The Lichenologist 46(1): 51–67 (2014) 6 British Society, 2014 doi:10.1017/S0024282913000649

Notoparmelia, a new of () based on overlooked reproductive anatomical features, phylogeny and distribution pattern

Zuzana FERENCOVA, Paloma CUBAS, Pradeep Kumar DIVAKAR, M. Carmen MOLINA and Ana CRESPO

Abstract: The importance of the anatomy and fine morphology of reproductive structures for the systematics of the family Parmeliaceae is highlighted by the new genus Notoparmelia, described here for Australasian species of . These species were known to form a monophyletic lineage but correlated characters for its delimitation were lacking. A major characteristic used here for the circum- scription of this genus is the overlooked apothecial anatomy. The proper exciple is reduced to one layer formed exclusively by large hyphae without any clear branching pattern and embedded in an abundant polysaccharide matrix. This feature differs from the rest of Parmeliaceae which have a strati- fied three-layered proper exciple composed of a thin hyaline layer, intermediate layer and basal cor- tex-like structure. The anatomy of proper exciple, together with the thickness of spore walls and other morphological characters such as lobe morphology, pseudocyphellae and rhizine type, allow a precise diagnosis of the new genus. The area of distribution is also useful for characterizing this genus. Sixteen new combinations are proposed. Key words: Australasia, , proper exciple, spore wall, taxonomic characters Accepted for publication 5 August 2013

Introduction et al. 2006; Amo de Paz et al. 2010; Crespo et al. 2010b). Phylogenetic studies showed For many years, the delimitation of genera in that some genera, circumscribed on the basis the lichenized fungi was based on morpho- of a few morphological and/or chemical logical, anatomical and chemical characters, characters, were polyphyletic and that some and in the last three decades a number of of the smaller monophyletic groups tended genera were described in Parmeliaceae using to have distinct distribution patterns (Crespo these features (e.g. Hale 1974a, b, 1976, et al. 2010a, b; Divakar et al. 2010). These 1984, 1986a, b; Culberson & Culberson studies also revealed examples of previously 1981; Krog 1982; Elix et al. 1986; Elix & undetected morphological characters of phy- Hale 1987; Henssen 1991, 1992; Kurokawa logenetic or taxonomic significance (del 1991; Elix 1993a). However, more recently Prado et al. 2007; Crespo et al. 2010a, b), or the delimitation of these genera has been re- allowed segregation of new genera using both evaluated based mainly on molecular phy- molecular and morphological data (Blanco et logenies (e.g. Blanco et al. 2004a, b, 2005; al. 2004b). Divakar et al. 2006; Thell et al. 2006; Wirtz Parmelia was described by Acharius (1803) in a very broad sense, encompassing a large Z. Ferencova, P. Cubas, P. K. Divakar and A. Crespo number of foliose lichens with lecanorine (corresponding author): Departamento de Biologı´a apothecia, including such diverse genera as Vegetal II, Facultad de Farmacia, Universidad Com- plutense de Madrid, E-28040 Madrid, Spain. Cetraria, Lobaria, Parmelia s. lat., Physcia, Email: [email protected] and Xanthoria. By the end of the 19th cen- M. C. Molina: Departamento de Biologı´a y Geologı´a, tury, Parmelia began to assume its modern ESCET, Universidad Rey Juan Carlos, Mo´stoles, circumscription, being described as a foliose E-28933 Madrid, Spain. 52 THE LICHENOLOGIST Vol. 46 rhizinate genus with laminal apothecia and tenuirima, P. cunninghamii and P. signifera) simple spores (Fries 1861). The controver- forms a well-supported (clade B) but sial history of Parmelia with segregation into no distinct morphological characteristics new genera, followed by synonymization of were found. A monophyletic clade C, com- some of them, is discussed in Hale (1987) posed of the genera Relicina and Relicinopsis, and Crespo et al. (2011). Hale (1987) in- is sister group of the Australasian species of cluded in Parmelia s. str. a small assemblage clade B, although with very low statistical of 38 species, typified by P. saxatilis, and 12 support. The third group of Parmelia (clade new species were later added (Elix 1993b, D) contains mostly temperate species (P. 2007; Kurokawa 1994; Elix & Kantvilas saxatilis, P. discordans, P. serrana, P. sulcata 1995; Calvelo & Adler 1999; Feuerer & and P. squarrosa), with a centre of distribu- Thell 2002; Divakar et al. 2003, 2005; tion in the Northern Hemisphere (Crespo et Molina et al. 2004, 2011a, b). In its present al. 2010b). delimitation, Parmelia is a widespread genus In a general survey of the morphology and with three centres of diversification (Hale anatomy of the reproductive structures in 1987), one in boreal-temperate Europe and Parmeliaceae, Ferencova (2012) found greater North America, a second one in eastern Asia variability than expected, and promising fea- and the third one in Australasia. tures that could help in the morphological Parmelia belongs to the major ‘parmelioid’ characterization of the genera. Five types of clade within the large and widely distributed , based on their size and form family Parmeliaceae. Parmelioid lichens can together with the thickness of their spore be distinguished by their mainly foliose thalli wall, were established for parmelioid lichens: (rarely subcrustose, subfruticose, peltate and type I, small ascospores (50–100 mm long) umbilicate), the rhizinate lower surface, lam- with a thin spore wall (<600 nm); type II, inal cupulate apothecia, Lecanora-type asci, medium-sized ascospores (100–150 mm and simple ellipsoid hyaline ascospores long) with a thin to medium spore wall (Blanco et al. 2006; Crespo et al. 2007, (<10 mm); type III, medium to large asco- 2010b). The Parmelia species are charac- spores (100–200 mm long) with a thick terized by adnate, sublinear to subirregular spore wall (10–20 mm); type IV, very large lobes without cilia; an upper surface with ascospores (>200 mm long) with a very effigurate pseudocyphellae, lower surface thick spore wall (>2 mm); and type V, large black, rhizinate (rhizines simple, furcate or to very large ascospores (>150 mm long) squarrosely branched); 8 simple spores per with a thin to medium spore wall (<10 ascus; conidia cylindrical or weakly bifusi- mm). In addition, different types of internal form, less than 80 mm long; with atranorin organization of the apothecium were found and chloratranorin in the cortex (Hale 1987). and described, differing mainly in the anat- In a comprehensive molecular study based omy of the proper exciple. on a multi-locus dataset of parmelioid lichens The present study aims to find good diag- (Crespo et al. 2010b), the genus Parmelia was nostic morphological and anatomical char- shown to split into three separate : acters to circumscribe the monophyletic lin- A, B and D (Fig. 1). The first of these, the eage of Australasian species (clade B) found Nipponoparmelia clade (clade A), contains in the assemblage of Parmelia, with special East Asian species (Nipponoparmelia laevior emphasis on ascomata anatomy and asco- and N. ricasolioides) that differ morphologi- spore type. cally from other Parmelia species by having small punctate pseudocyphellae on the lobe Materials and Methods edges. This group of species, previously organized by Kurokawa (1994) in the small Taxon sampling subgenus Nipponoparmelia, was elevated to In the present study, we investigated 23 fertile speci- generic rank (Crespo et al. 2010b). A second mens from the Parmelia and Nipponoparmelia clades group of predominantly Australasian species (Crespo et al. 2010b). The sampling included two Nip- (Parmelia subtestacea, P. crambidiocarpa, P. ponoparmelia species (N. laevior and N. ricasolioides) that 2014 Notoparmelia—Ferencova et al. 53

