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Turczaninowia 27, 1: 92-101 (2024) DOI: 10.14258/turczaninowia.27.1.12 http://turczaninowia.asu.ru
ISSN 1560-7259 (print edition)
TURCZANINOWIA
ISSN 1560-7267 (online edition)
y^K 582.293.322:581.95(470+571)
Umbilicaria aprina and U. rhizinata (Umbilicariaceae, lichenized Ascomycota) in Russia
E. A. Davydov1' 9* L. S. Yakovchenko2' 10, T. M. Kharpukhaeva3' 11, E. V. Zheludeva4' 12, S. V. Chesnokov5' 6' 13, L. A. Konoreva5' 7' 14, O. A. Kataeva6' 15, E. S. Kuznetsova6' 8' 16, Yu. V. Storozhenko1' 175 P. Yu. Ryzhkova1' 185 D. E. Himelbrant6' 8' 19
1 Altai State University, Lenina Pr., 61, Barnaul, 656049, Russian Federation
2 Federal Scientific Center of the East Asia Terrestrial Biodiversity FEB RAS, Stoletiya Vladivostoka Pr., 159, Vladivostok, 690022,
Russian Federation
3 Institute of General and Experimental Biology of SB RAS, Sakh'yanova St., 6, Ulan-Ude, 670047, Russian Federation 4 Institute of Biological Problems of the North FEB RAS, Portovaya St., 18, Magadan, 685000, Russian Federation 5Botanical Garden-Institute FEB RAS, Makovskogo St., 142, Vladivostok, 690024, Russian Federation 6Komarov Botanical Institute RAS, Prof. Popova St., 2, St. Petersburg, 197376, Russian Federation 7Polar-Alpine Botanical Garden-Institute KSC RAS, Botanicheskiy Sad St., Kirovsk, 184256, Russian Federation
8 St. Petersburg State University, Universitetskaya Emb., 7-9, St. Petersburg, 199034, Russian Federation 9E-mail: eadavydov@yandex.ru; ORCID iD: https://orcid.org/0000-0002-2316-8506 10E-mail: lidiyakovchenko@mail.ru; ORCID iD: https://orcid.org/0000-0002-4342-7771 11 E-mail: takhar@mail.ru; ORCID iD: https://orcid.org/0000-0003-2213-3202 12E-mail: elena.zheludeva.88@mail.ru; ORCID iD: https://orcid.org/0000-0002-3882-7981 13E-mail: lukinbrat@mail.ru; ORCID iD: https://orcid.org/0000-0001-9466-4534 14E-mail: ajdarzapov@yandex.ru; ORCID iD: https://orcid.org/0000-0002-4487-5154 15E-mail: kataevaoa@mail.ru; ORCID iD: https://orcid.org/0000-0002-4845-7144 16E-mail: igel_kuzn@mail.ru; ORCID iD: https://orcid.org/0000-0003-1404-9182 17E-mail:yulia_storozhenko@mail.ru; ORCID iD: https://orcid.org/0000-0002-4357-478X 18E-mail:polina.ryzhkova.yu@mail.ru; ORCID iD: https://orcid.org/0000-0003-1648-9739 19E-mail: d_brant@mail.ru; ORCID iD: https://orcid.org/0000-0002-2310-1950 * Corresponding author
Keywords: Arctic, biogeography, ITS nrDNA, phylogeny, thalloconidia.
Summary. The distribution of Umbilicaria aprina and U. rhizinata in Russia was revised basing on morphological and molecular-phylogenetic data. Umbilicaria aprina is new to Alexandra Land Island (Franz Josef Land Archipelago), Sverdrup Island (Taimyr Dolgano-Nenets District), the republics of Altai, North Ossetia-Alania and Sakha-Yakutia. Umbilicaria rhizinata is new to the republics of Tyva and Buryatia, Putorana Plateau, Kamchatka Peninsula, and the Magadan Region and is therefore reported for the first time to the Asian Subarctic. New localities of the species in other regions are cited. The ITS\5.8S phylogenetic tree supports the distinctness of U. aprina and U. rhizinata. The distribution map is drawn and patterns of distribution of two species are discussed. Umbilicaria aprina occurs in the high Arctic between 74°N and 81°N, whereas the northernmost locality of U. rhizinata is in the vicinity of Norilsk on the Putorana Plateau (ca. 70°N). In mountains U. aprina grows at higher maximal elevations compared to U. rhizinata.
