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
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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
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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, Honeysuckle Bay, Murramarong adpressed, with flat, subtruncate to truncate National Park, 10 km N of Batemans Bay, on apices, margins plane, smooth and sinuous to bark, 3538’S, 15015’E, leg. K. Ralston 2628, crenate or subirregular, entire, scarcely 2-VII-2002 (MEL). Idem, Queensland, sublacinulate, axils oval. Upper surface smooth Keperra, near corner Glengarry Road and Uper and continuous, becoming slightly rugose and Kedron Road, on Acacia sp., leg. R. Rogers & irregularly cracked in some parts, laminal ciliar C. Beasley 3408, 12-V-1975 (MEL). bulbs absent. Adventitious marginal lacinulae Comments – The holotype (Fig. 1) scarce and restricted to older parts, short, consists of several small fragments in good 0.20.6 0.1–0.2 mm, plane, simple, apices condition, on bark, not being glued on truncate, lower side concolorous to the lower cardboard. There are several isidia at different marginal zone. Maculae absent. Cilia black to stages of maturation, but no apothecia were partially brown, apices simple or sometimes found in the material, although pycnidia are not distinct, 0.05–0.35 ca. 0.03 mm, with common. The isotype mentioned by Hale sessile to emergent bulbate bases 0.050.30 (1986) was not located. Only immature mm wide, the bases eventually enlarged and ecoronate apothecia are known for Bulbothrix reniform, abundant along the margin, spaced australiensis, without a description of ca. 0.05 mm from each other, or contiguous, ascospores. solitary or in small groups at the crenae and There is no sign of maculae in the upper axils, scarce to absent at the apices of the cortex of any of the specimens studied. The 3
Mycosphere Doi 10.5943/mycosphere/4/1/1 isidia are thick and robust, often above 0.5 mm laciniate or sublaciniate, greyish olivaceous high, and in some parts they can become green in herbarium, fragments up to 8.5 cm in densely branched, reaching more than 1 mm in diam., coriaceous, saxicolous, upper cortex height. The rhizines have conspicuous and dark 22.5−40.0 µm thick, algal layer 42.5−65.0 µm bulbate bases, similar to those of the cilia. thick, medulla 100.0−130.0 µm thick, lower This species was compared by Hale cortex 27.5−50.0 µm thick. Laciniae (1986) to B. subtabacina and B. isidiza. The anisotomic to irregularly dichotomously first differs by the strongly maculate and branched, 0.62.8 (−3.5) mm wide, contiguous strongly cracked upper cortex, narrower to imbricate becoming partially crowded at the laciniae (ca. 0.5−1.0 mm wide), cilia with more center, strongly adnate and adpressed, with subtle bulbs and branched apices, by the plane to slightly involute, subtruncate apices, smaller, often simple and ciliate isidia, a black the margins plane, sinuous to subcrenate or lower cortex, and by the the dichotomously irregular, entire, scarcely sublacinulate, the branched rhizines without basal bulbs. The axils oval. Upper surface smooth, irregularly second differs by its maculate upper cortex, cracked except by the younger distal parts, and smaller, mostly simple isidia, and its laminal ciliar bulbs absent. Adventitious wider, more irregularly branched laciniae ca. marginal lacinulae scarce on random parts, 1.5−5.0 mm with rounded apices, and paler short, 0.50.6 0.2–0.4 mm, plane, simple or rhizines that lack bulbate bases. irregularly branched, apices truncate, lower Some small specimens of B. isidiza side concolorous with the lower marginal zone. collected on substrates in which they had little Maculae absent. Cilia black, apices simple or room to develop have laciniae with minimum absent, frequently bent downwards, 0.05–0.40 widths for the