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A preliminary study of Badimia Vězda (Ramalinaceae) in East Asia
Wei-Cheng Wang1,2 , Ek Sangvichien3, Kawinat Buaruang3, Shu-Hua Jiang1, Tie-Zheng Wei1,4 and Jiang-Chun Wei2,1
1
State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China;
2
University of Chinese Academy of Sciences,
Beijing 100049, China;
3
Department of Biology, Faculty of Science, Ramkhamhaeng University, Bangkok 10240, Thailand and
4
Southeast Asia Biodiversity Research
Institute, Chinese Academy of Sciences, Yezin, Nay Pyi Taw 05282, Myanmar
Abstract
The tropical areas of eastern Asia contain a high diversity of foliicolous lichens, including various species of the genus Badimia.Badimia
xanthocampylidia W. C. Wang & J. C. Wei is described from tropical rainforests in southern China and Thailand based on morphology,
chemistry, and combined mtSSU, ITS and nrLSU sequences. It is characterized by a pale green thallus with yellow verrucae and bright
yellow campylidia and the presence of isousnic acid. Three other species, B. multiseptata Papong & Lücking, B. pallidula (Kremp.)
Vězda and B. polillensis (Vain.) Vězda, are discussed and the genus Badimia is newly reported from China. A worldwide key to currently
known species in the genus is presented.
Key words: foliicolous lichens, ITS, mtSSU, new species, nrLSU
(Accepted 16 February 2021)
Introduction
Badimia Vězda was introduced as a segregate of the artificial
genus Bacidia De Not. based on its conidia structure, originally
containing six foliicolous species (Vězda 1986). Subsequently,
additional species have been described. As a result, the genus cur-
rently comprises 18 species and shows a pantropical distribution
(Santesson 1952; Kalb & Vězda 1987; Lücking et al.1994; Lücking
& Lücking 1995; Aptroot et al. 1997; Lücking 1998,2008; Lücking
& Kalb 2001; Schubert et al. 2003; Lumbsch et al.2011; Farkas
2015). Among the 18 known species, 10 have been reported
from the eastern Paleotropics.
The genus Badimia is characterized chiefly by the crescent-
shaped campylidia, producing filiform conidia with lateral appen-
dages, and by the flesh-coloured or yellow to orange apothecia
(Vězda 1986). It is a predominantly foliicolous genus with only
two species described from bark (Kalb & Vězda 1987; Aptroot
et al. 1997).
Initially, Badimia was placed in the Ectolechiaceae due to the
presence of campylidia. Subsequently, Ectolechiaceae, including
Badimia, was treated as a synonym of Pilocarpaceae (Lücking
et al. 1994; Lücking 1999). However, a recent molecular phylogen-
etic analysis, based on mtSSU sequences (Kistenich et al. 2018),
suggested that Badimia should be placed in Ramalinaceae. The
genus Pseudogyalecta Vězda was established by Vězda (1975)to
accommodate a single species, P. verrucosa Vězda, which was sub-
sequently placed in Badimia (Lücking & Vězda 1995;Vězda &
Lücking 1995).
The Flora Neotropica monograph by Lücking (2008) included
seven foliicolous species of Badimia for the Neotropics, dividing
the genus into two sections based on morphological characters:
Badimia sect. Badimia and Badimia sect. Pseudogyalecta. The
first has apothecia with a yellow or dark brown, opaque disc, a
crystalline excipulum and ferruginous brown or bright yellow
campylidia, and currently includes 14 species, whereas the second
has flesh-coloured to pinkish, often slightly translucent apothecia
lacking excipular crystals, chamois-coloured to white campylidia
and contains four species.
In our ongoing studies of foliicolous lichens in East Asia we
have recently focused on this genus, discovering an undescribed
species that is described below as Badimia xanthocampylidia
W. C. Wang & J. C. Wei. Three additional species belonging to
the Badimia sect. Pseudogyalecta,B. multiseptata Papong &
Lücking, B. pallidula (Kremp.) Vězda and B. polillensis (Vain.)
Vězda, were also collected and studied phylogenetically. A key
to all described species in the genus is presented.
Materials and Methods
Morphology and chemistry
The study is based mainly on material collected by the first author
in China, Thailand and Malaysia, deposited in the herbaria
HMAS-L and RAMK.
Micrographs of morphological and anatomical features were
taken with a Leica M125 dissecting microscope and a Zeiss
Imager A2 compound microscope, respectively.
