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Research Article
Squamarina (lichenised fungi) species described from China belong to at least three unrelated genera
expand article infoYan-Yun Zhang§, Xin-Yu Wang, Li-Juan Li§, Christian Printzen|, Einar Timdal, Dong-Ling Niu#, An-Cheng Yin, Shi-Qiong Wang, Li-Song Wang
‡ Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China
§ University of Chinese Academy of Sciences, Beijing, China
| Senckenberg Research Institute, Frankfurt am Main, Germany
¶ University of Oslo, Oslo, Norway
# Ningxia University, Yinchuan, China
Open Access

Abstract

New collections of six Squamarina species from type localities in China were studied. The comparison of morphological characteristics and secondary metabolites with those of the type specimens and phylogenetic analyses suggest that S. callichroa and S. pachyphylla belong to Rhizoplaca, S. semisterilis belongs to Lobothallia and S. chondroderma should be retained in Lecanora temporarily. Only two species, S. kansuensis and S. oleosa, remain in Squamarina. The new combinations Lobothallia semisterilis (H. Magn.) Y. Y. Zhang, Rhizoplaca callichroa (Zahlbr.) Y. Y. Zhang and R. pachyphylla (H. Magn.) Y. Y. Zhang are proposed. Detailed descriptions to aid the identification of these species, distributions and phylogenetic trees, based on multiple collections, are presented. The generic concept of Squamarina is recircumscribed in this study.

Keywords

Squamarinaceae, Petroplaca, Rhizoplaca, Lobothallia, Lecanora, type study

Introduction

The genus Squamarina Poelt was first erected by Poelt (1958) and is characterised by thick squamules, large apothecia and a “Squamarina-type” thallus, consisting of a well-separated and more or less equally high upper cortex, algal layer and medulla. Two sections, S. sect. Squamarina and S. sect. Petroplaca, were distinguished by Poelt (1958), based on the former having a larger thallus and larger apothecia, and the latter smaller thallus and apothecia. Hafellner (1984) accommodated the genus in a new family, Squamarinaceae, based on asci with an evenly amyloid tholus without any axial body. However, the circumscription of Squamarina or Squamarinaceae has been disputed for a long time and molecular studies for this genus are largely lacking (Hafellner 1984; Haugan and Timdal 1992; Hertel and Rambold 1988; Poelt 1958). Recent studies showed that the species of the sect. Squamarina have asci with an amyloid tube in the tholus, resembling those of Porpidiaceae and that the ascus structure of sect. Petroplaca resembles that of Protoparmeliopsis muralis (Schreb.) Rabenh. (Haugan and Timdal 1992; Hertel and Rambold 1988). Hence, the detailed circumscription of the genus Squamarina is urgently needed and it was also one of the aims of this study.

Nine species of Squamarina have so far been reported from China (Wei 1991), of which six were originally collected in China by Birger Bohlin and Heinrich Frh. von Handel-Mazzetti: S. callichroa (Zahlbr.) Poelt, S. chondroderma (Zahlbr.) Wei, S. kansuensis (H. Magn.) Poelt, S. oleosa (Zahlbr.) Poelt, S. pachyphylla (H. Magn.) Wei and S. semisterilis (H. Magn.) Wei. Although these species were published about 100 years ago (Magnusson 1940; Zahlbruckner 1930), no more collections have, however, been reported since then, except for S. chondroderma and molecular data are not available for any of them in GenBank. Therefore, studies on the identification, distribution and phylogeny of these species are necessary. We have undertaken several field trips along the collection routes of Birger Bohlin (1930–1932) and Handel-Mazzetti (1914–1915) in the past few years and collected fresh material of the six species from the type localities for the molecular study presented here.

Methods

Morphological and chemical studies

Type specimens were loaned from the Museum of Natural History Vienna (W) and the Swedish Museum of Natural History (S). The fresh material collected for this study is deposited in Kunming Institute of Botany, Chinese Academy of Sciences (KUN-L). Morphological features were studied under a dissecting microscope (Nikon SMZ745T). Apothecia and thalli were sectioned with an S-30 microtome with a KS-34 cryostat (Zeiss, Jena) and microscopic traits were observed and measured using a microscope (Leica 020-518.500). Secondary metabolites were analysed by spot reactions and thin-layer chromatography (TLC) in solvents A, B and C (Orange et al. 2001).

DNA extraction, PCR and sequencing

Total DNA was extracted from dry or fresh specimens using the DNeasy Plant Mini Kit (Qiagen, Germany), according to the manufacturer’s instructions. Amplifications were performed in a 25 μl volume containing 12.5 μl 2 × MasterMix (TaqDNA Polymerase [0.1 units/μl], 0.4 mM MgCl2, 0.4 nM dNTPs) (Aidlab Biotechnologies Co. Ltd.), 0.5 μl of each primer, 10 μl ddH2O and 1 μl of DNA. The PCR settings and the primers of nrITS (ITS1-5.8S-ITS2), nrLSU, RPB1, RPB2 and mtSSU follow Zhao et al. (2015). All PCR reactions were sequenced by TsingKe Biological Technology (Kunming, China) using the amplification primers.

Phylogenetic analyses

Sequences were assembled and edited using SeqMan 7.1 (DNAstar packages). An nrITS matrix of Lobothallia (Clauzade & Cl. Roux) Hafellner, an nrLSU matrix of Squamarina and a 5-locus (nrITS, nrLSU, RPB1, RPB2 and mtSSU) concatenated matrix of Rhizoplaca Zopf and related genera were generated using Geneious R8. Single-gene analyses were conducted, based on the Maximum Likelihood (ML) method to assess the conflict amongst individual genes and no significant incongruence was detected. Matrices were aligned with MAFFT, using the web service (http://mafft.cbrc.jp/alignment/server/index.html). Ambiguous positions were removed, using the web service of Guidance (http://guidance.tau.ac.il/ver2/). MrModeltest2.3 (Nylander 2004), based on Akaike Information Criterion (AIC), was used to estimate the best-fitting substitution model for each dataset for Maximum Likelihood (ML) and Bayesian Inference (BI). The selected model for nrITS-Lobothallia was HKY+I and, for the other matrices, GTR+I+G. Bayesian reconstructions of phylogenies were performed with MrBayes 3.1.2 (Huelsenbeck and Ronquist 2001), using four Markov chains running for 2 million generations for single locus matrices and 10 million generations for the concatenated dataset. Trees were sampled every 100 generations. ML analyses were performed with RaxmlHPC, using the General Time Reversible model of nucleotide substitution with the gamma model of rate heterogeneity (GTRGAMMA). Support values were inferred from the 70% majority-rule tree of all saved trees obtained from 1000 non-parametric bootstrap replicates. Trees were visualised in FigTree v1.4.0 (Rambaut 2012).

