The Lichenologist 44(3): 401–418 (2012) 6 British Lichen Society, 2012 doi:10.1017/S0024282911000843
Absence of anthraquinone pigments is paraphyletic and a phylogenetically unreliable character in the Teloschistaceae
Jan VONDRA´ K, Jaroslav Sˇ OUN, Olga VONDRA´ KOVA´ , Alan M. FRYDAY, Alexander KHODOSOVTSEV and Evgeny A. DAVYDOV
Abstract: It has been suggested that the absence of anthraquinones is not a synapomorphic character, but appears independently in unrelated lineages of Teloschistaceae. We analyzed ITS nrDNA regions in species of the genus Caloplaca and present evidence for five such examples: the Caloplaca cerina group, C. obscurella,theC. servitiana group, the C. xerica group and the C. variabilis group (Pyrenodesmia). In some cases, loss of anthraquinones is observed only in individuals within ordinarily pigmented popula- tions, but sometimes the loss covers whole lineages containing one or more species. Both situations are observed in the C. servitiana group. Loss of anthraquinones is always followed by the synthesis of ‘alternative’ pigments (often Sedifolia-grey). In the specimens with anthraquinone-containing apothecia studied, these pigments are not visible in apothecial sections after dissolving anthraquinones in K. Fully unpigmented apothecia have not been observed. The Caloplaca xerica group is a newly established, infraspecific grouping of species related to, and similar to, C. xerica. The Caloplaca servitiana group is also newly established and represents an isolated lineage covering two rather different, but related species. Caloplaca neotaurica is described here as a new species with apothecia of two colour variants; orange-red (with anthraquinones) and grey (with Sedifolia-grey). The genus Huea represents another taxon lacking anthraquinones within Teloschistaceae. The genera Apatoplaca and Cephalophysis, which lack anthraquinones, are tentatively placed in Teloschistaceae, but their phylogenetic identity has not been recognized. Hueidea is reported to have no anthraquinones, but its secondary metabolites should be studied further and its possible placement in Teloschistaceae assessed. We suggest that Caloplaca abbreviata var. lecideoides and C. celata represent variants of C. stillicidiorum lacking anthraquinones. Key words: Apatoplaca, Caloplaca neotaurica, Cephalophysis, Huea, Hueidea, lichens, phylogeny, taxonomy, UV-radiation Accepted for publication 11 October 2011
Introduction J. Vondra´k: Institute of Botany, Academy of Sciences, Za´mek 1, Pru˚honice, CZ-25243, Czech Republic, and In one of the largest lichen families, Teloschis- Faculty of Science, University of South Bohemia, Brani- taceae, the majority of lichens produce yellow- sˇovska´ 31, CZ-370 05, Cˇ eske Budejovice, Czech Re- orange-red anthraquinone pigments in the public. Email: [email protected] J. Sˇ oun: Department of Botany, Faculty of Science, superficial tissues of their fruiting bodies University of South Bohemia, Branisˇovska´ 31, Cˇ eske´ and/or thallus (e.g., Søchting 1997). They Budeˇjovice, CZ-370 05, Czech Republic. are produced in various Teloschistaceae in 1) O. Vondra´kova´: Institute of Steppe (Urals Branch of both thallus and apothecia, 2) in apothecial Russian Academy of Sciences), Pionerskaya st. 11, disc and margin only, 3) in apothecial disc Orenburg, RF-460000, Russia. A. M. Fryday: Herbarium, Department of Plant Biology, only or 4) are entirely absent. Anthraqui- Michigan State University, East Lansing, MI 48824- nones are known to protect lichens from 1312, USA. absorption of UV radiation (Solhaug et al. A. Khodosovtsev: Kherson State University, 40 Rokiv 2003); their content in Xanthoria parietina Zhovtnya str. 27, 73000 Kherson, Ukraine. E. A. Davydov: Altai State University, Lenin Ave. 61, (L.) Beltr. (Teloschistaceae) significantly in- Barnaul, RF-656049, Russia; Tigirek State Reserve, creases with exposition to solar radiation Nikitina, 111, Barnaul, RF-656043, Barnaul, Russia. (Gauslaa & McEvoy 2005). 402 THE LICHENOLOGIST Vol. 44
Some Teloschistaceae also have the ability 2006; Muggia et al. 2008; Vondra´k et al. to synthesize green or grey pigments of 2008; Xahidin et al. 2010). unknown structure, for example, ‘Lecidea- Although the absence of anthraquinones green’ (Wetmore 1996; Arup et al. 2007) or in Teloschistaceae has often been treated as ‘Sedifolia-grey’ (e.g., Wetmore 1996; Meyer an important grouping character, no studies & Printzen 2000), which may have the same to date have tested whether or not this function, that is, protection against UV radia- is a reliable character for classification, or tion (e.g., Hauck et al. 2007). These pigments whether species with such characters repre- usually occur in parts of the thalli or apo- sent a monophyletic group. The purpose of thecia where anthraquinones are absent, al- the present study is to test this hypothesis though both pigments may co-occur in the