Mycosphere Doi 10.5943/mycosphere/3/1/5 Three resurrected species of the Bulbothrix Hale (, Lichenized Fungi)

Benatti MN1*

1Instituto de Botânica, Seção de Micologia e Liquenologia, Caixa Postal 68041, São Paulo / SP, CEP 04045-972, Brazil. [email protected]

Benatti MN 2012 – Three resurrected species of the genus Bulbothrix Hale (Parmeliaceae, Lichenized Fungi). Mycosphere 3(1), 46-55, Doi 10.5943/mycosphere/3/1/5

Bulbothrix laeviuscula, B. pseudocoronata and B. subscortea are proposed as new combinations in the Parmeliaceae based on type studies. Descriptions are presented and their characters discussed.

Key words – bulbate cilia – Bulbothrix fungicola – Bulbothrix goebelii – Bulbothrix isidiza – Bulbothrix viridescens – Parmeliaceae

Article Information Received 7 October 2011 Accepted 26 January 2012 Published online 19 February 2012 *Corresponding author: Michel N. Benatti – e-mail – [email protected]

Introduction treated as synonyms by Hale (1976). Conse- The genus Bulbothrix Hale (Hale 1974) quently three new combinations are presented is based on the Series Bicornutae (Lynge) Hale here. & Kurokawa of the genus Acharius. Its species are easily identifiable by the small, Methods deeply laciniate thalli with marginal bulbate The morphological and anatomical cilia (the main characteristic), atranorin as characters of the specimens were analysed cortical substance (what differentiates it from using standard stereoscopic and compound the genus Relicina), hyaline, unicellular, microscopes. Anatomical sections, including ellipsoid or bicornute ascospores, and bacilli- those of apothecia and pycnidia when present, form to bifusiform conidia. The medullary were made with a razor blade by hand. The chemistry is variable, containing several subs- chemical constituents were checked by spot tance sets and some unknown substances. Hale tests with potassium hydroxide (K), sodium (1976) bundled all available taxonomic hypochlorite (C) and para-phenylenediamine information in a monograph. Afterwards several (P), and also examined under UV light (360 additional taxa have been found, mainly in the nm). Chemical constituents were identified by Neotropics (e.g., Aptroot & Aubel 1999, Elix thin-layer chromatography (TLC) using solvent 1993, 1995, Hale 1986, Jungbluth et al. 2008, C (Bungartz 2001), and compared with the data Krog 1993, Marcelli 1993, Marcelli & Ribeiro on labels left with the specimens. 2002, Morales-Méndez et al. 1995, Sérusiaux The morphological terms for lobe 1984, Sipman & Aubel 1992, Spielmann & development are in agreement with recent Marcelli 2008) and a revision of the genus publications, with two exceptions. Lacinules are became opportune. During this (Benatti 2010) adventitious, ribbon-like secondary outgrowths many type specimens were examined, which from the primary lobe margins or sometimes resulted in new interpretations of some names from the upper surface. Lobules are similar, but

