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The genus Bulbothrix (Parmeliaceae) in China

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The morphology, chemistry and phylogenetic relationships of Chinese populations of Bulbothrix are described. Nine species, including two new species B. mammillaria Y. Y. Zhang & Li S. Wang sp. nov. and B. lacinia Y. Y. Zhang & Li S. Wang sp. nov., and two newly recorded for the flora, B. scortella and B. meizospora , are reported. Bulbothrix mammillaria can be recognized by the sparse cilia that are reduced to a bulbate structure and the broad lobes (3–11 mm). Bulbothrix lacinia differs from other species of the genus by dark brown, spherical to short-cylindrical isidia and common lacinulae on the upper surface. Phylogenetic relationships of currently known ITS sequences from Bulbothrix were inferred to assess the affinities of the new species. A key to all known species from China is presented.
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The Lichenologist 48(2): 121133 (2016) © British Lichen Society, 2016
doi:10.1017/S0024282915000560
The genus Bulbothrix (Parmeliaceae) in China
Yan Yun ZHANG, Xin Yu WANG, Dong LIU, Hai Xia SHI, Xin YE,
Mei Xia YANG and Li Song WANG
Abstract: The morphology, chemistry and phylogenetic relationships of Chinese populations of
Bulbothrix are described. Nine species, including two new species B. mammillaria Y. Y. Zhang & Li S.
Wang sp. nov. and B. lacinia Y. Y. Zhang & Li S. Wang sp. nov., and two newly recorded for the ora,
B. scortella and B. meizospora, are reported. Bulbothrix mammillaria can be recognized by the sparse cilia
that are reduced to a bulbate structure and the broad lobes (311 mm). Bulbothrix lacinia differs from
other species of the genus by dark brown, spherical to short-cylindrical isidia and common lacinulae on
the upper surface. Phylogenetic relationships of currently known ITS sequences from Bulbothrix were
inferred to assess the afnities of the new species. A key to all known species from China is presented.
Key words: bulbate cilia, diversity, lichenized fungi, taxonomy
Accepted for publication 16 November 2015
Introduction
Hale (1974) erected the genus Bulbothrix as a
segregate from Parmelia Ach. to accommodate
species with marginal bulbate cilia; the cilia
can be simple or branched. Bulbothrix is
further characterized by laciniate lobes,
cortical atranorin, hyaline unicellular, ellipsoid
to bicornute ascospores, and bacilliform to
bifusiform conidia (Hale 1976; Elix 1993;
Benatti 2014). Bulbate cilia also occur in
Relicina Hale, which differs, however, in the
presence of usnic acid. Although the two
genera exhibit similar morphologies, they are
quite distinct as Bulbothrix belongs to the
Parmelina-clade, and Relicina to the Parmelia-
clade (Crespo et al. 2010). As currently
circumscribed, Bulbothrix is a polyphyletic
genus composed of two clades. The rst, the
B. isidiza group, is sister to Parmelinella Elix &
Hale (Divakar et al. 2006, 2010; Masson et al.
2015) which leads to this clade either nesting
in the genus Parmelinella or being a small
genus that contains salazinic acid (Benatti
2013; Kirika et al. 2015). The second clade
is the Bulbothrix goebelii (Zenker) Hale
group, and the type species of Bulbothrix,
B. semilunata (Lynge) Hale, may belong in
this clade (Kirika et al. 2015) on account of its
distribution and morphological characteristics.
Twenty-nine species of Bulbothrix were
accepted by Hale (1976). This number has
grown to 61 (Bungartz et al. 2013; Benatti
2015; Masson et al. 2015), with many species
from Brazil, which may be the centre of
diversity for Bulbothrix (Spielmann &
Marcelli 2008; Benatti 2012a). The genus is
widespread in tropical and subtropical
regions and reaches its highest diversity in
semi-arid woodlands and secondary forests
Y. Y. Zhang and M. X. Yang: Key Laboratory for Plant
Diversity and Biogeography of East Asia, Kunming
Institute of Botany, Chinese Academy of Sciences,
Heilongtan, Kunming, Yunnan 650201, China;
University of Chinese Academy of Sciences, Yuquanlu,
Beijing, 100049, China.
X. Y. Wang, H. X. Shi and L. S. Wang (corresponding
author): Key Laboratory for Plant Diversity and Biogeo-
graphy of East Asia, Kunming Institute of Botany, Chinese
Academy of Sciences, Heilongtan, Kunming, Yunnan
650201, China. Email: wanglisong@mail.kib.ac.cn
D. Liu: Key Laboratory for Plant Diversity and Biogeo-
graphy of East Asia, Kunming Institute of Botany,
Chinese Academy of Sciences, Heilongtan, Kunming,
Yunnan 650201, China; Korean Lichen Research
Institute (KoLRI), Sunchon National University,
255 Jungang-Ro, Sunchon, Korea.
X. Ye: Yunnan University of Traditional Chinese
Medicine, Chenggong, Kunming, Yunnan 650500,
China.
(Hale 1976; Marcano et al. 1996). Species
concepts within the genus rely primarily on the
branching patterns of cilia and rhizines,
presence or absence of isidia, maculate or
emaculate upper cortex, colour of the lower
surface and secondary chemistry in the medulla.
Seven species of Bulbothrix have been
reported from China: B. goebelii,B. isidiza
(Nyl.) Hale, B. setschwanensis (Zahlbr.) Hale,
B. tabacina (Mont. & Bosch) Hale, B. asiatica
Y. Y. Zhang & Li S. Wang, B. subscortea
(Asahina) Marcelli & Benatti and B. yunnana
(Wang et al. 2000; Chen et al. 2009; Zhang
et al. 2014). However, Bulbothrix yunnana was
transferred to Parmotrema as P. yunnanum
(Sheng L. Wang et al.) Marcelli & Benatti
because the cilia have an enlarged base instead
of being truly bulbate (Benatti & Marcelli
2010).
