Notes on the lichen genus leptogium (collemataceae, ascomycota) in South Korea.

Leptogium (Ach.) Gray is distributed throughout South Korea; however, for nearly two decades no detailed taxonomic or revisionary research on this lichen genus has been conducted. This study examined the specimens deposited in the lichen herbarium at the Korean Lichen Research Institute, and samples were identified using descriptions recently published in the scientific literature. In this revisionary study, a total of fourteen species of Leptogium were documented, including new records of Leptogium delavayi Hue, Leptogium denticulatum Nyl., and Leptogium trichophoroides P. M. Jørg. & A. K. Wallace. Detailed descriptions of each species are given, including their morphological, anatomical, and chemical characteristics. A key to all Leptogium species known to occur in South Korea is also presented.

Leptogium (Ach.) Gray is a well-known lichen genus distributed throughout the tropical regions of the world. This genus is classified in the family Collemataceae, which was divided into seven sections [1] on the basis of habit and anatomy of the thallus, nature of the cortex, presence or absence of tomentum, and the nature of spores [2]. Among the seven sections, Sect. Mallotium (Ach.) Vain and Sect. Leptogium are known to occur in South Korea. The section Mallotium is distinguished by the presence of a tomentum on the surface of a well-developed and foliose thallus, while the section Leptogium lacks tomentum on either surface and has muriform spores [1].

The genus Leptogium is characterized by a foliose to subsquamulose thallus, which can be gelatinous, blue-grey to brown or blackish, adnate to loosely adnate, with isidia or lobules; flat to plicate, spreading to erect lobes; non-layered medulla with an outer cortex of isodiametric cells in a single layer; smooth, wrinkled or ridged, glabrous or non-glabrous surfaces; lower surface with simple rhizines, irregular holdfasts, and hairs; interwoven, or columnar paraplectenchymatous, medullary hyphae; presence of the cyanobacterial photobiont (Nostoc); lecanorine, laminal to marginal, sessile to short stalked apothecia; ascospores colorless, ovoid, ellipsoid or fusiform, septate, submuriform to muriform, acute, acuminate or obtuse; and laminal or marginal pycnidia with bacilliform, simple, colorless conidia [1, 3, 4, 5]. This genus comprises many species, which are widely distributed in tropical and temperate regions, with a few species distributed in Arctic and sub-Antarctic regions [4, 6, 7]. The genus Collema closely resembles the genus Leptogium in external appearance, but the former is distinguished by the absence of cortical layers on either side of the thallus [8, 9]. Furthermore, recent phylogenetic studies revealed that Collema and Leptogium are not monophyletic genera [10, 11].

Several studies have investigated the taxonomy, ecology, and distribution of Leptogium [2, 3, 5, 8, 12, 13, 14, 15, 16]; however, the reported number of known species comprising this genus varies among these publications, ranging from 150 to 400 [9, 17, 18]. In South Korea, no comprehensive study of Leptogium has been conducted to date, and existing information is based on scant data from different reports. According to previous studies, eleven species have been reported, including one variety [19, 20]. These species include Leptogium azureum (Sw. ex Ach.) Mont., Leptogium burnetiae C. W. Dodge, Leptogium cochleatum (Dicks.) P. M. Jørg. & P. James, Leptogium cyanescens (Pers.) Körb., Leptogium hildenbrandii (Garov.) Nyl., Leptogium hirsutum Sierk, Leptogium lichenoides (L.) Zahlbr., Leptogium moluccanum (Pers.) Vain., Leptogium moluccanum var. myriophyllinum (Müll. Arg.) Asahina, Leptogium pedicellatum P. M. Jørg., Leptogium rugosum Sierk, and Leptogium saturninum (Dicks.) Nyl. The present study reports three additional species: Leptogium delavayi Hue, Leptogium denticulatum Nyl., and Leptogium trichophoroides P. M. Jørg. & A. K. Wallace. A revised key to all species of Leptogium from South Korea is provided based on the current study and data from the scientific literature.

MATERIALS AND METHODS

The study was based on specimens collected from South Korea over the past ten years. A Nikon SMZ645 dissecting microscope (Nikon Corp., Tokyo, Japan) was used for identifying morphological characteristics of the thallus and reproductive structures, including color, size, and shapes, and a Zeiss Scope, A1 compound microscope (Carl Zeiss, Oberkochen, Germany) was used for studying the anatomy of thalli and ascomata. Spot test reactions were performed on thalli under a compound microscope.

Chemicals were extracted in analytical grade acetone in a 1 mL Eppendorf tube. Thin layer chromatography (TLC) was performed using a glass plate coated with TLC Silica gel 60, in solvent system A (toluene : dioxin : acetic acid = 180 : 45 : 5) [21]. Acetone extracts of lichen thalli were also subjected to high performance liquid chromatography (HPLC) analyses (LC-20A; Shimadzu, Kyoto, Japan) on a YMC-Pack ODS-A (150 × 3.9 mm I.D.) reversed-phase column containing fully end-capped C18 material (particle size, 5 µm; pore size, 12 nm). Elution was performed at a flow rate of 1 mL/min under the following conditions before subsequent injection: column temperature, 40℃; solvent system, methanol : water : phosphoric acid (80 : 20 : 1, v/v/v). Analyses were monitored by a photodiode array detector (SPD-M20A; Shimadzu) with a range of 190~800 nm throughout the HPLC run. Observed peaks were scanned between 190 and 400 nm. Voucher specimens were deposited in the herbarium of the Lichen & Allied Bioresource Centre at the Korean Lichen Research Institute, Sunchon National University, South Korea.

