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A New Species of Graphis and New Lichen Records from Vietnam, Including a Second Worldwide Report of Sarcographina cyclospora

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Mycobiology
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Graphis upretii is a new lichen species discovered in Vietnam. The species is characterized by a loosely corticate, rough, whitish grey to greyish green thallus, elongate and irregularly branched lirellae with an apically thin complete thalline margin (negrosina morph), laterally carbonized, entire proper exciple, clear hymenium, hyaline, 16~20 transversely locular ascospores, and about 50~95 × 10~15 µm in size. In addition, members of the taxon produce norstictic and stictic acids. Currently, the lichen flora of Vietnam include Arthonia radiata, Brigantiaea tricolor, Coenogonium implexum, Dirina paradoxa, Herpothallon sipmanii, Pertusaria pertusa, and Sarcographina cyclospora.
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17
Mycobiology
A New Species of Graphis and New Lichen
Records from Vietnam, Including a Second
Worldwide Report of Sarcographina cyclospora
Santosh Joshi1, Udeni Jayalal1, Soon-Ok Oh1, Thi Thuy Nguyen2, Nguyen Anh Dzung2 and Jae-Seoun Hur1,3,*
1Korean Lichen Research Institute, Sunchon National University, Suncheon 540-950, Korea
2Department of Basic Biology, Faculty of Natural Science and Technology, Tay Nguyen University, 567 Le Duan, Buon Ma Thuot,
Vietnam
3School of the Environment, Faculty of Science and Engineering, Flinders University, Adelaide 5001, South Australia
Abstract Graphis upretii is a new lichen species discovered in Vietnam. The species is characterized by a loosely corticate,
rough, whitish grey to greyish green thallus, elongate and irregularly branched lirellae with an apically thin complete thalline
margin (negrosina morph), laterally carbonized, entire proper exciple, clear hymenium, hyaline, 16~20 transversely locular
ascospores, and about 50~95 × 10~15 µm in size. In addition, members of the taxon produce norstictic and stictic acids.
Currently, the lichen flora of Vietnam include Arthonia radiata, Brigantiaea tricolor, Coenogonium implexum, Dirina paradoxa,
Herpothallon sipmanii, Pertusaria pertusa, and Sarcographina cyclospora.
Keywords Corticolous, Dak Lak Province, Graphidaceae, Mt. Doi Sao, New species, Norstictic acid, Taxonomy
The tropical rainforests of Vietnam have experienced extensive
species migration from China, India-Himalaya, Malaysia-
Indonesia, and other neighboring temperate regions because
of its varied climate and topographic position. These
rainforests are thus currently comprised of a wide variety
of corticolous, lichenized acomycetes [1-6]. During a
recent visit to a central highland region of the country,
several interesting lichenized fungi were encountered in
the relatively shaded side of the vegetation belt and in
semi-exposed isolated tree pastures.
A luxuriant diversity of Graphidaceae was noted and was
previously recorded from different parts of the country [2, 3].
However, the genus Graphis has been less thoroughly studied
and until recently was represented by only six species:
Graphis caesiella Vai n . , G. dussii Vain., G. leptogramma
Nyl., G. librata C. Knight, G. proserpens Vai n . , a n d G.
rimulosa (Mont.) Trevis. In a more recent study on the
Graphidaceae from the northern and central highlands of
Vietn a m , Joshi et al. [4] additionally recorded 11 Graphis
species, namely G. caesiocarpa Redinger, G. cervinonigra
Zahlbr., G. cycasicola A. W. Archer & Elix, G. epiphloea
Zahlbr., G. handelii Zahlbr., G. japonica (Müll. Arg.) A. W.
Archer & Lücking, G. renschiana (Müll. Arg.) Stizenb., G.
schroederi Zahlbr., G. subserpentina Nyl., G. subvittata
Adaw. & Makhija, and G. supracola A. W. Archer. This study
describes a new species, G. upretii, which was recently
discovered and collected from the Dak Lak Province of
Vietnam. Superficially, the new taxon more closely resembles
Diorygma or Platythecium, but it is distinguished as Graphis
in having a whitish grey to greenish grey thallus, irregularly
branched lirellae with complete thalline margin, a black and
entire labia, a slit-like disc, and laterally carbonized proper
exciple, as well as being transversely septate, possessing I+
blue ascospores, and a thallus that produces norstictic acid
as the major lichen compound.