species, and can resemble those ca. 0.03 mm, with semi-immerse to sessile of B. australiensis, but these are always bulbate bases (0.05) 0.100.15 (0.25) mm maculate. Even in well developed specimens of wide, these sometimes stretched and wilted, B. australiensis the laciniae are always frequent throughout the margins, spaced emaculate, more sublinear, with truncate 0.05−0.10 mm from each other becoming apices, not exceeding 2 mm in width. contiguous at the axils, to scarce at the apices Among other relatively similar species, of the laciniae. Soredia, and pustules absent. B. tabacina (L! lectotype, PC! duplicate) Isidia frequent, laminal, granular to short differs from B. australiensis by nearly identical smooth cylindrical with a papillar aspect, characters as B. isidiza, except this species has straight, 0.050.10 (0.15) ca. 0.05 mm, a black lower cortex. Bulbothrix cinerea simple, erect, firm to ± caducous, usually Marcelli & Kalb differs by its saxicolous blackened and shiny already as soon as the growth habit, the usually brown or blackish, isidia are being formed (sometimes the simple and smaller isidia, and by the presence blackening is restricted to their apices), eciliate. of medullary norstictic acid. Medulla white. Lower surface black to occasionally dark brown, shiny to opaque, Bulbothrix decurtata (Kurok.) Hale. smooth to subrugose, moderately rhizinate. Phytologia 28: 480. 1974. Figs 2−3 Marginal zone brown to dark brown, black or Mycobank MB 341597 variegated, attenuated to indistinct from the Basyonym − Parmelia decurtata center, ca. 0.5−1.5 mm wide, shiny to opaque, Kurok. Contributions from the United States smooth, moderately rhizinate. Rhizinae black National Herbarium 36: 139. 1964. to brown, occasionally with whitish apices Holotype − Union of South Africa, when close to the margins, simple to Transvaal, District Lydenburg, 10 miles SE of occasionally irregularly branched, often with Lydenburg on sandstone rocks near road, leg. bulbate bases, 0.100.60 (−0.90) ca. 0.05 O. Almborn 7388, 20-X-1953 (LD!, isotype at (0.10) mm, frequent but becoming scarcer at US!). the margins, occasionally adglutinated, evenly Thallus subirregular to sublinear
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Mycosphere Doi 10.5943/mycosphere/4/1/1
Figs 1–3 – 1 Holotype of Bulbothrix australiensis (US). 2 Holotype of Bulbothrix decurtata (LD). 3 Detail of the small blackish isidia of the holotype. Scale bars = 1 cm (1, 2), 1 mm (3). 5
Mycosphere Doi 10.5943/mycosphere/4/1/1 distributed. Apothecia not found. Pycnidia somewhat similar to what occurs in the rimose submarginal, scarce, immerse, with black thalli of Parmotrema species with reticulate ostioles. Conidia weakly to distinct bifusiform, maculae (ex Rimelia), even though this species occasionally their cell lumina of unequal size, has none. The isidia are unique and easy to 5.0−9.0 × ca. 1.0 µm. distinguish from specimens of B. tabacina, TLC/HPLC − cortical atranorin, since early in its formation they are blackened medullary salazinic acid (see also Hale & and bright, with a papillate aspect. In the light Kurokawa 1964, Hale 1976). microscope they show the typical anatomical Distribution − Africa: South Africa structure, covered by a thin, dark "skin", of (Hale & Kurokawa 1964), Ivory Coast, and uncertain origin. Most isidia are entirely Uganda (Hale 1976). darkened, while some, usually the taller ones, Additional specimens examined − have the darkening restricted to their apices. South Africa, Natal, District Bergville, Both cilia or pycnidia are often formed from Cathedral Peak Area, alt. 6000 ft. Indument the isidia. Forest, on sandstone rocks, leg. O. Almborn Hale (1976) mentioned that B. 9328, 6-XI-1953 (LD, NY); idem, O. Almborn decurtata appeared to be the only obligatory 9329, 6-XI-1953 (MSC); idem, Cape Province, saxicolous species of the genus, but a few