Secondary metabolites were tested by spot reactions with KOH
(a 10% aqueous solution of potassium hydroxide), I (a 10% aque-
ous solution of potassium iodide), P (saturated solution of
p-phenylenediamine in 95% ethyl alcohol), and standardized
thin-layer chromatography (TLC) techniques with solvent system
C (Orange et al. 2010).
Author for correspondence: Jiang-Chun Wei. E-mail: weijc2004@126.com
Cite this article: Wang W-C, Sangvichien E, Buaruang K, Jiang S-H, Wei T-Z and
Wei J-C (2021) A preliminary study of Badimia Vězda (Ramalinaceae) in East Asia.
Lichenologist 53, 327–334. https://doi.org/10.1017/S002428292100013X
© The Author(s), 2021. Published by Cambridge University Press on behalf of the British Lichen Society
The Lichenologist (2021), 53, 327–334
doi:10.1017/S002428292100013X
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DNA extraction, PCR amplification and sequencing
PCR amplification of the mtSSU rDNA was performed with the
primers mrSSU1 and mrSSU3R (Zoller et al. 1999), of the ITS
with E9 and SL4R (Zhang & Wei 2017), and of the nrLSU
rDNA with AL1R (Döring et al. 2000) and LR5 (Vilgalys &
Hester 1990). Total DNA extraction, PCR cycling parameters,
PCR product purification and sequencing were performed as
described in Wang et al. (2020).
Sequence alignment and phylogenetic analysis
Sequence fragments were assembled and edited using Geneious
v.6.1.2 (Biomatters Ltd, Auckland, New Zealand); a total of 31
sequences were analyzed, including 12 sequences retrieved from
GenBank (Table 1).
Ramalina dilacerata (Hoffm.) Hoffm., R. fraxinea (L.) Ach.
and Toninia bullata (Meyen & Flot.) Zahlbr. were chosen as out-
group based on previous phylogenetic analyses (Kistenich et al.
2018). The assembled sequences were aligned with the online ver-
sion of MAFFT v.7 (Katoh et al.2009).
Ambiguously aligned regions were delimited using Gblocks
v.0.91b (Castresana 2000) with the least stringent selection,
which yielded alignment lengths of 776 bp (mtSSU), 563 bp
(ITS) and 922 bp (nrLSU). After checking for topological conflict,
the three alignments were concatenated in Geneious v.6.1.2 for
the multi-locus phylogenetic analysis.
Maximum likelihood (ML) analyses were used to reconstruct
phylogenetic trees based on the combined mtSSU, ITS and nrLSU
data set, using RAxML-HPC v.8.2.6 (Stamatakis 2014)onthe
Cipres Science Gateway (http://www.phylo.org), and support values
were based on 1000 non-parametric bootstrap pseudoreplicates.
The data were also analyzed using Bayesian Inference (BI) in
MrBayes v.3.2.6 (Huelsenbeck & Ronquist 2001; Ronquist &
Huelsenbeck 2003). The GTR + G model was selected for
mtSSU, the TIM3 + I model for ITS and the TIM2 + G model
for nrLSU, based on analysis using jModelTest 2.1.4 (Darriba
et al.2012). Markov chain Monte Carlo (MCMC) was initiated
from a random tree using 5 million generations and sampling
every 1000 steps, with the first 25% of trees discarded as burn-in.
Stationarity of analysis was determined by examining the standard
deviation of split frequencies (< 0.01). A majority-rule consensus
tree was calculated to obtain posterior probabilities (PP). The
phylogenetic tree was visualized using FigTree v.1.4.3.
Results
The final alignment consisted of 15 mtSSU sequences, seven ITS
sequences and nine nrLSU sequences representing the ingroup
Badimia (Table 1).
As maximum likelihood (ML) and Bayesian inference (BI)
resulted in the same topology, we present only the ML tree with
support values from both analyses combined (Fig. 1).
Four sequences of Badimia xanthocampylidia (one from
China, three from Thailand) are combined in a well-supported
(BS = 100, PP = 1) clade, and this species forms a highly sup-
ported (BS = 100, PP = 1) sister group to B. dimidiata (Bab. ex
Leight.) Vězda. Three species belonging to Badimia sect.
Pseudogyalecta,B. multiseptata,B. pallidula and B. polillensis,
form a strongly supported (BS = 100, PP = 1) clade, which in
turn is strongly supported (BS = 100, PP = 1) as sister to the B.
xanthocampylidia-dimidiata clade, agreeing with the distinction
of sections Badimia and Pseudogyalecta by Lücking (2008).