using a broad sampling of species lacking superficial tissues of the apothecia of some anthraquinones, which would traditionally species. These species, for example, Calo- be treated as closely related (e.g., Muggia placa conversa (Kremp.) Jatta, C. exsecuta et al. 2008). Specifically, we will test whether (Nyl.) Dalla Torre & Sarnth., C. oleicola (J. or not these species can be recovered as a Steiner) van den Boom & Breuss and C. well-supported monophyletic group. pollinii (A. Massal.) Jatta, may resemble those with an entire absence of anthraqui- nones, because their old apothecia turn Materials and Methods black as they contain large amounts of mela- nin pigments. In these cases, the anthraqui- Lichen samples were collected by the authors from vari- ous localities in the Northern Hemisphere. Detailed nones may be identified by the reactions of herbarium data for specimens used in our phylogenetic the apothecial sections (K+ strongly purple- studies are given in Table 1. Data for paratypes of C. violet, K ! HCl+ yellow, N+ orange, N ! neotaurica are abbreviated; full information for samples K+ purple-violet-blue, N ! K ! HCl+ yel- from CBFS is available at http://botanika.bf.jcu.cz/ low; Vondra´k et al. 2010a). lichenology/data.php. The absence of anthraquinones is known at various levels; their absence in the thallus Morphological examinations has arisen in many lineages throughout Telo- A detailed morphological description is given only for schistaceae, for example, the C. cerina group the new species. Measurements are accurate to 0 25 mm (Sˇ oun et al. 2011). Occasional loss of anthra- for cells (e.g., conidia and ascospores), 1 mm for width quinones in the thallus is also documented of asci, or 10 mm for larger structures (e.g., hymenium, width of exciple). All measurements of cells (ascospores, in individuals or populations of species that conidia, asci, paraphyses) include their walls. Paraphyses usually have a pigmented thallus (Søchting tips were observed after treatment with c. 10% KOH. 1973; Vondra´k et al. 2010b). Aberrant popu- Only those ascospores with well-developed septa were lations lacking anthraquinones completely measured; in these ascospores, loculi were connected are suggested in C. tiroliensis Zahlbr. (Hansen with a thin cytoplasmatic channel, never disconnected. Measurements with more than ten repeats (n b 10) are et al. 1987; Søchting 1989) or C. xerica Poelt given as (min.-- ) x#eSD (-- max.), where x#¼ mean value &Veˇzda (Poelt 1975). and SD ¼ standard deviation. Morphological terminol- Species (or individuals) of Teloschistaceae ogy follows Smith et al. (2009). with a complete loss of yellow-orange-red pig- ments, sometimes grouped under Pyrenodes- Chemistry mia (Caloplaca variabilis group), have been The acetone extracts from apothecia were subjected studied since the 19th century but attempts to high-performance liquid chromatography (HPLC) to treat them systematically began with Mag- analysis. Reverse phase column (C18, 5 mm, Lichrocart nusson (1950), followed by Wunder (1974) 250-4) was eluted with MeOH / 30%MeOH+ in the Old World and Wetmore (1994) in 1%H3PO4 for 77 min and the absorbances at 270 nm North America. More recently, several works were recorded (for details see Søchting 1997). The compounds were determined on the basis of their reten- have dealt with this group using single locus tion times and absorption spectra. In the newly described (ITS) molecular data (Arup & Grube 1999; species, five specimens were examined (CBFS JV2048, Tretiach et al. 2003; Tretiach & Muggia 5925, 6023, 7094, 7105). 2012 Teloschistaceae without anthraquinones—Vondra´k et al. 403
Table 1. Sample data, engaging to groups and GenBank accession numbers of the ITS sequences newly generated for phylogenetic analyses.
GenBank Species Specimen Group accession number
Caloplaca Greece: Crete: Sternes, on calcareous stone, C. xerica group JN641762 albolutescens 2005, J. Vondra´k (CBFS JV4098) C. aractina Sweden: Bohusla¨n: Askum par., Barlindarna, C. haematites group JN641763 2006, U. Søchting 10579 (C) C. atroflava Czech Republic: North Moravia:Sˇ umperk, C. xerica group JN641764 Rasˇkov, on serpentinite, 2007, Palice 11741 (PRA) C. cerina, grey Greece: Astakos, on bark of Olea, 2010, C. cerina group JN641765 J. Vondra´k (CBFS JV8329) C. cerina, orange Greece: Astakos, on bark of Olea, 2010, C. cerina group JN641766 J. Vondra´k (CBFS JV8329) C. erythrocarpa Bulgaria: Strandzha Mts: Malko Tarnovo, on C. xerica group JN641767 limestone, 2005, J. Vondra´k (CBFS JV3208) C. fuscoatroides Bulgaria: Black Sea coast: Burgas, Sozopol, C. xerica group JN641768 2007, J. Vondra´k (CBFS JV6468) C. haematites Russia: Caucasus: ‘‘Dagestanskiy zapovednik’’ C. haematites group JN641769 National park, 2009, A. Gabibova (CBFS) C. neotaurica Great Britain: Wales: seashore rocks, U. Arup C. xerica group JN641770 (LD, material lost) C. neotaurica