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13Gymnocolea borealis (Anastrophyllaceae, Marchantiophyta) in Asia and Russia: morphology, ecology, distribution, and differentiation
A. D. Potemkin1, A. A. Vilnet2, E. I. Troeva3, K. A. Ermokhina4
'Komarov Botanical Institute of the Russian Academy of Sciences, St. Petersburg, Russia 2Polar-Alpine Botanical Garden-Institute of the Russian Academy of Sciences, Apatity,
Murmansk Region, Russia 3Institute for Biological Problems of Cryolithozone, Siberian Branch of the Russian Academy of Sciences, Yakutsk, Russia 4A. N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Moscow, Russia Corresponding author. A. D. Potemkin, Potemkin_alexey@binran.ru
Abstract. Gymnocolea borealis is reported for the first time for Asia from Russia based on the morphological and subsequent molecular-genetic comparison of rbcL cpDNA sequence of the specimen from the Gydansky Peninsula, West Siberian Arctic. An extended morphological description, generalizing the species characters throughout its range, and data on its variation, differentiation and ecology, and photomicrographs are provided. The occurrence of G. borealis growing as separate shoots among dense mire vegetation makes it easy to overlook. Presently known isolated records of G. borealis support its disjunctive circumpolar distribution.
Keywords: Gymnocolea, distribution, liverworts, hepatics, rbcL, West Siberian Arctic.
Gymnocolea borealis (Anastrophyllaceae, Marchantiophyta) в Азии и России: морфология, экология, распространение и отличия
А. Д. Потемкин1, А. А. Вильнет2, Е. И. Троева3, К. А. Ермохина4
'Ботанический институт им. В. Л. Комарова РАН, Санкт Петербург, Россия 2Полярно-альпийский ботанический сад им. Н. А. Аврорина Кольского научного центра РАН,
Апатиты, Мурманская область, Россия
3Институт биологических проблем криолитозоны СО РАН, Якутск, Россия 4Институт проблем экологии и эволюции им. А. Н. Северцова РАН, Москва, Россия Автор для переписки: А. Д. Потемкин, Potemkin_alexey@binran.ru
Резюме. Gymnocolea borealis впервые приводится для Азии из России на основании морфологического и последующего молекулярно-генетического сравнения последовательности rbcL cpDNA образца с Гыданского полуострова, Западно-Сибирской Арктики. Приведены расширенное морфологическое описание, учитывающее признаки вида на протяжении всего его ареала, подробное описание экологии, изменчивости и отличий, а также микрофотографии. Gymnocolea borealis легко пропустить при сборах в связи с произрастанием отдельными побегами среди густой болотной растительности. Известные в настоящее время указания вида предполагают его дизъюнктивное циркумполярное распространение.
Ключевые слова: Gymnocolea, печеночники, распространение, rbcL, Западно-Сибирская Арктика.
https://doi.org/1031111/nsnr/2021.55.2.487
487
Gymnocolea borealis (Frisvoll et Moen) R. M. Schust. is a rather recently described liverwort with most locations in Scandinavia (Frisvoll, Moen, 1980). It was described as a species of the subgenus Leiocolea Müll. Frib. of the genus Lophozia (Dumort.) Dumort. and transferred by Schuster (1986) to the genus Gymnocolea (Dumort.) Dumort. Its search by the first author in European Russia and the Arctic resulted in the discovery and description of G. fascinifera Potemkin (Potemkin, 1993). Despite the rather broad distribution of G. borealis in northern Scandinavia and its discovery in Greenland (Damsholt, 2013), it was not recorded for European Russia and the Russian Arctic until now. Its reports in GBIF from Khanty-Mansi Autonomous Area, West Siberia (Melechin et al., 2021a, b), are not correct. The goal of this paper is to report G. borealis for the first time for Asia from Russia based on morphological and molecular analysis, describe its morphology, ecology, and discuss distribution and differentiation.