Molecular methods

Total DNA was extracted directly from the thalli of selected specimens according to Ekman [22], and was purified with a DNeasy Plant Mini Kit (Qiagen, Hilden, Germany). The nuclear ribosomal RNA gene, including the internal transcribed spacers (ITS) 1 and 2 and the 5.8S subunit, was amplified using the primers ITS1F [23] and LR5 [24]. Amplifications were performed using a TaKaRa JP/TP600 PCR thermal cycler (TaKaRa Bio Inc., Otsu, Japan). PCR products were then sent to the sequencing facilities of the Genotech Cooperation (Seoul, South Korea) for purification and sequencing.

Alignment of DNA sequences was performed using BioEdit [25]. Ambiguous regions were delimited [26] and excluded from the alignment. Three species (Collema furfuraceum Du Rietz, Staurolemma weberi Henssen & P. M. Jørg., and Physma byrsaeum (Ach.) Tuck.) were selected as outgroups based on BLAST sequence similarity searches in GenBank. Phylogenetic relationships among taxa were investigated using MEGA 5.2 software [27]. Phylogenetic trees were constructed using neighbor joining (NJ), minimum evolution, and maximum likelihood methods. Bootstrap support values were obtained with 1,000 pseudoreplicates.

RESULTS AND DISCUSSION

Phylogenetic analysis

The final alignment included 1,165 characters, 648 of which were variable. The NJ tree shows that the Leptogium species comprised two main clades, supported by bootstrap values of 99% (Fig. 1). All species within the clade comprising Sect. Leptogium have no tomentum on the thallus surface, while species clustered within the clade Sect. Mallotium have tomentum on the lower surface of the thallus. The Sect. Leptogium and Sect. Mallotium have a monophyletic origin. Leptogium delavayi is a sister group to L. saturninum. As some specimens are somewhat old, it was difficult to extract the total DNA from these thalli, thus limiting the number of specimens used in the phylogenetic analysis.

Fig. 1

Phylogenetic relationships among species of Leptogium for which molecular data are currently available in GenBank. This phylogeny was constructed using ITS-5.8S rDNA sequences. The tree was inferred by neighbor joining (NJ), minimum evolution (ME), and maximum likelihood (ML) analyses using the software MEGA 5. Bootstrap values are shown near the corresponding branch (NJ/ME/ML), and bold lines indicate values greater than 95%.

Key to species of Leptogium from South Korea

1. Thallus isidiate ... 2

1a. Thallus not isidiate, sometimes lobulate ... 5

2. Lower surface of lobes without white-gray tomentum ... 3

2a. Lower surface of lobes with white-grey tomentum ... 4

3. Isidia squamuliform, never cylindrical ...

3a. Isidia granular to cylindrical, occasionally squamuliform ... L. cyanescens

4. Thallus olivaceous-blackish, isidia usually granular ... L. saturninum

4a. Thallus and isidia blue-grey, isidia cylindrical coralloid, apothecia pedicellate ... L. burnetiae

5. Lower surface of lobes with white-grey tomentum ... 6

5a. Lower surface of lobes without white-grey tomentum ... 10

6. Thallus smooth, apothecia prominently stalked ... L. pedicellatum

6a. Thallus wrinkled ... 7

7. Thallus with distant wrinkles, euparaplectenchymatous layer above the cyanobiont layer ... 8

7a. Thallus densely wrinkled, apothecia with supporting layer below the cyanobiont layer ... 9

8. Thallus olivaceous, apothecia on stalks, without long marginal hairs, spores 30~38 × 8~12 µm ...

8a. Thallus dark greenish, apothecia on stalks, whitish marginal hairs on young apothecia, spores 19~24 × 8~11 µm ...

9. Thallus very heavily wrinkled, spores fusiform ... L. rugosum

9a. Thallus moderately wrinkled, spores ellipsoid ... L. hildenbrandii

10. Thallus wrinkled, isidia-like marginal outgrowth ... L. lichenoides

10a. Thallus not wrinkled ... 11

11. Thallus dark leaden grey, thalline exciple wrinkled ... L. cochleatum

11a. Thallus bluish or olivaceous, thalline exciple smooth ... 12

12. Thallus bluish, thick (50~100 µm) ... L. azureum

12a. Thallus olivaceous, thin (30~60 µm) ... L. moluccanum

Species description

Leptogium azureum

(Sw. ex Ach.) Mont., in Webb & Berthelot, Hist. Nat. Iles Canar. (Paris) 3: 129 (1840)

Thallus foliose, closely to loosely adnate, 1~6 cm wide, 70~120 µm thick, dark grey to bluish. Lobes round to oblong, 2~5 mm wide; margins entire; surface smooth, isidia absent. Lower surface with sparse, tufted rhizines. Apothecia laminal, sessile to shortly pedicellate, 1~2 mm wide; disc concave to flat, pale to dark red-brown; thalline exciple smooth, pale brown, pedicel wrinkled, to 0.5 mm long. Ascospores ellipsoid, muriform, 20~30 × 10~15 µm; pycnidia submarginal. Conidia 1~3 µm long (Fig. 2A).

Fig. 2

A, Leptogium azureum, A1: Habitus, A2: Section through apothecium margin, A3: Ascospores; B, Leptogium burnetiae habitus; C, Leptogium burnetiae var. hirsutum, C1: Habitus, C2: Section through apothecium margin, C3: Ascospores; D, L. cyanescens, D1: Habitus, D2: Section through apothecium margin, D3: Ascus with ascospores (scale bars: A1, B, C1, D1 = 1 cm, A2, D2 = 50 µm, C2 = 20 µm, A3, C3, D3 = 10 µm).