Table 1. Fertile specimens used in this study, with their location and collection details.

Species Voucher specimens Locality Collector (s)

Nipponoparmelia laevior MAF-Lich 7278 Japan, Hokkaido H. Harada N. ricasolioides MAF-Lich 15526 China, Yunnan, Jian Chuan Co. A. Crespo et al. Notoparmelia MAF-Lich 4965 New Zealand, South Island, West Coast H. A. Imshaug crambidiocarpa N. erumpens MAF-Lich 7529 Australia, Australian Capital Territory M. C. Molina & J. A. Elix N. erumpens MAF-Lich 7576 Australia, New South Wales M. C. Molina & J. A. Elix N. signifera MAF-Lich 7545 Australia, Australian Capital Territory M. C. Molina & J. A. Elix N. subtestacea MAF-Lich 17026 New Zealand, South Island, Otago A. Knight N. tenuirima MAF-Lich 17027 New Zealand, South Island, Southland A. Knight N. tenuirima MAF-Lich 7663 New Zealand, South Island, West Coast M. E. Hale Parmelia adaugescens MAF-Lich 7277 Japan, Hokkaido H. Harada P. adaugescens MAF-Lich 9870 Japan, Hokkaido H. Harada P. cochleata MAF-Lich 7280 Japan, Hokkaido H. Harada P. cochleata MAF-Lich 9880 Japan, Hokkaido H. Harada P. fertilis MAF-Lich 9871 Japan, Hokkaido H. Harada P. omphalodes MAF-Lich 6798 Spain, Madrid A. Crespo P. omphalodes MAF-Lich 15485 Spain, Zamora A. Crespo & O. Blanco P. saxatilis MAF-Lich 12518 Spain, La Rioja A. Crespo et al. P. saxatilis MAF-Lich 11541 Spain, Cadiz A. Crespo et al. P. sulcata MAF-Lich 13883 Spain, Madrid A. Crespo P. sulcata MAF-Lich 15421 Ireland, Kerry Dunkerron A. Crespo et al. quercina MAF-Lich 13949 Spain, La Rioja A. Crespo et al. Relicina limbata MAF-Lich 10504 Australia, New South Wales J. A. Elix Relicinopsis intertexta MAF-Lich 15372 Thailand, Nakhon Nayok W. Polyiam R. rahegensis MAF-Lich 15373 Thailand, Nakhon Nayok W. Polyiam

form clade A; four (P. subtestacea, P. crambidiocarpa, P. in 30–50 ascospores per specimen. Mean values of the tenuirima, P. signifera) of the five species included in the size and ratio between length and breadth Australasian clade B plus P. erumpens; three species (Re- (Q) were calculated. Thallus morphology of the speci- licina limbata, Relicinopsis intertexta and R. rahegensis) mens was studied using a dissecting for the closely related to species of clade C; and six Parmelia assessment of lobe shape, width and other vegetative species (Parmelia adaugescens, P. cochleata, P. fertilis, P. features. omphalodes, P. saxatilis and P. sulcata), two of them (P. saxatilis and P. sulcata) included in clade D of the molec- ular phylogeny (Crespo et al. 2010b). One Parmelina species (P. quercina) was included for comparison. De- Results tails of the material studied (locality and collection data) are summarized in Table 1. In addition, we con- The ascospore morphology, together with sidered the descriptions of all species of the Parmelia apothecium morphology and anatomy of assemblage, in particular the Australasian species, found fertile specimens of Nipponoparmelia (clade in the bibliography (Hale 1987; Elix 1993a, 2007; Elix & A) and three minor clades (B, C and D) of Kantvilas 1995) to complement our own observations. the Parmelia clade (Fig. 1), were investi- gated. The new diagnostic reproductive fea- Morphological studies tures based on ascospore type (defined by Vertical sections through the central part of three spore size and spore wall thickness) and apothecia per specimen were cut with a razor blade structure of the proper exciple are summar- under the dissecting microscope (Leica Wild M 8) and mounted in water and lactophenol cotton-blue (Panreac, ized in Tables 2 and 3. These features, com- Barcelona). The structure of the sections and morphology bined with the morphological diagnostic of the ascospores were observed and photographed with characters currently known (Table 4), allow a light microscope (Nikon Eclipse 80i; Nikon, Badhoe- us to clearly separate the four clades. The vedrop, Netherlands) using Nomarski differential inter- ference contrast optics. The length and breadth of asco- species of the four clades can be distinguished spores, and the thickness of their wall, were measured by a combination of features such as lobe 54 THE LICHENOLOGIST Vol. 46

