fungal biology 120 (2016) 1341e1353
journal homepage: www.elsevier.com/locate/funbio
Arthonia parietinaria e A common but frequently misunderstood lichenicolous fungus on species of the Xanthoria parietina-group
Antonia FLEISCHHACKERa, Martin GRUBEa,*, Andreas FRISCHb, Walter OBERMAYERa, Josef HAFELLNERa aInstitut fur€ Pflanzenwissenschaften, NaWi Graz, Karl-Franzens-Universitat,€ Holteigasse 6, 8010 Graz, Austria bDepartment of Ecology, Swedish University of Agricultural Sciences, P.O. Box 7044, 750 07 Uppsala, Sweden article info abstract
Article history: Arthonia parietinaria is described as new to science. Host of the type and at the same time Received 31 December 2015 the only confirmed host species is the foliose macrolichen Xanthoria parietina. Sequence Received in revised form data of nucLSU rRNA genes reveal a close relationship to Arthonia molendoi. A. parietinaria 29 May 2016 is recorded for many countries in Europe, western Asia, and northern Africa. Accepted 6 June 2016 ª 2016 British Mycological Society. Published by Elsevier Ltd. All rights reserved.
Corresponding Editor: Ana Crespo
Keywords: Arthoniales Arthoniomycetes Ascomycetes Lichen parasites
Introduction includes 38 species, while the current version of an online- synopsis lists 115 species (Lawrey & Diederich 2015). In a pri- According to the traditional concepts, Arthonia Ach. (1806) rep- vate database we accumulated about 200 heterotypic names resents one of the large genera of ascomycetes, comprising that would be relevant in connection with a generic revision both lichenized and lichenicolous species. The number of ac- (J.H., unpubl.). And the process of inventory is still going on cepted species is given with 491 in the latest edition of the with additional species described almost every year. ‘Dictionary of the fungi’ (Kirk et al. 2008), which seems to be Due to high values of nitrogen deposition in European a rather conservative approximation. A search in MycoBank landscapes, the eutrophic conspicuous orange Xanthoria parie- (http://www.mycobank.org) reveals more than 1200 infrage- tina is one of the few foliose macrolichens with populations neric names linked to the genus. Also the proportion of lichen- increasing both in number and size since about the 1990s icolous taxa in Arthonia is remarkable. The somewhat out- (e.g. Frahm et al. 2009), whereas even common acidophytic dated, but still most comprehensive key for lichenicolous species like Hypogymnia physodes responded by decreasing Arthonia species at a world wide scale (Clauzade et al. 1989) thallus population numbers (e.g. Herk et al. 2003). As
* Corresponding author. E-mail address: [email protected] (M. Grube). http://dx.doi.org/10.1016/j.funbio.2016.06.009 1878-6146/ª 2016 British Mycological Society. Published by Elsevier Ltd. All rights reserved. 1342 A. Fleischhacker et al.
a consequence lichenicolous fungi confined to X. parietina as agarose gel stained with GelRed (Biotium, Hayward, Califor- their host face a situation with much more substrate available nia, USA) under UV light. PCR products were purified either us- for colonization. The fungus flora of decaying thalli of X. pari- ing the QIAquick PCR Purification Kit (Qiagen) or gel extracted etina has already been studied by Etayo & Berger (2009).Itis and purified using the QIAquick Gel Extraction Kit (Qiagen). dominated by anamorphic states of both ascomycetes and ba- Sequencing of the amplicons was provided by Uppsala Ge- sidiomycetes. In contrast, vital thalli are colonized by a differ- nome Centre (Sweden). The sequences were assembled in Bio- ent set of species. The entire fungal flora of X. parietina as Edit v.7.1.3 (Hall 1999) and their identity checked with the Blast single host species was studied in a project resulting in the search in GenBank and the local Blast functionality imple- master thesis for one of us (Fleischhacker 2011). mented in the BioEdit v.7.1.3 package. The nLSU sequences One of the fungi we frequently came across during this sur- were aligned in RNAsalsa (Stocsits et al. 2009) using the sec- vey was an Arthonia species, commonly determined as Artho- ondary structure of Saccharomyces cerevisiae (nLSU; Kjer 1995) nia molendoi (e.g., Santesson et al. 2004). However, a closer as template. The final alignment comprised 676 sites and the analysis revealed fine phenotypic differences, and here, we phylogeny was reconstructed with a Maximum Likelihood also confirm the distinctiveness of this lichenicolous fungus (ML) approach using RAxML (Stamatakis 2014) with raxmlGUI by molecular data. We therefore describe the species below interface (v.1.5, Silvestro & Michalak 2012). Myriostigma candi- as new to science and provide a discussion of apparently re- dum was used as outgroup lineage. A GTR þ GAMMA model lated species. was applied and 1000 bootstrap replicates were run. The phy- logenetic tree was visualized in FigTree v.1.4. In addition to the specimens cited below together with the Material and methods treatment of Arthonia parietinaria, the following material was compared: Methods for phenotype analyses
Arthonia anjutae S. Kondr. & Alstrup (on Teloschistes spinosus For the morpho-anatomical investigation air-dried herbarium (th.)) specimens have been analysed. External morphology was Note: Following ICN Art. 60.12, Note 4, the gender of the epi- e studied with a dissecting microscope (WILD M3, 6.4 40 ). An- thet with the original spelling ‘anjutii’ is corrected because atomical studies of the thallus and the ascomata were carried the epithet is derived from the female first name Anyuta. e out under the light microscope (LEICA DMRE, 100 1000 ). Sec- Australia: South Australia, Roopera station near Whyalla, tioning was performed with a freezing microtome (LEITZ, sec- eastern fence of Extension Paddock, 1969, R. Rogers, det. J. e m tions of 12 15 m) but squash preparations were also used, Hafellner (herb. Hafellner 19576). especially for ascus analysis. Preparations were mounted in water. When necessary, contrasting was performed by a pre- Arthonia clemens (Tul.)Th.Fr. (on Rhizoplaca chrysoleuca (ap.)) treatment with lactic acidecotton blue (MERCK 13741). Amy- Europe: Italy: Prov. Sondrio, Ortler Gruppe, Pian di Cembro € loid reactions in hymenia were observed both progressively uber dem Val di Cortena, an der Straße von San Pietro nach and regressively by the use of Lugol’s reagent (MERCK 9261). Trivigno, 1400e1450 m alt., 1975, H. Mayrhofer (herb. Hafellner Conidiogenesis of pycnoconidia was studied in erythrosin B 933 in GZU). e Asia: Russia: Siberia, Chukotka, on the upper (ALDRICH 19,826-9) in 10 % ammonia. Sections and squash reaches of the river Milkera, 1977, M. P. Andreev, det. J. Hafell- preparations were not pretreated with KOH unless otherwise ner (GZU). stated, namely for the detection of hemiamyloid reactions in Arthonia epiphyscia Nyl. the hymenium. Measurements refer to dimensions in tap wa- Hosts: Physcia caesia (th.) (1, T), Physcia dubia (th.) (2), Physcia ter. The terminology of pycnidial characters follows Vobis & phaea (th., ap.) (3). Hawksworth (1981). Europe: Austria: Burgenland, Sudburgenland,€ in Deutsch- Kaltenbrunn, ca. 265 m, GF 8962/2, (1), 1990, J. Hafellner 26075 Molecular analyses & W. Maurer (GZU). e Karnten€ (Carinthia), Nationalpark Hohe Tauern, Glockner-Gruppe, S Hange€ des Fuscherkar Kopfes, N Hymenia (about 20e50 50e100 mm in size) of four to five ober der Hofmannshutte€ [47 0501000N/12 4402000E], ca. 2500 m, ascomata of the lichenicolous species were carefully cut GF 8942/1, (3), 1988, J. Hafellner 32049, M. Walther, & A. Hafell- from the host tissue, placed in 1.5 ml microtubes using a ster- ner (GZU). e Steiermark (Styria), Niedere Tauern, Wolzer€ ilized forceps (Dupont Nr. 5), and used for a direct PCR ap- Tauern, Hochgroßen,€ nordostlicher€ Seitengipfel, im Gratber- proach (Grube 2005). Parts with either amorphous pigments eich [47 2705000N/14 1503500E], ca. 2050 m, GF 8551/2, (2), 1989, J. (incl. melanized portions) were removed from the cuttings Hafellner 26309 (GZU). e Norway:Oppland,Gem.V ag a, N- as far as possible as these pigments impair PCR efficiency. Ufer des Sees V ag avatn ca. 2 km W von V ag amo, ca. 450 m, PCR reactions of 20 ml (DNA extractions) and 30 ml (direct (2), 1984, J. Hafellner 11424 & A. Ochsenhofer (herb. Hafellner). PCR) were used. Each 10 ml of PCR mix contained 0.5e1 ml geno- Arthonia molendoi (Heufl. ex Frauenf.) R. Sant. (on Xanthoria mic DNA extraction (or the lichen sample), 0.4 ml of each elegans (th., ap.)) primer (20 pmol ml 1), and 5 ml HotStarTaq Plus Mastermix Europe: Austria:Karnten€ (Carinthia), Hohe Tauern, Kreuzeck- Kit (Qiagen). Primers LIC24R and LR7 were used for PCR ampli- Gruppe, Schwarzsteinwande€ (Sudw€ ande€ des Schwarzsteins) E fication of nuclear ribosomal large subunit RNA gene frag- der Hochtristen, N der Turgger Alm [46 4705500N/13 0901000E], ments (nLSU) (Vilgalys & Hester 1990; Miadlikowska & 1950e2150 m, GF 9244/2, 1978, J. Hafellner 3875 (GZU). e Lutzoni 2000). The PCR products were visualized in a 0.5 % A. parietinaria e A common but frequently misunderstood lichenicolous fungus 1343
Steiermark (Styria), Nordalpen (Nordliche€ Kalkalpen), ‘Ragnitzbach’ at lower end of Dr Hanischweg, 47 0403500N/ Ennstaler Alpen, Gesauseberge€ E von Admont, Gr. Buchstein, 15 2805000E, ca. 380 m s. m., GF 8958/2, old orchard, on canopy NW-Abhange,€ am W-Fuß der Abbruche€ der Admonter Frauen- branches of recently felled Juglans regia,onXanthoria parietina, mauer, 47 3605500N/14 3503000E, ca. 1720 m, GF 8353/4, 2005, J. 1 July 2010, J. Hafellner 77067 & W. Obermayer (GZU e holo- Hafellner 67595 & A. Hafellner (herb. Hafellner). e Liechten- type, BCN, BR, CANB, E, GZU, LE, M, NY, PRM, UPS e isotypes). stein: Eastern Alps, Ratikon,€ mountain ridge between Aug- Isotypes to be distributed in Hafellner, Lichenicolous Biota no. stenberg and Nospitz, SSW above the village Malbun, S adhuc ined. above Vaduzer Tali,€ 47 0502000N/09 3601500E, ca. 2060 m, 2008, Etymology: parietinarius 3 (Lat.), belonging to [Xanthoria] J. Hafellner 72834 (GZU). e Spain: Prov. Gerona, Pyrenaen,€ parietina. Nuria N von Ribas de Freser, NE von der Bergstation der Zahn- Iconography: Vezda 1970: 223, Fig 1 (drawings of asci, asco- radbahn, 2100e2200 m, 1983, J. Hafellner 17386 (GZU). e Africa: spores, and paraphysoids); Giralt 1996: 365, Fig 54 A (drawing Canary Islands: Tenerife, Las Canadas,~ Montana~ Guajara, auf of ascospores); this paper, Fig 1A (habit), Fig 2AeC (close ups der S-Seite knapp unter dem Gipfel, 28 1300000N/16 3604000W, of habit), Fig 3A and B (vertical sections of ascomata), Fig 4 ca. 2680 m, 1989, J. Hafellner 36202 & A. Hafellner (herb. (young stages of ascoma development), Fig 5A, B, D, E (asci), Hafellner). C (ascospores), F (vertical section of conidioma). Note: The concept of Arthonia molendoi applied here is consis- Description: Infection not gall-inducing, not causing severe tent with that of Santesson (1986) who has revised the holotype destruction of the thallus but sometimes slight discoloura- of its basionym Tichothecium molendoi preserved in W. tions can be observed. Vegetative hyphae intramatrical, in- conspicuous, K/Iþ blue, Cresyl-blueþ violet. Ascomata mat Arthonia sytnikii S. Kondr. black, dull, often with a slight brownish tinge, up to 0.25 mm Hosts: Xanthoria ligulata (1, T) (th.), Xanthoria sp. (2) (th.). in diam., arranged in groups of up to (10e)20e30(e50), convex, Africa: South Africa: Cape Province, 15 km SE of Oudtshoorn, immarginate, more or less roundish, distributed over the sur- by the road above Blossoms, (2), 1998, W. L. Culberson face of the host thallus including apothecial margins and hy- 22493a & R. Ornduff, det. J. Hafellner, separated from Kashi- menia. Exciple lacking. Hymenium pale greyish, with K/Iþ wadani, Lich. Minus Cogniti Exs. 200 (GZU). e Australasia: blue hymenial gel, 30e45 mm tall. Epihymenium dark brown New Zealand: North Island, Wellington, Manurewa Point W (due to the pigmented paraphysoidal tips) with a bluish tinge of Tora, S of Martinborough, 41 300S/175 320E, (1), 1992, H. (due to a slight pigmentation of the hymenial gel), Kþ Mayrhofer 13279 & E. Hierzer, det. J. Hafellner (GZU). chestnut-brown. Hypothecium pale brownish with some brown agglomerations, K/I , the hyphae directly underneath K/Iþ blue. Interascal filaments paraphysoidal, septate, Results branched, and anastomosed, 1e1.5 mm thick, with only slightly thickened terminal cells, apically about 2e5 mm thick, Molecular analyses with pigmented caps (‘Pigmentkappen’ in the sense of Kilias 1981). Asci of Arthonia-type, clavate, 8-spored, with hemiamy- In the nucLSU phylogeny (Fig 6) Arthonia parietinaria is posi- loid (K/Iþ blue) ring structure in the innermost layer of the tioned as sister species of Arthonia molendoi. The sequence of endoascus, dehiscence fissitunicate, 26e35(e37) (11e) the Swedish A. parietinaria sample is identical to sequences 12e15.5(e16.5) mm. Ascospores hyaline, K/I , 1-septate, upper of the three Austrian samples, and differs in few nucleotide cell somewhat broader, and mostly shorter, with thin hyaline positions. Both species belong to the well-supported Bryos- perispore (getting condensed and brownish with age; atten- tigma clade (Frisch et al. 2014), which comprises both liche- tion: perispore from deliberated spores easily squeezed off) nized as well as lichenicolous species. (9e)10e12(e13.5) (3e)4e5(e6) mm. Pycnidia subglobose to pyriform. Nonpigmented parts of the pycnidial wall K/Iþ Taxonomy blue. Conidiophores of type IeII (Vobis & Hawksworth 1981) producing ellipsoid pycnospores. Lichenicolous fungus grow- Arthonia parietinaria Hafellner & A. Fleischhacker, sp. nov. ing on Xanthoria parietina (and possibly also on other taxa of (Figs 1A, 2e5). the X. parietina-group). MycoBank No.: MB817180 Remarks: Arthonia parietinaria is not rare but in the past it has Species nova Arthoniae molendoi similis sed ab ea differt asco- not been recognized as a distinct species. Previous records of matibus plus aggregatis, in gregibus ad (10e)20e30(e50), triste A. parietinaria usually have been published under either the nigris haud atris et ascosporis aliquot minoribus, name A. molendoi (Fig 1B) or A. epiphyscia. Concerning the apo- 10e12 4e5 mm. Species aliae xanthoriicolae different aut in thecial characters, A. parietinaria is a hardly variable species. It chemia epithecii (A. destruens var. nana cum epithecio Kþ pur- differs from A. molendoi and A. epiphyscia in causing larger in- purascente), aut in numero ascomatum in quaque grege (in A. fection spots and also by the higher mean numbers of asco- molendoi apothecia in quaque grege solum 2e5), aut in reac- mata [(10e)20e30(e50)] per infection spot (1e5(e10) in A. tione hospitis contra infectionem (A. sytnikii cecidiogena), molendoi (1e)5e10 in A. epiphyscia). A. parietinaria can be distin- aut in colore ascosporarum (A. anjutae ascosporis fuscis). guished from A. molendoi by the less intense colouration (mat Infectio in hospite gregis Xanthoriae parietinae non cecidiogena black) of the ascomata (pure black in A. molendoi). The differ- solum thallum hospitis aliquot decolorans. ence in colour recalls that between dark morphs of Lecanora Type: Austria, Steiermark (Styria), Oststeirisches Hugelland,€ cenisia and Tephromela atra at high elevations. Remnants of Graz, eastern suburban area, Ragnitztal, near the rivulet 1344 A. Fleischhacker et al.