Discussion
Previous studies on the taxonomy of the genus Badimia were
based on morphological, anatomical and chemical characteristics,
and the only molecular data available were for a single specimen
of Badimia dimidiata from Costa Rica (Kistenich et al. 2018). Our
study substantially expands molecular sampling for this genus,
both taxonomically and geographically, including four additional
species collected in China, Thailand and Malaysia, allowing us to
present the first multi-locus phylogenetic analysis of the genus.
Table 1. Specimens of Badimia and outgroup species used in the phylogenetic analyses (Fig. 1) with voucher information and GenBank Accession numbers. New
sequences generated for this study are in bold.
Taxon Locality Voucher specimens mtSSU ITS nrLSU
Badimia dimidiata Costa Rica Lücking 16013 (BG) AY567774 MG925956 MG926052
B. multiseptata Thailand Wang KYW0277 (RAMK 31634) MT791326
B. pallidula China, Hainan Wang HN20170295-2 (HMAS-L 146147) MW349653 MW349651 MT791315
B. pallidula China, Hainan Wang 20192889 (HMAS-L 146151) MT791324 MW349649 MT791317
B. pallidula China, Hainan Wang 20192892 (HMAS-L) MW349652 MW346680
B. polillensis China, Hainan Wang HN20170142 (HMAS-L 139502) MT791319
B. polillensis China, Hainan Wang HN20170147-1 (HMAS-L 146146) MT791320
B. polillensis Malaysia Wang WWC386 MT791325 MW349650 MT791318
B. xanthocampylidia Thailand Wang KYW0283 (RAMK 31637) MT791321
B. xanthocampylidia Thailand Wang KYW0640 (RAMK 31681) MT791322
B. xanthocampylidia Thailand Wang KYW0285 (RAMK 31638) MT791327
Ramalina dilacerata USA Wetmore 83868 (BG) MG925917 MG926013 MG926104
R. fraxinea Sweden Ekman 3686 (UPS) MG925918 MG926014 MG926105
Toninia bullata Australia Elix &Streimann 40393 (O) MG925929 MG926026 MG926116
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The data also revealed a new species, supported by molecular,
morphological and chemical data.
The unique crescent-shaped campylidia, producing conidia
with lateral appendages, make Badimia a readily recognized
genus. Within this genus, two types of apothecia and campylidia
occur: either flesh-coloured apothecia lacking excipular crystals,
always combined with chamois-coloured to white campylidia, or
brightly coloured apothecia with excipular crystals, always com-
bined with ferruginous brown to bright yellow campylidia. This
distinction corresponds to the separation of the two sections
Pseudogyalecta and Badimia and our molecular results strongly
support this distinction. However, given that three out of the
four known species of section Pseudogyalecta but only two out
of the 18 of section Badimia have been sequenced so far, these
results are to be considered preliminary.
Although species of the genus are widely distributed, the genus
is not frequently collected due to its preference for well-preserved
primary rainforest (Lücking 1995,1997), which is unfortunately
on the decline in South-East Asia. It has been proposed as a char-
acter genus for tropical rainforests, with a high degree of biogeo-
graphical differentiation (Lücking & Kalb 2001), underlining the
importance of molecular phylogenetic studies to fully clarify spe-
cies delimitation and taxonomic relationships within this genus.
Taxonomy
Badimia xanthocampylidia W. C. Wang & J. C. Wei sp. nov.
Fungal Names No.: FN 570750
Similar to Badimia dimidiata but differs by having brown apothe-
cia with orange excipular crystals, bright yellow-orange campyli-
dia, a yellowish green to greyish green thallus with yellow
crystal contents of the verrucae, and producing isousnic instead
of usnic acid.
Type: China, Yunnan Province, Xishuangbanna City, nature
reserve of Mengla, Bubang observation station, 21.61°N, 101.58°E,
522 m alt., on leaves, 28 January 2018, W. C. Wang 140602
(HMAS-L—holotype; RAMK—isotypes).
(Fig. 2)
Thallus epiphyllous, continuous, 1–2 cm diam., sparsely to irregu-
larly verrucose, yellowish green in outer part and greyish green in
central part, K−,P−;verrucae wart-shaped, 0.1–0.2 μm diam.,
bright yellow, filled with yellow crystals. Prothallus sometimes dis-
tinct along the margin, composed of radiate white hyphae.
Photobiont chlorococcoid with globose, green cells, 10–18 μm
diam.
