: 27.04.2022. Revised: 26.06.2022. Accepted: 10.07.2022.

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References

Ahti T., Hämet-Anti L., Jalas J. 1968. Vegetation zones and their sections in northwestern Europe. Annales Botanici Fennici 5(3): 69–211.
Boch S., Prati D., Hessenmöller D., Schulze E.D., Fischer M. 2013. Richness of lichen species, especially of threatened ones, is promoted by management methods furthering stand continuity. PLoS ONE 8(1). Article: e55461. DOI: 10.1371/journal.pone.0055461
Bogdanov G.A. 2015. A list of lichens of the State Nature Reserve «Bolshaya Kokshaga». Proceedings of the State Nature Reserve «Bolshaya Kokshaga» 7: 206–244. [In Russian]
Brackel von W. 2016. Preliminary checklist of the lichenicolous fungi of Italy. Notiziario della Società Lichenologica Italiana 29: 95–145.
Coppins B.J., Kashiwadani H., Moon K.H., Spribille T., Thor G. 2021. The genera Brianaria (Psoraceae) and Micarea (Pilocarpaceae) in Japan, with reports on other interesting species in Asia. Lichenologist 53(1): 35–44. DOI: 10.1017/S0024282920000468
Czarnota P. 2007. The lichen genus Micarea (Lecanorales, Ascomycota) in Poland. Polish Botanical Studies 23: 1–199.
Dymytrova L., Brändli U.-B., Ginzler C., Scheidegger C. 2018. Forest history and epiphytic lichens: Testing indicators for assessing forest autochthony in Switzerland. Ecological Indicators 84: 847–857. DOI: 10.1016/j.ecolind.2017.08.009
Etayo J. 2010. Líquenes y hongos liquenícolas de Aragón. Guineana 16: 1–501.
Gerasimova J., Urbanavichene I., Urbanavichus G., Beck A. 2021. Morphological and phylogenetic analyses of Toniniopsis subincompta s. lat. (Ramalinaceae, Lecanorales) in Eurasia. Lichenologist 53(2): 171–183. DOI: 10.1017/S0024282921000013
Hafellner J. 2018. Lichenicolous Biota (Nos 271–300). Fritschiana 90: 1–22.
Hashimoto A., Masumoto H., Endoh R., Degawa Y., Ohkuma M. 2021. Revision of Xylonaceae (Xylonales, Xylonomycetes) to include Sarea and Tromera. Mycoscience 62(1): 47–63. DOI: 10.47371/mycosci.2020.11.001
Hawksworth D.L. 1981. The lichenocolous Coelomycetes. Bulletin of the British Museum (Natural History), Botany Series 9: 1–98.
Himelbrant D.E., Efimova A.A., Khanov Z.M., Leostrin A.V., Makryi T.V., Stepanchikova I.S. 2018. New records of lichens and lichenicolous fungi. 1. Novosti Sistematiki Nizshikh Rastenii 52(2): 445–453. DOI: 10.31111/nsnr/2018.52.2.445
Hofmeister J., Hošek J., Brabec M., Dvořák D., Beran M., Deckerová H., Burel J., Kříž M., Borovička J., Běťák J., Vašutová M., Malíček J., Palice Z., Syrovátková L., Steinová J., Černajová I., Holá E., Novozámská E., Čížek L., Iarema V., Baltaziuk K., Svoboda T. 2015. Value of old forest attributes related to cryptogam species richness in temperate forests: A quantitative assessment. Ecological Indicators 57: 497–504. DOI: 10.1016/j.ecolind.2015.05.015
Hofmeister J., Vondrák J., Ellis C., Coppins B.J., Sanderson N., Malíček J., Palice Z., Acton A., Svoboda S., Gloor R. 2022. High and balanced contribution of regional biodiversity hotspots to epiphytic and epixylic lichen species diversity in Great Britain. Biological Conservation 266: 109443. DOI: 10.1016/j.biocon.2021.109443
Ismailov A., Urbanavichus G., Vondrák J., Pouska V. 2017. An old-growth forest at the Caspian Sea coast is similar in epiphytic lichens to lowland deciduous forests in Central Europe. Herzogia 30(1): 103–125. DOI: 10.13158/heia.30.1.2017.103
Ismailov A.B., Vondrák J., Urbanavichus G.P. 2019. The express-method of estimation of epiphytic lichens diversity. Russian Journal of Forest Science 4: 294–303. DOI: 10.1134/S0024114819030045 [In Russian]
IUCN. 2001. IUCN Red List Categories and Criteria: Version 3.1. IUCN Species Survival Commission. Gland, Switzerland, Cambridge, UK: IUCN. 48 p.