46 Mycosphere Doi 10.5943/mycosphere/3/1/5 short and rounded (Marcelli et al. 2011). 1.7 mm diam., substipitate, margins smooth when young, then subcrenate, occasionally Bulbothrix laeviuscula (Räsänen) Benatti & interrupted by ciliary bulbs, amphithecia Marcelli, comb. et stat. nov. Fig. 2 smooth, normally with many ciliary bulbs, MycoBank: MB 519637 irregularly coronate (see comments); discs light Basionym – Parmelia marginalis var. brown, epruinose, imperforate, epithecium 7.5– laeviuscula Räsänen, Arch. Soc. Zool. Bot. 10.0 µm, hymenium 42.5–62.5 µm, subhyme- Fenn. Vanamo 2: 45, 1947. nium 20.0–27.5 µm; ascospores subspherical to Holotype – Uruguay, Depto. Canelones, ellipsoid, 5.0–8.5 × 4.0–5.5 µm, epispore ca. Carrasco National Park, arboricola, leg. I.M. 0.75 µm thick; pycnidia laminal, common, Lamb 3081, 22-II-1946 (H! designated by Hale immersed, with brown or black ostioles (hard to 1976, but cited as lectotype). discern amidst the many laminal ciliary bulbs); Thallus fragments up to 2.8 cm wide, conidia bacilliform to weakly bifusiform, 5.0– subcoriaceous, corticolous, becoming dusky 9.0 × ca. 0.75 µm. grey in the herbarium; upper cortex 7.5–12.5 Color reactions – upper cortex K+ µm thick, algal layer 37.5–50.0 µm thick, yellow, UV–; medulla K–, C–, KC–, P–, UV–. medulla 20.0−30.0 µm thick, lower cortex TLC – cortical atranorin; no medullary 10.0–17.5 µm thick. Laciniae sublinear, 0.4–1.7 substances (see also Hale 1976). mm wide, dichotomously, anisotomically to Distribution – Uruguay (Räsänen 1947). irregularly branched, imbricate to crowded, Additional specimens examined: Urugu- adnate, attached; apices plane to involute, ay, Depto. Montevideo, planted grove of Pinus truncate to subtruncate; margin subcrenate to & Eucalyptus, Charrasco National Park crenate or irregular, flat, entire to incised, often (Franklin D. Roosevelt National park), leg. sublacinulate, ciliate, axils oval to irregular. H.A. Imshaug & R.C. Harris 42530, 23-II-1968 Upper surface continuous, smooth to subrugose (MSC). Idem., Dept. Maldonado, Sierra de las with few occasional irregular cracks, laminal Animas, on branches of Dodonea viscosa along ciliary bulbs common, small and frequent; the road to the Mirador Nacional, 34o42’S, maculae absent. Adventitious lacinules scarce 55o19’W, ca. 200 m, leg. H.S. Osorio 2305, 20- on older parts, very short, simple to furcate or II-1950 (US). Idem., Piriapolis, Cerro Del Toro, irregularly branched, flat, 0.2–0.8 × 0.1–0.4 southern slope of the hill, on trunk of Dodonea mm, truncate, underside concolorous with the viscosa, 50-100 m, leg. H.S. Osorio 4584, 01- lower margin. Cilia black, simple or without V-1961 (US). Brazil, Rio Grande do Sul State, apices, 0.05–0.10(–0.15) × ca. 0.03 mm, Itapuã Municipality, Praia da Pedreira, leg. sometimes bent down, with semi-immersed to S.M. Martins & A. Lemos 197, 02-VII-2003 emersed basal bulbs ca. 0.05 mm wide, frequent (HAS). along the margins, spaced 0.05–0.15 mm from Comments – Bulbothrix laeviuscula is each other to rarely contiguous mainly in the characterized by the narrow, sublinear laciniae, laciniae axils, absent or scarce at the laciniae the emaculate upper surface commonly with apices. Medulla white. Soredia, pustulae and small laminal ciliary bulbs, bulbate cilia with isidia absent. Lower surface black, slightly simple or without apices, a black underside with shiny to opaque, smooth to rugose, moderately brown margins, simple to irregularly branched rhizinate; marginal zone brown, attenuated, ca. rhizines without basal or dislocated bulbs, 0.5 mm wide, sometimes black and indistinct irregularly coronate apothecia with ciliary bulbs from the center, slightly shiny, smooth, weakly in the amphitecium, containing small, papillate, partially rhizinate; rhizines black, subellipsoid ascospores, and by the lack of occasionally dark brown when next to the medullary substances. margins, simple to furcate or sometimes This species was treated by Hale (1976) irregularly ramified, without basal or dislocated as a synonym of B. viridescens (Lynge) Hale (S bulbs, 0.10–0.30(–0.45) × ca. 0.05 mm, lectotype!), and has similar laciniae, cilia and frequent, homogeneously distributed. Apothecia rhizinae. However, the analyzed specimens of laminal or submarginal, common, concave, 0.2– B. laeviuscula deviate from the lectotype, a