In this study, two new species are described
and two species are newly recorded, resulting
in a total of nine species of Bulbothrix occur-
ring in China. Morphological and chemical
descriptions, phylogenetic analyses together
with a key to these species are presented.
Materials and Methods
Morphological and chemical studies
Approximately 400 specimens from the lichen herbar-
ium of the Kunming Institute of Botany (KUN-L) and the
Chinese Academy of Sciences were examined. Morpho-
logical characters were studied using standard stereoscopy
and light microscopy. We sectioned apothecia, thalli,
pycnidia and cilia with a razor blade under a NIKON
SMZ745T dissecting microscope, then examined and
measured traits using a micrometer under a NIKON
Eclipse Ci-S microscope.Size of the thallus, apothecia and
lobes are based on measurements for each specimen, and
ascospore dimensions reect ten measurements from a
single apothecium per specimen. Size is represented by the
range between the smallest and largest values. The
chemical composition of each specimen was assessed
using spot reactions and thin-layer chromatography with
solvent system C (Orange et al. 2001).
DNA extraction
Total genomic DNA was extracted from dry herbar-
ium or fresh specimens using AxyPrep Multisource
Genomic DNA Miniprep Kit 50prep (Qiagen)
according to the manufacturers instructions. The fungal
internal transcribed spacer region (ITS) of the rDNA
repeat was amplied via polymerase chain reaction
(PCR) using the primers ITS1-LM (Myllys et al. 1999)
and ITS2-KL (Lohtander et al. 1998). Amplications
were performed in a 25 μl volume comprising 12·5µlof
MasterMix (TaqDNA Polymerase, 0·1 units/µl
1
;
4 mM MgCl
2
;0·4 nMdNTPs; produced by Aidlab Bio-
technologies Co., Ltd), 0·4µl of each primer, 11 µl
ddH
2
O, and 0·7µl of DNA. PCR amplications were
performed using the following temperature prole:
initial denaturation at 94 °C for 3 min, 30 cycles each
composed of 94 °C for 40 s, 50 °C for 1 min, 72 °C for
1·5 min, and a nal extension at 72 °C for 7min. PCR
products were sequenced using amplication primers by
the company Sangon Biotechnology (Shanghai, China).
Sequence alignments
Sequence fragments obtained were assembled with
SeqMan 7.0 (DNAStar) and manually adjusted. DNA
sequences were aligned with MAFFT version 7 with the
L-INS-I alignment algorithm (Katoh et al. 2005) using
the web server (http://mafft.cbrc.jp/alignment/server/
index.html) with all parameters set to default values.
Phylogenetic analyses
The ITS matrix was analyzed using a maximum
likelihood (ML) optimality criterion and a Bayesian (BI)
Markov chain Monte Carlo approach (B\MCMC), with
Myelochroa aurulenta (Tuck.) Elix & Hale selected as
outgroup.
ML analyses were performed using RAxML7.0.4
(Stamatakis 2006), implementing default settings.
Support values were inferred from the 70% majority-
rule tree of all saved trees obtained from 1000 non-
parametric bootstrap replicates.
The Bayesian analyses were performed using MrBayes
v3.1.2 (Huelsenbeck & Ronquist 2001), with 2 000 000
generations and four incrementally heated chains.
MrModeltest 2.3 (Nylander 2005) was used in
conjunction with PAUP* (Swofford 2003) to estimate
the best-tting substitution model (i.e., GTR + I + G)
based on the AIC by jModelTest 3.7 (Posada 2008).
MCMC started from a random tree and was sampled
every 1000th generation, with the rst 10% of trees
discarded as burn-in. The remaining trees were used to
generate a majority-rule consensus tree with posterior
probability (PP), inferred from consensus values, 0·95
considered as strongly supported. We used the program
Tracer v1. 6 (Rambaut & Drummond 2003) to ensure
that stationarity was achieved by checking whether the
log-likelihood values of sample points reached a stable
equilibrium. Phylogenetic trees were visualized using the
program FigTree 1.4.0 (Rambaut 2012).
Results
The ITS matrix contained a total of 35
sequences, including 12 that were newly
generated (Table 1). The ITS topologies
122 THE LICHENOLOGIST Vol. 48
obtained by the maximum likelihood and
Bayesian approaches were congruent, and ML
topology was selected to represent the phylo-
genetic relationship (Fig. 1).
Two main clades that were identical to
Kirika et al. (2015) were recovered in the
phylogenetic trees. Clade 1 is characterized
by narrow lobes usually with a truncate to
subtruncate apex, branched rhizines and cilia
(dichotomously, trichotomously to irregularly,
densely branched), and the absence of
medullary substances or containing secondary
metabolites such as gyrophoric, conlensoinic,
lecanoric, lobaric acids. Clade 2 is character-
ized by broad lobes (to 11 mm) generally with
a round to subrotund to subtruncate apex,
simple rhizines and cilia, and the
presence of salazinic acid in the medulla.
The two new species, B. mammillaria
and B. lacinia, formed highly supported
clades (MLBS =100%, PP =1·0 and
MLBS =97%, PP =1·00, respectively).
Bulbothrix lacinia is sister to B. subscortea but
differs by granular to short cylindrical isidia
that are dark brown or have a dark brown
apex, and an upper surface with numerous
lacinulae; it is also close to B. setschwanensis
but differs by the presence of isidia.
Bulbothrix mammillaria is sister to B. asiatica
but the cilia of the latter are frequent along
TABLE 1. Specimen information and GenBank accession numbers for taxa used in this study. Newly obtained sequences are in bold.