Johansson P., Gustafsson L. 2001. Red-listed and indicator lichens in woodland key habitats and production forests in Sweden. Canadian Journal of Forest Research 31(9): 1617–1628. DOI: 10.1139/x01-091
Kataeva O.A. 2018. Additions to the lichen flora of Rdeiskii Nature Reserve (Novgorod Region). Botanicheskii Zhurnal 103(S8): 3–9. DOI: 10.7868/S0006813618080124 [In Russian]
Kubiak D., Osyczka P., Rola K. 2016. Spontaneous restoration of epiphytic lichen biota in managed forests planted on habitats typical for temperate deciduous forest. Biodiversity and Conservation 25(10): 1937–1954. DOI: 10.1007/s10531-016-1169-8
Kuznetsova E.S., Skazina M.A. 2010. Contribution to the lichen studying to the Kostroma Region. Novosti Sistematiki Nizshikh Rastenii 44: 200–209. [In Russian]
Ladyzhenskaya K.I. 1931. Ecological list of lichens of the surroundings of the Kologriv city. Journal of Russian Botanical Society 16(5–6): 544–553. [In Russian]
Lavrenko E.M., Geptner V.G., Kirikov S.V., Formozov A.N. 1958. Perspective plan of the geographical network of state nature reserves of the USSR (project). Nature Conservation and Conservation Science in the USSR 3: 3–92. [In Russian]
Lebedev A.N. 2018. Through pages of the history of the «Kologriv Forest». Kologrivskii Les 5: 4–5. [In Russian]
Malíček J., Palice Z., Acton A., Berger F., Bouda F., Sanderson N., Vondrák J. 2018. Uholka primeval forest in the Ukrainian Carpathians – a keynote area for diversity of forest lichens in Europe. Herzogia 31(1): 140–171. DOI: 10.13158/099.031.0110
Malíček J., Palice Z., Vondrák J., Kostovčík M., Lenzová V., Hofmeister J. 2019. Lichens in old-growth and managed mountain spruce forests in the Czech Republic: assessment of biodiversity, functional traits and bioindicators. Biodiversity and Conservation 28(13): 3497–3528. DOI: 10.1007/s10531-019-01834-4
McCarthy P.M., Elix J.A. 2020. New species and new records of Micarea (Pilocarpaceae) from Australia. Australasian Lichenology 87: 62–71.
Millanes A.M., Diederich P., Westberg M., Wedin M. 2016. Three new species in the Biatoropsis usnearum complex. Herzogia 29(2): 337–354. DOI: 10.13158/heia.29.2.2016.337
Muchnik E.E., Konoreva L.A., Kazakova M.V., Sobolev N.A. 2019. The lichen biota of the Meshchera National Park (Vladimir Region, Russia) and Meshchersky National Park (Ryazan Region, Russia). Nature Conservation Research 4(1): 64–82. DOI: 10.24189/ncr.2019.005 [In Russian]
Notov А.А., Himelbrant D.E., Stepanchikova I.S., Volkov V.P. 2016. Lichens of Central Forest State Nature Biosphere Reserve. Tver: Tver State University. 332 p. [In Russian]
Ogureeva G.N., Leonova N.B., Miklyaeva I.M., Bocharnikov M.V., Fedosov V.E., Muchnik E.E., Urbanavichus G.P., Emelyanova L.G., Khlyap L.A., Rumyantsev V.Yu., Kuzikov I.V., Lipka O.N., Arkhipova M.V., Buldakova E.V., Kadetov N.G. 2020. The Biodiversity of Russian Biomes. The Biomes of Plains. Moscow: IGKE. 623 p. [In Russian]
Orange A., James P.W., White F.J. 2001. Microchemical methods for the identification of lichens. London: The British Lichen Society. 101 p.