Fig. 1. Simplified tree showing the splitting of the genus Parmelia into three independent monophyletic lineages A, B and D (based on Fig. 1 in Crespo et al. 2010b; phylogram obtained from a Maximum likelihood analysis of the 3GENE dataset, showing the phylogenetic relationships among Parmeliaceae). 2014 Notoparmelia—Ferencova et al. 55

Table 2. Ascospore dimensions and ascospore type in the species studied, and overall range of dimensions for each genus.

Length Width Wall mean e SD mean e SD thickness Ascospore type* Species (mm) (mm) (nm) (Ferencova 2012) Fig.

Nipponoparmelia laevior 1775 e 073 841 e 065 600 V 2A N. ricasolioides 1952 e 103 1220 e 097 700 V 2B Nipponoparmelia 170–20575–130 <1000 Large to very large ascospores with medium walls Notoparmelia crambidiocarpa 1760 e 048 1133 e 053 1000 III 2G N. erumpens 1262 e 054 799 e 044 500 II 2C N. subtestacea 1243 e 085 842 e 064 500 II 2E N. signifera 1454 e 090 799 e 051 700 II 2D N. tenuirima 1480 e 068 944 e 077 700 II 2F Notoparmelia 115–155(–180) 75–100(–120) a1000 Medium (rarely large) ascospores with thin to medium (rarely thick) walls Parmelia adaugescens 2301 e 152 1245 e 109 2800 IV 2K P. cochleata 1241 e 056 696 e 030 1000 III 2J P. fertilis 1461 e 053 789 e 065 1300 III – P. omphalodes 1392 e 073 845 e 063 1500 III 2L P. saxatilis 1508 e 065 1095 e 072 1900 III 2M P. sulcata 1339 e 081 855 e 056 1000 III – Parmelia 12.0–16.0(–24.5) 6.5–11.5(–13.5) b1000 Medium to large (rarely very large) ascospores with thick to very thick walls Relicina limbata 650 e 054 422 e 034 400 I 2H Relicinopsis intertexta 624 e 044 407 e 034 400 I – Relicinopsis rahegensis 716 e 033 418 e 031 400 I 2I Relicina + Relicinopsis 60–7535–45 400 Small ascospores with thin walls

*see Introduction morphology, rhizine type, pseudocyphella The ascospores of Nipponoparmelia laevior structure, ascospore type (Fig. 2) and struc- and N. ricasolioides fit ascospore type V as ture of the proper exciple (Figs 3 & 4). described for parmelioid lichens (Ferencova Chemistry, conidiospore features and asco- 2012). They are large to very large (170– spore ratio Q overlap and do not help to dis- 205 75–130 mm) with medium spore tinguish these monophyletic groups. wall thickness (600–800 nm) (Fig. 2A & Clade B is described here as a new genus, B). They are ellipsoidal in N. ricasolioides Notoparmelia. The species included in this (Q ¼ 161) and elongated in N. laevior clade, and all the Australasian species mor- (Q ¼ 212). phologically closely related (formerly included Notoparmelia erumpens, N. tenuirima, N. in Parmelia) are combined in this new genus. signifera and N. subtestacea have ascospores of type II, medium-sized (115–155 75– Ascospores 100 mm), broadly ellipsoidal to ellipsoidal (Q ¼ 148–183), and with a thin to medium The ascospore features in the Nipponopar- spore wall (500–700 nm) (Fig. 2C–F). melia and Parmelia clades are shown in Table Notoparmelia crambidiocarpa ascospores (Fig. 2 and represented in Fig. 2. 2G) fit type III because they are large (170– 56 THE LICHENOLOGIST Vol. 46

Table 3. Main apothecium features in Nipponoparmelia, Notoparmelia, ‘‘Relicina + Relicinopsis’’ and Parmelia s. str. clades.

Nipponoparmelia Notoparmelia Relicina + Relicinopsis Parmelia s.str. Character (clade A) (clade B) (clade C) (clade D)

Apothecium substipitate stipitate to substipitate, substipitate substipitate, rarely mostly large, large, and splitting splitting radially radially with age with age Proper exciple 3-layered: 1-layered: 3-layered: 3-layered: structure thin to thick hyaline thick hyaline layer thin to thick hyaline thin to thick hyaline layer (30–70 mm) layer layer thin intermediate thin intermediate layer thin intermediate layer cortex-like basal layer layer cortex-like basal cortex-like basal layer layer