Apothecia rare, sessile, basally constricted, regularly rounded,
0.4–0.6 mm diam., 180–200 μm high; disc concave, rather dark
brown, non-pruinose; margin distinct, thick, prominent, of the
same colour as disc or paler. Excipulum well developed, colour-
less, with indistinct structure due to heavy encrustation with
orange pigment granules, appearing as bright yellow crystals in
polarized light and partly dissolving in KOH; excipulum laterally
45–55 μm wide, composed of short hyphae with inflated cells, K−,
P−;apothecial base colourless, heavily encrusted with hyaline
crystals, not dissolving in K; hypothecium 45–55 μm high, pale
orange, K−,P−;epithecium c.15–20 μm high, encrusted with yel-
low pigment granules, not dissolving in K, K−,P−;hymenium
55–65 μm high, colourless; paraphyses 1μm thick, unbranched,
not thickened at their apices, coherent. Asci clavate, 45–50 × 9–
11 μm, ascus apex I+ dark blue; ascospores 8 per ascus, fusiform,
3-septate, without constrictions at septa, 15–18 × 5–6μm, 2.5–3.5
times as long as wide, colourless.
Campylidia numerous, sessile, slightly or strongly curved,
half-moon-shaped, 0.3–0.5 mm wide, 0.9–1.2 mm long; bright
yellow in both inner and outer parts, but outer parts usually
with an orange pruina, dull, wall encrusted with yellow crystals.
Fig. 1. Phylogram of Badimia species using maximum
likelihood (ML) inferred from a concatenated data set
of mtSSU + ITS + nrLSU. Bootstrap support ≥75% for
ML before the slash and posterior probabilities
(PP) ≥0.95 after the slash are indicated above the
branches and are considered to be significant. The
newly described species is marked in bold. Scale =
0.03 substitutions per site.
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Conidia filiform, 3–9-septate, 70–80 × 1.5–2μm, with 4–5 lateral
appendages up to 10 μm long, colourless.
Chemistry. Isousnic acid, zeorin, and an unknown substance
(R
f
= 50, blue after acid and heating, probably representing the
major pigment) present.
Etymology. The epithet of the new species ‘xanthocampylidia’is
a Greek composite consisting of the words ‘xantho-’(= yellow)
and ‘campylidia’because of the conspicuous yellow campylidia
of the species.
Habitat and distribution. Badimia xanthocampylidia is currently
known from the Yunnan Province in China and from Thailand.
In China, only one locality is known from submontane rainforests
(alt. 500–700 m) in the Xishuangbanna Nature Reserve, where the
species was found growing on smooth leaves of trees in well-
preserved stands. In Thailand it has been found in Khao Yai
Fig. 2. Badimia xanthocampylidia (holotype, Wang 140602, HMAS-L). A, thallus with apothecia and campylidia. B, thallus with campylidia. C & D, section of apothe-
cium showing pigmentation in normal light (C) and yellow crystals in exciple in polarized light (D). E, 3-septate ascospores. F, filiform conidia with lateral appen-
dages. (D–F are all observed in differential interference mode). Scales: A & B = 500 μm; C & D = 50 μm; E & F=10μm. In colour online.
330 Wei‐Cheng Wang et al.
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National Park, growing in the shady understorey of a lowland
rainforest.
Notes. This new species is distinctive within the genus because of
its predominantly bright yellow verrucae and campylidia, and also
the presence of isousnic acid. The presence of crystals in the exci-
pulum and campylidia wall, and the apothecia and campylidia
pigmentation, support its placement in sect. Badimia.The
neotropical-African B. dimidiata is morphologically similar to
B. xanthocampylidia in the irregularly verrucose thallus but differs
in having chamois-coloured verrucae and orange apothecia with a
chamois-coloured margin and colourless crystals, and in the pres-
ence of usnic instead of isousnic acid (Lücking 2008). The neotrop-
ical B. tuckermanii and the new species share the characteristic
orange excipular crystals, but B. tuckermanii differs in having
chamois-coloured to at best pale yellow thallus verrucae, orange
apothecia, and in the presence of the 3-methyl-asemone chemosyn-
drome (Lücking 2008). The paleotropical B. galbinea and the new
species have yellow thallus verrucae in common, but the thallus of
B. galbinea is distinctly bluish, the apothecia are yellow-orange, and
it also produces usnic instead of isousnic acid.
Additional specimens examined. China: Yunnan Province:
Xishuangbanna City, nature reserve of Mengla, Wangtianshu
scenic spot, 21°37′N, 101°35′E, 689 m alt., on leaves, 2018,
W. C. Wa ng 140603 (HMAS-L).—Thailand: Nakhon Ratchasima
Province: Khao Yai National Park, Pha Kluay Mai Waterfall
trail to Haew Suwat Waterfall, 14°23′N, 101°22′E, 800 m alt., on
leaves, 2018, W. C. Wang 31637, 31638, 31681, 31811, 31922
(RAMK).