Поступило в редакцию 10.12.2023 Принято к публикации 22.03.2024
Submitted 10.12.2023 Accepted 22.03.2024
Распространение Umbilicaria aprina и U. rhizinata (Umbilicariaceae, лихенизированные Ascomycota) в России
Е. А. Давыдов1, Л. С. Яковченко2, Т. М. Харпухаева3, Е. В. Желудева4, С. В. Чесноков5' 6, Л. А. Конорева5, 7, О. А. Катаева6, Е. С. Кузнецова6, 8, Ю. В. Стороженко1, П. Ю. Рыжкова1, Д. Е. Гимельбрант6, 8
1 Алтайский государственный университет, пр. Ленина, д. 61, г. Барнаул, 656049, Россия
2 Федеральный научный центр биоразнообразия наземной биоты Восточной Азии ДВО РАН, пр. Столетия Владивостока, д. 159, г. Владивосток, 690022, Россия
3 Институт общей и экспериментальной биологии СО РАН, ул. Сахьяновой, д. 6, г. Улан-Удэ, 670047, Россия 4 Институт биологических проблем Севера ДВО РАН, ул. Потапова, д. 18, г. Магадан, 685000, Россия 5 Ботанический сад-институт ДВО РАН, ул. Маковского, д. 142, г. Владивосток, 690024, Россия 6 Ботанический институт им. В. Л. Комарова РАН, ул. Проф. Попова, д. 2, г. Санкт-Петербург, 197376, Россия 7Полярно-альпийский ботанический сад-институт КНЦ РАН, ул. Ботанический сад, г. Кировск, 184256, Россия
8 Санкт-Петербургский государственный университет, Университетская набережная, д. 7-9, г. Санкт-Петербург, 199034, Россия
Ключевые слова: Арктика, биогеография, таллоконидии, филогения, ITS ярДНК.
Аннотация. Выявлено распространение Umbilicaria aprina и U. rhizinata в России на основе морфологических и молекулярно-филогенетических данных. Umbilicaria aprina является новым видом на островах Земля Александры (архипелаг Земля Франца-Иосифа), Свердруп (Таймырский Долгано-Ненецкий округ), в республиках Алтай, Северная Осетия-Алания и Саха (Якутия). Umbilicaria rhizinata является новым для республик Тыва и Бурятия, плато Путорана, полуострова Камчатка и Магаданской области. Таким образом, вид U. rhizinata впервые зарегистрирован в Азиатской Субарктике. Указаны новые местонахождения в других регионах. Представлено филогенетическое дерево, подтверждающее различие U. aprina и U. rhizinata. Составлена карта распространения и обсуждены закономерности распространения двух видов. Umbilicaria aprina встречается в высоких широтах Арктики между 74° и 81° северной широты, тогда как самым северным местонахождением U. rhizinata являются окрестности Норильска на западе Плато Путорана (около 70° северной широты). Аналогично, в горах максимальные отметки U. aprina выше, чем у U. rhizinata.
Introduction
Species of Umbilicariaceae Chevall. are predominantly saxicolous lichens mostly found in higher latitudes or at higher elevations worldwide. Umbilicaria aprina Nyl. and U. rhizinata (Frey et Poelt) Krzewicka are related species from the ' Umbilicaria aprina group' - a monophyletic batch of morphologically similar taxa within Umbilicaria Hoffm. subg. Umbilicaria. Species of the Umbilicaria aprina group have a slightly areolate or reticulate center of the grey-coloured upper thallus surface, scarce to dense, simple or branched rhizinomorphs, non-septate to 10-septate thalloconidia, and omphalodisc apothe-cia with asci containing hyaline, unicellular asco-spores. Species of the Umbilicaria aprina group are characteristic to harsh environments in polar and high mountain regions (Davydov et al., 2017).
Umbilicaria aprina is a cosmopolitan species that occurs in the Arctic and Antarctic, as well as almost all highest mountains with glaciers (Ryvar-den, 1968; Crespo, Sancho, 1982; 0vstedal, Lewis Smith, 2001; Hansen, 2003; Kristinsson et al., 2010; Hestmark, 2016). The first record of the species for Russia was made by A. V. Dombrovskaya (1970), as Gyrophora canescens Dombr. (= U. aprina) from Khi-biny Mountains (Kola Peninsula). Umbilicaria aprina has been also reported for the Arctic: Franz Josef Land Archipelago (Konoreva et al., 2019), Severnaya Zemlya Archipelago and Novosibirskie Is. (Davydov, Zhurbenko, 2008), in the Caucasus (Davydov et al., 2019b), Baikal area in South Siberia (Urbanavi-chene, Urbanavichus, 2001), and Kamchatka Peninsula (Dombrovskaya, 1970; Davydov et al., 2011), as well as for Yakutia in the Lichen Flora of Russia (Davydov, 2017) but without exact location.