180 110–120 mm) and ellipsoidal (Hale 1987; Calvelo & Adler 1999; Feuerer (Q ¼ 156), with a thick wall (1000 nm). & Thell 2002; Divakar et al. 2003) were not Another eleven species reported by Hale studied here due to the lack of fertile mate- (1987), Elix (1993a, 2007) and Elix & Kant- rial. After Hale’s description, most of them vilas (1995), which possibly form part of this present ascospores of types III and IV, ex- group because of the morphology and dis- cept two species with ascospores of type I tribution pattern (restricted to Australia (P. meiophora and P. submutata). and/or New Zealand), were not studied here because of the lack of fertile material, or of Anatomy of the apothecium any material at all. According to the data pro- The most important character found here, vided by those authors, they also have asco- and unique for the Australasian clade B, spores of type II, medium-sized with a thin Notoparmelia, is the internal structure of the to medium spore wall. apothecium (Table 3). Notoparmelia spp. Ascospores of Relicina limbata (Fig. 2H), Relicinopsis intertexta and R. rahegensis (Fig. have large apothecia with the disc usually splitting radially. The proper exciple of those 2I) are of type I, small (60–75 35–45 apothecia is formed by a thick cupulate hya- mm) with a thin spore wall (400 nm). All the line layer (HL), composed of large hyphae species from both genera have been reported embedded in an abundant polysaccharide to have small ascospores, corresponding to matrix (Fig. 3A–E) and surrounded directly type I (Hale 1975; Elix et al. 1986). by a continuous algal layer. The hyphae of Parmelia cochleata (Fig. 2J), P. fertilis, P. the thick hyaline layer do not show any orga- omphalodes (Fig. 2L), P. saxatilis (Fig. 2M) nization or stratification: they are large and and P. sulcata have ascospores of type III; without any clear branching pattern, appar- they are medium to large (120–160 65– ently connecting the subhymenium with the 115 mm), broadly ellipsoidal to ellipsoidal medulla (Fig. 3C–E). In Notoparmelia tenuir- (Q ¼ 138–186) with a thick spore wall ima, some kind of stratification can be ob- (1000–1800 nm). Parmelia adaugescens (Fig. 2K) has ascospores of type IV, very large served and the hyphae in the lower part of the hyaline layer change direction and are verti- (210–245 115–135 mm), ellipsoidal cally orientated (Fig. 3E). (Q ¼ 180) with a very thick wall (2500– 3500 nm). Other species which possibly In all other species studied here (clades A, form part of this group because of the mor- C and D), the fungal hyphae connecting the phological features and distribution pattern subhymenium and the medulla (i.e. the hy- phae of the proper exciple) form three clearly 2014 Notoparmelia—Ferencova et al. 57

Fig. 2. Ascospore morphology. A, Nipponoparmelia laevior;B,N. ricasolioides;C,Notoparmelia erumpens;D,N. signifera;E,N. subtestacea;F,N. tenuirima;G,N. crambidiocarpa;H,Relicina limbata;I,Relicinopsis rahegensis;J, Parmelia cochleata;K,P. adaugescens;L,P. omphalodes;M,P. saxatilis. Bar ¼ 10 mm. The relation between ascospore length and ascospore width in the species belonging to clades Parmelia and Nipponoparmelia is shown in the box below. The diameter of the circle reflects the relative thickness of the spore wall. 58 THE LICHENOLOGIST Vol. 46

Fig. 3. A & B, cross- through the apothecium of Notoparmelia species; C–E, details showing the cupulate proper exciple F & G, early ontogenic stage of the apothecium. A & C, Notoparmelia signifera;B,N. erumpens;D,N. tenuirima;E,N. subtestacea;F,Notoparmelia tenuirima;G,Parmelina quercina. Alg ¼ algal layer; BL ¼ basal layer; HL ¼ hyaline layer; Hym ¼ hymenium; Med ¼ medulla; PExc ¼ cupulate proper exciple. Scales: A, B, F & G ¼ 100 mm; C–E: 10 mm. 2014 Notoparmelia—Ferencova et al. 59 differentiated layers (Fig. 4): the thin hyaline layer (HL), the intermediate layer (IL) and Notoparmelia A. Crespo, Ferencova & the cortex-like basal layer (BL). Differences Divakar gen. nov. in the thickness and anatomy of these layers can be observed between different genera MycoBank No.: MB 805031 (Fig. 4B, D & F) but are not discussed here. Thallus foliose, adnate to loosely adnate, irregularly In contrast, clade B completely lacks the lobate, lobes 20–70 mm wide; apices rounded. three-layered organization of the proper exci- Pseudocyphellae usually effigurate. Rhizines squarrosely ple present in all other species of clades A, C branched. Apothecia substipitate to stipitate; splitting radially with age; cupulate proper exciple hyaline and 1- and D (Fig. 4B, D & F), and in the rest of layered, lacking differentiation into three layers as other the Parmeliaceae studied (data not shown). parmelioids. Ascospores ellipsoid, spore wall less than The structure of the proper exciple reflects 1 mm thick. Distribution in Australasia. the organization of the apothecium at the Type species: Notoparmelia signifera early ontogenetic stages. In the Notoparmelia (Fig. 5) species (clade B), the hyphae between the ascogenous hyphae and the thalline tissue of Thallus foliose, adnate to loosely adnate, the young apothecia (Fig. 3F) are radially irregularly lobate. Lobes flat, narrow, sublin- oriented, and, as mentioned above, the ma- ear to subirregular; apices rounded, lacking ture apothecium (Fig. 3A, B) has the proper cilia. Upper surface whitish to mineral grey, exciple formed by a single layer. In compari- greenish grey to grey-green, sometimes with son, in all other parmelioid species the devel- brownish tips to the lobes, the pseudocyphel- oping proper exciple at the same ontogenetic lae usually effigurate, sometimes fusing into stage is subdivided into an upper hyaline the continuous white rim around the lobe layer and a lower part composed of densely margins, with or without soredia and isidia. packed hyphae (Fig. 3G). Finally, the mature Medulla white, loosely packed. Lower surface apothecia of species from clades A (Nippono- flat, smooth, black or black with brown pap- parmelia,Fig.4A),C(‘‘Relicina & Relicinopsis’’, illate marginal zone. Rhizines short, squar- Fig. 4C) and D (Parmelia s. str., Fig. 4E) have rosely branched. Ascomata apothecial, lami- a three-layered proper exciple, due to the later nal, substipitate to stipitate; disc imperforate differentiation of the lower part into an inter- or rarely perforate, concave, dark to pale mediate layer and a cortex-like basal layer. brown, splitting radially with age; thalline margin usually pseudocyphellate; cupulate Thallus morphology proper exciple consisting of hyaline layer, Both species of Nipponoparmelia (clade A) (30–)40–60(–70) mm thick surrounded by present circular pseudocyphellae along the continuous algal layer. Asci elongate, clavate, lobe margins which were not found in any Lecanora-type, apically thickened, without an other species studied here. Relicina and Reli- internal apical beak, 8-spored. Ascospores me- cinopsis (clade C) are morphologically very dium to large, broadly ellipsoid to ellipsoid, different to all other species included in the (110–)115–155(–180) (70–)75–100 present study. They present cilia in the lobe (–120) mm; spore wall thin to medium, margins and lack any pseudocyphellae. No (400–)600–700(–1000) nm. major differences were found in thallus mor- Conidiomata pycnidial, immersed, laminal. phology between Notoparmelia (clade B) and Conidia cylindrical to weakly bifusiform Parmelia s. str. (clade D). Although some (50–)55–70 1 mm long. features are typical for clade B (e.g. squar- rose rhizines), they can also be found in Chemistry. Cortex containing atranorin some species of clade D. No single macro- and chloratranorin; medulla containing orci- morphological character is suitable for dif- nol depsidones (lobaric acid), b-orcinol dep- ferentiating between these two clades. A sidones (salazinic, consalazinic, protocetra- summary of the main macromorphological ric and fumarprotocetraric acids), aliphatic features that characterize the clades is shown acids (protolichesterinic acid), echinocarpic in Table 4. acid and unidentified fatty acid. 60 THE LICHENOLOGIST Vol. 46