Greece: Peloponnese: 2010, on serpentinite, C. xerica group JN641771 J. Vondra´k & O. Vondra´kova´ (CBFS JV8322) C. neotaurica Ukraine: Crimean Peninsula: Alushta, 2007, C. xerica group JN641772 on siliceous stone, J. Vondra´k (CBFS JV6023) C. neotaurica Ukraine: Crimean Peninsula: Karadag, 2007, C. xerica group JN641773 on siliceous stone, J. Vondra´k (CBFS JV6229, isotype) C. neotaurica Ukraine: Crimean Peninsula: Yalta, on C. xerica group JN641774 siliceous stone, 2009, J. Vondra´k& A. Khodosovtsev (CBFS JV7121) C. neotaurica, grey Ukraine: Crimean Peninsula: Alushta, on C. xerica group JN641775 schist, 2007, J. Vondra´k (CBFS JV5475) C. neotaurica, Greece: Peloponnese: Argolis Peninsula, C. xerica group JN641776 grey (1) on serpentinite, 2010, J. Vondra´k& O. Vondra´kova´ (CBFS JV8322) C. neotaurica, Greece: Peloponnese: Argolis Peninsula, C. xerica group JN641777 grey (2) on serpentinite, 2010, J. Vondra´k& O. Vondra´kova´ (CBFS JV8322) C. servitiana Greece: Pindos Mts: Profitis Ilias, on bark of C. servitii group JN641778 Qercus coccifera, 2005, T. Spribille 16225 (CBFS JV6974) C. servitiana Greece: Crete: Psiloritis Mts, upper end of C. servitii group JN641779 Rouvas Gorge, on Quercus coccifera, 2004, T. Spribille 13700 (hb. T. Spribille) C. soralifera Ukraine: Khmelnitsk’ region: Kamenets- C. xerica group JN641780 Podolsky, on limestone, 2006, J. Vondra´k (CBFS JV4594) C. aff. soralifera Czech Republic: Prachatice, on gneiss, 2009, C. xerica group JN641781 J. Vondra´k & O. Vondra´kova´ (CBFS JV8325) 404 THE LICHENOLOGIST Vol. 44
Table 1. Continued
GenBank Species Specimen Group accession number
Caloplaca sp. Russia: Southern Ural Mts: Orenburg, Pyrenodesmia 2 JN641784 on limestone, 2009, J. Vondra´k (CBFS JV8182) Caloplaca sp. Russia: Southern Ural Mts: Orenburg, Pyrenodesmia 2 JN641783 on conglomerate, 2009, J. Vondra´k (CBFS JV8179) Caloplaca sp. Russia: Southern Ural Mts: Orenburg, Pyrenodesmia 2 JN641782 on conglomerate, 2009, J. Vondra´k (CBFS JV8326) Caloplaca sp. Kazakhstan: Mangistau region: Beyney, Pyrenodesmia 2 JN641785 on limestone, 2009, J. Vondra´k& A. Khodosovtsev (CBFS JV7635) Caloplaca sp. Ukraine: Doneck upland: Luhansk, Rozkishne, Pyrenodesmia 2 JN641786 on marl, 2007, O. Nadyeina (hb. O. Nadyeina) Caloplaca sp., grey China: Xinjiang: Qinghe county, Mongolian C. servitii group JN641787 Altai, west slope of Mt. Kara-Balchigtau, alt. 2400 m, on plant debris, 2007, E. A. Davydov 6876b (CBFS JV8413) Caloplaca sp., China: Xinjiang: Qinghe county, Mongolian C. servitii group JN641788 yellow Altai, west slope of mt. Kara-Balchigtau, alt. 2400 m, on plant debris, 2007, E. A. Davydov 6876a (CBFS JV8414) C. stillicidiorum, USA: Alaska: Atqasuk, on bone, 2001, C. cerina group JN641789 grey A. Fryday 8158 (MSC 57393) C. teicholyta Romania: Dobrogea: Tulcea, on limestone, C. xerica group JN641790 2007, J. Vondra´k (CBFS JV5381) C. teicholyta Ukraine: Crimean Peninsula: Bakhchisaray, C. xerica group JN641791 on limestone, 2006, J. Vondra´k (CBFS JV5675) C. xerica Greece: Crete: Ano Viannos, on siliceous rock, C. xerica group JN641792 2005, J. Vondra´k (CBFS JV4119) C. xerica Czech Republic: Krˇivokla´tsko: Horˇovice, C. xerica group JN641793 on siliceous rock, 2003, J. Vondra´k (CBFS JV1124)
Apothecial pigments were also examined by reactions manually trimmed to eliminate the unaligned ends and in sections with Cl (C), KOH (K), HCl and HNO3 (N) ambiguously aligned regions of ITS1 and ITS2. Baye- according to Meyer & Printzen (2000). sian phylogenetic analyses were carried out using the program MrBayes 3.1.1 (Ronquist & Huelsenbeck 2003). DNA extraction and amplification The optimal nucleotide substitution models were found using the program MrModeltest v2.3 (Nylander 2004). Direct PCR was used for PCR-amplification of the The MCMC analyses were performed in two runs, each ITS regions including the 5.8S gene of the nuclear with four chains starting from a random tree and using rDNA following Arup (2006). Primers for amplification the default temperature of 0 2. Every 100th tree was were ITS1F (Gardes & Bruns 1993) and ITS4 (White sampled and standard deviation of splits between runs et al. 1990). PCR cycling parameters follow Ekman less than 0 01 as a convergence criterion was used to (2001). assess burn-in. Models of nucleotide substitution, num- Phylogenetic analyses bers of generations and discarded generations, numbers of sequences and lengths of each alignment are given in Sequences were aligned using MAFFT 6 (on-line ver- Table 2. Posterior probabilities are shown in all depicted sion in the Q-INS-i mode; see Katoh et al. 2002) and phylogenetic trees (Figs 1–6). Tree terminals of samples 2012 Teloschistaceae without anthraquinones—Vondra´k et al. 405
Table 2. Models of nucleotide substitution, numbers of generations and discarded generations, numbers of sequences and lengths of alignments for the molecular analyses.