Chemistry

Two unknown chemicals were detected using HPLC and TLC (Fig. 3).

Fig. 3

High performance liquid chromatography and thin layer chromatography (solvent system A) profiles of Leptogium species. 1, Leptogium azureum with unknown chemicals 1 (a) and 2 (b); 2, Leptogium burnetiae; 3, Leptogium burnetiae var. hirsutum; 4, Leptogium cyanescens; 5, Control [Lethariella cladonioides (Nyl.) Krog] with atranorin (c), norstictic acid (d); 6, Leptogium delavayi; 7, Leptogium denticulatum; 8, Leptogium hildenbrandii; 9, Leptogium moluccanum; 10, Leptogium pedicellatum; 11, Leptogium saturninum; 12, Leptogium trichophoroides.

Remarks

Leptogium azureum is characterized by the presence of smooth thallus without isidia. This species is similar to L. cyanescens in external appearance, but the latter species differs in having isidia on the thallus. According to Sierk [8], this species closely resembles L. tremelloides Mont., but the latter species has well-developed proper exciple and slightly larger spores.

Selected specimens examined

Mt. Deogyu, on bark, 35°48'32.5" N, 127°43'36.3" E, elev. 1,320 m, J. S. Hur, 050198, 30 Apr 2005; Mt. Halla, on bark, 33°22'6.77" N, 126°34'38.0" E, elev. 1,158 m, S. Y. Kondratyuk, L. Lökös, S. O. Oh, S. Joshi, 121469, 6 Jul 2012; on bark, 33°22'13.0" N, 126°31'49.0" E, elev. 1,530 m, S. O. Oh, U. Jayalal, S. Joshi, J. S. Park, F. H. Tian, J. S. Hur, 121101, 19 Jun 2012; Mt. Jogae, on bark, 34°59'27.9" N, 127°20'01.8" E, elev. 201 m, J. S. Hur, 040007, 31 Jan 2004; on bark, 34°59'23.6" N, 127°20'23.5" E, elev. 201 m, J. S. Hur, 040001, 31 Jan 2004.

Ecology and distribution

According to Park [28], L. azureum is a common species on the bark of Abies sp. and deciduous trees. This species has been recorded in different elevation ranges in South Korea. Many reports are from Halla Mountain on Jeju Island (Fig. 4A). In East Asia, this species has also been reported from North Korea [29], China, Taiwan [30], and Japan [31].

Fig. 4

Distribution of Leptogium species in South Korea. A, Leptogium azureum; B, Leptogium burnetiae; C, Leptogium burnetiae var. hirsutum; D, Leptogium cyanescens; E, Leptogium denticulatum; F, Leptogium pedicellatum; G, Leptogium saturninum; H, Leptogium delavayi (●), Leptogium hildenbrandii (▲), Leptogium moluccanum (♦), Leptogium trichophoroides (★).

Leptogium burnetiae

C. W. Dodge, Beih. Nova Hedwigia 12: 120 (1964)

Thallus foliose, closely to loosely adnate, 1~6 cm wide, 70~150 µm thick, grey to bluish grey. Lobes round to oblong, 4~10 mm wide; upper surface smooth to roughened, isidiate; isidia dense, clustered, coralloid, width 0.07~0.09 mm, height 0.2~0.7mm, laminal, slightly darker than thallus; sometimes phyllidiate, phyllidia laminal. Lower surface pale, long-celled white hairs, up to 1~1.5 mm long. Apothecia and pycnidia not seen (Fig. 2B).

Two unknown chemicals were detected using HPLC and TLC (Fig. 3).

Leptogium burnetiae is characterized by the presence of gray thallus with the clustered coralloid isidia. This species closely resembles L. sphaerosporum P. M. Jørg. & L. Olley in external appearance, but the latter species differs in always having phyllidia on the thallus [32]. Leptogium hirsutum is also closely related to L. burnetiae, but the former species differs by the presence of gray thallus, and the cylindrical to granular, branched, somewhat large isidia. Leptogium saturninum differs from L. burnetiae by the presence of darker to blackish, thick thallus, and the short to flattened isidia.

Mt. Baekseokbong, on rock, 37°28'7.39" N, 128°39'7.60" E, elev. 494 m, Y. Joshi, X. Y. Wang, J. A. Ryu, J. Y. Hur, 090433, 090509, 16 May 2009; Mt. Hambaek, on bark (Quercus sp.), 37°10'23.5" N, 128°54'56.0" E, elev. 1,403m, J. S. Hur, 070726, 19 Jun 2007; Mt. Jiri, on rock, 35°20'04.6" N, 127°42'50.6" E, elev. 1,547m, J. S. Hur, 060730, 16 Sep 2006; on bark (Betula sp.), 35°17'52.7" N, 127°33'19.9" E, elev. 1,360 m, J. S. Hur, 060247, 17 Jun 2006; on bark (Quercus sp.), 35°17'8.39" N, 127°33'19.8" E, elev. 1,364 m, Y. Joshi, X. Y. Wang, J. Y. Hur, 091095, 13 Oct 2009; Mt. Jumbong, on bark (Quercus sp.), 38°03'46.7" N, 128°26'44.6" E, elev. 680 m, J. S. Hur, 041329, 9 Oct 2004; Mt. Maebong, on bark (Quercus sp.), 37°54'6.98" N, 127°58'9.92" E, elev. 617 m, X. Y. Wang, H. S. Jeon, L. V. Lei, J. A. Ryu, 100602, 26 May 2010; Mt. Sobaek, on a mossy rock, 36°57'21.3" N, 128°26'02.5" E, elev. 495 m, J. S. Hur, 030695, 1 Oct 2003; Mt. Songni, on rock, 36°32'43.6" N, 127°51'31.5" E, elev. 470 m, J. S. Hur, 060032, 21 Apr 2006; Mt. Sorak, on rock, 38°11'16.4" N, 128°21'42.7" E, elev. 450 m, J. S. Hur, 041504, 041521, 11 Oct 2004; Micheongol Valley, on rock, 37°56'10.6" N, 128°31'8.77" E, elev. 420m, Y. Joshi, X. Y. Wang, J. A. Ryu, J. Y. Hur, 090327, 14 May 2009.