Fig. 4. A, C & E, cross-sections through the apothecia of Nipponoparmelia, Relicina and Parmelia s. str.; B, D & F, details showing three-layered cupulate proper exciple. A & B, Nipponoparmelia laevior;C&D,Relicina limbata; E&F,Parmelia adaugescens. Alg ¼ algal layer, Cor ¼ cortex, Hym ¼ hymenium, Med ¼ medulla, PExc ¼ cupulate proper exciple composed of hyaline layer (HL), intermediate layer (IL) and cortex-like basal layer (BL). Scales: A, C&E¼ 100 mm; B, D & F ¼ 10 mm. 2014

Table 4. Main macromorphological characters and geographical distribution of Nipponoparmelia, Notoparmelia, ‘‘Relicina + Relicinopsis’’ and Parmelia s. str., based on our observations and bibliographic references (Hale 1975, 1987; Elix 1993a, 2007; Kurokawa 1994; Elix & Kantvilas 1995). Notoparmelia Nipponoparmelia Notoparmelia Relicina + Relicinopsis Parmelia s.str. Character (clade A) (clade B) (clade C) (clade D)

Lobes sublinear sublinear to subirregular sublinear to linear sublinear Pseudocyphellae small, punctate at effigurate laminal or/and lacking; pored epicortex present effigurate laminal or marginal, rarely — lobe edges marginal fusing and forming white rim mostly forming white rim Ferencova Rhizines simple to furcate squarrosely branched simple to sparsely branched simple to furcate and squarrosely branched

Cilia absent absent present absent 61 al. et Distribution East Asia Australasia (two species also Australasia, South-East Asia, boreal-temperate Northern in S America, and one Indonesia, India, Neotropical Hemisphere species widespread in S Asia) 62 THE LICHENOLOGIST Vol. 46

Fig.5. Notoparmelia signifera. A, habit. Scale ¼ 1 cm.

Etymology. The epithet refers to the South- and N. protosulcata) also occur in South ern Hemisphere distribution (noˇto- in Greek America, and one species (N. erumpens) also meaning southern, south), and the species occurs in South Africa and is more wide- superficially resembling Parmelia. spread in East Asia. Species clustered in this genus are mainly distributed in the Southern Remarks. Notoparmelia is characterized by Hemisphere. the following combination of characters: sublinear to subirregular lobes with rounded New combinations apices, short, squarrose rhizines, substipitate to stipitate large apothecia usually splitting We make the following 16 new combinations: radially with age and having the proper exci- ple formed only by one layer without stratifi- Notoparmelia crambidiocarpa (Zahlbr.) cation (stratified proper exciple in Parmelia s. A. Crespo, Ferencova & Divakar str. with the basal cortex-like structure), and comb. nov. medium to large broadly ellipsoid ascospores MycoBank No.: MB 805032 ranging from (110–)115–165(–180) Parmelia crambidiocarpa Zahlbr., Lichenes Novae Zelan- (70–)75–100(–120) mm with thin to me- diae 104: 109 (1941). dium walls, less than 1 mm (more than 1 mm in Parmelia s. str.). The genus includes 16 Notoparmelia crowii (Elix) A. Crespo, species that grow on bark and rocks in south- Ferencova & Divakar comb. nov. ern and eastern Australia, Tasmania and New Zealand. Two species (N. cunninghamii MycoBank No.: MB 805033 Parmelia crowii Elix, Mycotaxon 47: 116 (1993a). 2014 Notoparmelia—Ferencova et al. 63