Results and discussions

A total of 84 sequences of the nrITS, nrLSU, RPB1, RPB2 and mtSSU were newly generated for the species Squamarina chondroderma, S. semisterilis, S. callichroa, S. pachyphylla, S. gypsacea (Sm.) Poelt, S. kansuensis and S. oleosa in this study (Table 1). The BLAST results showed that these species belong to at least three unrelated genera, Lobothallia, Squamarina and Rhizoplaca, respectively. Given the large evolutionary divergence of these species, we reconstructed three separate phylogenies focusing on the three genera, based on nrITS, nrLSU and a 5-locus (nrITS, nrLSU, RPB1, RPB2 and mtSSU) concatenated matrix, respectively (Figs 2, 4, 6), to clarify the phylogenetic position of the six species. The results showed that Squamarina semisterilis is nested within the genus Lobothallia, which is closely related to the species L. alphoplaca (Wahlenb.) Hafellner, L. melanaspis (Ach.) Hafellner and L. praeradiosa (Nyl.) Hafellner, but differs in having a pruinose thallus and grows on soil. The Aspicilia-type ascus and bacilliform conidia clearly distinguish this species from the genus Squamarina. Squamarina callichroa and S. pachyphylla were nested within the Rhizoplaca chrysoleuca (Sm.) Zopf group. The exclusion of the two species from Squamarina is also supported by their Lecanora-type ascus and the orange or black apothecia. Therefore, the new combinations Lobothallia semisterilis (H. Magn.) Y. Y. Zhang, Rhizoplaca callichroa (Zahlbr.) Y. Y. Zhang and R. pachyphylla (H. Magn.) Y. Y. Zhang are proposed here.

Table 1.

Specimens and DNA sequences for nrITS, nrLSU, RPB1, RPB2 and mtSSU used in this study, with the corresponding voucher information from GenBank indicated. Sequences, newly obtained in this study, are indicated in boldface.