Fig 1 e Arthonia species on teloschistalean macrolichens. (A) Arthonia parietinaria on Xanthoria parietina (from holotype). (B) Arthonia molendoi on Xanthoria elegans (from Santesson, Fungi Lichenicoli Exs. 54 in GZU). (C) Arthonia sytnikii on Xanthoria ligulata (from Mayrhofer 13279). (D) Arthonia anjutae on Teloschistes spinosus (two views from Hafellner 19576). Bar [ 500 mm.
anthrachinones originating from the host may still be present The only taxon of still unclear relationship is an infraspecific in ascomata of all Arthonia species infesting Teloschistaceae. widely neglected one, Conida destruens f. maculans Rehm These remnants may cover partly the epihymenium (Fig 3B) Rabenh. Krypt. Fl. 1(3): 423 (1891). For the species Conida des- or may even be included in the ascomata. Therefore the reac- truens the ascospores are correctly described as becoming tion of ascoma sections namely the epihymenium with K is brownish and there is no indication that the ascospores of sometimes misleading. Differences between Arthonia parieti- the form maculans should differ in this respect. The only dif- naria, A. molendoi, and A. epiphyscia are summarized in Table 1. ference distinguishing it from the typical form should be the Several other Arthonia species are already known to grow on aggregated ascomata (.‘schwarze Punkte, welche manchmal foliose or fruticose Teloschistaceae, namely A. molendoi gehauft€ beisammenstehen’). A single collection, Arnold Lich. (Fig 1B), A. sytnikii (Fig 1C), A. anjutae (Fig 1D), and A. destruens Exs. no. 397, is cited, consequently constituting the type. How- var. nana Grube & Hafellner. All of them infest the thallus, and ever, Arnold, Lich. Exs. no. 397 is also listed among others as some of them also develop fruiting bodies on the apothecia exsiccate of Conida destruens [f. destruens]. Arnold, on the other (hymenia) of their hosts. Selected character states of these hand distributed no. 397 under the name Arthonia destruens taxa have been summarized in Table 2. var. maculans Rehm and the label data [Germany, Bavaria]: A. parietinaria e A common but frequently misunderstood lichenicolous fungus 1345
Fig 2 e Arthonia parietinaria on Xanthoria parietina. (A) Holotype in GZU. (B) Close up of ascomata on thallus (from isotype in CANB). (C) Close up of ascomata on thallus and young apothecium (Hafellner 77067 in GZU). (D) Close up of ascomata on apothecial margin and disc (from isotype in NY). Bar [ 200 mm.
Auf der Oberseite des Thallus der Ph.[yscia] parietina an Feld- Beside these arthonioid fungi the opegraphoid species Phaco- birnbaumen€ bei Sugenheim in Franken, Sommer 1868, leg. thecium varium (Tul.) Trevis (syn. Opegrapha physciaria (Nyl.) Rehm [label data from specimen in M published on the Inter- D. Hawksw. & Coppins) is occasionally found on Xanthoria. net: http://pictures.snsb.info/BSMlichfungicoll/web/M-0040/ That species was treated in detail by Hafellner (2009). Further- M-0040694_20031022_114338.jpg] as a nomen nudum. There- more, Arthonia-species can also colonize Caloplaca species fore we regard it as likely that the form constitutes a hetero- with noneffigurated thallus organization. This was recently typic synonym of Arthonia destruens var. nana Grube & shown with Arthonia insularis Kantvilas & Wedin, a species Hafellner, a taxon described from Nepal and growing there with ascospores becoming pale reddish brown and which upon Xanthomendoza fallax (compare Grube et al. 1995) but it causes severe infections on Caloplaca eos S. Kondr. & Karnefelt€ cannot be excluded with certainty that the taxon is identical in Australia (Kantvilas & Wedin 2015). with Arthonia parietinaria. Because of the confusing circum- Hosts: Xanthoria parietina (1, T) (thallus and apothecia). Fur- stances we decided not to consider whether the name could thermore the foliose Teloschistaceae Xanthoria parietina var. be used but to describe the taxon as new species founded on adpressa, X. mediterranea, X. lobulata, X. polycarpa, X. candelaria a recent rich collection. var. torulosa, and X. fallax are recorded in the literature (see 1346 A. Fleischhacker et al.
Habitats: Arthonia parietinaria is found together with its host li- chen in various habitats ranging from solitary trees in pas- tures, rows of trees along roads or creeks, fruit trees in orchards but also deciduous trees at the edge or in open for- ests. It is not rare and has been rather frequently reported in recent years. This might correlate with the permanently in- creasing occurrence of the host lichen due to nitrogen pollution. Distribution: Arthonia parietinaria is widely distributed. The species is so far with certainty known only from Europe, west- ern Asia, and northwestern Africa (Canary Islands). We saw only a few specimens from outside Europe, namely from Armenia and the Canary Islands. In Central Europe specimens have been seen from lower and medium altitudes. It is not un- likely that A. parietinaria can also be proven to be present in further continents as well because the host lichen is ex- tremely common and widely distributed in entire Europe and is also known from other parts of Asia, Africa, South America, and Australasia. A larger number of earlier records of an Arthonia upon Xan- thoria parietina that have been published under various names are likely to represent the species described here as new. Names used in these publications include Arthonia molendoi, A. epiphyscia, A. destruens, and A. clemens plus their homotypic synonyms namely in the genus Conida. The following distribution data, of which we think that e Fig 3 Arthonia parietinaria on Xanthoria parietina. (A) As- they refer to Arthonia parietinaria, are based on records from coma in longitudinal section upon apothecium of the host various Arthonia species always with Xanthoria parietina as re- (from isotype in NY). (B) Ascoma in longitudinal section ported host. For a compact presentation of the data we use the upon thallus of the host. Note the orange anthraquinone following abbreviations: Arthonia molendoi or A. aff. molendoi pigments originating from the host cortex still covering (A), A. molendoi p.p. or A. aff. molendoi p.p. (A#), A. epiphyscia partly the apothecial surface of the Arthonia ascoma to the or A. epiphyscia s. l. (B), A. epiphyscia p.p. (B#), A. clemens or Con- left (from isotype in CANB). Medium: tap water. Bar ida c. (C), Arthonia destruens or Conida d. (D), C. destruens f. mac- A [ 50 mm, B [ 20 mm. ulans (E), and Conida lecanorina (F). As we have screened thousands of thalli of Xanthoria parietina and could detect only the species described above we are fairly convinced that all these records refer to the same species. The abbrevia- geographic distribution). A considerable number of these re- tion p.p. means that the authors mentioned Xanthoria parietina cords would need a critical reevaluation also under in view as one of several hosts. Therefore we regard it as likely that of the recent knowledge about phylogenetic relationships the record refers to more than one lichenicolous taxa. Teloschistaceae. For some of these host taxa a transfer in Judging from the cited hosts the species is so far known other genera of Teloschistaceae has been proposed but the from the following European countries (records on Teloschis- taxonomy appears to not have yet settled. It cannot be ex- tales other than Xanthoria parietina uncertain): Austria (Berger cluded that further Arthonia species are hidden under these re- et al. 2015: 8 as (A), Keissler 1913: 386 as (F), 1930: 72 ff. as (C), cords with unusual hosts. Rehm 1891: 423 f. as (E)), Belgium (Ertz et al. 2008: 39 f. as (A), So far known, Arthonia parietinaria appears to be restricted to Santesson 2008: 10 as (A)), Denmark (Alstrup et al. 2013:57as the X. parietina group. X. parietina is by far the most common (A)), Estonia (Suija et al. 2010: 105 as (A)), France (Roux et al. host, but it cannot be excluded that the species will be 2014: 85 as (A#)), Germany (Rehm 1891: 423 f. as (E), Brackel detected also on X. aureola or X. calcicola in the future. An infec- 2010: 9 as (A), 2014: 30 ff. as (A#), Cezanne & Eichler 2015:56 tion with Arthonia parietinaria causes no significant destruc- as (A), Cezanne et al. 2008: 45 as (B), 2013: 189 as (A), John tion of the host tissue outside of the infection spots. The et al. 2011: 305 as (A), 2014: 1202 as (A), Triebel & Scholz 2001: hyphae, which according to their reactivity (K/I(Lugol)þ, 214 as (B)), Italy (Brackel 2011: 67 as (A#) including a record CrBþ) belong to the inhabiting fungus, occur in the plecten- on an additional host Caloplaca cerina, 2015: 224 as (A)), Lithua- chyma of the host as well as in the vicinity of living algal cells nia (Motiejunait e_ et al. 2011: 40 as (A)), Luxembourg (Cezanne of the host thallus. The behaviour of Arthonia parietinaria is & Eichler 2013: 276 as (A), 2014: 234 as (A), Van den Broeck therefore regarded as commensalic (or ‘parasymbiotic’). How- et al. 2013: 66 as (A)), the Netherlands (Brand et al. 2013:19as ever, larger groups of ascomata may cause slight discoloura- (A#)), Norway (Santesson 1993: 17 as (A#) with additional tions on the host thallus and the fungus could be considered host Xanthoria polycarpa), Poland (Czyzewska & Kukwa 2009: weakly parasitic as well. In summary, A. parietinaria is a nonli- 17 f. as (A#), Kukwa 2004: 67 as (A) with short description), Por- chenized, obligately lichenicolous, highly specialized species. tugal (Boom & Giralt 2012: 164 as (A)), Slovakia (Vezda 1970: 221 A. parietinaria e A common but frequently misunderstood lichenicolous fungus 1347
Fig 4 e Arthonia parietinaria on Xanthoria parietina. (A) Ascoma primordium developing in the hymenium of the host in longitudinal section. (B) Young ascoma in longitudinal section and vegetative hyphae penetrating the hymenium of the host (from isotype in NY). Medium tab water after treatment with Lactic acideCotton blue. Bar [ 20 mm.