Leptogium burnetiae is a common species on bark and rock at higher elevations (greater than 1,200 m), with few specimens recorded at lower elevations (400~500 m) (Fig. 4B). This species was reported for the first time in South Korea by Park [33]. In East Asia, this species has also been reported from Japan [31] and Taiwan [34].

Leptogium burnetiae C. W. Dodge var. hirsutum (Sierk) P. M. Jørg., Herzogia 2: 457 (1973)

According to Jørgensen [3], specimens of L. hirsutum are classified a variety of L. burnetiae due to the absence of euparaplectenchymatous proper exciple. Awasthi and Akhtar [2] followed the same method, and all the specimens belong to L. hirsutum have been classified as a variety of L. burnetiae. Our specimens show the following characters.

Thallus foliose, closely to loosely adnate, 1~6 cm wide, 70~150 µm thick, grey to bluish grey. Lobes round to oblong, 4~10 mm wide; upper surface smooth to roughened, isidiate; isidia dense, clustered, coralloid, width 0.07~0.09 mm, height 0.2~0.7 mm, laminal, slightly darker than thallus, isidioid lobules on the surface and the margin. Lower surface pale, sometimes with partly pinkish, long-celled white hairs, up to 1~1.5mm long. Apothecia somewhat rare; laminal 0.5~1.5 mm wide, shortly pedicellate, 1~1.5 mm high; disc concave to flat, reddish to dark brown; thalline exciple entire, smooth. Ascospores oval to ellipsoid, muriform, 25~30 × 12~15 µm; pycnidia not seen (Fig. 2C).

Two unknown chemicals were detected using HPLC and TLC (Fig. 3).

This species was reported for the first time in South Korea by Park [28]. According to his descriptions, isidioid lobules and lobes with partly pinkish lower surface were present. Further, we suggest all species recorded as L. hirsutum to be treated as a variety of L. burnetiae.

Mt. Baekseokbong, on rock, 37°28'7.39" N, 128°39'7.60" E, elev. 494 m, Y. Joshi, X. Y. Wang, J. A. Ryu, J. Y. Hur, 090506, 16 May 2009; Mt. Baekwoon, on bark, 35°06'44.6" N, 127°36'51.1" E, elev. 1,068 m, J. S. Hur 060437, 27 Jun 2006; Mt. Baekwoon, on bark (Quercus sp.), 35°37'08.5" N, 127°38'04.9" E, elev. 1,169 m, J. S. Hur, 060622, 17 Aug 2006; Mt. Deogyo, on bark (Quercus sp.), 35°51'05.3" N, 127°44'55.4" E, elev. 1,576 m, J. S. Hur, 060508, 10 Aug 2006; Mt. Halla, on bark, 33°22'38.8" N, 126°34'16.4" E, elev. 1,181 m, S. Y. Kondratyuk, S. O. Oh, Y. Kusama, J. S. Hur, 121663, 7 Aug 2012; Mt. Hambaek, on bark (Quercus sp.), 37°10'23.5" N, 128°54'56.0" E, elev. 1,403m, J. S. Hur, 070725, 19 Jun 2007; Mt. Jiri, on bark (Quercus sp.), 35°17'8.39" N, 127°33'19.8" E, elev. 1,364 m, Y. Joshi, X. Y. Wang, J. Y. Hur, 091112, 13 Oct 2009; Mt. Naejang, on bark, 35°29'44.3" N, 126°53'02.4" E, elev. 632 m, J. S. Hur, 030615, 8 Aug 2003; Mt. Odae, on bark, 37°46'06.9" N, 128°35'38.7" E, elev. 1,240 m, J. S. Hur, 040491, 8 May 2004; Mt. Sobaek, on bark (Quercus sp.), 36°57'57.8" N, 128°30'31.8" E, elev. 1,331m, J. S. Hur, 070511, 11 Jun 2007; Mt. Sorak, on a mossy rock, 38°07'31.7" N, 128°22'09.0" E, elev. 1,310m, J. S. Hur, 041496, 10 Oct 2004; Micheongol Valley, on rock, 37°56'10.6" N, 128°31'8.77" E, elev. 420m, Y. Joshi, X. Y. Wang, J. A. Ryu, J. Y. Hur, 090322, 14 May 2009.

Leptogium burnetiae var. hirsutum is a common species on bark and rock at higher elevations (> 1,000 m), with few specimens recorded at lower elevations (400~500 m) (Fig. 4C).

