Mycol Progress (2013) 12:231–269
DOI 10.1007/s11557-012-0830-1
ORIGINAL ARTICLE
Phylogeny and taxonomy of the ‘manna lichens’
Mohammad Sohrabi & Soili Stenroos & Leena Myllys &
Ulrik Søchting & Teuvo Ahti & Jaakko Hyvönen
Received: 9 December 2011 / Revised: 17 May 2012 / Accepted: 23 May 2012 / Published online: 20 July 2012
# German Mycological Society and Springer 2012
Abstract We present ataxonomic revision of the ‘manna
lichens’ based on morphological, chemical, ecological and
molecular data. A large number of herbarium specimens and
fresh collections were examined. Phylogenetic analyses were
performed using nuclear ribosomal (nrITS, nrLSU) and mitochondrial small subunit (mtSSU) sequences. Some notable
phenotypic characters were plotted on the phylogenetic tree,
and the analysis reveals that some of these characters are useful
for genus and species level distinction of certain ‘manna
lichens.’ Phylogeny of the Megasporaceae was revised using
a combined data set of nrLSU and mtSSU and performing
parsimony and Bayesian analyses. Five genera (Aspicilia,
Circinaria, Lobothallia, Megaspora and Sagedia) are recognized. Further, the relationships of five presumably closely
related genera of ‘manna lichens’, namely Agrestia (vagrant),
Aspicilia (crustose) Circinaria (crustose), Chlorangium
M. Sohrabi : S. Stenroos : L. Myllys : T. Ahti
Botanical Museum, University of Helsinki,
P.O. Box 7, 00014 Helsinki, Finland
M. Sohrabi : J. Hyvönen
Department of Biosciences, University of Helsinki,
P.O. Box 65, 00014 Helsinki, Finland
M. Sohrabi (*)
Department of Biotechnology,
Iranian Research Organization for Science and Technology (IROST),
P.O. Box 15815-3538, 15819 Tehran, Iran
e-mail: mohammad.sohrabi@helsinki.fi
M. Sohbari
e-mail: msohrabi@myco-lich.com
U. Søchting
Department of Biology, University of Copenhagen,
Universitetsparken 15,
2100 Copenhagen Ø, Denmark
(vagrant) and Sphaerothallia (vagrant) with different growth
forms were analysed. The analyses revealed that ‘manna
lichens’ do not form a monophyletic group but occur in different clades within the genus Circinaria. The genera Agrestia,
Chlorangium and Sphaerothallia are assigned as new synonyms under the genus Circinaria and no vagrant or erratic
species remain in the genus Aspicilia. The analyses also show
that five new erratic, vagrant and crustose species can be
recognized. In this study two ‘manna lichens’, viz. Circinaria
rostamii sp. nov. (Azerbaijan, Iran and Turkey), and Circinaria
gyrosa sp. nov. (Armenia, Azerbaijan, Iran, Turkey,
Turkmenistan and Spain) are described as new to science.
Three potentially new species with crustose and erratic forms
need additional study. Aspicilia fruticolosofoliacea is reduced
to synonymy under C. alpicola, and a lectotype is designated
for C. aspera. Thirteen new combinations in Circinaria are
presented. The phenomenon of vagrancy is briefly discussed,
and the biogeography of the ‘manna lichens’ is outlined.
Illustrations, distribution maps, and an identification key to
the species are provided.
Keywords Aspicilia . Circinaria . Eurasia . Iran . ‘Manna
lichens’ . Sphaerothallia . Vagrant
Introduction
During the last two centuries, a group of vagrant species
with subfruticose and subfoliose thalli in the genus
Lecanora Ach., Sphaerothallia Nees and Aspicilia A.
Massal. has been termed ‘manna lichens’. Examples of these
species include, e.g., A. esculenta (Pall.) Flagey, A. fruticulosa (Eversm.) Flagey and A. vagans Oxner with their
synonyms. The term vagrant (or ‘vagant’) has been applied
by Büdel and Wessels (1986); Rosentreter (1993); Pérez
232
(1994, 1997a, b); Sohrabi and Ahti (2010), and Sohrabi et
al. (2011a, b) to describe the peculiar morphotype or growth
form of some lichens that have no proper substrate. Almost
all ‘manna lichens’ are vagrant. The informal term ‘manna
lichens’ is mostly associated with historical and ethnolichenological records rather than taxonomy. A brief history of
‘manna lichens’ and relevant references before 1901 were
summarized by Elenkin (1901d), and several other references
were also listed by Donkin (1980). In fact, this list is one of the
most comprehensive lists of references related to ‘manna
lichens’. In addition to the ‘manna lichens’, several species
of plants, insects and even fungi have also been thought to be
the source of the Biblical manna. The general circumscription
of the ‘manna lichens’ was outlined by Sohrabi and Ahti
(2010) and Sohrabi et al. (2011a, 2011b). In the nomenclatural
evaluation it was shown that several generic names, viz.
Agrestia J. W. Thomson (Thomson 1960), Chlorangium Link
(Link 1849) and Sphaerothallia (Nees von Esenbeck 1831)
have been used for ‘manna lichens’. Subsequently, all of these
were united under the conserved generic name Aspicilia by
Laundon and Hawksworth (1988). For ‘manna lichens’, the
genus name Aspicilia has been widely used in many publications and checklists (e.g., Elenkin 1901a, b, c, d, 1907;
Mereschkowsky 1911a, b; Oxner 1971; Andreeva 1987;
Kulakov 2002, 2003; Litterski 2002; Seaward et al. 2008;
Sohrabi and Ahti 2010; Sohrabi et al. 2010a, d;
Urbanavichus 2010; Sohrabi et al. 2011a,b). The genus name
Lecanora was used in the Catalogus Lichenum Universalis by
Zahlbruckner (1921–1940) and by Poelt (1969). The genus
Aspicilia was segregated from Lecanora based on a different
reaction of the ascus with iodine (I), Hafellner (1991a, b)
Recently, Nordin et al. (2010) revised the phylogeny of the
Megasporaceae using a combined data set of nrLSU and
mtSSU. They resolved the family as monophyletic within
the Pertusariales, supporting the previous results of Schmitt
et al. (2006), Lumbsch et al. (2007), and Lumbsch and
Huhndorf (2007). In the same study by Nordin et al. (2010),
the division of the Megasporaceae into the following genera
was proposed: 1) Aspicilia A. Massal., 2) Circinaria Link, 3)
Lobothallia (Clauzade & Cl. Roux) Hafellner, 4) Megaspora
(Clauzade & Cl. Roux) Hafellner & V. Wirth, and 5) Sagedia
Ach. Some important distinguishing characters of these
genera were also tabulated. Their results were mainly based
on fairly extensive sampling from the Megasporaceae,
Pertusariaceae and Ochrolechiaceae. They were, however, in
conflict with Miadlikowska et al. (2006), who proposed that
Aspicilia belongs to the family Pertusariaceae.
In Nordin et al. (2010) and Owe-Larsson et al. (2011) the
genus Circinaria Link was resurrected after 200 years and
several new combinations were proposed. For the first time
the segregation of two ‘manna lichens’, viz C. emiliae
(Tomin) A. Nordin, S. Savić & Tibell, and C. hispida
(Mereschk.) A. Nordin, S. Savić & Tibell from the genus
Mycol Progress (2013) 12:231–269
Aspicilia was presented. The newly revived genus Circinaria
is the fifth but the oldest one so far introduced for ‘manna
lichens’. In its resurrected form, the genus is quite heteromorphic and its generic type species C. contorta (Hoffm.) A.
Nordin, S. Savić & Tibell (syn. Aspicilia contorta (Hoffm.)
Kremp.) is saxicolous. The genus also includes several other
saxicolous species, i.e., C. arida Owe-Larss., A. Nordin &
Tibell., C. caesiocinerea (Nyl. ex Malbr.) A. Nordin, S. Savić
& Tibell, C. calcarea (L.) A. Nordin, S. Savić & Tibell, C.
contorta (Hoffm.) A. Nordin, S. Savić & Tibell, C. cupreogrisea (Th. Fr.) A. Nordin, S. Savić & Tibell, C. gibbosa (Ach.)
A. Nordin, S. Savić & Tibell, C. elmorei (E.D. Rudolph) OweLarss., and C. leprosescens (Sandst.) A. Nordin, S. Savić
& Tibell. All of these species, except C. elmorei, are
morphologically very distinct from ‘manna lichens’. For
example, the subfruticose species C. hispida and subfoliose species C. emiliae are distinguished from all of the
above mentioned saxicolous species by having a well
developed cortex (e.g., two layers in C. hispida) and thick
medulla, and by having pseudocyphellae and lacking secondary metabolites.
Subfruticose and subfoliose vagrant lichens (0 ‘manna
lichens’) are morphologically very distinct from both crustose
Aspicilia and Circinaria (sensu Nordin et al. 2010). For this
reason Sphaerothallia, with its subfruticose vagrant type species S. esculenta (Pall.) Reichardt, might be assumed to be an
appropriate generic name. This name has been used for ‘manna
lichens’ by some authors (e.g., Szatala 1957; Follmann and
Crespo 1974). It includes several subfruticose and subfoliose
vagrant species such as S. affinis (Eversm.) Follmann & A.
Crespo, (≡ Aspicilia vagans), S. aschabadensis (J. Steiner)
Szatala, S. emiliae (Tomin) Follmann & A. Crespo, S. fruticulosa (Eversm.) Follmann & A. Crespo, S. hispida (Mereschk.)
Follmann & A. Crespo, S. jussuffii (Link) Follmann & A.
Crespo and S. lacunosa (Mereschk.) Follmann & A. Crespo.
The genus also includes several crustose species such as S.
aspera (Mereschk.) Follmann & A. Crespo, S. desertorum
‘(Kremp.)’ Follmann & A. Crespo, nom. illeg., S. foliacea
(Elenkin) Follmann & A. Crespo and S. straussii (J. Steiner)
Follmann & A. Crespo. All of these species are morphologically, ecologically and chemically different from the present
circumscriptions of the crustose Aspicilia and Circinaria (sensu
Nordin et al. 2010). Therefore, the term ‘sphaerothallioid’ is
introduced here to unite this group of subfruticose and subfoliose vagrant or erratic species with few crustose species that
are characterized by a well-developed cortex, rather massive
medulla, large conidium size (c. 8–35 μm), distribution pattern
of the algal cells, presence of pseudocyphellae, absence of
aspicilin as a key lichen substance, as well as their ecological
preference for arid climatic conditions.
Büdel and Wessels (1986) stated that the facultatively
unattached species should be termed ‘erratic’ while the term
for the obligatory unattached lichens should be ‘vagrant’,
Mycol Progress (2013) 12:231–269
and we follow them here. Therefore, the substrate preferences and growth forms of sphaerothallioid species are as
follows: vagrant (0 obligatory unattached, seen only in
vagrant growth form), erratic (0 facultatively attached, primarily crustose on pebbles or basally attached to soil, and in
later stages partially vagrant, semivagrant or crustosevagrant), and crustose (0 obligately attached to soil or
rocks). The term ‘manna lichen’ is accepted here in its strict
sense, only for subfruticose and subfoliose sphaerothallioid
species with vagrant morphotypes and excluding any crustose
morphotypes. A saxicolous habit is not in accordance with the
biblical definition of manna, which is supposed to be edible
material and probably portable by wind (see also Sohrabi and
Ahti 2010). In addition to the typical thallus morphologies of
lichens, i.e., subfruticose, subfoliose and crustose some members of sphaerothallioid species develop a peculiar phenotype
which cannot be easily classified into any of the commonly
recognized types described in Grube and Hawksworth (2007).
Therefore, the term ‘amorphous’ is used here as subdivision
for subfruticose form to better describe the thallus shape of
some species (e.g., C. rostamii sp. nov.).
Sphaerothallioid species have never been comprehensively monographed. They are distributed throughout semiarid deserts and arid steppes in the Northern Hemisphere.
They can be found in the mountain steppes of the large
Irano-Turanian region (sensu Takhtajan 1986) as well as in
the arid steppes of North Africa, the semiarid steppes of the
Mediterranean region, the grasslands and shrublands of
southern Europe, and the arid shrub-steppes of northwestern
North America. Sphaerothallioid species are frequently
reported from continental deserts and steppes with saline
soils, low humidity, hot summers and cold winter with
below-zero temperatures. It is assumed that their thallus
morphology is able to transform in response to different
environmental conditions, and thus that they can grow on
the surfaces of small pebbles or else remain vagrant.
However, within both life-forms they retain their physical
mobility and are blown around by strong winds, washed into
depressions by rain water, or attached to the hoofs of some
animals (e.g., sheep and goats), in this way extending their
distributions.
Since the last century, the morphological and genetic
variations shown by some crustose and vagrant growth
forms have been a subject of debate. For instance,
Mereschkowsky (1918), Klement (1950), Weber (1967,
1977) and Kunkel (1980) proposed that crustose and vagrant morphotypes might be genetically connected.
The main goal of the present study is to clarify the
generic and infrageneric status of the ‘manna lichens’, mainly those species commonly or periodically treated under
Agrestia, Aspicilia, Chlorangium and Sphaerothallia, and
lately also Circinaria. We also attempt to clarify their relationships to allied saxicolous species of Aspicilia and
233
Circinaria. Another aim is to assess the pattern of vagrancy
among the sphaerothallioid species and also test the usefulness of molecular data for evaluating connections between
selected crustose and vagrant morphotypes of the erratic
species. Finally, we examine the consequences of the wider
sampling of sphaerothallioid species for phylogeny of the
Megasporaceae and the monophy of Sphaerothallia.
Material and methods
This study is based on approximately 500 herbarium and
fresh specimens and includes evaluation of anatomical,
morphological, chemical and sequence level characters.
The specimens examined were mostly obtained from the
following herbaria: ANES, ASU, B, C, CANB, CANL, E,
F, FH, FR, G, CBFS, GFW, GZU, H, H-NYL, HAL,
HMAS, IRAN, LE, M, MAF, MIN, MSK, O, PRA, S,
SPR, TNS, TSB,TU, TUR, TUR-V, UPS, US, and W (all
duplicates of Obermayer´s Lich. Graecenses No. 321 were
examined before distribution; therefore, all herbaria where
they were deposited are listed here). Herbarium acronyms
follow Thiers (2011). Additional specimens were from the
private herbaria of M. Sohrabi (hb. M. Sohrabi) and M.R.D.
Seaward (hb. Seaward).
The specimens were analysed by standard techniques
using dissecting and compound microscopes. External morphology was studied under a dissecting microscope. Thallus
anatomy (e.g., photobiont, conidia, ascospores and apothecia) was studied using a Leica Dialux 20 compact light
microscope and photographed with a Leica DFC490 digital
camera mounted on a Leica DM 2500 compact light microscope. For cortex observation pieces of thalli were cut using
a razor blade. Microtome sections (8–12 and 16–20 μm
thick) from thalli were prepared using a Leica CM 3050S
freezing microtome. These sections were mounted in lactophenol cotton-blue or water. All microscopy measurements
were made in water mounts. Measurements of external
morphology, i.e. thallus mass size and branch thickness,
were made with the digital vernier calliper. As a rule, ≥30
mature spores were measured from each specimen unless
otherwise indicated. Measurements were taken as described
in Sohrabi et al. (2010b). Exceptionally, in Circinaria emiliae, only a single apothecium was found and 10 ascospores
were measured. The general description of the external
morphology was based on dry material observed under a
dissecting microscope.
Chemical analyses of selected specimens were carried out
using thin layer chromatography (TLC), following Orange et
al. (2001) and using solvents A, B, and C. High performance
liquid chromatography (HPLC) was used as described in
Søchting (1997). Calcium oxalate was detected under the light
microscope by adding a drop of 10 % H2SO4 to a piece of
234
Mycol Progress (2013) 12:231–269
thallus (0.3–1 mm) and placing a cover-slip over it after 1–
2 min, causing the crystals to dissolve and recrystallize to
produce needle shaped crystals of calcium sulphate. The width
of conidia was frequently equal to or less than 1 μm and thus
smaller than the ocular scale of the microscope at ×1000
magnification. Occasionally they were found to be over 1.2–
1.5 μm. Therefore, only conidium length as well as the width
and length of the ascospores were recorded according to the
formula (min.–) arithmetic mean–SD–arithmetic mean + SD
(–max.). The term paraphysoids follows Roux et al. (2011),
Janex-Favre (1985) and Lumbsch (1997). Moniliform and
submoniliform are used as defined by Magnusson (1939)
and Owe-Larsson et al. (2007), and the presence of the epihymenium pigment ‘caesiocinerea-green’ follows Meyer and
Printzen (2000). Apothecia in vagrant forms of sphaerothallioid species are rare. A species was considered fertile if any
number of apothecia was observed on examined specimens,
otherwise it was considered sterile.
Distribution maps of species are based only on the vouchers examined. However, some literature records were evaluated, and omissions or corrections of doubtful records are
proposed. The geographical names (mainly country and some
provinces or cities) are in accordance with Room (2009),
Brummitt (2001) or Merriam-Webster's Geographical
Dictionary, 3rd rev. ed. 2001, when possible. Additional colour photographs and online distribution maps are available at
the Myco-Lich website (www.myco-lich.com) edited by
Sohrabi et al. (2010c).
were prepared. The following reaction conditions were
used: initial denaturation for 5 minutes at 95 °C, followed
by five cycles of 30 seconds at 95 °C, 30 seconds at 58 °C,
and 1 minute at 72 °C; in the remaining 30 or 35 cycles the
annealing temperature was decreased to 56 °C. Following
the last cycle a final extension step of 7 minutes at 72 °C
was included. For the primer pairs ITS1F, ITS1LM and
ITS4, ITS2KL, an annealing temperature of 56 °C in the
first five cycles and 54 °C in the remaining cycles was also
successfully used. For the primer pairs LR0R, LR7 and LR5
the annealing temperature was set to 55 °C during the first
five cycles and 52 °C in the remaining cycles. With some
minor variations, the annealing temperature for mtSSU1 and
mtSSU3R was set to 52 °C during the first five cycles and
52 °C in the remaining cycles. DNA concentrations of the
PCR products were measured using a Thermo Scientific
NanoDropTM 1000 Spectrophotometer. The PCR products
were sent to Macrogen Inc. (http://www.macrogen.com/) for
sequencing. For the majority of the obtained PCR products
purification was performed by Macrogen Inc. For some
samples PCR products were cleaned using the GFX PCR
DNA and Gel Band Purification Kit (GE Healthcare) following the protocol and eluting with 20–30 μl sterile water
included with the kit. DNA concentrations of the uncleaned
PCR products sent for sequencing were measured. The
primers used for the PCR reactions were also used for
sequencing. The obtained sequences were assembled with
SeqMan II version 4.0 (DNASTAR).
DNA extraction, PCR-amplification and sequencing
Sequence alignments
DNA was extracted from both fresh (up to 2 years old) and
old (30–75 years) specimens. Generally the medulla or a
small part of thallus was sampled. Total DNA was extracted
using the DNeasy Blood and Tissue Kit or Plant Mini Kit
(QIAGEN) according to the instructions given in the manufacturer’s protocol, except that the liquid nitrogen stage
was omitted. Full details are provided in Sohrabi et al.
(2010a, 2011b). For some specimens (e.g., Circinaria alpicola and C. cerebroides) the ITS1–5.8 S–ITS2 region was
also obtained using direct PCR, following Arup (2006). The
ITS1–5.8 S–ITS2 region was amplified using the primer
pairs ITS1F (Gardes and Bruns 1993) and ITS4 (White et
al. 1990), or ITS1LM (Myllys et al. 1999) and ITS2KL
(Lohtander et al. 1998). For PCR amplification of the
nrLSU region the primers LR0R, LR7 and LR5 (Vilgalys
and Hester 1990), and for the mtSSU region the primers
mtSSU1 and mtSSU3R (Zoller et al. 1999) were used. PCR
reactions were performed using ‘Ready-To-Go’ PCR beads
in 0.2 ml tubes (GE Healthcare). Twenty-five microlitre
samples containing 19 μl of sterile water, 4 μl of DNA
dilution, and 1 μl of each primer at 10 μM concentrations
A number of nrITS, nrLSU and mtSSU sequences of specimens from the families Ochrolechiaceae, Pertusariaceae and
Megasporaceae were obtained from GenBank (http://
www.ncbi.nlm.nih.gov). Altogether, 87 new sequences were
generated for this study, including 54 sequences of nrITS,
16 nrLSU and 17 mtSSU. Voucher information is provided
in Table 1. All new sequences have been deposited in
GenBank. The combined analysis of the data set of nrLSU +
mtSSU sequences included 67 (Fig. 1), and the nrITS data set
101 terminals (Fig. 2). The alignments were obtained using
the MUSCLE 3.6 web server (Edgar 2004) with the default
settings and then adjusted manually in PhyDE® (Phylogenetic
Data Editor, Müller et al. 2005). Ambiguously aligned regions
both in the nrLSU and mtSSU data sets were removed manually prior to the phylogenetic analyses. However, for the
nrITS data sets ambiguous alignment positions were removed
using the program Gblocks v. 0.91b, applying settings allowing for smaller final blocks, gap positions within the final
blocks, and less strict flanking positions (Castresana 2000).