Notoparmelia cunninghamii (Cromb.) Notoparmelia pseudotenuirima (Gyeln.) A. Crespo, Ferencova & Divakar comb. A. Crespo, Ferencova & Divakar comb. nov. nov. MycoBank No.: MB 805034 MycoBank No.: MB 805043 Parmelia cunninghamii Cromb., Journal of the Linnean Parmelia tenuirima f. isidiosa Mu¨ll. Arg., Bull. Herb. Society of London 15: 228 (1876). Bossier 4: 90 (1896). Parmelia brownii C. W. Dodge, Nova Hedwigia 19: 449 Parmelia pseudotenuirima Gyeln., Repertorrium Specie- (1970). rum Novarum Regni Vegetabilis 29: 289 (1931).

Notoparmelia erumpens (Kurok.) A. Notoparmelia salcrambidiocarpa (Hale) Crespo, Ferencova & Divakar comb. A. Crespo, Ferencova & Divakar comb. nov. nov. MycoBank No.: MB 805036 MycoBank No.: MB 805044 Parmelia tenuirima f. corallina Mu¨ll. Arg., Flora 66: 46 Parmelia salcrambidiocarpa Hale, Smithsonian Contr. Bot. (1883). 66: 38 (1987). Parmelia erumpens Kurok., Journal of Japanese Botany 44: no.74 (1969). Notoparmelia signifera (Nyl.) A. Notoparmelia norcrambidiocarpa Crespo, Ferencova & Divakar comb. (Hale) A. Crespo, Ferencova & Divakar nov. comb. nov. MycoBank No.: MB 805046 MycoBank No.: MB 805037 Parmelia signifera Nyl., Lichenes Novae Zelandiae:25 Parmelia norcrambidiocarpa Hale, Smithsonian Contr. Bot. (1888). 66: 31 (1987). f. signifera (Nyl.) Mu¨ll. Arg., Compte- Rendu Socie´te´ Royale Belgique 31: 30 (1892). Notoparmelia nortestacea (Elix) A. Crespo, Ferencova & Divakar comb. Notoparmelia subtestacea (Hale) A. nov. Crespo, Ferencova & Divakar comb. nov. MycoBank No.: MB 805038 Parmelia nortestacea Elix, Biblioth. Lichenol. 95: 203 (2007). MycoBank No.: MB 805048 Parmelia subtestacea Hale, Smithsonian Contr. Bot. 66: 45 Notoparmelia novae-zelandiae (Hale) (1987). A. Crespo, Ferencova & Divakar comb. nov. Notoparmelia tarkinensis (Elix & Kantvilas) A. Crespo, Ferencova & MycoBank No.: MB 805039 Divakar comb. nov. Parmelia novae-zelandiae Hale, Smithsonian Contr. Bot. 66: 31 (1987). MycoBank No.: MB 805050 Parmelia tarkinensis Elix & Kantvilas, Pap. Proc. R. Soc. Notoparmelia queenslandensis (Hale) Tasm. 129: 65 (1995). A. Crespo, Ferencova & Divakar comb. nov. Notoparmelia tenuirima (Hook. f. & MycoBank No.: MB 805041 Taylor) A. Crespo, Ferencova & Divakar comb. nov. Parmelia queenslandensis Hale, Smithsonian Contr. Bot. 66: 36 (1987). MycoBank No.: MB 805051 Notoparmelia protosulcata (Hale) A. Parmelia tenuirima Hook. f. & Taylor, Hooker’s London Journal of Botany 3: 645 (1844). Crespo, Ferencova & Divakar comb. Parmelia tenuiscypha Taylor, Hooker’s London Journal nov. of Botany 6: 175 (1847). Parmelia tenuirima var. platyna Zahlbr., Lichenes Novae MycoBank No.: MB 805042 Zelandiae 104: 108 (1941). Parmelia protosulcata Hale, Mycotaxon 16: 162 (1982). 64 THE LICHENOLOGIST Vol. 46