Simonstown District, Cape of Good Hope others have been discovered since. The author Nature Reserve, S.H. Skaife Field Station at also commented on a single anomalous Olofantsbosbaai, 34 18 AD, seaside cliffs with specimen due to the additional presence of the scattered trees, leg. W.R. Buck 13866, 21-I- substance norlobaridone found together with 1986 (NY); idem, Transvaal, Tzaneen District, salazinic acid, but noting that the specimen was Woodbush Forest Reserve, around radio masts indistinguishable from the normal population near Houbosdorp at Schnellskop, 23 30 CC, of the species. 2050 m, dwarf Forest with rock flats, leg. R.C. Bulbothrix tabacina (L! lectotype, PC! Harris 18609, 12-I-1986 (NY). duplicate) was the only species compared to B. Comments − The holotype (Fig. 2) decurtata in literature (Hale & Kurokawa consists of three fragments in good condition, 1964). Despite the similarities (presence of growing on rock glued to cardboard. The isidia, bulbate cilia with simple apices, isotype consists of a single fragment in the medullary salazinic acid spinal cord), they can same conditions as the holotype. None of the be differentiated by the fact that B. decurtata type materials displays apothecia, even has an emaculate, very cracked upper cortex, rudimentary ones, and few pycnidia were narrower subtruncate laciniae, cilia often found, some with conidia. Apothecial without apices, and by the smaller, blackened characteristics are unknown. and bright isidia, a somewhat variable lower Swinscow & Krog (1988) considered B. cortex colour, besides also being strictly decurtata a synonym of B. tabacina (L! saxicolous. lectotype, duplicate at PC!), claiming that it Bulbothrix isidiza (H-Nyl!, holotype), is was only a saxicolous form and that it did not also isidiate and presents medullary salazinic differ significantly. Due comparisons between acid, but differs by the presence of upper the specimens studied, and the consistent cortex maculae, the pale brown lower cortex, differences found between the specimens, B. and the larger, concolorous isidia often with decurtata is accepted here as a distinct species. darkened apices. As with B. tabacina, it is also It is possible that part of the material examined primarily found corticolous. by Swinscow & Krog (1988) are saxicolous Bulbothrix cinerea (Kalb pers. herb!, specimens of B. tabacina intermixed with true holotype), which also appears to be a strictly B. decurtata. A loan of the material was saxicolous species, differs by the somewhat requested several times from herbarium O, but relatively narrower laciniae, generally 0.51.5 all requests were unanswered. (2.5) mm wide, a pale brown lower cortex and The thallus surface of B. decurtata is of rhizines, and by the presence of acid very cracked, except for the young parts, medullary norstictic acid. 6
Mycosphere Doi 10.5943/mycosphere/4/1/1 Interestingly, thalli of B. cinerea also tend to plane, simple or irregularly branched, apices have blackened isidia much like those found on truncate, lower side concolorous to the lower B. decurtata (Fig. 3). However, the isidia marginal zone. Maculae distinct, punctiform to blackening of B. cinerea more often become effigurate, laminal. Cilia black, apices simple, eventually restricted only to the apices, not rarely furcate or irregularly branched, 0.05– enveloping the isidia as much as in B. 0.35 ca. 0.03 mm, with semi-immerse to decurtata. Developed isidia of B. cinerea are sessile bulbate bases 0.050.10 (0.20) mm partly dilated (due a common presence of a wide, frequent throughout the margins, in small parasitic fungi as found on specimens studied) groups at the crenae, spaced 0.05−0.15 mm or sometimes flatten acquiring lobule aspect, from each other, becoming contiguous at the being also larger and thicker than those found axils, occasionally juxtaposed as if they were on B. decurtata (Benatti 2012a). fused, usually scarce at the apices of the Bulbothrix ventricosa (Hale & Kurok.) laciniae. Soralia subcapitate or irregular, Hale (TUR-V! lectotype) is only found laminal to occasionally subapical, initially corticolous, and also differs by the constant hemispheric becoming flattened and extensive, development of laminal ciliar bulbs, larger apparently arising by gradual disintegration of concolorous isidia partially with brownish the upper cortex, soredia farinose to ± apices, a variable, often mixed coloration of the subgranular, 20.0−55.0 (−90.0) µm in diam. lower cortex, and by the presence of medullary Pustules and isidia absent (although some norstictic (Benatti 2012a). small soralia have a pustular aspect). Medulla white. Lower surface black, shiny, smooth, to Bulbothrix imshaugii (Hale) Hale. Phytologia subrugose, moderate to densely rhizinate in the 28: 480. 1974. Fig.4 center, occasionally less densely rhizinate Mycobank MB 341601 along the margins. Marginal attenuated, 0.5– Basyonym − Parmelia imshaugii Hale. 2.5 mm wide, brown to occasionally black, Phytologia 22: 31. 1971. opaque to shiny, smooth to subrugose, weakly Holotype − Chile, Prov. Valparaiso, papillate, becoming rhizinate towards the Montana Campana, coastal range, near center. Rhizinae black, occasionally dark Granizo, root of Notofagus, elevation 4000 ft., brown at the margins, simple to rarely furcate, leg. H. A. Imshaug 36670, 21-XI-1965 (MSC!, without bulbate bases or displaced bulbs, 0.10 isotype at US!). 0.60 (0.80) ca. 0.03 mm, frequent at the Thallus subirregular to partially margins becoming abundant at the center, sublinear laciniate, whitish dusky grey in evenly distributed. Apothecia not found herbarium, fragments up to 4.7 cm in diam., (accordingly to Hale 1976, they are substipiate, subcoriaceous, corticolous or rarely saxicolous, 2.04.0 mm in diam., ecoronate, with 8 upper cortex 17.5−22.5 µm thick, algal layer ascospores per ascus, measuring 8.0 4.0 µm). 25.0−37.5 µm thick, medulla 85.0−110.0 µm Pycnidia not found. thick, lower cortex 17.5−27.5 µm thick. TLC/HPLC – cortical atranorin, Laciniae irregularly to partially anisotomic medullary salazinic acid (see also Hale 1971, dichotomously branched, (1.4−) 2.14.6 mm 1976). wide, contiguous, slightly adnate and Distribution – South America: adpressed, with subplane, subtruncate to Argentina (Calvelo & Adler 1999), Chile (Hale irregular apices, the margins subplane, smooth 1971, 1976, Galloway & Quilhot 1998) and to crenate or irregular, incised, occasionally Venezuela (López-Figueiras 1986, Marcano et sublacinulate, the axils oval to irregular. Upper al. 1996). cortex smooth and continuous, becoming Additional specimens examined: Chile, subrugose with occasional irregular cracks on National Park La Campana, 33oS, over older or densely sorediate parts, laminal ciliar Nothofagus obliqua, leg. G. Guzmán 3368, 26- bulbs absent. Adventitious marginal lacinulae II-1985 (US); idem, over rock, 1000 m, G. scarce, randomly scattered, short (although Guzmán 3357, 26-II-1985 (US); idem, Prov. sometimes wide), 0.20.5 0.2–2.0 mm, Santiago, 8 km W of Tiltil, shrub chaparral 7
Mycosphere Doi 10.5943/mycosphere/4/1/1 (IBP Primary Site), on east slope of Cuesta de substance) with variable amounts of lecanoric la Dormida, 1000-1300 m, on shaded boulder and orsellinic acids, instead of the salazinic in ravine, leg. W.A. Weber & B. Johnston s.n., acid. 9-XI-1976 (US); idem, Cuesta de la Dormida, Calvelo & Adler (1999) mentioned a east slope, on trunk of Nothofagus obliqua single specimen as B. imshaugii with much (Mirb.) Oerst., 950 m, leg. P.W. Rundel 7316, longer cilia than those seen in the material 29-VII-1972 (US). examined here (0.11.5 mm long). The authors Comments This was the first also noticed a pustular origin of some soralia, sorediate Bulbothrix species described (Hale and while they