MATERIALS AND METHODS
The material collected in April 2012 and 2013 from the
northern and central highland areas of Vietnam, was
deposited in the herbarium of the Korean Lichen Research
Institute, South Korea (KoLRI) and subjected to morpho-
anatomical and chemical analyses. A Nikon SMZ-168
Research Article
Mycobiology 2014 March, 42(1): 17-21
http://dx.doi.org/10.5941/MYCO.2014.42.1.17
pISSN 1229-8093 • eISSN 2092-9323
© The Korean Society of Mycology
*Corresponding author
E-mail: jshur1@sunchon.ac.kr
Received November 4, 2013
Revised January 23, 2014
Accepted February 3, 2014
This is an Open Access article distributed under the terms of the
Creative Commons Attribution Non-Commercial License (http://
creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted
non-commercial use, distribution, and reproduction in any medium,
provided the original work is properly cited.
18 Joshi et al.
dissecting microscope (Nikon, Tokyo, Japan) was used for
obser vation of morphological features, whereas the anatomical
details were investigated under an Olympus BX-50 compound
microscope (Olympus, Tokyo, Japan). Ten to fifteen apothecial
sections were examined thoroughly for confirmation of the
species. Thin, hand-cut sections were observed in water
and lactophenol cotton blue solution. Additionally, Lugol’s
iodine (I) was applied to check the amyloidity of the ascus,
ascospores, and interascal filaments. All measurements
were made under higher magnifications of 40× and 1,000×
prior to the application of KOH. Chemical analysis was
conducted by using thin-layer chromatography (solvent
systems C and A) and color spot tests as described by Orange
et al. [7]. The relevant literature describing Graphidaceae
[8-11] was consulted for identification of the new taxon.
RESULTS AND DISCUSSION
Taxonomic treatment of the species.
G. upretii S. Joshi & Hur sp. nov. (Fig. 1A~1F)
Mycobank No.: MB 807869.
Similar to G. longispora, but differing in having a complete
thalline margin, smaller ascospores, and a thallus that
produces norstictic and stictic acids.
Typ e : Vietnam, Dak Lak Province, Buon Ma Thuot City,
Mt. Doi Sao, 12o40'31.8'' N, 108o05'24.4'' E, alt. c. 539 m, on
tree bark, Oh & Thanh VN130043 (holotype KoLRI).
Description: Thallus corticolous, epiperidermal, crustose,
continuous, spread in patches up to 15 cm, loosely corticate,
rough, rather delicate, crystalline, whitish grey, greenish
grey or greyish white, ± dull, 100~200-µm thick in cross-
section. Cortex poorly developed, 10~20-µm thick. Photobiont
layer densely interspersed with calcium oxalate crystals,
70~90-µm thick. Crystalline layer more distinct below algal
cells, 40~70-µm thick. Medulla endoperidermal, indistinct
to absent; prothallus whitish.
Ascomata lirelliform, erumpent to prominent. Lirellae
completely covered by thalline margin (10~12-µm thick
apically), elongate and irregularly branched (negrosina morph),
up to 3cm long, with ends mostly acute to sub-acute.
Labia entire, black, appearing greyish in the cross-section
because of the thin cortex cover being absent from algal
cells. Disc slit-like, epruinose, concealed. Thalline margin
complete, sometimes flaking off and exposing black labia,
laterally 80~95-µm thick. Proper exciple entire, laterally
carbonized, convergent, apically 10 µm to laterally 60~
90-µm thick. Epihymenium greyish, crystalline, 15~20-µm
high. Hymenium hyaline, clear, 100~130-µm high, I.
Paraphyses simple, rather lax, apically granulate, ± conglutinate,
1~2-µm thick. Hypothecium hyaline, indistinct to 20-µm
high, I. Ascus clavate, 2~6-spored, 120~150 × 15~20 µm,
I. Ascospores hyaline, fusiform, clavate to ellipsoidal with
rounded to sub-acute ends, transversely 15~19 septate,
about 50~95 × 10~15 µm, locules lenticular, halo not seen,
I+ violet to blue.
Chemistry: Thallus and medulla K+ yellow turning red,
P+ yellow-orange, C, KC; norstictic (major) and stictic
acids (trace) detected in thin-layer chromatography.