Material and Methods
The Russian specimen of Gymnocolea borealis was gathered in the course of a vegetation plot description in the vicinity of Yambuto Lake, Gydansky (Gyda) Peninsula, Yamal-Nenets Autonomous Area, West Siberian Arctic. The collecting site is located 500 m from the north-western part of the lakeshore, 71°13'21.3"N, 79°17'38.9"E. The landform represents a cryogenic complex of flat mounds and bogs in the bottom of a former lake depression.
The study of the moss collections containing liverworts from the plot resulted in an unexpected discovery of a minute specimen of G. borealis, which identification was confirmed by a molecular study.
DNA was extracted from dried liverwort tissue with DNeasy Plant Mini Kit (Qia-gen, Germany). Amplification and sequencing of rbcL cpDNA were performed using primers given by Kress and Erickson (2007).
PCR was carried out in 20 |il volumes with the following amplification cycles: 3 min at 94 °C, 30 cycles (30 s 94 °C, 40 s 56 °C, 60 s 72 °C) and 2 min of final extension time at 72 °C. Amplified fragments were visualized on 1% agarose TAE gels by EthBr staining, purified using the QIAquick Gel Extraction Kit (Qiagen, Germany), and then used as a template in sequencing reactions with the ABI Prism Big-Dye Terminator Cycle Sequencing Ready Reaction Kit (Applied Biosystems, U.S.A.) following the standard protocol provided for 3100 Avant Genetic Analyzer (Applied Biosystems, USA).
The newly obtained rbcL sequence of G. borealis specimen from the Gydansky Peninsula was assembled and combined in a dataset with rbcL sequence data of three Gymnocolea specimens downloaded from GenBank in BioEdit 7.0.1 (Hall, 1999), including one sequence of G. borealis (JX305563, Sweden) and two of G. inflata (Huds.) Dumort. (KF852306, Norway, JX305549, United Kingdom). The sequence variability among samples and species was estimated as the value of p-distances in Mega 5.1 (Ta-mura et al, 2011).
Results
The nucleotide difference among both Gymnocolea borealis specimens from remote localities counts 0.6%, among G. inflata specimens — 0.4%, both species differ by more than 3% (Table 1).
Table 1
The value of^-distances among tested Gymnocolea specimens.
Specimens ^-distances, rbcL, %
1 2 3
1 Gymnocolea inflata Norway KF852306
2 Gymnocolea inflata UK JX305549 0.4
3 Gymnocolea borealis Sweden JX305563 3.3 3.3
4 Gymnocolea borealis Russia MZ032229 3.7 3.4 0.6
Thus, the level of sequence divergence in Gymnocolea borealis is within the frame of infraspecific variability in the genus Gymnocolea. The molecular results data confirm the morphological identification of the Russian G. borealis specimen. The new find of G. borealis from the Gydansky Peninsula expands our knowledge on the distribution of this species.
Description of Gymnocolea borealis based on plants from the Gydansky Peninsula with additional morphological characteristics [in square brackets] from previous treatments (Frisvoll, Moen, 1980; Damsholt, 2002, 2013) and examined Norwegian specimens is below.