47 Mycosphere Doi 10.5943/mycosphere/3/1/5 duplicate (W!) and other specimens examined Basionym – Parmelia subscortea Asahi- (Marcelli 8076a, SP, and Fleig & Riquelme na, Journal of Japanese Botany 32: 99, 1957. 125, 147, ICN) of B. viridescens by the Holotype – Taiwan, Keitau, saxicolous, presence of laminal and amphitecial ciliary leg. Y. Asahina 3324, 24-XII-1933 (TNS!, bulbs, irregular coronate apothecia and larger designated by Hale 1976, but cited as ellipsoid ascospores 5.0−9.0 × 4.0−5.5 μm. In lectotype). contrast, B. viridescens develops at no stage Thallus fragments up to 8.0 cm wide, laminal or amphithecial ciliary bulbs, and subcoriaceous, saxicolous, becoming light curiously, this species can present both regular dusky in the herbarium; upper cortex 10.0–15.0 coronate and ecoronate mature apothecia on the µm thick, algal layer 20.0–27.0 µm thick, same thallus. The confusion may have arisen medulla 67.5−85.0 µm thick, lower cortex from the numerous pycnidia seen in B. 12.5–15.0 µm thick. Laciniae subirregular to viridescens, which resemble ciliary bulbs, but sublinear, (0.9–)1.6–4.5(–5.5) mm wide, differ by the typical structure containing irregularly to sometimes dichotomously aniso- conidiogenous hyphae and conidia, instead of tomically branched, slightly imbricate becom- the idioblast roundish cells and an oily ing more or less crowded in the center, adnate, substance (Hale 1974, Feuerer & Marth 1997, loosely attached; apices plane, subrounded to Benatti 2011). sometimes subtruncate; margin smooth and Similar laminal ciliary bulbs occur in B. sinuous or irregular, ±flat, entire, rarely bulbochaeta (Hale) Hale (LWG holotype!), sublacinulate, ciliate, axils oval. Upper surface which shares also the absence of propagules continuous, smooth, becoming irregularly and the medullary chemistry. However, this cracked in some parts of the center, laminal species, known so far only from the ciliary bulbs absent; maculae absent (scars left palaeotropics (Hale 1976), differs by the by fallen isidia might resemble them). smaller and more rounded ascospores Adventitious lacinules scarce and restricted to measuring ca. 4.0−6.0 × 4.0−5.0 µm, the larger older parts, short, simple or sometimes laciniae (ca. 1.0–2.5 mm wide), much thicker irregularly branched, flat, 0.2−0.9 × 0.1–0.3 thalli (ca. 120–200 μm thick) and the more mm, truncate, underside concolorous with the branched cilia and rhizinae. lower margin. Cilia black, simple and long, The material from Uruguay mentioned 0.05–0.80 × ca. 0.03 mm, with semi-immersed by Hale (1976) as B. viridescens may actually to emerse basal bulbs 0.05−0.35 mm wide, be B. laeviuscula. The specimens are cited as frequent along the margins, spaced 0.05–0.10 "strongly pycnidiate" and with "pycnidiate mm from each other to contiguous on the amphithecia", which might actually be laminal laciniae axils, scarce at the laciniae apices. and amphithecial ciliary bulbs. As to reports of Medulla white. Soredia and pustulae absent. B. viridescens from Argentina by Adler (1988), Isidia abundant, laminal, granular to smoothly the description fits quite well with our concept cylindric, straight to slightly tortuous, of B. laeviuscula, including the laminal ciliary 0.05−0.40(−0.55) × ca. 0.05 mm, simple to bulbs that were noted by the author. However, sometimes slightly branched, erect, firm to no vouchers could be localized at IMG. caducous, concolorous or with brown apices Bulbothrix semilunata (Lynge) Hale (S when more developed, eciliate. Lower surface holotype!) differs by the narrower laciniae (ca. light brown except for slightly darker venations 0.2–0.5 mm wide), dichotomously ramified and some few scattered spots, shiny, smooth to cilia and rhizinae, and by the more regularly subrugose, densely rhizinate; marginal zone coronate apothecia containing larger, bicornute, light brown, usually indistinct from the center, sigmoid or crescent-shaped ascospores (12.0– sometimes slightly darker or rarely blackish, 23.0 μm long). shiny, smooth to subrugose or venate, weakly papillate, partially rhizinate; rhizines light Bulbothrix subscortea (Asahina) Marcelli & brown to brown, simple, with basal or displaced Benatti, comb. nov. Fig. 3 darkened bulbs, 0.05−0.70 × 0.03−0.05 mm, MycoBank: MB 519638 abundant becoming less frequent close to the