Etymology: The specific epithet is named in honor of an
eminent lichenologist, Dr. D. K. Upreti, from the CSIR-
National Botanical Research Institute, Lucknow, India.
Distribution and ecology: The type locality is situated in
the central (or western) highlands (Tây Nguyên) of Vietnam,
more toward neighboring Cambodia, in Mt. Doi Sao of
Dak Lak Province. The region has many primitive forests
growing on basalt soil and is conserved as a protected area.
The new species was widely dispersed in large or small
patches on thick tree bark in an evergreen forest and
collected at a height of c. 1m from the tree base in semi-
exposed or shaded conditions. The other taxa sharing
similar microclimate at an elevation between 400~500 m
belonged to Chiodecton, Pyrenula, and Diorygma, in addition
to several associated members of foliicolous lichens.
The forest composition of Vietnam shares several
characteristics (vegetation, climate, habitat, and distribution)
with those of other southeast Asian countries and shows a
greater affinity toward the Indo-Burman region. Hence,
existence of the new species in lowland areas of Cambodia,
Laos, Thailand and the eastern part of India cannot be denied.
Remarks: The new species is well characterized by whitish
grey to greenish grey, loosely corticate thallus, lirellae with
apically thin, complete thalline margin (negrosina morph) and
Fig. 1. Graphis upretii (holotype). A, B, Habitat; C, Habit; D,
Ascomata (the arrow indicates the complete thalline margin);
E, Cross-section of ascomata; F, Ascospores (scale bars: A =
15 cm, B, C = 5 cm, D = 1 cm, E = 100 µm, F = 50 µm).
Graphis upretii, a New Species in Vietnam 19
entire labia, concealed disc, convergent, laterally carbonized
proper exciple, transversely septate ascospores of about
50~95 × 10~15 µm, 2~6-spored asci, and the presence of
norstictic and stictic acids as lichen substances.
G. upretii belongs to a group with taxonomic characteristics
that include an entire labia, laterally carbonized excipulum,
clear hymenium, and transversely septate ascospores. The
organism closely resembles G. longispora D. D. Awasthi &
S. R. Singh in having ± erumpent, elongate and irregularly
branched lirellae, a thallus containing norstictic acid, and
a similar geographical distribution (Indo-Burma region).
However, the latter differs in having a thick, but lateral
thalline margin, slightly larger ascospores reaching up to c.
130 µm in length, saxicolous habitat, and a thallus that
produces salazinic acid in place of stictic acid [11, 12].
Another similar species of the group is G. salacinilongiramea
Adaw. & Makhija, which has elongate and erumpent lirellae
and long ascospores that are comparable to G. upretii, but
is distinct in having a lateral thalline margin and produces
salazinic acid together with stictic acid. G. ajarekarii Patw.
& C. R. Kulk. is closely related to the new taxon in
producing norstictic and stictic acids, and has lirellae with
a concealed disc and epruinose labia, but differs markedly
in having very small ascospores of 15~45 µm in size.
G. assamensis Nagarkar & Patw resembles G. upretii in
having erumpent lirellae, complete thalline margin, concealed
disc, non-pruinose labia, the presence of stictic acid in the
thallus, and a similar geographical distribution, but differs
in having a completely carbonized proper exciple, smaller
ascospores of 45~70 µm, and a thallus that produces salazinic
acid in addition to stictic acid.
G. verminosa Müll. Arg. shares some characteristics with
G. upretii such as irregularly branched, erumpent lirellae
covered by an apically thin complete thalline margin, laterally
carbonized proper exciple, transversely septate ascospores,
and the presence of norstictic acid in the thallus, but
differs in having a striate labia and a thallus lacking stictic
acid as an associated lichen compound.
The thin and complete thalline margin of the new taxon
gives the appearance of a pruina, which differs in
composition, being made up of a dead hyphae and crystals.
However, in the cross-section of lirellae, a thin layer of
cortex lacking algal cells reaching apically can easily be
observed. The new taxon can easily be mistaken as the
pruinose Carbacanthographis, but non-amyloid ascospores
and spinulose periphysoids, which are characteristics of the
latter, are absent in G. upretii.
Additional specimen examined: Vietnam , D a k L a k
Province, Buon Ma Thuot City, Mt. Doi Sao, 12o40'31.8'' N,
108o05'24.4'' E, alt. 539 m, on tree bark, 19 Feb 2013, Oh &
Thanh, VN130042 (KoLRI).