as (B) with short description), Spain (Atienza et al. 2014 as (A), Exsiccata (all on Xanthoria parietina): Isotypes and duplicates of Boom & Etayo 2014: 46 f. as (A), Burgaz et al. 2007: 139 as (A), three paratypes will be distributed in Hafellner, Lichenicolous Calatayud et al. 1995: 369 as (A#), Etayo 2010: 36 ff. as (A#), Biota (for data and herbaria see below). e Santesson, Fungi Giralt 1996: 364 ff. as (B) with short description, Giralt & Lichenicoli Exs. no. 377, sub Arthonia molendoi (GZU). Gomez-Bolea 1988: 195 as (B), Mart ınez et al. 2002: 46 as (B), Further specimens examined (all on Xanthoria parietina): Serin~a et al. 2014: 39 as (B)), Sweden (Santesson 1993:17as Europe: Austria: Burgenland, Sudburgenland,€ Rauchwart, (A#) with additional host Xanthoria polycarpa), Switzerland Rauchwarter Berghauser€ ca. 6 km SE von Stegersbach, (Rehm 1891: 424 as Arthonia nephromiaria (this record remains 47 0701800N/16 1301700E, ca. 265 m, GF 8863/3, 2010, A. Fleisch- doubtful because Stizenberger 1882: 479 to which Rehm refers hacker 10010 & B. Fleischhacker (GZU). e Burgenland, to cites only Physcia stellaris as host under that name; other re- Sudburgenland,€ Urbersdorf, am Stausee, 47 0303600N/ cords of the species from Switzerland to which Rehm might 16 2200400E, 210 m, 2012, F. Berger 26201 (herb. Berger). e refer to we could not trace; however, the presence in Switzer- Karnten€ (Carinthia), Sattnitz, Sabuatach ca. 13 km ESE von Kla- land confirmed with records cited below)), Ukraine genfurt, ca. 700 m WSW des Gehofts€ Wlattnig, 46 3501900N/ (Kondratyuk & Khodosovtsev 1997: 589 as (C), as (D) with addi- 14 2705700E, ca. 580 m, GF 9452/2, 2011, F. Schlatti, det. A. Fleisch- tional host Xanthoria lobulata), the British Isles (Coppins 1992: hacker 11012 (GZU). e Karnten€ (Carinthia), Zentralalpen, 81 as (B#), Hawksworth 1975: 186 as (B#), Hitch 2010: 120 as Saualpe W von Wolfsberg, ca. 1 km W von St. Michael an der (A), 2012: 68 as (A), 2015: 62 as (A)). From Africa it is reported Straße nach Lading, 46 5000500N/14 4701000E, ca. 550 m, GF from Morocco (Werner 1932: 163 as (C), 1938: 134 as (C)) and 9154/4, 2010, J. Hafellner 76737 (BCN, BR, CANB, GZU, LE, NY, the Canary Islands (Boom & Clerc 2015: 1 sub (A#), Boom & UPS) (duplicates distributed in Hafellner, Lichenicolous Biota Ertz 2012: 73 sub (A#)). Asian reports exist for Israel no. adhuc ined.). e Niederosterreich€ (Lower Austria), Wiener- (Kondratyuk et al. 2005: 106 as (A#) including an additional wald, am sudwestlichen€ Stadtrand von Modling,€ am NE-Fuß host Xanthoria mediterranea). In Australasia it has been re- des Anninger-Massivs, 48 0403500N/16 1605000E, ca. 275 m, GF ported from New Zealand (Kondratyuk & Galloway 1994:26 7963/2, 2011, J. Hafellner 78980 (GZU). e Steiermark (Styria), as (B#) with additional host Xanthoria parietina var. adpressa) Nordliche€ Kalkalpen, Ennstaler Alpen, Radmer an der Hasel but the specific identity with the species we describe here ca. 9 km SW von Hieflau, S Hange€ N ober dem Schloß Greifen- should be rechecked. In America it might already be known berg, 47 3105000N/14 4204500E, ca. 940 m, GF 8454/3, 2006, J. Hafell- from Chile (Etayo & Sancho Garcia 2008: 46 as (A) on Xantho- ner 69282 (GZU). e Steiermark (Styria), Nordalpen, Nordliche€ mendoza fallax), and also the record by Werner (1937:64as Kalkalpen, Hochschwab-Gruppe, Seetal W von Seewiesen, ca. (C) on Xanthoria candelaria var. torulosa) from Spain should be 10 km NE von Aflenz, 47 3701500N/15 1502000E, ca. 930 m, GF confirmed by restudying the specimens, because the hosts be- 8357/4, 2007, J. Hafellner 69400 (GZU, herb. Hafellner). e Steier- longs to a different clades of xanthorioid lichenized fungi. mark (Styria), Steirisches Randgebirge, Fischbacher Alpen Based on specimens cited below the species is added to the [‘Oststeirisches Hugelland’€ ex errore], an der Straße von Birk- mycoflora of Croatia, Greece, Slovenia, and Armenia. feld nach Ratten, N der Abzweigung nach Strallegg, 1348 A. Fleischhacker et al.
Fig 5 e Arthonia parietinaria on Xanthoria parietina. (A) Young ascus (DIC, from holotype). (B) Mature asci (DIC, from holotype). (C) Ascospores (DIC, from holotype). (D) Two ascus tips with apical ring structure in the endoascus (from holotype). (E) Two asci, one semimature, one immature (from holotype). (F) Conidioma in longitudinal section (from holotype). Medium: A, B, C, F tap water; D, E I(Lugol) after pretreatment with K. Bar [ 10 mm.