Species Locality* Voucher specimens Accession number*
nrITS nrLSU RPB1 RPB2 mtSSU
Aspicilia cinerea Sweden Nordin 6213 (UPS) JF703115
A. epiglypta Sweden Nordin 6105 (UPS) HQ259262
Cladia aggregata Australia HTL 19970f (F) GQ500969
C. deformis Australia HTL 19994d (F) GQ500967
Cladonia digitata na Ekman 3424 (BG) AY756319
C. stipitata na AFTOL-ID 1657 (DUKE) DQ973026
C. sulcata Australia HTL 19975i (F) GQ500959
Herteliana schuyleriana USA: North Carolina 1885671 MH887488
H. taylorii na Hertel 39599 (UPS) AY756351
Heterodea muelleri Australia Elix 39643 (CANB) GQ500962
Lecanora achroa Thailand Papong 6458 (F) JN943714 na JN987926 KT453937 JQ782663
L. caesiorubella Australia Lumbsch 19974k (F) JN943728 JN939508 JN987920 na na
L. chondroderma 1 China: Yunnan 16-54907 (KUN-L) MK778053 MK778013 MK766421 MK766441 na
L. chondroderma 2 China: Xizang 16-52925 (KUN-L) MK778052 MK778012 MK766420 MK766440 MN192155
L. chondroderma 3 China: Xizang 16-53527 (KUN-L) MK778056 MK778016 MK766423 MK766443 MN192156
L. chondroderma 4 China: Yunnan 17-55591 (KUN-L) MK778057 MK778017 MK766424 MK766444 na
L. conizaeoides na K. Molnar U0505/M (DUKE) na na KJ766862 KJ766956 KJ766418
L. contractula na AFTOL-ID 877 (DUKE) HQ650604 DQ986746 DQ986817 DQ992428 DQ986898
L. dispersa USA: Illinois Leavitt 12-002 KT453733 na KT453888 KT453921 na
L. farinacea Australia Lumbsch 20003 (F) JN943725 JN939513 JN987924 na JQ782672
L. flavopallida Australia Lumbsch 19972d (F) JN943723 JN939516 JN987925 KT453938 JQ782673
L. formosa China: Xinjiang ZX 20129045-2 (SDNU) KT453771 KT453773 na KT453978 KT453819
L. hybocarpa na Lumbsch s.n. (F) EF105412 EF105421 EF105430 na EF105417
L. intricata na U166 (GZU) AF070022 DQ787345 na na DQ787346
L. novomexicana USA 55026 (BRY-C) HM577257 na KU935390 KU935136 na
L. polytropa na AFTOL-ID 1798 (DUKE) HQ650643 DQ986792 na DQ992418 DQ986807
L. saligna USA Leavitt 5702 (BRY-C) KU934539 na KU935293 KU935036 na
L. tropica Kenya Lumbsch 19573a (F) JN943718 JN939537 JN987936 na na
Lecidella carpathica China: Xinjiang ZX 20140367-2 (SDNU) KT453741 KT453784 KT453905 KT453944 KT453831
L. stigmatea China: Xinjiang ZX 20140838 (SDNU) KT453766 KT453803 KT453918 KT453971 KT453849
L. tumidula China: Xinjiang ZX XL0009 (SDNU) KT453810
Lepraria bergensis na Tonsberg 28875 (BG) AY756324
L. incana na AFTOL-ID 1792 (DUKE) DQ986795
Lobothallia alphoplaca China 20117616 (SDNU) JX499233
L. alphoplaca China 20117646 (SDNU) JX476025
L. crassimarginata China 20122565 (SDNU) JX476026
L. crassimarginata China 20122583 (SDNU) KC007439
L. helanensis China 20122517 (SDNU) JX476030
L. helanensis China 20122791 (SDNU) JX476031
L. melanaspis Sweden Nordin 6622 (UPS) HQ259272
L. melanaspis Norway Owe-Larsson 8943a (UPS) JF825524
L. praeradiosa China 20126314 (SDNU) JX499232
L. praeradiosa China 20126613 (SDNU) JX499234
L. pruinosa China 20123278 (SDNU) JX476028
L. pruinosa China 20123630 (SDNU) JX476027
L. radiosa Sweden Nordin 5889 (UPS) JF703124
L. recedens Sweden Nordin 6035 (UPS) HQ406807
L. semisterilis China: Qinghai 18-59262 (KUN-L) MK778040 MK778009 na na na
L. semisterilis China: Qinghai 18-59322 (KUN-L) MK778039 MK778008 MK766413 na na
L. semisterilis China: Qinghai 18-59345 (KUN-L) MK778042 MK778011 MK766415 na na
L. semisterilis China: Gansu 18-59596 (KUN-L) MK778041 MK778010 MK766414 na na
Metus conglomeratus Australia HTL 19982b (F) GQ500958
Miriquidica complanata Poland: Karkonosze Mts Szczepanska 935 (herb. Szczepanska) KF562187 KF562179 KF601233 na KR995349
M. garovaglii Slovakia: Karpaty Mts Szczepanska 538 (herb. Szczepanska) KF562188 na KF601234 na na
Mycoblastus affinis na AFTOL-ID 1047 (DUKE) na KJ766601 na KJ766958 na
M. sanguinarius na AFTOL-ID 196 (DUKE) DQ782842 DQ912333 na DQ782867 DQ912276
Paralecia pratorum Italy M-0045925 (M) KP224503
Pilophorus cereolus na na AY340559
P. strumaticus na na AY340560
Protoparmeliopsis achariana na U525 na DQ787341 DQ973051 DQ973088 DQ972976
P. garovaglii USA Leavitt 106 (BRY-C) KU934546 na KU935300 KU935043 na
P. muralis na K. Molnar U0501/AO (EGR) na KJ766634 KJ766830 KJ766943 KJ766466
P. peltata Iran MS014622 KT453723 na KT453892 KT453927 na
P. zareii Iran SK 480 KP059049 na na na KP059055
Ramboldia gowardiana na Bjork 9447 (UBC) na KJ766649 KJ766889 na KJ766483
R. sanguinolenta Australia: Queensland Elix 28835 (F) EU075548 EU075523 KT453920 na EU075534
Rhizoplaca callichroa 1 China: Sichuan 14-43348 (KUN-L) MK778045 na na na na
R. callichroa 2 China: Sichuan 14-43357 (KUN-L) MK778046 na na na na
R. callichroa 3 China: Sichuan 14-43359 (KUN-L) MK778043 na na na na
R. callichroa 4 China: Yunnan 14-43308 (KUN-L) MK778044 na na na na
R. chrysoleuca 1 USA 55000 (BRY-C) HM577233 KT453812 KU935335 KU935084 KT453856
R. chrysoleuca 2 Iran MS014636 KT453731 na KT453898 KT453934 na
R. huashanensis China Wei 18357 (HAMS) AY530885 AY648104 na na na
R. marginalis 1 USA: California Leavitt 739 (BRY-C) KT453732 na KT453901 KT453936 na
R. marginalis 2 USA 0020826b (BRY-L) KU934655 na KU935370 KU935123 na
R. melanophthalma Iran MS014628 (H) JX948271 na JX948317 JX948355 na
R. pachyphylla 1 China: Gansu 18-59466 (KUN-L) MK778048 na MK766417 MK766436 MN192152
R. pachyphylla 2 China: Gansu 18-59446 (KUN-L) MK778047 na MK766416 MK766435 MN192151
R. pachyphylla 3 China: Gansu 18-59482 (KUN-L) MK778049 na MK766416 MK766437 MN192153
R. pachyphylla 4 China: Gansu 18-59561 (KUN-L) MK778050 na MK766419 MK766438 MN192154
R. polymorpha USA 55095 (BRY-C) HM577326 na KU935411 KU935159 na
R. porterii USA 55149 (BRY-C) HM577380 na JX948341 JX948380 na
R. shushanii USA 55065 (BRY-C) HM577286 na JX948334 JX948372 na
R. subdiscrepans Russia Vondrak 9408 (PRA) KU934898 na KU935435 KU935187 na
Squamarina cartilaginea na AFTOL-ID 1281 DQ986763
S. gypsacea Greece O-L-196249 (O) na MK778021 na na na
S. gypsacea Greece O-L-196255 (O) na MK778020 na na na
S. gypsacea Greece O-L-59266 (O) na MK778019 na na na
S. gypsacea Spain O-L-16444 (O) na MK778022 na na na
S. kansuensis China: Xizang 16-54052 (KUN-L) MK778059 MK778023 MK766425 MK766446 na
S. kansuensis China: Ningxia 14-09-1429 (NXAC) MK778060 MK778024 MK766426 MK766447 na
S. kansuensis China: Xinjiang 20139103 (XJU) MK778061 MK778025 MK766427 MK766448 na
S. kansuensis China: Qinghai 18-59260 (KUN-L) MK778062 MK778026 MK766428 MK766449 na
S. kansuensis China: Gansu 18-59601 (KUN-L) na MK778031 na na na
S. lentigera na Haugan & Timdal 4801 (O) AY756363
S. oleosa China: Yunnan 19-66398 (KUN-L) MN904892 MN904896 na MN923191 MN915135
S. oleosa China: Yunnan 19-66399 (KUN-L) MN904893 MN904897 MN923189 MN923192 MN911318
S. oleosa China: Yunnan 19-66401 (KUN-L) MN904894 MN904898 MN923190 MN923193 MN915136
Stereocaulon alpinum Austria AT1194 (HBG) JN941201
S. sasakii Japan AT1187 (TUR) JN941206
S. tomentosum Finland AT1084 (TUR) JN941203

Lecanora chondroderma (= Squamarina chondroderma) is sister to the genus Rhizoplaca, but differs in growing on moss and meadow and the presence of numerous rhizinose strands that are never present in its related genera. It is also distinct from the genus Squamarina by the Lecanora-type ascus and the strongly gelatinised lower cortex. This species could belong to a genus separate from Lecanora s. str. and closely related to the genera Rhizoplaca and Protoparmeliopsis, but as only one species from this group was included here, further exploration is needed in the future and we prefer to retain this species in Lecanora here. The remaining two species, Squamarina kansuensis and S. oleosa, proved to belong in Squamarina. Squamarina kansuensis is sister to S. lentigera, but differs in the larger thallus and the presence of psoromic and 2’-O-demethylpsoromic acids. Squamarina oleosa is a basal clade of the genus, which is close to the species S. cartilaginea (With.) P. James and S. gypsacea.