Arthonia radiata (Pers.) Ach. (Fig. 2A)
K. Vetensk-Acad. Nya Handl. 29: 131 (1808).
Description: The corticolous species is characterized by
a lichenized, 55 to 75-µm thick, pale grey to olive, immersed
thallus delimited in patches; linear to aggregated, irregular
to substellate ascomata of 1~1.5-mm diameter; flat to
slightly convex, black, epruinose disc; brown or olive-
brown, hyaline, clear and gelatinous I+ blue hymenium, up
to 40-µm high; 8-spored, broadly clavate asci, 35~40 ×
14~16 µm; hyaline to grey-brown, oblong-ovoid to oblong,
transversely 3-septate, gelatinous, I ascospores, 14~16 ×
4~5 µm, and the absence of lichen substances. Arthonia
radiata is widely distributed across Europe, North America,
Asia, Africa, and New Zealand [13].
Specimen examined: Vietnam, Dak Lak Province, Buon
Ma Thuot City, Museum, 12o40'32.2'' N, 108o02'28.9'' E,
alt. 516 m, on tree trunk, 19 Feb 2013, Oh & Thanh,
VN130048 (KoLRI).
Brigantiaea tricolor (Mont.) Trevis. (Fig. 2B)
Spighe Paglie: 9 (1853).
Description: The species is characterized by a whitish
grey to grey green, effuse, indistinctly sorediate thallus;
sessile, round ascomata constricted at the base, 1~1.5 mm;
disc brownish, plane, covered by ± yellow pruina, with
prominent, shiny, reddish brown margin reacting K+ blue-
violet; biatorine exciple; hyaline, clear to slightly inspersed
hymenium, 120~130 µm; 1-spored asci, 90~100 × 30~45 µm;
hyaline, ellipsoidal to oblong, muriform ascospores, 65~
80 × 25~30 µm, and a thallus containing atranorin and
zeorin as the major lichen compounds. B. leucoxantha R.
Sant. & Hafellner differs from B. tricolor in having an
orange ascomatal margin reacting K+ purple, and a disc
containing yellow-orange pruina. B. tricolor is widely
distributed in Africa, Australia, eastern and southern Asia,
the Hawaiian Islands New Caledonia, and Papua New
Guinea [14].
Specimens examined: Vietnam, Kon Tum Province, Kon
Plong District, Mt. Kon Plong, PAK-SY waterfall, 14o35'46.1'' N,
108o15'24.3'' E, alt. 1,033 m, on dead tree branch, 21 Feb
2013, Oh & Thanh, VN130127 (KoLRI); Dak Lak Province:
Yok D o n Na t i ona l Par k , 12 o51'20.0'' N, 107o45'58.1'' E, alt.
c. 760 m, on tree trunk, 22 Apr 2012, Hur & Oh,
VN120228 (KoLRI).
Coenogonium implexum Nyl. (Fig. 2C)
Ann. Sci. Nat., Bot., Ser. 4. 16: 92 (1862).
Description: The species is characterized by filamentous
(very densely woven filaments of Trentepo hlia cells, 30~35
×14~16µm), pannose, ecorticate, yellow-green thallus, up
to 50 mm; sessile and round ascomata, 0.18~0.2 × 0.5~
1 mm; flat, yellow-orange; smooth cream-colored disc with
a thin margin; hyaline, paraplectenchymatous proper exciple
of radiating isodiametric hyphal cell rows, 40~70 µm;
hyaline, clear hymenium reacting I+ blue to sordid green
to reddish brown, 60~80 µm; 8-spored asci, 50~60 × 6~
7µm; hyaline, ellipsoid, 1-septate ascospores, 6~8 × 2~3 µm,
and a lack of lichen compounds in the thallus. C. implexum
is also distributed across the Neotropics, as well as in the
eastern Palaeotropics [15].
20 Joshi et al.
Specimen examined: Vi etnam, Vin h P huc Pro vince, Ta m
Dao National Park, 21o27'21.7'' N, 105o39'0.8'' E, alt. c.
1,092 m, on tree trunk, 25 Apr 2012, Hur & Oh, VN120324
(KoLRI).
Dirina paradoxa (Fée) Tehler (Fig. 2D)
Lichenologist 18: 296 (1986).