47 2500500N/15 4104000E, ca. 645 m, GF 8560/3, 1989, J. Hafellner Loimeth ca. 8 km NW von Furstenfeld,€ 47 0605200N/16 0105600E, 22193 & A. Hafellner (GZU). e Steiermark (Styria), Steirisches ca. 335 m, GF 8862/3, 2010, A. Fleischhacker 10001 (GZU). e Randgebirge, Grazer Bergland, Bergrucken€ NE vom Steiermark (Styria), Oststeirisches Riedelland, 7 km NE of the Horgasgraben,€ ca. 2.8 km N von Stift Rein, beim SE Ende des centre of Graz, along the road from Stifting to Schaftal, close Kaschlsteiges, 47 0904000N/15 1702000E, ca. 620 m, GF 8857/2, to the junction to Schillingsdorf, 47 0600900N/15 3004200E, ca. 2013, J. Hafellner & A. Hafellner (GZU). e Steiermark (Styria): 435 m, GF 8859/3, 2010, W. Obermayer 11931 (BR, CANB, E, Steirisches Randgebirge, Grazer Bergland, Weizbach Graben, GZU, M, NY, UPS) (duplicates distributed in Hafellner, Lichenic- an der Straße vom Dorf Schmied in der Weiz auf den Sattel olous Biota no. adhuc ined.). e Steiermark (¼Styria), Oststeir- Brandlucken, ca. 0.8 km NE des Ghf. Granitzer, Waldstreifen isches Riedelland, 6.5 km E of the centre of Graz, 380 m SSE of zwischen Bach und Straße, 47 2001000N/15 3501500E, ca. 940 m, Eichenhof, 47 0404000N/015 3101200E, 440 m s. m., GF 8959/1, GF 8659/4, 2011, J. Hafellner 78997 (GZU). e Steiermark (Styria), mixed forest, on branches of trees lying on ground, 30 May Sausal, Kitzeck ca. 9 km W von Leibnitz, am NW Ortsrand, 2012, W. Obermayer 12467, det. J. Hafellner (GZU). e Belgium: 46 4703500N/15 2600000E, ca. 480 m, GF 9258/2, 2011, J. Hafellner De Panne, Westhoek, NE border of nature reserve. 51 050N/ 77054 (GZU). e Steiermark (Styria), Oststeirisches Hugelland,€ 02 340E. Grid: IFBL, C056, 2008, P. Diederich (n. A. parietinaria e A common but frequently misunderstood lichenicolous fungus 1349
Fig 6 e Phylogenetic position of Arthonia parietinaria (in bold) according to partial nucLSU rRNA gene sequences. Maximum likelihood tree, with bootstrap support values from 1000 replication above branches.
Table 1 e Selected character states of Arthonia parietinaria and the often confused Arthonia species (data for Arthonia destruens from Grube et al. 1995). A. parietinaria A. molendoi A. epiphyscia A. destruens (incl. var. nana)
Number of ascomata (10e)20e30(e50) 1e5(e10) (1e)5e10 2e10 per infection spot Colour of ascoma Dull black Pure black Pure black Dull black in surface view Colour of hymenium Pale greyish bluish Pale brownish Pale brownish Yellowish Pigmentation of epihymenium Dark brown with Blackish brown with Brown with Brownish with bluish tinge dark olive tinge dark olive tinge yellowish tinge Chemical reactions Kþ chestnut-brown K K Kþ purplish violet then of epihymenium dissolving Colour of hypothecium Brownish with some Pale yellowish to Olive brown Brown with yellowish tinge brown agglomerations medium brown Colour of ascospores Hyaline Hyaline Hyaline Soon brown, verrucose Size of ascospores 10e12 4e5 mm10e13 4e6 mm10e13 3.5e5 mm14e17 5e7 mm (v. destruens) 10.5e13 5e7 mm (v. nana)
16731) ¼ Santesson, Fungi Lichenicoli Exs. 377 (GZU). e Croatia: Hafellner 77194 (GZU). e Greece: Western Macedonia, Kozani Dalmatien, Insel Korcula, nahe der Stadt Korcula, 47 5702000N/ distr., Mt. Vourinon, on slopes exposed to the E, 1956, K. H. 17 0705500E, ca. 70 m, 2004, N. Cernic (herb. Hafellner 41734). e Rechinger, det. J. Hafellner (GZU). e Italy: Sardinien [Prov. France:Rhone-Alpes,^ Haute-Savoie, Western Alps, Bornes Nuoro], Gennarentu, Monte Tonneri, Funt na Pauli, Massif (Le Massif des Bornes), Burzier NW above Sallanches, 39 5403800N/9 2304200E, 650 m, 2011, F. Berger 25439 (herb. Berger) SE below the parking area at Route de Doran, 45 5702200N/ as admixture in specimen of Xanthoriicola physciae. e Liechten- 6 3604200E, ca. 935 m, 2011, J. Hafellner 82562 (GZU). e Germany: stein: Eastern Alps, Ratikon,€ W below the village Triesenberg by Bayern (Bavaria), Unterfranken, Kreis Kitzingen, Schwanberg- the road to Vaduz, 47 0604500N/09 3203000E, ca. 750 m, 2008, J. Sudhang€ SW Kirchberglein, ca. 300 m, MTB 6227/4, 2010, W. v. Hafellner 83053 (GZU). e Luxembourg: distr. Lorrain, Lorentz- Brackel 5307 (herb. Brackel). e Bayern (Bavaria), Allgau,€ Bayer- weiler, Roude Bam., alt. 225 m., IFBL: L8.46.31, UTM: KA.90, niederhofen NE vom Bannwaldsee, ca. 10 km NE von Fussen,€ 2010, P. Diederich 16909 (herb. Diederich). e distr. Lorrain, Entre am SE Ortsrand, 47 3702500N/10 4801500E, ca. 800 m, 2004, J. Dudelange et Kayl, Haardt, IFBL: M8.54.23, UTM: KV.88, 1350 A. Fleischhacker et al.
together with Xanthoriicola physciae, 2011, P. Diederich 17158 (herb. Diederich). e Slovenia: Central Alps, Kobansko, Koralpe, Bistrica (Feistritz) valley ca. 9 km NW of Muta (Hohenmauthen), nana close to the border to Austria, surroundings of former border v. m 0 00 m station on E (¼ orographically left) river bank, 46 39 15 N/ 7 0 00 e
5 15 07 10 E, ca. 460 m, 2008, J. Hafellner 77110 & L. Muggia
(GZU). e Southern Alps, Julian Alps, Cezsoca S of Bovec, SE
13 0 00 0 00
e above the village, 46 19 10 N/13 33 20 E, ca. 380 m, 2003, J. purplish violet 10 þ e
and own observations). Hafellner 77510 (BR, CANB, E, GZU, NY, PRM, UPS) (duplicates Soon brown, verrucose then dissolving Xanthoria fallax yellowish tinge distributed in Hafellner, Lichenicolous Biota no. adhuc ined.).
; e Switzerland: Kanton Bern, Berner Alps, by the road from Meiringen to Rosenlaui, S above Meiringen near the inn Zwirgi, 46 4204500N/08 1005500E, ca. 980 m, 2006, J. Hafellner 77458 (GZU). nodulosus e € f. Kanton Graubunden, Engadiner Alps, Sesvenna group, San
m 10.5 Nicla ca. 12 km NE of Scuol, N of the church close to the right Kondratyuk 1996 m 0 00 0 00 7 river bank of the Inn, 46 51 30 N/10 25 35 E, ca. 1080 m, 2006, e 5 J. Hafellner 77196 (GZU). e Asia: Armenia: Syunik province, road from Dilijan to Ijevan; SW of Ijevan along the river Agh- 15 or olive greenish K 20, fusing 2
e 0 00 0 00 e stev, 40 49 08 N/45 06 26 E, ca. 600 m, slopes along the road, finally dark brown Teloschistes spinosus Teloschistes velifer 2005, S. Harutyunyan 33-30b, det. J. Hafellner (GZU). e Africa: Canary Islands: El Hierro, Mirador de las Playas NE ober dem Ort Taibique, am Rand der SE-exponierten Abbruche,€ 27 440N/17 580W, ca. 1060 m, 1995, J. Hafellner 48238 (herb. Hafellner). ; m12 m 5 e spec. 3 10 5
e Discussion 13 or greenish K e Hyaline Pigmented in early stage, K Australasia, S. Africa, coastal Australasia Himalaya Brown with dark olive tinge Dark brown Brownish with Xanthoria ligulata Xanthoria As shown in the phylogenetic tree of a restricted set of related Arthonia species (14 taxa, Fig 6), Arthonia parietinaria apparently represents a sister species of Arthonia molendoi, both occurring group,
species on teloschistalean macrolichens (data from on members of Teloschistaceae as hosts. However, we are not sure that this will be confirmed when the study is based on a more representative set of lichenicolous arthonioid taxa. X. elegans group ;
Arthonia Judging from morpho-anatomy we would not be surprised m10
m when other lichenicolous Arthonia species are closer related 6
e to A. parietinaria than A. molendoi (e.g. Arthonia diploiciae Calat. 4
10) ca. 5 & Diederich, Arthonia peltigerina (Almq.) H. Olivier), but this is e and other 13
5( just a guess. e e Hyaline with thin perispore, slightly pigmented with age Pale yellowish to medium brown Hyaline Dark brown Brown with yellowish tinge Caloplaca saxicola Xanthoria elegans Bipolar, in the temperate zone at higher altitudes with dark olive tinge Arthonia molendoi was also included in a thorough phyloge- netic reconstruction of arthonioid fungi, both comprising liche- nized and nonlichenized species (Frisch et al. 2014). In the present analysis, A. molendoi forms a lineage together with lichenized Arthonia muscigena Th.Fr., a species to which Bryos- ; tigma leucodontis Poelt & Dobbeler€ is regarded to represent m10 Arthonia parietinaria 50) 1 m a younger heterotypic synonym (Sundin et al. 2012). As this e 5 group
e clade has a basal position to the majority of other arthonioid 4 30( e A. parietinaria A. molendoi A. sytnikii A. anjutae A. destruens fungi and is strongly supported in a Bayesian consensus tree )20 12 chestnut-brown K
e it was called ‘Bryostigma clade’. Judging from the sister position e þ slightly pigmented with age agglomerations (10 K X. parietina Xanthoria parietina the temperate zone at lower altitudes Dull blackDark brown with bluish tinge Blackish brown Pure blackof A. Pure black parietinaria and A. molendoi Pure blackin our phylogenetic Dull black reconstruc- tion we can expect that A. parietinaria, once included in a rean- alysis of a larger set of species, will also belong to the ‘Bryostigma clade’. However, due to the limited number of mo- lecular data for many other Arthonia species we still refrain Bryostigma Selected character states of from accepting taxonomically at the level of genus.