Gymnocolea borealis (Frisvoll et Moen) R. M. Schust. 1986, Lindbergia 12: 7. = Lophozia borealis Frisvoll et Moen, 1980, Lindbergia 6: 138. (Plate I)
Plant 0.7-2 [3(5.5)] cm long and [0.3](0.7)1.2-1.7[2.5] mm wide, when wet lustrous golden-brown to yellowish-green and yellow-brownish green, [in mod. parvifolia occasionally olive brown], when shaded usually entirely green, without reddish pigmentation, simple or sometimes with terminal furcate branches [branching of Frullania-type, supporting leaf undivided or bilobed]. Stems almost terete to slightly and occasionally rather strongly flattened, (80)150-200 jm high and (100)130-225(325) ^m wide, (90)150-200 |im thick, (6-7)9-10(11) cells high, cortical cells becoming golden-brown with age and somewhat incrassate, 12-20(25) x 25-65(100) [12-17(20) x (30)50-80(90)] jim, with finely striolate papillose surface, punctate in cross sections. In cross section stem medulla homogenous, of larger cells with ± thickened walls and rounded cavities, usually with few cells ± mycorrhizal [illustrated by Frisvoll and Moen (1980: Fig. 2B) but not described]; cortical cells with mostly rounded cavities or ±
tangentially flattened. Rhizoids absent, few or ± abundant in separate shoot sectors, solitary occasionally from the postical leaf base. Flagella and stolons not seen. Leaves succubous, mostly very oblique inserted, ± decurrent dorsally, usually spreading at right angles to the stem, distant and either not overlapping or occasionally slightly so, variable, mostly bilobed, rare solitary 3(4)-lobed or entire, ca. [1.1] (1.05)1.1-1.2(1.35) as long as wide, (500)650-800 ^m long x (350)600-750 ^m wide [840 ^m long x 740 jm broad to 1230 jm long x 1060 jm broad]; smallest measurements of lowermost leaves and leaves of immature shoots; [margins usually repand and sometimes in part slightly crenulate]; lobes variable, rounded, blunt, or ± acute with apiculus of two subisodiametric cells; ventral lobes often longer and broader than dorsal lobes, with ventral leaf margin more convex than dorsal, which often less convex, ± straight and mostly ± concave near the base; lobes ± subequal in larger leaves; sinus acute, [occasionally ± reflexed and gibbous], v- or y-like, (0.25)0.35-0.45 the leaf length. Cells rounded-polygonal, with small acute, never bulging trigones and thin to moderately thickened walls. Marginal cells (13)20-28(30) jm measured along margins, median leaf cells (20)22-28(30) x 24-30(37) jm, increasing to 22-32 x (20)30-50 jm at leaf base; cell walls usually deeper pigmented than cell surface, yellow to ± brown in pigmented plants. Leaf surface usually ± remarkably striolate-papillose, with often weaker or distinct rounded papillae in the distal part of leaves. [Oil bodies few and relatively large, 1-5(6) in each lobe cell and (1)3-6(8) in each leaf base cell, finely granulose, subspherical to ovoid, ellipsoid or even reniform, from 4 x 4 jm to usually 6-8 x 8-10 jm, with single oil bodies up to 12 x 16 jm, often of unequal size in the same cell]. Underleaves usually minute and hardly discernible, mostly resembling fused (1)3(4)-stalked slime papillae of 1-4 cells each, rarely lanceolate, present throughout. Gemmae lacking. [Dioicous. Androecia intercalary, loosely spicate, of 3-4 pairs of 2-androus subtransversely inserted strongly concave to saccate at base male bracts, lacking marginal lobes or teeth. Gynoecia terminal, often with innovation below the perianth or from inside the perianth, with perianth forming a sheath at the base of the shoot. Innermost bracts smaller than outer involucral leaves, which are larger and more transversely inserted and orientated than lower sterile leaves. Female bracts very variable, large or small, strongly crispate, mostly 2-4 lobed. Perianth strongly exerted from female bracts, elongate-obovate to slightly pyriform, weakly 3-4 plicate in the upper part, abruptly contracted at apex, sporadically 2-stratose in the lower half, mouth plicate and not beaked, margin lobulated, lobules usually 2-3 cells wide at the base, terminated by (1)2-7-celled uniseriate end. Sporophyte unknown.]
Specimens examined. Norway: MR Rinndal. Kbl. 1421 II UTM NQ 0494, alt. 550 m., loc. Nord-marka, s for Skakleiva, s for Finnraa. Hab. Kilde, Scorpidium dom., 1 X 1968 Moen (H); ST. Rehne-bu. Kbl. 1520 IV UTM NQ 32,70. Loc. Heldalen. Hab. Sammen med. Campylium stellatum, 24 VII 1979, A. Moen 79510 (H). Russia: West Siberian Arctic, Gydansky Peninsula, vicinities of Yambuto Lake, 500 m from the north-western part of the lakeshore, 71°13'21.3"N, 79°17'38.9"E, the bottom of the former lake depression, in wet hollows of cotton grass-sedge bog between flat mounds, single
Plate I. Gymnocolea borealis (Troeva G1-138, LE). 1, 2 — shoot sectors; 3 — lobe; 4, 5 — cross sections of stem; 6 — basal leaf cells. Scale bars: 1, 2 — 750 |m; 3 —18 |m; 4, 5 — 30 |m; 6 — 19 |m.
shoots among Rhizomnium sp., 17 VII 2017, Troeva G1-138 (LE). GenBank accession number for rbcL cpDNA: MZ032229.