Species Locality
Voucher
specimens
GenBank
number
Bulbothrix apophysata Costa Rica F 16650b DQ279481
B. asiatica 1 Cambodia: MondulKiri KUN 12-37239 KM249891
B. asiatica 2 China: Yunnan KUN 14-44427 KM285403
B. coronata South Africa MAF 13987 DQ279482
B. decurtata South Africa MAF 13988 DQ279483
B. goebelii South Africa MAF 13985 DQ279484
B. isidiza 1 Madagascar TinoRuibal: Ertz 12878 JN943847
B. isidiza 2 Madagascar BR 12878 GQ919263
B. isidiza 3 China: Yunnan KUN 12-33001 KP776573
B. isidiza 4 China: Yuanmou KUN 13-39821 KP776574
B. klementii Costa Rica F 15170a DQ279485
B. lacinia 1 China: Yunnan KUN 13-41296 KP780410
B. lacinia 2 China: Yunnan KUN 13-41301 KP776570
B. laevigatula Costa Rica F: Lücking 15045b GQ919264
B. lyngei Cambodia: PreahVihear KUN 12-37404 KM249892
B. mammillaria 1 China: Yunnan KUN 14-44233 KP776571
B. mammillaria 2 China: Yunnan KUN 13-41171 KP776572
B. mammillaria 3 China: Yunnan KUN 14-43407 KT729545
B. mammillaria 4 China: Yunnan KUN 13-40814 KT729546
B. meizospora 1 India: Uttaranchal GPGC 02-000786 AY611068
B. meizospora 2 India TinoRuibal: GPGC 02-000786? BUME351 JN943846
B. scortella 1 China: Yunnan KUN 14-44441 KP776565
B. scortella 2 China: Yunnan KUN 14-44442 KP776566
B. sensibilis 1 Rwanda Ertz 11025 GU994541
B. sensibilis 2 Rwanda BR 11025 GQ919265
B. setschwanensis 1 China: Yunnan MAF 10212 AY611069
B. setschwanensis 2 China: Yunnan KUN 13-41167 KP776567
B. setschwanensis 3 China: Yunnan KUN 13-39866 KP776568
B. subscortea 1 Cambodia: Kampot KUN 12-37479 KM249895
B. subscortea 2 Cambodia: MondulKiri KUN 12-37270 KM249897
B. sufxa Madagascar BR 12889 GQ919266
B. tabacina 1 Kenya MAF-Lich 16112 GQ919268
B. tabacina 2 Republic of the Congo MAF-Lich 16111 GQ919267
Myelochroa aurulenta Canada F. Lutzoni & J. Miądlikowska 07.02.03-3 (DUKE) JQ301701
Parmelinella wallichiana China MAF 10411 DQ279532
2016 Bulbothrix in ChinaZhang et al. 123
the lobe margins with a simple or rarely
branched apex and its lower surface is
uniformly black with a pale brown margin.
Taxonomy
New species
Bulbothrix mammillaria Y. Y. Zhang &
Li S. Wang sp. nov.
MycoBank No.: MB 812997
Similar to B. asiatica, but differs by the sparse cilia
reduced to a bulbate structure without a tapering apex to
rarely with a very short apex, shorter isidia (60360 μm),
broader lobes (311 mm), variable colour of lower
surface, broader pale brown lower marginal zone
(25 mm), and rhizines normally with white apices.
Type: China, Yunnan Prov., Yongsheng Co., Dashan
Village, on bark, 5 December 2013, L. S. Wang et al.
1341171 (KUN-L22067holotype).
(Fig. 2)
Thallus greenish grey to tan, to 10 cm
diam., submembranaceous to subcoriac-
eous; upper cortex 12·517·0μm thick, algal
layer 12·522·0μm thick, medulla 7582 μm
thick, lower cortex 7·525·0μm thick. Lobes
irregularly branched, 311 mm wide,
contiguous and crowded at the centre, very
Myelochroa aurulenta
Bulbothrix suffixa
B. klementii
B. goebelii
B. scortella 2
B. scortella 1
B. lyngei
B. coronata
B. apophysata
B. laevigatula
B. asiatica 1
B. asiatica 2
B. mammilaria 2
B. mammilaria 4
B. mammilaria 3
B. mammilaria 1
B. meizospora 1
B. meizospora 2
B. lacinia 1
B. lacinia 2
B. subscortea 2
B. subscortea 1
B. setschwanensis 3
B. setschwanensis 1
B. setschwanensis 2
B. sensibilis 2
B. sensibilis 1
B. decurtata
B. isidiza 4
B. isidiza 2
B. isidiza 1
B. isidiza 3
B. tabacina 1
B. tabacina 2
Parmelinella wallichiana
Clade 1
Clade 2
1.00/91
1.00/100
1.00/100
1.00/81
1.00/88
1.00/100
1.00/100
1.00/100
1.00/100
1.00/70
1.00/-
1.00/93 1.00/97
1.00/74
1.00/74
1.00/92
1.00/99
1.00/94
1.00/100
1.00/94
1.00/100
1.00/100
1.00/-
0.05
1.00/71
1.00/86
1.00/97
1.00/92
FIG. 1. Phylogenetic relationships of the species used in this study based on Maximum Likelihood and Bayesian
analyses of ITS sequences.
124 THE LICHENOLOGIST Vol. 48
A
B C
D E
FIG.2.Bulbothrix mammillaria habitus (holotype). A, thallus; B, isidia; C, upper surface of thallus; D, cilia reduced
to a bulbate structure; E, lower surface of thallus. Scales: A =1 cm; B =1 mm; C & E =4 mm; D =2 mm.
In colour online.