We revised the previously reported ascus structure for the two sections of Squamarina (Haugan and Timdal 1992; Hertel and Rambold 1988) and verified that the species in sect. Squamarina display a Porpidia -type ascus and the species in sect. Petroplaca form a Lecanora-type ascus. Our phylogenetic analyses, containing the type species of the two sections, S. callichroa and S. gypsacea, were in accordance with the ascus type: the sect. Squamarina is close to the genus Stereocaulon (Schreb.) Schrad., which also has a Porpidia-type ascus (Högnabba 2006); section Petroplaca is nested within the genus Rhizoplaca having a Lecanora-type ascus. Therefore, we suggest excluding the section Petroplaca from the genus Squamarina and recircumscribe this genus as follows: thallus saxicolous or terricolous, squamulose, placodioid or subfoliose, squamules or lobes dispersed, continuous to irregularly overlapping, very thick, usually with a white, thickened and slightly upturned marginal rim; upper surface white, yellowish-green, grey green to olive green, smooth to strongly cracked and wrinkled; lower surface white, pale brown to blackish-brown, well defined but without cortex; thallus section with well-differentiated upper cortex, algae layer and medulla; upper cortex with pale brown granules, turning colourless in potassium hydroxide (KOH); algal layer continuous; medulla very thick, filled with grey calcium oxalate crystals that become needle shaped after treatment with 25% sulphuric acid (H2SO4); apothecia lecanorine type, algal layer usually absent from the margin and only present under hypothecium, rarely biatorine type because of the strong convex disc; disc light yellow, yellow, pale brown to reddish-brown, pruinose or not; ascus narrowly clavate, Porpidia-type, 8-spored; ascospores colourless, ellipsoid to subfusiform, non-septate; pycnidia yellowish-brown, conidia filiform, curved; usnic acid always present and psoromic acid also present in most species.

Taxonomy

Lobothallia semisterilis (H. Magn.) Y. Y. Zhang, comb. nov.

MycoBank No: 832199
Fig. 1A–E

Lecanora semisterilis H. Magn., Lichens from Central Asia 1: 123–124 (1940) (Basionym). ≡ Squamarina semisterilis (H. Magn.) J.C. Wei, Enumeration of Lichens in China: 232 (1991). Type: China, Gansu Province, 2450–2600 m elev., on soil, 1931, Birger Bohlin 38L (S–Holotype!).

Description

Thallus to 5 cm across, areolate centrally, with irregularly elongate lobes at the margin, closely to loosely attached to soil; areoles angular, plane to slightly convex, continuous to crowed, ca. 1 mm across; marginal lobes ca. 1 mm wide and 2–3 mm long; upper surface white to grey, pruinose, the pruina on the marginal lobes becoming granular; lower surface white, attached to soil directly with medullary hyphae. Upper cortex colourless with pale brown upper part, 22–55 μm high; epinecral layer colourless, 10–20 μm high; algal layer ca. 95 μm high, not continuous, the interval between different groups of algae 16–32 μm wide; medulla filled with grey granules, lower cortex lacking.

Apothecia rounded, sessile, constricted at the base, up to 2 mm in diam.; disc plane to slightly convex, blackish-brown, non-pruinose; thalline margin entire, concolorous with thallus; hymenium colourless, ca. 60 μm high; subhymenium and hypothecium colourless, I + blue; epihymenium consisting of brown granules, ca. 15 μm high; paraphyses simple, slightly thickened at the apex, ca. 3 μm in diam.; asci Aspicilia-type, 8-spored; ascospores colourless, ellipsoid, 9–13 × 5–9 μm.

Pycnidia prominent, sometimes protruding from the thallus-like apothecia, with blackish-brown ostioles, numerous, 0.1–0.4 mm across; conidia bacilliform, 5.5–6.5 × ca. 1 μm.

Figure 1. 

Lobothallia semisterilis (KUN-L 18-59656). A Habit B apothecial anatomy (LCB) C ascus and spores (Lugol’s) D section of pycnidia (LCB) E section of thallus (LCB). Scale bars: 100 μm (B, E); 5 μm (C); 20 μm (D).

Chemistry

Upper cortex K + red, C-, P-, medulla K + red, C-, P + yellow; norstictic acid.

Ecology and distribution

Growing on soil in very dry habitats at elevations of 1760–3151 m. This species was previously only known from Gansu Prov. and is reported here as new to Qinghai Prov., China.

Notes

The holotype consists of numerous fragments on soil, without apothecia but numerous pycnidia. This species was originally described as a Lecanora by Magnusson (1940) and transferred to Squamarina by Wei (1991). We initially treated our materials as “S. semisterilis” since their morphology was identical with the holotype, which is characterised by the pruinose and lobate thallus containing norstictic acid, terricolous habit, pycnidia resembling apothecia and bacilliform conidia. We transfer this species to the genus Lobothallia, based on the phylogenetic reconstruction. Its position within this genus is supported by the lobate and slightly convex thallus, the Aspicilia-type ascus, the bacilliform conidia and the absence of usnic acid.

The genus Lobothallia is a small genus mainly growing on rocks, containing twelve species (Kou et al. 2013; Lücking et al. 2017). We added eight of these species as intergroups to assess the phylogenetic position of Lobothallia semisterilis in the genus. The results show that Lobothallia semisterilis is close to L. alphoplaca, L. melanaspis and L. praeradiosa in the phylogeny (Fig. 2). However, L. alphoplaca differs in the epruinose thallus and the presence of constictic and stictic acids, L. melanaspis differs in the saxicolous habit and the distinctly rosette-forming thallus. L. praeradiosa can be distinguished by the epruinose and green grey to orange brown thallus (Galloway and Ledingham 2012; Kou et al. 2013). Lobothallia pruinosa Kou & Q. Ren is similar to L. semisterilis in having a pruinose upper surface, but differs in the saxicolous habit and the presence of constictic acid (Kou et al. 2013).

Figure 2. 

Maximum Likelihood phylogeny of the genus Lobothallia, based on nrITS. ML bootstrap value ≥ 70% and posterior probabilities ≥ 0.95 from the Bayesian analysis are given adjacent to nodes.

Rhizoplaca callichroa (Zahlbr.) Y. Y. Zhang, comb. nov.

MycoBank No: 832200
Fig. 3A–D

Lecanora callichroa Zahlbr., in Handel-Mazzetti, Symb. Sinic. 3: 172–173 (1930) (Basionym) ≡ Squamarina callichroa (Zahlbr.) Poelt, Mitt. Bot. Staatssamml., München 1–20: 527 (1958). Type: China, Yunnan Province, 2100 m elev., on rock, 1914, Heinrich Frh. von Handel-Mazzetti 35 (W–Isotype!)