Number of Number of Number of retained Substitution Number of discarded Tree sequences positions model generations generations
Caloplaca cerina group 25 433 GTR+G 1 106 297 000 Caloplaca obscurella 21 528 GTR+I+G 1 106 259 000 Caloplaca servitii group 15 536 SYM+G 1 106 135 000 Caloplaca xerica group 21 477 GTR+G 10 106 726 000 Pyrenodesmia group 28 480 GTR+G 10 106 615 000 Teloschistaceae 33 398 GTR+I+G 10 106 1 582 000
without anthraquinones are in green (absence on popu- grey/black thallus without anthraquinones, lation level) or yellow (absence on species level). and lecanorine apothecia with distinct thal- line exciple lacking anthraquinones but with anthraquinone pigmented (yellow/orange/red) Results and Discussion discs. We generated 29 new sequences and used We have observed individuals entirely lack- them in six different alignments. Five align- ing anthraquinones in the Mediterranean ments were for specifically studied groups lineage of Caloplaca cerina (Hedw.) Th. Fr. ˇ and one for a broad context. We found that s. lat. (group A in Soun et al. 2011) and in the character of anthraquinone absence is the arctic lineage of Caloplaca stillicidiorum ˇ polyphyletic, occurring in five different clades; (Vahl) Lynge (group 3 in Soun et al. 2011). the Caloplaca cerina group, C. obscurella,theC. Both examples are morphologically similar servitiana group, the C. xerica group and the to their closest relatives; important similari- C. variabilis group (Pyrenodesmia). In some ties are lecanorine exciples, distinct cortex cases, whole lineages of anthraquinone-con- in lower exciple and presence of Sedifolia- taining species contain one or more species grey pigment in the thalline exciple. The arc- that lack these pigments (‘absence on species tic sample has smaller ascospores (c. 10– level’), whereas in others loss of yellow-orange 15 6–8 mm) than the phylogenetically pigments is restricted to individuals or popu- closest observed specimens of C. stillicidio- lations of species that normally contain an- rum with orange discs (c. 13–16 7–9 mm). thraquinones (‘absence on population level’). Both samples differ from other specimens In the latter case, specimens lacking anthra- in the C. cerina group by the presence of quinones always have some alternative pig- Sedifolia-grey in the apothecial disc (in sec- ment in their apothecia (usually Sedifolia- tion: K+ violet, C+ orange-carmine, N+ grey), which is not identified in apothecia orange-red-purple); we have not observed with anthraquinones; that is, it is not apparent this pigment in orange, anthraquinone- in the apothecial sections after dissolving the containing discs. Both specimens investi- anthraquinones in K. Each case will be dis- gated are placed into the named groups cussed specifically. (PP ¼ 1 00 in both; Fig. 1A). In the avail- able material, non-anthraquinone phenotypes Caloplaca cerina group (absence on occur side by side with their counterparts population level) with orange discs (Fig. 1B & C). The arctic specimen of C. stillicidiorum This homogeneous group (Sˇoun et al. 2011) lacking anthraquinones is probably conspe- clusters crustose Teloschistaceae with a white/ cific with C. celata Th. Fr., which appears to 406 H LICHENOLOGIST THE o.44 Vol. Fig.1. Caloplaca cerina group. A, Bayesian phylogeny (ITS nrDNA regions) of a part of the group containing lineages of C. cerina and C. stillicidiorum with individuals lacking anthraquinones (in green); B, two phenotypes of C. cerina (CBFS JV8329), grey apothecia without anthraquinones (left) and normally coloured apothecia (right); C, C. stillicidiorum (Fryday 8158; MSC) with grey, white pruinose apothecia (right) and with orange, normally coloured apothecia (left) and with C. cf. tiroliensis in the upper part. Scales: B & C ¼ 1mm. 2012 Teloschistaceae without anthraquinones—Vondra´k et al. 407 have the same ecology and identical mor- this pigment is present only in the thallus of phology (Magnusson 1950; Poelt 1955; the variant with red apothecia. The non- Hansen et al. 1987; Søchting et al. 2008). anthraquinone specimen from the Crimean Caloplaca abbreviata var. lecideoides H. Magn., Peninsula (CBFS JV6942) nests safely inside a lignicolous lichen from the Russian arctic, the C. neotaurica monophylum (PP ¼ 1 00), seems to be another name referring to C. but specimens examined from Greece have stillicidiorum lacking anthraquinones; the type aberrant ITS sequences and the Bayesian specimen in S (http://andor.nrm.se/kryptos/ phylogeny placed them as a sister group to kbo/kryptobase/200803/max/32948.jpg) ap- other C. neotaurica samples (Fig. 2A). parently contains a mixed population with Although he did not do so explicitly, Poelt orange and grey apothecia. (1975) already recognized the absence of an- The description of Pyrenodesmia monacensis thraquinones at the population level within Leder., currently known as Caloplaca mona- this group in Caloplaca xerica; its anthra- censis (Leder.) Lettau, is also based on non- quinone-lacking populations are named C. anthraquinone containing specimens (Lederer xerica var. venostana. 1896). Nevertheless, our data have shown that C. monacensis is a well-characterized, widely Pyrenodesmia group (absence on distributed and usually anthraquinone-con- species level) taining species from the C. cerina group (Sˇ oun et al. 2011). The C. variabilis group (Pyrenodesmia)isa well-known group containing most of the Caloplaca xerica group (absence on European saxicolous species without an- population level) thraquinones but with Sedifolia-grey in the apothecia (in section K+ violet, C+ orange- The ‘Caloplaca xerica group’ represents a carmine, N+ orange-red-purple-black). Our monophyletic group (PP ¼ 1 00 in Fig. 2A) data show that Pyrenodesmia is unresolved of mainly saxicolous species with the follow- within the Caloplaca xerica group and the C. ing characters: thallus without orange-red haematites group (PP ¼ 0 97 for the whole pigmentation, devoid of anthraqinones but group; Fig. 3). The internal taxonomy and with Sedifolia-grey in cortical tissues (K+ phylogeny of this group have been reported violet reaction in sections); apothecia orange (Tretiach et al. 2003; Tretiach & Muggia to red, containing anthraquinones; ascospores 2006; Muggia et al. 2008; Vondra´k et al. never narrowly ellipsoid, length/breadth ratio 2008), but the group is still only partially 1 4–2 6; pycnidia grey-black, devoid of an- known in Europe and North America and it thraqinones. The C. xerica group is related is little known in Asia. For instance, the to Pyrenodesmia and the C. haematites com- group is species-rich in Central Asia (J. plex (Fig. 3). Vondra´k, unpublished data). Based on our This species-rich group contains many set of sequences, two main internal lineages unnamed taxa, one of which is Caloplaca are to be found within Pyrenodesmia; Pyre- neotaurica (Fig. 2B) that is formally described nodesmia 1 with most of the European at the end of this paper. Caloplaca neotaurica taxa (unsupported) and Pyrenodesmia 2 is unusual within the group because it also containing mainly unknown taxa from the has phenotypes with complete loss of anthra- southern Ural Mountains, the Near East quinones, which usually occur along with and the steppe-desert zone of the most SE phenotypes with red apothecia (Fig. 2C). region of Europe (PP ¼ 0 97). Non-anthraquinone phenotypes are morpho- logicallyeidentical to their counterparts with Caloplaca obscurella (absence on red apothecia, but all samples observed with- species level) out anthraquinones had apothecia contain- ing Sedifolia-grey (in section K+ violet, C+ Currently, we know little about the closest orange-carmine, N+ orange-red-purple-black); phylogenetic relatives of Caloplaca obscurella 408 H LICHENOLOGIST THE o.44 Vol. Fig.2. Caloplaca neotaurica. A, Bayesian phylogeny (ITS nrDNA regions) of the C. xerica group (delimited by the red line) with the monophylum of C. neotaurica (delimited by the blue line); species without anthraquinones in yellow; specimens of C. neotaurica without anthraquinones in green; B, C. neotaurica, isotype (CBFS JV6229); C, C. neotaurica, phenotype with anthraquinones (left) and phenotype with grey apothecia (right) in Peloponnese (CBFS JV8322). Scales: B & C ¼ 1mm. 2012 Teloschistaceae without anthraquinones—Vondra´k et al. 409
Fig. 3. Bayesian phylogeny of ITS nrDNA regions showing the two groups of Pyrenodesmia in polytomy with the C. haematites group and the C. xerica group; species without anthraquinones highlighted in yellow.