Description: The species is characterized by a whitish
grey, greenish grey to greyish white, pruinose, rimose
cracked, verrucose c. 100-µm thick thallus flaking off the
substratum and exposing loose white medulla; solitary to
aggregate, pluricarpocentral, discothecia, numerous, sessile,
circular to distinctly undulate ascomata constricted at base,
0.5~2.5 mm; dark brown, thinly white prinose disc; entire
to undulating thalline margin, 0.1~0.9 mm, thin to indistinct
proper exciple; hyaline and inspersed hymenium, 80~100 µm;
8-spored, clavate asci, 75~90 µm; hyaline, fusiform (one
end thick than other), transversely 3-septate ascospores,
20~23 × 4~6 µm, and the presence of erythrin, lecanoric
acid, and a yellowish brown unknown substance in the
thallus. The species has previously been reported in the
coastal regions of the Caribbean, in the Bahamas, Netherland
Antilles, Venezuela, and Trinidad [16].
Specimen examined: Vietnam, Dak Lak Province, Buon
Ma Thuot City, Museum, 12o40'32.2'' N, 108o02'28.9'' E, alt.
516 m, on tree trunk, 19 Feb 2013, Oh & Thanh, VN130046
(KoLRI).
Herpothallon sipmanii Aptroot, Lücking & Rivas Plata
(Fig. 2E)
Bibl. Lichenol. 99: 64 (2009).
Description: The species is characterized by a distinctly
byssoid, pale mineral grey to green or whitish green thallus,
± firmly appressed to the substrate; compact brown
hypothallus; a prothallus made up of radiating whitish
hyphae; numerous, pale to off-white, flattened to slightly
convex, disc-shaped (schizidia) outgrowths (pseudisidia) of
round to wavy margin, up to 1 mm in diameter, and the
presence of protocetraric and hypoprotocetraric acids. The
species is distributed in Papua, New Guinea, the Philippines,
and Thailand. For more details, see Aptroot et al. [17].
Specimen examined: Vietnam, Kon Tum Province, Sa
Thay district, 14o41'48.9'' N, 107o52'15.3'' E, alt. 768 m, on
tree trunk, 22 Feb 2013, Oh & Thanh, VN130040 (KoLRI).
Pertusaria pertusa (Weigel) Tuck. (Fig. 2F)
Enum. N. Am. Lich.: 56 (1845).
Description: The species is characterized by a pale grey
to greenish grey, ± shiny, smooth, wrinkled or warted
thallus delimited by a brown line; semi-globose, crowded
fertile warts constricted at the base, 1~2-mm in diameter;
immersed, perithecioid apothecia, 1~5 per wart; punctiform,
brownish disc; hyaline and clear hymenium, 300~400 µm;
2~4-spored asci; hyaline and simple ascospores, 100~140 ×
35~40 µm, and a thallus containing norstictic and stictic
acids. The species has been reported in Europe, Macaronesia,
Africa, and Asia [18].
Specimen examined: Vietnam, Dak Lak Province, Yok
Don National Park, 12o51'20'' N, 107o45'58.1'' E, alt. 760 m,
on tree trunk, 22 Apr 2012, Hur & Oh, VN120223 (KoLRI).
Sarcographina cyclospora Müll. Arg. (Fig. 2G)
Flora Jena 70: 425 (2887).
Description: The species is characterized by pale fawn,
thin, smooth, glossy thallus; lirellate ascomata immersed in
white, round to irregular stromata of 2~5 mm in diameter;
Fig. 2. New records of lichens in Vietnam. A, Arthonia radiata; B, Brigantiaea tricolor; C, Coenogonium implexum; D, Dirina
paradoxa; E, Herpothallon sipmanii; F, Pertusaria pertusa; G, Sarcographina cyclospora (the arrow indicates the stromatoid
ascomata) (scale bars: A~F = 1 mm, G = 5 mm).
Graphis upretii, a New Species in Vietnam 21
thin, black, ± open lirellae in irregular stellate clusters;
black disc covered by white pruina; non-carbonized, pale
yellow to brownish proper exciple; hyaline and clear
hymenium, 80~100 µm; 8-spored asci; pale brown to dark-
brown, narrowly ellipsoidal, 2 × 2-locular, I ascospores,
9~12 × 5~7 µm, and the presence of psoromic acid
chemosyndrome. This is the second record of the species
and has been previously reported only in Australia [8].