2016 Bulbothrix in ChinaZhang et al. 125
appressed, with subrotund and incised
apices. Upper surface often rough and rugose,
rarely cracked at the centre, but smooth
distally. Maculae absent. Cilia black, sparse,
bulbate without a tapering apex or rarely with
a very short apex. Isidia granular to occa-
sionally short cylindrical, with black to brown
apex, occasionally concolorous with upper
thallus surface, evenly distributed on upper
surface but lacking on distal part of lobes.
Medulla white. Lower surface usually black,
dark brown, rarely pale brown, rugose and
often with ridge-like folds, with a wide
(25 mm), papillate or smooth, pale brown,
usually shiny marginal zone. Rhizines sparse to
moderately abundant, pale brown to brown,
usually with white apices that are sometimes
branched and conglutinated, occasionally
with a bulbate base near lobe margin.
Apothecia extremely rare, only one was
found among 58 collections, and then small
and immature.
Pycnidia not seen.
Chemistry. Upper cortex K+ yellow, medulla
K+ yellow to red, C,KC; atranorin and
salazinic acid.
Ecology and distribution. Growing on bark
of Pinus spp. and Quercus spp., on branches
of Phyllanthus emblica and Cotoneaster spp.,
and on rocks at an elevation of 12743160 m
in semi-arid environments; known only from
southern China.
Comments.Bulbothrix mammillaria is
characterized by the sparse and very short
cilia which are usually reduced to a bulbate
structure, mostly wide lobes (511 mm),
rugose and tan upper surface if it is exposed to
sunlight, rhizines with normally white apices,
mostly granular isidia with a black apex, and a
black to dark, rarely pale brown lower surface,
withapalebrownmarginalzone.
Even though Bulbothrix mammillaria exhibits
a wide range of colour in the upper and lower
surfaces and lobe width, it can be recognized by
the cilia reduced to a bulbate structure. The
phylogenetic tree based on ITS sequence data
also supports the evolutionary independence of
this species. Specimens collected from the open
habitats tend to have a tan-coloured upper
surface that may be due to exposure to the sun.
Bulbothrix isidiza resembles this new
species in the short cilia and presence of
medullary salazinic acid, but differs by the
cilia commonly having a simple apex,
uniformly pale brown lower surface (Benatti
2013) and a distinctly maculate and pale
dusky grey upper surface. Bulbothrix decurtata
(Kurok.) Hale shares the granular to short
cylindrical isidia and black to occasionally
dark brown lower surface, but differs by
the sparse, reduced cilia and by its broader
lobes (311 mm). Bulbothrix subscortea can be
recognized by longer, simple to occasionally
branched cilia (200825 μm), and the con-
sistently pale brown lower surface. Bulbothrix
mammillaria differs from B. tabacina in its
rugose and often tan upper surface and the
strictly bulbate cilia.
Selected specimens examined (here, and elsewhere, all
specimens deposited in KUN-L unless otherwise stated).
China: Guangxi Prov.: Longsheng Co., 760 m, 25°47'N,
110°02'E, decayed wood, 2001, J. B. Chen et al. 20178
(HAMS-L). Sichuan Prov.: Dukou, Ji Mt., 1200 m, on
Quercus sp., 1983, L. S. Wang 8365. Yunnan Prov.:
Fumin Co., Chahe Village, 1540 m, 26°14'N, 101°25'E,
on branches, 2013, L. S. Wang et al. 1341275; near
Pudu River, 1650 m, 25°31'N, 102°36'E, on rocks, 2014,
L. S. Wang et al. 1443075; Lancang Co., Taipingzheng
Village, 1537 m, 22°36'N, 99°48'E, on bamboo, 2014,
L. S. Wang et al. 1444450; Lijiang Co., from Jinjiang to
Heqing, 3160 m, 26°38'N, 100°17'E, on bark, 2013, L. S.
Wang et al. 1340923; Luquan Co., from Luquan to
Yunlong water reservoir, 1952 m, 25°42'N, 102°29'E, on
Quercus sp., 2014, L. S. Wang et al. 1443131; Nanjian
Co., 1426m, 24°41'N, 100°04'E, on rocks, 2012, L. S.
Wang et al. 1234234; Puer, Tongxin Village, 870m, 22°
58'N, 101°03'E, on bark, 2014, L. S. Wang et al.
1444579; Yongren Co., 1543 m, 26°13'N, 101°25'E, on
rocks, 2013, L. S. Wang et al. 1340814; on bark, L. S.
Wang et al. 1340771, 1340772; Yongsheng Co.,
Dashan Village, 2200 m, 26°27'N, 101°07'E, on bran-
ches, 2013, L. S. Wang et al. 1341208, 1341169, 13
41187; Yuanmou Co., Langbapu Village, 1521m, 25°
41'N, 101°41'E, on Phyllanthus emblica,2014,L. S. Wang
et al. 1443538; Liangshan Mt., 2148 m, 25°43'N, 101°
57'E, on bark, L. S. Wang et al. 1339736, 1339823.
Bulbothrix lacinia Y. Y. Zhang &
Li S. Wang sp. nov.
MycoBank No.: MB 812998
Similar to B. subscortea (Asahina) Marcelli & Benatti,
but differs by common lacinulae on the upper surface,
126 THE LICHENOLOGIST Vol. 48
spherical to short-cylindrical isidia that are dark brown
(longer ones concolorous with thallus but with dark
brown apices) and by the narrower lobes (1·03·5 mm).
Type: China, Yunnan Prov., Chuxiong, Chahe Vil-
lage, 2013, L. S. Wang et al. 1341296 (KUN-L22192
holotype).