e The taxonomy of the group of hosts here in focus, the Telo- schistaceae, is strongly debated in recent years (e.g. Gaya et al. 2008, 2012; Arup et al., 2013; Kondratyuk et al. 2014). A consis- Size of ascospores 10 Colour of ascospores Hyaline with thin perispore, Colour of hypothecium Brownish with some brown Fungus gall inducingNumber of ascomata per infection spot NoReactions of epihymenium No Yes No No Table 2 Type host; further hosts Phytogeography Widespread in Holarctis, in Colour of ascoma in surface view Pigmentation of epihymenium tent taxonomic implementation of molecular data gained by A. parietinaria e A common but frequently misunderstood lichenicolous fungus 1351
various working groups is still not in sight, but questions about Berger F, Braun U, Heuchert B, 2015. Gonatophragmium lichenophi- the interrelationship of selected xanthorioid and caloplacoid lum sp. nov. e a new lichenicolous hyphomycete from Austria. e species groups can well be addressed with the published phy- Mycobiota 5:7 13. Boom and Clerc, 2015Boom PPG van den, Clerc P, 2015. Further logenetic trees. These relationships are relevant in connection new or interesting lichens and lichenicolous fungi from Gran Artho- € with the observed host spectra of selected lichenicolous Canaria (Canary Islands, Spain). Osterreichische Zeitschrift fur€ nia-species. Both A. parietinaria and A. molendoi have their hosts Pilzkunde 24:1e8. nesting in the Xanthorioideae-clade (Gaya et al. 2012). The Xan- Boom PPG van den, Ertz D, 2012. Lichens and lichenicolous fungi thoria parietina clade (including type host of A. parietinaria) has from El Hierro (Canary Islands), a survey, including five new e a more distant relationship to the Xanthoria elegans clade (in- species. Cryptogamie Mycologie 33:59 97. cluding type host of A. molendoi) than the latter to the lineage Boom PPG van den, Etayo J, 2014. New records of lichenicolous fungi and lichenicolous lichens from the Iberian Peninsula, comprising Caloplaca decipiens and Caloplaca arnoldii which in- with the description of four new species and one new genus. cludes the effigurate Caloplaca species that are often observed Opuscula Philolichenum 13:44e79. as additional hosts of A. molendoi. Thus, the lichenicolous fun- Boom PPG van den, Giralt M, 2012. Checklist and three new spe- gus taxonomy reflects ‘cum grano salis’ the taxonomy of the cies of lichens and lichenicolous fungi of the Algarve (Portu- host species, an often observed phenomenon in parasitic fungi gal). Sydowia 64: 149e208. (see e.g. Savile 1979; Hijwegen 1979). Brackel W von, 2010. Weitere Funde von flechtenbewohnenden Pilzen in Bayern e Beitrag zu einer Checkliste V. Berichte der The anamorph briefly described above clearly belongs to A. Bayerischen Botanischen Gesellschaft 80:5e32. parietinaria and is the state that produces the microconidia Brackel W von, 2011. Lichenicolous fungi and lichens from Puglia (spermatia) for the fertilization of ascogons. As we saw them and Basilicata (southern Italy). Herzogia 24:65e101. only tightly attached to or in between ascomata we do not ex- Brackel, 2014Brackel W von, 2014. Kommentierter Katalog der pect that they can appear also alone and outside of infection flechtenbewohnenden Pilze Bayerns. Bibliotheca Lichenologica spots of A. parietinaria and in greater distance to its ascomata. 109:1e476. Formally the pycnidia are Phoma-like except that they are Brackel W von, 2015. Lichenicolous fungi from central Italy with notes on some remarkable hepaticolous, algicolous and li- smaller and that they produce conidia distinctly smaller chenized fungi. Herzogia 28: 212e281. than what is regarded to represent vegetative diaspores. Brand AM, Sparrius LB, Aptroot A, 2013. Nieuwe soorten korst- Two Phoma-like fungi are known to grow on X. parietina, both mossen en lichenicole fungi voor Nederland. Buxbaumiella 97: with distinctly larger conidia and both now classified in Didy- 17e22. mocyrtis (Ertz et al. 2015). One constitutes an anamorphic state Burgaz AR, Arguello A, Atienza V, Fernandez-Brime S, Fernandez- of the Didymocyrtis slaptoniensis (D. Hawksw.) Hafellner & Ertz, Salegui AB, Figueras-Balague G, Garcıa Otalora M, Gomez- an ascomycete obviously restricted to X. parietina, the other Bolea A, Hawksworth DL, Hladun N, Llimona X, Llop E, Mar- cos-Laso B, Muniz~ D, Perez-Llamazares A, Paz-Bermudez G, with a broader host spectrum was named Didymocyrtis epiphy- Perez-Ortega S, Del Prado R, Rodrigues SA, Terron A, 2007. Li- scia Ertz & Diederich and is only known in its anamorphic chens and lichenicolous fungi of Sierra de San Lorenzo (La state. Rioja Community, Spain). Cryptogamie Mycologie 28: 133e153. Calatayud V, Atienza V, Barreno E, 1995. Lichenicolous fungi from the Iberian Peninsula and the Canary Islands 1. Mycotaxon 55: 363e382. Acknowledgements Cezanne R, Eichler M, 2013. Die Flechten (Lichenes) des Natur- waldreservates “Grouf” (2011). In: Murat D (ed.), Grouf. Zoo- logische und botanische Untersuchungen 2007e2011. We thank F. Berger, W. v. Brackel, and P. Diederich for loan of Naturwaldreservate in Luxemburg, vol. 10. Naturverwaltung, specimens. We are also grateful to M. Pinter, F. Schlatti, N. Luxemburg, pp. 244e281. Cernic who provided substantial collections of Xanthoria pari- Cezanne R, Eichler M, 2014. Flechtenkundliche Erhebungen im etina to screen for the presence of lichenicolous fungi. AF Naturwaldreservat “Haard” (2012). In: Murat D (ed.), Haard. e thanks the Austrian Science Foundation for financial support Zoologische und botanische Untersuchungen 2011 2013. Natur- waldreservate in Luxemburg, vol. 12. Naturverwaltung, Luxem- (FWF P24114). burg, pp. 186e243. Cezanne R, Eichler M, 2015. Verbreitungsatlas der Flechten von references Darmstadt e einschließlich flechtenbewohnender Pilze. Bota- nik und Naturschutz in Hessen, Beiheft 12:1e239. Cezanne R, Eichler M, Hohmann ML, Wirth V, 2008. Die Flechten des Odenwaldes. Andrias 17:1e520. Alstrup V, Søchting U, Dragsholt C, Læssøe T, Thell A, Kukwa M, Cezanne R, Eichler M, Teuber D, 2013. Erganzungen€ zur Liste der 2013. Additions to the lichens and lichenicolous fungi of Flechten und flechtenbewohnenden Pilze Hessens e 4. Folge. Denmark 8. Graphis Scripta 25:56e63. Botanik und Naturschutz in Hessen 26: 181e196. € Arup U, Søchting U, Froden P, 2013. A new taxonomy of the family Clauzade G, Diederich P, Roux C, 1989. Nelikenigintaj fungoj lik- Teloschistaceae. Nordic Journal of Botany 31:16e83. enlogaj. Ilustrita determinlibro. Bulletin de la Soci et e Linn eenne Atienza V, Araujo E, Arroyo MR, Burgaz AR, Figueras G, Gomez- de Provence, Num ero Sp ecial 1:1e142. Bolea A, Hladun NL, Llimona X, Llop E, Lopez de Silanes ME, Coppins BJ, 1992. Arthonia Ach. (1806). In: Purvis OW, Coppins BJ, ~ Marcos B, Perez-Vargas I, Pino-Bodas R, Serina E, Rico VJ, 2014. Hawksworth DL, James PW, Moore DM (eds), The Lichen Flora of € Lichenized and lichenicolous fungi from the Pitiuses Archi- Great Britain and Ireland. Natural History Museum Publications, pelago (Eivissa and Formentera Islands and Islets), Balearic London, pp. 74e88. Islands, Spain. Mycotaxon 126: 247e248 þ suppl. file URL: http: Czyzewska K, Kukwa M, 2009. Lichenicolous Fungi of Poland. A //www.mycotaxon.com/resources/checklists/atienzasesli- Catalogue and Key to Species. (Grzyby naporostowe Polski. v126-checklist.pdf 1352 A. Fleischhacker et al.