Gblocks provides an objective and repeatable method for
excluding poorly aligned regions within multiple sequence
Mycol Progress (2013) 12:231–269
235
Table 1 Material used in this study. Vouchers, their geographical origin, and herbaria where vouchers are deposited are also listed. GenBank
accession numbers of the newly obtained sequences are in boldface
Species
Locality and collector number (Herbarium)
nrITS
mtSSU
nrLSU
Aspicilia
Aspicilia
Aspicilia
Aspicilia
Aspicilia
Aspicilia
Aspicilia
Aspicilia
Aspicilia
Aspicilia
Aspicilia
Aspicilia
Aspicilia
cernohorskyana
cinerea
cinerea
cinerea
cinerea
cupreogrisea
cyanescens
dendroplaca
dendroplaca
dudinensis
dudinensis
epiglypta
haeyrenii
Iran, South Khorasan, ex dupl. TARI 2311 (B)
Sweden, Östergötland, Nordin 5542 (UPS)
Sweden, Uppland, Hafellner 37308 (GZU)
Austria, Styria, Hafellner 40563 (GZU)
Sweden, Dalarna, Hermansson 13275 (UPS)
Sweden, Nordin 6046 (UPS)
U.S.A., California, Owe-Larsson 9151 (UPS)
Sweden, Torne Lappmark, Nordin 5952 (UPS)
Finland, Enontekiön Lappi, Nordin 6366 (UPS)
Sweden, Torne Lappmark, Nordin 6036 (UPS)
Sweden, Torne Lappmark, Nordin 5971 (UPS)
Sweden, Västergötland, Nordin 6303 (UPS)
Sweden, Torne Lappmark, Nordin 5997 (UPS)
–
–
AF332111
AF332110
EU057899
EU057903
–
–
–
–
–
EU057907
–
JQ797481
HM060696
–
–
HM060695
–
HM060707
HM060706
HM060720
HM060710
HM060719
HM060718
HM060717
JQ797496
HM060734
–
–
HM060733
–
HM060745
HM060744
HM060758
HM060748
HM060757
HM060756
HM060755
Aspicilia
Aspicilia
Aspicilia
Aspicilia
Aspicilia
indissimilis
laevata
laevata
mashiginensis
nikrapensis
Sweden, Torne Lappmark, Nordin 5943 (UPS)
Finland, Åland, Nordin 5846 (UPS)
Sweden, Uppland, Tibell 23659 (UPS)
Sweden, Hälsingland, Nordin 5790 (UPS)
Svalbard, Ebbestad SVL21 (UPS)
EU057909
–
EU057910
–
–
HM060708
HM060697
HM060692
HM060694
HM060746
HM060735
HM060730
HM060732
Aspicilia permutata
Aspicilia rivulicola
Aspicilia supertegens
Aspicilia supertegens
Aspicilia tibetica
Aspicilia verruculosa
Aspilidea myrinii
Circinaria affinis
Circinaria affinis
Circinaria affinis
Circinaria alpicola
Circinaria alpicola
Circinaria alpicola
Sweden, Torne Lappmark, Nordin 6027 (UPS)
Sweden, Torne Lappmark, Nordin 5957 (UPS)
Norway, Troms, Owe-Larsson 9002 (UPS)
Sweden, Torne Lappmark, Nordin 6023 (UPS)
China, Tibet, Obermayer 04386 (H, isotype)
Norway, Troms, Owe-Larsson 9007 (UPS)
Sweden, Jämtland, Nordin 6205 (UPS)
Russia, Astrakhan Region, Kulakov 1408 (M)
China, Xinjiang, Abbas 20081364 (H)
Russia, Astrakhan Region, Kulakov 1408B (M)
Kyrgyzstan, Aksai-Tal, Ringel & Jaschhof 5183 (H)
Kyrgyzstan, Tian-Shan, Ringel 5137 (H)
Kyrgyzstan, SW Tian-Shan, Ringel 5241 (H)
–
–
–
–
GU289915
–
–
HQ171237
HQ389194
HQ389196
JQ797524
JQ797552
JQ797554
HM060721
HM060709
HM060715
HM060704
HM060713
–
HM060703
HM060716
–
–
JQ797492
–
–
–
HM060759
HM060747
HM060753
HM060742
HM060751
–
HM060741
HM060754
–
–
JQ797502
–
–
–
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
alpicola
arida
arida
arida
aschabadensis
JQ797556
HQ406800
EU057905
HQ406801
–
–
–
–
–
–
–
–
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
aschabadensis
aspera
caesiocinerea
calcarea
cerebroides
cerebroides
cerebroides
contorta
contorta
contorta
contorta
contorta
Kyrgyzstan, Maltabar Mt., Litterski 4848 (H)
U.S.A., Arizona, Owe-Larsson 8759 (UPS)
U.S.A., Arizona, Owe-Larsson 8770 (UPS)
U.S.A., California, Knudsen 2046 (UPS)
Turkmenistan, Kopet-Dagh Mt., Borisova s.n. (LE)
Turkmenistan, Kopet-Dagh Mt., Borisova s.n.(LE)
Russia, Astarakhan Region, Owe-Larsson 9792 (H)
Sweden, Uppland, Tibell 22612 (UPS)
Sweden, Öland, Nordin 5888 (UPS)
Kyrgyzstan, Terskej Alatau, Ringel & Jashhof 5180 (H)
Kyrgyzstan, Innerer Tian-Shan, Ringel 5138 (H)
Kyrgyzstan, Aksai-Tal, Ringel 5184 (H)
Sweden, Öland, Nordin 5895 (UPS)
Austria, Styria, Hafellner 43516 (GZU)
Austria, Styria, Wilfling s.n. (GZU)
Finland, Vantaa, Pykälä 30701 (H)
Finland, Karjalohja, Pykälä 28872 (H)
JQ797519
GU289916
JQ797531
–
EU057898
JQ797529
JQ797534
JQ797553
EU057900
AF332109
AF332108
–
–
–
–
–
HM060693
HM060705
–
JQ797484
–
–
–
–
JQ797477
JQ797478
–
–
–
HM060731
HM060743
–
JQ797506
–
–
–
–
JQ797499
JQ797500
236
Mycol Progress (2013) 12:231–269
Table 1 (continued)
Species
Locality and collector number (Herbarium)
nrITS
mtSSU
nrLSU
–
HQ171236
HQ171230
HQ389200
HQ406802
JQ797551
JQ797542
JQ797526
HQ389203
–
JQ797512
JQ797513
JQ797479
–
–
–
HM060689
–
–
–
–
HM060691
HM060690
–
JQ797501
–
–
–
HM060727
–
–
–
–
HM060729
HM060728
–
JQ797511
JQ797510
JQ797535
HQ171226
HQ389195
JQ797485
–
–
–
–
JQ797493
–
–
–
–
JQ797486
–
–
–
–
HM060702
–
–
–
–
JQ797487
–
–
JQ797505
–
–
–
–
HM060740
–
–
JQ797504
–
–
–
–
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
contorta
digitata
digitata
elmorei
elmorei s.lat.
elmorei s.lat.
elmorei s.lat.
elmorei s.lat.
elmorei s.lat.
emiliae
emiliae
emiliae
Finland, Lohja, Pykälä 22463 (H)
Kyrgyzstan, Jangy-Jer Range, Ringel 5185-B (H)
Kyrgyzstan, Jangy-Jer Range, Ringel 5185 (H)
U.S.A., Nevada, Rosentreter 3689 (TU)
Russia, Astarakhan Region, Owe-Larsson 9814 (UPS)
Ukraine, Crimea, Vondrák 5671B (CBFS)
Iran, East Azerbaijan, Sohrabi 10128 (IRAN)
Iran, East Azerbaijan, Sohrabi 10405 C (IRAN)
Iran, East Azerbaijan, Sohrabi 10205 (hb. M. Sohrabi)
Kazakhstan, Atyrau, Kulakov 3798 (UPS)
Kazakhstan, Atyrau, Kulakov 3702 (UPS)
Kazakhstan, Atyrau, Kulakov 3702B (UPS)
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
esculenta
esculenta
fruticulosa
fruticulosa
fruticulosa
fruticulosa
Russia, Astrakhan Region, Owe-Larsson 9796 (UPS)
Russia, Astrakhan Region, Owe-Larsson 9796 (UPS)
Turkey, Anatolia prov., John 9538 (M)
China, Xinjiang, Abbas 2008363-a (H)
Iran, East Azerbaijan, Sohrabi 10405A (hb. M. Sohrabi)
Kazakhstan, Tarbagatai, Lange 5186 (H)
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
fruticulosa
fruticulosa
fruticulosa
fruticulosa
gibbosa
gyrosa
gyrosa
gyrosa
gyrosa
gyrosa
gyrosa
hispida s.lat.
Russia, Astrakhan Region, Kulakov s.n. (M)
Ukraine, Crimea, Vondrák 5670 (CBFS)
China, Xinjiang, Abbas 940001(H)
Ukraine, Crimea, Vondrák 5188 (CBFS)
Sweden, Uppland, Nordin 5878 (UPS)
Spain, Guadalajara, Printzen 8087 (FR)
Iran, Golestan, Sohrabi 9496 (hb. M. Sohrabi)
Iran, East Azerbaijan, Sohrabi 10085 (hb. M. Sohrabi)
Spain, Guadalajara, MAF-Lich 15363 (H)
Iran, East Azerbaijan, Sohrabi 10401A (hb. M. Sohrabi)
Turkey, Kırıkkale, John 11984A (M)
Iran, East Azerbaijan, Søchting 11187 (hb. M. Sohrabi)
HQ171228
HQ171227
JQ797555
HQ171229
HQ389199
EU05790
JQ797514
JQ797539
JQ797540
JQ797557
JQ797528
JQ797532
JQ797558
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
hispida
hispida
hispida
hispida
hispida
s.lat.
s.lat.
s.lat.
s.lat.
U.S.A., Wyoming, Muscha & Rosentreter 121 (SRP)
Russia, Kalmyk Region, Kulakov s.n. (M)
Greece, Mayrhofer 15811B (GZU)
Greece, Mayrhofer 15811A (GZU)
HQ171234
HQ389201
JQ797523
JQ797522
–
–
–
–
–
–
–
–
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
s.lat.
s.str.
s.str.
s.str.
s.str.
s.str.
hispida
hispida
hispida
hispida
hispida
jussuffii
jussuffii
lacunosa
lacunosa
leprosescens
leprosescens
rogeri
rogeri
Iran, East Azerbaijan, Sohrabi 10405 (IRAN)
Turkey, Malatya, Candan 11 (ANES)
Russia, Kalmyk Region, Ochirova s.n. (LE)
U.S.A., Idaho: Rosentreter 16233 & Cochrane (SRP)
Iran, East Azerbaijan, Sohrabi 10212b (hb. M. Sohrabi)
Iran, Golestan, Sohrabi 15099 (hb. M. Sohrabi)
Morocco, Vězda: Lich. Sel. Exs. No. 2381 (H)
Algeria, Esnault 2033 (GZU)
China, Xinjiang, Abbas 940003 (H)
Kazakhstan, South Peribalkhashya, Piregoudov s.n. (LE)
Sweden, Uppland, Nordin 5906 (UPS)
Sweden, Västergötland, Nordin 6059 (UPS)
U.S.A., Wyoming, Rosentreter 16373 (SRP)
U.S.A., Oregon, Rosentreter 16333 (SRP)
JQ797509
HQ406806
HQ171235
HQ389198
HQ389197
HQ171233
JQ797521
JQ797518
JQ797517
JQ797520
EU05791
–
HQ171231
HQ171232
–
HM060722
–
–
–
JQ797488
–
JQ797489
JQ797490
–
HM060711
HM060714
–
–
–
HM060760
–
–
–
JQ797503
–
JQ797495
JQ797494
–
HM060749
HM060752
–
–
Mycol Progress (2013) 12:231–269
237
Table 1 (continued)
Species
Locality and collector number (Herbarium)
nrITS
mtSSU
nrLSU
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
rostamii
rostamii
rostamii
rostamii
sp. 1
sp. 1
sp. 1
sp. 2
sp. 2
sp. 2
sp. 3
sp. 3
Iran, Semnan, Sohrabi 9364 (IRAN)
Iran, East Azerbaijan, Sohrabi 10212 (IRAN)
Iran, East Azerbaijan, Sohrabi 10095 (IRAN)
Iran, East Azerbaijan Sohrabi 10212 (IRAN)
Russia, Astrakhan Region, Owe-Larsson 9821 (UPS)
Iran, East Azerbaijan, Sohrabi 4758 (H)
Iran, East Azerbaijan, Sohrabi 10117B (hb. M. Sohrabi)
Iran, Semnan, Sohrabi 9380b (IRAN)
Iran, Semnan, Sohrabi 9380b (IRAN)
Iran, East Azerbaijan, Sohrabi 10092A (IRAN)
Iran, Semnan, Sohrabi 9347 (IRAN)
Iran, Semnan, Sohrabi 9357 (IRAN)
JQ797541
JQ797527
JQ797533
JQ797538
HQ389202
JQ797550
JQ797544
JQ797547
JQ797548
JQ797549
JQ797546
JQ797530
–
–
–
JQ797491
–
–
–
–
–
–
–
–
–
–
–
JQ797507
–
–
–
–
–
–
–
–
Circinaria
Circinaria
Circinaria
Circinaria
Circinaria
sphaerothallina
sphaerothallina
sphaerothallina
sphaerothallina
sphaerothallina
Iran, East Azerbaijan, Sohrabi 10117A (hb. M. Sohrabi)
Iran, East Azerbaijan, Sohrabi 3679 (H)
Armenia, Mayrhofer & Harutyunyan 13-491 (GZU)
Iran, Semnan, Sohrabi 9369 (hb. M. Sohrabi)
Iran, Tehran, Sohrabi 5083 (H)
JQ797543
JQ797537
JQ797525
JQ797545
JQ797536
–
–
–
JQ797476
–
–
–
JQ797508
Coccotrema coccophorum
Coccotrema maritimum
Coccotrema pocillarium
Lobothallia alphoplaca
Lobothallia alphoplaca
Lobothallia farinosa
Lobothallia melanaspis
Lobothallia radiosa
Lobothallia recedens
Lobothallia recedens
Megaspora verrucosa
Megaspora verrucosa
Megaspora verrucosa
Argentina, Prov. Neuquén, Messuti 2001(F)
Canada, British Columbia, Brodo 30130 (CANL)
U.S.A., Alaska, Printzen (ESS 20863)
Iran, East Azerbaijan, Sohrabi 4362 (H)
Iran, East Azerbaijan, Sohrabi 3677 (hb. M. Sohrabi)
France, Rhône-Alpes, Roux 25286 (UPS)
Sweden, Jämtland, Nordin 6622 (UPS)
Switzerland, Lumbsch (F)
Sweden, Nordin 6035 (UPS)
Sweden, Dalarna, Nordin 6582 (UPS)
Austria, Styria, Trinkaus (GZU)
Austria, Styria, Hafellner 48544 & Ivanova (GZU)
Iran, East Azerbaijan, Sipman 55434 (B)
–
–
–
JQ797515
JQ797516
–
HQ259272
–
HQ406807
–
AF332121
AF332122
–
–
AF329168
AF329163
AF329166
–
JQ797480
HM060723
HM060688
DQ780274
–
HM060724
–
–
JQ797483
–
AF274096
AF329164
AF274093
–
–
HM060761
HM060726
DQ780306
–
HM060762
–
–
JQ797498
Megaspora verrucosa
Megaspora verrucosa
Ochrolechia oregonensis
Ochrolechia parella
Ochrolechia tartarea
Turkey, Prov. Çorum, Kinalioglu 1679 (B)
Sweden, Jämtland, Nordin 6495 (UPS)
Canada, Schmitt (F)
France, Brittany, Feige (ESS 20864)
Scotland, Coppins (ESS 21493)
–
–
–
–
JQ797482
HM060687
DQ780276
AF329173
JQ797497
HM060725
DQ780308
AF274097
Ochrolechia yasudae
Ochrolechia yasudae
Pertusaria albescens
Pertusaria amara
Pertusaria amara
Pertusaria hemisphaerica
Pertusaria hemisphaerica
Pertusaria lactea
Pertusaria ophthalmiza
Pertusaria velata
Sagedia mastrucata
Sagedia mastrucata
Sagedia simoënsis
Culture 0217M (AKITA)
AFTOL-ID 882
Czech Republic, Bohemia, Schmitt (ESS 20967)
AFTOL-ID 379
Germany, Rheinland-Pfalz, Killmann (ESS 20865)
AFTOL-ID 959
Germany, Nordrhein-Westfalen, Schmitt (ESS 21065)
Germany, Rheinland-Pfalz, Schmitt (ESS 21070)
Scotland, Coppins (ESS 21498)
Australia, Archer (ESS 21500)
Sweden, Lycksele Lappmark, Nordin 5481 (UPS)
Norway, Troms, Nordin 5708 (UPS)
Norway, Troms, Owe-Larsson 9000 (UPS)
–
–
–
–
–
–
–
–
–
–
–
EU057914
EU057913
–
AY300899
DQ780282
–
AF329175
AY584713
–
DQ973000
–
AF381564
AY567993
AY300906
M060699
HM060698
HM060701
AY300848
–
DQ986776
AF329176
–
AF274101
–
AF381556
AF381557
AY568006
AY300855
HM060737
HM060736
HM060739
238
Mycol Progress (2013) 12:231–269
Table 1 (continued)
Species
Locality and collector number (Herbarium)
nrITS
mtSSU
nrLSU
Sagedia zonata
Sagedia zonata
Sagedia zonata
Sweden, Nordin 6006 (UPS)
Sweden, Nordin 5949 (UPS)
Norway, Troms, Owe-Larsson 8942 (UPS)
EU057952
EU057953
–
–
–
HM060700
–
–
HM060738
alignments, a procedure that has been shown to improve
phylogenetic accuracy in some cases (Talavera and
Castresana 2007). The Gblocks-modified nrITS data sets were
used for subsequent phylogenetic anlyses.
Phylogenetic analyses
Phylogeny of the Megasporaceae using a combined data set
(mtSSU + nrLSU) In order to study generic relationships of
the Megasporaceae we used a combined data set of nrLSU and
mtSSU sequences. Phylogenetic analyses were performed
using both parsimony and Bayesian inference. Selected taxa
from the genera Coccotrema Müll. Arg., Ochrolechia A.
Massal., Pertusaria DC. and Varicellaria Nyl. were chosen
as outgroup terminals and the tree was rooted at Coccotrema
maritimum Brodo. Bayesian analysis was performed using the
software MrBayes 3.1.2 (Huelsenbeck et al. 2001; Ronquist
and Huelsenbeck 2003). MrModeltest was used to determine
the most appropriate model using AIC, with GTR + I + G
found to be the best-fitting model of nucleotide evolution.
Two independent runs, each with four incrementally heated
simultaneous Markov chains and a temperature of 0.2 were
executed and run for ten million generations. Trees were
sampled every 1000 generations resulting in an overall sampling of 2002 trees. From these, the first 1001 trees were
discarded (burnin 0 1000). A stationary phase was reached
before the burn-in threshold, as revealed by the plot of the
MrBayes cold chain likelihood values against the generation
number. Trees were visualized using the program FigTree
v1.3. (http://tree.bio.ed.ac.uk/software/figtree/). In order to
obtain additional measures of branch support, we conducted
parsimony analysis using TNT 1.0 (Goloboff et al. 2008a, b).
Gaps were treated as missing data in the combined data
matrix. Branch support was assessed with 1000 bootstrap
replicates using tree bisection reconnection (TBR) branch
swapping with 100 random addition replicates in each replicate and holding 20 trees in memory during each round of
swapping. The topology of the parsimony and Bayesian trees
were congruent and only the Bayesian tree is shown (Fig. 1).
Phylogeny of ‘manna lichens’ and allied species using nrITS
rDNA To examine the infrageneric relationships of ‘manna
lichens’, nrITS rDNA sequences were obtained from several
of the earlier sampled genera such as Aspicilia, Agrestia,
Chlorangium and Sphaerothallia, and a data set with 101
terminals was assembled. Phylogenetic analysis was performed using Bayesian inference. Outgroup taxa were chosen from the genera Aspicilia, Lobothallia, Megaspora and
Sagedia and the tree was rooted at Lobothallia melanaspis
(Ach.) Hafellner. The genus Lobothallia was found to be the
sister genus to Aspicilia, Circinaria, Megaspora and
Sagedia in the analysis of Megasporaceae based on a combined data set of nrLSU and mtSSU sequences (see also
Nordin et al. 2010). MrModeltest suggested SYM + I + G as
the best-fit model of DNA substitution. For the Bayesian
analysis, parameters similar to those used for the combined
data set (mtSSU + nrLSU) were applied, and the resulting
trees were visualized using the program FigTree. The
majority-rule consensus tree is shown in Fig. 2. Branch
support values (PP ≥0.50) are indicated above branches.
Results
The family Megasporaceae The final data set consisted of
67 terminals with 1357 nucleotide positions and included
923 constant characters, 102 variable parsimony uninformative characters, and 332 informative ones. The strict consensus tree from the parsimony analysis was congruent with
the Bayesian tree. Twenty-seven internodes have bootstrap
values ≥75 %, and 34 have posterior probabilities ≥0.95
(Fig. 1). Relationships of the major lineages within the
Megasporaceae differ somewhat from those in Nordin et
al. (2010). Sagedia was confirmed as the sister genus to
Aspicilia. Furthermore, Aspicilia and Sagedia (sensu Nordin
et al. 2010) were recovered as sister to Circinaria and
Megaspora, and Lobothallia was placed as sister to all other
genera within the Megasporaceae; this is in accordance with
Nordin et al. (2010). Circinaria and Aspicilia are monophyletic
and sister groups (Fig. 1). The ‘manna lichens’ Sphaerothallia
esculenta (Pall.) Reichardt, Chlorangium jussuffii (Link) Link,
Fig. 1 The majority-rule concensus trees inferred by Bayesian analy-
sis of the combined data sets of the nrLSU and mtSSU gene regions
and using the GTR + I + G parameter model. The numbers above the
branches refer to bootstrap and posterior probability support values
(BS/PPS). Five genera are defined and indicated by distinguishing
morphological characters
Mycol Progress (2013) 12:231–269
239
0.04
Circinaria
‘Sphaerothallioid lichens’
1-4-6 rarely 8 spored ascus, subglobose, globose, some ellipsoid
present
Megasporaceae
Megaspora
absent
aspicilin in some
subfruticose, few crustose, medulla massive
aspicilin absent
thick, two layers in some
crustose
6–12 µm
8–35 µm
100/1.00
Family
Genera
Sagedia
Aspicilia
8 spored ascus, ellipsoid
absent
absent
thin, one layer
crustose, some radiating or lobate, medulla thin
absent
Lobothallia
Spore per ascus, shape
Thallus,medula mass
Cortex thickness
Conidia length
3–8 µm
8–12 µm
8–12 µm
99/1.00
11–40 µm
97/1.00
100/1.00
0.95
1.00
0.96
0.75
0.99
100/1.00
99/1.00
substictic acid present in some, aspicilin absent
Pertusaria ophthalmiza
Pertusaria albescens
Pertusaria amara
Varicellaria rhodocarpa
99/1.00
Pertusaria velata
0.82
Pertusaria hemisphaerica
100/1.00
Pertusaria lactea
Ochrolechia parella
100/1.00
0.75
Ochrolechia tartarea
1.00
Ochrolechia oregonensis
0.75
Ochrolechia yasudae
Aspicilia myrinii
Lobothallia melanaspis
95/1.00
100/0.95
Lobothallia alphoplaca
82/1.00 95/1.00
Aspicilia cernohorskyana
Lobothallia farinosa
0.55
Lobothallia radiosa
99/1.00
Lobothallia recedens
0.82
99/1.00
Sagedia mastrucata
99/1.00
Sagedia mastrucata
Sagedia simoensis
0.99
Sagedia zonata
63/086
Aspicilia cinerea
Aspicilia cinerea
99/1.00
100/1.00
Aspicilia dudinensis
Aspicilia dudinensis
83/1.00 Aspicilia indissimilis
Aspicilia laevata
Aspicilia laevata
Aspicilia haeyrenii
Aspicilia permutata
Aspicilia verruculosa
Aspicilia supertegens
0.74
Aspicilia supertegens
86/1.00
Aspicilia nikrapensis
0.86
Aspicilia rivulicola
61/1.00
Aspicilia mashiginensis
77/1.00
Aspicilia dendroplaca
67/1.00
Aspicilia dendroplaca
Megaspora verrucosa
100/1.00
Megaspora verrucosa
0.62
Megaspora verrucosa
Circinaria gibbosa
99/1.00
79/1.00
Circinaria leprosescens
Circinaria leprosescens
Circinaria contorta
Circinaria contorta
57/1.00
Circinaria contorta
Circinaria caesiocinerea
Circinaria calcarea
0.96
Circinaria elmorei s. lat.
1.00
Circinaria esculenta
0.60
Circinaria emiliae
85/1.00
Circinaria emiliae
71/1.00
Circinaria fruticulosa
94/1.00
Circinaria hispida s. str.
Circinaria hispida s. str.
0.55
Circinaria gyrosa
Circinaria cerebroides
0.75
Circinaria jussuffii
100/0.77
Circinaria sphaerothallina
Circinaria rostamii
0.78
Circinaria affinis
Circinaria lacunosa
68/0.94
100/1.00
Chemistry: substictic acid, aspicilin
Pseudocyphellae, clustered algal cells
Coccotrema maritimum
Coccotrema pocillarium
Coccotrema coccophorum
240
Mycol Progress (2013) 12:231–269
Lobothallia melanaspis HQ259272
Lobothallia alphopalca JQ797515
Lobothallia alphoplaca JQ797516
Aspicilia tibetica GU289915
Lobothallia recedens HQ406807
Megaspora verrucosa AF332121
Megaspora verrucosa AF332122
Sagedia zonata EU057952
Sagedia zonata EU057953
Sagedia mastrucata EU057913
0.52
Sagedia mastrucata EU057914
Aspicilia epiglypta EU057907
0.81
Aspicilia indissimilis EU057909
0.90
Aspicilia laevata EU057910
0.89
Aspicilia cinerea EU057899
Aspicilia cinerea AF332110
Aspicilia cinerea AF332111
Circinaria cupreogrisea EU057903
Circinaria gibbosa EU057908
Circinaria leprosescens EU057911
Circinaria arida HQ406801
Circinaria arida HQ406800
Circinaria arida EU057905
Circinaria calcarea EU057898
Circinaria calcarea HQ406804
0.80
Circinaria contorta EU057900
0.83
Circinaria contorta AF332108
0.60
Circinaria contorta AF332109
0.91
Circinaria sp HQ389202 C
SP1
Circinaria sp JQ797544 V
Circinaria sp JQ797550 C
Circinaria alpicola JQ797556 V
Circinaria alpicola JQ797554 V
Circinaria alpicola JQ797524 C
Circinaria alpicola JQ797552 V
Circinaria sphaerothallina JQ797537 C
0.51
Circinaria sphaerothallina JQ797525 C
Circinaria sphaerothallina JQ797536 C
Circinaria sphaerothallina JQ797543 C
Circinaria aschabadensis GU289916 V
0.98
Circinaria aschabadensis JQ797519 C
Circinaria aspera JQ797531 C
Circinaria jussuffii JQ797518 V
0.89
Circinaria jussuffii JQ797521 V
Circinaria gyrosa JQ797532
Circinaria gyrosa JQ797528
Circinaria gyrosa JQ797540
Circinaria gyrosa JQ797539
Circinaria gyrosa JQ797557
0.86
Circinaria gyrosa JQ797514
Circinaria fruticulosa HQ171226
Circinaria fruticulosa HQ171229
Circinaria fruticulosa HQ171227
Circinaria fruticulosa HQ171228
Circinaria fruticulosa HQ389195
Circinaria fruticulosa JQ797535
Circinaria fruticulosa HQ389199
Circinaria fruticulosa JQ797555
Circinaria affinis HQ171237 V
Circinaria affinis HQ389196 V
Circinaria affinis HQ389194 V
Circinaria sp JQ797549 C
SP2
Circinaria sp JQ797547 V
63/0.84 Circinaria sp JQ797548 C
Circinaria emiliae JQ797512 V
Circinaria emiliae JQ797513 V
Circinaria elmorei s.lat. HQ406802 C
Circinaria esculenta HQ406803 V
0.85
Circinaria esculenta JQ797511 V
Circinaria esculenta JQ797510 V
Circinaria lacunosa JQ797517
Circinaria lacunosa JQ797520
Circinaria cerebroides JQ797553
Circinaria cerebroides JQ797534
0.59
Circinaria cerebroides JQ797529
0.80
Circinaria rostamii JQ797541
Circinaria rostamii JQ797533
0.98
Circinaria rostamii JQ797527
Circinaria rostami JQ797538
Circinaria elmorei s.lat. HQ389203 C
0.60
Circinaria digitata HQ171230 V
Circinaria digitata HQ171236 V
Circinaria elmorei s.lat. JQ797558 C
0.80
0.96
Circinaria elmorei s.lat. JQ797542 C
Circinaria elmorei s.lat. JQ797526 C
0.89
Circinaria elmorei s.lat. HQ389200 C
0.70
Circinaria rogeri HQ171232 V
Circinaria rogeri HQ171231 V
Circinaria elmorei s.lat. JQ797551 C
Circinaria sp JQ797530 C
SP3
Circinaria sp JQ797546 C
Circinaria
hispida
s.str.