Notoparmelia testacea (Stirt.) A. their area (Australasia) but, independent of Crespo, Ferencova & Divakar comb. their relationship, they are morphologically nov. so different (see Table 4) that they cannot be misidentified. In addition to macromor- MycoBank No.: MB 805053 phological traits (presence/absence of pseu- Parmelia testacea Stirt., Scottish Naturalist 4: 203 (1878). docyphellae and cilia, type of rhizines), the Parmelia tenuirima * P. rudior Nyl., Lichenes Novae micromorphological differences (anatomy of Zelandiae: 25 (1888). proper exciple and ascospore type) are also Parmelia tenuirima var. erimis Nyl., Lichenes Novae very clear (Figs 2, 3, 4C & D; Tables 2 & 3). Zelandiae: 25 (1888). Parmelia rudior (Nyl.) Zahlbr., Catalogus lichenum uni- Nipponoparmelia (clade A) contains four versalis 6: 198 (1929). species with a special type of circular mar- Parmelia erimis (Nyl.) Hillmann, Hedwigia 78: 259 ginal pseudocyphella, distinct from those of (1939). other Parmelia species (Crespo et al. 2010b). Parmelia signifera f. pallidior Zahlbr., Lichenes Novae Zelandiae 104: 107 (1941). Usually it presents simple to furcate rhizines. Also, the type of ascospores of the species studied differs from the rest of Parmelia studied, Notoparmelia being of type V (i.e. large ascospores with This newly described genus includes a medium spore wall thickness) (Fig. 2A & group of Australasian species previously placed B). Moreover, the anatomy of the proper in Parmelia s. str. (Hale 1987) that differ exciple is three-layered in Nipponoparmelia morphologically from other species in this (Fig. 4A & B) and so very different to the genus by having thinner spore walls and a one-layered proper exciple of Notoparmelia proper exciple that is reduced to one layer (Fig. 3A–E). without zonation and composed exclusively On the other hand, Notoparmelia (clade B) of loosely branched large hyphae embedded and Parmelia s. str. (clade D) are similar in in an abundant polysaccharide matrix. The most of the macromorphological features but proper exciple is surrounded by a continuous in spite of this apparent homogeneity, they algal layer. differ in fine morphological details, especially the ascospore type (Table 2) and ascoma anatomy (Table 3). The range of their asco- Discussion spore size overlaps but they differ in the thickness of the spore wall (Table 2, Fig. 2). Notoparmelia, the new genus described here, Parmelia s. str. has ascospores of type III and has been previously shown to form an inde- IV, medium to very large, with spore walls pendent monophyletic lineage of Parmelia more than 1 mm thick (Fig. 2J–M), while (Crespo et al. 2010b). Although the different Notoparmelia has ascospores of type II, distribution pattern of the group was noted medium-sized, with the spore wall of thin to (Hale 1987; Crespo et al. 2010b), no macro- medium thickness, less than 1 mm (Fig. 2C– morphological features were known to sepa- F), with the exception of N. crambidiocarpa rate these Australasian species from the rest (Fig. 2G) which has ascospores of type III of Parmelia. Here, we offer some overlooked (large ascospores with e1 mm thick spore reproductive features that are typical for this wall). lineage, confirming once again the usefulness The main distinctive, previously over- of the micromorphological and anatomical looked, character that distinguishes Notopar- characters for genus delimitation in Parmelia- melia from Parmelia s. str. is the internal ceae (e.g. del Prado et al. 2007; Crespo et al. structure of the apothecia (Figs 3 & 4). Hale 2010a; Divakar et al. 2010). (1987) noted that Australasian species of Relicina and Relicinopsis (clade C) form the Parmelia have large apothecia with the disc sister group of Notoparmelia (clade B), al- splitting radially with age, and a usually bro- though with very low support (Crespo et al. ken and inward folded margin. The reason 2010b). Both groups are sympatric in part of for these features was never investigated and 2014 Notoparmelia—Ferencova et al. 65 we offer the hypothesis that these features are examined in the present study and they probably a consequence of the internal struc- show the one-layered proper exciple char- ture of the apothecium. As shown in the re- acteristic for the genus. Two species, N. sults, the proper exciple of Notoparmelia is norcrambidiocarpa and N. salcrambidiocarpa, formed exclusively by the thick cupulate hya- were described by Hale (1987) as morpho- line layer, composed of large hyphae without logically identical (whitish grey thalli with a clear orientation and embedded in an the dense rhizines projecting a mat around abundant polysaccharide matrix. This is a lobe margins) to N. crambidiocarpa. Their unique feature that is exceptional in Parme- differences are related to ascospore size, liaceae (although present also in the unre- chemistry and distribution pattern. Due to lated genus Platismatia, Ferencova 2012). the lack of fertile material it was not possible The proper exciple of the Notoparmelia to study their apothecial anatomy but, as apothecium does not show the characteristic pointed out by Hale (1987), they have stratification of all other Parmeliaceae; it lacks ascospores that fit type II similar to the rest the intermediate layer and cortex-like basal of Notoparmelia and, thus, we included both layer. The latter is thought to function as a species in the new genus. The case of N. supportive and protective tissue because its subtestacea and N. nortestacea is similar. Both composition is similar to the cortical tissue. species were described by Hale (1987) and It is formed by short-branched and intercon- Elix (2007), respectively, as morphologically nected hyphae that probably act as a skeleton identical (pale greenish to grey thalli with which prevents the disruption of the apothe- roundish marginal secondary lobes and lower cia during changing hydration states. The surface black with distinct bare to papillate hydrophilic polysaccharide matrix in which brown zone around the margins) but differ- the hyphae are embedded may allow mainte- ing in chemical pattern from N. testacea. nance of the integrity of the whole structure Both were reported to have ascospores that of the apothecia. Why the species of Notopar- fit into the same ascospore type II (Hale melia do not present such an organization of 1987; Elix 2007), and so we also included the proper exciple is unknown. them in the new genus Notoparmelia. Moreover, the geographical areas of the The second monophyletic group of Noto- three groups previously included in Parmelia parmelia is composed of three species, N. are different. Nipponoparmelia is distributed signifera, N. cunninghamii and N. tenuirima in East Asia. Notoparmelia is restricted to the (see Crespo et al. 2010b), which morphologi- Southern Hemisphere, with the centre of dis- cally share small effigurate pseudocyphellae. tribution in Australia and New Zealand, two Two of them, N. signifera and N. tenuirima, species also in South America (N. cunningha- show the one-layered proper exciple charac- mii and N. protosulcata), and one also wide- teristic for the genus and ascospores of type spread in South-East Asia (N. erumpens). It II. The isidiate counterpart of N. tenuirima, should be noted that these three more ex- N. pseudotenuirima (Hale 1987), was not tended species are sorediate. Parmelia s. str. is studied due to the lack of material, but is centred in boreal-temperate Northern Hemi- included in the new genus because it was sphere areas, although some species are dis- reported to have ascospores of type II (Hale tributed worldwide (Hale 1987; Molina et 1987). Similarly, five other species N. crowii al. 2004). (Elix 1993a), N. novae-zelandiae (Hale 1987), The new genus Notoparmelia has been N. protosulcata (Hale 1982), N. queenslandensis shown to form two monophyletic groups (Hale 1987) and N. tarkinensis (Elix & Kant- (see Crespo et al. 2010b). The first one con- vilas 1995), originally described as Parmelia tains two corticolous species (N. crambidio- species, are included in Notoparmelia because carpa and N. subtestacea), with sublinear to they share morphological traits, distribution subirregular lobes with an almost continuous area and ascospore type with the rest of Noto- white rim around the lobe margins formed parmelia species. by pseudocyphellae. Both species have been 66 THE LICHENOLOGIST Vol. 46