Umbilicaria rhizinata was first described as U. decussata (Vill.) Zahlbr. var. rhizinata Frey et Poelt from Himalaya Mts. in Nepal (Poelt, 1977), and subsequently raised to the species level by Krze-wicka (2010) who additionally reported this taxon to Kilimanjaro Mt. (Tanzania) and the South American Andes in Bolivia (Krzewicka, 2010). The synonymy of U. rhizinata was clarified recently (Davydov, 2022) and the distribution of the species has been expanded to North America and Xinjiang in China. In Russia the species was recorded from the Altai Mts. and the Stanovoye Nagor'e Highlands (Davydov et al., 2019a, b; Davydov, 2022).
Umbilicaria rhizinata is closely related to U. aprina and differs mainly by a smaller size of 3-4 cellular (vs. 1-2 cellular) thalloconidia. The species boundaries are not clear for many taxa, and U. rhizinata is represented in the GenBank by a single ITS sequence. The aim of the study was to provide additional data on the distribution of two species in Russia mostly basing on recently collected specimens and to test the monophyly of U. rhizinata by molecular phylo-genetic method using ITS sequences.
Materials and methods
Sampling andphenotypic studies
The core material for the study was collected by authors between 2009 and 2022 in different regions of Russia and deposited in herbaria ALTB, LE, LECB, MAG, UHU, and private collections of the authors.
Additionally, specimens were studied from the herbaria HMAS, KPABG, KW, LE, and NS.
The specimens were examined using a stereo-microscope (Zeiss Stemi 2000-C) and a compound microscope (Zeiss Axio Lab.A1). Anatomical examination was undertaken using hand-cut sections mounted in water. Lichen substances were studied using high performance thin-layer chromatography (HPTLC) with solvent systems B' (hexane: methyl tert-butyl ether: formic acid, 140 : 72 : 18) and C (toluene: acetic acid = 170 : 30) (Culberson, Kris-tinsson, 1970; Culberson, Johnson, 1982; Orange et al., 2001). We used a scanning electron microscope (SEM) to visualize thalloconidia. Microphotographs were obtained using a Carl Zeiss EVO MA 10 SEM. The samples were dried in air and fixed on aluminum stubs with double-sided sticky film, and then, gold was sprayed on them.
DNA extraction, amplification and sequencing
Single thallus parts (100-200 mg) were carefully checked for fungal infections and thoroughly
cleaned of extraneous matter, excised under a magnifying lens, and transferred to sterile 1.5 ml reaction tubes. The samples were frozen in liquid nitrogen and powderized in the tubes using sterile pestles. DiamondDNA Plant Kit (ABT) was used for DNA extraction as recommended by the manufacturer.
To test the phylogenetic relationships within the species, the internal transcribed spacer region of nuclear ribosomal DNA (ITS) was amplified in a single reaction using ITS 1F-5' as a forward primer and ITS 4-3' or LR3-3' as a reverse primes (Vilgalys, Hester, 1990; White et al., 1990; Gardes, Bruns, 1993). Same primers were used for sequencing. Cycling conditions included initial denaturation at 94 °C for 35 cycles of 95 °C for 20 s, 52 °C for 40 s, 72 °C for 60 s, and a final extension step at 72 °C for 7 min. The program Geneious 6.0 (Biomatters Ltd., New Zealand) was used for assembling sequence reads and datasets. Consensus sequences were compiled from double-stranded sequenced parts of the sequences.
Sequences and phylogenetic reconstructions
To test the phylogenetic relationships of Umbili-caria aprina and U. rhizinata collected in Russia, the ITS region of the nrDNA (ITS1, 5.8S, and ITS2 nrDNA) was sequenced (Table). These markers were chosen because they were used in phylogenetic analyses recently (Davydov et al., 2017).
