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8The genus Parmelina (Parmeliaceae) in the Russian Caucasus I. N. Urbanavichene
Komarov Botanical Institute RAS, Professor Popov Str., 2, St. Petersburg, 197376, Russia; [email protected]
Abstract. The present study provides a brief survey of the genus Parmelina in the Russian Caucasus (Western Transcaucasia, Western, Central and Eastern Caucasus) with a special emphasis on species distribution. The study area is located in the largest nature reserves of the Russian Caucasus — Kavkazskiy, Utrish, Severo-Osetinskiy, Erzi. This paper contributes to a better understanding of the genus in the Caucasus, focusing mainly on the author's collections in different regions of the Northern Caucasus in 2008-2016. Four species have been identified from the Russian Caucasus — Parmelina carporrhizans, P. pastillifera, P. quercina and P. tiliacea. Notes on their morphology, anatomy, ecology and distribution are based on data obtained from a study of ca. 20 specimens of each species. The presence of whitish macules on the upper surface of P. carporrhizans (after Clerc, Truong, 2008) as an important diagnostic feature was shown. The Caucasian material shows the differences in size and proportions of ascospores, size and shape of pycnoconidia between critical species P. car-porrhizans and P. quercina. An identification key for Caucasian Parmelina species is composed for the first time and can be used for central regions of Russia.
Keywords: lichens, genus Parmelina, taxonomic review, key to species, Caucasus, nature reserves, Russia.
Род Parmelina (Parmeliaceae) на Российском Кавказе И. Н. Урбанавичене
Ботанический институт им. В. Л. Комарова РАН, лаборатория лихенологии и бриологии, ул. Профессора Попова, д. 2, Санкт-Петербург, 197376, Россия; [email protected]
Резюме. Представлен краткий обзор рода Parmelina для основных российских районов Кавказа — Западного, Центрального, Восточного и Северо-Западного Закавказья. Район исследований включает территории четырех крупнейших на Кавказе российских заповедников — Кавказского, Северо-Осетинского, Утриш, Эрзи. Особое внимание уделено морфологическим, анатомическим признакам и распространению выявленных видов. Анализ особенностей строения и распространения представителей рода Parmelina в изученных районах основан на сборах 2008-2016 гг. Четыре вида рода Parmelina были выявлены для российской части Кавказа — P. carporrhizans, P. pastillifera, P. quercina and P. tiliacea. Данные получены при изучении в среднем более чем 20 образцов каждого вида. В качестве важного диагностического признака, согласно работе Clerc и Truong (2008), использовано наличие беловатых макул на верхней поверхности у P. carporrhizans. На кавказском материале показаны различия между видами P. carporrhizans и P. quercina, заключающиеся в размерах и пропорциях аско-спор, а также в размерах и форме пикноконидий. Впервые составлен ключ для
кавказских видов рода Parmelina, который может быть использован и при изучении лихенофлоры центральных регионов России.
Ключевые слова: лишайники, род Parmelina, таксономический обзор, ключ для определения видов, Кавказ, природные заповедники, Россия.
The Parmelina Hale species have been studied by numerous researchers. There are many papers on the morphology and taxonomy of the genus Parmelina, as well as a lot of molecular data and population genetics studies in the Mediterranean, Southern and Central European regions (Alors et al., 2014; 2017; Arguello et al, 2007a, b; Clerc, Truong, 2008; NMez-Zapata, 2013; NMez-Zapata et al, 2011; 2015). The present paper continues the series of those on the lichen flora the Russian Caucasus (Urbanavichene, Urbanavichus, 2014, 2016; Urbanavichus, Urbanavichene, 2014, 2015). The aim of this study is to refine our knowledge of the morphological and anatomical features in the delimitation of Parmelina species. Research by NMez-Zapata (2013), combining molecular, chemical, geographical and ecological characters within the genus Parmelina, especially P quercina s. l., served as the basis for our work.
Since its establishing by Hale (1976), the circumscription of the genus Parmelina has undergone significant changes: of the 47 species, only 9 species remained (Elix, Hale, 1987; Divakar et al., 2010; Nelson et al., 2012), namely P quercina (Willd.) Vain., P carporrhizans (Taylor) Poelt et Vezda, P. pastillifera (Harm) Hale, P. tiliacea (Hoffm.) Hale, P. atri-cha (Nyl.) P. Clerc, P. coleae Arguello et A. Crespo, P. cryptotiliacea A. Crespo et NMez-Zapata, P. gyrophorica Elix et al. and P. yalungana (Zahlbr.) P. R. Nelson et Kepler. Only three species of Parmelia now treated as Parmelina were mentioned by Rassadina (1971) from Russia and the Caucasus in general: Parmelia quercina (Willd.) Vain., P. carporrhizans Tayl. and P. scortea Ach. (P scortea f. scortea and P. scortea f. coerulescens Harm).
Currently four species of Parmelina are identified from the Russian Caucasus, namely P. carporrhizans, P. pastillifera, P. quercina and P. tili-acea. All Parmelina species are common in the lowlands up to ca. 1850 m a. s. l. in the virgin or slightly anthropogenically disturbed woods. The habitats of Parmelina species in the Caucasus are confined to broadleaved and mixed coniferous-broadleaved forests. In the studied territory P. quer-cina, P. pastillifera and P. carporrhizans are corticolous, and only P. tili-acea may be saxicolous.
Material and methods
Specimens of Parmelina were collected in the Russian Caucasus in 2008-2016. The study is based on the author's collections and mostly field identifications (with light microscope). In such cases the author's name is not specified in the lists of examined specimens below. Some specimens were collected by the author together with G. Urbanavichus and J. Vondrak. Only representative specimens are deposited in the Herbarium of the Komarov Botanical Institute and marked by the Herbarium abbreviation (LE).