Illustrations. Schuster, 1969: Fig. 251: 14-18, as Gymnocolea inflata (illustrated specimen RMS 45791 attributed to G. borealis by Schuster, 1986: 6); Frisvoll, Moen, 1980: Figs. 1-4; Damsholt, 2002: Plate 53, reprinted in Damsholt, 2013: Plate 46.
Differentiation. Pigmented plants of Gymnocolea borealis are distinct in their golden brown lustrous color most characteristic of wet plants, papillose leaf, and stem surface, and more eutrophic than in G. inflata and G. fascinifera wet habitats. Sporadically occurring as admixture ± green or darker brown plants has similar distinctive leaf areolation with papillose surface and stem structure. Gymnocolea borealis may be confused with G. fascinifera because of solitary rhizoids originating from the posti-cal leaf base. However, the distinctions in the color of pigmented wet plants (golden brown lustrous in G. borealis vs. ± scorched brown in G. fascinifera), mostly shallower sinus [0.25-0.35(0.45) vs. 0.33-0.5], narrower outer cortical cells [12-20(25) |im vs. (20)23-28(30) |im wide or when subisodiametric (28)30-34(38) |im wide], and ecological requirements (basi- and neutrophilous vs. acidophilous) are remarkable. Sporadically occurring as admixture ± green or darker brown plants are distinct in the sinus depth, width of cortical cells, and ecological requirements.
Distribution. Gymnocolea borealis is known from Norway, Sweden, Finland (Damsholt, 2002), West Siberian Arctic, Russia (present record only), North, North-West, and West Greenland (Damsholt, 2013). Moreover, Grant and von Konrat (2020) provided data on the specimen from Baffin Island, Canada, identified by R. M. Schuster in 1991 with a question mark, and Damsholt (2013) cited specimen Holmen 61-398 from Alaska.
Earlier, Gymnocolea borealis was erroneously recorded from Russia based on a specimen from the Khanty-Mansi Autonomous Area — Yugra (Konstantinova, Lapshina, 2017). According to N. A. Konstantinova (e-mail to Potemkin from 11 I 2021), the material belongs to G. inflata. The record was excluded in a species list of the area (Konstantinova, Lapshina, 2017) but the erroneous identification was accidentally retained in the lists of associated species of Nardia japonica Steph. and Scapania ob-cordata (Berggr.) S. W. Arnell, given in the latter paper.
Ecology. In Scandinavia, Gymnocolea borealis grows in moderately to rich fens, in carpets to lawns, never in intermediate fens and on hummocks, and prefers rather dense vegetation. It associates with Aneurapinguis (L.) Dumort., Warnstorfia sarmentosa (Wahlenb.) Hedenas, Campylium stellatum Lange et C. E. O. Jensen, Scorpidium cossonii (Schimp.) Hedenas, Odontoschisma elongatum (Lindb.) A. Evans, Saccobasis polita (Nees) H. Buch, and Tritomaria scitula (Taylor) Jerg. preferably in rather dense vegetation, where it often occurs as single shoots (Frisvoll, Moen, 1980; Damsholt, 2002, 2013). All associated bryophyte species have a broad ecological amplitude and are mostly subneutrophyte-basiphytes or acidophyte-subneutrophytes (e.g., Warnstorfia sarmentosa), preferring wet habitats. Dierssen (2001) characterizes G. borealis
as hygrophyte, subneutrophyte, photophyte, occurring on peaty soils in Scheuchze-rio-Caricetea, especially Caricion atrofusco-saxatilis communities.