Leptogium cyanescens

(Pers.) Körb., Syst. Lich. Germ. (Breslau): 420 (1855)

Thallus foliose, closely to loosely adnate, 5~10 cm wide, 70~120 µm thick, dark grey to bluish. Lobes round to broadly oblong, 2~5 mm wide; margins entire with isidia; upper surface smooth, shiny, isidiate; isidia dense, cylindrical, simple, same color as thallus or darker. Lower surface with sparse, tufted rhizines. Apothecia very rare; laminal, sessile to shortly pedicellate, 1~2 mm wide; disc concave to flat, pale to dark red-brown; thalline exciple smooth, pale brown. Ascospores ellipsoid, muriform, 20~30 × 6~12 µm; pycnidia not seen (Fig. 2D).

Two unknown chemicals were detected using HPLC and TLC (Fig. 3).

Leptogium cyanescens is characterized by the presence of smooth thallus with dense, simple, and cylindrical isidia. This species is quite similar to L. azureum in external appearance, but the latter species differs in not having isidia on the thallus. According to Sierk [8], this species closely resembles L. dactylinum Tuck., but the latter species has olivaceous to brownish thallus, and very small, squamuliform lobes with abundant apothecia.

Mt. Deogyu, on bark, 35°51'15.9" N, 127°44'55.9" E, elev. 1,557m, J. S. Hur, 050163, 30 Apr 2005; Mt. Duta, on moss (rock), 37°34'39.0" N, 128°36'23.3" E, elev. 989 m, X. Y. Wang, H. S. Jeon, L. Lei, J. A. Ryu, 100769, 27 May 2010; Mt. Eungbok, on moss (rock), 37°51'6.92" N, 128°31'5.22" E, elev. 706 m, Y. Joshi, X. Y. Wang, J. A. Ryu, 090724, 23 May 2009; Mt. Gitdaebong, on moss (rock), 37°18'36.7" N, 128°56'7.66" E, elev. 1,222m, J. S. Hur, X. Y. Wang, J. A. Ryu, J. Y. Hur, 090404, 090383, 090386, 15 May 2009; Mt. Halla, on rock, 35°20'20.0" N, 127°41'09.9" E, elev. 755 m, J. S. Hur, 040946, 4 Sep 2004; Mt. Jobong, on moss (rock), 37°56'10.7" N, 128°33'7.47" E, elev. 980m, Y. Joshi, X. Y. Wang, J. A. Ryu, J. Y. Hur, 090318, 14 May 2009; Mt. Seorak, on bark (Quercus sp.), 38°09'9.81" N, 128°27'26.7" E, elev. 463 m, Y. Joshi, X. Y. Wang, J. A. Ryu, 090779, 24 May 2009; Mt. Songni, on a moss (rock), 36°32'41.6" N, 127°51'19.0" E, elev. 440 m, J. S. Hur, 060027, 21 Apr 2006; Backdam Temple, on rock, 38°10'40.9" N, 128°22'23.2" E, elev. 455 m, J. S. Hur, 041550, 11 Oct 2004; Kwaneum Temple, on bark (Quercus sp.), 33°25'6.78" N, 126°32'9.38" E, elev. 565 m, J. S. Hur, X. Y. Wang, J. A. Ryu, J. Y. Hur, 090070, 19 Apr 2009; Micheongol Valley, on moss (rock), 37°56'10.6" N, 128°31'8.77" E, elev. 420m, Y. Joshi, X. Y. Wang, J. A. Ryu, J. Y. Hur, 090318, 14 May 2009.

This species is distributed in different altitudes in South Korea. Most of the species were collected from mossy rock surfaces, and a few specimens were collected from tree bark (Fig. 4D). This species was reported for the first time in South Korea by Kim [35]. In East Asia, this species has also been reported from North Korea [29], China, Taiwan [30], and Japan [31].

Leptogium delavayi

Hue, Bull. Soc. Bot. Fr., 36: 25 (1889)

Thallus foliose, closely to loosely adnate, 3~5 cm wide, 100~130 µm thick, dark grey to olivaceous. Lobes round to orbicular, 4~7 mm wide; margins entire to crenate without isidia or phyllidiate; upper surface dull, wrinkled. Lower surface pale, with dense, long-celled white hairs, up to 1 mm long. Apothecia common; laminal 0.5~1 mm wide, shortly pedicellate, 1~1.5 mm in height; disc concave to flat, reddish brown; thalline exciple entire to wrinkled without white hairs. Ascospores ellipsoid with acute ends, muriform, 30~38 × 8~12 µm; pycnidia not seen (Fig. 5A).

Fig. 5

A, Leptogium delavayi, A1: Habitus, A2: Section through apothecium margin, A3: Ascospores; B, Leptogium denticulatum, B1: Habitus, B2: Section through apothecium margin, B3: Ascospores; C, Leptogium hildenbrandii habitus; D, Leptogium moluccanum, D1: Habitus, D2: Section through apothecium margin, D3: Ascospores (scale bars: A1, B1, C, D1 = 1 cm, A2, B2, D2 = 50 µm, A3, B3, D3 = 10 µm).

Two unknown chemicals were detected using HPLC and TLC (Fig. 3).

Leptogium delavayi is characterized by the presence of olivaceous, wrinkled thallus with pedicellate apothecia. This species closely resembles L. arisanense Asah., which has sessile apothecia and long marginal hairs [13]. This is the first record for the lichen mycota of South Korea.

Specimens examined

Mt. Hwangbyeng, on moss (bark), 37°44'47.6" N, 128°37'31.5" E, elev. 772 m, J. S. Hur, 080442, 14 Jul 2008.

This species was recorded at a mid-elevation range (c. 772 m) in South Korea (Fig. 4H). In East Asia, this species has also been reported from Taiwan, China [30], and Japan [31].