The presented results are based on ca. 80 field identifications and representative specimens of Parmelina from the Caucasian nature reserves — Utrish (coll. by I. Urbanavichene et G. Urbanavichus), Kavkaz-skiy (coll. by I. Urbanavichene, G. Urbanavichus et J. Vondrak), Severo-Osetinskiy (coll. by I. Urbanavichene et G. Urbanavichus), Erzi (coll. by I. Urbanavichene et G. Urbanavichus).
Morphology and anatomical structure of the species were studied by Zeiss microscopes (Axio Scope A1, Stemi 2000CS). Selected specimens were analyzed for secondary metabolites by high performance thin-layer chromatography (HPTLC) (Arup et al., 1993). When searching for new and cryptic species and identification of problematic species P. quercina and P. carporrhizans, the ITS 1 and 2, including 5,8S rDNA sequences were obtained.
The key with morphological and anatomical characters, based on an analysis of our herbarium material from the Russian Caucasus, uses indicative characteristics, including the ascospores length to width ratio (abbreviated as l/w) measured in 20-30 well developed ascospores and pycnoconidia of fertile specimens.
The subdivision of the Caucasus in the lists of studied specimens below follows Menitskiy (1991): Western Caucasus, Central Caucasus, Eastern Caucasus, North-Western-Transcaucasia, and Western Transcaucasia.
Results
The genus Parmelina Hale is characterized by a foliose greyish white thallus with linear to sublinear lobes and cilia in the axils or margins, lecanorine apothecia, white medulla with black lower cortex; simple, black rhizines reaching the edge of the lobes; ellipsoid ascospores, thin-walled excipular cells darkly pigmented at the edge of the apothecium; presence of lecanoric or gyrophoric acid in the medulla (C+ rose-red), atranorin in the cortex (K+ yellow) (Hale, 1976; Clerc, Truong, 2008; Crespo et al., 2010; Divakar et al., 2010; Nelson et al., 2012; Nunez-Za-pata, 2013). The morphologically closest genus Myelochroa (Asahina)
Лриморско-Ахтарск
Timashevsk Тимашевск
Iихорецк
Kropotkin 0Korenovsk Кропоткин Кореновск
ipatovo Ипатово
Slavyansk-na-Kubani0 Славянск-на-Кубани
Anapa Анапа
Svetlograd Светлофад
Novoro'__
Новороссийск"
Gelendzhik Геленджик
Krasnodar Краснодар
I n ,|jp Goryachy Klyuch Горячий Ключ
Tuapse Туапсе
Armavir Армавир
Stavropol Ставрополь
Blagodamy Благодарный
Maykop Labinsk Майкоп Лабинск
Nevinnomyssk Невинномысск
Budyonnovsk
Буденновск Nefwkumrt о Нефтекумск
Pyatigorsk Пятигорск
Racha-Le'etTkhum-Kverr. ~ SvaneUPIanned National Pan
ШгЛок Моздок
Vladikavkaz Владикавказ .
о
Grozny Грозный
Fig. Location of the Caucasian nature reserves/ 1 — Utrish, 2 — Kavkazskiy, 3 — Severo-Osetinskiy, 4 — Erzi.
Elix et Hale is distinguished from Parmelina by chemistry (atranorin in medulla) and K+ yellow and C- reactions of the medulla.
In the review, the most important characters for determination of Par-melina species are presented. The main synonyms for every species are
given.
Parmelina carporrhizans (Taylor) Hale, 1974, Phytologia, 28(5): 482. = Parmelia carporrhizans Taylor, 1847, in Hook., London J. Bot. 6: 163. = Parmelina quercina (Willd.) Halle var. carporrhizans (Taylor) V. Wirth, 1994, Stuttgarter Beitr. Naturk., A, 517: 62.
Upper surface of thallus light grey, smooth, maculate, apothecia common, rhizinate on underside, usually numerous at the centre of thallus.
Well-developed ascospores ellipsoid, mostly c. 10 ^m or more long, (7.0)9.0-11.7(12.8) x (5)5.1-5.8(7) ^m, l/w = (1.56)1.65-2.0(2.1). Co-nidiomata black, immersed pycnidia, frequently present.
Pycnoconidia always acicular (5.8)6.7-10.0(11.0) x 1 ^m.
Contains atranorin in the cortex (K+ yellow); lecanoric acid in the medulla (C+ and KC+ rose-red).
In the Russian Caucasus, P. carporrhizans was found mostly in broad-leaved or in coniferous-broadleaved forests. It grows on the trunks and twigs of Abies nordmanniana, Acer trautvetteri, Betula sp., Carpinus orientalis, C. betulus, Castanea sativa, Fagus orientalis, Fraxinus excelsior, Pinus sp. and Quercus spp.
Distribution of Parmelina carporrhizans in the world follows the same distribution pattern as P. quercina, but restricted of regions with sub- or Mediterranean climates (Thell, 2011).
Similar species P. carporrhizans and P. quercina are extremely variable. P. carporrhizans is most readily recognized by maculate («frosted") upper surface and presence of dense rhizines on the underside of the apo-thecia, and typical P. quercina is without both macules on upper surface and rhizines under the apothecia, and also often somewhat rugose in the centrum of thallus.
Specimens examined. Russia, KrasnodarTerritory, Western Caucasus: Mt. Malyi Ahun, broadleaved forest, on fallen twigs Carpinus betulus, 43°32'09"N, 39°51'09"E, alt. 350 m, 12.10.2008 (LE); North-Western-Transcaucasia: Kavkazs-kiy Nature Reserve, Achipse River valley, Rudovaya, southern slope, Fagus orienata-lis-Carpinus betulus forest, on Carpinus betulus twig, 43°44'24.5"N, 40°13'34.3"E, alt. 800 m, 13.07.2013 (LE); ibid., Achipse River valley, between Rudovaya and Turovaya, southern slope, Fagus orienatalis forest with Abies nordmanniana and Castanea sativa, on bark of Castanea sativa, 43°44'46.2"N, 40°13'15.0"E, 1000 m, 11.07.2013; ibid., Achipse River valley, Asmanovy balagany, Carpinus betulus-Abies nordmanniana forest, on twig of Abies nordmanniana, 43°45'56"N, 40°11'34"E, alt.