Badimia multiseptata Papong & Lücking
In Lumbsch et al., Phytotaxa 18, 19 (2011).
(Fig. 3A &B)
Chemistry. Both usnic acid and zeorin present.
Habitat and distribution. Eastern Paleotropics. Collected in the
shady understorey of lowland rainforests.
Notes. This species was described by Papong and Lücking
(Lumbsch et al. 2011) and is so far known only from Thailand,
where it occurs in lowland rainforests. It is characterized mainly
by its 5–7-septate ascospores. Only two species of Badimia (B.
xanthocampylidia and B. multiseptata) are currently known
from Thailand (Buaruang et al. 2017).
Fig. 3. A&B,Badimia multiseptata (Wang 31636, 31933; RAMK). C & D, Badimia polillensis (Huang 112922, Wang 146146; HMAS-L). E & F, Badimia pallidula (Wang
146151, 146147; HMAS-L). A, C & E, thalli with apothecia. B, D & F, thalli with campylidia. Scales: A–F = 0.5 mm. In colour online.
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Specimens examined. Thailand: Nakhon Ratchasima Province:
Khao Yai National Park, Pha Kluay Mai Waterfall trail to Haew
Suwat Waterfall, 14°23′N, 101°22′E, 800 m alt., on leaves, 2018,
W. C. Wang 31632, 31634, 31636, 31706, 31712, 31851 (RAMK).
Badimia pallidula (Kremp.) Vězda
Folia Geobot. Phytotax.21(2), 215 (1986).—Lecidea pallidula
Kremp., Lich. foliicolae quos legit O. Beccari, 9 (1874).—Bacidia
pallidula (Kremp.) Zahlbr., Cat. Lich. Univers.4, 135 (1926).
(Fig. 3E &F)
Chemistry. Usnic acid and zeorin present.
Habitat and distribution. Eastern Paleotropics and Neotropics
(Lücking 2008). Growing in the shaded to semi-exposed under-
storey of moist rainforest.
Notes. The genus Badimia is newly reported here from China.
Three species are now known from China and all are reported
for the first time in this study: B. xanthocampylidia,B. pallidula
and B. polillensis. They all occur in the Hainan and Yunnan pro-
vinces of China.
Badimia pallidula is a pantropical species and has been
reported from Malesia, the Philippines and Borneo in eastern
Asia as well as from the Neotropics (Santesson 1952; Lücking
2008). It is closely related to B. polillensis, which also has
chamois-coloured to white campylidia and contains zeorin and
usnic acid. However, B. pallidula has sparse, large thallus verrucae
(0.1–0.2 mm diam.), whereas in B. polillensis the thallus verrucae
are dense and smaller (0.07–0.1 mm diam.).
Specimens examined. China: Hainan Province: Wuzhishan City,
Wuzhishan National Forest Park, 18°54′N, 109°41′E, 800 m alt.,
on leaves, 2017, W. C. Wang 146147 (HMAS-L); ibid., 2019,
W. C. Wang 146150, 146151, 146152, 146153, 146154, 146155
(HMAS-L).
Badimia polillensis (Vain.) Vězda
Folia Geobot. Phytotax. 21(2), 215 (1986).—Bilimbia polillensis
Vain., Ann. Acad. Sci. Fenn., ser. A 15(6), 28 (1921).—
Bacidia polillensis (Vain.) Zahlbr., Cat. Lich. Univers. 4, 136
(1926).
(Fig. 3C &D)
Chemistry. Usnic acid and zeorin present.
Habitat and distribution. Eastern Paleotropics and Neotropics
(Lücking 2008). Growing in moist rainforests.
Notes. In South-East Asia, this taxon was originally known
only from the Philippines (Santesson 1952); it is newly
reported here for China and Malaysia. Although it is also
known from the Neotropics (Lücking 2008), it seems to be rare
there.
