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A Review of the Genus Bulbothrix Hale: the Isidiate, Sorediate, and Pustulate Species with Medullary Salazinic Acid

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A Review of the Genus Bulbothrix Hale: the Isidiate, Sorediate, and Pustulate Species with Medullary Salazinic Acid Mycosphere Doi 10.5943/mycosphere/4/1/1 A review of the genus Bulbothrix Hale: the isidiate, sorediate, and pustulate species with medullary salazinic acid Benatti MN1 1Instituto de Botânica, Núcleo de Pesquisa em Micologia, Caixa Postal 68041, São Paulo / SP, CEP 04045-972, Brazil e-mail: [email protected] Benatti MN 2013 – A review of the genus Bulbothrix Hale: the isidiate, sorediate, and pustulate species with medullary salazinic acid. Mycosphere 4(1), 1–30, Doi 10.5943 /mycosphere/4/1/1 This study is a taxonomic review of ten Bulbothrix (Parmeliaceae, Lichenized Fungi) species containing salazinic acid in the medulla that reproduce by vegetative propagation or form pustules that erode into coarse granules. The current species delimitations are confirmed. New characteristics are detailed, some synonyms are rejected, others confirmed, and range extensions are added. Key words – bulbate cilia – norstictic acid – Parmeliaceae – Parmelinella Article Information Received 27 November 2012 Accepted 10 December 2012 Published 23 January 2013 *Coresponding Author: Michel N. Benatti – e-mail – [email protected] Introduction 2010). Bulbothrix Hale was proposed for a This paper deals with several of the group of species previously called Parmelia species related to Parmelinella, as did a Series Bicornutae (Lynge) Hale & Kurokawa previous one (Benatti 2012c). Recent molecular (Hale 1974), characterized by small, laciniate research (Divakar et al. 2006, Crespo et al. and usually adnate thalli, simple to branched 2010) points out that Bulbothrix species bulbate marginal cilia, cortical atranorin, containing medullar salazinic acid may actually simple to branched rhizinae, smooth to belong to Parmelinella, or even be another coronate apothecia, hyaline unicellular small genus closely related to it. Eventually, ellipsoid to bicornute ascospores 5.0−21.0 × with the advancement of research to resolve 4.0−12.0 µm, and bacilliform to bifusiform open questions about the phylogeny of many conidia 5.0−10.0 × 0.5−1.0 µm (Hale 1976, species that constitute Bulbothrix, including the Elix 1993a). Crespo et al. (2010) presented a type, species with bicornute ascospores revised generic concept of Parmelioid lichens containing salazinic acid might eventually turn based on molecular, morphological and out to still be included in the genus or perhaps chemical evidence and included other form a new one. diagnostic features such as a pored epicortex, During a revision of the genus lack of cortical pseudocyphellae, and presence Bulbothrix (Benatti 2010) the type specimen of isolichenan in the cell walls. Bulbothrix is and additional material of Bulbothrix was currently nested in the Parmelina clade and studied. These species have cilia with hollow some species are grouped with Parmelinella, basal bulbs, which contain differentiated making the genus paraphyletic (Crespo et al. (round) cells and a characteristic oily substance 1 Mycosphere Doi 10.5943/mycosphere/4/1/1 (Hale 1975, Feuerer & Marth 1997, Benatti Material and methods 2011). The first published part of Benatti’s Type material and additional species (2010) thesis concerns new combinations of were studied from BM, CANB, DUKE, H, four species, Hypotrachyna tuskiformis (Elix) HUFSCAr, L, LD, MEL, MSC, NY, PC, SP, Benatti & Marcelli, Parmelinopsis pinguiacida TNS, and US, originating from Oceania, Asia, (Louwhoff & Elix) Marcelli & Benatti, P. North Pacific Ocean islands, Africa, North subinflata (Hale) Benatti & Marcelli and America, Central America, Caribbean, and Parmotrema yunnanum (Sheng L. Wang, J.B. South America, as well as material collected in Chen & Elix) Marcelli & Benatti, previously Brazil during the last 30 years, mainly by the placed in Bulbothrix (Benatti & Marcelli 2010) author and members of the Lichenological and excluded due to the lack of true bulbate Study Group of the Instituto de Botânica (GEL) cilia. The second part treats the species in Brazil. containg medullary norstictic and protocetraric The methodology and conventions are acids (Benatti 2012a). The third part treats the detailed in Benatti (2012a). Bulbs on cilia, species with medullary salazinic acid that do rhizines, apothecia and other thallus parts were not form isidia, soredia, lacinulae or pustules checked using the clarification method (Benatti (Benatti 2012c). 