( J. Lahm) Th. Fr. (Fig. 4A). It forms a the C. obscurella clade contains only a single strongly supported clade (PP ¼ 1 00), sister species. We suggest that the North American to the large monophylum containing the C. species C. brunneola Wetmore, C. camptidia haematites group, the C. xerica group and (Tuck.) Zahlbr. C. dakotensis Wetmore (Wet- Pyrenodesmia (PP ¼ 1 00), but we failed to more 1994) and C. lecanoroides Lendemer find closer relatives. It is also unclear whether (Lendemer et al. 2010) might belong here 410 THE LICHENOLOGIST Vol. 44
Fig.4. Caloplaca obscurella. A, Bayesian phylogeny of ITS nrDNA regions; sister relationship of C. obscurella is shown to the clade containing C. haematites group, C. xerica group and Pyrenodesmia (delimited by the red square); species without anthraquinones highlighted in yellow; B, richly fertile specimen from Russia (CBFS JV7641). Scale ¼ 1mm. 2012 Teloschistaceae without anthraquinones—Vondra´k et al. 411
Fig.5.Caloplaca servitiana group. A, Bayesian phylogeny of ITS nrDNA regions containing C. servitiana with absence on species level (in yellow) and a species from China with absence on population level (in green); B, C. servitiana (Spribille 13705); C, species from China (Davydov 6876; CBFS) with yellow and grey apothecia growing side by side; D, species from China, the phenotype with grey apothecia (Davydov 6876b; CBFS) together with C. stillicidiorum (orange apothecia with white margins). Scales: B–D ¼ 1 mm.
because all these species contain brown pig- (absence on population level; Fig. 5C & D). ments in the epihymenium that resemble This group is the only one with the lack of those in C. obscurella (K-- ,C-- ,N-- , acetone anthraquinones found in the ‘Lineage 1’ of insoluble, not detectable by HPLC). Teloschistaceae (sensu Gaya et al. 2008; Fig. 6). It is a rather isolated group with no known closely related lineages. Caloplaca servitiana group (absence on both species and population level) 1) A brief description of C. servitiana is available in Vondra´k et al. (2010a). It is We revealed two species in the Caloplaca known only from several sites in the eastern servitiana group (Fig. 5A); 1) C. servitiana Mediterranean, where it grows on trees with Szatala s. str. (absence on species level; Fig. various other Caloplaca species. Our com- 5B) and 2) an unnamed species from China parison of this phenotype with co-occurring 412 THE LICHENOLOGIST Vol. 44
Fig. 6. Bayesian phylogeny (ITS nrDNA regions) of Teloschistaceae with two sequences of Physciaceae as an out- group. Representatives of the main lineages within the family have been selected for the tree terminals. Lineages lacking anthraquinones at the population level are in green and at species level in yellow.