1500 m, 14.07.2013; ibid., Utrish Nature Reserve, south of Vodopadnaya Schel', in juniper forest, on bark and twig of Carpinus orientalis, 44°44'43.1"N, 37°24'39.1"E, alt. 85 m, 14.09.2016; ibid., Schel' Savina, secondary Carpinus orientalis-forest with Quercus sp., on Quercus twig, 44°47'27.1"N, 37°25'27.8"E, alt. 145 m, 27.06.2014; ibid., Schel' Savina, secondary Carpinus orientalis-forest, on twig of Carpinus orientalis, 44°47'16.3"N, 37°24'59.0"E, alt. 195 m, 27.06.2014; ibid., southern slope of Mt. Lysaya, pistacia-juniper forest, on Quercus sp., 44°42'37.7"N, 37°28'00.7"E, alt. 80-90 m, 23.09.2014; ibid., Schel' Gorchichnaya, Carpinus orientalis-forest with Quercus sp., on Carpinus orientalis, 44°46'49.2"N, 37°27'39.1"E, alt. 250 m, 19.06.2015; ibid., broadleaved forest on the nothern slope of Mt. Shakhan, on oak twig, 44°46'26.9"N, 37°28'22.6"E, alt. 275 m, 19.06.2015; ibid., Schel' Mokraya, oak-pine forest, 44°42'30.2"N, 37°31'06.2"E, alt. 350 m, 10.09.2015; ibid., the southern west rocky slope of Mt. Lysaya, on Fraxinus excelsior, 44°42'55.2"N, 37°27'59.6"E, alt. 150-160 m, 11.09.2015. Republic of Adygeya, Western Caucasus: Kavka-zskiy Nature Reserve, Lagonaki Plateau, southeast facing slope with solitary fir trees and juniper shrubs among limestone boulders, on Salix sp., 43°56'02.00"N, 39°54'57.90"E, alt. 1870 m, 16.09.2010; ibid., Kamennoe More Ridge, virgin conif-erous-broadleaved forest on limestone bedrock and outcrops, on Abies nordmanni-ana, 44°04'40.9"N, 40°00'41.6"E, alt. 1800 m, 30.06.2013; ibid., Kamennoe More Ridge, virgin coniferous-broad-leaved forest on limestone bedrock and outcrops, on Sorbus sp., 44°04'45.7"N, 40°00'45.6"E, alt. 1780 m, 15.07.2011; ibid., Kamennoe More Ridge, virgin coniferous-broadleaved forest, on Acer sp., 44°04'18.0"N, 40°00'44.9"E, alt. 1800 m, 12.07.2011; ibid., Sukhoj Kurdzhips, pine-birch forest on western facing steep slope, on Betula sp., 44°03'23.3"N, 40°01'00.0"E, alt. 1800-1820 m, 04.07.2011; ibid., upper course of Kurdzhips River, pine forest with limestone outcrops, on Sorbus sp., 44°03'40.6"N, 40°00'14.5"E, alt. 1700-1750 m, 26.06.2013; ibid., pine forest on western facing slope, limestone cliff, canyon, on Salix sp., 44°03'54.1"N, 40°00'00.3"E, alt. 1650-1700 m, 27.06.2013; ibid., virgin coniferous-broadleaved forest with limestone outcrops, on Betula sp., 44°04'07.9"N, 40°00'05.8"E, alt. 1600-1650 m, 28.06.2013; ibid., Guzeripl, the Belaya River basin, virgin coniferous-broadleaved forest, on twigs of Acer trautvetteri and Fagus orientalis, 43°59'12"N, 40°08'29"E, alt. 920-960 m, 07.06.2016; ibid., Guzeripl, the Belaya River basin, timberline, on bark of Betula sp., 43°55'35.4"N, 40°09'05.8"E, alt. 1810-1920 m, 11.06.2016 (LE); ibid., Guzeripl, the Belaya River basin, virgin conif-erous-broadleaved forest, on twigs of Acer trautvetteri, 43°56'10"N, 40°08'53"E, alt. 1730 m, 12.06.2016 (LE); ibid., Guzeripl, the Belaya River basin, virgin coniferous-broadleaved forest, on bark of Abies nordmanniana, , 43°57'53"N, 40°07'50"E, alt. 1465 m, 13.06.2016 (LE). Republic of North Ossetia — Alania, Central Caucasus: Severo-Osetinskyi Nature Reserve, Shubi, broadleaved forest with Pinus sp., on fallen twig, 42°55'17.1"N, 44°12'09.5"E, alt. 1290 m, 26.06.2016 (LE).
Parmelina pastillifera (Harm.) Hale, 1976, Smithsonian Contr. Bot. 33: 39. = Parmelia scortea (Ach.) Ach. var. pastillifera Harm. 1910 [1909], Lich. Fr. 4: 558. = Parmelia tiliacea (Hoffm.) Ach. var.pastillifera (Harm.) Grummann, 1963, Cat. Lich. Germ. (Stuttgart): 21. = Parmelia pastillifera (Harm.) R. Schub. et Klem. 1966, Nova Hedwigia, 1: 58.
Upper surface of thallus smooth and bluish, isidia abundant, mostly blackish, apically flattened «button-like», generally distributed across the surface of the thallus, leaving indistinct scars when detached (Clerc, Truong, 2008). The upper surface of thallus of the examined Caucasian specimens with small (10-70 цт) whitish macules.
All specimens examined lacked apothecia.
Conidiomata black, immersed pycnidia, very rarely formed, not observed in the Caucasian specimens.
Contains atranorin in the cortex (K+ yellow); lecanoric acid in the medulla (C+ and KC+ rose-red).