did mention the occasional 1971). Besides B. imshaugii, this kind of presence of basal bulbs in the rhizines, these propagule is known for only one other species were not observed here. in the genus, B. leprieurii Aubel (Sipman & None of the morphologically close Aubel 1992). Both species are only known species containing medullary salazinic acid from South America. develop soredia. Bulbothrix pustulata (US!, The holotype (Fig. 4) consists of six holotype, LG and O isotypes n.v.) differs by fragments in good condition on soft bark of the formation of pustules, which tend to remain roots from Notofagus obliqua (Mirb.) Oerst., intact, that occasionally could form rough with soralia on all of them. Although the granules by disintegration of the cortex, instead fragments are not glued to cardboard, most of of forming soralia with typical soredia grains. them are still attached to their substrate. The Bulbothrix pustulata is an emaculate species material is very brittle. The isotype is a large with larger ascospores, 9.0−14.0 × 6.0−8.0 µm. fragment, larger than those of the holotype, and Bulbothrix tabacina (L! lectotype, PC! under the same conditions, but partially glued duplicate) and B. isidiza (H-Nyl! holotype) to cardboard. Part of the isotype soralia were both differ by forming isidia instead of soredia, damaged (compressed) or with few soredia. the weaker maculae, a more continuous upper There are no apothecia or pycnidia in any of cortex, and larger ascospores ca. 12.0−16.0 × the type specimens fragments. 6.0−9.0 µm. Bulbothrix isidiza also differs by At early stages, the soralia in B. the pale brown colour of the lower cortex. imshaugii are somewhat similar to the pustular Bulbothrix meizospora (Nyl.) Hale (H- soralia found on specimens of B. leprieurii (U!, Nyl!, holotype) and B. hypocraea (TUR-V!, holotype), but they soon become flattened and lectotype, BM!, duplicate) both differ by spread over the upper cortex. Unlike those on forming only apothecia, a continuous upper B. leprieurii, the soralia of B. imshaugii do not cortex, and by their larger ascospores, erode until exposed, the medulla and the upper respectively 12.0−22.0 × 8.0−14.0 µm and portion of the lower cortex being more similar 8.0−14.0 × 6.0−8.0 µm. Thalli of B. hypocraea to those on Canoparmelia texana (Tuck.) Hale also differ by a pale brown lower cortex. & Elix, for example. The soredia of B. Bulbothrix setschwanensis (Zahlbr.) imshaugii are somewhat finer compared to Hale (WU!, lectotype) and B. sensibilis (J. those of B. leprieurii. The upper cortex of B. Steiner & Zahlbr.) Hale (W!, holotype) also imshaugii is strongly maculate, causing a differ by having a continuous upper cortex and whitish appearance to the herbarium by forming only apothecia, the first with specimens. There are many transverse cracks ascospores ca. 5.0 × 4.0 µm while the second on the specimens, specially at older parts or on has ascospores 8.0−12.0 × 6.0−8.0 µm. Thalli the more sorediate laciniae. of B. setschwanensis are also emaculate and Besides the more granular soredia have a pale brown lower cortex. formed at capitate or pustular soralia, that Hale (1971) compared B. imshaugii usually originate at the apical portions of the only to Parmelia brevirhiza Kurok. [= laciniae, Bulbothrix leprieurii also differs from Hypotrachyna brevirhiza (Kurok.) Hale], due B. imshaugii by the narrower emaculate the overall aspect and by the fact that both have laciniae (0.30.7 mm wide), and by the the same medullary substance salazinic acid. presence of medullary gyrophoric acid (main As cited by Hale, the species are 8