48 Mycosphere Doi 10.5943/mycosphere/3/1/5 margins, homogeneously distributed. Apothecia be distinguished as follows. Bulbothrix taba- not found, but according to Asahina (1957) cina (Montagne & Bosch) Hale (L!, lectotype, cupuliform, up to 5.0 mm diam., margins incur- selected by Hale 1976) is corticolous, has ved and crenulate, amphithecia smooth, conco- similar wide laciniae 1.5−4.5 mm but with a lorous to the thallus; no mention of any kind of maculate upper surface, eciliate isidia without ornamentations; discs ferruginous brown, bulbs and a black lower side with brown epruinose, hymenium ca. 50 µm, reaching 90 margins. Bulbothrix australiensis Hale (US!, µm including epithecium and subhymenium; holotype) is also corticolous and has narrower, ascospores ellipsoid, 8 per asci, 16.0 × 9.0 µm; sublinear laciniae (0.5−2.0 mm wide), eciliate pycnidia not found. and longer isidia without bulbs, up to 1.0 mm Color reactions – upper cortex K+ long, and a brown to light brown lower side. yellow, UV−; medulla K+ yellow→dark red, Bulbothrix subglandulifera (Hue) Hale (PC!, C−, KC−, P+ yellow, UV−. holotype, mentioned as lectotype by Hale 1976) TLC – cortical atranorin; medullary also differs by the narrower laciniae (ca. salazinic acid (fide Asahina 1957, Hale 1976). 0.5−1.5 mm wide), more ramified and partially Distribution – Asia: India, Nepal, ciliate isidia with small ciliary bulbs, rhizinae Taiwan (Asahina 1957). with basal bulbs, and smaller ascospores Additional specimen examined: Japan, usually 6.0−10.0 × 5.0−8.0 µm. Izu, Central Japan, Simoda, Mt. Buzan, leg. S. The morphologically similar and equally Kurokawa 58628, 02-XII-1958 (US). saxicolous Bulbothrix cinerea Marcelli & Kalb Comments – Bulbothrix subscortea is (herb. Kalb!, holotype) has thallus with a characterized by the broad, subirregular laci- deeper grey tonality, eciliate isidia always with niae, an emaculate upper surface, simple cilia, blackish apices, coronate apothecia, and simple to little ramified isidia, a usually light medullary norstictic acid. The equally similar brown underside, simple brown rhizinae with and norstictic acid-containing B. ventricosa basal or dislocated dark bulbs, and the presence (Hale & Kurokawa) Hale (TUR-V!, lectotype) of medullary salazinic acid. Asahina (1957) is corticolous, and differs by the variable described apothecia, but there are none in the coloration of the lower cortex, the coronate lectotype material. The author also described apothecia and also by the laminal ciliary bulbs. the laciniae width twice as large as found in the lectotype (1 cm). Bulbothrix pseudocoronata (Gyelnik) Benatti Bulbothrix subscortea resembles B. & Marcelli, comb. nov. Fig. 4 isidiza closely but there are several differences MycoBank: MB 561687 which set them clearly apart: the thallus is stiff Basionym – Parmelia pseudocoronata instead of membranaceous, saxicolous instead Gyelnik, Fedde´s Repertorium Specierum of (mostly) corticolous; the upper surface is Novarum 29: 289, 1931. smooth and maculate instead of rough, rugged, Synonyms – Parmelia coronata f. and emaculate; the cilia have usually longer isidiosa Müller Argoviensis, Revue Mycolo- apices, up to 0.8 instead of up to 0.3 mm; and gique 10: 56, 1888. the rhizines have basal or displaced bulbs, Lectotype – Paraguay, Cerro Yaguarón, instead of being without these structures. sur l'écorce des arbres, leg. Balansa 4176, 17- Hale (1976) treated Parmelia subscortea VI-1879 (G! selected by Hale 1976; duplicates as a synonym of B. isidiza (H-Nyl!, holotype; at M! and W!). mentioned as lectotype by Hale 1976). Swins- Bulbothrix lacinulata Marcelli, Jung- cow & Krog (1988), Elix (1994), Kurokawa & bluth & Elix, Mycotaxon 104: 54, 2008. Lai (2001) and Divakar & Upreti (2005) appa- (Brazil, São Paulo State, Itirapina Municipality, rently followed his concept, because they cite Estação Ecológica do Instituto Florestal, saxicolous specimens of B. isidiza, which do 22°15’S 47°49’W, 770 m alt., woodland, on a probably all belong to B. subscortea. tree trunk, L.S. Canêz, P. Jungbluth & A.A. There are several further Bulbothrix Spielmann 1083A, 27-III-2004, SP!, holotype). species with salazinic acid and isidia. These can Thallus fragments up to 4.5 cm wide [entire