In the Russian Caucasus, P. pastillifera was found mostly in broadleaved and coniferous-broadleaved forests, on the trunks and twigs of Abies nordmanniana, Acer trautvetteri, Betula sp., Carpinus betulus, C. orientalis, Fagus orientalis, Fraxinus excelsior, Juniperus excelsa, Prunus sp., Quercus spp. and Tilia sp.
Temperate Western, Central and Southern Europe to Ural Mts., Caucasus, with oceanic tendencies (Thell, 2011).
From the similar species P. tiliacea differs by apical flattened, black isidia.
Specimens examined. Russia, Republic of Ingushetia, Eastern Caucasus:
Erzi Nature Reserve, mixed forests, on trunks and twigs of Prunus sp., Tilia sp., Betula sp., 42°49'31.8"N, 44°54'01.4"E, alt. 1530-1570 m, 05.07.2016. Krasnodar Territory, North-Western-Transcaucasia: Utrish Nature Reserve, Schel' Savi-na, broadleaved forest, on Juniperus excelsa, Quercus sp. and Carpinus orientalis, 44°46'57.5"N, 37°25'06.3"E, alt. 165 m, 24.06.2014; ibid., between Schel' Savina and Schel' Zyubina, broadleaved forest, Fraxinus excelsior, Quercus sp. and Carpinus orientalis, 44°46'29.4"N, 37°25'10.1"E, alt. 375 m, 29.06.2014; ibid., Mt. Ly-saya, broadleaved forest, on Juniperus excelsa, Quercus sp. and Pistacia mutica, alt. 330-335 m, 44°42'53.7"N, 37°28'10.9"E, 21.09.2014; ibid., Kazennyy Bugor, broadleaved forest, on Carpinus betulus, Fraxinus excelsior, Quercus sp. and Tilia sp., on sandstone, alt. 440 m, 44°43'50.0"N, 37°28'08.5"E, 24.09.2014; ibid., broadleaved forest, on Carpinus betulus and Fagus orientalis, on trunks of Quercus sp., Fraxi-nus excelsior and Tilia sp., alt. 340-360 m, 44°45'53.9"N, 37°29'17.1"E, 27.06.2015; oak forest with outcrops, on Quercus sp., Tilia sp. and Fraxinus excelsior, sandstone, 44°43'39.6"N, 37°29'17.6"E, alt. 190-200 m, 09.09.2015. Republic of Adygeya, Western Caucasus: Kavkazskiy Nature Reserve, Guzeripl, the Belaya River basin, virgin coniferous-broadleaved forest, on twigs of Acer trautvetteri and Fagus orientalis, 43°59'12"N, 40°08'29"E, alt. 920-960 m, 07.06.2016 (LE); ibid., the Belaya River basin, virgin coniferous-broadleaved forest, on twigs of Abies nordmanniana and Fraxinus sp., 43°57'53"N, 40°07'50"E, alt. 1465 m, 14.06.2016; ibid., virgin co-niferous-broadleaved forest, on twigs of Carpinus orientalis, 43°56'10"N, 40°08'53"E, alt. 1730 m, 12.06.2016; ibid., Lagonaki, virgin coniferous-broad-leaved forest, on twigs of Tilia sp., Fagus orientalis and Acer trautvetteri, 44°04'41"N, 40°00'51"E, alt. 1830 m, 16.06.2016. Republic of North Ossetia — Alania, Central Cauca-
sus: Severo-Osetinskiy Nature Reserve, Shubi, broadleaved forest with Pinus sp., on bark of Fraxinus sp., 42°54'05.2"N, 44°11'06.2"E, alt. 1615 m, 21.06.2016 (LE); ibid., Shubi, broadleaved forest, on Fagus orientalis, 42°57'05.1"N, 44°15'56.5"E, alt. 1450 m, 23.06.2016; ibid., Shubi, broadleaved forest with Pinus sp., on fallen twig, 42°55'17.1"N, 44°12'09.5"E, alt. 1290 m, 26.06.2016 (LE).
Parmelina quercina (Willd.) Hale, 1974, Phytologia, 28(5): 483. = Lichen quercinus Willd. 1787, Fl. Berol. Prodr.: 353. = Parmelia quercina (Willd.) Vain. 1899, Term. Fuz. 22: 279.
Upper surface of thallus light mineral grey, often rugose in the centre, without macules, partly pruinose, apothecia numerous, especially in thallus centre. In the Caucasian specimens rhizinate apothecia were not observed.
Well-developed ascospores wide, short ellipsoid, nearly round, mainly less than 10 ^m long, (6.0)7.4-7.9(10.0) x (5.0)6.0-6.2(7.0) ^m, l/w = (1.15)1.2-1.34(1.4).
Conidiomata black, immersed pycnidia, frequently formed. Pycnoco-nidia mostly short bacilliform (4.5)5.0(6.0) x (1.0)1.5-1.8(2.6) ^m, very rarely short acicular, less than 8 ^m long.
Contains atranorin in the cortex (K+ yellow); lecanoric acid in the medulla (C+ and KC+ rose-red).
In the Russian Caucasus, P. quercina is found as an epiphyte in deciduous broadleaved forests, less often in coniferous-broadleaved forests, on trunks and twigs of Abies nordmanniana, Alnus sp., Betula sp., Carpinus orientalis, Fagus orientalis, Fraxinus excelsior, Pistacia mutica, Quercus spp. and Tilia sp.
Widely distributed in the Central Europe and the Mediterranean; the records of P. quercina s. str. in North America are not confirmed by recent research (Nelson et al., 2012; Esslinger, 2016).
For differences from a similar species in the Caucasus see comments to P. carporrhizans. In the Southern Europe and Mediterranean regions the, closest to quercina-group, obligate saxicolous P. atricha (Nyl.) P. Clerc is characterized by non-pruinose thallus without macules on the upper cortex, and the presence in the centrum of narrow, overlapping secondary panniform lobules, and a black undersurface with thin and long, dense rhizines (Clerc, Truong, 2008).