HQ406806
V
0.75
Circinaria hispida s.str. HQ171233 V
Circinaria hispida s.lat. HQ389201C
0.56
Circinaria hispida s.lat. JQ797509 C
Circinaria hispida s.str. HQ171234 V
Circinaria hispida s.str. Q171235 V
0.96
Circinaria hispida s.str. HQ389197 V
Circinaria hispida s.str. HQ389198 V
Circinaria hispida s.lat. JQ797522 V
Circinaria hispida s.lat. JQ797523 C
0.1
erratic or vagrant
Circinaria
vagrant
erratic or vagrant
0.92
Sphaerothallioid species
vagrant
erratic or vagrant
0.57
0.77
0.93
0.55
0.70
0.94
crustose
0.58
Mycol Progress (2013) 12:231–269
The majority-rule concensus trees produced by the Bayesian
analysis of the nrITS rDNA sequences and using the SYM + I + G
parameter model. Numbers above branches indicate posterior probabilities obtained from analysis. Branches in bold indicate PP ≥95 %.
Three species are designated as ‘Circinaria sp’ and will be described
elsewhere
Fig. 2
and Agrestia hispida (Mereschk.) Hale & W.L. Culb., were
included in the analysis and these type species of the old genera
were found to be nested within Circinaria. Therefore, these
genera are synonymized under Circinaria. Vagrant and crustose sphaerothallioid species form a separate clade of their own
(Fig. 1). Inside Circinaria clade some crustose species (C.
caesiocinerea, C. calcarea, C. contorta, C. gibbosa and C.
leprosescens) with certain morphological and chemical differences are distinguished from sphaerothallioid species and form
a small group of their own. Aspicilia cernohorskyana
(Clauzade & Vězda) Cl. Roux is nested in the Lobothallia
clade. Its formal combination of Lobothallia cernohorskyana
(Clauzade et Vězda) A. Nordin, Cl. Roux et Sohrabi was made
in Roux (2012).
241
paraplectenchymatous tissue that is indistinct in the inner part,
mixed with prosoplectenchymatous tissue of the medulla.
The results also show that C. elmorei and C. hispida s.str.
are not monophyletic. These two species remain in need of
more detailed study. Some taxa in this clade are crustose,
growing on pebbles (e.g., C. elmorei s.lat., C. hispida s.lat.)
while others are vagrant (e.g., C. digitata, C. hispida s.str.,
and C. rogeri). Circinaria sp. 3 is terricolous-crustose, and a
vagrant form of this species has not been found. C. hispida
s.str. in Fig. 2 refers only to the vagrant morphotype that is
shown to be morphologically corresponding with the type
specimen (TU). The C. hispida clade includes specimens
that are morphologically distinct from each other, although
these two forms do not form monophyletic groups. All
undescribed crustose species in Circinaria are represented
by multiple specimens. Since these species are primarily
crustose they will be studied separately and in detail elsewhere, together with additional saxicolous species.
Identifying sphaerothallioid species
‘Manna lichens’ and allied species This data set consisted
of 101 terminals with 437 nucleotide positions and included
255 constant characters, 43 variable characters that were
parsimony uninformative, and 169 parsimony informative
ones. The majority rule consensus tree resulting from the
Bayesian analysis with posterior probability support values
is shown in Fig. 2. The analyses resulted in 37 internodes
with posterior probabilities ≥0.95.
The basal clades include the following crustose species,
all of which lack pseudocyphellae and some of which contain aspicillin. These are Circinaria arida, C. calcarea, C.
contorta, C. cupreogrisea, C. gibbosa and C. leprosescens.
Sphaerothallioid species are divided into four clades. One of
these consists of an undescribed species (Circinaria sp. 1),
while another is formed by C. alpicola, C. aschabadensis,
C. aspera, C. jussuffii and C. sphaerothallina. C. fruticulosa
and C. gyrosa are combined in a clade of their own, with the
rest of the species forming a single clade. The relationships
of vagrant and crustose species remain unresolved. The
largest clade includes several vagrant species (C. emiliae,
C. cerebroides, C. esculenta, C. lacunosa and C. rostamii).
This clade also includes an undescribed erratic species
(Circinaria sp. 2), which is shown to be monophyletic, and
also a crustose species which is placed in a clade together with
C. elmorei and C. hispida. The results also show that species
with a distinct two-layer cortex (outer part paraplectenchymatous, inner part prosoplectenchymatous) are not monophyletic. For example, C. digitata, C. fruticulosa, C. hispida and
C. rogeri have two distinct layers in their cortices, although
they group together with other crustose species that have
single layered cortices. C. fruticulosa and C. gyrosa form a
clade, while C. gyrosa has an uneven cortex layer with
Important anatomical, chemical, ecological and morphological features for distinguishing the different sphaerothallioid
species are: 1) thallus growth form, 2) presence of pseudocyphellae, 3) presence and shape of lobes/branches/subsquamulose, 4) cortex thickness: presence/absence of two different
tissues (paraplectenchymatous and prosoplectenchymatous),
5) conidium size and 6) presence/absence of certain chemical
compounds (aspicilin, stictic acid and hypostictic acid).
Key to the world’s ‘manna lichens’
The first attempt to provide an identification key to the
‘manna lichens’ dates back to the middle of last century
(Szatala 1957) and the resultant work has subsequently been
improved by Poelt (1969), Oxner (1971) and Andreeva
(1987). The present revision shows that 15 species of ‘manna lichens’ can be distinguished and a key is presented to
cover them. Saxicolous forms are excluded from the key
until further data becomes available.
1 Thallus vagrant, subfruticose or subfoliose, surface
even, with shallow cracks, integrated, cortex thickness
uneven.........................................................................................2
─ Thallus vagrant, subfruticose, sometimes erratic (attached or imbedded in soil or invades pebbles), surface
uneven and detached, cortex thickness even when thallus
distinctly branched...............................................................5
2 (1) Thallus subfoliose, tube-like, wrinkled, c.10–40
(–50) mm wide, margin sometimes incised, often yellowish grey or muddy color, conidia (8–)9–11(–12)
μm..............................................................C. emiliae (Fig. 4b)
242
─ Thallus subfruticose, truffle-like, cerebriform, nodulose, strongly folded.............................................................3
3 (2) Thallus large, c.10–30(–40) mm wide; found in
high mountains (alpine zone), hard, surface without large
rounded pits, conidia (10–)12–13(–15) μm.......................C.
cerebroides (Fig. 4c)
─ Thallus medium sized, c.10–20(–30) mm wide; below
alpine zone...........................................................................4
4 (3) Thallus c.10–20(–30) mm wide, rather crumbly,
surfaces with rounded pits, larg up to 0.5–1.5(–2) mm
diam., conidia (8–)11–16(–21) μm, mostly found in
lowlands..........................................C. lacunosa (Fig. 4a)
─ Thallus c. 10–25(–35) mm wide, rounded to irregular,
folded in some parts, flexuose, often brain-like appearance,
with rimose surfaces and areole-like lobes, conidia (8–)10–
12(–16) μm...................................C. rostamii (Fig. 3e, f, h)
5 (1) Thallus broadly ellipsoidal to globose, gyroid, comprises brain-like lobes or forming compact subsquamulose
pieces, 5–40 mm wide.........................................................6
─Thallus more or less subglobose distinctly branched,
dwarfed form, 5–30 mm wide............................................13
6 (5) Thallus vagrant, subglobose to irregular, severely
wrinkled, forming compact subsquamulose pieces, surfaces
cracked, lobes pressing against one another........................7
─ Thallus often vagrant, rarely found erratic gyroid,
brain-like lobes....................................................................9
7 (6) Thallus forming compact pieces, small c. 3-15 mm
wide.........................................................................................8
─ Thallus forming undulating surface, large, c. 10–30(–40)
mm wide..................................................................................9
8 (7) Thallus vagrant, small (c. 3–8 mm), yellowish to
grey, apothecia abundant, pseudocyphellae uncommon, conidia (15–)17–22(–25) μm......................C. tominii (Fig. 4i)
─ Thallus vagrant, large (c. 3–15 mm), forming compact
subsquamulose pieces, more or less elevated in some parts,
often reddish brown (stictic acid and hypostictic acid present
in some thalli), pseudocyphellae whitish spots, dotting the
surface, conidia (8–)10–14(–16) μm........C. jussuffii (Fig. 4d)
9 (7) Thallus c. 10–40 mm wide, subsquamulose, forming
undulating surface, in large pieces (3–8 mm wide), often angular, uneven, wavy or bent, pieces densely joined together by
flexuose, thickened margins, apothecia and pycnidia rare, conidia (10–)18–30(–35) μm.....................C. esculenta (Fig. 4f)
─ Thallus c. 5–30 mm wide, gyroid, more or less irregular, surfaces forming short dumpy to conical lobes, undulating in some parts, verrucose..........................................10
10 (9) Thallus vagrant, forming brain-like lobes, pycnidia
rare, without carbonized ostiole.........................................11
─ Thallus often vagrant, sometimes erratic (invades pebbles), folded, forming short dumpy lobes, more or less
conical lobes, pycnidia common often erumpent, with carbonized ostiole...................................................................12
Mycol Progress (2013) 12:231–269
11 (10) Thallus folded, composed of tiny (0.7–1.5 mm)
dumpy lobes, somewhat depressed, conidia (15–)18–20
(–25) μm...................................................C. affinis (Fig. 5e)
─ Thallus more or less globose, dumpy lobes rather large
(0.7–3 mm), densely jointed, conidia (8–)10–16(–18)
μm.......................................................C. gyrosa (Fig. 3a, c)
12 (10) Thallus, medium sized, c. 5–12 mm wide, twisted in
some parts, surface somewhat warty to verrucose, more or less
areolate, apothecia and pycnidia abundant, conidia (8–)13–18
(–20) μm.............................................C. aschabadensis (Fig. 5d)
─ Thallus variable, c. 5–30 mm wide, appears more
or less branching form with distinct conical lobes, thallus erratic, (sometimes on pebbles), composed of areoles, apothecia and pycnidia rare, conidia (7–)8.2–10.5
(–12) μm..............................................C. alpicola (Fig. 4g, h)
13 (5) Branching polytomic, isotomic or anisotomic,
irregular, some branches occasionally dichotomic.............14
─ Branching commonly dichotomic, regular, sometimes
anisotomic with thin branches............................................15
14 (13) Thallus 10–20 mm wide, central branches
often thick, pycnidia common with conspicuous black
ostiole, conidia (7–)10–13(–16) μm..................C. rogeri
(Sohrabi et al. 2011b. Fig 2)
─ Thallus 5–10 mm, branches more or less single and
distinct, digitate, irregularly divided, pycnidia and conidia
not seen......................C. digitata (Sohrabi et al. 2011a. Fig 2)
15 (12) Thallus c. 5–20(–30) mm, well-branched mostly
dichotomic, often narrow to thick branches, radiating from
central part, branchlets slender, usually with hollow or small
depression on apices, pycnidia rare, usually located in depression at the uppermost part of branchlets, conidia (8–)9–12
(–13) μm............................................C. fruticulosa (Fig. 5f-h)
─ Thallus different, primarily terricolous (attached or
imbedded in soil) later stages turning vagrant, appear both
in vagrant and erratic forms...............................................16
16 (15) Thallus terricolous, with numerous branches,
mostly anisotomic infrequently dichotomic, often narrow
and cylindrical, with black tips on top of branches, conidia
8–12(–14) μm..............................C. hispida s.str. (Fig. 5a-c)
─ Thallus usually saxicolous (on rocks) or rarely terricolous (imbedded in soil) in later stages turning into vagrant
or erratic forms...................................................................17
17 (16) Thallus distinctly areolate, thorn-like extensions
elevated and elongated in some parts...........C. hispida s.lat.
─ Thallus more or less areolate, without thorn-like extensions (vagrant form not seen), conidia variable between
8 and 25 μm..................................................Circinaria spp.
Note: Several additional saxicolous or erratic species are
included in Circinaria spp., i.e. C. aspera, C. elmorei,
Circinaria sp. 1, Circinaria sp. 2, Circinaria sp. 3, and
Aspicilia (Circinaria) tortuosa (H. Magn.) N.S. Golubk.,
but will be studied in detail later.
Mycol Progress (2013) 12:231–269
Fig. 3 a-d Habit and habitats of Circinaria gyrosa in Iran. a C. gyrosa
(Sohrabi 9496, H, IRAN, hb. M. Sohrabi). b The habitat of the species
in open Juniper forest in Shah Kuh and Jahan Nama district in Golestan
Province. c C. gyrosa (holotype). d 32 km N of Marand towards Jolfa,
habitat of C. gyrosa on low calcareous rock outcrops in Astragalus
steppe. e-i Habit and habitats of C. rostamii in Iran. e-f Habit of C.
243
rostamii (holotype). g Habitat of C. rostamii in Jolfa district 1 km N of
Asiab Kharabeh waterfall, Stachys steppe with gravelly, loamy soil and
low calcareous outcrops. h-i Habit of C. rostamii (Sohrabi 9364, hb.
M. Sohrabi) and Zygophyllum steppe with gravelly soil in Semnan, c.
80 km S of Shahrud
244
Mycol Progress (2013) 12:231–269
Fig. 4 a Circinaria lacunosa (Piregoudov, LE). b C. emiliae (Savicz:
Lich. Ross. No. 115, H). c C. cerebroides (Ringel & Jaschhof 5184, H).
d C. jussuffii (Rabenhorst, Lich. Europaei, No. 199, H). f C. esculenta
(Savicz: Lich. Ross. No. 63 C, H). g C. alpicola (Litterski 4848, H).
h C. alpicola (Ringel & Jaschhof 5183, H). i C. tominii (Baranov, H)
The species
1907. ≡ Aspicilia alpinodesertorum f. esculenta-alpina
Elenkin in Izv. Imp. S.-Peterburgsk. Bot. Sada 1: 36. 1901
(16 July), as ‘esculenta alpina’ or ‘esculenta (alpina)’. 0
Aspicilia alpinodesertorum f. fruticulosofoliacea Elenkin in
Izv. Imp. S.-Peterburgsk. Bot. Sada 1: 27, 36, 39, tab. 2,
rows IX & X, figs. 1-7. 1901, as ‘fruticuloso-foliacea’ ≡
Circinaria alpicola (Elenkin) Sohrabi comb. nov. (Fig. 4g-h).
MB 563021
Basionym: Aspicilia alpicola Elenkin, Fl. Lishaynikov
Sredney Rossii [Lichenes Florae Rossiae Mediae] 2: 222.
Mycol Progress (2013) 12:231–269
245
Fig. 5 a-c Circinaria hispida s.str. (Sohrabi 15068, hb. M. Sohrabi, H). d C. aschabadensis (Borisova, LE). d C. affinis (Mereschkowsky, Lich.
Ross. Exs. No. 19, H). f-h C. fruticulosa (Obermayer: Lich. Graecenses No. 321, GZU)
Aspicilia fruticulosofoliacea (Elenkin) Sohrabi in Taxon 59:
627. 2010. Lectotype: designated by Sohrabi and Ahti
(2010), Kyrgyzstan. ‘Ad terram argillosam in regione
alpina montium Tian-Shan (Kaschgariae: Werchnij Syrt
12000 ft. ped)’, 1889, Roborowsky in Elenkin, Lich. Fl.
Ross. No. 24d (H, isolectotypes LE 4 specimens).
Thallus vagrant, subfruticose, consists of folding short
dumpy lobes, 0.5–2 cm tall and 0.5–2(–3) cm broad, often
irregularly shaped, rarely spherical, sometimes flat, rarely
flattened, regularly and plainly lobate, lumps consists of
short lobes, 0.2–0.6 cm, dense, compact, areole-like, verrucose, radiating from the central part. Axial part hard, variable in size, up to 1.5–5 mm in diam. Surface deeply
cracked, and often covered by dust, otherwise dull brown,
brownish grey to greyish green, sometime whitish grey, pale
olive-brown to pale brown; surface in covered side usually
darkish green, dark brown, greenish brown or almost dark
green-brown, (sometime reddish brown when ferriferous
sediments are present in soil). Pseudocyphellae common,
±white pit-like, conspicuous spots along the lobes. Cortex
246
thickness uneven, one layer, paraplectenchymatous, (40–)
60–90(–110) μm thick, cells (4–)6–7(–10) μm in diameter,
inner part indistinct, more or less prosoplectenchymatous
tissue, mixed with anticlinal hyphae of medulla. Epinecral
layer 4–10(–15) μm thick. Photobiont chlorococcoid, cells
5–8(–22) μm in diam., clustered in small groups, each group
up to 80–180×50–110 μm broad. Medulla prosoplectenchymatous with irregularly oriented hyphae (textura intricata), white, I-, containing crystals of calcium oxalate,
visible in (H2SO2 10 % solution). Apothecia immersed,
aspicilioid, rare, up to 0.5–1.5(–2) mm broad, among the
branches in older parts. Disc black to brownish black, pruinose, concave to convex when young, becoming more flat
when old. Thalline exciple flat to ± elevated and prominent
in older apothecia, entire, concolorous with thallus or with a
thin to thick white rim. True exciple (45–)65–85(–100) μm
wide, ± I + medially blue, uppermost cell brown, ± globose,
4–5(–7) μm in diam. Epihymenium brown, K + fading from
brown to light yellowish green, N + pale green (caesiocinerea-green). Hymenium hyaline, occasionally with few oil
drops, (100–)110–120(–130) μm tall. Paraphysoids moniliform to submoniliform, with upper cells ± globose, 4–7 μm
wide, in lower part 5–9 × 2–3 μm wide, branched.
Hypothecium and subhymenium pale, (40–)50–65(–75) μm
thick. I + blue. Asci broadly clavate, (75–)80–95(–100)×
20–30(–35) μm, with thick apical dome, up to (20–30 μm
thick); 2–4(–5) spored. Ascospores hyaline, simple, globose
to subglobose, (16–)19–[22.1]–24(–26)×(16–)19–[21.6]–
23(–25) μm (n030). Pycnidia rare, immersed, sometimes
occur in the pseudocyphellae, single, stretch flask-shaped,
ostiole frequently black to brownish but occasionally pale
brown and slightly raised, pale, internal wall colourless.
Conidia filiform, straight to very slightly curved (8–)9–11
(–13)×1–1.2 μm (n037). Chemistry: All spot-tests (K, C,
KC, CK, P) negative both in the cortex and medulla. TLC
and HPLC: No substances detected. UV: Negative.
Ecology and distribution (Fig. 6c). Circinaria alpicola is
widely distributed in Kyrgyzstan. It grows in vagrant form
on the gravely soil, but some specimens have been found on
pebbles as well. They are usually sparse forming scattered
populations. All examined specimens originated from high
altitudes in Tian-Shan Mountains that have a cold winter
climate. Alpine plants such as Festuca and Kobresia spp.
were reported as dominant in these habitats. According to
the data derived from the labels of examined specimens, C.
cerebroides and C. hispida are two other vagrant or erratic
species growing in similar habitats in Kyrgyzstan.
Remarks. The epithet ‘alpicola’ has been overlooked for
many years and it was recently resurrected by Sohrabi and
Ahti (2010). The lectotype of C. alpicola is poorly characterized (without fertile apothecium and conidia). It is aggregated into a compact, vagrant thallus and differs from the
type of Aspicilia fruticulosofoliacea by lacking conical and
Mycol Progress (2013) 12:231–269
short dumpy lobes. This type of dissimilarities of thallus
form is particularly evident in the mixed collection of both
species. Both taxa appear to be confined to alpine habitats in
the Tian-Shan Mountains. Therefore, Sohrabi and Ahti
(2010) recognized them as distinct taxa. In order to check
the affinity of A. fruticulosofoliacea with C. alpicola we
examined several collections, including fresh specimens,
and found that the conidia, ascospores, and ecology of both
species were identical. Nonetheless C. alpicola seems to be
a very polymorphic taxon representing high rate of plasticity
in some external features (e.g., lobe shapes). Molecular
study was conducted on fresh specimens of both variants
(see Figs. 3 and 4). These results supported the conclusion
that the two taxa are conspecific, and the lobe morphology is
not a reliable character to distinguish them.
C. alpicola is morphologically similar to C. gyrosa, a
new species which is described below. It seems that C.
gyrosa has different habitat preference and distribution. So
far C. gyrosa is known from steppes and shrub lands with
outliers in the Mediterranean area in Spain and SW Asia
(Armenia, Azerbaijan, Iran, Turkey and Turkmenistan) and
it was recorded at lower altitudes at c. 1000–2000 m, while C.
alpicola is an alpine species known from high altitudes of
Tian-Shan Mountains, recorded at c. 2000–4000 m. Our nrITS
analysis clearly showed that the two taxa are distinct (Fig. 2).
Additional literature reports. In Spain, reports of
Aspicilia fruticulosofoliacea Elenkin (nom. inval.) by
Barreno et al. (1998) and Sancho et al. (2000) most probably
refer to a species described as A. gyrosa. Some specimens of
C. alpicola have been misidentified as A. fruticulosa (syn. C.
fruticulosa) in Litterski (2002) and they are corrected here.
Specimens examined. Kyrgyzstan. Depression of Sonköl
Lake, 3023 m, 1970, Bredkina 445 (LE). Alai-Tal, S
(Berhalb) Fluss Kysylcy, W Berg Maltabar, Matten,
3400 m, 1999, Litterski 4848 (H). Tian-Shan, Kashgaria,
Roborowsky (LE). Central Tian-Shan, Moldo-Too, near
River Mengoush, c. 3100 m, 1970, Bredkina 434 (LE).
Vicinity of Bishkek, Ak-Say River, 2000 m, sine dato,
Fetisov (H), Central Tian-Shan, reach At-Bashi, Crosing
Kandi 3300 m, 1970, Bredkina (LE). Tian-Shan, NE AtBashi, c. 3 km from E Bosagu, 2700 m, 1970, Bredkina
(LE). Tian-Shan, At-Bashi, Kyndy velley, 3300 m, 1970,
Bredkina 558 (LE). Central Tian-Shan, 3820 m, 1949,
Kozlova (H). Central Tian-Shan, Sothern slope, At-Bashi,
valley of Ak-Say River, 4 km higher from Kyzyl-say River,
3300 m, 1970, Bredkina (LE). Tian-Shan, Samir Region,
high mt., in place like ‘Nomadic camps’, Ak-Say, 1903,
Lipsky (LE). Southwest Spor, of the Teskey Ala-Too Ridge
(S of Sanköl Lake), Kala Fiorgo, Dolon, 3040 m, 1970,
Bredkina (LE). Valley of Kalmak River, 3200 m, 1970,
Bredkina (LE). Fergansky Mountain, Ken-köl, EspeeTawo, c. 3000 m, 1911, Tagantsev (LE). Tian-Shan, AtBashi-Gebirge, pass (Ottotisch) im SW des Gebiges
Mycol Progress (2013) 12:231–269
247
Fig. 6 Known distribution of the ‘manna lichens’ in Eurasia and North Africa based on specimens of this study. The map outline was produced
using PanMap software (http://www.pangaea.de/software/PanMap/)
Hochgebirgssteppe, Grasland, 3300 m, 2000, Ringel 5137
(H). Alai-Gebirge, Paβ Talbyk, Matten, 3600 m, 1999,
Litterski 4802 (H). SW Tian-Shan, NE Abhange des
Fergana Gebirges, SW Chatyr-Kol, 3261 m, 2003, Ringel
5241 (H). Son-Köl-Plateau, Südufer der Son-Köl, 2007,
Ringel & Jaschhof 5179 (H). Terskej Alataou, Arabel-Suu
Hochebene, 3800 m, Ringel & Jaschhof 5181 (H). AksaiTal, Dshangy-Dsher, Karagerme Fluss, 3700 m, 2007,
Ringel & Jaschhof 5183, 5186 (H). Issyk-Kulskaya
Region, Sirtybakrovsky district, Karasay, 3200 m, 1957,
Popova (LE). Tian-Shan, Verkhnii Syrt, 3600 m, 1889,
Roborowsky (LE). Tian-Shan, Ak-Say, 3000 m, 1882,
Fetisov (LE), ibidem, 3300 m, Fetisov (LE).