Caloplaca species showed that it had a strong is not closely related to any known European similarity with C. aegatica Giralt et al., which species. challenged us to test if C. aegatica and C. 2) The unnamed specimen from the Altai servitiana are a single species. Our results Mountains (north-west China) is character- show that C. aegatica is closely related to C. ized by an inconspicuous, simplified thallus cerinella (Nyl.) Flagey, whereas C. servitiana and biatorine to zeorine apothecia with a 2012 Teloschistaceae without anthraquinones—Vondra´k et al. 413 distinct, c. 70–100 mm wide, proper exciple. ments contained in herbarium specimens of The thalline exciple is usually reduced and some little-known arctic species, Caloplaca restricted to the lower part of the apothecial atrocyanescens (Th. Fr.) H. Olivier, C. conci- margin. The ascospores, c. 14–18 7–9 mm, nerascens (Nyl.) H. Olivier and C. diphyes have a characteristic ‘obtuse rhomboid’ (Nyl.) H. Olivier. These species have blackish shape. In the specimen observed, the apothe- apothecia without anthraquinones, but con- cia have two colour variants (Fig. 5C & D). tain different pigments (blue-green-olive) The first is yellow, contains anthraquinones with various reactions with K, N and C in and lacks Sedifolia-grey, whereas the second sections, but the identity of these pigments is grey, devoid of anthraquinones, and con- is unknown. The phylogenetic positions of tains Sedifolia-grey (in section K+ violet, C+ these taxa are also not yet known. Other red, N+ red) in the epihymenium and super- rare and little-known European species with ficial cells of the excipulum. black apothecia that contain unknown pig- ments are C. concilians (Nyl.) H. Olivier and C. conciliascens (Nyl.) Zahlbr. In addition, Other Teloschistaceae without anthraquinones Caloplaca sorocarpa (Vain.) Zahlbr. has brown apothecia but is very rarely fertile and it is Among the genera of Teloschistaceae, the not known which pigments are present in its entire loss of anthraquinones is known only apothecia. in the paraphyletic genus Caloplaca (Fig. 6). Caloplaca atrosanguinea (G. Merr.) I. M. Species or populations with entire loss of Lamb is a North American corticolous spe- anthraquinones are not known within foliose cies which has brown (young) or black (old) and fruticose genera of Teloschistaceae,al- apothecia. Its apothecial pigment is violet- though in some specimens of, for example, blue in section and reacts: K+ violet-blue Seirophora lacunosa (Rupr.) Fro¨de´nandsome intensifying, K ! HCl+ sordid green, N-- Teloschistes species, whole thalli are grey with unchanged, N ! K+ weekly purple ! dis- anthraquinones restricted to the apothecial coloured, N ! K ! HCl-- discoloured, C-- discs and the walls of pycnidia (e.g., Søchting discoloured. These reactions do not corre- & Fro¨de´n 2002). spond to anthraquinones, which are typically Our study has been carried out only on K ! HCl+ strongly yellow. The HPLC chro- specimens from arctic-temperate-(subtropi- matogram shows one major unknown sub- cal) zones of the Northern Hemisphere, but stance with a short retention time (Rt ¼ 13 6 species without anthraquinones are known min, which is less than any known anthraqui- from the tropics and the Southern Hemi- none in Teloschistaceae) but also a minor sub- sphere: for example, Caloplaca filsonii Hafell- stance (Rt ¼ 33 3 min) with the absorption ner et al. (Australia; Kondratyuk et al. 2007), spectrum similar to emodin that we identified C. gambiensis Aptroot (Gambia; Aptroot as an unknown anthraquinone. Caloplaca atro- 2001), C. jatolensis Y. Joshi & Upreti (India; sanguinea is related to, but not within, the C. Joshi et al. 2008), C. lewis-smithii (Antarc- cerina group ( J. Vondra´k, unpublished data). tica; Søchting & Øvstedal 1998), Caloplaca Caloplaca demissa (Ko¨rb.) Arup & Grube yammeraensis S. Y. Kondr. et al. (Australia; also lacks anthraquinones, but it has proba- Kondratyuk et al. 2009) and some tropical bly never been found with apothecia. If it is species with tri- to tetralocular ascospores able to produce apothecia, they may contain (Hafellner & Poelt 1979). It is probable that anthraquinones because its closest related spe- these species belong to diverse groups that cies, C. carphinea (Fr.) Jatta (Gaya et al. 2008), are unrelated to the lineages shown in this has anthraquinone-containing apothecia. study. Another lineage in Teloschistaceae that lacks Additional lineages with species or indi- anthraquinones is represented by the genus viduals that do not produce anthraquinones Huea C. W. Dodge & G. E. Baker (Dodge will also certainly be found in the Northern & Baker 1938). This genus was erected for a Hemisphere. We have examined the pig- group of crustose Antarctic species of Telo- 414 THE LICHENOLOGIST Vol. 44 schistaceae characterized by lacking anthra- suggesting the presence of anthraquinones quinones, and having black apothecia with and that the genus may be better placed in a carbonaceous exciple and a bright blue Teloschistaceae. epihymenium. The status of Huea is con- troversial, with some authors accepting it Conclusions (Øvstedal & Lewis Smith 2001) whereas others include the species in Caloplaca (e.g., 1. Non-anthraquinone lineages or popula- Poelt & Hafellner 1980). Søchting et al. tions represent a minor part of Teloschistaceae (2004) cited unpublished preliminary molec- but they originated repeatedly in various ular data showing that the two species trans- sites in the phylogeny of the family (Fig. 6). ferred to Huea by Dodge & Baker (1938) formed a distinct clade in Caloplaca. Un- 2. We have observed individuals without an- fortunately, there are problems with the typ- thraquinones (absence on population level) ification of Huea because Dodge & Baker in the Caloplaca cerina group, the