49 Mycosphere Doi 10.5943/mycosphere/3/1/5 thalli up to 5.4 cm wide], submembranaceous, without asci) subrounded to ellipsoid, corticolous, becoming light dusky grey in the (5.0)7.09.5 × 4.55.5 µm, epispore ca. 1.0 herbarium; upper cortex 7.5–15.0 µm thick, µm; pycnidia scarce to abundant, laminal to algal layer 10.0–25.0 µm thick, medulla submarginal or on the lacinulae, immersed, with 20.0−40.0 µm thick, lower cortex 12.5–22.5 µm black ostioles; Conidia (not found on type) thick. Laciniae sublinear, 0.1–0.6(–1.0) mm bacilliform to weakly bifusiform, 5.08.0 × 1.0 wide, dichotomously anisotomic to irregularly µm. branched, contiguous becoming little imbricate Color reactions – upper cortex K+ or crowded at the center, tightly adnate, yellow, UV; medulla K or + weak yellowish, strongly attached; apices plane, truncate to C+ rose to reddish rose, KC+ rose to reddish subtruncate; margin smooth and sinuous to rose, P or + weak yellowish, UV. (Occasio- subcrenate or irregular, flat, entire to slightly nal yellowish K and P medullary reactions are incised, commonly sublacinulate, ciliate, axils probably due to small amounts of atranorin). oval or subirregular. Upper surface continuous, TLC/HPLC – cortical atranorin and smooth, frequently hidden by lacinulae except chloroatranorin; medullary gyrophoric (major) at distal parts [with occasional transversal and lecanoric (minor/traces/absent) acids (see cracks], laminal ciliary bulbs absent; maculae also Hale 1976, Jungbluth et al. 2008). absent (see comments). Lacinules frequent to Distribution – South America: Paraguay abundant, marginal to laminal, short, subcanali- (Müller Argoviensis 1888, sub Parmelia culate or semi-cylindrical like cleaved isidia to coronata f. isidiosa), Brazil: SP (Jungbluth flat and lingulate, those laminal ascending and 2006, Jungbluth et al. 2008, sub Bulbothrix procumbent, simple or irregularly branched, lacinulata). This species was treated by Hale 0.100.80  0.05–0.20 mm, truncate or acute, (1971 1976) as a synonym of B. fungicola, and ciliate, underside concolorous with the lower due to a confusion involving these species and margin light brown. Cilia black, apices absent also B. suffixa and B. lacinulata; the or simple to partially furcate, 0.05–0.10(–0.15) distributions of B. fungicola and B.  ca. 0.03 mm, with semi-immersed basal bulbs pseudocoronata are possibly mixed. Additional ca. 0.05(0.10) mm wide, abundant along the Specimen examined – Dominican Re- margins, spaced ca. 0.05 mm from each other to public, Prov. Santiago, pine forest on ridge occasionally contiguous, scarce or absent at the around hospital north of San Jose de las Matas, laciniae apices or on the most densely lacinulate leg. H.A. Imshaug & C.M. Wetmore 3881, 17- margins. Medulla white. Soredia and pustulae VIII-1958 (US). Dominica, Bois Serpé (trail absent. Isidia absent (but see lacinulae). Lower from South Chiltern to Soulfrière Bay), ca. surface black to dark brown, shiny, smooth to 1000 ft., Parishes of St. Luke and St. Marks, subrugose, weakly papillate, slightly to mode- H.A. Imshaug & F.H. Imshaug 32758, 6-XI- rate to densely rhizinate; marginal zone light 1963 (MSC). Trinidad, South slope of El brown, attenuate, ca. 0.5 mm wide, shiny, Tucuche (above gap between El Tucuche and smooth to weakly papillate, partially rhizinate; Naranja), north of St. Joseph, Northern Range, rhizines black to dark brown or rarely light leg. H.A. & F.H. Imshaug 32971, 13-X-1963 brown, simple to partially furcate, frequently (MSC). Honduras, Distrito Central, above San with basal bulbs, 0.050.30  ca. 0.03 mm, Juancito, along a trail in the cloud forest, on a frequent to abundant, homogeneously freshly felled Liquidambar, elev. above 6410 distributed. Apothecia laminal, absent to ft., leg. W.L. & C.F. Culberson 18423, 29-XII- common, plane to convex, coronate with small 1979 (DUKE). Paraguay, Depto. Paraguarí, bulbs, 0.2–2.3 mm diam., adnate, margins Parque Nacional Ybycuí, along road/trail to smooth to subcrenate, amphithecia smooth, Salto Mbocaruzú on Rio Corrientes, ca. 200 m, sometimes with few lacinulae or scarce ciliary ca. 26º 05’ S, 56º 53’ W, dry forest and bulbs; discs light brown, epruinose, imper- extensive sandstone outcrops in cerrado, on forate, epithecium 10.012.5 µm, hymenium palm trunk, leg. W.R. Buck 12082, 6-X-1984 20.0–32.5 µm, subhymenium 17.525.0 µm; (NY). Brazil, Pará, Serra do Cachimbo, aprox. ascospores (not found on type, hymenium 10 km N of Base Aérea do Cachimbo, along the