Specimens examined. China: Hainan Province: Ledong County,
Jianfeng Ridge, Mingfeng Valley, 18°44′N, 108°50′E, 960 m alt.,
on leaves, 2017, W. C. Wang 139531, 146146, 139502
(HMAS-L); ibid., 18°44′N, 109°10′E, 1000 m alt., on leaves,
2000, M. R. Huang 108866, 112922, 112795 (HMAS-L); ibid.,
hydrometric station, 18°44′N, 109°10′E, on leaves, 2006,
J. C. Wei 112827, 112835, 112943, 112955, 112958
(HMAS-L).—Malaysia: Pahang State: Raub, Fraser Hill, 3°
42′50′′N, 101°44′6′′ E, 900–1100 m alt., Jeriau Waterfall Trail, on
leaves, 2019, W. C. Wang WWC357, WWC368; Pine Tree Trail,
on leaves, 2019, W. C. Wang WWC386.
World key to the species of the genus Badimia
1 Excipulum and campylidial wall lacking crystals, distinctly paraplectenchymatous; apothecia slightly translucent, with pinkish
to flesh-coloured disc and thin, concolorous and usually paler margin; campylidia outer parts chamois-coloured to white
(Badimia sect. Pseudogyalecta).................................................................2
Excipulum and campylidial wall strongly encrusted with colourless or yellow crystals, their structure difficult to discern;
apothecia opaque, with yellow to orange or dark brown disc and thick, white to chamois-coloured or yellow margin; cam-
pylidia ferruginous brown to bright yellow (Badimia sect. Badimia) .....................................5
2(1) Ascospores 3-septate, 11–16 μm in length . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
Ascospores 5–7-septate, 20–32 μm in length . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3(2) Thallus verrucae larger (0.1–0.2 mm), sparse, and irregularly scattered; eastern Paleotropics and Neotropics . . . . . . . . . . .
.................................................................. B. pallidula (Kremp.) Vězda
Thallus verrucae small (0.07–0.1 mm), dense; eastern Paleotropics and Neotropics . . . . . . . . . B. polillensis (Vain.) Vězda
4(2) Conidia 50–60 μm in length; ascospores 5–7-septate; Thailand . . . . . . . . . . . . . . . . . . B. multiseptata Papong & Lücking
Conidia 100–120 μm in length; ascospores becoming partly submuriform; Tanzania . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
.......................................................... B. verrucosa (Vězda) Lücking & Vězda
5(1) Campylidia bright yellow to orange; thallus yellowish green in outer part and greyish green in central part, verrucae bright
yellow; eastern Paleotropics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. xanthocampylidia W. C. Wang & J. C. Wei
332 Wei‐Cheng Wang et al.
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Campylidia ferruginous brown, at least in upper and outer parts; thallus bluish grey or greenish grey, verrucae chamois-
coloured to rarely bright yellow or verrucae absent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
6(5) Excipular crystals colourless; apothecial disc pale or brownish orange, dark brown or dark reddish brown, margin white to
chamois-coloured . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
Excipular crystals yellow-orange to yellowish brown; apothecial disc bright yellow to orange or purplish brown, margin yellow
or pale grey or chamois-coloured . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
7(6) Thallus smooth, verrucae and soredia absent, containing unidentified substance of the 3-methyl-asemone chemosyndrome;
apothecial disc yellowish orange to ochraceous yellow; Neotropics . . . . . . . . . . . . . . . . . . . . . B. montoyana Lücking
Thallus with verrucae or soredia; apothecial disc yellow-orange to dark reddish brown, pale or brownish orange . . . . . . . 8
8(7) Thallus with soredia or large verrucae that soon break into soredia, more than 0.2 mm diam., corticolous or foliicolous. . .
.......................................................................................9
Thallus with smaller whitish to chamois-coloured verrucae, less than 0.15 mm diam., foliicolous . . . . . . . . . . . . . . . . . 11
9(8) Foliicolous, thallus with rather dense soredia, grey to almost white with a greenish pigment, 0.3–0.8 mm; apothecia dark red-
dish brown with white margin; eastern Paleotropics . . . . . . . . . . . . . . . . . . . . . . . . . .B. cateilea (Vain.) Lücking et al.
Corticolous, thallus with verrucae that soon break into soredia, 0.2–0.3 mm, soredial mass pure white or pale yellowish green;
apothecia pale orange to pinkish orange or absent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
10(9) Thallus white to pale green, soredial mass pure white; campylidia pale brown; apothecia absent; Brazil . . . . . . . . . . . . . . .
....................................................................B. corticola Kalb & Vězda
Thallus bluish green, soredial mass pale yellowish green; campylidia absent; apothecia pale orange to pinkish orange with paler
margin; eastern Paleotropics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. lucida Aptroot & Sérus.