Exsiccata. Kyrgyzstan. In valle Ak-Sai (10 000 ft. ped)
jugi Tian-Schan, ad fines Kaschgariae, 1882, Fetisov, in
Elenkin: Lich. Fl. Ross. No. 24i, as Aspicilia
248
alpinodesertorum f. fruticuloso-foliacea (H, LE, W). TianShan, the valley of Akh-Say River, 3300 m, 1862, Fetisov in
Elenkin: Lich. Fl. Ross. No. 24a, as Aspicilia alpinodesertorum f. fruticuloso-foliacea (H, LE L1987) ‘Ad terram
argillosam’ 1889, Roborowsky, in Elenkin: Lich. Fl. Ross. No.
24 h, as A. alpinodesertorum f. fruticuloso-foliacea (H, LE).
Circinaria affinis (Eversm.) Sohrabi comb. nov.
(Fig. 5e). MB 563034
≡ Lecanora affinis Eversm. in Nova Acta Phys. Med.
Acad. Caes. Leop. Carol. Nat. Cur. 15: 351. 1831.
Lectotype: designated by Sohrabi and Ahti (2010),
Kazakhstan. ‘Desertis Kirgisorum’ [1820], Eversmann in
Elenkin: Lich. Fl. Ross. No. 24e (H).
Thallus vagrant, subfruticose, almost subglobose, rarely
irregular in shape, sometimes slightly bent or convoluted, or
flattened, (0.5–)1–2.5(–3) cm in diam., wide, wavy, confluent, verrucose, with elevated areole-likes lobes, lobes at top
depressed or flattened, varying in size, 0.5–1(–1.5) mm
wide. Surface earthy, grey, grey-green, brick- to rustcoloured (when ferriferous sediments are presentin soil),
rarely yellowish brown and matt; with shallow to deep
cracks. Pseudocyphellae dot-like, rounded or extremely narrow, infrequently with whitish pruinose depressions. Cortex
indistinctly delimited, thickness uneven, paraplectenchymatous, (40–)60–90(–100) μm thick, cells (4–)5–8(–11) μm in
diam., ± brown, in some parts inner part indistinct, mixed
with prosoplectenchymatous tissue of medulla and usually
appearing as distinct layer (30–)40–80(–90) μm thick.
Epinecral layer 4–15(–20) μm thick. Medulla white, I–,
often muddy, depend on thallus size, 0.3–10 mm in central
core, consists of calcium oxalate crystals. Photobiont chlorococcoid, cells 5–15(–22) μm in diam., often in groups up
to 100–250×100–180 μm wide. Apothecia aspicilioid, rare,
often single, up to 1–2 per lobe, deeply immersed. Disc
black to brown, irregular in shape, rounded to fissure-like,
white-pruinose, concave, surrounded by very thick margin,
which is emergent, more or less flexuose, curved inside,
surrounded by thin white rim. Thalline exciple 0.2–0.9 mm
thick, entire or slightly cracked, more or less even or slightly
flexuose, curved inside. True exciple black-brown, 45–60(–
70) μm wide. Epihymenium brown, 15–30 μm tall, K +
colour fading from brown to yellowish green, contains
insoluble crystals of calcium oxalat, N + pale green (caesiocinerea-green). Hymenium colourless, 100–125 μm tall, I +
blue. Paraphysoids moniliform to submoniliform, tightly
conglutinate in hymenial gelatine, with upper cells ± globose, 4–5 μm wide, in lower part with ± cylindrical cell 4–
6×1.5–2.5 μm wide; occasionally branched. Hypothecium
and subhymenium colourless, 70–85 μm thick. Asci clavate, strongly thickened above, 95–120×25–35 μm, 2–3
(–4), with 1–4 spores. Ascospores almost globose, 18–
24 μm diam. Pycnidia common, immersed, sometimes
occur in the pseudocyphellae, single, stretched flask-
Mycol Progress (2013) 12:231–269
shaped, internal wall colourless, frequently with black
to brownish ostiole. Conidia filiform, straight to very
slightly curved (15–)16–20(–25) × 1–1.2 μm (n 049)..
Chemistry: All spot-tests (K, C, KC, CK, P) negative
both in cortex and medulla. TLC and HPLC: No substances detected. UV: Negative.
Ecology and distribution (Fig. 6h). Occurs between small
pebbles in stony steppes and deserts, sometimes on salty soil
in plains and mountain slopes of Central Asia. It is often found
in the same habitat with Circinaria esculenta and C. emiliae.
Associated plants include: Anabasis salsa, A. turanica,
Artemisia glauca, Atriplex cana, Camphorosma monspeliaca,
Haloxylon aphyllum, H. persicum, Kochia prostrata,
Nanophyton erinaceum and Salsola arbusculiformis.
Remarks. In some publications the name Aspicilia vagans
Oxner was used for this species (e.g., Oxner 1971, Andreeva
1987, Sohrabi and Ahti 2010, Urbanavichus 2010).
This was because of homonymy between Aspicilia affinis
Anzi and A. affinis (Eversm.) Mereschk. (see also Sohrabi
and Ahti 2010). Morphologically C. affinis is somewhat
similar to C. aschabadensis and C.gyrosa. All three species
have short dumpy lobes, verrucose thallus surface, with
uneven thickness in their cortex. Circinaria aschabadensis
is fertile, often with several apothecia per thallus, pycnidia
are abundant, erumpent, often with a carbonized ostiole,
sometimes located in the pseudocyphellae, and its conidia
are (8–)10–12(–16) μm. It is known from a very small area
in Kopet-Dagh, the area close to the border of Turkmenistan
and Iran. Circinaria affinis is often found sterile, and apothecia and pycnidia are very rare. Carbonized ostioles are lacking
in the pycnidia and conida size is (15–)16–20(–25) μm. Its
range is very wide, including many localities in Central Asia.
Circinaria gyrosa produces irregular, large, dumpy lobes, is
more or less brain-shaped, and has deep cracks and very large
pseudocyphellae. Its conidia are rather small, (8–)10–16(–18)
μm long. It is distributed in the Mediterranean area mostly in
the shrub-steppes of the mountains of Spain, Turkey and Iran.
Phylogenetic relationships of the three species are shown in
Fig. 2.
Additional literature reports. Circinaria affinis has been
reported from Central Asia by (Eversmann (1831;
Mereschkowsky 1911a, b)”. It is also reported from
Mongolia by Klement (1966). Mongolia by Klement (1966).
The record from Turkmenistan by Dzhuraeva (1978) needs to
be confirmed. The record by (Crum 1993) from Iran is referred to as C. aschabadenis (see also Sohrabi and Ahti 2010).
Circinaria affinis is also reported from Turkey (Berkeley
1856, as Lecanora affinis). The report by Berkeley (1856,
1857, as Lecanora affinis) most probably refers to C. gyrosa.
Reports from Kyrgyzstan by Bredkina (1981) need to be
confirmed. Some specimens of Aspicilia fruticulosofoliacea
(Litterski 2002; No. Litterski 4848, 4876, and 5137; H) have
been misidentified as A. vagans. They belong to C. alpicola.
Mycol Progress (2013) 12:231–269
The record Aspicilia affinis (Eversm.) Mereschk. (syn. C.
affinis) from Tunisian steppes by Seaward (1996) needs to
be confirmed.
Specimens examined. China. Xinjiang, Tacheng Toli,
1232 m, 2007, Abbas & Xahidin 20080364 (H).
Kazakhstan. Akmola Region, valley of Shebdar, 1957,
Andreeva (LE); ‘Asia Media, Deserto Kirkisorum’, 1822,
Fischer (G, LE). ‘Deserto Kirgizorum’, 1820, Eversmann
(G). Karagandinskaya Region, Aktogaysky district, KonurTobe, 1967, Leontieva (LE). Karkaralinsky district, mountain
range Konur Tobe, 1967, Leontieva (LE). Central
Khazakhstan, near Kanour Tobe, c. 25–30 km from village
Kenistan on SE direction, 1967, Leontieva (LE). Mountain
Berchogur, 1904, Dubiansky (LE). ‘Around the Caspian Sea’
(probably in N of the Caspian Sea in Russia), sine coll., in the
same envelope with C. fruticulosa (UPS). Saarat Mountain,
Cherichen, 1903, Keller (LE, W). Aqtöbe Region, East slope
of Mughalzhar Mts., Birshogir, 1904, Dubiansky (LE).
Mugoder, ‘Mugodzharskaya’ Mountain, N of Ust-Urt, near
Koshkar-Ata, 1904, Dubiansky (LE). Pesky Bolshye Barsuky
or Ust-Urt, 1904, Dubiansky (LE). Togayisk Region, 30 km N
of Lake Chalkar, 1898, Krukov (LE). Mongolia. Altai, the
road from Chench Somona to Bolghan Somon, c. 1500 m,
1981, Choy 5224 (LE). Govi-Altai aimag, ‘Gulin sum’ [no
such sum any more], 3 km along Zavkhan River from ‘Gulin’,
1978, Biazrov 8389 (LE). Russia. Altai Republic, Tarkhatty
River (tributary of Chuya), 1931, Rassadina (LE). Deserto
Czuensi, Altai Austro-Orientalis, 1926, Baranov (S), ibidem,
1929, Baranov (S). Altai, Ovrutsky Region, near Tarkhaty
River Chuy, 1931, Rasadina (LE). Astrakhan Region,
Aktobinsky Region, vicinity of Lake Bashkunchak, 1926,
Savicz (FH). Astrakhan, Berg Bogdo, 1927, Tomin (FH, S,
US), ibidem, 1926, Tomin (FH, H, S, TUR, US). Berg Bogdo,
1910, Mereschkowsky (TU, US, W). Astrakhan Region,
Bogdo Mt., semidesert, 1903, Keller (LE). Near the Lake
Baskunchak, 1903, Keller (LE). Near Lake Baskunchak, W
slope of mount big Bogdo, 1996, Kulakov 1408 (LE, M).
Akhtuba District, E shore of Baskunchak Lake, Vakh-Tau
Upland, 20 m, 1997, Kulakov (LE). Semipalatinsk Region,
Zaysansky uyezd, river Ul-kut-Togas, 1914, Prasolov (LE);
‘Tartaria’, sine dato & coll. (determined by Nees von
Esenbeck), in the same envelope with C. esculenta (UPS).
Uzbekistan. Fergana, near airport, 1948, Schafeev (LE)
Exsiccata. Kazakhstan. ‘Ad terram in deserto Kirgizorum’,
1820, Eversmann in Elenkin: Lich. Fl. Ross. 24e, as Aspicilia
alpinodesertorum f. affinis (H, LE, W). Regio
Actjubinskensis, montes Mugodzhary, prope ad terram cagatur, 1927, Krascheninnikov, in Savicz: Lich. Ross. 78, as A.
affinis f. alutacea (LE). Russia. [Altay Republic], Altai
Austro-Orientalis in Deserto Czuensi [Chuy Desert]’, 1926,
Smirnow, in Gyelnik, Lich. No. 69, as A. esculenta f. altaica
(H, TUR). Ad terram et inter lapides montis Bogdo prope
lacu Baskuntschak, in gub. Astrachan, 120 m, 1910
249
Mereschkowsky in Mereschkowsky: Lich. Ross. Exs. No.
19, as A. affinis (B, H, LE, TU, W, hb. M. Sohrabi).
‘Regio Astrachanensis, in viciniis lacus Baskunczak in decliviis montis Bogdo’, 1926, Savicz in Savicz: Lich. Ross. No.
167 (H). Regio Astrachanensis, in viciniis lacus Baskunczak
in decliviis montis Bogdo’, 1926, V.P. Savicz in Savicz: Lich.
Ross. No. 77, as A. affinis f. affinis (H)
Circinaria aschabadensis (J. Steiner) Sohrabi comb.
nov. (Fig. 5d). MB 563023
Basionym: Lecanora esculenta subsp. aschabadensis J.
Steiner in Ann. Mycol. 8: 227. 1910. Lectotype: designated
by Sohrabi and Ahti (2010), Turkmenistan. ‘Regio transcaspica: Aschabad [Ashgabat] ad fines Persiae’, sine dato,
Sintenis in Zahlbruckner, Lich. Rarior. Exs. No. 32 (error
‘39’) (W; isolectotypes B, LE, PC)
Thallus vagrant, invades tiny pebbles, subfruticose, up to
1–2(–3) cm long, (0.5–)1–1.5(–2) cm wide, folding with
tiny appressed warts forming areolete surface, lobes usually
wider up to 1.5–5 mm in diam., convoluted, verrucose, with
(0.3–)0.5–1(–1.5) mm in diam., dense, very compact, short
and dumpy, radiating from the central axial. Surface mudcovered, whitish to yellowish-grey, dull brown, brownish
grey to greyish green, sometimes pale olive-brown to pale
brown, ±white spots along the branches and often also on
top of the lobes. Pseudocyphellae common, white to grey,
conspicuous, often located on tip of lobes. Cortex thickness
uneven, one layer, paraplectenchymatous, (40–)60–90(–
110) μm thick, ± brown, cells (4–)5–7(–8) μm in diam.,
inner part prosoplectenchymatous, interrupted with anticlinal hyphae of the medulla. Photobiont chlorococcoid, cells
5–15(–18) μm in diam., clustered in small groups, each
group up to 60–180×50–110 μm broad. Medulla prosoplectenchymatous, with irregularly oriented hyphae (textura
intricata), white, I–, muddy in microtome sections, containing crystals of calcium oxalate. Apothecia aspicilioid (urceolate), sometimes appear crypto-lecanorine, deeply
immersed and surrounded by whitish rim. Disc black to
brown-black, concave to convex when young, becoming
more flat when old, often pruinose or sometime with thin
white pruina, 0.5–1 mm in diam. Thalline exciple flat to ±
elevated and prominent in older apothecia, entire, concolorous
with thallus or with a thin to thicken white rim. True exciple
(25–)35–85(–90) μm thick, ± I + blue, uppermost cell brown ±
globose, 4–5(–7) μm in diam. Epihymenium brown to dark
brown, K + fading from brown to light yellowish green, N +
pale green (caesiocinerea-green). Hymenium hyaline, occasionally with few oil drops, (100–)110–130(–150) μm thick.
Paraphysoids moniliform to submoniliform, with upper cells ±
globose, 4–7 μm wide, in lower part 5–9×2–3 μm wide,
slightly branched. Hypothecium and subhymenium pale,
(35–)45–70(–85) μm thick. I + blue. Asci broadly clavate, 2–
4 spored, more rarely 1–3–spored with thickened apex, I–, 70–
120 × 20–35(–45) μm Ascospores hyaline, globose to
250
subglobose, (15–)17.2–[21.0]–25.1(–29)×(14–)15.1–[18.6]–
22.1(–26) μm (n032). Pycnidia immersed, abundant, conspicuous (often occur in the pseudocyphellae), with black ostiole
slightly raised, globose to somewhat pyriform, internal wall
colourless, 0.1–0.2 mm in diam., occurring singly or a few
together. Conidia filiform, straight to very faintly curved,
(8–)10–12(–16)×1–1.3 μm (n030). Chemistry: All spot-tests
(K, C, KC, CK, P) negative both in the cortex and medulla.
TLC and HPLC: No substances detected. UV: Negative.
Ecology and distribution (Fig. 6d). Circinaria aschabadensis grows as vagrant but may rarely invade tiny pebbles. It has
been collected from two localities within a small area in the
Kopet-Dagh Mountains between Iran and Turkmenistan,
where there are arid and sub-arid mountains with steppe
vegetation and shrub lands with peculiarly subdivided topography. This species most probably grows also in the Firyuza
area, between Iran and Turkmenistan. According to
Kamakhina (1994) the diversity of mountain habitats in the
Firyuza drainage supports rich biological diversity still poorly
known. This is an area in Turkmenistan where many rare
species might be found.
Remarks. This species was described by Steiner (1910)
from Kopet-Dagh and after that there are no additional reports.
This species is easily recognized by its peculiar characters
such as whitish-grey colour, presence of black ostiole in its
pycnidia, and abundance of apothecia. This species was first
mistaken for other similar species, such as Circinaria affinis
(e.g., Crum 1993). Circinaria aschabadensis differs from C.
affinis by its shorter conidia (8–)13–18(–20) μm and lack of
greenish to greenish brown colour and exposed pseudocyphellae. Further, C. affinis has a wider range in central Asia.
Among Borisova’s collection (LE), a small number of
individual thalli were found on tiny pebbles. It shows that
some thalli uncharacteristically become crustose on pebbles.
All important characters such as colour, conidia and spore
size are exactly same as in vagrant thalli. The nrITS sequence of crustose specimen was identical with the sequence of vagrant specimen (see Fig. 2).
Additional literature reports. Iranian report of Circinaria
aschabadensis was provisionally excluded by Sohrabi et al.
(2010d) as uncertain locality for the species. To confirm the
report, further collections from the Iranian side of KopetDagh are needed.
Specimens examined. Turkmenistan. Central part of
Kopet-Dagh district, next to the border of Iran, stony part
of mountain to the SW of Solukli, 1934, Borisova (LE).
Circinaria cerebroides (Mereschk.) Sohrabi comb. nov.
(Fig. 4c). MB 563025
Basionym: Aspicilia cerebroides Mereschk. in Ann. Mag.
Nat. Hist., ser. 9, 8: 266. 1921. Type: Kyrgyzstan. ‘Turkestan,
prope Kaschgariae (Rossia)’, ?Roborowsky (not seen, ?KAZ).
Corresponding to original material: Icons in Elenkin, Izv. Imp.
S.-Peterburgsk. Bot. Sada 1: p.38, tab. 1, row IV, figs. 6, 8 and
Mycol Progress (2013) 12:231–269
row V, figs. 6, 7. 1901. Corresponding specimen: Kyrgyzstan.
Tian-Shan, 12 000 ft. ped, 1889, Roborowsky (LE).
Thallus vagrant, lumps subglobose to irregular, amorphous, resembles to tiny truffles, convoluted, variable in
size, 1–3(–4) wide, (0.5–)1–2.5(–3) cm thick. Lobes folded
forming large wide, entire, flexuose, rounded. Surface
smooth, muddy brown, grey-brown, or reddish brown
(when substrate soil contain ferriferous sediments), often
with very shallow cracks at the surface, rarely partly depressed. Pseudocyphellae common, pale, greyish brown
dot-like pits, rarely whitish or concolorous with thallus
surface. Cortex thickness uneven, one layer, paraplectenchymatous, 35–60(–80) μm, consists of isodiametric cells,
rounded to rounded-angular in section, thin-walled, with
lumen about (2–)3–6 μm in diam., inner part indistinct,
mixed with anticlinal hyphae of medulla and appears as
prosoplectenchymatous tissue. Epinecral layer a yellowish
brown zone, developed above cortex, 10–15(–30) μm thick.
Photobiont chlorococcoid, cells 5–15(–17) μm in diam.,
clustered in small groups, each group up to 80–160×50–
110 μm broad. Medulla prosoplectenchymatous, irregularly
oriented hyphae in the center and anticlinal hyphae between
algal clusters, white, I–, (in microtome sections appear as
white layer, very dence, up to 20 mm thick). Apothecia not
seen. Pycnidia very rare, deeply immersed, 1–2 in a lobe,
(65–)90–125(–140) μm in diam., punctiform, with pale
ostiole (35–)50–70(–85) μm in diam. Conidia colourless,
filiform, (10–)10–13(–15) × 1–1.2 μm μm (n 033).
Chemistry: All spot-tests (K, C, KC, CK, P) on thallus and
cortex negative both in the cortex and medulla. TLC and
HPLC: No substances detected. UV: Negative.
Ecology and distribution (Fig. 6a). Circinaria cerebroides grows on soil and is usually found among pebbles.
Known from the alpine range of the high mountains in the
central Tian-Shan. Grasses of the genera Festuca and Stipa
have been given as main associated plants. Some other
vagrant lichens such as C. alpicola and C. hispida occur
together with C. cerebroides.
Remarks. Circinaria cerebroides was first illustrated in a
plate by Elenkin (1901a; LE). Additional information on
this species is found in Mereschkowsky (1921). The species was examined closely and it is clearly distinguished
from other species of the genus by its unique appearance
(often resembles to small truffles). The species is at a first
glance somewhat similar to C. lacunosa, but the latter has
small rounded pits (1–2 mm wide) on the surface, and a
flabby medullary layer. According to available material,
C. lacunosa grows in the lowland regions (average elevation c. 200–1300 m) in Kazakhstan and China. Circinaria
cerebroides grows at higher altitudes, frequently above
3000–4000 m. According to the analysis of nrITS data
these two are distinct and group with other new species C.
rostamii.
Mycol Progress (2013) 12:231–269
Specimens examined. Kyrgyzstan. Tian-Shan, 12000 ft.,
1889, Roborowsky (LE). Terskej Alatao, Arabel-SuuHochebene, 3800 m, Ringel & Jaschhof 5180 (H). AksaiTal, Dshangy-Dsher, Karagerme-Fluss, 3700 m, 2007,
Ringel & Jaschhof 5184 (H). Innerer Tian-Shan, At-BashiGebirge, pass (Ottotisch), 3300 m, 2007, Ringel 5138 (H).
Exsiccata. Kyrgyzstan. Ad terram argillosam regione
alpina montium Tian-Shan (Kaschgariae: Werchnij Syrt
12000 ft ped.)", 1889, Roborowsky, in Elenkin: Lich. Fl.
Ross. No. 24d, as Aspicilia alpinodesertorum f. esculenta
alpina, in the same envelope with C. alpicola (W).
Circinaria digitata (Sohrabi & Litterski) Sohrabi comb.
nov. Figure in Sohrabi et al. (2011a). MB 563026
Basionym: Aspicilia digitata Sohrabi & Litterski,
Lichenologist 43: 41. 2011. Holotype: Kyrgyzstan. JangyJer Range (Dshangy-Dsher), Jal-Jyr River (‘Dshal-dshirFluss’), mouth of Archaly River (‘Artschaly-Mündung’),
on soil (‘epigäisch’), 41°18 15 N, 76°44 36 E, 2900 m, 6
July 2007, H. Ringel & C. Jaschhof 5185 (H).
See full description in Sohrabi et al. (2011a).
Circinaria emiliae (Tomin) A. Nordin, S. Savic & Tibell
in Mycologia 102: 1346. 2010. (Figure. 4b).
Basionym: Lecanora emiliae Tomin in Prir. Sel’sk. Khoz.
Zasushl.-Pustyn. S.S.S.R. 2 (3): 58 [reprint p. 4.]. 1928.
Lectotype: designated by Sohrabi and Ahti (2010),
Kazakhstan. Ural’skaya gub, [(Ural) Oral Prov.],
‘Inderskoe ozero’, July 1927, Emilia Keller 60 (LE L91).
Thallus vagrant, subfoliose, usually dorsiventrally flattened, diversely bent or folded marginally, occasionally
rolled up almost to a tube 1–4(–6) cm long, (0.4–)0.50–
0.75(–1.5) mm thick, usually irregularly thickened, wavy,
somewhat flattened in the middle, thin, margin thickened,
knobby at places, sometimes incised, rolled down, and
mostly tightly pressed to the lower side. Upper surface
yellowish grey, brownish, muddy, yellow-orange, matt,
smooth, slightly knobby here and there, with very low, flat
protuberances, or somewhat wrinkled, covered (particularly in
old specimens) with a net of shallow cracks (visible at 20–40×
magnification), about 0.12–0.25(0.75) mm wide, irregular in
shape, giving a somewhat scabrous appearance.