Description

Thallus saxicolous, to 4 cm across, squamulose to placodioid; squamules pruinose on the edges, more or less umbilicate when young; central squamules scattered to continuous, closely attached to the substrate, 1–2 mm across; marginal squamules larger than those in the centre, 2–4 mm across, with 1–2 mm free margin; upper surface yellowish-brown, smooth, plane to slightly convex; lower surface pale to pale brown, without rhizinose strands. Upper cortex filled with yellowish-brown granules dissolving in KOH, ca. 32 μm high; epinecral layer also filled with yellowish-brown granules, ca. 15 μm; algal layer continuous, 64–80 μm high; medulla thick, filled with grey to pale brown granules; lower cortex of free margin poorly developed, non-gelatinised, ca. 30 μm.

Apothecia lecanorine, laminal, dispersed, sessile, becoming slightly constricted at the base, round to irregular, 0.5–1.5 mm; disc orange, covered with pale pruina, plane to slightly convex; thalline margin entire and thick when young, becoming thin and occasionally flexuose with age; hymenium with scattered orange granules, I+ blue, ca. 80 μm high; thalline margin with evenly thick cortex, ca. 26 μm thick; epihymenium yellowish-brown, ca. 10 μm high; subhymenium and hypothecium colourless; ascus Lecanora-type, 8-spored; paraphyses slightly branched, without anastomoses; ascospores subfusiform to ellipsoid, 9.5–13.5 × 6–9 μm. Pycnidia immersed in the thallus, with pale brown ostioles; conidia filiform, straight to slightly curved, 19–26 × ca. 0.7 μm.

Figure 3. 

Rhizoplaca callichroa (A–D KUN-L 19-62900): A habit B apothecial anatomy (LCB) C ascus and spores (Lugol’s) D section of pycnidia (LCB). R. pachyphylla (E–H KUN-L 18-59446): E habit F section of apothecia G ascus and spores (LCB) H section of thallus (LCB). Scale bars: 100 μm (B, F, H); 10 μm (C, G); 20 μm (D).

Chemistry

Upper cortex K-, C-, P-, medulla K + yellow, C-, P-; usnic and placodiolic acids.

Ecology and distribution

Growing on rock in arid environments at elevations of 984–2100 m. Previously only known from Yunnan Prov., here reported as new to Sichuan Prov., China.

Notes

The isotype grows on quartzitic rock ca. 2 cm across, containing several intact apothecia. The spore size of “Squamarina callichroa”, given in the protologue, is 15–20 × 8–9 μm (Zahlbruckner 1930); however, Poelt (1958) measured the spore size of the type material as 11–12 × 8–9 μm. Our measurements of the freshly collected materials, 9.5–13.5 × 6–9 μm, are in accordance with Poelt’s results and the other characteristics, elevation and locality of our collections are more or less identical with the isotype. We did not find any specimens around the type locality having those long ascospores as in the description of the protologue. Therefore, we treat our specimens as “Squamarina callichroa” .This species was originally described as a Lecanora by Zahlbruckner (1930) and transferred to Squamarina as the type species of the section Petroplaca by Poelt (1958). We transfer this species to the genus Rhizoplaca, primarily based on its nested position within the R. chrysoleuca group in the phylogeny (Fig. 4) and also based on the orange apothecia, the Lecanora-type ascus and the presence of usnic and placodiolic acids. The genus Rhizoplaca is a small genus containing eleven species (Lücking et al. 2017). We added nine of these species as intergroups to assess the phylogenetic position of R. callichroa in the genus. The results show that R. callichroa is sister to R. chrysoleuca and R. huashanensis J.C. Wei, which differ by the umbilicate thallus, narrower ascospores, (7)8.5–12 × 3.5–6 μm and the monophyllus thallus and black apothecia, respectively (Nash et al. 2002; Wei 1984). Rhizoplaca subdiscrepans (Nyl.) R. Sant. is similar to R. callichroa in the squamulose thallus and orange apothecia, but differs in the very convex and smaller (0.3–1 mm) squamules and the narrower ascospores 7–12 × 3.5–5 μm.

Figure 4. 

Maximum Likelihood phylogeny of the genus Rhizoplaca and related genera of Lecanoraceae, based on combined nrITS, nrLSU, RPB1, RPB2 and mtSSU. ML bootstrap value ≥ 70% and posterior probabilities ≥ 0.95 from the Bayesian analysis are given adjacent to nodes.

Specimens examined (KUN-L)

China: Sichuan Province: Huili Co., beside Jiaopingdu bridge, near to the Jinsha river, 1550 m elev., 26°18'N, 102°22'E, on rock, 2014, Li-Song Wang et al. 14-43348, 14-43357, 14-43359; Yunnan Province: Luquan Co., beside Jiaopingdu bridge, 984 m elev., 26°18'N, 102°22'E, on rock, 2014, Li-Song Wang et al. 14-43308.

Rhizoplaca pachyphylla (H. Magn.) Y. Y. Zhang, comb. nov.

MycoBank No: 832201
Fig. 3E–H

Lecanora pachyphylla H. Magn., Lichens from Central Asia 1: 120–121 (1940) (Basionym) ≡ Squamarina pachyphylla (H. Magn.) J.C. Wei, Enumeration of Lichens in China: 232 (1991).Type: China, Gansu Province, 3800–3850 m elev., on rock, 1932, Birger Bohlin (S–Holotype!).

Description

Thallus saxicolous, areolate without lobate margin, to 4 cm across, to 5 mm thick; areoles continuous, plane to slightly convex, 1–2 mm across; upper surface yellow, densely shallow rimose; lower side with thick, grey to white hypothallus. Upper cortex uneven, filled with yellowish-brown granules dissolving in KOH, 32–48 μm thick, algal layer continuous, variable in height, 80–128 μm; medulla very thick, filled with grey to pale brown granules; lower cortex lacking.

Apothecia common, usually densely grouped, irregular in shape, up to 5 mm in diam.; disc black, pruinose at the centre, plane when young, strongly concave with age; thalline margin thin and crenate, strongly bending towards inside with age; hymenium colourless, I+ blue, ca. 50 μm high; epihymenium containing yellowish-brown granules, ca. 9.5 μm high; subhymenium and hypothecium colourless; paraphyses evenly septate, simple, 2–3 μm in diam., apex more or less swollen and bluish-green, ca. 4.5 μm in diam.; ascus Lecanora-type, 8-spored; ascospores regular in shape, ellipsoid, colourless, 5.8–8 × 3–4.5 μm.

Chemistry

Upper cortex K-, C-, P-, medulla K-, C-, P-; usnic acid and traces of unknown substances.

Ecology and distribution

Growing on rock at elevations of 3291–3909 m. Only known from Gansu Prov., China.