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Figs 1–3 The type specimens of B. laeviuscula and B. subscortea. 1 Holotype of B. laeviuscula. 2 Detail of a tiny laminal ciliar bulb cut showing the internal cells and escaping oily substance. 3 Holotype of B. subscortea. Bars = 1 cm, except when indicated.

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Cuiaba-Santarém highway (BR-163), ca. ca. 70 µm high, ellipsoid ascospores 14.018.0 o o 9 22´S, 54 54’W, ca. 430-480 m, leg. L. Brako × 9.012.0 µm. The spores are much larger than & M.J. Dibben 6280, 28-IV-1983 (NY). Idem., we observed in our material, therefore it is Mato Grosso, BR-163 highway, km 37 of the possible that Vainio had a different species at Coxim-Rondonópolis stretch, near Itiquira hand. Gyelnik (1931) raised P. coronata f. River, 500 m alt., cerrado, on tree trunk, leg. isidiosa to species level using a new epithet, P. M.P. Marcelli 8448, 8450, 30-VI-1980 (SP). pseudocoronata, but without adding any Idem., São Paulo, Cachoeira das Emas description or comment. Municipality, 530 m alt., annually burnt cerrado The lectotype of Parmelia coronata f. field, over mangabeira trunk (Hanchornia isidiosa and B. pseudocoronata, selected by speciosa Gomes), leg. M.P. Marcelli 16351, Hale (1976), consists of two fragments in good 16353, 23-IX-1978 (SP). Idem., Santa Rita do condition, only slightly damaged at some parts, Passa Quatro Municipality, Vassununga farm, on tree bark. There are few pycnidia (conidia km 259 of the Anhanguera Highway, 760 m were not found), and only one underdeveloped alt., transition from cerrado to cerradão, on apothecium without asci in the hymenium. The twig, leg. M.P. Marcelli & B.L. Morretes duplicate from W consists of two smaller 16056, 27-IX-1978 (SP). Idem., Itirapina fragments, which are in even better condition, Municipality, Estação Ecológica do Instituto with more flat lacinulae, pycnidia and Florestal, dense cerrado, on tree trunk, leg. L.S. apothecia. The duplicate from M is also in good Canêz, P. Jungbluth & A.A. Spielmann 1083, condition, consisting of two small fragments 2 27-III-2004 (SP). Idem., Mogi-Guaçu cm diam. and one ca. 5 cm diam., has virtually Municipality, Reserva Biológica de Mogi- the same proportion of semi-cylindrical and flat Guaçu, Campininha farm, on tree trunk at lacinulae, and several full-grown apothecia cerradão border, M.P. Marcelli & A.E. Luchi without asci. 34658, 19-IX-2000 (SP). The material fits well the description of Comments – Bulbothrix pseudocoronata B. lacinulata (Jungbluth & Marcelli 2008), and is characterized by the sublinear, narrow laci- since Parmelia pseudocoronata antedates B. niae, an emaculate upper surface densely lacinulata, the latter becomes a synonym of B. covered by semi-cylindrical to subcanaliculate pseudocoronata. It deviates cleary from B. or flat lacinulae, simple or furcate cilia, a black fungicola (Lynge) Hale, where the species had lower cortex with brown margins, simple to been included before as synonym (e.g., Hale furcate rhizinae with basal bulbs, coronate 1976), by the presence of abundant lacinules apothecia containing rounded to ellipsoid small rather than rather scattered, cylindrical isidia. ascospores, and by the presence of gyrophoric While B. fungicola produces only short, acid as main medullary substance. cylindrical isidia, B. pseudocoronata has longer In the protologue of Parmelia coronata lacinulae, which may look like isidia at very f. isidiosa Müller Argoviensis (1888) mentions early stages, but become flattened soon. Also very ramified and abundant isidia, leaving free the first has more abundant rhizinae without only the apical parts of the laciniae. Despite the basal bulbs, while in B. pseudocoronata the several apothecia in the duplicates, the author rhizinae are less frequent and commonly with mentioned that ascospores were not found. basal bulbs. One of the fragments that compose Vainio (1890) separated P. coronata f. isidiosa the type collection of B. fungicola (S!) is in fact from P. coronata Fée by the "infrequently" of B. pseudocoronata, and the probable reason isidiate thallus. As further details he mentions why Lynge (1914) and Hale (1976) believed light colored, not cracked and emaculate thalli, that B. fungicola formed isidia as well as with much larger laciniae (0.52.5 mm wide), laminal lacinulae and were inclined to accept B. with whitish isidia(?), a densely rhizinate black pseudocoronata as a synonym of B. fungicola. lower cortex, and negative K- and C-reactions. For differentiation from this and other He also mentions imperforate apothecia similar species, see also Jungbluth & Marcelli ornamented with isidia and black spots 2008, Table 1. To this can be added, that the (corona?), with a brown epithecium, hymenia spores of B. pseudocoronata (B. lacinulata)