Pseudocyphellae rare, usually inconspicuous, pale (±white),
when getting wet appear as tiny dots. Cortex indistinctly
delimited, in some parts in two layers, upper part paraplectenchymatous, 25–45(–55) μm thick, with globose or rounded
cells, lumina 3.5–5(–6) μm wide, in inner part algal cells
sinking deeper into the medulla, a prosoplectenchymatous layer
develops over algal cells, usually 10–70 μm distanced from the
upper part. Epinecral layer brownish, 10–25 μm thick.
Photobiont chlorococcoid, cells 5–15(–20) μm in diam., arranged in an uneven to rather even layer and often clustered in
small groups (70–)100–130(–150)×(90–)100–200(–250) μm
broad. Medulla prosoplectenchymatous, with more or less irregular hyphae, white, I–. Apothecia very rare, all measurement
251
are based on a single apothecium in specimen at (hb.
Seaward115150). Disc black to brownish black, pruinose, c.
0.5 mm broad. Thalline exciple flat to ± elevated, entire, concolorous with thallus. True exciple (25–)35–45(–60) μm wide,
± I + blue, uppermost cell pale brown, ± globose, 4–5(–6) μm
in diam. Epihymenium brown, K + fading from brown to light
yellowish green, N + pale green. Hymenium hyaline, (80–)100–
120(–130) μm. Paraphysoids submoniliform, upper cells ±
globose, 4–7 μm wide, in lower part cells rectangular, 5–9×
2–3 μm wide, sometimes branched. Hypothecium and subhymenium pale, (30–)45–50(–65) μm thick. I + blue. Asci and
ascospores not found as mature. Pycnidia rare, immersed, with
whitish ostiole, flask-like to ± globose, inner part colourless.
Conidia simple, bacilliform and ± straight, colourless, (7–)9–12
(–14)×1 μm (n039). Chemistry: All spot-tests (K, C, KC, CK,
P) negative both in the cortex and medulla. TLC and HPLC: No
substances detected. UV: Negative.
Ecology and distribution (Fig. 6b). Circinaria emiliae is
vagrant and mainly found between small pebbles and salty
soils in semi-desert steppes of the central Asia. It has been
collected from the lowlands near Volgograd Region in Russia,
and from some localities near Almaty in Kazakhstan. Habitats
of this species are rather poorly known, however several plant
species, such as Artemisia glauca, Calligonum spp. and
Haloxylon aphyllum are reported as dominant plants in the
localities (see also Andreeva 1987).
Remarks. The subfoliose thallus is conspicuous in the
field. Thallus turns weakly brown or brownish-yellow to
green when wet. It is somewhat similar to the deformed
thalli of Dermatocarpon spp., but it can be easily distinguished by the absence of perithecia and other characters
such thallus cortex layer and clustered algal cells. This is the
only subfoliose member of ‘manna lichens’. The umbilicate
Aspicilia oxneriana is somewhat similar in morphology and
ecology with Circinaria emiliae, but it grows on calcareous
rocks and is frequently fertile. Additional information on
this species can be found in Savicz (1962).
Additional literature reports. The record from Turkey by
Candan and Türk (2008) needs further study. The reported
specimen by Biazrov et al. (1989) from Mongolia is confirmed here.
Specimens examined. Kazakhstan. Near Koshkarbay,
2009, Teshernyshev (hb. Seaward 115150). West
Kazakhstan Region, Ura'sk ('Yaitskiy gorodok'), Kalmyk
fort ('Krepost' Kalmykova'), 1769–1770, Pallas (H-NYL
3936, LE). Mongolia. Zavkhan [correctly Govi-Altai]
aimag, Taishir sum, right bank of Zavkhan River, c.
3 km N of Taishir Town, 1978, Biazrov 8364 (LE).
Exsiccata. Kazakhstan. Regio Gurjevensis, lacus jnder,
1927, G. S. Grigorijev, in Savicz: Lich. Ross. No. 115 (H,
TU, hb. Seaward).
Circinaria esculenta (Pall.) Sohrabi comb. nov.
(Fig. 4f). MB 563027
252
Basionym: Lichen esculentus Pall., Reise Russ. Reich. 3
(2, Anhang): 760, tab. 1, fig. 4. 1776. Lectotype: designated
by Sohrabi and Ahti (2010), [icon in] Pallas, Reise Russ.
Reich. 3 (2, Anhang): 760, tab. 1, fig. 4 (dextra) (1776).
Epitype: designated by Sohrabi and Ahti (2010) Russia.
‘Russia europaea, regio Stalingradensis [Volgograd
Region], in viciniis lacus Elton, declivium collis Ulagan’
1938, Leisle & Janischevsky, in Savicz: Lich. Ross. No.
63 C (H, isolectotypes LE, TU).
Thallus vagrant, globose-angular, subglobose or irregular
in shape, 1–3(–4) cm wide, formed undulating to compressed
subsquamulose, squeezed in appearance, subsquamulose
pieces 1–8 mm wide, 0.6–1.5 mm thick, edges flexuose, irregularly elevated, rounded, crenate, uneven, knobby or tuberculose, turned in or curved to wavy, closely adpressed by
their margins in exterior parts and completely concrescent in
interior parts. Surface olive-brown to grey-brown, or light grey,
muddy, or more rarely rusty red (when ferriferous sediments
are present in soil), rarely with some dove-coloured pruina on
the swelling parts. Pseudocyphellae common, ±white, dot-like,
normally visible on subsquamulose pieces. Cortex thickness
uneven, one layer, paraplectenchymatous, (40–)60–80(–100)
μm thick, ± brown, cells (4–)5–7(–10) μm in diam., inner part
mixed with prosoplectenchymatous layer derived from medulla; sometimes anticlinal hyphae expand over algal cells making
uneven layer up to 10–50 μm thicker. Epinecral layer 5–25(–
30) μm thick. Photobiont chlorococcoid, cells 5–20 μm in
diam., clustered in small groups, each group up to 80–160×
90–150 μm broad. Medulla paraplectenchymatous with more
or less irregular hyphae, white, pale, muddy color, containing
crystals of calcium oxalate. Apothecia urceolate or aspicilioid,
rare, up to 0.5–0.8(–1.2) mm wide, deeply immersed when
young, very slightly elavated when mature, 1–3 (rarely 5) per
subsquamulose, often located in older parts of the thallus. Disc
black to brownish black, densely white-pruinose, weakly concave or flat, more or less rounded, rarely irregular, up to 0.5–
1 mm wide, surrounded by strongly emergent, whitish, crenulate rim. Thalline exciple thin, slightly flat, but ± elevated,
entire, concolorous with thallus. True exciple (25–)35–45(–
85) μm wide, ± I + blue, uppermost cell light brown ± globose,
4–5(–7) μm in diam. Epihymenium brown, K + fading from
brown to light yellowish green, contains insoluble crystals of
calcium oxalat, N + pale green (caesiocinerea-green).
Hymenium hyaline, (90–)110–135(–155) μm thick.
Paraphysoids submoniliform or moniliform, upper cells ±
globose, 3–7 μm wide, in lower part cells rectangular, 5–7×
2–2.5 μm wide, often branched. Hypothecium and subhymenium pale, (45–)65–95(–110) μm thick, I + blue. Asci broadly
clavate, (80–)90–110(–120)×27–35 μm, with thick apical
dome 20–30 μm tall, 1–3(–4) spored. Ascospores more or less
globose, (20–)21.8–[25.3]–28.8(–33)×(19–)19.9–[23.0]–26.1
(–30) μm (n031). Pycnidia common, immersed, 1–2(–4) per
subsquamulose, stretched flask-shaped, punctiform, internal
Mycol Progress (2013) 12:231–269
surface colorless, often with black to brownish ostiole.
Conidia filiform, straight to somewhat curved (10–)13–26(–
35)×1 μm (n0143). Chemistry: All spot-tests (K, C, KC, CK,
P) negative both in the cortex and medulla. TLC and HPLC:
No substances detected. UV: Negative.
Ecology and distribution (Fig. 6f). This species is usually
found on loamy soil, sometimes also on salty soil, in between small pebbles and stony places in the lowland steppes
and deserts. It usually occurs at the average altitude of 200 m
in certain areas NE of the Caspian Sea (e.g., Astrakhan area),
where the soil is normally frozen for some months of the year.
Other ‘manna lichens’ such as Circinaria emiliae, C. fruticulosa, C. hispida and C. affinis are reported from these same
habitats. A list of additional associated lichen species was
summarized in Kulakov (2002, 2003) and Shustov (2006)
For example (Xanthoparmelia camtschadalis (Ach.) Hale, X.
subdiffluens Hale, and X. desertorum (Elenkin) Hale are aften
reported from same habitats. Some associated angiosperm
species are Artemisia pauciflora, A. glauca, A. sublessingiana, Anabasis salsa, and Salsola arbusculiformis.
Remarks. Circinaria esculenta was the first of the ‘manna
lichens’ described by Pallas (1776). Although C. esculenta
is a well-known ‘manna lichen’, it has a very complicated
nomenclatural history. This is due to the earlier wide concept of ‘manna lichens’, in which many of what we presently now identify as vagrant species, including C.affinis, C.
esculenta, C. fruticulosa, C. gyrosa and C. jussuffii, , as well
as a variant of the saxicolous species Aspicilia ‘desertorum’,
were included. We noticed that the material earlier referred
to C. esculenta was not homogeneous. Many of the specimens were referred to the saxicolous A. ‘desertorum’ sensu
Krempelhuber (1867), a crustose species with a massive
medulla. A. ‘desertorum’ has often been reported as a common species in the semiarid areas of Iran (Seaward et al.
2008) and Central Asia (Mereschkowsky 1911a, b;
Andreeva 1987; Dzhuraeva 1978). Recently C. elmorei,
another saxicolous species with a massive medulla, was redescribed from arid regions of North America by OweLarsson et al. (2011). It is morphologically more or less
identical to A. ‘desertorum’ sensu Krempelhuber (1867),
and most probably the two are conspecific. The application
of the name C. elmorei would reduce the nomenclatural
confusion surrounding the crustose A. ‘desertorum’ sensu
Krempelhuber (1867) and the vagrant A. esculenta. Our
observations show that C. elmorei is heteromorphic and probably includes some morphologically poorly known or undescribed species. Therefore, we decided to retain this
saxicolous group for the time being with a view to conducting
more detailed studies using multiple approaches including
analysis of morphological and molecular markers. Earlier
reports of both A. ‘desertorum’ sensu Krempelhuber and A.
esculenta need to be reviewed. Occasionally, the name C.
esculenta has erroneously been used for the North African
Mycol Progress (2013) 12:231–269
vagrant species C. jussuffii. This is due to the large variation
present in both species. For example, when the subsquamulose lobes of C. jussuffii are wrinkled, they greatly resemble to
C. esculenta. However, C. esculenta can be easily distinguished by its large thalli and subsquamulose lobes (c. 1–
5 mm), greenish grey colour and larger conidia (10–35 μm),
as compared to the smaller reddish or brownish thalli and
shorter conidia (up 8–16 μm) of C. jussuffii. In some thalli
of C. jussuffii secondary metabolites were detected.
Additional literature reports. The reports from Kyrgyzstan
by Litterski (2002), Bredkina and Makarova (2005), and from
Mongolia by Klement (1966), need to be confirmed. Some of
the available historical collections from Iran and Turkey examined in this study, many collectively named Aspicilia esculenta, were found to be crustose, and are referred to Circinaria
elmorei s.lat., a species currently under revision by Sohrabi et
al. (in prep.). The vagrant manna specimens report from Iran
by Göbel (1830 as Parmelia esculenta (Pall.) Spreng.) most
probably referable to one of the other two newly described
vagrant species C. gyrosa or C. rostamii). A disjunct population of C. esculenta was also found from the surroundings of
the Don River in southwest Russia. A report by Léveillé
(1842) and Kopachevskaya (1986) from the Ukrainian steppes
need to be confirmed.
Specimens examined. Kazakhstan. Prov. Ural [Oral] in
deserto Kirghisorum, Ak-Kerege, 1904, Dubiansky (G).
Mongolia. Zavkhan [correctly Govi-Altai] aimag, Taishir
sum, right bank of Zavkhan River, c. 3 km N of Taishir
Town, 1978, Biazrov 8370 (LE). Russia. Astrakhan, near
the Lake Baskunchak, 1926, Tomin (FH, H, S). Berg Bogdo,
1926, Tomin (S, UPS, US, W), ibidem, 1928, (US). Berg
Bogdo, 1910, Mereschkowsky (TU, UPS, US), ibidem,1920,
Keller (UPS), ibidem, 1927, Keller (US, W). Near the Lake
Baskunchak, W slope of mount big Bogdo, 1990, Sagalaev
(M). Berg Bogdo, Tartary ‘Tartaria’ sine loc. & dato. (determined by Nees von Esenbeck), in the same envelope with C.
affinis (UPS); Saratow Region, 1093, Keller (W); Volgograd
Region, near Lake Elton, Ulagan Mt., 1938, Leisle &
Yanishevskii (W). Uzbekistan. Bukhara, Zwockh (UPS).
Exsiccata. Kazakhstan. ‘desertis Kirgisorum’ Eversmann
1820, in Elenkin: Lich. Fl. Ross. No. 24c, as Aspicilia alpinodesertorum f. esculenta-tesquina (FH, H, W). ‘regio
Aktjubinskensis [Aktobe Prov.], montes cretacei Bish-tau in
steppa deserta’, 1926, Iljin in Savicz: Lich. Ross. No. 64, as A.
esculenta f. cretata (H, LE, TU, W). Regio Gurjevskensis,
montis Inder prope Akssaj. 1926, Iljin and Grigorjeff, in
Savicz: Lich. Ross. No. 65, as A. esculenta f. pallida (H,
LE). Russia. ‘Regio Astrachanensis, mons Bogdo prope
lacum Baskunczak, Declivia septentrionalia in steppa deserta
paulum saxosa’ 1926, ‘Ad ripas lacus Baskunczak, prope p.
Nizhnij Baskunczak, in steppa deserta ad terram salinam
structuram habentem’. 1926, ‘Regio Satlingradensis
(Volgograd Region) in viciniis lacus Elton, decliveium collis
253
Ulagan’, 1938, Leisle & Janischevsky in Savicz: Lich. Ross
No. 63A-C, as A. esculenta (H, TU, W). Astrachan, in declivibus montis Bogdo prope lacum Baskunczak, in Krypt. exs.
Vindobonensi. No. 3158, as A. esculenta (S, US). ‘Ad terram
et inter lapides montis Bogdo prope lacu Baskuntschak, in gub
Astrachan, 100 m, 1910, Mereschkowsky, in Mereschkowsky:
Lich. Ross. Exs. No. 18, as A. esculenta (B, TU, hb. M.
Sohrabi). ‘Ditio Astrachanensis. Distr. Wladimirskii, haud
procul pag. Nizhnij Baskunczak’, Ad terram, in steppis,
1962, Kopaczewskaja & Zubec, in Vězda: Lich. Sele. Exc.
No. 584, as A. esculenta (BM, H, S). ‘Regio Astrachanensis in
viciniis lacus Baskunczak in decliviis montis Bogdo’. 1926,
Savicz in Savicz: Lich. Ross. No. 66, as A. esculenta f.
ferruginea (H, LE, TU). ‘Auf Kreidebergen des Don-Flusses
ungefähr unter dem 48½ 0 nördl, Br. (Russland) Pitra in
Charkow’, in Rabenhorst Lich. Eur. No. 825, as
Chlorangium esculentum (B, FH, H, S, W).
Circinaria fruticulosa (Eversm.) Sohrabi comb. nov.
(Fig. 5f-h). MB 563028
Basionym: Lecanora fruticulosa Eversm. in Nova Acta
Phys.-Med. Acad. Caes. Leop.-Carol. Nat.Cur. 15: 352, tab.
78A. 1831. Lectotype: designated by Sohrabi and Ahti
(2010), Kazakhstan. ‘Desertis Kirgisorum’ [1820],
Eversmann (H-NYL 25676).
Thallus vagrant, subfruticose, convoluted, 10–20(–35)
mm wide, subglobose, with numerous branches, variable
in size (0.4)0.5–0.9(1.4) mm, often dichotomous, more or
less rounded to cylindrical, radiating in different directions
from the center, central axis sometimes up to 2–4 mm thick.
In uppermost part of branchlets dot-like depressions.
Surface blackish olive, greyish brown, earthy, sometimes
rusty red (when soil contains ferriferous sediments).
Pseudocyphellae common, white, conspicuous, often located at tip of branchlets. Cortex thickness even, distinctly two
layered, exterior part paraplectenchymatous (10–)15–25(–
30) μm thick, ± brown, cells (4–)5–6(–8) μm in diam., inner
part prosoplectenchymatous (25–)40–50(–65) μm thick.
Epinecral layer 5–15(–19) μm. Photobiont chlorococcoid,
cells 5–18(–22) μm, clusterd in groups of 100–250×90–
200 μm. Medulla I–, white, solid, sometimes wobbly, crystals of calcium oxalate not common. Apothecia cryptolecanorine, rare, in aggregates of 1–2(–3), at tips of short
branchlets, immersed when young, constricted at base when
mature, somewhat elevated, up to 2 mm wide. Disc brownblack, dark brown, with dense, thick dove-coloured pruina,
rounded, more or less flat, c. 0.8–1.5(–2) mm in diam.
Thalline exciple ± elevated and prominent in older apothecia,
entire, concolorous with thallus or with a thin to thickened
white rim. True exciple poorly developed, I + blue, 30–40
(–50) μm wide, evident only laterally, where it is colourless,
of short-celled hyphae; sometimes exciple inconspicuous.
Epihymenium brownish to dark brown, 15–30 μm tall, K ±
fading from brown to light yellowish green, N + pale green
254
(caesiocinerea-green). Hymenium hyaline, sometimes few oil
drop, 100–125 μm tall, colourless. Paraphysoids moniliform
to submoniliform, very thin, lower parts joined with ellipsoid
cells, 1.2–2 μm thick, uppermost cell broadly ellipsoid to
globose, 4–5.5 μm wide, often branched. Hypothecium and
subhymenium colourless, 30–50(–65) μm, I + blue, turbid of
granules, muddy, with soluble crystal in KOH. Asci clavate,
75–100×25–33 μm, with thick apical dome 20–30 μm tall,
3–4 spored. Ascospores hyaline, simple, broadly ellipsoid to
globose, (10–)17.2–[21.5]–25.9(–35)×(10–)16–[19.5]–23.9
(–30) μm (n035). Pycnidia rare, usually at tips of branchlets,
sometimes on pseudocyphellae, 0.1–0.15 mm. Conidia filiform, needle-shaped, straight, (8–)8–12(–16)×1–1.3 μm μm
(n039). Chemistry: All spot-tests (K, C, KC, CK, P) negative
both in the cortex and medulla. TLC and HPLC: No substances detected. UV: Negative.
Ecology and distribution (Fig. 6e). This true vagrant species is found on loamy or salty soil, sometimes in stony places
in lowland deserts and mountain steppes. The overall distribution of Circinaria fruticulosa is outlined by Oxner (1971)
including SE Ukraine, Russia (Bashkortostan, Volgograd and
Astrakhan Region), Central Asia (Kazakhstan, Kyrgyzstan),
Transcaspian Region (Turkmenistan), Caucasus regions and
North Africa. The species is found from lowlands to highlands. In Russia, Ukraine and Kazakhstan it is most frequently
found in the lowlands below the average altitude of 500 m. Its
highest recorded elevation is c. 1500 m in the NW of Iran,
Kyrgyzstan and China. The species has not been found in
North America. The American species provisionally known
as C. fruticulosa turned out to be a new taxon described as
Aspicilia rogeri (≡ Circinaria rogeri) in Sohrabi et al.
(2011b). Circinaria fruticulosa has been frequently collected
in Central Asia together with other vagrant taxa, e.g., C.
esculenta, C. hispida s.str. and C. affinis as well as saxicolous
species of the C. elmorei s.lat. Several plant species have been
reported as accompanying C. fruticulosa in Central Asia, e.g.,
Artemisia spp., Stipa capillata, Anabasis salsa, Salsola arbusculiformis, and Kochia prostrata (see also Andreeva 1987).
Remarks. This member of the ‘manna lichens’ is characterized by thalli with dichotomous patterns of branching, and lacking the black tips or spots in the topmost part
of the branchlets. Some of the branches are closely aggregated, rounded-cylindrical, slightly thickened at the
apex. Due to this thallus surface looks finely verrucose
to granulose. According to our observations, the average
size of thalli in the lowland populations is up to 3 cm,
which is generally larger than in highland populations,
which are often only up 1–1.5 cm. The low amount of
genetic variation found in the populations might suggest
that the morphological differences observed be some kind
of ecological adaptation for better surviving in higher
altitudes. This is comparable to some alpine plants (dwarf
forms).
Mycol Progress (2013) 12:231–269
Circinaria fruticulosa can rarely be confused with other
‘manna lichens.’ However, during past decades the name C.
fruticulosa (as Aspicilia fruticulosa) was used for some
vagrant specimens in Spain (Sancho et al. 2000; Llimona
and Hladun 2001). Our nrITS analysis clearly shows that
Spanish and Eurasian C. fruticulosa are two genetically
distinct taxa (Fig. 2). Spanish specimens together with other
specimens from Iran and Turkey are described as new
species (see C. gyrosa).
Additional literature reports. Circinaria fruticulosa (as
A. fruticulosa) from Turkey (Candan and Türk 2008) and
Morocco (Egea 1996) need to be confirmed. It has been
reported from Spain by numerous authors (see Llimona and
Hladun 2001). In this study, some of the voucher specimens
were examind (formerly reported in Follmann and Crespo
1974; Crespo and Barreno 1978; Follmann and Huneck
1968). Almost all of them were C. gyrosa. However, some
of the specimens were not accessible and therefore their
identification still needs to be confirmed.
Specimens examined. Algeria. ‘(Constantine), Plateau du
telegraphe, 1880’, Cosson & Rebaud (PC). China.
Xinjiang, Tuo Li County, Laofeng Kou, 1994, Abbas
940001 (H). Xinjiang, Tacheng Toli, 1232 m, 2008, Abbas
& Xahidin 20080363-a (H). Russia. Astrakhan Region,
Bolshaya Bogdo, 1952, Savicz (LE). Omsk Oblast,
Russkaya Polyana District, S of Stepanovka village, steppe,
1920, Knorring (LE), Berg Bogdo, 1910 Mereschkowsky
(US, W), Berg Bogdo, 1926, Tomin (FH, H, US), ibidem,
1927, Tomin (S), ibidem, 1928 Tomin (S, US). Berg Bogdo,
1920, sine coll. (US). Near the Lake Baskunchak, 1926,
Tomin (H, US). Bolshaya Bogdo, 1924, Kazekevish (LE).
Bogdo Mt., 1926, Savicz (FH). Near the Lake Baskunchak,
Vach-Tau, 1997, Kulakov (M). Bolshaya Bogdo, 1952,
Nashli (LE). Berg Bogdo, 1910, Mereschkowsky (H, UPS,
US); Volgograd, Lake El’ton, Ulagan Mt., 1938, Leisle &
Yanishevskii (LE), Volgograd Region, Kalachovsky district,
vicinity of Bolshegolubinsky garden. Northern slope of the
River Bolshaya Golubaya, 1994, Kulakov (LE); Kalmyk
Republic, Sarpinsky district, Kirowsky village, 2002,
Ochirova (LE). Orenburg Region, Kovkenski district, near
the village sosnovka, 2002, Merkulova (LE). Ad terram in
viciniis Sarepta (Saratowsk Region), 1864, Becker (LE).
Sarepta, sine coll. (H-NYL 25679). Kazakhstan,
Akmolinskaya district, 12 km to the north Ladizhenka,
1954, Isachenko (LE). Akmolinskaya district, 25 km to the
south of Akmola, 1954, Isachenko (LE). Akmola Region,
Atbassar district, Togushkensky mt. along Ter Akken River,
1904, Gordiagin (LE). Akmola Region, Omsky district,
1920, Kroing (LE, US). Atbassar district, Arganat Mt. on
the left bank of Bazay River, on the foot of Mukty-Yuy,
1904, Gordiagin (LE). Atbassar district, Karaganda Region,
saline lands in semideserts by the military post Kokchetav
[Kökshetau Town], on Ulutau-Atbasar road, 1914,
Mycol Progress (2013) 12:231–269
Ganeschin (LE). Along the beach of Obala Lake, 1914,
Ganeschin (LE). Karakaralinsky district, mountain range
Konurtobe, 1967, Leontieva (LE). Aqtöbe Region, east
slope of Mughalzhar Mts., Birshogir, 1904, Dubiansky
(LE). Pavlodar Region [Prov.], Kaganovich [Assu] district,
120 km from Pavlodar, terraces of the Lake Altybai-Sor, 1938,
Smirnova (MSK). Karaganda, Aktogaysky district, about 4–
5 km, SW of village Birlestyk, 1967, Leontieva (LE). ‘Deserto
kirgizorum, Eversmann 1820, (B, FH, H-NYL 25676).