Leptogium denticulatum

Nyl., Ann. Sci. Nat., Bot., Sér. 5 7: 302 (1867)

Thallus foliose, closely to loosely adnate, 3~10 cm wide, 70~120 µm thick, dark grey to bluish. Lobes round to broadly oblong, 2~5 mm wide; margins entire, dentate or phyllidiate, often ascending; upper surface smooth, shiny, phyllidiate, never isidiate; phyllidia granular-flattened at first, becoming coralloid-squamuliform to expanded-lobulate, laminal and marginal. Lower surface naked with sparse, tufted rhizines. Apothecia rare; laminal, sessile to shortly pedicellate, 1~2 mm wide; disc concave to flat, pale to dark red-brown; thalline exciple smooth to lobulate, pale brown. Ascospores ellipsoidal, muriform, 15~30 × 7~12 µm; pycnidia not seen (Fig. 5B).

Two unknown chemicals were detected using HPLC and TLC (Fig. 3).

Leptogium denticulatum is characterized by the presence of smooth, non-wrinkled thallus, with well-defined phyllidia (never isidioid) on the margins and upper surface. This species closely resembles L. cyanescens, but the latter species has isidia on the thallus and margins. Leptogium azureum closely resembles L. denticulatum in external appearance, but the former species differs in having neither isidia nor phyllidia on the thallus.

Mt. Baeka, on rock, 34°32'33.1" N, 126°55'46.7" E, elev. 334 m, J. S. Hur, 050561, 8 Oct 2005; Mt. Gakhuel, on rock, 38°06'24.8" N, 127°23'20.5" E, elev. 535 m, J. S. Hur, 080339, 28 Jul 2008; Mt. Geumwon, on rock, 35°43'39.0" N, 127°47'31.4" E, elev. 704 m, X. Y. Wang, H. S. Jeon, G. S. Han, 100559, 25 Jun 2010; Mt. Halla, on bark, 33°19'16.0" N, 126°33'21.0" E, elev. 957m, S. O. Oh, U. Jayalal, S. Joshi, J. S. Park, F. H. Tian, J. S. Hur, 121268, 121259, 20 Jun 2012; Mt. Taebaek, on rock, 36°44'42.5" N, 128°15'54.6" E, elev. 1,118 m, J. S. Hur, 070833, 18 Jun 2007; Mt. Worak, on rock, 36°52'01.3" N, 128°06'34.3" E, J. S. Hur, 041248, 19 Sep 2004; Ulleung Island, on rock, 37°29'21.8" N, 130°53'15.2" E, elev. 545 m, J. S. Hur, 050322, 22 Jun 2005.

This species is distributed in different altitude ranges in South Korea. Most of the species were collected from mossy rock surfaces, and a few specimens were collected from tree bark (Fig. 4E). This is the first report of this species from South Korea. In East Asia, this species has also been reported from China [30], Taiwan [34], and Japan [31].

Leptogium hildenbrandii

(Garov.) Nyl., Act. Soc. Linn. Bordeaux, Trois. Sér. 21: 272 (1856)

Thallus foliose, closely to loosely adnate, often forming rounded patches, 3~12 cm wide, 70~150 µm thick, black gray to brownish. Lobes rounded to orbicular, 5~10 mm wide, margins entire to wavy; upper surface wrinkled, rough, isidia and phyllidia absent. Lower surface pale, with long-celled white hairs, up to 1~1.5 mm long. Apothecia not seen. Pycnidia immersed on thallus, marginal to submarginal, 0.1~0.3 mm wide. Conidia bacilliform, apices swollen, 4.3~5.5 × 1.3~1.6 µm (Fig. 5C).

Two unknown chemicals were detected using TLC (Fig. 3).

Leptogium hildenbrandii is characterized by the presence of black gray to brownish, wrinkled, thallus, which often forms rounded patches. According to Jørgensen [3], this species is distinguished by the presence of euparaplectenchymatous supporting tissue in the lower part of the apothecium, below the algal layer in the cortical region. This species closely resembles Leptogium rugosum Sierk, but the latter species is distinguished by the presence of heavily wrinkled thallus, fusiform, somewhat large spores, and absence of the thallus forming rounded patches [13].

Mt. Odae, on bark, 37°46'22.4" N, 128°36'05.8" E, elev. 1,450 m, J. S. Hur, 040507, 8 May 2004.

Leptogium hildenbrandii is a rare species, and is found on bark at higher elevations (> 1,000 m) (Fig. 4H). The species has been reported from South Korea by Moon [36]. In East Asia, this species has also been reported from China [30] and Japan [31].

Leptogium moluccanum

(Pers.) Vain., Acta Soc. Fauna Flora Fenn. 7: 223 (1890)

Thallus foliose, closely to loosely adnate, 2~3 cm wide, 50~70 µm thick, dark grey to olivaceous. Lobes round to broadly oblong, 1~3 mm wide; margins entire, confluent; upper surface smooth, shiny, without isidia or phyllidia. Lower surface lighter than the upper surface, without hairs. Apothecia rare; laminal, sessile to shortly pedicellate, 0.5~1.5 mm wide; disc concave to flat, pale to dark red-brown; thalline exciple smooth to wavy, upper most margin same as thallus color. Ascospores ellipsoid, submuriform, 20~30 × 6~12 µm; pycnidia not seen (Fig. 5D).

Two unknown chemicals were detected using HPLC and TLC (Fig. 3).