Specimens examined. Russia, Krasnodar Territory, North-Western-Transcaucasia: Kavkazskiy Nature Reserve, Shakhe River, floodplain, deciduous forest, on bark of Alnus sp., 43°53'02.5"N, 39°50'12.5"E, alt. 410 m, 05.07.2014; Utrish Nature Reserve, Schel' Atmacheva, broadleaved forest, on Quercus sp., Tilia sp. and Fraxinus excelsior, 44°46'02.2"N, 37°26'26.4"E, alt. 400 m, 26.06.2014; ibid., Schel' Savina, broadleaved forest, on Quercus sp. and Carpinus orientalis, 44°47'27.1"N, 37°25'27.8"E, alt. 145 m, 27.06.2014; ibid., broadleaved forest near Schel' Savi-
na, on Quercus sp. and Carpinus orientalis, 44°47'16.3"N, 37°24'59"E, alt. 195 m, 27.06.2014; ibid., Mt. Medved', broadleaved forest, on Juniperus excelsa, Quercus sp. and Fraxinus excelsior, 44°43'53.6"N, 37°26'42.8"E, alt. 370-380 m, 19.09.2014; ibid., Mt. Lysaya, pistacia-juniper forest, on Juniperus excelsa and Pistacia mu-tica, 44°43'00.5"N, 37°28'16.8"E, alt. 300 m, 21.09.2014; ibid., Kazennyy Bugor, sparse juniper forest, on twigs and trunks of oak, 44°43'40.6"N, 37°28'27.8"E, alt. 290-300 m, 24.09.2014; ibid., Mt. Shakhanchik, southern slope, on twig of Quercus sp., 44°45'27,2"N, 37°28'19,3"E, alt. 390-400 m, 23.06.2015 (LE); ibid., Schel' Shtankivskaya, southern slope, on Carpinus orientalis, 44°46'45.1"N, 37°32'30.8"E, alt. 315 m, 24.06.2015; ibid., Shosseynyy Bugor, rocky oak forest, on Carpinus orientalis, 44°43'39.6"N, 37°29'17.6"E, alt. 190-200 m, 09.09.2015; ibid., Schel' Mokraya, broadleaved forest, on Carpinus orientalis, 44°42'31.5"N, 37°31'26"E, alt. 145 m, 10.09.2015; ibid., southern slope near the Schel' Vodopadnaya, pistacia-juniper forest, on Quercus sp. and Pistacia mutica, 44°43'16.0"N, 37°29'24.7"E, alt. 200-240 m, 13.09.2015; ibid., tectonic fault, pistacia-oak forest, on Quercus sp., 44°45'22.9"N, 37°23'56.7"E, alt. 120 m, 07.09.2016; ibid., southern slope near the Schel' Vodopadnaya, juniper-pistacia forest, on bark of Quercus sp., 44°45'06.2"N, 37°24'23.6"E, alt. 220-230 m, 13.09.2016; ibid., south of Vodopadnaya Schel', in juniper forest, on Quercus sp., 44°44'42.6"N, 37°24'3.7"E, alt. 40-50 m, 14.09.2016; ibid., south of Vodopadnaya Schel', in juniper forest, on Pistacia mutica, Carpinus orientalis, 44°44'43.1"N, 37°24'39.1"E, alt. 85 m, 14.09.2016; ibid., range Navagir, pine-oak forest with limestone outcrops, on Quercus sp., 44°45'38.8"N, 37°25'19.2"E, alt. 285 m, 15.09.2016; ibid., Schel' Savina, middle part, broadleaved forest, on Quercus pubescens Willd., 44°46'57.5"N, 37°25'06.3"E, alt. 165 m, 24.06.2014. Republic of Adygeya, Western Caucasus: Kavkazskiy Nature Reserve, Guzeripl, the Belaya River basin, virgin coniferous-broadleaved forest, on bark of Abies nordmanniana and Fraxinus sp., 43°57'53"N, 40°07'50"E, alt. 1465 m, 14.06.2016; ibid., coniferous-broadleaved forest, on bark of Tilia sp., 44°00'02"N, 40°08'38"E, alt. 710-740 m, 15.06.2016; ibid., open mixed forest near timberline, north slope of the Mt. Abago on bark of Betula sp., 43°55'35.4"N, 40°09'05.8"E, alt. 1810-1920 m, 12.06.2016.
Parmelina tiliacea (Hoffm.) Hale, 1974, Phytologia, 28(5): 481. = Lichen tiliaceus Hoffm. 1784, Enum. Lich.: 96. = Parmelia tiliacea (Hoffm.) Ach. 1803, Methodus: 215.
= Lichen scorteus Ach. 1799 [1798], Lich. Suec. Prodr.: 119. = Parmelia scortea (Ach.) Ach. 1803, Methodus: 215.
Isidia pale, brownish, with blackened tips, elongated, subcylindrical, grainiform, usually numerous in the centre of thallus, leaving very distinct scars when detatched (Clerc, Truong, 2008). Upper surface pale grey, partly pruinose. All specimens lacked apothecia. Conidiomata black, immersed pycnidia, very rarely formed (absent in Caucasian specimens).
Contains atranorin in the cortex (K+ yellow); lecanoric acid in the medulla (C+ and KC+ rose-red).
Being the most common species in the Russian Caucasus, P. tiliacea is found as an epiphyte in deciduous broadleaved forests, less often in co-
niferous-broadleaved forests, on trunks and twigs of Abies nordmanniana, Alnus sp., Betula sp., Carpinus betulus, C. orientalis, Fagus orientalis, Fraxinus excelsior, Juniperus excelsa, Pistacia mutica, Prunus sp., Quercus spp. and Tilia sp. Among the Caucasian Parmelina species it is the only sandstone inhabitant.
Common in temperate and subtropical areas of the Central and Southern Europe with continental tendencies, extending to Macaronesia, North Africa and eastwards to Asia (Nùnez-Zapata et al., 2015).