Katalog i klucz do gatunkow). In: Biodiversity of Poland, vol. 11. Hijwegen T, 1979. Fungi as plant taxonomists. Symbolae Botanicae W. Szafer Institute of Botany, Polish Academy of Sciences, Upsaliensis 22: 146e165. Krakow, p. 133. Hitch C (ed.), 2010. New, Rare and Interesting Lichens. British Li- Ertz D, Diederich P, Brand AM, Boom P van den, Serusiaux E, 2008. chen Society Bulletin 107: 118e131. New or interesting lichens and lichenicolous fungi from Bel- Hitch C (ed.), 2012. New, Rare and Interesting Lichens. British Li- gium, Luxembourg and northern France. XI. Bulletin de la chen Society Bulletin 110:63e84. Soci et e des Naturalistes Luxembourgeois 109:35e51. Hitch C (ed.), 2015. New, Rare and Interesting Lichens. British Li- Ertz D, Diederich P, Lawrey JD, Berger F, Freebury CE, Coppins B, chen Society Bulletin 116:59e73. Gardiennet A, Hafellner J, 2015. Phylogenetic insights resolve John et al., 2011John V, Bruyn U de, Dolnik C, Schumm F, Spier L, Dacampiaceae (Pleosporales) as polyphyletic: Didymocyrtis Stapper NJ, Brackel W von, 2011. Flechten und flechenbe- (Pleosporales, Phaeosphaeriaceae) with Phoma-like ana- wohnende Pilze im Pfalzerwald€ (BLAM-Exkursion 2010). Her- morphs resurrected and segregated from Polycoccum (Trype- zogia 24:297e313. theliales, Polycoccaceae fam. nov.). Fungal Diversity 74:53e89. John V, Cezanne R, Eichler M, Zimmermann DG, 2014. Neue und http://dx.doi.org/10.1007/s13225-015-0345-6 published online bemerkenswerte Funde von Flechten und flechtenbewoh- 11 Sep. 2015. nenden Pilzen aus Rheinland Pfalz (Sudwest-Deutschland).€ Etayo J, 2010. L ıquenes y hongos liquen ıcolas de Aragon. Guineana Fauna und Flora in Rheinland-Pfalz 12: 1189e1220. 16:1e501. Kantvilas G, Wedin M, 2015. Lichenicolous species of the asco- Etayo J, Berger F, 2009. About a fast developing community of li- mycete genus Arthonia Ach. from Kangaroo Island. Journal of chenicolous deuteromycetes decaying Xanthoria parietina. the Adelaide Botanic Gardens 29:1e6. € € Osterreichische Zeitschrift fur€ Pilzkunde 18: 111e115. Keissler K von, 1913. Uber einige Flechtenparasiten aus Steier- Etayo J, Sancho Garcia L, 2008. Hongos liquen ıcolas del Sur de mark. Centralblatt fur€ Bakteriologie und Parasitenkunde, 2. Abtei- Sudamerica, especialmente de Isla Navarino (Chile). Bibliotheca lung 37: 384e392. Lichenologica 98:1e302. Keissler K von, 1930. Die Flechtenparasiten. In: Dr. L. Rabenhorst’s € Fleischhacker A, 2011. The Lichenicolous Fungi Invading Xanthoria Kryptogamen-Flora von Deutschland, Osterreich und der Schweiz,2. parietina (Magisterarbeit, unpublished). Naturwissenschaft- Aufl., vol. 8, Akademische Verlagsgesellschaft, Leipzig, liche Fakultat€ der Karl-Franzens-Universitat€ Graz, Graz. pp. IeXI 1e712. Frahm et al., 2009Frahm JP, Janssen AM, Schumacher J, Kilias H, 1981. Revision gesteinsbewohnender Sippen der Flech- Thonnes€ D, Hensel S, Heidelbach B, Erler D, 2009. Das Nitro- tengattung Catillaria Massal. in Europa. Herzogia 5: 209e448. phytenproblem bei epiphytischen Flechten e eine Synthese. Kirk PM, Cannon PF, Minter DW, Stalpers JA (eds), 2008. Ainsworth The nitrogen problem of epiphytic lichens e a synthesis. Ar- & Bisby’s Dictionary of the Fungi, 10th edn. CAB International, chive for Lichenology 5:1e8. Wallingford, p. 771. Frisch A, Thor G, Ertz D, Grube M, 2014. The Arthonialean chal- Kjer KM, 1995. Use of ribosomal-RNA secondary structure in lenge: restructuring Arthoniaceae. Taxon 63: 727e744. phylogenetic studies to identify homologous positions e an Gaya E, Navarro-Rosines P, Llimona X, Hladun N, Lutzoni F, 2008. example of alignment and data presentation from the frogs. Phylogenetic reassessment of the Teloschistaceae (lichen- Molecular Phylogenetics and Evolution 4: 314e330. forming Ascomycota, Lecanoromycetes). Mycological Research 112: Kondratyuk SY, 1996. Four new species of lichenicolous fungi. 528e546. In: Wasser SP (ed.), Botany and Mycology for the Next Millen- Gaya E, Hognabba€ F, Holguin A, Molnar K, Fernandez-Brime S, nium: collection of scientific articles devoted to the 70th anniver- Stenroos S, Arup U, Sochting€ U, Boom P van den, Lucking€ R, sary of academician K. M. Sytnik.N.G.KholodnyInstituteof Sipman HJM, Lutzoni F, 2012. Implementing a cumulative Botany, National Academy of Sciences of Ukraine, Kiev, supermatrix approach for a comprehensive phylogenetic pp. 309e315. study of the Teloschistales (Pezizomycotina, Ascomycota). Kondratyuk SY, Galloway DJ, 1994. Additional lichen records from Molecular Phylogenetics and Evolution 63: 374e387. New Zealand. 10. Australasian Lichenological Newsletter 34: Giralt M, 1996. L ıquens ep ıfits i contaminacio atmosf erica a la plana i 25e29. les serralades litorals tarragonines. Institut d’Estudis Catalans, Kondratyuk SY, Khodosovtsev AY, 1997. Novi dlja mikobioty Uk- SecciodeCi encies Biologiques, Barcelona, p. 525. rainy vydy lichenofilnich hrybiv. (The new for Ukraine species Giralt M, Gomez-Bolea A, 1988. Alguns fongs liquen ıcoles trobats of lichenicolous fungi). Ukrayinskyj Botanicnyj Zhurnal 54: sobre l ıquens ep ıfits de Catalunya. Actes del Simposi Internacio- 588e590. nal de Botanica Pius Font i Quer 1: 195e203. Kondratyuk S, Nevo E, Wasser S, 2005. New and rare lichen- Grube, 2005Grube M, 2005. Nucleic acid isolation from ecological forming and lichenicolous fungi from the Carmel Mountains, samples e fungal associations, lichens. Methods in Enzymology Israel. Ukrayinskyj Botanicnyj Zhurnal 62: 100e110. 395:48e57. Kondratyuk SY, Karnefelt€ I, Thell A, Elix JA, Kim J, Jeong MH, Grube M, Matzer M, Hafellner J, 1995. A preliminary account of the Yu NN, Kondratiuk AS, Hur JS, 2014. A revised taxonomy for lichenicolous Arthonia species with reddish, Kþ reactive pig- the subfamily Xanthorioideae (Teloschistaceae, Ascomycota) ments. The Lichenologist 27:25e42. based on molecular phylogeny. Acta Botanica Hungarica 56: Hafellner J, 2009. Phacothecium resurrected and the new genus 141e178. Phacographa (Arthoniales) proposed. In: Thell A, Seaward MRD, Kukwa M, 2004. New or interesting records of lichenicolous fungi Feuerer T (eds), Diversity of Lichenology e Jubilee Volume. Biblio- from Poland II. Species mainly from northern Poland. Herzogia theca Lichenologica, vol. 100, pp. 85e121. 