More extensive sampling including other Blanco, O., Crespo, A., Divakar, P. K., Elix, J. A. & species is required to confirm that the molec- Lumbsch, H. T. (2005) Molecular phylogeny of parmotremoid lichens (Ascomycota, Parmeliaceae). ular based phylogenetic topology parallels Mycologia 97: 150–159. the morphological traits, to refine the species Blanco, O., Crespo, A., Ree, R. H. & Lumbsch, H. T. concept in this genus and to further confirm (2006) Major clades of parmelioid lichens (Parme- the position of all mentioned species within liaceae, Ascomycota) and the evolution of their mor- this genus. phological and chemical diversity. Molecular Phylo- genetics and Evolution 39: 52–69. Calvelo, S. & Adler, M. T. (1999) Parmelia araucana Conclusions sp. nov. and new reports in the Parmeliaceae sensu stricto (lichenized Ascomycotina) from Patagonia The structure of the proper exciple is an and Tierra del Fuego (Argentina). Sydowia 51: important character for Parmeliaceae (Crespo 145–154. et al. 2010a; Divakar et al. 2010) that has Crespo, A., Lumbsch, H. T., Mattsson, J.-E., Blanco, been neglected in systematic studies due to O., Divakar, P. K., Articus, K., Wiklund, E., Bawin- gan, P. A. & Wedin, M. (2007) Testing morphol- the frequent absence of ascomata in samples. ogy-based hypotheses of phylogenetic relationships Our results corroborate the segregation of in Parmeliaceae (Ascomycota) using three ribosomal Nipponoparmelia based on molecular and markers and the nuclear RPB1 gene. Molecular morphological vegetative data (Crespo et al. Phylogenetics and Evolution 44: 812–824. Crespo, A., Ferencova, Z., Perez-Ortega, S., Elix, J. A. 2010b), and indicate that the two mono- & Divakar, P. K. (2010a) Austroparmelina, a new phyletic groups formed by Parmelia species Australasian lineage in parmelioid lichens (Parme- clearly differ in anatomical characteristics of liaceae, Ascomycota). Systematics and Biodiversity 8: the proper exciple, ascospore type and geo- 209–221. graphy. Based on these correlated features, Crespo, A., Kauff, F., Divakar, P. K., del Prado, R., Perez-Ortega, S., de Paz, G. A., Ferencova, Z., we have proposed the segregation of Parmelia Blanco, O., Roca-Valiente, B., Nu´n˜ez-Zapata, J. into two genera. Since the type species (P. et al. (2010b) Phylogenetic generic classification saxatilis) is included in clade D, it is consid- of parmelioid lichens (Parmeliaceae, Ascomycota) ered as Parmelia s. str. and clade B (Austral- based on molecular, morphological and chemical evidence. Taxon 59: 1735–1753. asian Parmelia) is described as a new genus, Crespo, A., Divakar, P. K. & Hawksworth, D. L. (2011) Notoparmelia. Generic concepts in parmelioid lichens, and the phylogenetic value of characters used in their cir- This project was supported by the institutional funds of cumscription. Lichenologist 43: 1–25. 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(2010) The morphologically deviating (2003) New species and records in the lichen family genera Omphalodiella and Placoparmelia belong to Parmeliaceae (Ascomycota) from India. Mycotaxon Xanthoparmelia (Parmeliaceae). Bryologist 113: 376– 88: 149–154. 386. Divakar, P. K., Molina, M. C., Lumbsch, H. T. & Blanco, O., Crespo, A., Elix, J. A., Hawksworth, D. L. & Crespo, A. (2005) Parmelia barrenoae, a new lichen Lumbsch, H. T. (2004a) A molecular phylogeny species related to (Parmeliaceae) and a new classification of parmelioid lichens con- based on molecular and morphological data. Lichen- taining Xanthoparmelia-type lichenan (Ascomycota: ologist 37: 37–46. ). Taxon 53: 959–975. Divakar, P. K., Crespo, A., Blanco, O. & Lumbsch, H. Blanco, O., Crespo, A., Divakar, P. K., Esslinger, T. L., T. (2006) Phylogenetic significance of morphol- Hawksworth, D. L. & Lumbsch, H. T. (2004b) ogical characters in the tropical Hypotrachyna clade Melanelixia and Melanohalea, two new genera of parmelioid lichens (Parmeliaceae, Ascomycota). segregated from Melanelia (Parmeliaceae) based on Molecular Phylogenetics and Evolution 40: 448–458. molecular and morphological data. Mycological Re- Divakar, P. K., Lumbsch, H. T., Ferencova, Z., del search 108: 873–884. Prado, R. & Crespo, A. (2010) Remototrachyna,a 2014 Notoparmelia—Ferencova et al. 67

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