All newly obtained sequences were supplemented with sequences obtained during our previous study of Umbilicariaceae phylogeny (Davydov et al., 2017), representing species of the U. aprina group, as well as selection of sequences from different subgenera of Umbilicaria (Fig. 1); Xylopsora friesii (Ach.) Ben-diksby et Timdal was used as the outgroup. Selection of the outgroup is based on our previous study (ibid.). GenBank Accession numbers are provided on Fig. 1. Newly generated sequences are listed in Table. ITS\5.8S 484 bp matrix were aligned using the MAFFT algorithm (Katoh et al., 2005). The most likely tree and 1000 rapid bootstrap replicates were calculated using RAxML 8.0.26 (Stamatakis, 2014) by raxmlGUI software version 1.3.1 (Silvestro, Michalak, 2012) applying the GTRGAMMA model of substitution to ITS1, 5.8S, and ITS2 subsets.
The tree topologies are taken from RAxML (Fig. 1). Bootstrap support values were noted onto the best scoring tree.
Table
Sample numbers and GenBank accession numbers for the newly obtained sequences of Umbilicaria aprina and U. rhizinata
Species name Source: collection location and collection number or reference GenBank accession number
Umbilicaria aprina Russia, Franz Josef Land, Alexandra Land, Severnaya Bay, S. V. Chesnokov (ALTB-L7730) OR916138
Umbilicaria aprina Russia, Krasnoyarsk Territory, Sverdrup Is., L. A. Konoreva (ALTB-L7371) OR916139
Umbilicaria aprina Russia, Republic of Buryatia, Urgedeevsky Range, T. M. Kharpukhaeva (UUH, ALTB-L6594) 0R916140
Umbilicaria rhizinata Russia, Republic of Altai, Altai Mts., Katunsky Range, E. A. Davydov 7446 (ALTB) 0R916141
Umbilicaria rhizinata Russia, Republic of Altai, Altai Mts., Katunsky Range, E. A. Davydov 7421 (ALTB) 0R916142
Umbilicaria rhizinata Russia, Kamchatka Peninsula, Petropavlovsk-Kamchatsky, Mishennaya Sopka Hill, D. E. Himelbrant and E. S. Kuznetsova K-1 (LE-L7465) 0R916143
Umbilicaria rhizinata Russia, Altai Territory, Altai Mts., Tigireksky Range, E. A. Davydov 7562 (ALTB) 0R916144
Umbilicaria rhizinata Russia, Krasnoyarsk Territory, Norilsk, A. A. Ul'yanovskiy (ALTB) 0R916145
Umbilicaria rhizinata Russia, Republic of Buryatia, Nam-Tzagan-Khutliyn-Nuruu Range, T. M. Kharpukhaeva (UUH-L01925) 0R916146
Umbilicaria rhizinata Russia, Magadan Region, Malyk Lake, E. V. Zheludeva SU4883 (MAG) 0R916147
Umbilicaria rhizinata Russia, Magadan Region, Urultun Lake, E. V. Zheludeva SU4884 (MAG) 0R916148
Results
Specimens of U. aprina and U. rhizinata were identified basing on their morphology and anatomy. Phylogenetic analysis supported the identifications. Thus, septation of thalloconidia is a constant diagnostic trait for U. aprina and U. rhizinata.
The phylogenetic study.
According to the ITS/5.8S phylogram (Fig. 1), the sequences of species of Umbilicaria aprina group cluster together with high statistical support (RAx-ML 100 % BS). Within U. aprina group, sequences of U. aprina and U. rhizinata clustered separately, which indicates distinctness of two species. Nine sequences of Umbilicaria rhizinata from different regions of Russia clustered together with high support (RAxML 87% BS), which indicates their identity. Six sequences of Umbilicaria aprina clustered in three subclades at the basal part of U. aprina group, but this segregation lacks bootstrap support.
The secondary chemistry.
All studied specimens were investigated by TLC. Both species showed the same spots pattern in TLC, and contain gyrophoric acid as a major and lecanoric as a minor compound.
The species and their distribution.
Umbilicaria aprina Nyl., 1869, Syn. Meth. Lich. 2: 12. (Fig. 2 A-D).
Holotype: [Ethiopia] "Abyssinia. Dedschen Mts, elev. 14200 ft. W. Schimper" (H-NYL! [H-NYL31742]).
= Umbilicaria canescens (Dombr.) N. S. Golubk.
= Gyrophora canescens Dombr.
Holotype: [Russia, Murmansk Region] "Peninsula Kolaënsis, montes Chibinensis, ad declivi-tatem australem montis Vudjavrczorr, elev. 380 m, in schistosis ad lapides nudis, No. 6. 05 VI 1965. A. V. Dombrovskaya" (LE! [L-266]).