(Fig. 3)
Thallus pale grey-white, to 8 cm diam.,
subcoriaceous; upper cortex 1025 μm
thick, algal layer 2540 μm thick, medulla
5075 μm thick, lower cortex 7·517·5μm
thick. Lobes irregularly branched, 1·0
3·5 mm wide, imbricate, very crowded at the
centre, appressed, with plane, crenate to
subtruncate apices. Upper surface smooth and
shiny at the apices of lobes, covered with
dense isidia in the centre, commonly lacinu-
late. Maculae absent. Cilia black, simple,
moderately distributed along the margins,
with irregularly inated base, sometimes
without bulbs. Isidia spherical to short
cylindrical (90500 × 80160 μm), simple to
rarely forked, shiny, dark brown or pale grey
with dark brown apex. Medulla white. Lower
surface pale brown, smooth; marginal zone
shiny, brown, darker than centre, slightly
papillate. Rhizines brown, simple, moderately
distributed, without bulbate base.
Apothecia not seen.
Pycnidia scarce, with black ostioles, the
thallus protruding around them. Conidia
bacilliform, 5·07·5×0·75 μm.
Chemistry. Upper cortex K+ yellow,
medulla K+ yellow to red, C,KC;
atranorin and salazinic acid.
Ecology and distribution. Growing on rocks
in secondary forest in dry to semi-arid
environments; so far known only from
Yunnan Province, China.
Comments.Bulbothrix lacinia is character-
ized by the narrow and irregularly branched
lobes (1·03·5 mm), dense, dark brown,
spherical to short-cylindrical isidia, emacu-
late upper surface, simple cilia and rhizines,
irregularly inated base of cilia, pale brown
lower surface and the presence of medullary
salazinic acid.
Bulbothrix decurtata resembles B. lacinia in
terms of lobe size, saxicolous habitat, pre-
sence of isidia and medullary salazinic acid,
but differs by its very cracked upper surface,
black to occasionally dark brown lower
surface, rhizines with bulbate bases and the
greyish olive-green thallus (Benatti 2013);
Bulbothrix australiensis Hale differs by having
longer isidia (0·51·1 mm), rhizines com-
monly with a bulbate base, pycnidia usually
abundant and a corticolous habitat. Bulbo-
thrix subtabacina (Elix) Elix can be differ-
entiated by its black lower surface, branched
cilia and rhizines, maculate and cracked
upper surface, and narrower lobes 0·41·1
(1·5) mm (Benatti 2013), and B. mammil-
laria by its broader lobes (311 mm) and cilia
reduced to a bulbate structure.
Additional specimens examined. China: Yunnan Prov.:
Chuxiong State, Chahe Village, 1540 m, 26°14'N,
101°25'E, on sandstone, 2013, L. S. Wang et al.
1341301, 1341265; Fumin Co., beside Pudu River,
1650 m, 25°31'N, 102°36'E, on sandstone, 2014,
L. S. Wang et al. 1443065; Yongren Co., from Menghu
to Wanma, 1543 m, 26°13'N, 101°25'E, on sandstone,
2013, L. S. Wang et al.1340794.
New records
Bulbothrix meizospora (Nyl.) Hale
Phytologia 28(5):480 (1974); type: India, Nilgiri
Mountains (H-NYL 35107lectotype).
Bulbothrix meizospora is characterized by: a
lack of vegetative propagules; a weak to
distinctly maculate upper cortex; cilia that
are scarce, short, with a bulbate base, without
or with simple to double apices; black lower
surface with a brown marginal zone (0·5)
2·04·0 mm; and rhizines that are black
without a bulbate base. Apothecia 0·8
6·2 mm diam., ascospores ellipsoid to oval,
pycnidia laminal, and conidia bacilliform.
For other details see Benatti (2012b).
Chemistry. Upper cortex K+ yellow,
medulla K+ yellow to black-red, C,KC;
atranorin and salazinic acid.
Ecology and distribution. The single specimen
from China was growing on Cinnamomum sp.
2016 Bulbothrix in ChinaZhang et al. 127
A B
DC
EF
FIG.3.Bulbothrix lacina habitus (holotype). A, thallus; B, spherical and dark black isidia; C, common lacinulae on
upper surface of thallus; D, marginal black line and irregular cilia; E, uniformly pale brown lower surface of
thallus; F, scarce pycnidia. Scales: A =4 mm; B, C & F =0·5 mm; D & E =1 mm. In colour online.
128 THE LICHENOLOGIST Vol. 48
World distribution: Asia, Africa and South
America (Benatti 2012b), and added here to
the ora of China.
Comments. This species is similar to
B. setschwanensis, but can be distinguished by
a black lower surface with a pale brown
marginal zone, and the maculate upper
surface. In Asia, B. meizospora has been
reported from India, Pakistan, Nepal and
Thailand, and only one population is known
from Xizang.
Specimen examined. China: Xizang Prov.: Nyalam
Co., 2450 m, 28°N, 86°E, on the bark of Cinnamomum
sp., 1966, J. C. Wei & J. B. Chen 673 (HAMS-L
0021966).
Bulbothrix scortella (Nyl.) Hale
Phytologia 28(5):480 (1974); type: USA, Texas,
C. Wright (FH-Tucklectotype (Hale 1976); H-NYL
duplicate).
Bulbothrix scortella is characterized by: a
smooth to cracked upper cortex; simple,
straight, granular to cylindrical isidia; black
to brown, branched cilia; pale brown to
brown lower surface with dense rhizines; and
rhizines that are pale brown to cream,
densely branched with a bulbate base.
Apothecia and pycnidia not seen in Chinese
specimens, but described by Benatti & Elix
(2012).
Chemistry. Upper cortex K+ yellow,
medulla K, C+ rose, KC+ rose; atranorin
and gyrophoric acid.
Ecology and distribution. Growing on bark
of deciduous trees in China. World distribu-
tion: Asia, Africa, Caribbean, USA and
South America, as detailed by Benatti & Elix
(2012); reported here as new to China.
Comments. Bulbothrix scortella is character-
ized by simple to occasionally branched
isidia, branched rhizines and cilia, and
the presence of gyrophoric acid in the
medulla.