Aktyubinsk, Aktyubinskaya Region, Chelkarskay district,
Mountains Kizil-choku elong Sarlibay-Sago river, inflose into
Chit-Irgiz, 1927, Krasheninnikov (LE); Tarbagatai, nordwest.
Vorgebirge, c. 40 km E Stadt Tarbagatai, 1000 m, 2001, Lange
5186 (H). Iran. East Azerbaijan, Kaleybar district: 35 km S of
Kaleybar along road to Ahar, 1750 m, 2007, Sohrabi et al.
10405A, ibidem, Sipman et al. 55488 (B, H, IRAN, UPS).
Mongolia. Zavkhan [correctly Govi-Altai] aimag, Taishir
sum, right bank of Zavkhan River, c. 3 km N of Taishir
Town, 1978, Biazrov 8371 (LE). Turkey. Casikoporan,
Surmalinsky district, Iravanskay Region, 1896, Koenig , filed
in the same envelope with C. gyrosa (LE). Ukraine. Peninsula
Taurica. ‘In decliviis Stepposis Tauriae borealis in viciniis
pag. Monoj’, 1932, Kozlov (TUR); Crimean Peninsula,
Alupka, Aj-Petrinskaja jajla c. 1 km SE of Bedene-kyr Mt.,
c. 1100 m, 2006, Vondrák 5188, 5258 (CBFS), ibidem,
Vondrák 5670 & Šoun (CBFS), Crimea, Simpheropol steppes,
1910, Mereschkowsky (H); "Ad terram calcaream inter rupes
calcareas e viciniis Theodossiae in peninsula Taurica, 1893,
Lipsky (station G in envelope) (LE).
Exsiccata Russia. Regio Astrachanensis, in viciniis lacus
Baskunczak in decliviis montis Bogdo, 1926, Savicz in Savicz:
Lich. Ross. No. 95, as Aspicilia fruticulosa (H, FH, TU, W, hb.
Seaward). Regio Astrachanensis, in viciniis lacus Baskunczak
in decliviis montis Bogdo, 1926 Savicz, in Savicz: Lich. Ross.
No. 96, as A. fruticulosa f. ferruginea (FH, H, LE, TU, W). Ad
terram et inter lapides montis Bogdo prope lacu Baskuntschak,
in gub Astrachan, 1910, Mereschkowsky, in Mereschkowsky:
Lich. Ross. Exs. No. 20 (H, TU, W). "Baschkirarss, districtus
Zilairsky, collis (ssopka) invalle fluminis Tanalyk non procul p.
Mambetova, ad terram inter lapides", 1929, Krascheninnikov,
in Savicz. Lich. Ross. No. 54, as A. fruticulosa (FH, H, TU, US,
W). "Ad terram in viciniis Sarepta (Gub. Saratowsk), 1864,
Becker, in Elenkin: Lich. Fl. Ross. 24f, as A. alpinodesertorum
f. fruticulosa (H, LE). "In den Wolgasteppen bei Sarepta",
Wenck, Rabenhorst Lich. Eur. No. 874, as Chlorangium affine
(H, FH, S, TUR-V 5751, W). Kazakhstan. Akmolinskaya
Oblast (0Akmola Prov.), 20 km SE of the Tengiz Lake, banks
of the river Kulanotpes, 4 km NNW of the town Kulanotpes,
340 m, Wagner (L-0070) in Obermayer: Lich. Graecenses No.
321 (H, all dupls. examined before distribution in ASU, B, C,
CANB, CANL, E, G, GZU, HAL, HMAS, LE, M, MAF, MIN,
O, PRA, TNS, UPS). Ukraine. Crimea (Krym), ‘ad terram
regionum stepporum prope Simpheropolin, in Peninsula
255
Taurica’, 1910, Mereschkowsky in Mereschkowsky: Lich.
Ross. Exs. No. 21 (B, H, LE, TU, hb. M. Sohrabi). "Ad terram
calcaream et inter rupes calcareas e viciniis Theodossia in
peninsula Taurica", 1893, Lipsky, in Elenkin: Lich. Fl. Ross.
24 g, as A. alpinodesertorum f. fruticulosa (H, LE, W). Turkey.
Anatolia prov., Çorum, limestone hills near road from Merzion
to Çorum, 30 km S of Merzifon, 950 m, 1997, John 9538, Yildiz
& Zeybek, in Lumbsch and Feige: Lecanoroid Lich. Exs. No.
82 (BM, H, M).
Circinaria gyrosa Sohrabi, Sipman, V. John & V.J. Rico,
sp. nov. (Fig. 3a-d). MB 563029
Diagnosis. Thallus vagrant, more or less globose, brainlike, deeply divided into short and coralloid, surface dull
brown, brownish grey, sometimes whitish grey, pale olivebrown to pale brown. Very similar to Circinaria affinis, but
differentiated by its shorter conidia (10–15 μm), wider
distribution in the highland (1000-2000 m) or steppe mountains of the Mediterranean region and monophyletic poistion
of the nuclear ribosomal ITS phylogeny analysis.
Type: Iran. East Azerbaijan, Marand district, 32 km N of
Marand towards Jolfa, 38° 40.58' N, 45° 39.44' E., 1440 m, 2
Nov. 2007, M. Sohrabi 10085, H. Sipman, U. Søchting & M. R.
Asef, (IRAN 14444, holotype; B, H, hb. M. Sohrabi, isotypes).
Thallus vagrant, more or less globose, 0.5–2 cm tall and
0.5–2(–3) cm broad, brain-like, deeply divided into short
and coralloid, flattened lobes or folds 1–3 mm broad, with
rimose-verrucose surface, rather flattened on top. Surface
dull brown, brownish grey, sometimes whitish grey, pale
olive-brown to pale brown, on covered sides usually darkish
green to dark brown, greenish brown or almost dark greenbrown (sometimes reddish brown when ferriferous components are present in soil). Pseudocyphellae very common,
visible as whitish spots usually along or on top of the folded
lobes. Cortex (40–)60–90(–110) μm thick, outer part paraplectenchymatous, ± brown, c. 2–3 cells thick, cells (4–)5–7
(–8) μm in diam., inner part indistinct, mixed with prosoplectenchymatous tissue of medulla, sometimes forming a
distinct layer (30–)40–80(–90) μm tall (variable presence of
algal cells in the medulla layer makes it uneven, poorly
delimited and difficult to distinguish from the true cortex
layer). Epinecral layer 1–5(–12) μm thick. Photobiont
chlorococcoid, cells 5–22 μm in diam., clustered in small
groups, each group up to 80–180 × 50–110 μm broad.
Medulla white, I–, 0.3–4(–6) mm thick, containing crystals
of calcium oxalate. Apothecia aspicilioid, rare, up to 0.5–1.5
(–2) mm wide, among the lobes in older parts. Disc black to
brown-black, pruinose, concave to convex when young,
becoming more flat when old. Thalline exciple flat to ±
elevated and prominent in older apothecia, entire, concolorous with thallus or with a thin to thick white rim. True
exciple (35–)45–75(–85) μm wide, I ± more or less blue,
uppermost cells brown, ± globose, 4–5(–7) μm in diam.
Epihymenium brown, K+, colour fading from brown to light
256
yellowish green, N + pale green (caesiocinerea-green).
Hymenium hyaline, occasionally with few oil drops,
(100–)110–140(–150) μm tall. Paraphysoids branched, apically moniliform to submoniliform, with upper cells ± globose, 4–7 μm wide, and lower cells cylindrical, 4–9×2–
3 μm wide, usually branched. Hypothecium and subhymenium pale, (35–)45–65(–85) μm thick, I + blue. Asci broadly
clavate, (80–)90–100(–110)×25–35 μm, with thick apical
dome 20–30 μm tall, 2–4(–5) spored. Ascospores hyaline,
simple, globose to subglobose, (16–)19–[22.1]–24(–26)×
(16–)19–[21.6]–23(–25) μm (n030). Pycnidia immersed
(sometimes occurring in pseudocyphellae), single, stretched
flask-shaped, internal wall colourless, with black to brownish
ostiole. Conidia filiform, straight to very slightly curved, (8–)
10–14(–18)×1–1.2 μm (n0132). Chemistry: All spot-tests
(K, C, KC, CK, P) negative both in the cortex and medulla.
TLC and HPLC: No substances detected. UV: Negative.
Etymology. The specific epithet ‘gyrosa’ refers to the
brain-like lobes of the thallus.
Ecology and distribution (Fig. 6c). The thalli of this
species are found scattered on bare calcareous soil, mixed
with gravel in several different habitats: in open grassland
with isolated trees and shrubs, with a Mediterranean type
climate, with mainly junipers and Astragalus spp. and in the
sub-montane forest zone in Golestan province of Iran. In
Spain it has been reported from same habitat types, however
the main species composition and vegetation type is different and mixed with other Juniperus species. In NW Iran
(Azerbaijan province) and in a similar habitats in SE Turkey
the species has bee found in dry steppes with Artemisia spp.
and Verbascum spp. In general, C. gyrosa appears to prefer
very open habitats that are ephemerally moist in the winter
or spring, and dry most of the year. The main associated
plant communities include Artemisia spp., Poa spp. and
Verbascum spp. Other associated lichen species on soil are
Circinaria hispida, and C. fruticulosa, and on pebbles
Caloplaca deceptoria (Flagey) J. Steiner, C. chalybaea
(Fr.) Müll. Arg., C. ferrugineoides H. Magn., and
Lecanora garovaglioi (Körb.) Zahlbr. Circinaria gyrosa is
widespread and locally common, at elevations of c. 1000–
2000 m. Its range includes the Mediterranean and IranoTuranian regions.
Remarks. Circinaria gyrosa is easily confused with the
very similar vagrant species C. fruticulosa and C. affinis. In
general Circinaria gyrosa is characterized by its large, 10–
30 mm wide, folded, vagrant thalli with brain-like morphology and its eye-catching light brown to dark grey-brown surface colour. Moreover, the conidia in C. gyrosa are up to 10–
15 μm long, and in C. affinis 15–25 μm. There are also
ecological and distributional differences, C. affinis is so far
known from low altitudes (from see level up to c. 1000 m) in
Central Asia, while C. gyrosa grows in mountains, usually at
1000 to 2000 m. As to the differentiation from C. fruticulosa,
Mycol Progress (2013) 12:231–269
C. gyrosa bears folded, rounded, flattened, dumpy lobes with
an irregular pattern of radiation in the central part, whereas C.
fruticulosa forms tiny, branched lumps with often dichotomous radiation. Microtome sections shave shown that
Circinaria fruticulosa has a conspicuously two layered cortex,
while the cortex in C. gyrosa consists of only one layer, is of
very uneven thickness and is often interrupted by prosoplectenchymatous medulla tissue. Pseudocyphellae in C. gyrosa
are very conspicuous and large (up to 0.6 mm), whereas in C.
fruticulosa they are rather small (up to 0.3 mm) and usually
located at the tips of the branchlets.
Circinaria gyrosa is morphologically very similar to C.
affinis. However, conidia in C. gyrosa are up to 10–15 μm
long, and in C. affinis up to 15–25 μm. There are also some
ecological and distributional differences between the two
species, i.e., C. affinis is so far known from low altitudes
(from see level up to c. 1000 m) in the Central Asia, while
C. gyrosa grows in mountainous areas, usually at the altitudes of 1000 to 2000 m. Circinaria gyrosa is also rather
similar to C. aschabadensis, with which it may grow together. Then its general appearance, e.g., reddish-brown
colour, brain-shaped thalli, larger lobes, abundance of white
spot-like pseudocyphellae, and lack of black ostioles in its
pycnidia easily distinguish it from the latter species.
In Sancho et al. (2008: Fig.3) a specimen presented
as ‘Aspicilia fruticulosa’ is illustrated which greatly
resembles to Circinaria gyrosa. The specimen had been
sent to space for physiological research on lichens species
(Sancho et al. 2008).
The oldest specimen known from Iran was collected by
Aucher-Éloy in 1825 from the surroundings of Hamadan and
labeled as Lecanora esculenta. After 186 years it turned out to
belong to our new species. A specimen of "L. esculenta"
reported by Aucher-Éloy (1843) from Uromia (Reżā'iyeh)
could not be located so that its true identity remains uncertain.
Specimens examined and paratypes. Armenia. ‘Kurdistan’,
[probably from South Armenia, NW Iran E Turkey and NW
Iraq], Radde (LE). Near the Ararat mountain, 1872, Demidova
(LE). Casikoporan, Surmalinsky district. Iravanskay Region,
1896, Koenig, in the same envelope with C. fruticulosa (LE).
Azerbaijan. Baku, near railway station, Sumgait, 1901,
Alexeenko 11214 (LE); Naxjivan (0 Naxjivan Autonomous
Region), Ordubad district, 1864, Radde (LE). Iran. [Persia,
‘Elevant’], Hamadan, Alvand-Kuh, 1825–1830 Aucher 909
(PC). East Azerbaijan, Kaleybar district 35 km S of Kaleybar
along road to Ahar, 1750 m, 2007, Sohrabi et al. 10405B (B,
IRAN, hb. M. Sohrabi). Golestan, Gorgan district Jehan-Nema
plain, c. 24 km S of Gorgan along minor road to Shahrad,
2250 m, 2007, Sohrabi et al. 9496 (H, IRAN, hb. M. Sohrabi).
Spain. Prov. Soria, Hochfläche (Paramera) W Calatayud, Kurz
W des Ortes Judes SE Arcos de Jalòn, c. 1200 m, 1983,
Mayrhofer 3656 & Crespo (GZU), ibidem, Poelt (GZU).
Guadalajara, Zaorejas, 1240 m, 2003, Printzen 8087 (FR).
Mycol Progress (2013) 12:231–269
Olmedillas, junto al pueblo, 2007, ladera con caliza, en el suelo,
I. González (MAF-Lich 15363, H). Turkey. Prov. Kırıkkale,
1100 m, 1990, Doumez (hb. Seaward); Prov. Kirşehir, Kizil
Dağ NE of Mucur, 1300 m, 2001, John 11984B (M). Anatolia
(0 Anatolian Prov.), sine coll. (H-NYL 25671); Harput
[‘Charput, Karput’], (0 Elâzığ & Diyarbakır provinces).
Harput, 1864, Haidinger (PC). Karput Mt., Diyarbakir, sine
coll. (W). Diyarbakir, sine coll. (LE). ‘Kurdistan Region’
(0 East Turkey), Schehid duri 1863, Mayer (W). Niğde prov.,
Erdschias-Dagh, Argaeus, 1000 m, 1902, Zederbauer (W).
Turkmenistan. Central part of Kopet-Dagh district, next to
the border of Iran, Stony part of mountain, to the SW of
Solukli, 1934, Borisova, packed under C. aschabadensis (LE).
Exsiccata. Spain. Soria, plateau (Paramera) W of
Calatayud, W of village Judes SE Arcos of Jalòn, c. 1200 m,
1983, Hafellner 17527, Crespo, et al. (GZU) in Obermayer:
Lich. Graecenses: No. 211 (CANB, GZU, M, NY, UPS).
‘Prov. Soria, Prope vicum Judes Paramera’, c. 1250 m,
1983, Barreno et al. in Vězda: Lich. Sel. Exs. No 1904
(BM, US). Prov. Teruel, der Sierra de la Costera, Cañada
Vellida, 1050 m, Follmann & Follmann-Schrag, 1973, in
Follmann, Lich. Exs. Casselensi No. 99 (BM, H, TUR).
Circinaria hispida (Mereschk.) A. Nordin, S. Savić &
Tibell in Mycologia 102: 1346. 2010. (Fig. 5a-c).
Basionym: Aspicilia hispida Mereschk. in Trudy Obshch.
Estestvoisp. Imp. Kazansk. Univ. 43 (5): 10, 35. 1911.
Lectotype: designated by Sohrabi and Ahti (2010), Russia.
‘Ad terram argilloso-calcaream montis Bogdo prope lacu
Baskuntschak in gub Astrachan’, 50–120 m, 1910,
Mereschkowsky in Mereschkowsky: Lich. Ross. Exs. No.
34 (TU; isolectotypes LE L1988, W).
Note: for the moment the treatment below includes the
whole C. hispida s.str., but excluding its crustose form.
Thallus subfruticose, erratic, usually basally attached or
imbedded in soil, in later stages become vagrant, (probably
also rarly on pebbles, however this need further study),
about 5–20 mm tall, 5–20(–30) mm broad, forming small
tufts, branching irregular to dichotomous, main branches
variable in width, (0.3–) 0.5–1.5(–2) mm in diam., but
distinctly tapering and pointed at the tips. Surface grey,
green–grey, olive–grey, yellow–grey, brown–grey to green,
olive, olive–brown or almost brown, dull, at branch tips
black. Pseudocyphellae whitish, round to elongated, 0.1–
0.8 mm in diam., common along the branches. Cortex two
layered, outer part (30–)40–80(–90) μm thick, paraplectenchymatous, ± brown, c. 3–5 cells thick, cells (4–)5–7(–8)
μm in diam., inner part prosoplectenchymatous c. 2–3 times
as thick as the outer layer, cortex covered with a thin
epinecral, amorphous layer 1–10(–15) μm thick.
Photobiont chlorococcoid, cells 5–15(–20) μm in diam.,
clustered in small groups. Medulla white, I–, containing
crystals of calcium oxalate. Apothecia not seen; for more
information, see Sohrabi et al. (2011b). Pycnidia common,
257
immersed, sometimes occurring in the pseudocyphellae,
often located along the branchlets, rarely at the apices,
flask-shaped, with black ostiole. Conidia filiform, straight
to slightly curved, (8–)10–12 (–14) × 0.8–1.2 μm.
Chemistry: All spot-tests (K, C, KC, CK, P) negative both
in the cortex and medulla. TLC and HPLC: No substances
detected. UV: Negative.
Ecology and distribution (Fig. 6g). The erratic species
Cricinaria hispida is an example of a steppe element found
in temperate and subtropical, semi–arid regions of the
Northern Hemisphere. Circinaria hispida has been found
in a wide range of ecological conditions in Eurasia. For
instance, the type specimen was collected from lowland
steppes in N Caspian Sea and other collections are reported
from alpine areas in Italy (Hafellner et al. 2004) and TianShan Mountains in Kyrgyzstan. The species is often
reported on ± calciferous soil in arid steppe or steppe–like
habitats and is usually growing in open stony slopes.
Vagrant forms accumulate in wind–deposited drifts. Some
of the accompanying plants were listed by Andreava (1978),
e.g., Anabasis salsa, Artemisia glauca, A. herba-alba, A.
pauciflora, Atriplex cana, Calligonum spp., and Salsola
arbusculiformis. Additional list of accompaning lichen species and plants can be found in Hafellner et al. (2004).
The species is widespread, so far reported from southern
Europe by Hafellner et al. (2004), from Russia by Kulakov
(2002, 2003), from Ukraine by Mereschkowsky (1911a, b),
Middle Asia by Andreeva (1987) and Iran by Seaward et al.
(2008) and Sohrabi et al. (2010d). In North America it is
known from Canada (Saskatchewan) and USA (eastern
Oregon to eastern Montana and northern Great Plains, south
to Utah, Colorado and Arizona; Owe–Larsson et al. 2007).
Remarks. Circinaria hispida s.str., a vagrant morphotype
sensu Mereschkowsky (1911b), is characterized by subfruticose, forming tiny, bushy, more or less Cladonia-like thallus with narrow cylindrical branches with black apices at tip
of branchlets and scattered whitish pseudocyphellae along
the branches. It initially grows on soil and later becomes
vagrant. Therefore, it is classified as erratic. C. hispida s.str.
has never been reported in fertile condition in Eurasia. So
far, its fertile specimens have previously been reported from
North America (see Thomson 1960; Brodo 1976; Sohrabi et
al. 2011b). In the nrITS analysis, C. hispida is grouped with
a few Eurasian saxicolous specimens that are fertile.
Although this morphological difference between vagrant
and crustose specimen of C. hispida is straightforward, the
present result of nrITS analyses did not support the monophyly of vagrant and crustose morphotypes. Several specimens of vagrant morphotype, identical with the type
specimen of C. hispida, were included in the study.
However, they did not form a monophyletic group, either.
Therefore, in this study vagrant morphotypes are accepted
as C. hispida s.str. and saxicolous specimens with crustose
258
morphotype as C. hispida s.lat. Thus, the final conclusions
concerning the status of C. hispida can not be made in the
present study.
According to Rosentreter (1998), Aspicilia californica
Rosentr. and A. filiformis Rosentr., are two terricolous subfruticose species that are known only from northwestern
North America. Up to this point, they have never been
observed in vagrant form. Both species bear prostrate and
patchy thalli and are clearly attached to soil. However, they
somewhat differ from C. hispida s.str. mainly by the lack of
pseudocyphellae and presence of secondary metabolites.
Our attempts for DNA extractions from these two species
were not successful.
Additional literature reports. Circinaria hispida has been
reported from several countries e.g., from Azerbaijan by
Barkhalov (1952); from Iran by Seaward et al. (2008 as
Aspicilia hispida); from Kyrgyzstan by Litterski (2002 as A.
hispida); Turkey by Candan and Türk (2008 as as A. hispida)
and from Turkmenistan by Dzhuraeva (1978 as as A. hispida).
Specimens examined (C. hispida s.str.) Kazakhstan.
Aklushenskaya district, Bayzhanshal limestone ridge,
1957, Andreeva (LE); Akmola Region, near Kökshetau
Mts., S direction, 1957, Andreeva (LE). Kyrgyzstan.
Northern side of Naryn-Too Mt., valley of River Naryn, 23
Km to the E. from Naryn Mt., 2250 m, 1970, Bredkina (LE).
SW Tian-Shan, NE Abhange des Fergana-Gebirges, SW
Chatyr-Kol, 3261 m, 2003, Ringel 5242 (H). SW TianShan, Susamyr, 2381 m, 2003, Ringel 5244 (H). Westl.,
Tian-Shan, Susamyr-Tal, c. 25 km W Susamyr, 2300 m,
1999, Litterski 5053 (H). Depression of Song-Köl Lake,
3023 m, 1970, Bredkina 445 (LE). Mountain Naryn-Too,
near River Naryn, c. 23 km from Naryn, on the E direction
from Naryn. 2250 m, 1970, Bredkina (LE). Iran. Hamadan,
foothills above Gholi-Abad, c. 60 km N of Hamadan,
1800 m, 1974, Alava 14749-d (TUR). East Azerbaijan,
Marand district, 32 km N of Marand towards Jolfa,
1440 m, 2007, Sohrabi et al. 10102 (hb. M. Sohrabi).
Marand district, Zonuz, 20 km N of Marand towards Jolfa,
1800 m, 2007, Sohrabi et al. 10064 (hb. M. Sohrabi). Jolfa
district 1 km S of Daran village, E of Hadishahr, 1700 m,
2007, Sohrabi et al. 10136 (hb. M. Sohrabi). Shabestar
district W along road Tabriz-Marand, 7 km N of Sufiyan,
1450 m, 2007, Sohrabi et al. 10032, 10022 (hb. M.
Sohrabi), Kaleybar district 35 km S of Kaleybar along road
to Ahar, 1750 m, 2007, Sohrabi et al. 10407, 10405D (hb.
M. Sohrabi). Golestan, Golestan National Park, Almeh valley, near the station, 1800 m, 2008, Sohrabi 15068, 15099 &
Ghobad-Nejhad (hb. M. Sohrabi, H). Gorgan district Shah
Kuh-e-Bala, c. 33 km S of Gorgan along minor road to
Shahrud, 2600 m, 2007, Sohrabi et al. 9501 (hb. M.