This species is characterized by the presence of leaden grey to olivaceous, thin thallus with smooth apothecial disc. Leptogium azureum closely resembles L. moluccanum, but the former species has a grayish, comparatively thick thallus [4]. Leptogium moluccanum var. myriophyllinum (Müll. Arg.) Asahina, another variety of the same species, has also been reported from South Korea by Park [28]. In East Asia, the same variety has also been reported from North Korea [29] and Japan [31].

Mt. Duryun (Daeheung Temple), on moss (rock), GPS data not given, J. S. Hur, 030103, 030311, 4 Apr 2003; Mt. Taebaek, on bark, 37°12'35.3" N, 128°55'11.9" E, elev. 1,399 m, J. S. Hur, 080267, 25 May 2008.

This species was reported from South Korea by Kashiwadani and Moon [37], and is distributed at higher elevations (Fig. 4H). In East Asia, this species has also been reported from China, Taiwan [30], Japan [31], and North Korea [29].

Leptogium pedicellatum

P. M. Jørg., Herzogia 3: 448 (1975)

Thallus foliose, closely to loosely adnate, 10~15 cm wide, 70~120 µm thick, dark grey to bluish. Lobes round to broadly orbicular, 5~10 mm wide; margins entire without isidia. Sometime phyllidiate; upper surface smooth, dull. Lower surface pale, with dense, long-celled white hairs, up to 1 mm long. Apothecia common; laminal 0.5~2 mm wide, shortly pedicellate, 1~1.5 mm height; disc concave to flat, reddish brown; thalline exciple entire, smooth, young apothecial margins with white hairs. Ascospores ellipsoidal, muriform, 27~30 × 12~15 µm; pycnidia not seen (Fig. 6A).

Fig. 6

A, Leptogium pedicellatum, A1: Habitus, A2: Section through apothecium margin, A3: Ascospores; B, Leptogium saturninum habitus; C, Leptogium trichophoroides, C1: Habitus, C2: Section through apothecium margin, C3: Ascospores (scale bars: A1, B, C1 = 1 cm, A2, C2 = 50 µm, A3, C3 = 10 µm).

Two unknown chemicals were detected using HPLC and TLC (Fig. 3).

Leptogium pedicellatum is characterized by the presence of grayish, smooth, thallus with pedicellate apothecia. This species closely resembles L. menziesii (Ach.) Mont., which has sessile apothecia and smaller spores [2]. According to Jørgensen and Olley [32], this species is closely related to L. sphaerosporum due to the occasional production of phyllidia; however, the latter species always produces phyllidia. In South Korea, this species was identified as L. menziesii by Kim [35]. According to the lichen checklist prepared by Hur et al. [19], all previously reported species of L. menziesii were classified as L. pedicellatum.

Mt. Deogyu, on bark (Oak sp.), 35°51'23.2" N, 127°45'02.5" E, elev. 1,560 m, J. S. Hur, 050105, 3 Apr 2005; Mt. Gyeokja, on rock, 34°08'50.4" N, 126°32'9.06" E, elev. 368 m, J. S. Hur, 100151, 5 Feb 2010; Mt. Halla, on bark, 33°23'54.0" N, 126°32'21.0" E, elev. 942m, S. O. Oh, U. Jayalal, J. S. Park, J. S. Hur, 121031, 121055, 1 Jun 2012; Mt. Hambaek, on bark (Acer sp.), 37°11'28.1" N, 128°54'53.2" E, elev. 1,456 m, J. S. Hur, 070685, 19 Jun 2007; Mt. Hugseok, on bark, 34°41'16.7" N, 126°40'18.1" E, elev. 456 m, J. S. Hur, 050511, 23 Sep 2005; Mt. Jiri, on bark, 35°19'38.5" N, 127°42'59.4" E, elev. 1,660m, J. S. Hur 040388, 24 Apr 2004; Mt. Juhul, on mossy rock, 36°46'16.9" N, 128°05'16.1" E, elev. 480 m, J. S. Hur 040129, 29 Feb 2004; Mt. Juwang, on rock, 36°24'09.6" N, 129°10'27.0" E, elev. 380 m, J. S. Hur, 050603, 15 Oct 2005; Mt. Odae, on bark, 37°46'51.4" N, 128°36'13.3" E, elev. 1,435 m, J. S. Hur, 040525, 8 May 2004; Mt. Sorak, on mossy bark, 38°08'53.5" N, 128°20'05.3" E, elev. 1,010 m, J. S. Hur, 050277, 16 Jun 2005; Mt. Taebaek, on bark, 37°06'31.0" N, 128°54'33.0" E, elev. 1,235 m, J. S. Hur, 040177, 040178, 24 Apr 2004; Wando Arboretum, on mossy bark, 34°21'10.3" N, 126°41'10.9" E, elev. 535 m, J. S. Hur, 050149, 13 Apr 2005; Singaemul Park, on rock, 33°30'31.3" N, 126°10'13.1" E, elev. 19 m, S. Y. Kondratyuk, L. Lökös, S. O. Oh, U. Jayalal, S. Joshi, J. S. Park, J. S. Hur, 121412, 121387, 5 Jul 2012; Gwanum Temple, on rock, 33°25'21.5" N, 126°33'34.8" E, elev. 615 m, S. Y. Kondratyuk, L. Lökös, 121917, 7 Jul 2012.

This species is distributed in both low (c. 400 m) and high elevations (> 1,000 m) in South Korea (Fig. 4F). This species was reported for the first time in South Korea by Kim [35]. In East Asia, this species has also been reported from North Korea [38], China [2], and Japan [31].