C. servitiana (1938) chose as the type species their newly group and the C. xerica group. Lineages con- described species Huea flava C. W. Dodge taining non-anthraquinone species (absence & G. E. Baker. This is usually considered to on species level) were recognized in Caloplaca be a sterile crust of uncertain identity but obscurella,theC. servitiana group and Pyreno- was shown by Fryday (2011) to be conspe- desmia. cific with Lecidea capsulata C.W. Dodge & 3. Loss of anthraquinones is always followed G. E. Baker. As this species is now included by synthesis of alternative pigments (often in the synonymy of Carbonea vorticosa (Flo¨rke) Sedifolia-grey); fully unpigmented apothecia Hertel, (http://www.indexfungorum.org/Names/ have not been observed by us. Anthraqui- NamesRecord.asp?RecordID=107792) this nones and the alternative pigments may per- makes Huea an earlier name for Carbonea. form the same function, perhaps protection Søchting et al. (2004) proposed a conserved of ascospores against absorption of the UV- type for Huea [Huea coralligera (Hue) C. W. B radiation. Dodge & G. E. Baker] but, because they did notdosoasaformalproposal,thishasno relevance. The typification of Huea is dealt Taxonomy with in detail by Fryday (2011). Caloplaca neotaurica Vondra´k, Apatoplaca Poelt & Hafellner and Cepha- Khodosovtsev, Arup & Søchting sp. nov. lophysis H. Kilias are monotypic genera with an absence of anthraquinones affiliated to MycoBank No: MB563136 Teloschistaceae mainly because of their Telo- Caloplacae fuscoatroidis similis sed thallo ambitu squa- schistaceae-type asci (Poelt & Hafellner 1980; mulis nullis, tenui, atrogriseo vel nigrescenti, epruinoso vel raro pruinoso. Kilias 1985); however, their phylogenetic Typus: Ukraine, Crimean Peninsula, Sudak, Kara- identities are uncertain. dag Mts, Mt Svyataya, alt. 320 m, 44 560 03 2700 N, Also of interest is the genus Hueidea Kant- 35 130 06 1700 E, on volcanic rock, 24 May 2007, J. vilas & P. M. McCarthy (Kantvilas & Vondra´k (CBFS JV5925—holotypus; CBFS JV5960, McCarthy 2003), which was erected for a 6022, 6229 & C—isotypi). ITS sequence of the isotypus: JN641773. single Australian species, H. australiensis Kantvilas & P. M. McCarthy, with charac- (Fig. 2) ters intermediate between Teloschistaceae Thallus thin, less than 150 (rarely 250) mm and Fuscideaceae V. Wirth & Veˇzda. The high, grey to brown-black, rarely white prui- authors characterized their new genus as nose, indistinctly areolate; areoles (150-- ) lacking thalline chemistry and showing all 322e112(-- 600) mmwide(n ¼ 20). Prothal- spot-test reactions negative, and placed it lusepresent, dark grey. Marginal squamules in Fuscideaceae. However, inspection of a and vegetative diaspores absent. Cortex ab- specimen of H. australiensis revealed a weak sent; alveolate cortex (sensu Vondra´k et al. K+ crimson reaction in the epihymenium, 2009) present in spots (<20 mm thick). 2012 Teloschistaceae without anthraquinones—Vondra´k et al. 415
Apothecia <0 7 mm diam., biatorine, grey, conidia ellipsoid. Chemosyndrome C2 orange to red (grey in variants without an- (details above). thraquinones), K+ purple, C+ purple, I-- Variability. Apart from two variants of (disc I+ blue due to reaction with asci), P-- (but red pigment dissolves in acetone solu- apothecia (with/without anthraquinones), the species varies strongly in the content of tion of P), UV-- ; no visible spot reactions in Sedifolia-grey in the thallus. While northern grey apothecia. Exciple usually paler than the specimens from Great Britain have a pale disc. Proper exciple c. 100–130 mmthickproso- grey thallus with an indistinct amount of the plectenchymatous. Thalline exciple c. 60–120 grey pigment, specimens from the Medi- mm thick. Hymenium c. 90–110 mm high. terranean regions have a darker thallus, with Paraphysesebranched and anastomosed, an observable Sedifolia-grey content in sections. with tips widened to (3 3–)4 4e1 5(–6 0) mm(n ¼ 10). Asci clavate, c. 55–75 18–26 Similar species. Caloplaca atroflava (Turner) mm. Ascospores (13 0-- )14 7e1 4(–17 3) Mong. differs in its paler and C-- apothecia (7 0–) 8 9e1 0(–11 3) mm(n ¼ 25); ratio (absence of chlorinated anthraquinones). of ascospore length/breadth (1 4–)1 7e Caloplaca crenularia (With.) J. R. Laundon 0 2(–2 0); (n ¼ 25); ascospore septa (3 5–) and related species have red pycnidial walls 5 7e0 9(–8 0) mm wide (n ¼ 25); asco- (with anthraquinones) and chemosyndrome spore septa/spore length (0 27–)0 39e C3 or C4 (with constant content of parietin 0 07(–0 54); (n ¼ 25). and fragilin). Caloplaca fuscoatroides J. Steiner Pycnidia common, usually observable as differs in its thick thallus (100–350 mmhigh), darker spots in thallus (higher concentration usual presence of marginal squamules (up of Sedifolia-grey around ostiole). Conidia ellip- to 2 mm diam.) and chemosyndrome C5 soid c. 2 5–3 5 1 0–1 5 mm. (with stable content of fragilin and absence Chemistry. In apothecia, the main anthra- of citreorosein and emodinal), while Calo- ˇ quinone is 7–Cl-emodin; additional anthra- placa xerica Poelt & Vezda has a blastidiate- ezeorine apothecia quinones: 7–Cl-emodinal, 7–Cl-emodic acid, isidiate-lobulate thallus, and chemosyndrome C5 (as in C. fuscoa- 7–Cl-citreorosein, ecitreorosein, eemodi- troides). nal, eemodin (chemosyndrome C2, sensu Søchting 2001). Sedifolia-grey in thallus and Chemosyndrome C2 (absence of parietin and fragilin and traces of citreorosein and in grey variants of apothecia (K+ violet, C+ emodinal) has been observed only in Calo- orange-red, N+ purple in section). placa ligustica B. de Lesd. (Søchting 2001), Etymology. The species is very common in which is probably unrelated to the new the Crimean Peninsula, which was known as species having narrow ascospores with thin ‘Taurica’ by the Greeks and Romans. The