11(8) Thallus verrucae 0.1–0.15 mm; apothecial disc orange to ferruginous brown, in young apothecia pale yellow, margin chamois-
coloured; campylidia ferruginous brown; Neotropics . . . . . . . . . . . . . . . . . . . . . B. dimidiata (Bab. ex Leight.) Vězda
Thallus verrucae 0.05–0.1 mm; apothecial disc reddish brown, even in young apothecia, margin white; campylidia unknown . .
.........................................................................................12
12(11) Thallus green, verrucae dense, 0.05–0.08 mm; hypothecium pale brown; ascospores 10–12 μm in length; Samoa . . . . . . . .
............................................................B. lecanorina (Zahlbr.) Lücking et al.
Thallus bluish to greenish white, verrucae not dense, 0.07–0.1 mm; hypothecium pale yellow; ascospores 10–16 μm in length;
eastern Paleotropics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. vieillardii (Müll. Arg.) Vězda
13(6) Thallus smooth, without verrucae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
Thallus with verrucae, 0.07–0.15 mm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
14(13) Apothecial disc purplish brown when mature, margin pale grey, excipular crystals K+ purple, then yellow; Neotropics . . .
............................................................. B. leioplacella (Müll. Arg.) Lücking
Apothecial disc yellow to orange-yellow or orange-brown, margin of the same colour as the disc or paler . . . . . . . . . . . 15
15(14) Thallus continuous; apothecial disc bright yellow to orange-yellow with pale yellow to chamois-coloured margin,
non-pruinose; campylidia in inner parts bright yellow, in outer parts pale yellow to chamois-coloured; eastern Paleotropics
.....................................................................B. elixii Kalb & Lumbsch
Thallus dispersed in outer parts; apothecial disc ochraceous yellow to orange-brown, margin same colour as the disc, often
with a pale yellowish or reddish yellow pruina; eastern Paleotropics . . . . . . . . . . . . . . . . . . . B. elegans (Vain.) Vězda
16(13) Thallus almost smooth to sparsely and irregularly verrucose; apothecial margin chamois-coloured, substances of the
3-methyl-asemone chemosyndrome present; Neotropics . . . . . . . . . . . . . . . . . B. tuckermanii (R. Sant.) Lücking et al.
Thallus with rather distinct verrucae; apothecial margin bright yellow, substances of the 3-methyl-asemone chemosyndrome
absent .................................................................................17
17(16) Thallus irregularly laciniate, with scattered and irregular, pale yellow verrucae; apothecia ferruginous orange; eastern
Paleotropics and Neotropics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. galbinea (Kremp.) Vězda
Thallus continuous, with distinct, densely arranged white verrucae with yellow content; apothecia yellow to yellowish orange;
Neotropics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. vezdana Lücking et al.
The Lichenologist 333
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Acknowledgements. We thank Dr H. Thorsten Lumbsch (Field Museum,
Chicago, USA) for revision of the content and language. This research was
funded by the Southeast Asia Biodiversity Research Institute, Chinese
Academy of Sciences (Y4ZK111B01) and the National Natural Science
Foundation of China (31800010).
Author ORCID. Wei-Cheng Wang, 0000-0002-8391-5120.
References
Aptroot A, Diederich P, Sérusiaux E and Sipman HJM (1997) Lichens and
lichenicolous fungi from New Guinea. Bibliotheca Lichenologica 64,1–220.
Buaruang K, Boonpragob K, Mongkolsuk P, Sangvichien E, Vongshewarat
K, Polyiam W, Rangsiruji A, Saipunkaew W, Naksuwankul K, Kalb J,
et al.(2017) A new checklist of lichenized fungi occurring in Thailand.
MycoKeys 23,1–91.
Castresana J (2000) Selection of conserved blocks from multiple alignments
for their use in phylogenetic analysis. Molecular Biology and Evolution
17, 540–552.
Darriba D, Taboada GL, Doallo R and Posada D (2012) jModelTest 2: more
models, new heuristics and parallel computing. Nature Methods 9, 772.
Döring H, Clerc P, Grube M and Wedin M (2000) Mycobiont specific PCR
primers for the amplification of nuclear ITS and LSU rDNA from liche-
nized ascomycetes. Lichenologist 32, 200–204.
Farkas E (2015) Names of Bacidia s. l. in current use for foliicolous lichens –
an annotated nomenclatural study. Acta Botanica Hungarica 57,51–70.
Huelsenbeck JP and Ronquist F (2001) MRBAYES: Bayesian inference of
phylogenetic trees. Bioinformatics 17, 754–755.
Kalb K and Vězda A (1987) Einige nicht-foliicole Arten der Familie
Ectolechiaceae (Lichenes) aus Brasilien. Folia Geobotanica et
Phytotaxonomica 22, 287–312.