Specimens of Bulbothrix scortella in China
were identied as B. goebelii by Chen
et al. (2009) and Lai (2000) who were
following the concept of Hale (1976), which
is composed of several morphologically and
chemically similar species. Benatti & Elix
(2012) recently showed that the type speci-
men, Parmelia goebelii Zenker (Bulbothrix
goebelii), comprises fragments of four differ-
ent species of Bulbothrix, and a lectotype was
chosen that conforms to the protologue of
Zenker (1827), whereby B. goebelii is
characterized by the lack of isidia and the
presence of lobaric, oxolobaric and colensoic
acids but without accessory gyrophoric acid
(Benatti & Elix 2012). Bulbothrix goebelii
previously reported from China has isidia
and gyrophoric acid, and is one of the
species included in HalesB. goebelii
concept. According to the current circum-
scription of species within that group, these
records in fact correspond to B. scortella, and
B. goebelii is therefore excluded from the ora
of China.
Bulbothrix scortella is similar to B. subdissecta
(Nyl.) Hale in sharing the presence of isidia
and gyrophoric acid in the medulla, but the
latter has a black lower surface and smaller
ascospores (Benatti & Elix 2012).
Specimens examined. China: Fujian Prov.: Wuyishan
Mt., 850 m, 26°54'N, 116°42'E, on deadwood, 1999,
J. B. Chen & S. L. Wang 14127 (HAMS-L 021931).
Yunnan Prov.: Lancang Co., Jinmai Mt., 1135 m,
22°12'N, 100°03'E, on Alnus nepalensis, 2014,
L. S. Wang et al.1444441, 1444442; Mengla Co.,
Longmen, on bark, 1974, M. Zang 528; Manla Village,
1079 m, 22°00'N, 101°26'E, on the branches of Camellia
sinensis, 2006, L. S. Wang et al. 0627337; Ruili Co.,
Nongdao, 780 m, on Quercus, 1983, L. S. Wang
832691a; Ninger Co., 1060 m, 23°16'N, 101°09'E, on
bark, 2013, L. S. Wang et al. 1340462.
Other species of Bulbothrix in China
Bulbothrix asiatica Y. Y. Zhang &
Li S. Wang
Bryologist 117: 379385 (2014); type: China, Yunnan,
L. S. Wang et al. (KUN-L 46314holotype).
Description. See Zhang et al. (2014).
Ecology and distribution. Growing on the
bark of Alnus nepalensis,Hevea brasiliensis and
other tree species, between 2901135 m.
Cambodia and China.
2016 Bulbothrix in ChinaZhang et al. 129
Comments. Specimens of this species
from China have usually been identied as
Bulbothrix tabacina (Chen et al. 2009). These
species are, however, clearly distinct as
revealed by the phylogenetic inference (Fig. 1)
and morphological characters: B. tabacina has a
maculate upper surface especially when wet,
whereas B. asiatica is emaculate.
New collections from Fujian Prov.in China. Wuyishan
National Reserve, 980 m, 27°41'N, 117°38'E, on bark,
L. S. Wang et al. 1547228, 1547240.
Bulbothrix isidiza (Nyl.) Hale
Phytologia 28(5):480 (1974); type: Angola, Serra Chella,
Newton (Hlectotype).
Description. See Benatti (2013).
Ecology and distribution. In China this
species usually grows on the bark of Pinus
yunnanensis and some other trees, rarely on
rocks, at altitudes of between 15002665 m.
World distribution: Oceania and North
Pacic, Asia, Africa, North America, Central
America and South America, as detailed by
Benatti (2013). China: Yunnan Province.
Comments. Bulbothrix isidiza is characterized
by the rough appearance of the upper surface,
very delicate and small isidia (Nylander 1884;
Hale 1976; Benatti 2013), and commonly
distinct maculae on the upper surface.
Moreover, specimens from China are usually
coriaceous, with a thicker thallus composed of
an upper cortex 37·562·5μm, algal layer
37·575·0μm, medulla 100 257 μmand
lower cortex 20 30 μm thick. The phyloge-
netic structure in the ITS tree lacks corres-
ponding morphological variation, hence we
treat all these specimens as B. isidiza.
Selected specimens examined. China: Yunnan Prov.:
Anning, 30 km SW of Kunming, 17501800 m, 24°55'N,
102°29'E, on Pinus yunnanensis, 1981, T. Koponen 37991;
Binchuan Co., Mt. Jizushan, 2620 m, 25°57'N, 100°22'E,
on bark, 2012, L. S. Wang & D. Liu 1233461; Chuxiong,
Mt. Zixishan, 2300 m, 25°04'N, 101°24'E, on rock, 2005,
L. S. Wang et al. 0525257; Jianchuan Co., Mt.
Shibaoshan, 2665 m, 26°22'N, 100°49'E, on bark, 2011,
L. S. Wang et al. 1132529; Jingdong Co., Wenjin,
1492 m, 24°21'N, 100°51'E, on Ficus, 2012, L. S. Wang
et al. 1234566; Kunming, Mt. Xishan, 1900 m, 1983,
L. S. Wang 8337891; Lufeng Co., Qinglongshao,
1700 m, 24°58'N, 102°30'E, on Pinus yunnanensis, 1987,
Teuvo Ahti et al. 46114; Luquan Co., 1952 m, 25°42'N,
102°29'E, on bark, 2014, L. S. Wang et al. 1443117;
Nanjian Co., Leqiu Village, 2060 m, 25°00'N, 100°21'E,
on Pinus yunnanensis, 2012, L. S. Wang & X. Y. Wang
1237816, 1237812; Mt. Wuliangshan, 2348 m,
24°52'N, 100°35'E, on bark, 2012, L. S. Wang et al.