Notes

The holotype grows on rock with Lecidea tessellata Flörke, Lecanora asiatica H. Magn. and Xanthoria elegans (Link) Th. Fr. and contains numerous apothecia.

This species was originally described as a Lecanora by Magnusson (1940) and transferred to Squamarina by Wei (1991). It is characterised by the yellowish, areolate and very thick thallus, the black lecanorine apothecia and the very small ascospores. We transfer this species to Rhizoplaca, primarily based on the phylogenetic results (Fig. 4) and also based on the yellow thallus, the large, concave apothecia with margins bending towards the inside and the Lecanora-type ascus. Rhizoplaca pachyphylla is phylogenetically closely related to R. callichroa, R. chrysoleuca and R. huashanensis, but differs in the very thick and areolate thallus without lobate margin and the very small ascospores, 5.8–8 × 3–4.5 μm. Rhizoplaca subdiscrepans is similar to R. pachyphylla in the squamulose thallus, but differs in the orange apothecia, longer ascospores, 7–12 × 3.5–4.5 μm, and the presence of pseudoplacodiolic or placodiolic acids. Rhizoplaca melanophthalma (DC.) Leuckert is also similar to the species in having black apothecia, but differs in the umbilicate thallus and the larger ascospores, 6.5–12 × 4–7 μm.

Specimens examined (KUN-L)

China: Gansu Province: Shubei Co., Mengke Glacier, 3942 m elev., 39°12'N, 95°23'E, on rock, 2018, Li-Song Wang et al. 18-59446, 18-59466, 3785 m elev., on rock, 2018, Li-Song Wang et al. 18-59482; Yumen Ci., Yuerhong Vi., 3291 m elev., 39°50'N, 96°45'E, on rock, 2018, Li-Song Wang et al. 18-59560, 18-59561.

Lecanora chondroderma Zahlbr., in Handel-Mazzetti, Symb. Sinic. 3: 174 (1930).

Fig. 5A, B

Squamarina chondroderma (Zahlbr.) J.C. Wei, Enumeration of Lichens in China: 231 (1991).Type: China, Sichuan Province, 3600–3900 m elev., 1914, Heinrich Frh. von Handel-Mazzetti 497 (W–holotype!)

Description

Thallus to 6 cm across, squamulose or lobate, growing on moss over rock or on the meadow; squamules 0.5–2 mm across, convex, continuous to slightly overlapped; marginal lobes branched, convex, 0.5–2 mm wide, 2–4 mm long; the apex of squamules and lobes rounded, bent downwards; upper surface smooth, pale green to straw, covered by white pruina; lower surface pale to dark brown in the centre and white to pale brown at the margin; rhizinose strands blackish-brown. Upper cortex very thin, ca. 16 μm, filled with yellowish-brown granules dissolving in KOH; algal layer continuous, 48–60 μm thick, medulla filled with grey to pale brown granules, 129–161 μm high, medullary hyphae very loose, more or less hollow in centre; lower cortex well separated from medulla, evenly thick with strongly gelatinised and anticlinally arranged hyphae, ca. 80 μm thick, colourless, hyphae at lower part brown. Apothecia lecanorine, sessile, with constricted base, rounded, scattered or in small groups, up to 3 mm in diam.; disc pruinose, reddish to dark brown, slightly concave when young, slightly convex with age; thalline margin concolorous with thallus, entire to flexuose, forming a well-delimited cortex consisting of strongly gelatinised and anticlinally arranged hyphae; hymenium colourless, 58–80 μm; epihymenium filled with yellowish-brown granules, 10–15 μm; paraphyses simple, evenly septate; ascus Lecanora-type, 8-spored; ascospores colourless, ellipsoid to slightly ovoid, 7–13 × 6.5–9 μm.

Figure 5. 

Lecanora chondroderma (A, B KUN-L 18-60317): A habit B apothecial anatomy (LCB) and ascospores (water). Squamarina kansuensis (C–G KUN-L 18-59601): C habit D apothecial anatomy (LCB) E ascus and ascospores (LCB) F apical structure of ascus (Lugol’s) G section of thallus (LCB). S. oleosa (H, I KUN-L 09−30043): H habit I ascus and ascospores (water). Scale bars: 100 μm (B-apothecia, D); 5 μm (B-ascospores, F); 10 μm (E); 20 μm (G); 25 μm (I).

Chemistry

Upper cortex K-, C-, P + yellow, medulla K+ yellow, C-, P-; usnic acid and zeorin present in each sample, placodiolic and isousnic acids also present in most samples.

Ecology and distribution

Growing on moss over rock or in meadow at 3600–4968 m elevation in the alpine zone. Worldwide distribution: China, India and Nepal. China: Sichuan Prov., reported here as new to Yunnan and Xizang provinces.

Notes

The holotype of Lecanora chondroderma consists of several fragments, containing numerous apothecia.

Lecanora chondroderma was originally described by Zahlbruckner (1930) and transferred to Squamarina by Wei (1991). We transfer this species back to Lecanora temporarily because of its Lecanora-type ascus and phylogenetic position being closely related to the genera Rhizoplaca and Protoparmeliopsis (Fig. 4). Although Lecanora chondroderma is highly supported as a basal clade of the genus Rhizoplaca in our topology, it differs in dwelling on moss and meadow and having numerous rhizinose strands. Given that there are still many taxa of Lecanora which have not been included in our analyses and the phylogenetic relationships between Rhizoplaca and its related genera have still not been thoroughly resolved, we prefer to retain this species in Lecanora temporarily, rather than treat it as Rhizoplaca. Lecanora chondroderma is only known from the Himalayan region at elevations between 3600–4968 m. The morphology of the species varies amongst localities, with samples growing on moss over rock in Yunnan and Sichuan provinces, having broad (1–2 mm) and pale green lobes and samples from meadows at higher altitudes in Xizang Prov. developing narrower (0.5–1 mm) and more branched lobes with a yellowish appearance. These populations, however, share a pruinose thallus, convex lobes with rounded and downwards bent apices, a loose medulla, a well-delimited cortex of the thalline margin and lower cortex and the presence of usnic acid and zeorin.

Lecanora geophila (Th. Fr.) Poelt is similar to L. chondroderma in morphology, chemistry and habitat, whereas the former forms a yellowish crustose, squamulose to placodioid thallus with loboid projections or phyllidia or terete lobes and epruinose, pale, flat to convex apothecia, including usnic acid, zeorin and methylplacodiolic acid (Brodo 1981; Obermayer and Kantvilas 2003); the latter presents a totally pruinose, squamulose to lobate thallus that never forms phyllidia and terete lobes, pruinose, reddish-brown to black apothecia, numerous rhizinose strands and absence of methylplacodiolic acid.