Katoh K, Asimenos G and Toh H (2009) Multiple alignment of DNA
sequences with MAFFT. Methods in Molecular Biology 537,39–64.
Kistenich S, Timdal E, Bendiksby M and Ekman S (2018) Molecular sys-
tematics and character evolution in the lichen family Ramalinaceae
(Ascomycota: Lecanorales). Taxon 67, 871–904.
Lücking R (1995) Biodiversity and conservation of foliicolous lichens in Costa
Rica. Mitteilungen der Eidgenössischen Forschungsanstalt für Wald, Schnee
und Landschaft 70,63–92.
Lücking R (1997) The use of foliicolous lichens as bioindicators in the tropics,
with special reference to the microclimate. Abstracta Botanica 21,99–116.
Lücking R (1998) Foliicolous lichens and their lichenicolous fungi collected
during the Smithsonian International Cryptogamic Expedition to Guyana
1996. Tropical Bryology 15,45–76.
Lücking R (1999) Ergänzungen und Verbesserungen zur Kenntnis der foliikolen
Flechtenflora Costa Ricas. Die Familie Ectolechiaceae. Phyton 39,131–165.
Lücking R (2008) Foliicolous lichenized fungi. Flora Neotropica Monograph
103,1–866.
Lücking R and Kalb K (2001) New Caledonia, foliicolous lichens and island
biogeography. Bibliotheca Lichenologica 78, 247–273.
Lücking R and Lücking A (1995) Foliicolous lichens and bryophytes from
Cocos Island, Costa Rica. A taxonomical and ecogeographical
study. I. Lichens. Herzogia 11, 143–174.
Lücking R and Vězda A (1995) Proposal to conserve Badimia against
Pseudogyalecta (lichenized Ascomycotina). Taxon 44, 227–228.
Lücking R, Lumbsch HT and Elix JA (1994) Chemistry, anatomy and morph-
ology of foliicolous species of Fellhanera and Badimia (lichenized
Ascomycotina: Lecanorales). Botanica Acta 107, 393–401.
Lumbsch HT, Ahti T, Altermann S, Amo De Paz G, Aptroot A, Arup U,
Bárcenas Peña A, Bawingan PA, Benatti MN, Betancourt L, et al.
(2011) One hundred new species of lichenized fungi: a signature of undis-
covered global diversity. Phytotaxa 18,1–127.
Orange A, James PW and White FJ (2010) Microchemical Methods for the
Identification of Lichens. 2nd edition. London: British Lichen Society.
Ronquist F and Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic
inference under mixed models. Bioinformatics 19, 1572–1574.
Santesson R (1952) Foliicolous lichens I. A revision of the taxonomy of the obli-
gately foliicolous, lichenized fungi. Symbolae Botanicae Upsalienses 12,1–590.
Schubert R, Lücking R and Lumbsch HT (2003) New species of foliicolous
lichens from ‘La Amistad’Biosphere Reserve, Costa Rica. Willdenowia 33,
459–465.
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and
post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
Vězda A (1975) Foliicole Flechten aus Tanzania (Ost-Afrika). Folia
Geobotanica et Phytotaxonomica 10, 383–432.
Vězda A (1986) Neue Gattungen der familie Lecideaceae s. lat. (Lichenes).
Folia Geobotanica et Phytotaxonomica 21, 199–219.
Vězda A andLücking R (1995) A restudy of Pseudogyalectaverrucosa, its systema-
tical affinities, and the nomenclatural consequences. Mycotaxon 55,501–506.
Vilgalys R and Hester M (1990) Rapid genetic identification and mapping of
enzymatically amplified ribosomal DNA from several Cryptococcus species.
Journal of Bacteriology 172, 4238–4246.
Wang WC, Sangvichien E, Wei TZ and Wei JC (2020) A molecular phyl-
ogeny of Pilocarpaceae Zahlbr., including a new species of Tapellaria
Müll. Arg. and some new records of foliicolous lichenized fungi from
Thailand. Lichenologist 52, 377–385.
Zhang Y and Wei JC (2017) Generic classification based on the symplesio-
morphy of genotype and phenotype of the family Umbilicariaceae
(Ascomycota). Mycosystema 36, 1089–1103.
Zoller S, Scheidegger C and Sperisen C (1999) PCR primers for the amplifi-
cation of mitochondrial small subunit ribosomal DNA of lichen-forming
ascomycetes. Lichenologist 31, 511–516.
334 Wei‐Cheng Wang et al.
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