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Figs 4–5 The type specimen of B. pseudocoronata. 4 Lectotype of B. pseudocoronata. 5 Detail of the lacinulae of B. pseudocoronata. Bars = 1 cm, except when indicated. measure (5.0) 7.09.5 × 4.55.5 µm, which is Ritter), LWG (Tariq Husain), M (Andreas slightly smaller than in B. suffixa. Beck), MSC (L. Alan Prather), GLAM (Keith The species is perhaps most easily Watson), NY(Barbara Thiers), PC (Bruno confusable with B. suffixa (Stirton) Hale, Dennètiere), S (Anders Tehler) TNS (Yoshihito because of the presence of lacinules, used as a Ohmura), TUR (Seppo Huhtinen), U (Erik key character for B. suffixa by, e.g., Hale Smets),US (Rusty Russell) and W (Uwe (1976). The type material of B. suffixa (Stirton) Passauer) for the loans of the type specimens Hale (BM!, duplicate at GLAM!) is the and additional materials, Dr. Harrie Sipman for probable cause of the confusion between these the linguistic review, comments, and sugges- species. It is very immature and it is not tions, and the reviewers for critical revision of possible to be sure if it develops laminal the manuscript. lacinulae, isidia, or both. Jungbluth et al. (2008) suggest that the lacinules are scarce and merely References adventitious, 0.1-0.6 mm long. A difference may be in the wider laciniae, 0.51.5 mm wide. Adler M. 1988 – La família Parmeliaceae (Liquenes Ascomycotina) en la província Acknowledgements de Buenos Aires: estúdio taxonomico- The author wishes to thank the curators floristico. Thesis, Universidad de Buenos of BM (Scott LaGrecca), DUKE (Kathleen Aires. Pryer), G (Philippe Clerc), H (Leena Myllys), Aptroot A, Aubel RJMT. 1999 – Bulbothrix HAS ( Suzana M. A. Martins), ICN (Mara R. sipmanii, a new species from