Specimens examined (all in KUN-L unless otherwise noted)

China: Sichuan Province: 4650 m elev., 1915, Heinr. Frh. & Handel-Mazzetti 1353 (W). Yunnan Province: Shangri-La Co., Mt. Hong Shan, 4470 m elev., 28°07'N, 99°54'E, on soil, 2018, Li-Song Wang et al. 18-60317; Luquan Co., Mt. Jiaozi Snow, 4000 m elev., 26°05'N, 102°51'E, on moss over rock, 2016, Li-Song Wang et al. 16-54907; Lijiang Co., Mt. Laojunshan, 4036 m elev., 26°37'N, 99°44'E, on rock, 2017, Li-Song Wang et al. 17-55591. Xizang Province: Linzhou Co., Mt. Qiala, 4830 m elev., 30°06'N, 91°16'E, on the meadow, 2016, Li-Song Wang et al. 16-53527; Zuogong Co., on the way from Rumei to Zuogong, 4968 m elev., 29°43'N, 98°01'E, on the meadow, 2016, Li-Song Wang et al. 16-52925, 16-53079, on the meadow, 2016, Li-Song Wang et al. 16-52931.

Squamarina kansuensis (H. Magn.) Poelt

Fig. 5C–G

Lecanora kansuensis H. Magn., Lichens from Central Asia 1: 116–117 (1940). Type: China, Gansu Province, 1500–1700 m elev., on soil, 1930, Birger Bohlin 202 (S–Holotype!) (Basionym)

Description

Thallus terricolous, loosely to tightly adnate on soil, irregular to radiate in outline and with elongate marginal lobes, up to 10 cm in diam.; lobes 2–4(5) mm long, 1–2(3) mm wide, 0.2–0.4 mm thick, with white, thickened and slightly upturned edges, more or less overlapping; upper surface greenish to straw, pruinose and strongly cracked at least in the centre of the thallus; lower surface well delimited, milk-white to pale, without rhizines, margins usually containing sparse white tomentum. Upper cortex filled with yellowish-brown granules, turning colourless in KOH, 26–32 μm thick; epinecral layer grey to brown, 5–15 μm thick; algal layer continuous, well delimited, ca. 50 μm high; medulla grey, filled with calcium oxalate crystals; lower cortex lacking.

Apothecia frequent, rounded, single or in small groups, usually less than 2 mm in diam. Disc pale brown to reddish-brown, slightly concave to flat when young, usually becoming strongly convex with age. Thalline margin distinctive when young and disappearing with age. Hymenium colourless, I + blue, ca. 65 μm high; epihymenium yellowish-brown turning colourless in KOH, ca. 12.5 μm high; thalline margin with evenly thick cortex filled with grey granules; paraphyses septate, ca. 2.5 μm in diam.; hypothecium colourless, 75–87 μm high; algal layer below hypothecium continuous, 62–87 μm high; ascus Porpidia-type, 8-spored; ascospores colourless, ellipsoid to slightly fusiform, variable in size and shape even within one ascus, 7.5–15 × 5–7.5 μm.

Chemistry

Upper cortex K-, C-, P-, medulla K-, C-, P+ yellow; isousnic, usnic, psoromic and 2’-O-demethylpsoromic acids.

Ecology and distribution

Growing on soil at 1310–4730 m of elevation. Previously only known from Gansu Prov. and reported here as new to Neimenggu, Ningxia, Sichuan, Xizang, Xinjiang and Yunnan provinces, China.

Notes

The holotype consists of several small fragments on soil, bearing a single small apothecium. This species was originally described as a Lecanora by Magnusson (1940) and transferred to Squamarina by Poelt (1958). It is characterised by the pruinose, greenish- to straw-coloured thallus, lobes with white, thickened and slightly upturned edges, exposing a milk-white to pale lower surface, without rhizines and the presence of psoromic and 2’-O-demethypsoromic acids. This species is very common in the deserts and alpine zones of China. In desert regions, the thallus is usually irregular in outline with wider lobes and becomes rosette-like with narrower lobes when growing in the alpine zone.

The genus Squamarina (= S. sect. Squamarina) includes eleven species (Poelt 1958) and there are three species with sequences in GenBank. We integrated the data from GenBank with the newly-produced data here to reconstruct the phylogeny of the genus Squamarina to assess the phylogenetic position of the species S. kansuensis (Fig. 6). The results show that S. kansuensis is a sister species to S. lentigera which, in turn, is also very similar in morphology, but differs in the larger thallus and by containing psoromic and 2’-O-demethypsoromic acids. Squamarina nivalis Frey & Poelt and S. provincialis Clauzade & Poelt are similar to S. kansuensis in having a strongly white pruinose thallus; however, S. nivalis differs in the smaller thallus, ca. 2 cm, not cracked upper surface, the apices of lobes bent downwards and the absence of psoromic acid; S. provincialis differs in the continuous but never overlapped lobes, the absence of the white thickened edges of lobes and the presence of atranorin. So far, the two species, S. nivalis and S. provincialis, are only known from very restricted places from Europe.

Figure 6. 

Maximum Likelihood phylogeny of the genus Squamarina and related genera, based on nrLSU. ML bootstrap value ≥ 70% and posterior probabilities ≥ 0.95 from the Bayesian analysis are given adjacent to nodes.

Specimens examined (all in KUN-L unless otherwise noted)

China: Gansu Province: Jiayuguan, 1500 m–1700 m elev., 1930, Briger Bohlin, S-L60805 (S); Yumen Ci., Moshan National Geological Park, 1760 m elev., 39°57'N, 97°14'E, on soil, 2018, Li-Song Wang et al. 18-59601; Sunan Co., Binggou Danxia landform Park, 1970 m elev., 38°56'N, 99°50'E, on soil, 2018, Li-Song Wang et al. 18-59658; Ningxia Province: Mt. Helanshan, 38°40'N, 1310 m elev., 105°46'E, on soil, 2014,Dong-Ling Niuet al. 14-09-1429 (NXAC); Qinghai Province: Wulan Co., Gobi desert along the way from Chaka to Wulan, 3151 m elev., 36°52'N, 98°55'E, on soil, 2018, Li-Song Wang et al. 18-59260, along the way from Wulan to Delingha, 3039 m elev., 36°59'N, 98°12'E, on soil, 2018, Li-Song Wang et al. 18-59274, 18-59306; Delingha Ci., Chayegou Station, 2974 m elev., 37°23'N, 96°37'E, on soil, 2018, Li-Song Wang et al. 18-59344, 18-59343. Sichuan Province: Derong Co., 1960 m elev., 28°12'N, 99°20'E, on soil, 2009, Li-Song Wang & Wang Jue 09-31112, 09-31118; Xizang Province: Linzhou Co., 3780 m elev., 29°54'N, 91°14'E, on soil, 2016, Li-Song Wang et al. 16-54052; Xinjiang Province: A-ke-tao Co., Oytagh observation zone, 2850 m elev., 38°54'N, 75°14'E, on soil, 2013, Hurnisa Shahidin et al. 20139103; Yunnan Province: Deqin Co., 2110 m elev., 28°13'N, 99°19'E, on soil, 2012, Li-Song Wang et al. 12-34756. Neimenggu Province: Beli-miao, 41°30'N, 110°10'E, on soil, 1929, Briger Bohlin, S-F304837 (S).