septa (Bouly de Lesdain 1936) similar to C. name Caloplaca taurica Mereschk. nomen subpallida s. lat. nudum [¼C. inconnexa (Nyl.) Zahlbr.] al- ready exists and, although this is not validly Phylogeny. Most sequences of the new published and so does not prevent the use species examined form a well-supported of that name for our species, we have decided monophylum (PP ¼ 1 00), but two sequences not to use it in order to avoid confusion. (not identical) of one Greek specimen with grey apothecia are somewhat different, and Diagnostic characters. Thallus dark grey to their relationship to the core clade is unsup- brown-black (rarely white pruinose), thin, ported. Based on phenotype similarities, we usually up to 150 mm thick; without marginal decided to place the Greek specimen (con- squamules and vegetative diaspores. Apothe- taining also individuals with red apothecia) cia small (up to 0 7 mm), biatorine, orange- into Caloplaca neotaurica. The nearest re- red, C+ purple (except in grey apothecial lated species may be a morphologically dif- variants). Ascospores c. 14–17 7 5–10 5 ferent C. xerica, but the relationship is un- mm, with septa c. 4 0–7 5 mm wide. Pycnidia supported. 416 THE LICHENOLOGIST Vol. 44
Ecology and distribution. The species occurs www.synthesys.info/, which is financed by European on siliceous cliffs, outcrops or stones not far Community Research Infrastructure Action under the from the sea coast and is only rarely observed FP7 ‘‘Capacities’’ Program. further inland (only in the Peloponnese and in the Rhodopes, Bulgaria). It is distributed References in the Mediterranean and the Black Sea coast Aptroot, A. (2001) Lichens from Gambia, with a new (especially in the Crimean Peninsula) and black-fruiting isidiate Caloplaca on savannah trees. Cryptogamie, Mycologie 22: 265–270. along the Atlantic coast of Europe (confirmed Arup, U. (2006) A new taxonomy of the Caloplaca citrina from Great Britain). Phenotypes with grey group in the Nordic countries, except Iceland. apothecia are known only from the Crimean Lichenologist 38: 1–20. Peninsula, Cyprus and Greece. Arup, U. & Grube, M. (1999) Where does Lecanora de- missa (Ascomycota, Lecanorales) belong? Lichenolo- gist 31: 419–430. Specimens examined with red apothecia. Bulgaria: Arup, U., Arneng, E. & Søchting, U. (2007) Caloplaca Black Sea coast: Burgas, Sinemorets, 2007, J. Vondra´k fuscorufa—a misunderstood species in northern (CBFS JV6497); Burgas, Sozopol, 2007, J. Vondra´k Europe. Lichenologist 39: 409–414. (CBFS JV6452). Rhodopes: Momchilgrad, Bregovo, Bouly de Lesdain, M. (1936) Notes liche´nologiques. 2004, J. Vondra´k (CBFS JV2043).—Cyprus: Distr. 29. Bulletin de la Societe´ Botanique de France 83: 5–9. Paphos: Tripylos, 1987, M. & H. Mayrhofer 7750 Dodge, C. W. & Baker, G. E. (1938) The Second Byrd (GZU).—Great Britain: Wales: V.C. 45 Permbro- Antarctic Expedition. Botany. II. Lichens and lichen keshire: 1992, U. Arup (LD 1118360, 1118540, parasites. Annals of the Missouri Botanical Garden 25: 1424694).—Greece: Peloponnese: Argolis Peninsula 515–718. (Peiraias administrative district), Driopi, 2010, J. Ekman, S. (2001) Molecular phylogeny of the Bacidia- Vondra´k & O. Vondra´kova´ (CBFS JV8322); Methana, ceae (Lecanorales, lichenized Ascomycota). Mycolog- Kypseli, 2010, J. Vondra´k & O. Vondra´kova´ (CBFS ical Research 105: 783–797. JV8435); Thermissia, Vlachaiika, 2010, J. Vondra´k& Fryday, A. M. (2011) How should we deal with the Ant- O. Vondra´kova´ (CBFS JV8436); Tripoli, Kastri, 2010, arctic and Subantarctic taxa published by Carroll J. Vondra´k & O. Vondra´kova´ (CBFS JV8438).—Italy: William Dodge? Opuscula Philolichenum 9: 89–98. Sardinia:Nu´oro, Barba´gia Seu´lo, alt. 950–1080 m, Gardes, M. & Bruns, T. D. (1993) ITS primers with 1986, H. Mayrhofer 6156, 5941 (GZU, sub C. atro- enhanced specificity for basidiomycetes. Application flava).—Turkey: Sea of Marmara coast: Kapıdag˘ı Penin- for the identification of mycorrhizae and rust. sula, 2007, J. Vondra´k (CBFS JV6459).—Ukraine: Molecular Ecology 2: 113–118. Crimean Peninsula: Alushta, Demerji Yayla, 2007, J. Gauslaa, Y. & McEvoy, M. (2005) Seasonal changes in Vondra´k (CBFS JV5996); Alushta, Kanakskaya balka, solar radiation drive acclimation of the sun-screen- 2007, J. Vondra´k (CBFS JV6023, 6041); Feodosia, ingcompoundparietininthelichenXanthoria parie- Karadag, Mt Levinsona-Lessinga, 2000, A. Khodo- tina. Basic and Applied Ecology 6: 75–82. sovtsev (KHER 200, 201 sub Caloplaca atroflava); Gaya, E., Navarro-Rosine´s, P., Llimona, X., Hladun, Feodosia, Mt Choba-Tepe, 2001, A. Khodosovtsev N. & Lutzoni, F. (2008) Phylogenetic reassessment (KHER 2874, 2873 sub Caloplaca scotoplaca); Sudak, of the Teloschistaceae (lichen-forming Ascomycota, Dachnoe, 2008, J. Vondra´k (CBFS JV7231); Sudak, Lecanoromycetes). Mycological Research 112: 528– Mt Echkedag, 2008, J. Vondra´k (CBFS JV7213, 7232); 546. Yalta, Foros, 2001, A. V. Yena (KHER 2889); Yalta, Hafellner, J. & Poelt, J. (1979) Die Arten der Gattung Oliva, 2009, J. 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Khodo- Joshi, Y., Upreti, D. K. & Sati, S. C. (2008) Three new sovtsev (KHER 1452). species of Caloplaca from India. Lichenologist 40: 535–541. We are grateful to Toby Spribille, Ulrik Søchting and Kantvilas, G. & McCarthy, P. M. (2003) Hueidea (Fus- Ulf Arup for their comments on this paper. Our re- cideaceae), a new lichen genus from alpine Australia. search received support from the Visegrad Fund (grants Lichenologist 35: 397–407. 51000067 and 51100753), the whole-Institute grant Katoh, K., Kuma, K., Toh, H. & Miyata, T. (2002) (AV0Z60050516) and the SYNTHESYS Project http:// MAFFT: a novel method for rapid multiple sequence 2012 Teloschistaceae without anthraquinones—Vondra´k et al. 417
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