1232998, 1233001; Xiaowandong, 1604m, 24°43'N,
100°08'E, on bark, 2012, L. S. Wang et al. 1234256,
1234265, 1234259; Songming Co., Baiyi Village,
2500 m, on Pinus yunnanensis, 2008, L. S. Wang &
J. Wang 0830314, 0829619; Tengchong Co.,
Mt. Kongshan, 1500 m, on Pinus yunnanensis, 1996,
L. S. Wang 9616791; Xiangyun Co., Mt. Shuimushan,
2440 m, 25°22'N, 100°37'E, on Pinus yunnanensis, 2013,
L. S. Wang et al. 1338923; Yuanmou Co., Mt. Liang-
shan, 2148 m, 25°43'N, 101°57'E, 2013, L. S. Wang et al.
1339820, 1339822, 1339829 (on bark), 1339846,
1339826, 1339821 (on Pinus).
Bulbothrix setschwanensis (Zahlb.) Hale
Phytologia 28(5):481 (1974); type: China, Sichuan,
Handel-Mazzetti 2739 (WUlectotype).
Description. See Benatti (2012b) and Hale
(1974).
Ecology and distribution. Usually growing on
the bark and branches of Pinus,Quercus or
Juglans, at altitudes of 12002800 m. World
distribution: Asia detailed by Benatti (2012b).
China: Sichuan and Yunnan Provinces.
Comments. This species is characterized
by the uniformly pale brown lower surface,
short cilia (0·3 mm), delicate and pale
brown rhizines, and salazinic acid in the
medulla.
Selected specimens examined. China: Sichuan Prov.:
Yanbian Co., Yankou, 1960 m, 1983, L. S. Wang
83535a; from Dukou to Yanbian, 2300 m, 1983,
L. S. Wang 83225, 83232; Miyi Co., Baiposhan Mt.,
1983, L. S. Wang 83735. Yunnan Prov.: Kunming,
Xishan Mt., Xiaoshilin, 2345 m, 24°55'N, 102°37'E, on
Pinus, 2013, D. Liu 1339868b; Lijiang Co., Xiangshan,
2500 m, on branches, 1985, L. S. Wang 850017,
850210a; Yufengsi, 2780 m, on Juglans sp., 1985,
L. S. Wang 850104; 2500 m, on Pinus armandii, 1982,
L. S. Wang 821087; Yongsheng Co., Dashan Village,
2200 m, 26°27'N, 101°07'E, on branches, 2013,
L. S. Wang et al. 1341164, 1341167; Yuanmou Co.,
Liangshan Village, Mt. Liangshan, 2148 m, 25°43'N,
101°57'E, 2013, L. S. Wang et al. 1339853 (on Pinus
yunnanensis), 1339743, 1339789 (on Quercus),
1339692, 1339747 (on bark).
130 THE LICHENOLOGIST Vol. 48
Bulbothrix subscortea (Asahina)
Marcelli & Benatti
Mycosphere 3: 4655 (2012); type: China, Taiwan,
Asahina 3324 (TNSlectotype).
Description. See Benatti (2012c) and Zhang
et al. (2014).
Ecology and distribution. Growing on rocks,
shrubs, and on Quercus spp., Pinus spp., in
open secondary forest, at elevations between
4302850m. World distribution: Asia. China:
Fujian, Guangxi, Hainan, Hong Kong,
Sichuan, Taiwan and Yunnan.
Comments. Bulbothrix subscortea is morpho-
logically very variable: cilia vary in length
(between 200825 μm), lobes range from
linear elongate to irregularly elongate regard-
less of habitat, and rhizines are with or without
basal or displaced bulbs. However, it can be
identied by the following characteristics:
emaculate upper surface, pale brown lower
surface and salazinic acid in the medulla.
New collections from Fujian Prov. in China. Wuyishan
National Reserve, 980 m, 27°41'N, 117°38'E, on bark,
L. S. Wang et al. 1547233; 580 m, 27°43'N, 117°42'E,
on bark, L. S. Wang et al. 1547053; 430 m, 27°41'N,
117°44'E, on Quercus sp., L. S. Wang et al. 1546797.
Bulbothrix tabacina (Mont. & Bosch)
Hale
Phytologia 28(5):481 (1974); type: Java, Junghuhn 335
(Llectotype; Pisolectotype).
Description. See Benatti (2013) and Hale
(1974).
Ecology and distribution. The single speci-
men cited here grew on branches at an
elevation of 860 m in Hainan. World
distribution: Oceania, Asia, Africa, North
America, Caribbean and South America.
This species was also reported from Taiwan
by Hale (1976) and Lai (2000).
Comments. This species can be recognized
by the maculate upper surface, black lower
surface with a pale brown marginal zone, and
the presence of salazinic acid in the medulla.
Specimen examined. China: Hainan Prov.: Ledong
Co., Jianfengling, 860 m, 18°44'N, 109°10'E, 2001,
J. B. Chen et al. 20770 (HAMS-L).
Discussion
Bulbothrix and Relicina can be easily recog-
nized by their bulbate cilia, and can be clearly
distinguished by secondary metabolites,
with the former containing atranorin versus
usnic acid in the latter. Although similar
overall, these genera belong to distinct clades
within the Parmeliaceae:Bulbothrix shares a
common ancestor with Parmelina, whereas
Relicina belongs to a group centred on
Parmelia (Crespo et al. 2010). Furthermore,
our phylogenetic trees agree with previous
studies (Divakar et al. 2006, 2010; Kirika
et al. 2015), whereby Bulbothrix species with
bulbate base cilia and atranorin do not com-
pose a monophyletic group. The Bulbothrix
isidiza group (Clade 2) is sister to Parmelinella
(Divakar et al. 2006, 2010; Masson et al.