Squamarina oleosa (Zahlbr.) Poelt

Fig. 5H, I

Lecanora oleosa Zahlbr., in Handel-Mazzetti, Symb. Sinic. 3: 175 (1930) (Basionym) Type: China, Yunnan Province, Lijiang Co., Mt. Yulongxueshan, on rock, 1914, Heinrich Frh. von Handel-Mazetti 3576 (W–holotype!)

Description

Thallus placodioid to subfoliose, rather closely attached to calcareous rocks, olive-green turning to yellowish-brown in the herbarium, up to 8 cm across and 5 mm high in the centre; lobes 2–4 mm long, 1.5–2.5 mm wide, ca. 1 mm thick, apices usually detached from the substrate with a white thickened edge; upper surface pruinose at least on the margins, matt to somewhat shiny, centrally cracked and faveolate-wrinkled, strongly convex, giving the thallus centre a bullate appearance, the base of the bullae carbonised, black; lower surface covered with pale brown to blackish-brown pulvinate hyphae, with sparse to numerous rhizinose strands; rhizinose strands brown to black, irregularly branched, up to 5 mm long. Upper cortex filled with yellowish-brown granules, turning colourless in KOH, 62–75 μm high, without epinecral; algal layer continuous, 65–70 μm thick; medulla filled with grey crystals of calcium oxalate and brick-red hyphae in lower part; lower cortex lacking.

Apothecia common but not abundant, laminal, scattered to slightly grouped, up to 4 mm in diam.; disc concave, plane to convex, light yellow, covered by yellowish pruina; thalline margin pruinose or not, darker than thallus, shiny, entire and distinctive when young, excluded with age. Hymenium 75–85 μm high, hyaline, I+ blue; epihymenium filled with yellowish-brown granules, not disperse into hymenium, turning colourless in KOH, 5–12.5 μm high; thalline margin without algae in the upper part, cortex filled with yellowish-brown granules, 112–125 μm thick; paraphyses septate, tips not swollen; hypothecium colourless, 100–162 μm thick, with pale brown granules forming a narrow line; algal layer below hypothecium continuous, 50–75 μm thick; ascus Porpidia-type, 8-spored. Ascospores ellipsoid to subfusiform, 15–20 × 5–7 μm. Pycnidia rare and small, ostioles yellow to yellowish-brown, conidia colourless, filiform, curved, 15–22.5 × ca. 0.7 μm.

Chemistry

Upper cortex K-, C-, P-, medulla K-, C-, P+ yellow; usnic, psoromic and 2’-O-demethylpsoromic acids.

Ecology and distribution

Growing on rock at elevations of 2623–3440 m. Only known from Yunnan Prov., China.

Notes

The holotype grows on calcareous rock and bears only one apothecium.

This species was originally described as a Lecanora by Zahlbruckner (1930) and transferred to Squamarina by Poelt (1958). It is characterised by the thick, olive-green, placodioid to subfoliose thallus, yellowish apothecia covered with yellow pruina, the ellipsoid to subfusiform ascospores and the filiform, curved conidia. This species is the most basal clade in our reconstruction of the genus and it is close to S. cartilaginea and S. gypsacea (Fig. 6); however, S. cartilaginea differs in the non-pruinose, yellowish- to reddish-brown apothecia, smaller ascospores 10–14 × 4–6 μm and S. gypsacea differs in the yellowish-green, squamulose thallus, the very large and thick squamules that adnate to the substratum only by the central part and the larger apothecia (up to 1 cm). Squamarina kansuensis and S. lentigera can be distinguished from this species by the strongly white pruinose thallus, thinner lobes (< 0.5 mm) and smaller (< 2 mm) apothecia with non-pruinose and reddish-brown disc.

Specimens examined (all in KUN-L unless otherwise noted)

China: Yunnan Province: Lijiang Co., 3440 m elev., on rock, 2009, Li-Song Wang & Wang Jue 09-30034, Yulong Snow Mt., 26°56'N, 100°12'E, 2623 m elev., on calcareous rock, 2019, Li-Song Wang & Yan-yun Zhang 19-66398, 19-66399, 19-66401, 19-66402, 19-66404.

Squamarina gypsacea (O)

Greece: Corfu, hill above Troumpetas, 420 m elev., 39°74'N, 19°86'E, on exposed limestone outcrops, 2014, Rui, S. & Timdal, E., O-L-196249, Sokrati – Zigos road, 370 m elev., 39°72'N, 19°80'E, on rather shady limestone boulders in olive groove, 2014, Rui, S. & Timdal, E., O-L-196255; Kavalla, Thassos, along dirt road from Maries to Theologos, near Vatos, 590 m elev., 40°70'N, 24°66'E, on E-facing limestone wall in/above steep pine forest, 2000, Rui, S. & Timdal, E., O-L-59266. Spain: Alicante, between Callosa de Ensarria and Confrides, 260 m elev., 38°68'N, -0°21'E, 1985, Timdal, E., O-L-16444.

Acknowledgements

We would like to express our deep thanks to Dr. Arne Anderberg from the Swedish Museum of Natural History (S) and the curator of the Vienna Museum of Natural History (W) for the loan of specimens. This study was supported by grants from the National Natural Science Foundation of China (Nos. 31660007, 31970022, 31670028), Flora Lichenum Sinicorum (31750001), Youth Innovation Promotion Association CAS, Biological Resources Programme, Chinese Academy of Sciences (KFJ-BRP-017-23) and China Scholarship Council. This work benefitted from the sharing of expertise within the DFG priority programme SPP 1991 “Taxon-Omics” and support from DFG grant PR567/19-1 to CP.

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