Leptogium saturninum

(Dicks.) Nyl., Act. Soc. Linn. Bordeaux, Trois. Sér. 21: 272 (1856)

Thallus foliose, closely to loosely adnate, 1~6 cm wide, 70~150 µm thick, brownish black to olivaceous black. Lobes round to orbicular, 4~8 mm wide, confluent in the central part of the thallus, margins entire to wavy; upper surface smooth to roughened, isidiate; isidia granular to coralloid, width 0.03~0.07 mm, height 0.1~0.3 mm, sparse to dense. Lower surface pale, long-celled white hairs, up to 1~1.5 mm long. Apothecia and pycnidia not seen (Fig. 6B).

Two unknown chemicals were detected using HPLC and TLC (Fig. 3).

Leptogium saturninum is characterized by the presence of olivaceous black, thick thallus with short to flattened, granular isidia. This species closely resembles L. burnetiae in external appearance, but the latter species differs in having large coralloid isidia, and thin, bluish thallus. According to Awasthi and Akhtar [2], coralloid isidia are also present in L. burnetiae, and some parts of such thallus may become blackened; therefore, it may be difficult to distinguish such specimens from L. saturninum.

Mt. Baekseokbong, on a mossy rock, 37°28'7.39" N, 128°39'7.60" E, elev. 494 m, Y. Joshi, X. Y. Wang, J. A. Ryu, J. Y. Hur, 090492, 16 May 2009; Mt. Cheongryang, on bark, 36°47'25.2" N, 128°55'25.4" E, elev. 885 m, J. S. Hur, 040105, 28 Feb 2004; Mt. Hambaek, on bark, 37°11'27.3" N, 128°54'52.9" E, elev. 1,445 m, J. S. Hur, 070689, 19 Jun 2007; Mt. Odae, on bark, 37°46'17.2" N, 128°36'04.1" E, elev. 1,454 m, J. S. Hur, 080550, 15 Jul 2008; Mt. Seok-byeong, on bark, 37°35'14.7" N, 128°52'57.1" E, elev. 969 m, J. S. Hur, 080244, 24 May 2008; on bark, 37°35'02.2" N, 128°52'29.1" E, elev. 901 m, J. S. Hur, 080232, 24 May 2008; Mt. Seorak, on bark (Quercus sp.), 38°09'9.81" N, 128°27'26.7" E, elev. 463m, Y. Joshi, X. Y. Wang, J. A. Ryu, 090777, 24 May 2009; Mt. Taebaek, on bark, 37°06'08.2" N, 128°55'53.1" E, elev. 1,349 m, J. S. Hur, 030668, 20 Aug 2003.

Leptogium saturninum is a common species on bark and rock at higher elevations (> 1,000 m), and few specimens were recorded at lower elevations (400~500m) (Fig. 4G). This species was reported for the first time in South Korea by Park [28]. In East Asia, this species has also been reported from North Korea [29], China [30], and Japan [31].

Leptogium trichophoroides

P. M. Jørg. & A. K. Wallace, in Jørgensen, Symb. Bot. Ups. 32: 123 (1997)

Thallus foliose, closely to loosely adnate, 3~5 cm wide, 130~170 µm thick, brownish to blackish grey. Lobes round to orbicular, 3~8 mm wide; margins entire to crenate without isidia or phyllidia; upper surface dull, wrinkled. Lower surface pale, with dense, long-celled white hairs, up to 1 mm long. Apothecia common; marginal to sub-marginal, 0.3~1.5 mm wide, shortly pedicellate; disc concave to flat, reddish brown; thalline exciple entire to wrinkled with white hairs on young apothecia. Ascospores ellipsoidal with somewhat round ends, muriform, 19~24 × 8~11 µm; pycnidia not seen (Fig. 6C).

Two unknown chemicals were detected using HPLC and TLC (Fig. 3).

Leptogium trichophoroides is characterized by the presence of brownish to blackish grey wrinkled thallus with pedicellate apothecia. This species closely resembles L. trichophorum Müll. Arg., but the latter species is distinguished by the presence of sessile apothecia with blackish hairs and large spores [13]. This is the first record for the lichen mycota of South Korea.

Mt. Duta, on moss (bark), 37°25'54.4" N, 128°58'33.6" E, elev. 1,352 m, J. S. Hur, 080166, 11 May 2008.

This species was recorded at higher elevations (c. 1,300 m) in South Korea (Fig. 4H). In East Asia, this species has also been reported from Taiwan [13] and Japan [13, 31].

The following species were not traceable; therefore, the descriptions were based on the published literature.

Leptogium cochleatum

(Dicks.) P. M. Jørg. & P. James, Lichenologist 15: 113 (1983)

This species has leaden grey thallus without isidia. It has sessile apothecia and wrinkled thalline exciple. This species closely resembles L. moluccanum and L. azureum, but both of the latter species have smooth thalline exciple [4].

This species was reported for the first time in South Korea by Park [33]. In East Asia, this species has also been reported from North Korea [29] and Japan [31].

Leptogium lichenoides

(L.) Zahlbr., Cat. Lich. Univ. 3: 136 (1924)

This species has small, dark brown to red brown cushion-like thallus. Lobes wrinkled, upright, and edges with finely divided, cylindrical isidia-like outgrowths [39].

The species was reported from South Korea by Park [40]. In East Asia, this species has also been reported from China [30] and Japan [31].

Leptogium rugosum

Sierk, Bryologist 67: 265 (1964)

This species is distinguished by the presence of dark gray to olivaceous thallus, with the surface covered by deep wrinkles without isidia or lobules [39].

This species was reported for the first time in South Korea by Moon [36]. In East Asia, this species has also been reported from Japan [31].