P. cryptotiliacea A. Crespo et Nùnez-Zapata is a cryptic taxon, morphologically similar to P. tiliacea but with a different genetic composition (ITS, mtLSU and EFA), and restricted to the central part of the Iberian Peninsula (Nùnez-Zapata et al., 2011; Nùnez-Zapata, 2013). The fertile specimens of P. cryptotiliacea are differentiated by narrower ascospores (3-5 ^m wide vs 5-7 ^m in P. tiliacea) and the thinner walls of the ex-ciple cells (Nùnez-Zapata et al., 2011). In the absence of apothecia, the comparison of the ITS sequences is the only means to distinguish this cryptic species. P. cryptotiliacea has not been found yet in the Russian part of the Caucasus.
Specimens examined: Russia, Caucasus, Republic of Ingushetia, Eastern Caucasus: Erzi Nature Reserve, broadleaved forest, on Prunus sp., Tilia sp. and Betula sp., 42°49'31.8"N, 44°54'01.4"E, alt. 1530-1570 m, 05.07.2016; Krasnodar Territory, North-Western-Transcaucasia: Utrish Nature Reserve, Schel' Savi-na, broadleaved forest, on Carpinus betulus, Juniperus excelsa and Quercus sp., 44°46'57.5"N, 37°25'06.3"E, alt. 165 m, 24.06.2014; ibid., Schel' Savina, broadleaved forest, on Carpinus orientalis and Quercus sp., 44°46'51.5"N, 37°24'51.7"E, alt. 245 m, 24.06.2014; ibid., Schel' Savina, broadleaved forest, on Carpinus betulus, Juniperus excelsa and Quercus sp., 44°47'23.8"N, 37°25'15.8"E, alt. 180 m, 25.06.2014; ibid., Schel' Zyubina, northern slope, broadleaved forest, on Carpinus betulus, Tilia sp. and Quercus sp., 44°46'24.7"N, 37°25'44.9"E, alt. 320-330 m, 25.06.2014; ibid., near Mt. Medved', broadleaved forest with Juniperus spp., on Juniperus excelsa, 44°43'05"N, 37°26'36,9"E, alt. 20-25 m, 18.09.2014 (LE); ibid., Schel' Gorchichnaya, broadleaved forest, on Fagus orientalis, 44°47'13"N, 37°27'32,4"E, alt. 90 m, 19.06.2015 (LE); ibid., Schel' Shtankivskaya, southern slope, on Carpinus orientalis, 44°46'45.1"N, 37°32'30.8"E, alt. 315 m, 24.06.2015; ibid., Shosseynyy Bugor, rocky oak forest, on Quercus sp., 44°43'39.6"N, 37°29'17.6"E, alt. 190200 m, 09.09.2015; ibid., Schel' Mokraya, on Carpinus orientalis, 44°42'31,5"N, 37°31'26,0"E, alt. 145 m, 10.09.2015; ibid., Mt. Medved', broadleaved forest with Tilia spp., on Juniperus excelsa, 44°43'47.7"N, 37°26'52,4"E, alt. 275 m, 19.09.2014; ibid., southern slope near the Schel' Vodopadnaya, pistacia-juniper forest, on Quercus sp. and Pistacia mutica, 44°43'16.0"N, 37°29'24.7"E, alt. 200-240 m, 13.09.2015; ibid., Schel' Savina, middle part, broadleaved forest, on Quercus pubescens Willd., 44°46'57.5"N, 37°25'06.3"E, alt. 165 m, 24.06.2014; ibid., between Lobanova Schel' and Navagirskaya Schel', juniper-pistacia forest, on Quercus sp. and Pistacia mutica, 44°43'16.0"N, 37°29'24.7"E, alt. 200-240 m, 13.09.2015; ibid., tectonic fault, pista-
cia-oak forest, on Quercus sp.; 44°45'22.9"N, 37°23'56.7"E, alt. 120 m, 07.09.2016; ibid., southern slope near the Schel' Vodopadnaya, juniper-pistachia forest, on bark of Quercus sp., 44°45'06.2"N, 37°24' 23.6"E, alt. 220-230 m, 13.09.2016; ibid., south of Vodopadnaya Schel', in juniper forest, on Quercus sp., 44°44'42.6"N, 37°24'3.7"E, alt. 40-50 m, 14.09.2016; ibid., south of Vodopadnaya Schel', in juniper forest, on Carpinus orientalis, 44°44'43.1"N, 37°24'39.1"E, alt. 85 m, 14.09.2016; ibid., range Navagir, pine-oak forest with limestone outcrops, on Quercus sp., 44°45'38.8"N, 37°25'19.2"E, alt. 285 m, 15.09.2016.
Key to the species of the genus Parmelina from the Russian Caucasus
1. Thallus without isidia, apothecia usually numerous in centre of thallus; mostly corticolous ........................................................................................................... 2.
— Thallus with isidia, apothecia very rare; corticolous and saxicolous .................. 3.
2. Upper surface of thallus smooth, maculate, apothecia common, rhizinate on underside. Well-developed ascospores ellipsoid, mostly c. 10 ^m and more long, (7.0)10.0-10.3(11.7) x (5.0)5.1-5.8(7), l/w = (1.5)1.7-2.0(2.1). Pycnoconidia always acicular (5.8)6.7-10.0(11.0) x 1 ^m, often more than 8 ^m long .................
......................................................................................................P. carporrhizans.
— Upper surface of thallus often rugose in the centrum, without macules, partly pru-inose, apothecia common without rhizines. Well-developed ascospores widely short ellipsoid, nearly round, mainly less than 10 ^m long, (6.0)7.4-7.9(10.0) x (5.0)6.0-6.2(7.0) ^m, l/w = (1.15)1.26-1.4(1.6). Pycnoconidia mostly short ba-cilliform (4.5)5.0(6.0) x (1.0)1.5-1.8(2.6) ^m, very rarely short acicular, less than 8 ^m long.....................................................................................P. quercina.
3. Upper surface of thallus greyish. Isidia pale, brownish, with blackened at tips,
elongated, subcylindrical to clavate, usually numerous in the centre of thallus .....