The morphological description of the species is given in the literature (Ryvarden, 1968; Wei, Jiang, 1993; Hestmark, 2015; Davydov, 2017).
Selected specimens examined. Here we omit specimens which have been cited in our previous publications (Davydov, Zhurbenko, 2008; Davydov et al., 2011; Davydov et al., 2019b; Konoreva et al., 2019). RUSSIA. Murmansk Region: "Khibiny Mts., Slope of Rasvumchorr Mt., elev. 744 m. 33.83661°N, 67.64343°E, on steep rock. 31 VII 2023. A. V. Mele-chin" (KPABG-L20976); "NW slope Woodyavrchorr Mt., elev. 400 m, 33.61900°N, 67.65508°E, on flat rocks. 28 VIII 1975. A. V. Dombrovskaya (KPABG-
L16332); "The slope of the valley of the Vuonnem-jok River near the Yuksporrlak Pass, elev. 670 m. 33.834457°N, 67.658081°E, mountain tundra, on a cliff. 21 VII 1974. A. V. Dombrovskaya" (KPABG -L4434); "Monchegorsky District, Nyavka-tundra Range, in the middle course of the Liva River, 9 km upstream of the Livozero Lake, elev. 140 m, 31.354993°N, 67.834112°E, spruce forest, on a stone. 21 VII 1973. A. V. Dombrovskaya" (KPABG-L2707). Arkhangelsk Region: "Franz Josef Land Archipela-
go, Alexandra Land Is., Severnaya Bay, the vicinity of the Omega research camp, elev. 15 m. 80°46'36.4"N, 47°48'00.9"E, rubble-moss-lichen community on the shore, on rocks. 13 VII 2019. S. V. Chesnokov" (ALTB-L7076); ibid., "elev. 14 m. 80°46'36.1''N, 47°48'35.0''E, large boulders on the shore, on rocks. 14 VII 2019. S. V. Chesnokov" (ALTB-L7730); Krasnoyarsk Territory: "Taimyr Dolgano-Nenets District, Sverdrup Is., elev. 1 m. 74°33'22.2"N, 79°30'32.6"E, hummock-grass community, on rocks. 10 IX 2021.
87
18
26 35
41
100
69
60 1!
OR916145, U. rhizinata ' OR916143, U. rhizinata OR916146, U. rhizinata OR916142, U. rhizinata OR916141, U. rhizinata KY948011, U. rhizinata OR916147, U. rhizinata OR916148, U. rhizinata OR916144, U. rhizinata
- KY947733, U. formosana
— KY947743, U. africana L- KY947849, U. antarctica
KY948014, U. aprina KY947859, U. aprina OR916138, U. aprina OR916139, U. aprina r OR91614Q, U. aprina
U. rhizinata
U. aprina
t
KY947810, U. aprina 0(Q_c KY947752, U. krascheninnikovii " KY947857, U. krascheninnikovii KY948001, U. decussata KY947830, U. polaris
EU909467, U. pustuiata
Cl
o
CD
cd
C
C;
cl
cd
- EU909462, U. pensyivanica
— KY947998, U. hyperborea KY947829, U. proboscidea - KY947834, U. angulata
— KY947735, U. pulvinaria
_I— KY947749, U. coriacea
^L- KY947850, U. ieiocarpa
- KY947746, U. torrefacta
- KY947734, U. lambii
d
KY947997, U. muehienbergii KY947753, U. deusta — KY947833, U. semitensis
KY947740, Xylopsora friesii
0.04
Fig. 1. The maximum likelihood (ML) phylogeny of the selected Umbilicaria ITS of nrDNA sequences. Numbers at the tree nodes indicate ML bootstrap percentages. Accession numbers are given to serve as operational taxonomic unit (OTU) names (www.ncbi.nlm.nih.gov). Originally produced sequence is marked in bold. Voucher specimens are listed in Table.