2011). Chemical constituents of the additional It is planned to publish six papers to specimens examined were identified by thin- provide a comprehensive understanding and layer chromatography (TLC) using solvent C easy assessment of all the data on this genus (Bungartz 2001), and compared with the data (comprising ca. 60 species) gathered in an on labels left with the specimens. The types unpublished study by Benatti (2010). The six had their chemical constituents examined by parts are: (I) species containing medullary high performance liquid chromatography norstictic and protocetraric acid; (II) species (HPLC), following the methods described in containing salazinic acid lacking vegetative Elix et al. (2003). propagules (both already published, see Benatti The presence of salazinic acid is 2012a, 2012c); (III) species containing evidenced by a K+yellowdark red spot test salazinic acid with vegetative propagules (this reaction. Its presence is also sometimes paper); (IV) species containing fatty acids or no perceived by the formation of bundles of thin medullary substances; (V) species containing elongated shaped crystals of a deep reddish the gyrophoric/lobaric/lecanoric acids lacking colour, observed under a light microscope after vegetative propagules; and (VI) species the transfer of hyphae onto a microscope slide containing the gyrophoric/lobaric/lecanoric and dropping the reagent on the fungal with vegetative propagules. This will material, such as cutting a small piece of the ultimately result in a synthesis of the whole thallus or of the apothecia. However, unlike the genus followed by a worldwide key. A crystals of norstictic acid (Benatti 2012a), the discussion about all the motives for such an crystals of salazinic acid depends on a higher extensive and detailed treatment and the concentration of the substance and take longer problems faced while working the review is to crystallize. explained in Benatti (2012c). The species selected for comparisons This paper discusses the ten species are those that show close morphological or with medullary salazinic acid [Bulbothrix chemical similarities, and those most often australiensis Hale, B. decurtata (Kurok.) Hale, compared by other authors due to peculiar B. imshaugii (Hale) Hale, B. isidiza (Nyl.) characteristics. Hale, B. microscopica Elix, B. pustulata (Hale) Hale, B. subglandulifera (Hue) Hale, B. Results and discussion subscortea (Asahina) Marcelli & Benatti, B. The study confirmed ten species subtabacina (Elix) Elix and B. tabacina (Mont. containing medullar salazinic acid that do form & Bosch) Hale], that do form isidia, soredia, or vegetative propagules (mainly isidia, but also pustules. soredia), or pustules. All species are described 2 Mycosphere Doi 10.5943/mycosphere/4/1/1 in detail and their diagnostic characters are laciniae. Soredia and pustules absent. Isidia discussed, with many unknown details about frequent, laminal to occasionally marginal, the morphology and secondary metabolites of granular to smooth cylindrical, straight to each taxa being clarified. slightly tortuous, 0.051.10 (0.05) 0.10 mm, With the exception of Bulbothrix simple but occasionally slightly branched, pustulata that is pustulate and B. imshaugii that erect, firm to ± caducous, usually with brown is sorediate, all other species are isidiate. apices, eciliate. Medulla white. Lower surface Bulbothrix australiensis, B. microscopic, B. brown to pale brown, shiny, smooth, weakly pustulata, B. subglandulifera and B. papillate, moderately rhizinate. Marginal zone subtabacina are corticolous, while B. decurtata brown to pale brown, indistinct from the center and B. subscortea are saxicolous. Bulbothrix to occasionally somewhat darker, shiny, imshaugii and B. isidiza are predominatly smooth, weakly papillate, weakly rhizinate. corticolous, rarely saxicolous. Rhizinae brown to black, commonly with whitish apices, simple, commonly with The species blackish bulbate bases, 0.050.45 0.030.05 mm, frequent but becoming scarcer close to the Bulbothrix australiensis Hale. Mycotaxon 25: margins, evenly distributed. Apothecia not 85. 1986. Fig.1 found (accordingly to Hale 1986 and Elix 1994, Mycobank MB 104075 they are sessile to adnate, 0.81.0 mm in diam., Holotype − Australia, New South ecoronate, only immature ascospores were Wales, Ku-rin-gai National Park, observation found). Pycnidia common, laminal to point, on tree in park area, leg. M.E. Hale submarginal, immerse, with black ostioles. 59360, 20-I-1982 (US!, MEL isotype n.v.). Conidia bacilliform to weakly bifusiform, Thallus sublinear laciniate, pale dusky 5.0−6.0 × ca. 1.0 µm. grey in herbarium, up to 3.2 cm in diam., TLC/HPLC: cortical atranorin and subcoriaceous, corticicolous, upper cortex chloroatranorin, medullary salazinic acid (see 12.5−17.5 µm thick, algal layer 15.0−27.5 µm also Hale 1976, Elix 1994). thick, medulla 75.5−90.0 µm thick, lower Distribution – Oceania: Australia (Hale cortex 15.0−17.5 µm thick. Laciniae 1986, Elix 1994). anisotomic to irregularly dichotomously Additional specimens examined – branched, 0.62.0 mm wide, contiguous to Australia, New South Wales, South Coast slightly imbricate, strongly adnate and District,
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