................................................................................................................ P. tiliacea.
— Upper surface of thallus bluish. Isidia mostly blackish, apically flattened «buttonlike», generally distributed across the surface of the thallus............P. pastillifera.
Discussion
The species of Parmelina are the most common and an important component of mountain forests in the Caucasus. In this study we tried to evaluate the diversity and the reliablity of morphological criteria of the treated Parmelina species. In the key we use a combination of morphological and anatomical characters to separate the isidiate (tiliacea-pas-tillifera) and fertile (carporrhizans-quercina) species. The presence of rhizines on the underside of the apothecia has been found to be a weak diagnostic characteristic (Clerc, Truong, 2008). P. quercina has a non-maculated upper cortex and short rhizines, whereas P. carporrhizans has a maculated upper cortex and longer rhizines (Clerc, Truong, 2008). Besides abovementioned characters we use as diagnostic the ridges on upper surface; size and shape of pycnoconidia; size of well-developed
Comparison of diagnostic characteristics of the Caucasian and European (Clerc, Truong, 2008; Nunez-Zapata, 2013; Thell,
2011) specimens of Parmelina carporrhizans and P. quercina
Characteristics Parmelina carporrhizans Parmelina quercina
Europe Russian Caucasus Europe Russian Caucasus
Upper surface:
macules (diam., |.im) usually 10-100 none none
pruina + rare + +
ridges at centrum none none sometimes wrinkles always
Lower surface:
rhizines ( length, mm) 0.8-1.4 1-2 0.5-1.0 0.5-1.0
Apothecia:
rhizinate always always rare none
Well-developed ascospores (repeatable values):
length (jim) (8)9-10(11) (7.0)9.0-11.7(12.8) (6)8-9(11) (6.0)7.4-7.9(10.0)
width (jim) 5-7 4(5)5.1-5.8(7) (4)5-6(7) (5.0)6.0-6.2(7.0)
length/width ratio ? (1.56)1.65-2.0(2.1) ? (1.15)1.26-1.4(1.6)
Pycnoconidia
shape acicular, bacilliform always acicular bacilliform, slightly dumbbell bacilliform, rarely short acicular
length (jim) 5-7 (5.8)6.7-10.0(11.0) 5-7 (4.5)5.0(6.0)
width (jim) 1 1 1 (1.0)1.5—(1.8)2.6
ui
ascospores and their length/width ratio (Table). In our opinion the above-mentioned criteria may be used as the most characteristic not only for the species in question but for the other fertile species of the genus Parmelina.
Acknowledgements
Many thanks are due to Gennadii Urbanavichus for the collaboration in expeditions and for the herbarium material used in this study. I am sincerely indebted to Prof. Mark Seaward and Irina Sokolova for their remarks, correction of English and recommendations. The study was supported by the Russian Foundation for Basic Research (grant 15-29-02396) and carried out within the framework of the current institutional research project (№ 01201255601) of the Komarov Botanical Institute RAS. The research was done using equipment of the Core Facility Centre «Cell and Molecular Technologies in Plant Science» at the Komarov Botanical Institute RAS (St. Petersburg, Russia).
References
Alors D., Grande F. D., Cubas P., Crespo A., Schmitt I., Molina M. C., Divakar P. K. 2017. Panmixia and dispersal from the Mediterranean basin to Macaronesian Islands of a macrolichen species. Sci. Rep. 7: 40879. doi:10.1038/srep40879 Alors D., Dal Grande F., Schmitt I., Kraichak E., Lumbsch H. T., Crespo A., Divakar P. K. 2014. Characterization of fungus-specific microsatellite markers in the lichen-forming fungus Parmelina carporrhizans (Parmeliaceae). Applications in Plant Sciences. 2(12): 1400081. doi:10.3732/apps.1400081 Argüello A., Crespo A., Hawksworth D. L. 2007a. Neo- and epitypifications to fix the application of the names Parmelina carporrhizans and P. quercina. Lichenologist. 39(4): 397-399.
Argüello A., DelPrado R., Cubas P., Crespo A. 2007b. Parmelina quercina (Parmeliaceae Lecanorales) includes four phylogenetically supported morphospecies. Biol. J. Linn. Soc. 91: 455-467. Arup U., Ekman S., Lindblom L., Mattsson J.-E. 1993. High performance thin layer chromatography (HPTLC), an improved technique for screening lichen substances. Lichenologist. 25(1): 61-71. Clerc P., Truong C. 2008. The non-sorediate and non-isidiate Parmelina species (li-chenized ascomycetes, Parmeliaceae) in Switzerland — Parmelina atricha (Nyl.) P. Clerc reinstated in the European lichen flora. Sauteria. 15: 175-194. Crespo A., Ferencova Z., Perez-Ortega S., Elix J. A., Divacar P. K. 2010. Austroparmelia, a new Australasian lineage in parmelioid lichens (Parmeliaceae, Ascomycota). Syst. Biodivers. 8: 209-221. Divakar P. K., Lumbsch H. T., Ferencova Z., Del Prado R., Crespo A. 2010. Remoto-trachyna, a newly recognized tropical lineage of lichens in the Hypotrachyna clade (Parmeliaceae, Ascomycota), originated in the Indian subcontinent. Amer. J. Bot. 97: 579-590.
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Elix J. A., Hale M. E. 1987. Canomaculina, Myelohroa, Parmelinella, Parmelinopsis and Parmotrenopsis, five new genera in the Parmeliaceae (lichenized Ascomyco-tina). Mycotaxon. 29: 233-244.
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Nelson P. R., Kepler R., Walton J., Fankhauser J., Nelson L., Song W. L. 2012. Parmelina yalungana resurrected and reported from Alaska, China and Russia. Bryologist. 115(4): 557-565.
Núñez-Zapata J. 2013. Variabilidad genética, especies crípticas y filogenia moleculae en hongos liquenizados del género Parmelina (Parmeliaceae, Ascomycota). Tes. Doct. Madrid: 194 p.