S. V. Chesnokov" (ALTB-L7370, L7373); ibid., "elev. 1 m. 74°33'22.5"N, 79°31'23.6"E, stones and driftwood on the shore, on rocks. 10 IX 2021. L. A. Ko-noreva" (ALTB-L7371, L7372); Republic of Yakutia: "Bulunsky District, Novosibirsk Archipelago, Bunge Land, the central part. 3 IX 1954. E. S. Korotkevich" (KW-42979); "Tomponsky District, Verkhoyansk Mts., basin of the Lower Aldan River, left bank of the Hunkhada River below the mouth of the Nekucheen River (right bank of the Tomp o River), elev. 1633.1 m, crustose epilithic lichen cold desert, on rocks. 18 IX 1951. V. Kuvaev 185/2" (LE-L6742); Kamchatka Territory: "The vicinity of Petropavlovsk-Kam-chatsky, the bank of the Halaktyrka River, elev. 100 m, 158.78351°N, 52.98618°E, on steep rock in Betula forest. 12 VII 1980. A. V. Dombrovskaya" (KPABG-L4410); "Valaginsky Range, peak of Pereval Mt., elev. 1780 m. 54°53'N, 159°55'E, on rocks. 25 VI 1984. A. Mikulin" (VLA 840625-18-1, ALTB-L6252); Mil'kovo District, SW slope of Tolbachik Volcano, lava stream, 55°46'35"N, 160°18'42"E, elev. 1610 m, dwarf shrub tundra. 16 VIII 2008. D. E. Himelbrant, I. S. Stepanchikova K-46-08" (LECB). Republic of Altai: "Kosh-Agach District, N macroslope of Seve-ro-Chuisky Range, elev. ca. 2500 m, on rocks. 19 VII 1981. N. V. Sedelnikova" (NS); Republic of Burya-tia: "Tunkinsky District, Urgedeyevsky Range, slope of the eastern exposition, high mountain lake, elev. 2350 m. 51°23'51.8"N, 102°12'33.3"E, lichen tundra, on rocks. 18 VII 2018. T. M. Kharpukhaeva" (ALTB-L6594).
Distribution in Russia: Murmansk Region (the Khibiny Range), Arkhangelsk Region (Franz Josef Land Archipelago), Krasnoyarsk Territory (Sverdrup Is., Severnaya Zemlya Archipelago), Republic of Yakutia (Novosibirsk Archipelago, Verkhoyansk Mts.), Kamchatka Territory (Gamchensky and Valaginsky Ranges), the Caucasus (republics of Kabardino-Balkaria and North Ossetia-Alania), Republic of Altai (Altai Mts.), Republic of Buryatia (Urgedeyevsky and Khamar-Daban ranges) (Fig. 3).
Umbilicaria rhizinata (Frey et Poelt) Krzewicka, 2010, Lichenologist 42(4): 491 (Fig. 2 E-H).
= Umbilicaria decussata (Vill.) Zahlbr. var. rhizinata Frey et Poelt in Poelt, 1977 Khumbu Himal 6(3): 419.
Lectotype: [Nepal]. "Mahalangur: Himal Khumbu, Moränen des Lobuche-Gletschers bei Lobuche, elev. 4950-5000 m. IX 1962. J. Poelt L247a" (M! [M0035585]; iso - M! [M0035586]).
= Umbilicaria aprina Nyl. var. halei Llano, 1956. J. Wash. Acad. Sci. 46: 183.
Holotype: [Canada]. "N.W.T.: Baffin Island, head of Clyde Fiord, on exposed gneiss boulders. 26 VIII 1950. M. E. Hale 450" (MIN! [MIN664956]).
The morphological description of the species is given in the literature (Poelt, 1977; Krzewicka, 2010; Hestmark, 2015; Davydov, 2017, 2022).