The collection of S. cyclospora from Vietnam increases the
possible distribution of this species in other neighboring
countries of tropics.
Specimens examined: Vietnam, Dak Lak Province, Buon
Ma Thuot City, Chu Yang Sin National Park (waterfall),
12o29'00.1'' N, 108o20'25.6'' E, alt. 450 m, on dry rock
(sandstone), 19 Feb 2013, Oh & Thanh, VN130022 (KoLRI);
Chu Yang Sin National Park, 12o27'57.0'' N, 108o20'34.9'' E,
alt. c. 780 m, on tree trunk, 21 Apr 2012, Hur & Oh, VN
120171 (KoLRI); Vinh Phuc Province, Tay Thien Mt.,
21o27'53.3'' N, 105o35'06.6'' E, alt. c. 77 m, on tree trunk, 26
Apr 2012, Hur & Oh, VN120377, VN120381 (KoLRI).
ACKNOWLEDGEMENTS
This study was supported by the National Research
Foundation of Korea (Grant #2011-0031494) and the
Korea National Research Resource Center Program (NRF,
2012M3A9B8021726). Santosh Joshi expresses his gratitude
to Dr. A. Aptroot for providing the lichen checklist of
Vietnam and Jung-Shin Park for the help in preserving the
study materials.
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A, Coppins BJ, Fletcher A, Gilbert OL, James PW, Wolseley
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... This species was also collected by Klaus Kalb in Northeastern Australia, who kindly sent us the material. In addition, revision of material of a record of Dirina paradoxa from Vietnam (Joshi et al. 2014) turned out to represent this species as well. A new species and genus is described below based on molecular and phenotypical data. ...
... Hence we performed a second analysis focusing on Malmideaceae. In the resulting tree (Fig. 2), the three specimens representing the new species clustered together in a strongly supported monophyletic group, supporting our re-identification of the Vietnamese material [recorded as Dirina paradoxa (Joshi et al. 2014)] as belonging to our new species. The new species, which is below described as Kalbionora palaeotropica, formed a strongly supported sister-group relationship to a clade including Malmidea, Savoronala, Lecidea plebeja, and L. cyrtidia. ...
Article
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A new species and genus, Kalbionora palaeotropica, is described for a crustose lichen occurring in coastal forests in Thailand, Vietnam, and northeastern Australia. It is morphologically similar to Malmidea and Eugeniella, but differing in morphological and chemical characters. The single known species in the new genus contains atranorin, zeorin, the stictic acid chemosyndrome and chlorinated xanthones. Morphologically it is characterized by having asci of the Catillaria-type, a yellowish brown colour, a granulose epihymenium, dark brown hypothecium, hyaline, 1–3 transversely septate ascospores. Molecular data strongly support a phylogenetic position in Malmideaceae, sister to a clade including Malmidea, Savoro-nala and two species currently placed in Lecidea s. lat. (including L. cyrtidia and L. plebeja).
... Aptroot & al., and Myriostigma candidum Kremp., together with some doubtful species records. Nguyen & al. (2011) recorded Arthonia accolens Stirt., while Joshi & al. (2014Joshi & al. ( , 2015 added Arthonia diorygmatis S. Joshi & Upreti, A. excipienda (Nyl.) Leight., A. radiata (Pers.) ...
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Arthonia complanata, A. elegans, A. pyrrhuliza, Arthothelium ruanum, A. spectabile, and Herpothallon minimum are newly reported from Vietnam. An identification key is provided to the 18 Arthoniaceae species known from Vietnam.
... Graphis Staiger (2002) is a major genus under the lichen family Graphidaceae, comprising of around 370 species worldwide (Kirk et. al. 2008, Lucking 2009, Joshi et al. 2010, Bárcenas-Peñta et al. 2014, Singh et al. 2014, Joshi et al. 2014. 111 species of Graphis are known from tropical, subtropical and temperate regions of India (Singh & Sinha 2010) and recent studies added 17 more species to the genus (Chitale et al. 2011, Singh & Swanlatha 2011a,b, Gupta & Sinha 2012, Singh et al. 2014. ...
... and P. pertusa (L.) Tuck. (Aptroot & Sparrius 2006, Joshi et al. 2014. ...
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