Paillet Y., Bergès L., Hjältén J., Odor P., Avon C., Bernhardt-Römermann M., Bijlsma R.J., de Bruyn L., Fuhr M., Grandin U., Kanka R., Lundin L., Luque S., Magura T., Matesanz S., Mészáros I., Sebastià M.T., Schmidt W., Standovár T., Tóthmérész B., Uotila A., Valladares F., Vellak K., Virtanen R. 2010. Biodiversity Differences between Managed and Unmanaged Forests: Meta-Analysis of Species Richness in Europe. Conservation Biology 24(1): 101–112. DOI: 10.1111/j.1523-1739.2009.01399.x
Red Data Book of the Kostroma Region. Kostroma: Kostroma State University, 2019. 432 p. [In Russian]
Red Data Book of the Russian Federation (plants and fungi). Moscow: KMK Scientific Press Ltd., 2008. 855 p. [In Russian]
Resl P., Fernández-Mendoza F., Mayrhofer H., Spribille T. 2018. The evolution of fungal substrate specificity in a widespread group of crustose lichens. Proceedings of the Royal Society B: Biological Sciences 285(1889): 20180640. DOI: 10.1098/rspb.2018.0640
Sheard J.W. 2010. The lichen genus Rinodina (Lecanoromycetidae, Physciaceae) in North America, North of Mexico. Ottawa: NRC Research Press. 246 p.
Sheard J.W. 2018. A synopsis and new key to the species of Rinodina (Ach.) Gray (Physciaceae, lichenized Ascomycetes) presently recognized in North America. Herzogia 31(1): 395–423. DOI: 10.13158/heia.31.1.2018.395
Sheard J.W., Mayrhofer H. 2002. New species of Rinodina (Physciaceae, Lichenized Ascomycetes) from western North America. Bryologist 105(4): 645−672. DOI: 10.1639/0007-2745(2002)105[0645:NSORPL]2.0.CO;2
Sheard J.W., Ezhkin A.K., Galanina I.A., Himelbrant D.E., Kuznetsova E.S., Shimizu A., Stepanchikova I., Thor G., Tønsberg T., Yakovchenko L.S., Spribille T. 2017. The lichen genus Rinodina (Physciaceae, Caliciales) in north-eastern Asia. Lichenologist 49(6): 617–672. DOI: 10.1017/S0024282917000536
Svensson M., Ekman S., Klepsland J.T., Nordin A., Thor G., von Hirschheydt G., Jonsson F., Knutsson T., Lif M., Spribille T., Westberg M. 2017. Taxonomic novelties and new records of Fennoscandian crustose lichens. MycoKeys 25: 51–86. DOI: 10.3897/mycokeys.25.13375
Terent'ev A.Yu. (Ed.). 2010. Chronicle of Nature of the Kologriv Forest State Nature Reserve. 1. 2009. Kologriv: Kologriv Forest State Nature Reserve. 99 p. [In Russian]
Tripp E.A., Lendemer J.C., McCain C.M. 2019. Habitat quality and disturbance drive lichen species richness in a temperate biodiversity hotspot. Oecologia 190(2): 445–457. DOI: 10.1007/s00442-019-04413-0
Urbanavichene I.N., Urbanavichus G.P. 2016. The lichen flora of the Mordovskii Reserve (an annotated species list): Flora and fauna of state nature reserves. Vol. 126. Moscow. 41 p. [In Russian]
Urbanavichene I.N., Urbanavichus G.P. 2019. New records of lichens and allied fungi from the Kostroma Region, Russia. Folia Cryptogamica Estonica 56: 53–62. DOI: 10.12697/fce.2019.56.06
Urbanavichene I.N., Urbanavichus G.P. 2020. Contributions to the lichen flora of the Kologriv Forest Nature Reserve (Kostroma Region). Novosti Sistematiki Nizshikh Rastenii 54(1): 127–138. DOI: 10.31111/nsnr/2020.54.1.127 [In Russian]
Urbanavichene I.N., Urbanavichus G.P. 2021. Additions to the lichen flora of the Kerzhensky Nature Reserve and Nizhny Novgorod Region. Novosti Sistematiki Nizshikh Rastenii 55(1): 195–213. DOI: 10.31111/nsnr/2021.55.1.195 [In Russian]