Selected specimens examined. Here we omit specimens which have been cited in our previous publications (Davydov, Zhurbenko, 2008; Davydov et al., 2011; Davydov et al., 2019a, b; Davydov, 2022). RUSSIA, Krasnoyarsk Territory: "the western part of the Putorana Plateau, Norilsk, the vicinity of the Talnakh District, elev. 371 m, 69.478630°N, 88.543432°E, steep slope-scree without vascular plants, on rocks. 04 IX 2021. A. A. Ulyanovskiy" (LE); Magadan Region: "Omsukchansky District, foothills of Kilganskie Range, vicinity of mining camp Dzuletta, ca. 500 km NE from Magadan, elev. 1480 m. 61°11'39.8"N, 153°58'49.8"E, local summit at the slope, on rocks. 11 VIII 2012. L. S. Yakovchenko 1265" (hb. Yakovchenko); "Susumansky District, left bank of Urultun Lake, elev. 975 m. 63°48'17.42"N, 148°14'37.34"E, rocky scattering on the slope, on rocks. 20 VIII 2021. E. V. Zheludeva" (MAG, ALTB-L6933); ibid., "Malyk Lake, mouth of the Okhandya River, mountain slope on the left bank, elev. 961 m. 63°34'39.96"N, 147°54'43.94"E, rocky area near the waterfall, on rocks. 25 VII 2020. E. V. Zhelude-va" (MAG, ALTB-L6934); Kamchatka Territory: "Elizovsky District, Petropavlovsk-Kamchatsky, E slope of Mishennaya Sopka Hill, elev. 370 m. 53°2'36''N, 158°38'28''E, on rocks (old lava). 29 VII 2002. D. E. Himelbrant, E. S. Kuznetsova K-1" (LE L-7465); Republic of Altai: "Kosh-Agachsky District, Sailjugem Range, left bank of the Bayan-Chagan River, at 5.5 km upstream of the junction of the Karasu River, elev. 2600-2800 m. 49°30'42"N, 88°46'48"E, on rocks. 13 VI 2014. E. A. Davydov 14502 and L. S. Yakovchenko" (ALTB); "Ust'-Koksinsky District, Ka-tunsky Range, upper reaches of the Ak-Kem River, right bank, elev. 2895 m. 49°57'23.3''N, 86°29'14.5''E, stone fields and rocks (Plot-21), on boulders. 12 VIII 2009. E. A. Davydov 7388" (ALTB); ibid., "watershed between the Ak-Kem and Kucherla Rivers, elev. 2605 m. 50°00'57.2''N, 86°27'09.8''E, stone fields and rocks (Plot-25), on stones. 15 VIII 2009. E. A. Davydov 14403" (ALTB); ibid., "elev. 2621 m. 50°00'28.9"N, 86°27'52.4"E, stone fields and rocks (Plot-30), on boulders. 19 VIII 2009. E. A. Davydov 7447" (ALTB); ibid., "elev. 2650 m. 50°01'16.9"N, 86°26'55.4"E, stone fields and rocks (Plot-24), on boulders. 15 VIII 2009. E. A. Davydov 7446" (ALTB); ibid., "elev. 2381 m. 50°01'58.9"N, 86°26'05.8"E,
stone fields and rocks, on boulders. 14 VIII 2009. Pinus sibirica forest with stones in a water, on rocks.
E. A. Davydov 7421" (ALTB); Katunsky Range, right 5 VII 2000. E. A. Davydov 5660" (ALTB); Repub-
bank of the Multa River near Verkhnee Multinskoe lic of Tuva: "Mongun-Taiginsky District, Mongun-
Lake, elev. 1773 m. 49°56'N, 85°51'E, Abies sibirica- Taiga Massif, headwaters of the Mugur River, at 27.5
Fig. 2. The habit and thalloconidia of Umbilicaria aprina and U. rhizinata. A-D. Umbilicaria aprina (ALTB-L7730): A -upper side; B - lower side; C - thalloconidia in water; D - SEM of thalloconidia on the lower surface. E-H. Umbilicaria rhizinata (ALTB-L6879): E - upper side; F - lower side; G - thalloconidia in water; H - SEM of thalloconidia on the lower surface. Scales: A, B, E, and F = 1 cm; C, D, G, and H = 20 цт.
km W from Mugur-Aksy, elev. 2800 m. 50°18'35"N, 90°04'06"E, alpine meadows and mountain tundra with stones, on a boulder. 13 VII 2014. E. A. Davy-dov 14477, 14503 and L. S. Yakovchenko" (ALTB); ibid., "at 27 km W from Mugur-Aksy, elev. 2720 m. 50°19'11"N, 90°04'31"E, alpine meadows and mountain tundra with stones, on a boulder. 13 VII 2014. E. A. Davydov 14471, 14476 and L. S. Yakovchenko" (ALTB); ibid., "left side of the Toolaity River's Valley, at 3.5 km upstream from the Eski-Toolaity Lake, elev. 2450-2600 m. 50°11'N, 90°09'E, mountain tundra, stone field, on a boulder. 04 VII 2014. E. A. Davydov 14475 and L. S. Yakovchenko" (ALTB); ibid., "right side of the Khairykan River's Valley, at 3.7 km upstream from its mouth (Mugur River), elev. 2520 m. 50°18'20"N, 90°12'06"E, stone fields within alpine meadows and mountain tundra, on a boulder. 12 VII 2014. E. A. Davydov 14472 and L. S. Yakovchenko" (ALTB); Altai Territory: "Zmeinogor-sky District, Tigireksky Range, headwaters of Bol-
shoy Tigirek River, at 11 km N of Tigirek Settlement and 2.7 km SE of Razrabotnaya Mt., elev. 1800 m. 51°02'53"N, 83°00'41"E, timberline, on stone field. 4 VIII 2010. E. A. Davydov 7562" (ALTB); ibid., "at 11.5 km S of Tigirek Settlement and 3 km NW of Razrabotnaya Mt., elev. 1540-1600 m. 51°02'53"N, 83°00'27"E, rocks and stonefields, on rocks at the top of the Range. 21 VII 2012. E. A. Davydov 7258" (ALTB); Republic of Buryatia: "Tunkinsky District, Nam-Tzagan-Khutliyn-Nuruu Mt., northern slope, elev. 1933 m. 51°22'15.7"N, 102°09'40.4"E, stream shore, silicate rock outcrops, on rocks. 16 VII 2018. T. M. Kharpukhaeva" (UUH-L01925).