Mycosphere Doi 10.5943/mycosphere/4/1/1 distinguishable by the absence of marginal cilia Soredia and pustules absent. Isidia frequent, and by the formation of dichotomously laminal, granular to smooth cylindrical, straight branched rhizines in Hypotrachyna brevirhiza. to slighty tortuous, 0.050.20 (0.30) 0.050.10 (0.15) mm, simple to sometimes Bulbothrix isidiza (Nyl.) Hale. Phytologia sparsely branched, erect, occasionally firm but 28(5): 480. 1974. Figs 5−7 often caducous, concolorous and usually with Mycobank MB 341602 brownish apices when developed, eciliate. Basyonym Parmelia isidiza Nylander. Medulla white. Lower surface pale brown, Boletim da Sociedad Broteriana Coimbra 3: except for veins or a few occasional slightly 130. 1884. darker, randomly scattered parts, shiny, Synonyms Parmelia tiliacea var. smooth, veined, moderately rhizinate. Marginal hypoleuca Müller Argoviensis. Engler´s zone pale brown, indistinct or slightly darker Botanische Jahrbücher 20: 257. 1894. than the center, shiny, smooth, sligthly Parmelia gillettii Dodge. Annals of the rhizinate. Rhizines light to dark brown, Missouri Botanical Garden 46: 86. 1959. sometimes whitish or with whitish apices, Holotype Angola, Serra da Chella, simple, without or partially with subtle Arraial de Cayonda, ad cortices arborum lecta blackish basal bulbs, 0.050.70 ca. 0.030.05 praesertim in arbore Mopane dicta, leg. mm, frequent, becoming scarce when near to Newton s.n., V-1883, (H-Nyl!). the margins, evenly distributed. Apothecia Thallus subirregular to sublinear concave to subplane, adnate to substipiate, sublaciniate, ±pale dusky grey in herbarium, up 0.3−3.6 mm in diam., laminal, ecoronate, to 12.4 cm in diam., submembranaceous, margin smooth to subcrenate or subirregular corticolous (rarely saxicolous or on manmade and involute, amphithecia smooth eventually substrates), upper cortex 15.0−25.0 µm thick, becoming isidiate, the isidia frequently larger algal layer 27.5−37.5 µm thick, medulla and more branched than those found on the 75.0−115.5 µm thick, lower cortex 15.0−22.5 upper cortex. Disc brown to pale brown, µm thick. Laciniae irregularly to partially epruinose, imperforate, epithecium 10.020.0 anisotomic dichotomously branched, 1.45.3 m high, hymenium 35.0−57.5 µm high, mm wide, slightly imbricate, adnate and subhymenium 15.0−22.5 µm high. Ascospores ±adpressed, with flat, subrotund apices, the ellipsoid to oval, 10.0−16.0 (−17.5) × 5.0−9.0 margins flat, smooth to slightly sinuous, µm, epispore 0.5−1.0 µm. Pycnidia not found subcrenate or subirregular, entire, rarely (accordingly to Elix 1994 and Nash & Elix sublacinulate, the axils oval. Upper cortex 2002, the conidia are bacilliform to weakly usually continuous with occasional irregular bifusiform, 5.06.0 1.0 µm). cracks, smooth to subrugose, laminal ciliar TLC/HPLC − cortical atranorin and bulbs absent. Adventitious marginal lacinulae chloroatranorin, medullar salazinic and absent to scarce on random parts, short, 0.2 consalazinic acids (see also Hale 1976, Elix 0.6 0.1–0.4 mm, plane, simple, apices 1994, Nash & Elix 2002). truncate to subtruncate, lower side concolorous Distribution − Oceania and North Pacific: to the lower marginal zone. Maculae weak, Australia (Elix 1994), Fiji Islands (Elix 2001), moderate or distinct, punctiform, laminal or in Cook Islands, Rarotonga (Louwhoff & Elix the amphithecia of the apothecia. Cilia black to 2002), Hawaii (Hale 1976), Papua New Guinea dark brown, apices simple to absent, often bent (Streimann 1986, Elix 1994), Tahiti (Hale downwards, 0.050.10 (0.15) ca. 0.03 mm, 1976). Asia: China (Wu et al. 1986), with semi- immerse to sessile bulbate bases ca. Philippines (Hale 1976), India (Hale 1976, 0.050.10 mm wide, scarce to frequent and Kumar & Siquiera 2001, Divakar & Upreti irregularly distributed along the margins but 2005), Indonesia (Hale 1976), Japan (Hale becoming frequent at the crenae and axils, 1976), Malaysia (Hale 1976, Din et al. 2004), spaced 0.50.20 mm from each other, usually Nepal, (Hale 1976, Kurokawa 1993), Thailand absent or scarce on the apices of the laciniae. (Wolseley & Aguirre-Hudson 1997), Taiwan
9