2015) leading to this clade either nesting in
the genus Parmelinella or being a small genus
that contains salazinic acid. The type species of
Bulbothrix (i.e., B. semilunata)maybelongto
Clade 1 (Kirika et al. 2015) on account of its
distribution and morphological character-
istics. The genus concept for Bulbothrix thus
requires further revision and a more extensive
sampling of species to resolve the
relationships and circumscription of Bulbothrix
and Parmelinella.
Our work builds on studies on Cambodian
Bulbothrix (Zhang et al. 2014), claries the
species of Bulbothrix from China, and
thereby contributes to our knowledge of the
lichen ora of Asia. Our phylogenetic infer-
ence shows that all Bulbothrix species
from China belong to Clade 2 and have
broader lobes, simple to rarely branched cilia
and rhizines, and salazinic acid except for
B. scortella, and conrms that Clade 2 is
predominantly paleotropical as reported by
Kirika et al. (2015). We discovered two new
species, B. mammillaria and B. lacinia,that
are distinguished by morphology and ITS
sequences. Even so, more new species in this
genus may eventually be found in southern
China, given the great biodiversity of this region.
2016 Bulbothrix in ChinaZhang et al. 131
The authors are grateful to Prof. Bruce McCune (Oregon
State University) and Prof. Bernard Gofnet (University
of Connecticut) for their help with improving the English
composition, and the curator (Yijian Yao) and specimen
manager (Hong Deng) of HAMS. We also thank Prof. Zi
gang Qian, Dr Zhizhi Du and Dr Dong Wang for their
help with the molecular and chemical analyses. This study
was supported by grants from the National Natural Sci-
ence Foundation of China (No. 31170023, 31370069,
31400022), West Light Foundation of The Chinese
Academy of Sciences, Foundation of Key Laboratory for
Plant Diversity and Biogeography, Kunming Institute of
Botany, CAS (201306), and Flora Lichenum Sinicorum
(KSCX2EWZ9).
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Salazinic acid present (medulla C), rhizines simple ....................... 2
2(1) Isidia absent ...................................................... 3
Isidia present ..................................................... 4
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Upper surface emaculate, with a smooth appearance .............B. subscortea
132 THE LICHENOLOGIST Vol. 48
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2016 Bulbothrix in ChinaZhang et al. 133
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... Room temperature equilibrium populations were calculated according to Boltzmann distribution law. 13 where δcorr = (δcalcd -b)/a and therefore corrects for systematic errors were presented. Rotation calculations were carried at the B3LYP/6-31+G (d,p) and B3LYP/6-311++G (2d,p) level with PCM model in MeOH based on B3LYP/6-31G (d,p) optimized geometries optical to determine absolute stereochemistry of 1. ...
... Supplementary Materials: The following 1 H-NMR, 13 C-NMR, 2D-NMR, HR-ESI-MS, OR, CD, UV and IR spectra are available as supporting data. Supplementary materials are available online. ...
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Twenty species of Hypotrachyna are recognized in China's mainland. One species, H. neostictifera, is described as new to science, and five species, H. addita, H. croceopustulata, H. granulans, H. novella and H. physcioides, are reported as new to China. A further five species, H. adjuncta, H. exsecta, H. flexilis, H. imbricatula and H. koyaensis, are recorded in China's mainland for the first time. Three species, H. asiatica, H. ciliata and H. neostictifera, are endemic to China.
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Four new lichen species are described from China: Balbothrix yunnana S. L. Wang, J. B. Chen & Elix, Hypotrachyna asiatica S. L. Wang, J. B. Chen & Elix, H. ciliata S. L. Wang, J. B. Chen & Elix and Parmelina gyrophorica Elix, S. L. Wang & J. B. Chen.
Article
Bulbothrix laeviuscula, B. pseudocoronata and B. subscortea are proposed as new combinations in the Parmeliaceae based on type studies. Descriptions are presented and their characters discussed.
Article
Bulbothrix johannis is described as new to science. The species is morphologically similar to the South American Bulbothrix pseudofungicola Benatti & Marcelli but has wider lobes, laminal ciliate isidia which frequently develop into phyllidia, larger cilia and rhizines, and longer ascospores. This epiphytic species occurs fairly frequently in the cloud forests and montane thickets on Réunion Island (Mascarene archipelago). The comparison of B. johannis with morphologically and chemically similar species shows that several different African taxa are currently grouped under the widely used but problematic name B. suffixa (Stirt.) Hale.
Article
Bulbothrix johannis is described as new to science. The species is morphologically similar to the South American Bulbothrix pseudofungicola Benatti & Marcelli but has wider lobes, laminal ciliate isidia which frequently develop into phyllidia, larger cilia and rhizines, and longer ascospores. This epiphytic species occurs fairly frequently in the cloud forests and montane thickets on Réunion Island (Mascarene archipelago). The comparison of B. johannis with morphologically and chemically similar species shows that several different African taxa are currently grouped under the widely used but problematic name B. suffixa (Stirt.) Hale.
Article
Eight species belonging to Bulbothrix Hale from NE Argentina were studied. Among them, Bulbothrix affixa (Hale & Kurok.) Hale is a new continental record, and five species, viz. B. cassa Jungbluth, Marcelli & Elix, B. coronata (Fée) Hale, B. isidiza (Nyl.) Hale, B. laeviuscula (Räsänen) Benatti & Marcelli, and B. tabacina (Mont. & Bosch) Hale, are new citations for the country. The specimens are described, commented, and illustrated. A key for species identification is also presented.
Article
Four species previously included in the genus Bulbothrix are shown not to form bulbate cilia and are combined into alternative genera as Hypotrachyna tuskiformis, Parmelinopsis pinguiacida, P. subinflata, and Parmotrema yunnanum. All species are described in detail and a lectotype is selected for Bulbothrix tuskiformis.