Sohrabi). Italy. Piemonte, Prov. Cuneo, Alpi Liguri, Cima
di Pertega W above the village Úpega, just E below the
summit, c. 2400 m, 2000, Hafellner & Hafellner 59353
Mycol Progress (2013) 12:231–269
(GZU, TSB). Piemonte, Prov. Cuneo, Alpi Cozie, crest
SW above Colle dell’Agnello, c. 2830 m, 2000, Hafellner
59364 (GZU). Greece. Parnassus Mt., Fterolaka, near the
cableway, 1850 m, 1989, Tretiach & Roux (TSB).
Mongolia. Zavkhan [correctly Govi-Altai] aimag, Taishir
sum, right bank of Zavkhan River, c. 2 km N of Taishir
Town, 1978, Biazrov 8373 (LE). Russia. Astrakhan, near
the Lake Baskunchak, 1926, Tomin (H), ibidem, 1926,
Tomin 37 (FH, H). ibidem, 1927, Tomin 56 (FH, H).
Mountain Bolshaya Bogdo, 1924, Kazakevich (LE). Near
the Lake Baskunchak, W slope of mount Big Bogdo, 1998,
Sagalaev (M). Bogdo Mt., northern slope, 1926, Savicz (FH,
LE). ‘Russia’ sine loc., 1907, Djungalien (H). Berg Bogdo,
1910, Mereschkowsky (H, W). Saratow Region, Elshanke,
1926, Yanishewski (LE). Volgograd Region, Kalachovsky
district, vicinity of Bolshegolubinsky house. Northern slop of
river Bolshaya Golubaya, 1994, Kulakov (LE). Orenburg
Region, to the northwest from Kutush village, beside the road,
1930, Sukhova (LE). Kalmyk Region, Elista town, ravin, close
to the street Ulan Tug, 2003, Ochirova (LE). Kalmyk Region,
Bergin village, E slope, 2002, Ochirova (LE). Spain. Prov.
Soria, Hochfläche ("Paramera") W Calatayud, Kurz W des
Ortes Judes SE Arcos de Jalòn, c. 1200 m, 1983, Crespo &
Poelt (GZU). Calatañazor, 1979, Barreno & Crespo 2139 (hb.
Seaward). Turkey. Malatya, Pınarbaşı mesire alanı ve çevresi,
931 m, 2003, Candan 11 (H). Ukraine. Crimea, Simpheropol
steppes, 1910, Mereschkowsky (H).
Exsiccata. Russia. Astrakhan, Ad terram argillosocalcaream montis Bogdo prope lacu, 50–120 m, 1910,
Mereschkowsky, in Mereschkowsky: Lich. Ross. Exs. No. 34
(LE, TU). Regio Astrachanensis per declive (in parte superiore)
montis Bogdo ad terram inter gramina, fruticulos lapidesque
crescit, saepe libere vagature, 1926 Savicz, in Savicz: Lich.
Ross. No. 97 (FH, GZU, H, W). Ukraine. Crimea (Krym),
Supra Terram stepporum prope Simpheropolin, in Peninsula
Taurica, 1910, Mereschkowsky, in Mereschkowsky: Lich.
Ross. Exs. No. 35 (LE).
Circinaria jussuffii (Link) Sohrabi comb. nov. (Fig.4d).
MB 563030
Basionym: Placodium jussuffii Link in Bot. Zeitung
(Berlin) 6: 666.1848. Lectotype: designated by Sohrabi
and Ahti (2010), Algeria. ‘Du désert Algerien’, 1847,
Jussuff (H-NYL 3312).
Thallus vagrant, rarely invades small pebbles, folded,
globose-angular in shape, convoluted subsquamulose, compact, forming areole-like surface, deeply cracked, hard,
densely imbricate, interconnected by the central axis, up to
3–10(–25) mm diam. Surface smooth, concave to convex,
often reddish brown, rusty red (when ferriferous sediments
are present in soil), yellowish brown, brown, more rarely
red-brown. Pseudocyphellae very common, conspicuous,
±white spots along the subsquamuloes. Cortex one layer,
(30–)50–75(–90) μm thick, paraplectenchymatous, ±
Mycol Progress (2013) 12:231–269
brown, cells (4–)5–7(–10) μm in diam., inner part indistinct,
more or less prosoplectenchymatous, mixed with anticlinal
hyphae of medulla. Epinecral layer 5–15(–25)μm thick, usually brown to red. Photobiont chlorococcoid, cells 5–15 μm in
diam., arranged and clustered in some small groups, each up
to 80–170×80–150 μm wide, distance between groups 20–
100 μm. Medulla prosoplectenchymatous with irregularly
oriented hyphae (textura intricata), white, I–, containing crystals of calcium oxalate, visible in (H2SO2 10 % solution).
Apothecia aspicilioid, urceolate, immersed, not common,
round, sometimes angular, 0.2–0.6 mm in diam., 1–2(–4)
per subsquamulose. Thalline exciple flat to ± elevated, prominent in older apothecia, entire, concolorous with thallus or
with a thin white rim. True exciple (30–)35–65(–85) μm, ± I +
blue, uppermost cell brown, ± globose, 4–5(–7) μm in diam.
Epihymenium brownish to dark brown, usually contain some
crystals, K + colour fading from brown to light yellowish
green, N + pale green (caesiocinerea-green). Hymenium hyaline, I + persistently blue, (80–)100–120(–135) μm tall.
Paraphysoids moniliform to submoniliform, with upper cells
± globose, 4–5 μm wide, in lower part with ± cylindrical cell
6–7×2–3 μm wide; branched. Hypothecium and subhymenium pale, (35–)50–65(–90) μm thick, I + blue. Asci broadly
clavate, with distinctly thickened apex dome (15–35 μm.
thick), I–, 70–110×20–35 μm, 1–4(–6) spored. Ascospores
hyaline, globose to subglobose, (15–)19.2–[22.5]–25.7(–
31)×(10–)15.8–[19.1]–22.3(–26) μm (n031). Pycnidia immersed, single, stretch flask-shaped, internal wall colourless,
frequently with black to brownish ostiole. Conidia filiform,
straight to very slightly curved, (8–)10–14(–16)×1–1.3 μm
(n034). Chemistry: All spot-tests (K, C, KC, CK) negative
both in the cortex and medulla, but in some thalli P±. TLC:
Three common chemotypes containing (1) stictic acid and
hypostictic acid, (2) only stictic acid, (3) no substances.
Ecology and distribution (Fig. 6f). Circinaria jussuffii
most commonly grows as vagrant on calcareous soil, or on
gypsum crusts. It is very rarely found on small pebbles. The
known distribution is restricted to North Africa, particularly
in the Northern Saharan (Algeria, Libya and Moroco)
steppes and semideserts areas. The total distribution of C.
jussuffii is rather poorly known, but in North Africa the
species seems to be very common, although overlooked,
or misidentified as C. esculenta. The easternmost collection
of the species was recently made from the Central Iran
(Tabas district); see also Rabenhorst (1871).
Additional literature reports. The first reports of
Circinaria jussuffii from North Africa were made by Link
(1848, 1849). Aspicilia esculenta was reported from Algeria
by Flagey (1896). The name A. esculenta is still in use,
rarely appears in North African lichen literature. However,
after extensive evaluation of both herbarium material and
recent publications (e.g., Donkin 1980, 1981; Crum 1993;
Thor and Nascimbene 2010), it became clear that the reports
259
of C. esculenta from North Africa is dubious and might be
referrabel to C. jussuffii.
Remarks. Morphologically, Circinaria jussuffii is somewhat similar to C. esculenta. However, there are certain
differences which can be highlighted. For example, C. esculenta is a lowland species (lower than c. 500 m), distributed
in the northeast of the Caspian Sea and some parts of Central
Asia. It can be easily distinguished from C. jussuffii by
having wrinkled large subsquamulose thalli as well as longer conidia (10–)18–30(–35) μm. C. jussuffii is usually
found in the open habitats from c. 100–1300 m and it has
shorter conidia (8–)10–14(–16) μm, smaller subsquamulose
with densely compact, more or less even thallus surface.
Thallus colour may vary in both species. Occasionally C.
esculenta grows on soil with ferriferous sediments and its
surface colour changes to dark reddish-brown or rusty colour.
Most of the herbarium specimens of C. jussuffii examined for
this study were reddish-brown to rusty. Our nrITS analysis
obviously revealed that the two taxa are distinct (Fig. 2).
The records of A. esculenta in North Africa are probably
based on C. jussuffii. Therefore, the exclusion of C. esculenta from the Libyan checklist (Thor and Nascimbene
2010) is proposed.
Specimens examined. Algeria. Laghouat, 1851, E. Ripart
(H-NYL 25672, UPS), ibidem, 1856, E. Ripart (UPS).
"Sahara", 1857, Montagne, sine coll. (PC, UPS). Sahara,
Laghouat, 1856, Jussuf & Rebaud (PC, W). ‘Der Sahara von
der Umgegend von Laghouat’, Hohenacker, No. 722 (FH).
Laghouat, 1857, Motelay 760 (PC). Auf steinigem boden in
der Sahara bei Laghouat, 1856, Jussuf & Rebaud in Djelfa;
No. 794 (FH, H-NYL 25670, PC, S, UPS, W). Environs de
Laghouat, Janvier 1857, Rebaud (FH, US, W). Satara la
Laghouat, 1856 Jussuf (W). Near Durandu, 1881, sine coll.
‘comm. Toepffer’ (W). ‘North Africa, in deserto Titteré’,
sine coll. (UPS). Sahara. sine coll. (W). ‘Africa Borealis’
("Algeria"), ibidem, Russel (S). Plaine du Zahrés, Région
des Haute-plateux, a nord de Djelfa, 1857, Rebaud (H, UPS,
W). E. Bourgeau, Pl. ďAlgerie, 1856, sine coll. (UPS).
‘Algeria’, sine coll. (UPS). El Aghwat im Norden der
Sahara, Jussuf (UPS). ‘In deserto Titteré’, sine dato & coll.
(PC, 6 specimens). ‘Sud de l' Algėriei", 1847, Jussuf (PC).
Hauts-Plateaux, Pâturages pierreux du Serson, prês de
Vfetor-Hugo, 9000–1000 m, Nom arabe, Oussekh-el ardh
(crasse de la terr.), 1929, Maire (PC). ‘Sud de l' Algėriei",
1846, Guyon, (PC). Iraq. c. 130 km N of Ar Rutba,
Fuggarai, 1966, Rami 34186 (BM). Iran. [‘Persia"], Yazd
prov., near Tabas (see also Rabenhorst 1870), Stapff (W).
Libya. Trigh el Abit, Slates, 1959, sine coll. (US).
Exsiccata. Algeria. Environs de Laghouat, Janvier 1857,
Rebaud. ‘Ex Herb. Durieu de Maisonneuve’, and Fragmenta
Flora Algeriensis Exs. No. 500, as Parmelia esculenta (H,
PC 2 specimens, UPS, W). ‘Sahara près de Laghouat’,
Janvier 1856, Rebaud. [Flora Galliae et Germaniae exsiccati
260
de C. Billot.] No. 1997, as Placodium esculentum (LE, PC,
S,). ‘Sahara près de Laghouat’, Janvier 1856, Rebaud
(Lichen Helv. Exs. Schaer, No. 1160, and Hepp Flecht.
Eur. No. 632 (FH, S, TUR-V 5824). ‘Sahara près de
Laghouat’, Janvier 1856, Rebaud, Rabenhorst, Lich.
Europaei, No. 199, as Chlorangium jussuffii (FH, H, S,
US); N of Djolfa plaine du Zahries, 1856, Rebaud, in
Bourgeau Fl. Algérie No. 247 (H, W). Morocco. ‘Regnum
Maroccanum’ inter Taourirt et Taza, 75 km ad occidentem a
Taza, 350 m, 1989, Hafellner & Follmann, in Vězda: Lich.
Sel. Exs. No. 2381, as Aspicilia jussuffii (H, S, UPS, US,
TSB). ‘Südmarokko, Distr. Ouârkziz, Hamadaformation bei
Aouinet Torkoz’, 400 m, Follmann, in Follmann: Lich. Sel.
Exs. No. 74 (TUR).
Circinaria lacunosa (Mereschk.) Sohrabi comb. nov.
(Fig. 4a). MB 563031
Basionym: Aspicilia lacunosa Mereschk. in Trudy Obshch.
Estestvoisp. Imp. Kazansk. Univ. 43 (5): 11. 1911. Lectotype:
designated by Sohrabi and Ahti (2010): Kazakhstan. Semipalatinsk Region [East Kazakhstan Prov.], Zaisan District,
Keller (icon seen in H, W, voucher not found).
Thallus vagrant, lumps subspherical to irregularly lobed,
amorphous, truffle-like, rounded, variable in size, 0.5–2(–3)
cm in diam. Surface flattened to uneven, folded, with narrow, thin cracks, broadly flexuose, obtuse, rounded at lobes,
often grey, grey-olive, more rarely rust colour (when ferriferous sediments present in soil), ochre to bright red-orange,
glabrous, often with rounded pores in different sizes, 0.5–1
(1.5) mm diam., occasionally surrounded by part of thallus.
Pseudocyphellae conspicuous, numerous, small white dotlike spots. Cortex indistinctly delimited, (40–)50–100(–110)
μm thick, paraplectenchymatous, consists of isodiametric,
rounded to rounded-angular, thin-walled cells (3–)5–7(–8)
μm in diam. Epinecral layer 3–10(–25) μm thick.
Photobiont chlorococcoid, cells 5–15(–18) μm in diam.,
arranged in single layer and clustered in few small groups,
each group up to 100–150×90–145 μm wide, often with
40–100 μm from each other. Medulla white, I–, irregularly
developed, 0.8–2 mm thick, white, crumbly, when thallus
broken hyphae appear giving tomentose appearance, arachnoid in the central part, occasionally with cavities, partially
turbid due to rather numerous granules covering hyphae,
containing crystals of calcium oxalate. Apothecia aspicilioid
(urceolate), very rare, immersed, up to 0.5–0.8(–1) mm
wide. Disc black to brown-black, pruinose, concave.
Thalline exciple ± flat to slightly elevated, entire, concolorous with thallus. True exciple (25–)30–35(–40) μm wide, ±
I + blue, uppermost cell brown ± globose, 4–5(–7) μm in
diam. Epihymenium brown, K + colour fading from brown
to light yellowish green, N + pale green (caesiocinerea
green), Hymenium hyaline, with few oil drops, (110–)120–
130(–140) μm tall. Paraphysoids moniliform to submoniliform, with upper cells ± globose, 4–7 μm wide, in lower
Mycol Progress (2013) 12:231–269
part 5–8 × 2–3 μm wide, more or less branched.
Hypothecium and subhymenium pale, (35–)45–70(–90) μm
thick. I + blue. Asci clavate, (70–)80–90(–95)×20–27 μm,
with rather thick apical dome (10–15 μm), 2–4 spored.
Ascospores hyaline, simple, globose to fairly subglobose,
14–18(–19)×(13–)15–17(–18) μm. Pycnidia immersed, single, stretched flask-shaped, internal wall colourless, frequently with black to brownish ostiole. Conidia filiform,
straight to very slightly curved (8–)11–13(–16)×1–1.3 μm.
Chemistry: All spot-tests (K, C, KC, CK, P) negative both in
the cortex and medulla. TLC and HPLC: No substances
detected. UV: Negative.
Ecology and distribution (Fig. 6a). The ecology of
Circinaria lacunosa is poorly known. It grows on gravely
or sandy clayey soils in steppes and semideserts. Winddrifted thalli sometimes accumulate nearby the cushion
plants. The following plant species have been reported as
dominant in the habitats of C. lacunosa: Artemisia glauca,
A. herba-alba, A. pauciflora, as well as Anabasis salsa,
Atriplex cana, Calligonum spp., Kochia prostrata, and
Salsola arbusculiformis.
Remarks. Circinaria lacunosa is characterized by its
subspherical to irregularly lobed, truffle-like, rounded,
sometimes flattened, ± addpresed thallus, with rounded pits
on the surface. Some of the thalli are narrowly flattened and
they can be confused with subfoliose thalli of C. emiliae.
However, C. lacunosa has a hole-like structure at some parts
of the thallus and it has a corticated surface. Circinaria
lacunosa may also greatly resemble to C. cerebroides but
in the latter spec, hole-like structures are lacking and it
grows in alpine-nival habitats (c. 2000–4500 m) of TianShan Mountains in the Central Asia. Circinaria lacunosa
prefers lowlands and lower montane habitats (c. 100–
1100 m). For the first time, a fertile specimen was examined
by Golubkova (1980) and the species description was somewhat improved. In the present study the same specimen was
re-examined as the only fertile sample of C. lacunosa.
Additional literature reports. Circinaria lacunosa was
reported from several contries i.e., by Abbas and Wu
(1998) from China; Schubert and Klement (1971) from
Mongolia; Bredkina and Makarova (2005) from
Kyrgyzstan, and Oxner (1971) from Uzbekistan. The report
from Turkey by John and Türk (2006) referable to a new
species Circinaria rostamii. However, additional specimens
needs be confirmed.
Specimens examined. China. Xinjiang, Tacheng Toli,
1050 m, 1994, Abbas 94003 (H). Kazakhstan. South
Peribalkhashya, Kenes-Anarkhay, 1976, Piregoudov, ibidem, 1976, Piregoudov (LE). Betpak-dala, along the road
to Kendyrlyk, 1957, Vasyagina (LE). SE Balkhash, 1951,
Kazichas (LE). Syrdaria River, Mayon Kumski district,
Koskaduski, Saksaoul village, 50-150 m from railway
station Tchu, Saksaoul, near Orta khdok-Karman Kuduk,
Mycol Progress (2013) 12:231–269
1929, Nikitin 3 (LE). Mongolia. Zavkhan [correctly
Govi-Altai] aimag, Taishir sum, vicinity of Taishir, 1978,
Biazrov 8375 (LE).
Circinaria rostamii Sohrabi sp. nov. (Fig. 3e-i). MB
563032
Diagnosis. Thallus vagrant, brain-shaped, subspherical,
surface even, more or less rimose, with shallow to deep
cracks, dull brown, brownish grey to greyish green Very
similar to Circinaria lacunosa and C. cerebroides, but differentiated by its more brain-like appearance, rimose surfaces, areole-like lobes, monophyletic poistion in the nuclear
ribosomal ITS phylogeny analysis.
Type: Iran. East Azerbaijan, Jolfa district, 1 km N of
Asiab Kharabeh waterfall, S of road Hadi Shahr Siyahrud., 950 m, 4 November 2007, 38°51.89'N, 45°
51.56'E, M. Sohrabi 10212, H. Sipman, U. Søchting & M.
R. Asef [IRAN 14442, holotype; F, GZU, H, hb. M. Sohrabi,
isotypes]
Thallus vagrant, lumps formed of folded lobes, brainshaped, subspherical, rounded, amorphous, occasionally
flat, variable in size, 0.5–2.5 cm tall, 0.5–2(–3) cm wide.
Surface even, more or less rimose, with shallow to deep
cracks, dull brown, brownish grey to greyish green, sometimes whitish grey, pale olive-brown to pale brown, sometime reddish brown (when ferriferous sediments are present
in soil). Pseudocyphellae very common, ±white, dot-like,
usually visible on areole-like lobes. Cortex indistinctly
delimited, one layer, (40–)60–90(–110) μm thick, paraplectenchymatous, ± brown, cells (4–)5–7(–8) μm in diam.,
inner part indistinct, mixed with prosoplectenchymatous
tissue of medulla sometimes forming distinct layer of
(30–)40–80(–90) μm thick, (floating of algal cells in the
medulla make it uneven, without distinct margin to distinguish it from the real cortex). Epinecral layer 1–10(–18) μm
thick. Photobiont chlorococcoid, cells 5–22 μm in diam.,
clustered in small groups, each group up to 80–180×50–
110 μm wide. Medulla white, I–, containing crystals of
calcium oxalate. Apothecia aspicilioid, rare, up to 0.5–1.5
(–2.5) mm wide, often among the lobes in older parts of the
thallus. Disc black to brown-black, pruinose, concave to
convex when young, becoming more flat when old.
Thalline exciple flat to ± elevated and prominent in older
apothecia, entire, concolorous with thallus or with a thin to
thick white rim. True exciple (40–)50–85(–90) μm wide, ± I +
blue, uppermost cell brown, ± globose, 4–5(–7) μm in diam.
Epihymenium brownish to dark brown, K + colour fading
from brown to light yellowish green, N + pale green (caesiocinerea-green). Hymenium hyaline, occasionally with few oil
drops, (95–)115–140(–155) μm tall. Paraphysoids moniliform to submoniliform, with upper cells ± globose, 4–7 μm
wide, in lower part 4–8×2–3 μm wide, more or less branched.
Hypothecium and subhymenium pale, (35–)50–65(–85) μm
thick, I + blue. Asci broadly clavate, (80–)90–100(–110)×25–
261
35 μm, with thick apical dome (20–30 μm), 2–4(–5) spored.
Ascospores hyaline, simple, globose to subglobose,
(16–)19–[22.1]–24 (–26)×(16–)19–[21.6]–23(–25) μm (n0
30). Pycnidia usually on top of branches, immersed, single,
stretched flask-shaped, internal wall colourless, frequently
with black to brownish ostiole. Conidia filiform, straight to
very slightly curved (8–)10–12(–16)×1–1.3 μm (n030).
Chemistry: All spot-tests (K, C, KC, CK, P) negative both in
the cortex and medulla. TLC and HPLC: No substances
detected. UV: Negative.
Etymology. The first author names this species after his
father Rostam Sohrabi on the occasion of his 60th birthday,
with thanks for the help provided during the initial stages of
his interest in lichenology of Iran.
Ecology and distribution (Fig. 6d). The thalli of this
species can be found on bare calcareous soil mixed with
gravel and big limestone outcrops. The species is found on
dry steppes, mainly associated with xerophytic plant communities including Artemisia spp., Verbascum spp. and
Zygophyllum spp. Other associated vagrant lichen species
on soil is Circinaria hispida, and on pebbles Caloplaca
chalybaea (Fr.) Müll. Arg., C. crenulatella (Nyl.) H.
Olivier, C. polycarpoides (J. Steiner) M. Steiner & Poelt,
Lecanora aff. dispersa, and L. garovaglioi (Körb.) Zahlbr.
Some populations of C. rostamii can be mixed with C.
gyrosa, the other vagrant species in the NW part of Iran.
Circinaria rostamii has a wide range inside Iran, which
extends from Kiamaky-Dagh Mts. in E. Azerbaijan province
towards Semnan province in the Central Iran. The species is
also known from Naxjivan, Ordubad district in Azerbaijan,
where it is located in the border between Iran and
Azerbaijan, very close (c. 10 km) to the type locality. It is
also known from the dry steppes of Kurdistan Region in SE
Turkey.
Remarks. Circinaria rostamii more or less resembles to
truffle-like thalli of C. cerebroides and C. lacunosa, and is
characterized by shallow to deep cracks and areole-like
lobes at the surface. C. rostamii differs from the alpine
species of C. cerebroides (growing above alpine zone) by
having smaller thallus lumps, having more or less areolelike surface and different ecology and habitat requirements.
In C. lacunosa thalline lumps are often larger and it consists
of flattened to wrinkled lobes, and possess hole-like structure in some parts of the thallus. The conidia size of all three
species are more or less overlapped and minutely differentiated in size, up to c. 1–2 μm. However the monophyly of
all three species was confirmed by using nrITS sequences
(see Fig. 2).
Examined specimens and paratypes. Azerbaijan.
Naxjivan (0 Naxjivan Autonomous Region), Ordubad district,
1864, Radde (LE), Note: this specimens was illustrated by
Elenkin (1901a). Iran. East Azerbaijan, Marand district,
32 km N of Marand towards Jolfa, 1440 m, 2007, Sohrabi et
262
al. 10095 ( H, IRAN, UPS, hb. M. Sohrabi). Semnan,
Damghan district 80.5 km S of Shahrud along road to
Torud, 1180 m, 2007, Sohrabi et al. 9364, (IRAN, hb. M.
Sohrabi). Turkey. Kurdistan Region (0 SE Turkey), Schehid
duri 1863, Mayer, in the same envelope with C. gyrosa (W).
Circinaria tominii (Oxner) Sohrabi comb. nov. (Fig. 4i).
MB 563033
Basionym: Aspicilia tominii Oxner in Novosti Sist.
Nizsh. Rast. 9: 291. 1972. ≡ Lecanora esculenta f. altaica
Tomin in Sist. Zametki Mater. Gerb. Tomsk. Univ. 5/6: 9.
1933. Lectotype:designated by Sohrabi and Ahti (2010):
Russia. [Altai Republic], Deserto Czuensi [Chuy Desert],
Altai Austro-orientalis, 24 September 1926, Baranov (H).