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Guyana. Mycotaxon 71, 139–140. cerrados do Estado de São Paulo. Asahina Y. 1957 – Lichenologische Notizen Dissertation, Instituto de Botânica, São (124–125). The Journal of Japanese Paulo. Botany 32, 97–100. Jungbluth P, Marcelli MP, Elix JA. 2008 – Five Benatti MN. 2010 – Revisão taxonômica do new species of Bulbothrix (Parmeliaceae) gênero Bulbothrix Hale (Parmeliaceae, from cerrado vegetation in São Paulo liquenizados). Thesis, State, Brazil. Mycotaxon 104, 51–63. Instituto de Botânica. Krog H. 1993 – Parmelina enormis (Hale) Hale Benatti MN. 2011 – Two new species of is Bulbothrix enormis (Hale) Krog comb. Bulbothrix Hale. Mycology (in press). nov. Lichenologist 25, 299–300. Bungartz F. 2001 – Analysis of lichen Kurokawa S, Lai MJ. 2001 – Parmelioid lichen substances. ASU lichen herbarium. genera and species in Taiwan. Mycotaxon http://nhc.asu.edu/ /lichen_info/ 77, 225–284. tlc.jsp#TLC2. Accessed 20 July 2008. Lynge B. 1914 – Die Flechten der ersten Divakar PK, Upreti DK. 2005 – Parmelioid Regnellschen Expedition. Die Gattungen Lichens in India - a Revisionary Study. Pseudoparmelia gen. nov. und Parmelia Bishen Singh Mahendra Pal Singh, Dehra Ach. Arkiv för Botanik 13, 1–172. Dun-248 001. Marcelli MP. 1993 – Pequenas Parmelia s.l. Elix JA. 1993 – New species in the lichen ciliadas dos cerrados brasileiros. Acta family Parmeliaceae (Ascomycotina) Botanica Brasilica 7, 25–70. from Australia. Mycotaxon 47, 101–129. Marcelli MP, Ribeiro, CH. 2002 – Twenty-one Elix JA. 1994 – Bulbothrix. In: Flora of new species of Parmeliaceae (lichenized Australia, Lichens. Introduction, Lecano- fungi) from southeastern Brazil. rales 2, vol. 55. (eds AE Orchard, C Mitteilungen aus dem Institut für Grgurinovic). Australia Government Allgemeine Botanik Hamburg 30–32, Publishing Service, Canberra 13–19. 125–155. Elix JA. 1995 – New species in the lichen Marcelli MP, Canêz LS, Benatti MN, family Parmeliaceae (Ascomycotina) Spielmann AA, Jungbluth P, Elix JA. from Australasia and Malaysia. Mycota- 2011 – Taxonomic novelties in xon 56, 231–241. Parmeliaceae. Bibliotheca Lichenologica Gyelnik V. 1931 – Additamenta ad cognitionem 106, 211-224. Parmeliarum. II. Feddes repertorium Morales-Méndez A, Marcano V, Galiz, L, specierum novarum regni vegetabilis 29, Mohali S, Palacios-Prü E. 1995 – 273–291. Bulbothrix amazonensis sp. nov., a new Hale ME. 1971 – Morden-Smithsonian species of Parmeliaceae () Expedition to Dominica: the lichens from Venezuelan Amazonia. (eds FJA (Parmeliaceae). Smithsonian Contribu- Daniëls, M Schulz, J Peine). In: Flechten tions to Botany 4, 1–25. Follmann. Contributions to lichenology in Hale ME. 1974 – Bulbothrix, Parmelina, Honour of Gerhard Follmann. Geobo- Relicina, and Xanthoparmelia, four new tanical and Phytotaxonomical Study genera in the Parmeliaceae. Phytologia Group, Botanical Institute, University of 28, 479–490. Cologne, Cologne, 281–286. Hale ME. 1976 – A monograph of the lichen Müller Argoviensis J. 1888 – Lichenes genus Bulbothrix Hale (Parmeliaceae). Paraguayenses a cl. Balansa lecti. Revue Smithsonian Contributions to Botany 32, Mycologique 10, 53-68, 113-120, 178- 1–29. 184. Hale ME. 1986 – New species in the lichen Räsänen V. 1947 – Lichenes Novi III. Family Parmeliaceae (Ascomycotina). Archivum Societatis Zoologicae Botani- Mycotaxon 25, 85–93. cae Fennicae Vanamo 2, 45–51. Jungbluth P. 2006 – A família Parmeliaceae Sérusiaux E. 1984 – Contribution to the study (fungos liquenizados) em fragmentos de of lichens from Kivu (Zaire), Rwanda and

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Burundi. VIII. New and interesting Mycotaxon 103, 201–205. species of parmeliaceous lichens. The Swinscow TDV, Krog H. 1988 – Macrolichens Bryologist 87, 1–11. of East Africa. British Museum of Natural Sipman HJM, Aubel RJMT. 1992 – New History, London. Parmeliaceae (Lichenes) from the Vainio (Wainio) EA. 1890 – Étude sur la Guianas and surroundings. Mycotaxon classification naturelle et la morphologie 44, 1–12. des Lichens du Brésil, pars prima. Acta Spielmann AA, Marcelli MP. 2008 – Bulbothrix Societatis pro Fauna et Flora Fennica 7, i– viatica Spielmann & Marcelli, a new xxix, 1–247. species of Parmeliaceae from Brazil.

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