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Notoparmelia, a New Genus of Parmeliaceae (Ascomycota) Based on Overlooked Reproductive Anatomical Features, Phylogeny and Distribution Pattern

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Notoparmelia, a New Genus of Parmeliaceae (Ascomycota) Based on Overlooked Reproductive Anatomical Features, Phylogeny and Distribution Pattern The Lichenologist 46(1): 51–67 (2014) 6 British Lichen Society, 2014 doi:10.1017/S0024282913000649 Notoparmelia, a new genus of Parmeliaceae (Ascomycota) 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 Parmelia. 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, lichens, 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 (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 ascospores, 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 (5Á0–10Á0 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 (10Á0–15Á0 mm and simple ellipsoid hyaline ascospores long) with a thin to medium spore wall (Blanco et al. 2006; Crespo et al. 2007, (<1Á0 mm); type III, medium to large asco- 2010b). The Parmelia species are charac- spores (10Á0–20Á0 mm long) with a thick terized by adnate, sublinear to subirregular spore wall (1Á0–2Á0 mm); type IV, very large lobes without cilia; an upper surface with ascospores (>20Á0 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 (>15Á0 mm long) squarrosely branched); 8 simple spores per with a thin to medium spore wall (<1Á0 ascus; conidia cylindrical or weakly bifusi- mm). In addition, different types of internal form, less than 8Á0 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 clades: 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. Parmelina 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 ascospore 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 microscope for the closely related to species of clade C; and six Parmelia assessment of lobe shape, width and other vegetative species (Parmelia adaugescens, P.
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