Thallus vagrant, subfruticose, rounded, globose to subglobose, up to 3–10(–13) mm in diam., lumps forming tiny
subsquamulose, 0.6–1.5(–2.5) mm long, 0.5–1(–1.5) mm
wide, sometimes areole-like lobes, compact, tightly attached
to each other. Surface even, often dusty, greyish to greyish
green, matt, muddy, flexuose in some part, margins of subsquamulose more or less imbricate, somewhat elevated from
the thallus surface. Pseudocyphellae conspicuous, tiny,
round, withish to elongate pits, 1–2(–3) per subsquamulose,
variable in size, up to 0.02–0.4(–0.7) mm wide. Cortex
indistinctly delimited, uneven in thickness, paraplectenchymatous (35–)60–90(–100) μm thick, ± brown, with cells
(4–)5–7(–8) μm in diam., inner parts often interrupted by
prosoplectenchymatous tissue of medulla, in some parts
becoming (30–)40–70(–95) μm thick. Epinecral layer dark
brown, 5–18(–30) μm thick. Medulla white, I–, in sections
often muddy, variable in different part of thallus, in central
part 0.3–10 mm thick, containing crystals of calcium oxalate. Photobiont chlorococcoid, cells 5–18(–22) μm in
diam., forming small clusters 120–180×80–150 μm wide.
Apothecia crypto-lecanorine to aspicilioid, deeply immersed, common, 0.4–0.8(–1.5) mm wide, 1–2 per subsquamulose. Disc black, brown-black, whitish pruinose, at first
rounded, later somewhat elongated or irregular in shape,
sometimes surrounded by very thin white rim. Thalline
exciple 0.2–0.6 mm thick, entire or slightly cracked, more
or less even or slightly flexuose. True exciple (35–)40–60(–
65) μm wide in upper parts, at base 100–150 μm thick, ± I +
blue, uppermost cell black-brown, ± globose, 4–5(–7) μm in
diam. Epihymenium brown, 15–25 μm thick, K + colour
fading from brown to yellowish green, contains insoluble
crystals of calcium oxalat, N + pale green (caesiocinereagreen). Hymenium hyaline, (90–)100–110(–120) μm thick, I
+ blue. Paraphysoids moniliform to submoniliform, tightly
conglutinate in hymenial gelatine, with upper cells ± globose, 4–5 μm wide, in lower part with ± cylindrical cell 5–
7×2–3 μm wide; branched. Hypothecium and subhymenium
colourless (40–)45–60(–70) μm thick, I+blue, aften muddy
in sections. Asci clavate, strongly thickened above, 90–
100×23–30 μm, with 2–3(4) spores. Ascospores hyaline,
Mycol Progress (2013) 12:231–269
globose or broadly ellipsoid, (15–)18.8–[21.6]–24.4(–27)×
(15–)18.4–[20.7]–23.0(–25) μm diam. (n032), spores often
I + yellow to redish yellow. Pycnidia immersed, sometimes
occur in the pseudocyphellae, 1–3 per subsquamulose, single, stretched flask-shaped, internal wall colourless, with
more or less brownish ostiole. Conidia filiform, (15–)18–
23(–26)×1–1.2 μm (n046). Chemistry: All spot-tests (K, C,
KC, CK, P) negative both in the cortex and medulla. TLC
and HPLC: No substances detected. UV: Negative.
Ecology and distribution (Fig. 6b). The ecology and
habitat of Circinaria tominii remains poorly known. It has
been reported from arid steppes of the Altai Region; an area
between Russia, Kazakhstan and Mongolia. Andreeva
(1987) gives some additional localities in Kazakhstan.
Remarks. Circinaria tominii is somewhat similar to small
thalli of C. esculenta, but differs by having consistent
smaller thallus lumps (c. 3–10 mm), being rounded subsquamulose, abundant apothecia (high rate of thallus fertility), and shorter conidia (15–25 μm). In C. esculenta
thalline lumps are often larger (10–40 mm), it consist of
wrinkled subsquamulose, deep cracks occur in between the
subsquamules, and it has larger conidia (10–35 μm).
Unfortunately, DNA extraction from the 80 years old herbarium collection (see also Sohrabi et al. 2010a) was not
successful. However, C. tominii might be yet another close
relative of C. esculenta. It is also found in the same habitats
with C. affinis, but these species have different type of
thallus mophology and are easily distinguished even in the
field. Circinaria affinis has a gyroid thallus and bears large,
conspicuose pseudocyphellae and it is often sterile.
Additional literature reports from Kazakhstan by Andreeva
(1987).
Specimens examined. Russia. Altai Austro-Orientalis, in
deserto Czuensi, 1926, Baranov (H, S); Deserto Czuensi,
Altai Austro-Orientalis, (Kosh-Agach, Altay), 1929,
Baranov (FH, LE, S), ibidem, 1929, Baranov (TUR).
Discussion
The results of the two analyses are only partially comparable
because of the differences in included species. Due to difficulties in getting fresh material of the key species for complete
amplification of selected loci (nrITS, nrLSU and mtSSU) and
missing data, especially from saxicolous species, two independent analyses were performed. One was aimed at the
delimitation of genera within the family Megasporaceae, the
other at species delimitation of ‘manna lichens’.
Generic delimitation The position of the sphaerothallioid
species in the genus Circinaria, and their relationship to
other allied genera of the Megasporaceae is still controversial. In order to study this group of species a combined data
Mycol Progress (2013) 12:231–269
set of mtSSU and nrLSU sequences was assembled. Our
analysis, compared to earlier analyses of the family Nordin
et al. (2010), included many additional specimens from
vagrant sphaerothallioid species, viz., C. affinis, C. cerebroides, C. esculenta, C. fruticulosa, C. hispida, C. gyrosa,
C. lacunosa, C. jussuffii and C. rostamiias well as two
crustose sphaerothallioid species viz., C. elmorei s.lat. and
C. sphaerothallina (see Fig. 1). The results indicated a
monophyletic Circinaria and supported Nordin et al.
(2010). In this study the type species of Chlorangium (C.
jussuffii) and Sphaerothallia (C. esculenta) were included in
addition to the type species of Agrestia (C. hispida) that was
included in Nordin et al. (2010). The results show that all of
these genera are within Circinaria. According to our results
the genus can be divided into two main groups and is quite
heteromorphic. The sphaerothallioid species form their own
clade separate from several saxicolous species (e.g., C. caesiocinerea, C. calcarea, C. contorta, C. gibbosa and C. leprosescens; see Fig. 1) All of these saxicolous species differ
from sphaerothallioid species by having primarily crustose
growth form, thin medulla and cortex layers, and shorter
conidium length (6–12 μm). They are without pseudocyphellae and some of them contain aspicilin. Hafellner (1991) stated
that pseudocyphellae, conidia, ascocarp structure and secondary metabolites are important taxonomic characteristics of the
Hymeneliaceae (including current Megasporaceae) and noted
that as the number of ascospores per ascus decreases there is
often an increase in the size of individual spores. This is also
true for sphaerothallioid species.
Species delimitation The sphaerothallioid group consists of
15 subfruticose and subfoliose vagrant species worldwide.
According to our results they all belong to the genus
Circinaria. Owing to the remarkable morphological plasticity in some populations of the vagrant sphaerothallioid
species, problems in defining monophyletic species were
expected. Likewise, the lack of informative morphological
characters in some species complexes, as well as the occurrence of intermediate forms of thalli between several species, has made accurate delimitation of these taxa difficult.
For these reasons several specimens of each species were
included, whenever possible, in the analysis of the nrITS
data set (Fig. 2). Species with a vagrant morphotype were
prioritized in sampling efforts. Some of the vagrant and
crustose specimens formed distinct clades but the morphology of these specimens is not uniform. They show both
vagrant and crustose morphotypes and are referred to as
erratic species. They comprise several taxa such as C. alpicola, C. aschabadensis, C. elmorei, C. hispida, Circinaria
sp. 1 and Circinaria sp. 2 that occasionally seem to shift
their substrate preference. Only two predominantly saxicolous
species, C. aspera and C. sphaerothallina were included in the
sphaerothallioid clade. It must be mentioned that still our
263
current knowledge of their morphological variation is deficient and more field observations are required. The only
terricolous species in the material is Circinaria sp. 3. which
grows on soil in the arid steppes of central Iran and for which
no vagrant morphotype has yet been observed. As shown in
Fig. 2, vagrant and crustose species of Circinaria are not monophyletic. Vagrant species include C.affinis, C. cerebroides, C.
emiliae, C. esculenta, C. fruticulosa, C. gyrosa, C. lacunosa and
C. rostamii , and they are distributed among crustose species.
The monophyly of C. esculenta and C. jussuffii is of particular
interest, because the application of these names has been confused. Therefore, two samples were included from North Africa
and three from Eurasia and it was confirmed that the two species
are distinct (Fig. 2).
Genetic similarity of crustose and vagrant morphotypes The
specimens of some erratic species included in the analysis
are from the same collection site and they turned out to be
microscopically identical. In the nrITS analyses crustose
and vagrant morphotypes of Circinaria alpicola and C.
aschabadensis confirm the conspecificity of the morphotypes (see Fig. 2). In C. aschabadensis the nrITS sequences
of morphotypes differ from each other only in one base pair,
and in C. alpicola by three positions. This suggests that
identification of erratic species based on external morphology might be misleading. The other example of an erratic
species is the heteromorphic C. hispida that grows on soil
(see Fig. 5c) or develops as a vagrant. This species has never
been reported in saxicolous form. The nrITS sequences were
obtained from seven vagrant specimens (matching the type
species of C. hispida in LE) and three crustose ones.
Although they form a monophyletic entity vagrant and
crustose specimens are not monophyletic but instead mixed
with each other. This result is somewhat congruent with the
findings of Owe-Larsson et al. (2011), which show that C.
hispida is in a group that includes several taxa earlier recognized as A. ‘desertorum’ sensu Krempelhuber (1867).
This implies that C. hispida s.lat. is a rather complicated
species that includes vagrant, terricolous (attached on soil)
and saxicolous specimens and it might comprise several
distinct taxa. Therefore, more extensive sampling and additional molecular markers from several geographically unrelated populations are required to resolve this problem.
Chemistry Only a few studies have been conducted on the
chemistry of sphaerothallioid species. Follmann and Huneck
(1968) traced stictic acid in some North African specimens
of Circinaria jussuffii. Esnault (1985) was able to detect one
additional substance, hypostictic acid. In the present study
no substances were detected in any of the examined species
except C. jussuffii. Here we confirm the earlier reports on
the chemical variation of North African specimens. Stictic
and hypostictic acids typically do not occur in all collections
264
of C. jussuffii. We analyzed several herbarium specimens
and detected that they were not chemically uniform even in
the same envelope. It is still not clear whether occurances of
stictic and hypostictic acids are reflecting at infraspecific
level or not. This issue needs more detailed study.
Note: Recently a new terricolous species, Aspicilia mansourii Sohrabi, was described in Lumbsch et al. (2011). It
contains aspicilin, and therefore its systematic position
needs to be tested and compared with other species in
Circinaria, in particular C. arida, C. caesiocinerea, C. calcarea, C. contorta, C. gibbosa and C. leprosescens, all of
which contain aspicilin. Circinaria sp. 3 is also a terricolous
species but differs from A. mansourii by having large lobes
and pseudocyphellae and lacking aspicilin.
Biogeography and distribution patterns Sphaerothallioid
taxa as a whole show a Holarctic distribution pattern. Most
species are widespread in the Irano-Turanian region in Asia,
the Mediterranean region in North Africa and southern
Europe, and the Madrean region in North America (sensu
Takhtajan 1986). In Eurasia, the largest proportion of vagrant species are Irano-Turanian (e.g., Circinaria affinis, C.
alpicola, C. aschabadensis, C. cerebroides, C. digitata, C.
emiliae, C. esculenta, C. fruticulosa, C. lacunosa, C. rostamii and C. tominii). Only C. jussuffii and C. gyrosa can be
considered as Mediterranean species, both with fairly wide
ranges. The same pattern of distribution is also known for
many plants and isoften referred to as a Mesogean distribution (including large areas of the Mediterranean, IranoTuranian and Saharo-Arabian regions, sensu Quézel 1978).
Circinaria rogeri is known exclusively from North
America. Circinaria hispida is widespread both in Eurasia
and North America, but has not yet been reported from
North Africa. Circinaria alpicola, C. aschabadensis, C.
cerebroides, C. digitata, and C. tominii have restricted distributions in localities with a particular vegetation type.
Circinaria affinis, C. esculenta, C. emiliae, C. fruticulosa
and C. lacunosa are all relatively widespread in the arid
steppes of Central Asia.
Based on altitude, vagrant species occuring in the IranoTuranian region can be divided into three groups: 1) species
found in the lowlands (0–700 m) such as Circinaria affinis,
C. esculenta, C. emiliae, C. fruticulosa, and C. lacunosa; 2)
species largely distributed at mid-elevations (below the alpine zone) on mountains (1000–2000 m) such as C. aschabadensis and C. rostamii; and 3) species with high alpine to
nival zone (2500–4500 m) range, such as C. alpicola, C.
cerebroides, C. digitata and even C. hispida s.str. The
Caspian lowland steppes are at the meeting point of the
Middle East, Europe and Asia. It is a semidesert area that
becomes increasingly arid from north to south and from
west to east (Laity 2008). This is the area where six species
namely C.affinis, C. esculenta, C. emiliae, C. fruticulosa, C.
Mycol Progress (2013) 12:231–269
hispida and C. lacunosa, can be found. Several other subfruticose or subfoliose vagrant lichens have been reported
from such habitats by Kulakov (2002, 2003). In the early
Miocene (c. 22 Mya) due to the dehydration of the eastern
part of the Tethys Sea, desert habitats expanded in Central
Asia (Reichert 1953, Guo et al. 2002). Favourable conditions for xerophytic species were thus formed across large
areas. The other aridification event in the Central Asia took
place during the Middle Pleistocene (c. 1- 0.5 Mya; Dennell
2004). We can assume that some ‘manna lichens’ might
have expanded their range during these aridification periods
and their diversification was possibly accelarated in such
favourable conditions.
The possible endemism of the ‘manna lichens’ is still poorly
known. Based on the data available it seems that some species
are restricted to certain geographical regions. Circinaria alpicola, C. cerebroides and C. digitata are restricted to high
altitudes in the Tian-Shan Mountains (Sohrabi 2011a) and are
exclusively found at around 3000 m. Circinaria aschabadensis
appears to be another ‘endemic’, its distribution restricted to
Kopet-Dagh Mountain on the border of Iran and Turkmenistan,
while C. tominii is known only from the Altai Region, although
our knowledge of its distribution is still very deficient. In North
America C. rogeri might be another example of ‘endemic’
species (see Sohrabi et al. 2011b).
In this study many vagrant species were found sterile and
have not been observed to produce apothecia. Apothecia
were found in the following vagrant species: C. affinis, C.
alpicola, C. aschabadensis, C. emiliae, C. esculenta, C.
fruticulosa, C. gyrosa, C. jussuffii, C. lacunosa, C. rogeri,
C. rostamii and C. tominii. Sufficient information is lacking
on the fertility of C. cerebroides, C. digitata and Eurasian C.
hispida s.str. In contrast to vagrant species, the crustose
morphotypes of the erratic species often produce fertile
thalli. The scarcity of sexual reproduction in vagrant species
raises questions about their dispersal. Many species probably disperse by fragmentation. It has been stated in several
studies (e.g., Bailey 1976, Rosentreter 1993, Leavitt et al.
2011) that fragmentation might be the only method of reproduction in vagrant species. Reproduction by fragmentation apparently restricts dispersal ability and genetic
exchange among populations (see also Leavitt et al. 2011).
During the summer, thalli of vagrant species can dry out
very rapidly, becoming light in weight, and can then easily
be distributed by wind. They are very brittle and their thalli
frequently have fractured or scraped apices, as observed for
example in C. hispida. As far as we know, none of the
vagrant Circinaria species produce isidia, soredia or other
specialized propagules. The sole widespread erratic species
is C. hispida s.lat., which can be found both in North America
and Eurasia (Sohrabi 2011a, b). Such a wide distribution
might be due to an older continuous range in Laurasia.
There are several examples of lichens with such distributions,
Mycol Progress (2013) 12:231–269
notably in the genera Toninia and Caloplaca (Weber 2003).
Finally, according to the present information and extensive
evaluation of literature from other parts of the world, it is clear
that none of the sphaerothallioid species (particularly ‘manna
lichens’) have been reported from deserts or dry lands in
Australasia (Eldridge and Rosentreter 1997), the Far East
(Oxner 1971, Urbanavichus 2010), South America (Redon
1982) and Namib in Africa (Lalley and Viles 2005).
Vagrancy among the sphaerothallioid species The vagrant
growth form of lichenized fungi has evolved in several distantly related fungal lineages, including Lecanoraceae (Rhizoplaca
Zopf), Megasporaceae (Circinaria), Parmeliaceae (Cetraria
Ach., Masonhalea Kärnefelt and Xanthoparmelia (Vain.)
Hale) and Verrucariaceae (Dermatocarpon Eschw.). Elenkin
(1901a, b, c, d, e), Mattick (1951), Weber (1967, 1977), Bailey
(1976), Rogers (1977), Hale (1990), Rosentreter (1993), Arup
and Grube (2000) and Honegger (2001), Sohrabi and Ahti
(2010), Sohrabi et al. (2011a, b) have all briefly discussed
vagrancy in traditional Aspicilia (including current genus
Circinaria). In the study by Elenkin (1901c: 24, 31) the
formation of the vagrant growth form was explained.
Elenkin´s assumptions about this formation process remained
tentative and need to be tested in the light of our current
understanding of thallus formation among the lichenized fungi. In the most recent studies by Honegger (2001), it is stated
that ‘a large number of morphologically less advanced vagrant
lichens do not roll and unroll during drought stress and
rehydration events, but instead have a more or less globose
shape’.
Sphaerothallioid species show different types of substrate
preference, and they can be divided basically into three
groups. Some species are vagrant (obligatorily unattached),
growing and reproducing without proper attachment to a
substrate, i.e., C.affinis, cerebroides, C. esculenta, C. fruticulosa, C. gyrosa, C. jussuffii, C. lacunosa andC. rostamii.
The other type of substrate preference is found in the erratic
species (facultatively unattached) C. alpicola, C. aschabadensis, C. hispida s.lat., Circinaria sp. 1. and sp. 2. These
species show two different morphotypes, probably associated with initially being attached to rocks and then later
developing a vagrant growth form. The third type is represented by crustose (obligatorily attached) species. Our nrITS
analysis shows that several saxicolous species belong to
sphaerothallioid species. Some of them grow on large stones,
some on tiny pebbles. Our results show that vagrancy has
evolved several times in distantly related lineages of the
sphaerothallioid species and several species are shown to be
existed both in vagrant and crustose morphotypes (Fig. 2).
This occurance of such erratic species indicates morphological
convergence and might be due to ecological adaptation. The
reason for the high plasticity in external morphology of vagrant and crustose species remains unknown.
265
Allied saxicolous sphaerothallioid species Several saxicolous or erratic species such as Circinaria alpicola, C. aschabadensis, C. aspera, C. elmorei C. hispida s.lat., C.
sphaerothallina and Circinaria sp. 1-3, are shown here to
belong to the sphaerothallioid clade. They differ from subfruticose vagrant species only by their external morphology.
Based on literature re ports (e.g., Steiner 1919;
Mereschkowsky 1911a, b; Magnusson 1940; Werner 1956,
1958; Oxner 1971; Kondratyuk and Zelenko 2002; Seaward
et al. 2008) several other saxicolous species are documented
that are morphologically and ecologically associated with
sphaerothallioid species (traditional ‘manna lichens’, or the
C. esculenta group). For example, Aspicilia albosparsa
(Werner) S.Y. Kondr., A. auricularis (Werner) S.Y. Kondr.,
A. ferruginea (J. Steiner) Szatala, A. oxneriana O.B. Blum,
A. ochraceoalba (H. Magn.) Golubkova, A. rhizophora
(Müll. Arg.) Hue, A. straussii (J. Steiner) Sohrabi, A.
syriaca (J. Steiner) Szatala, A. tortuosa (H. Magn.) N.S.
Golubk., A. transbaicalica Oxner and the ‘Aspicilia desertorum’ complex have been presented as being related to
‘manna lichens’. Their relationship to Circinaria has not
yet been studied using sequence level data. Obtaining fresh
or recently collected material of these species would be
essential for further study of this group.
New names and combinations
As a consequence of a revised generic concept of Aspicilia
and Circinaria several new combinations are necessary, and
these are listed below.
Circinaria rogeri (Sohrabi) Sohrabi comb. nov. MB
563035 ≡ Aspicilia rogeri Sohrabi, The Bryologist 114:
182, 2011. Type: U.S.A. Oregon: Wallowa Co., The
Nature Conservancy’s Zumwalt Prairie Nature Preserve,
NE of Summer Camp, barren rocky ephemeral seepage
area surrounded by Oregon Palouse Prairie, 1380 m
(4528 ft.), 45.578 N, 116.983 W, 7 August 2007,
Rosentreter 16333 (holotype: SRP, fertile specimen; isotypes:
H, fertile specimen & IRAN).
Circinaria aspera (Mereschk.) Sohrabi & Şenkard.
comb. nov. MB 563036 ≡ Aspicilia desertorum var aspera
Mereschk. in Trudy Obshch. Estest-voisp. Imp. Kazansk.
Univ. 43 (5): 13. 1911.
Lecanora aspera (Mereschk.) Tomin, Prir. Sel'sk. Khoz.
Zasushl.-Pustyn. Obl. S.S.S.R. 1/2: 4. 1927., nom. illeg.,
non. L. aspera Stizenb. (1890). Lectotype: here designated!
Azerbaijan ‘In rupibus calcareis e gub. Baku in Caucaso’,
1893 Lipsky in Elenkin: Lich. Fl. Ross. No. 24b, [(LE,
L2017 lectotype & L2016, L 2018, H isolectotypes). Note:
The specimen in position (A) is Aspicilia alpinodesertorum
f. foliacea Elenkin and belongs to a subumbilicate species in
Aspicilia s.lat. Its status will be discussed together with that
266
of Aspicilia oxneriana in a forthcoming paper by Sohrabi (in
prep). Further study is required of the variants Aspicilia
aspera var. evoluta Oxner and A. aspera var. hispidoides
(Mereschk.) Tomin.
Circinaria sphaerothallina (J. Steiner) Sohrabi comb.
nov. MB 563037 ≡ Aspicilia calcarea var. sphaerothallina
J. Steiner, Ann. Naturhist. Hofmus. 20. 379. 1907.
Additional study is required before a lectotype specimen
for this species can be designated.
In the analyses of the nrITS sequences (Fig. 2) A. tibetica
is included, is sampled in the nrITS analyses (Fig. 2). It was
confirmed that it is not belong to sphaerothallioid species
and is nested within the Lobothallia group. Its systematic
positions and nomenclature will be studied in the revision of
this genus (Sohrabi et al. in prep.).
Acknowledgments The senior author is grateful to O. Vitikainen, A.
Sennikov and N. Bell (all from Helsinki), H. Sipman (Berlin), V. Rico
(Madrid), V. Jhon (Bad Dürkheim), U. Arup (Lund), A. Nordin and B.
Owe-Larsson (both from Uppsala), F. Lutzoni (Durham, NC), A.
Şenkardeşler (Izmir) and W. Obermayer (Graz) for valuable information and discussions. Special thanks are due to B. Litterski
(Greifswald), A. Abbas and H. Xahidin (both from Urumqi), V. Wagner
(Halle), M. Seaward (Bradford), M. Candan (Eskişehir), R. Rosentreter
(Boise, Idaho), M. Andreev (St-Petersburg) and L. Biazrov (Moscow)
for providing fresh material for examination. Masoomeh Ghobad-Nejhad
(Helsinki) is acknowledged for her kind help during the lab work. We
also thank Pirkko Harju and Eija Rinne (both from Helsinki), who
helped us to make microtome sections for some samples, and also the
laboratory technicians at the Department of Biology (Copenhagen) who
helped us with HPLC. This study was supported by awards from the
Iranian Ministry of Science and Technology to the senior author enabling
him to study at the University of Helsinki. MS wishes to thank the
Societas pro Fauna et Flora Fennica for financial support of this study.
We also thank the curators of the indicated herbaria for their help in
searching and lending specimens and are indebted to the anonymous
reviewers for their critical advice and helpful suggestions.
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