Urbanavichene I.N., Urbanavichus G.P. 2021. Additions to the lichen flora of the Kologriv Forest Reserve and Kostroma Region. Turczaninowia 24(2): 28–41. DOI: 10.14258/turczaninowia.24.2.4
Urbanavichene I.N., Urbanavichus G.P. 2022. Addition to the lichen flora of the Kerzhenskiy Reserve (Nizhny Novgorod Region). Botanicheskii Zhurnal 107(7): 687–694. DOI: 10.31857/S0006813622070109 [In Russian]
Urbanavichus G., Urbanavichene I. 2020. Four lichen species new for Russia. Folia Cryptogamica Estonica 57: 5–8. DOI: 10.12697/fce.2020.57.02
Urbanavichus G.P., Urbanavichene I.N. 2022. First records of lichenised and lichenicolous fungi for the lichen flora of Russia and Eastern Europe. Nature Conservation Research 7(2): 95–97. DOI: 10.24189/ncr.2022.024
Urbanavichus G., Vondrák J., Urbanavichene I., Palice Z., Malíček J. 2020. Lichens and allied non-lichenized fungi of virgin forests in the Caucasus State Nature Biosphere Reserve (Western Caucasus, Russia). Herzogia 33(1): 90–138. DOI: 10.13158/heia.33.1.2020.90
Urbanavichus G.P., Urbanavichene I.N., Vondrák J., Ismailov A.B. 2021. Epiphytic lichen biota of Prielbrusie National Park (Northern Caucasus, Russia). Nature Conservation Research 6(4): 77–94. DOI: 10.24189/ncr.2021.048 [In Russian]
Volosnova L.F. 2019. New data on rare species of vascular plants, fungi and lichens in the Oksky State Nature Reserve and the Ryazan Region. Proceedings of the Oksky State Nature Biosphere Reserve 38: 366–372. [In Russian]
Vondrák J., Malíček J., Palice Z., Coppins B.J., Kukwa M., Czarnota P., Sanderson N., Acton A. 2016. Methods for obtaining more complete species lists in surveys of lichen biodiversity. Nordic Journal of Botany 34(5): 619–626. DOI: 10.1111/njb.01053
Vondrák J., Malíček J., Palice Z., Bouda F., Berger F., Sanderson N., Acton A., Pouska V., Kish R. 2018. Exploiting hot-spots; effective determination of lichen diversity in a Carpathian virgin forest. PLoS ONE 13(9): e0203540. DOI: 10.1371/journal.pone.0203540
Vondrák J., Urbanavichus G., Palice Z., Malíček J., Urbanavichene I., Kubásek J., Ellis C. 2019. The epiphytic lichen biota of Caucasian virgin forests: a comparator for European conservation. Biodiversity and Conservation 28(12): 3257–3276. DOI: 10.1007/s10531-019-01818-4
Westberg M., Moberg R., Myrdal M., Nordin A., Ekman S. 2021. Santesson's Checklist of Fennoscandian Lichen-Forming and Lichenicolous Fungi. Uppsala: Uppsala University. 933 p.
Yakovlev G.V. 1976. Natural features of spruce forests of the southern taiga subzone and their renewal. PhD Thesis. Moscow. 24 p. [In Russian]
Zaugolnova L.B., Morozova O.V. 2004. Distribution and classification of nemoral-boreal forests. In: O.V. Smirnova (Ed.): East-European Forests: History in the Holocene and Present. Vol. 2. Moscow: Nauka. P. 13–61. [In Russian]
Zhurbenko M.P. 2008. Lichenicolous fungi from Russia, mainly from its Arctic. II. Mycologia Balcanica 5(1–2): 13–22.
Zhurbenko M.P., Enkhtuya O., Javkhlan S. 2019. A first synopsis of lichenicolous fungi of Mongolia, with the description of five new species. Plant and Fungal Systematics 64(2): 345–366. DOI: 10.2478/pfs-2019-0023