17:67e75. Hall TA, 1999. BioEdit: a user friendly biological sequence align- Lawrey JD, Diederich P, 2015. Lichenicolous fungi e worldwide ment editor and analysis program for windows 95/98/NT. checklist, including isolated cultures and sequences available Nucleic Acids Symposium Series 41:95e98. URL: http://www.lichenicolous.net [5/29/2016] Hawksworth DL, 1975. Notes on British lichenicolous fungi, I. Kew Mart ınez I, Aragon G, Burgaz AR, 2002. Epiphytic lichens and li- Bulletin 30: 183e203. chenicolous fungi from the “Serran ıa de Cuenca” mountains Herk CM van, Mathijssen-Spiekman EAM, Zwart D de, 2003. Long (“Sistema Iberico”, Spain). Herzogia 15:37e49. distance nitrogen air pollution effects on lichens in Europe. Miadlikowska J, Lutzoni F, 2000. Phylogenetic revision of the ge- The Lichenologist 35: 347e359. nus Peltigera (lichen-forming ascomycetes) based on A. parietinaria e A common but frequently misunderstood lichenicolous fungus 1353
morphological, chemical and large subunit nuclear ribosomal Stizenberger E, 1882. Lichenes helvetici eorumque stationes et DNA data. International Journal of Plant Sciences 161: 925e958. distributio [part one]. Bericht uber€ die Thatigkeit€ der St. Gallischen Motiejunait e_ J, Brackel W von, Stoncius D, Preikða þ, 2011. Con- Naturwissenschaftlichen Gesellschaft wahrend€ des Vereinsjahres tribution to the Lithuanian flora of lichens and allied fungi. III. 1880e81: 255e522. Botanica Lithuanica 17:39e47. Stocsits RR, Letsch H, Hertel J, Misof B, Stadler PF, 2009. Accurate Rehm H, 1891. Ascomyceten: Hysteriaceen und Discomyceten. In: and efficient reconstruction of deep phylogenies from struc- € Dr. L. Rabenhorst’s Kryptogamen-Flora von Deutschland, Osterreich tured RNAs. Nucleic Acids Research 37: 6184e6193. und der Schweiz, 2. Aufl, vol. 1, E. Kummer, Leipzig, pp. 401e444 Suija A, Piin-Aaspollu~ T, Ahti T, Marmor L, Juriado€ I, Kannukene L, Lieferung 34. Lohmus~ P, 2010. New Estonian records. Lichens and lichenic- Roux C, Monnat JY, Van Haluwyn C, Chipon B, Poumarat S, olous fungi. Folia Cryptogamica Estonica 47: 105e107. Houmeau JM, Diederich P, Masson D, Carlier G, Bertrand M, Sundin R, Thor G, Frisch A, 2012. A literature review of Arthonia s. Boissiere JC, Bauvet C, Lagrandie J, Bricaud O, Gardiennet A, lat. In: Karnefelt€ I, Seaward MRD, Thell A (eds), Systematics, Derrien MC, Menard T, Farou JL, Blondel E, Guilloux F, Biodiversity and Ecology of Lichens. Bibliotheca Lichenologica, vol. Lorella B, Navarro-Rosines P, Esnault J, Gueidan C, Boissier X, 108, pp. 257e290. Agnello G, Franchon C, Offerhaus B, Sussey JM, Asta J, Triebel D, Scholz P, 2001. Lichenicolous fungi from Bavaria as Masse LJC, Lohezic-Le Dev ehat F, Davoust M, Quelen Y, represented in the Botanische Staatssammlung Munchen.€ Gonnet D, Gonnet O, Ferrez Y, Martin B, Martin JL, VaudoreD, Sendtnera 7: 211e231. Ragot R, Boumier R, Remy C, Wirth V, Dufrene^ P, Engler R, Van den Broeck D, Diederich P, Ertz D, 2013. Report on two li- Lacoux D, Schmitt A, Clerc P, Mary FJ, Mary J, Vermeulen JC, chenological field meetings in Luxembourg in 2011 and 2012. Montavont JP, Gaveriaux JP, Demeulant J, Beguinot J, Vallade J, Bulletin de la Soci et e des Naturalistes Luxembourgeois 114:65e76. Chapuis L, Hugueny P, Lerat C, Maggi F, Baubet R, Drouard F, Vezda A, 1970. Pr ıspevek k poznan ı lichenikolnich hub v Cesko- Serusiaux E, Deschatres^ R, Hairie F, 2014. Catalogue des lichens slovensku III. Beitrag zur Kenntniss der flechtenbewohnenden et champignons lich enicoles de France m etropolitaine. Editions Pilze aus der Tschechoslowakei III. Ceska Mykologie 24: d’art, Henry des Abbayes, Fougeres, p. 1525. 220e229. Santesson R, 1986. Fungi lichenicoli exsiccati. Fascicles 3 & 4 (Nos Vilgalys R, Hester M, 1990. Rapid genetic identification and map- 51e100). Thunbergia 3:1e18. ping of enzymatically amplified ribosomal DNA from several Santesson R, 2008. Fungi lichenicoli exsiccati. Fascicles 15 & 16 Cryptococcus species. Journal of Bacteriology 172: 4238e4246. (Nos 351e400) (Corrections. Index.). Thunbergia 36:1e28. Vobis G, Hawksworth DL, 1981. Conidial lichen-forming fungi. In: Santesson R, 1993. The Lichens and Lichenicolous Fungi of Sweden and Cole GT, Kendrick WB (eds), Biology of Conidial Fungi, vol. 1. Norway. SBT-forlaget,€ Lund, p. 240. Academic Press, New York, London & San Francisco, Santesson R, Moberg R, Nordin A, Tønsberg T, Vitikainen O, 2004. pp. 245e273. Lichen-forming and Lichenicolous Fungi of Fennoscandia. Museum Werner RG, 1932. Contribution a la flore cryptogamique du Maroc. of Evolution, Uppsala University, Uppsala, p. 359. Fascicule VI. Bulletin de la Soci et e des Sciences Naturelles du Maroc Savile DBO, 1979. Fungi as aids in higher plant classification. Bo- 12: 156e163. tanical Review 45: 377e503. Werner RG, 1937. Recherches phytogeographiques comparees sur Serin~a E, Arroyo R, Araujo E, Burgaz AR, Atienza V, Fernandez- la flore cryptogamique de l’Espagne meridionale et du Maroc. Brime S, Rico VJ, Llimona X, Llop E, Lopez de Silanes ME, Bulletin de la Soci et e des Sciences Naturelles du Maroc 17:32e66. Marcos-Laso B, Marques J, Merinero S, Perez-Ortega S, Rubio- Werner RG, 1938. Contribution a la flore cryptogamique du Maroc. Salcedo M, Vivas M, 2014. Hongos liquenizados y liquen ıcolas Fascicule XVII (Algae, Lichenes et Fungi). Bulletin de la Soci et e de la Sierra de Albarrac ın (Teruel, Espana).~ Botanica Complu- des Sciences Naturelles du Maroc 18: 126e136. tensis 38:35e52. Silvestro D, Michalak I, 2012. raxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution 12: 335e337. software Stamatakis A, 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics FigTree URL: http://tree.bio.ed.ac.uk/software/figtree/ 30: 1312e1313.