In the Gydansky Peninsula Gymnocolea borealis was collected at the bottom of a former lake depression, in wet hollows of cotton grass-sedge bog between flat mounds, as single shoots among Rhizomnium sp. with an admixture of Blepharostoma trichophyllum (L.) Dumort., Trilophozia quinquedentata (Huds.) Bakalin, Ptilidium ciliare (L.) Hampe, Riccardia latifrons (Lindb.) Lindb. subsp. arctica R. M. Schust. et Damsh., Spheno-lobus minutus (Schreb.) Berggr., and single shoots of Lophozia polaris (R. M. Schust.) R. M. Schust. et Damsh., Mesoptychia gillmanii (Austin) L. Soderstr. et Vana, and Or-thocaulis binsteadii (Kaal.) H. Buch. Associated mosses (det. by A. P. Dyachenko) are Aulacomnium turgidum (Wahlenb.) Schwagr., Bryum cryophilum Mártensson, Cincli-dium latifolium Lindb., C. subrotundum Lindb., Meesia triquetra (Jolycl.) Angstr., Po-lytrichastrum alpinum (Hedw.) G. L. Sm. var. fragile (Bryhn) D. G. Long, Scorpidium revolvens (Sw. ex anon.) Rubers, Warnstorfia sarmentosa (Wahlenb.) Hedenas.
According to data on vascular plants of this habitat, stagnant and excessive moisture conditions determine the species composition represented mainly by hygro- and mesohygrophilous plants: Carex aquatilis subsp. stans and C. chordorrhiza (25% of the cover value each) with Eriophorum russeolum as a sub-dominant (10%). Eriopho-rum polystachyon, C. bipartita, Saxifraga foliolosa, Pedicularis sudetica subsp. albola-biata, Cardamine pratensis, and Luzula wahlenbergii were scattered (1-3% each). The moss layer was dominated by Scorpidium revolvens (95%) with the participation of Cinclidium subrotundum, C. latifolium, Meesia triquetra, and Warnstorfia sarmentosa (3-5% each).
An analysis of the species lists above demonstrates the association of hygro- and mesohygrophilous plants with different pH requirements caused by moistening conditions. Together with species with a broad pH amplitude, the frequent occurrence of the basiphilous Cinclidium latifolium and several species, which prefer to grow in neutral to slightly basic conditions, is remarkable. They are the liverworts Blepharosto-ma trichophyllum, Lophozia polaris, Mesoptychia gillmanii, Trilophozia quinquedentata, mosses Scorpidium revolvens, Meesia triquetra, and Eriophorum polystachyon, Saxifraga cernua among vascular plants. A pH comparison with other locations is not possible by lack of data.
The discovery of Gymnocolea borealis in the Gydansky Peninsula is hard to explain from the phytogeographic point of view. Because of its common occurrence as a small admixture and its preference for dense vegetation, we presume its omission in northern European Russia resulted from the rare detailed bryological investigation of fens with dense vegetation. Frisvoll and Moen (1980: 141) stated that it is easily identifiable, both in the field and in the laboratory. Observation of alive or wet plants of G. borealis is desirable because of their characteristic lustrous golden color, resembling that of Cryptocolea imbricata R. M. Schust. This color becomes indiscernible in dry plants.
Acknowledgments
We are grateful to Jairo Patino and two anonymous reviewers for their careful reading, valuable comments, corrections, and improvements in the English of the first version of the manuscript. The help of James R. Shevock with the English in the final version of the manuscript is highly appreciated. The study of A. D. Potemkin was carried out within the framework of the institutional research project of the Komarov Botanical Institute of the Russian Academy of Sciences "Herbarium collections of BIN RAS (history, conservation, investigation and replenishment)" (АААА-А18-118022090078-2) and was supported by RFBR project 18-05-60093 Арктика. Research carried out by E. I. Troeva and K. A. Ermokhina was supported by RFBR grant 18-04-01010-A.
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