Núñez-Zapata J., Cubas P., Hawksworth D. L., Crespo A. 2015. Biogeography and genetic structure in populations of a widespread lichen (Parmelina tiliacea, Par-meliaceae, Ascomycota). PLoS ONE. 10(5): e0126981. doi:10.1371/journal. pone.0126981
Núñez-Zapata J., Divakar P. K., Del-Prado R., Cubas P., Hawksworth D. L., Crespo A. 2011. Conundrums in species concepts: the discovery of a new cryptic species segregated from Parmelina tiliacea (Ascomycota: Parmeliaceae). Lichenologist. 43(6): 603-616.
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Литература
Alors D., Grande F. D., Cubas P., Crespo A., Schmitt I., Molina M. C., Divakar P. K. 2017. Panmixia and dispersal from the Mediterranean basin to Macaronesian Islands of a macrolichen species. Sci. Rep. 7: 40879. doi:10.1038/srep40879
Alors D., Dal Grande F., Schmitt I., Kraichak E., Lumbsch H. T., Crespo A., Divakar P. K. 2014. Characterization of fungus-specific microsatellite markers in the
lichen-forming fungus Parmelina carporrhizans (Parmeliaceae). Applications in Plant Sciences. 2(12): 1400081. doi:10.3732/apps.1400081
Argüello A., Crespo A., Hawksworth D. L. 2007a. Neo- and epitypifications to fix the application of the names Parmelina carporrhizans and P. quercina. Lichenologist. 39(4): 397-399.
Argüello A., DelPrado R., Cubas P., Crespo A. 2007b. Parmelina quercina (Parmeli-aceae Lecanorales) includes four phylogenetically supported morphospecies. Biol. J. Linn. Soc. 91: 455-467.
Arup U., Ekman S., Lindblom L., Mattsson J.-E. 1993. High performance thin layer chromatography (HPTLC), an improved technique for screening lichen substances. Lichenologist. 25(1): 61-71.
Clerc P., Truong C. 2008. The non-sorediate and non-isidiate Parmelina species (li-chenized ascomycetes, Parmeliaceae) in Switzerland — Parmelina atricha (Nyl.) P. Clerc reinstated in the European lichen flora. Sauteria. 15: 175-194.
Crespo A., Ferencova Z., Perez-Ortega S., Elix J. A., Divacar P. K. 2010. Austroparmelia, a new Australasian lineage in parmelioid lichens (Parmeliaceae, Ascomycota). Syst. Biodivers. 8: 209-221.
Divakar P. K., Lumbsch H. T., Ferencova Z., Del Prado R., Crespo A. 2010. Remoto-trachyna, a newly recognized tropical lineage of lichens in the Hypotrachyna clade (Parmeliaceae, Ascomycota), originated in the Indian subcontinent. Amer. J. Bot. 97: 579-590.
Hale M. 1976. A monograph of the lichen genus Parmelina Hale (Parmeliaceae). Smithsonian Contr. Bot. 33: 1-60.
Elix J. A., Hale M. E. 1987. Canomaculina, Myelohroa, Parmelinella, Parmelinopsis and Parmotrenopsis, five new genera in the Parmeliaceae (lichenized Ascomyco-tina). Mycotaxon. 29: 233-244.
Esslinger T. L. 2016. A cumulative Checklist for the lichen-forming, lichenicolous and allied fungi of the continental United States and Canada, version 21. Opuscula Philolichenum. 15: 136-390.
[Menitskiy] Меницкий Ю. Л. 1991. Проект «Конспект флоры Кавказа». Карта районов флоры. Бот. журн. 76(11): 1513-1521.
Nelson P. R., Kepler R., Walton J., Fankhauser J., Nelson L., Song W. L. 2012. Parme-lina yalungana resurrected and reported from Alaska, China and Russia. Bryologist. 115(4): 557-565.
Núñez-Zapata J. 2013. Variabilidad genética, especies crípticas y filogenia moleculae en hongos liquenizados del género Parmelina (Parmeliaceae, Ascomycota). Tes. Doct. Madrid: 194 p.
Núñez-Zapata J., Cubas P., Hawksworth D. L., Crespo A. 2015. Biogeography and genetic structure in populations of a widespread lichen (Parmelina tiliacea, Parmeliaceae, Ascomycota). PLoS ONE. 10(5): e0126981. doi:10.1371/journal.pone.0126981
Núñez-Zapata J., Divakar P. K., Del-Prado R., Cubas P., Hawksworth D. L., Crespo A. 2011. Conundrums in species concepts: the discovery of a new cryptic species segregated from Parmelina tiliacea (Ascomycota: Parmeliaceae). Lichenologist. 43(6): 603-616.
[Rassadina] Рассадина К. А. 1971. Род Parmelia Ach. Определитель лишайников СССР. Вып. 1. Л.: 306-360.
Thell A. 2011. Parmelina Hale. Nordic lichen flora. Vol. 4: Parmeliaceae. Uppsala: 90-92.
[Urbanavichene, Urbanavichus] Урбанавичене И. Н., Урбанавичюс Г. П. 2014. К лихенофлоре долины реки Ачипсе (Юго-Западный Кавказ, Краснодарский край). Новости сист. низш. раст. 48: 315-326. [Urbanavichene, Urbanavichus] Урбанавичене И. Н., Урбанавичюс Г. П. 2016. К лихенофлоре долины реки Шахе (Краснодарский край, Западное Закавказье). Новости сист. низш. раст. 50: 243-256. Urbanavichus G., Urbanavichene I. 2014. An inventory of the lichen flora of Lagonaki
Highland (NW Caucasus, Russia). Herzogia. 27(2): 285-319. [Urbanavichus, Urbanavichene] Урбанавичюс Г. П., Урбанавичене И. Н. 2015. Материалы к лихенофлоре заповедника Утриш. Turczaninowia. 18: 86-95.