Mycosphere Doi 10.5943/mycosphere/4/1/1 (Kurokawa & Lai 2001). África: South Africa County, near Geneva, along Fla. 46, White (Hale 1976), Angola (Dodge 1959, Hale 1976, sand scrub, on limbs of Pinus clausa, leg. Nylander 1884, Vainio 1901), Ivory Coast B.J.Moore 2653, 26-XII-1965 (DUKE); idem, (Hale 1976), Ethiopia (Swinscow & Krog Hawaii, Maui, Puu Kukui, mossy Forest to 1988), Guinea, Malawi, Kenia, Tanzania, alpine bog, 4300-5500 ft., trail from cabin to Uganda (Hale 1976, Swinscow & Krog 1988, summit, leg. M.E. Hale 31247, VII-1965 (US). Krog 2000), Ruwanda (Killmann & Fischer Mexico, Chiapas, 2 km north of highway 190 2005, Bock et al. 2007), Tanzania (Müller on road to Puebla Nueva, west of Chiapas, Argoviensis 1894, as the synonym P. tiliacea 1070 m, pine pasture, on conifers, 23-III-1960, var. hypoleuca) Somalia (Dodge 1959, as the leg. M.E. Hale & T.R. Soderstrom 20170 (US). synonym P. gillettii), Zaire, Zambia, Brazil, Pará, Serra do Cachimbo, 842 km N of Zimbabwe (former Rhodesia) (Dodge 1959, Cuiabá on Mato Grosso on Cuiabá-Santarém Hale 1976). North America: United States of highway (BR-163), ca. 8º45’S, 54º57’W, ca. America, (Dey 1987, Harris 1987, Brodo et al. 350-500m, mature Forest along stream on 2001, Nash & Elix 2002), Mexico (Hale 1976, sandy soil with deep humus and roadbank Nash & Elix 2002). Central America: vegetation, on roadside Solanaceae, leg. Brako Guatemala (Hale 1976). South America: Chile & Dibben 6709, 5-V-1983 (NY); idem, São (Galloway & Quilhot 1998), Paraguay (Hale Paulo, Campo Limpo Paulista Municipality, on 1976), Venezuela (López-Figueiras 1986, hillside near the Botujuru railway station, on Marcano et al. 1996) and Brazil – Mato Grosso tree trunk, leg. M.P. Marcelli & A.E. Luchi do Sul, (Fleig & Riquelme 1991), Pará (Brako 2888, 13-VI-1980 (SP); idem, Itirapina et al. 1985), Paraná (Eliasaro 2001), Rio de Municipality, Experimental Station Janeiro (Hale 1976), Rio Grande do Sul (Fleig (Pedregulho) at the Instituto Florestal, 780 m & Grüninger 2000a, 2000b), and São Paulo alt., 22º14’32”S, 47º49’48”W, on tree trunk in (Hale 1976, Pereira & Marcelli 1989, Marcelli the open between pine and cerrado (savannah) 1990, 1993). vegetation, leg. L.S. Canêz, P. Jungbluth & Additional selected specimens A.A. Spielmann 1214, 24-III-2004 (SP); idem, examined − Australia, Queensland, dividing São Carlos Municipality, Universidade Federal range, few miles east of Atherton, E. Dahl s.n., de São Carlos (UFSCar) Campus, cerrado 15-VII-1970 (MEL). Philippines, Luzon, Prov. (savannah) area, 22o1’S, 47o53’W, alt. 855 m, Benguet, Mt. St. Tomas, exposed rocks near on small tree trunk near a firebreak, leg. M.N. the road, 1560 m, leg. G. Degelius As-900, 18- Benatti & G.G. Batista 2150, 4-IX-2006 IV-1964 (US). India, Karnataka, Humcha- (HUFSCAr); idem, São Paulo Municipality, Sagar Road, thorn Forest-pasture, ca. 600 m, Parque Estadual das Fontes do Ipiranga, leg. M.E. Hale 48010, 01-III-1977 (US). Instituto de Botânica, on palm trunk, leg. M.P. Malaysia, Pahang, Robinsons Waterfall near Marcelli & S.A.D. Andrade 34701, 24-VIII- Tanah Rata, leg. M.E. Hale 33702, 03-III-1965 2000 (SP); idem, Serra Negra Municipality, (US). Somalia, Libah Mele Mt., 1675 m (5200 Vale do Sol, near the km 12 of Serra Negra- ft.), above Buja Soldan, 10º20´N, 43oE, on Lindóia Highway, on ceramic tiles of the roofs twigs of Grewia sp.?, leg. J.B. Gillett 4699 pro of the cottages of the hotel, leg. M.P. Marcelli, parte, 3-XII-1932, (BM!, holotype of Parmelia O. Yano & A.B. Carvalho 22996, 4-IV-1993 gillettii). Tanzania, Ufipa, Chapota, 6500 ft., (SP). over roots of Polystachya on Brachystegia, leg. Comments − The holotype (Fig. 5) is a A.A. Bullock 2035 p.min.p., 11-XII-1949 small fragment not in a very good condition, (BM); idem, Usambara, auf Rinde, leg. Holst glued to cardboard and severely damaged (it 787 pro parte (G!, lectotype of Parmelia was necessary to remove part of the fragment tiliacea var. hypoleuca). Uganda, East Mengo, from the card to observe the lower cortex). It Bulemezi, near Kakinzi School, 0o57’N, contains two apothecia in good condition and a 32o28’E, 1100 m, on lage tree branches, leg. small part of a third apothecium, probably used K.A. Lye VS-41-04 L206, X-1969 (US). by Nylander to study the hymenium and United States of America, Florida, Seminole ascospores. The material contains several 10