Distribution in Russia: Krasnoyarsk Territory (Putorana Plateau), Magadan Region (Kilgan-skie and Cherskogo ranges), Kamchatka Territory (Mishennaya Sopka Hill), Altai Mts (Altai Territory, republics of Altai and Tyva), Republic of Buryatia (Nam-Tzagan-Khutliyn-Nuruu Range), Trans-Baikal Territory (Kodar Ridge). (Fig. 3).
Fig. 3. The known distribution of Umbilicaria aprina (red) and U. rhizinata (black) in Russia based on the investigated specimens.
Discussion
We proved the distinction of two species of Umbilicaria aprina group: U. aprina and U. rhizinata. Umbilicaria aprina is a well-known species from harsh Polar and glacial high mountain habitats.
Locally, especially in regions with a maritime climate, e.g. Kamchatka or Kola Peninsula, U. aprina can grow on rocks near the timberline or even in upper part of the forest belt. It is a common trait for other arctic alpine species and depends on a local climate. The species is widespread in continental Antarctica
and is a model for studies in physiology of lichens in harsh condition, e. g. photosynthetic activity in different water content (Kappen, Breuer, 1991), CO2 exchange and water relations in lichens at subzero temperatures (Schroeter et al., 1994; Schroeter, Scheidegger, 1995), photosynthesis and respiration at low temperatures and strong sun irradiance conditions (Green et al., 1998; Kappen et al., 1998; Sancho et al., 2003; Singh et al., 2012), seasonal activity (Schroeter et al., 2011), and dehydration resistance (Haranczyk et al., 2008). The distribution of U. aprina has been extensively studied (see the introduction). Nevertheless, here we report the species for the first time to Alexandra Land Island (Franz Josef Land Archipelago), Sverdrup Island (Taimyr Dolgano-Nenets District), and Yakutia.
In contrast to the previous species, the ecology and the distribution of U. rhizinata have so far been insufficiently studied, and the available data are scattered to discuss the range and ecological preferences of the species. The knowledge on the distribution of U. rhizinata has been increasing significantly; here we report the species as new to such macro regions as the republics of Tyva and Buryatia, Putorana Plateau, Kamchatka Peninsula, and the Magadan Region. Thus, for the first time, we have the opportunity to assess differences in ecology and distribution of two species. In Russia both species
occur in Arctic-Subarctic or high mountain ('alpine') saxicolous communities above the timberline, but we never collected both species in the same locality. This fact may point at different distributional patterns of the species. Umbilicaria aprina occurs in high Arctic between 74°N and 81°N, whereas the northernmost locality of U. rhizinata is in the vicinity of Norilsk in Putorana Plateau (ca. 70°N). Both species, U. aprina and U. rhizinata, occurred in different localities in the same mountain region, in the republics of Altai, Buryatia, the Magadan Region, and Kamchatka Peninsula. Similarly, in the mountainous regions, U. aprina grows in harsher environment conditions - higher elevations or north-exposed slopes.
Acknowledgements
We are grateful to Prof. O. Blum (KW) and Prof. M. P. Andreev (LE) and Dr I. A. Galanina (VLA), Dr. A. V. Melechin (KPABG), and Dr T. V. Makryi (NS) for their hospitality during the visits of ED to Kyiv, ED, LY, YS and PR to St. Petersburg, ED and PR to Vladivostok, and ED to Apatity and Novosibirsk, respectively. Authors thank A. A. Ul'yanovskiy (St. Petersburg) for providing the specimen from the vicinity of Norilsk. We are also indebted to Dr Anna Erst (Novosibirsk, Russia) for technical assistance with SEM. This study was funded by the Russian Science Foundation as research project № 22-24-00283.
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