Mycosphere Doi 10.5943/mycosphere/4/1/1 isidia, including in the apothecia. Ascospores with very wide laciniae (1.210.0 mm wide), are also in good condition. deeply divided, crenate and with truncate Hale (1976), Swinscow & Krog (1988) apices, with 1 mm long cilia. All other and Kurokawa & Lai (2001) mentioned that it characters, however, fit quite well. Nash & is particularly common in Africa, but as Elix (2002) mention isidia that are simple to demonstrated here it is also frequent in the coralloid in the specimens that they studied. Neotropics. Hale (1976) also corrected that the This is somewhat unusual for the genus, but specimen cited by Des Abbeys (1961) for otherwise their description agrees well with the Madagascar was actually of Parmelinella observations presented here. Divakar & Upreti wallichiana (Taylor) Elix & Hale. (2005) described the thalli as emaculate to The upper cortex of B. isidiza is usually weakly maculate, with simple to rarely rugose, somewhat different from other species coralloid, very tall isidia (up to 1.0 mm). They in the genus, giving the thalli a rough mentioned rhizines also larger than normally appearance, as described by Nylander (1884), found (1.01.5 mm long). Measurements of Hale (1976) and Ribeiro (1998). Besides the laciniae given in their key and in their roughness of the upper cortex, all these authors description are contradictory: in the key they also mentioned another easily observed feature are given as 2.06.0 (10.0) mm wide, in the in the specimens, including in the holotype, of description as 1.05.0 mm wide. Jungbluth the very delicate and small isidia. The (2006) also suggests that the cilia are longer apothecia are ecoronate, usually flat and (1.251.8 mm) and that the isidia are taller (up adnate, like in all other Bulbothrix species with to 0.5 mm) than can be confirmed here. medullar salazinic acid. Eliasaro (2001) commented Nylander (1884) did not notice the sporadically finding norstictic acid in her bulbate marginal cilia. He described the material of B. isidiza and of B. hypocraea. This ascospores, which also appear on a label substance is unusual and it may only included with the type material as ellipsoid, sporadically occur in the specimens, or could 9.012.0 6.08.0 m, although those be ascribed to contamination of the specimens observed in the holotype are somewhat larger, she examined. It cannot be confirmed for any 10.015.0 5.09.0 m. The larger spore specimen examined here, in no specimen the dimensions were also cited by Kurokawa & Lai formation of the characteristic norstictic (2001). Nash & Elix (2002) and Hale (1976) microcrystals could be observed nor was it described the ascospores as ellipsoid, 7.014.0 possible to observe norstictic acid by 5.08.0 µm. Swinscow & Krog (1988), Elix TLC/HPLC. A label from Patricia Wolseley (1994) and Marcelli (1993) also described the with the holotype of Parmelia gilletti Dodge ascospores as ellipsoid, but of slightly different also suggests that the material contains both dimensions, 10.0−16.0 × 6.0−8.0 µm, and more norstictic and salazinic acids, but the specimen in accordance to the general average sizes is morphologically indistinguishable from obsverved here. Ascospores 6.0−10.0 × typical B. isidiza and both her report and that 5.0−8.0 µm were found to be typical for B. of Eliasaro of norstictic acid in the material subglandulifera (see below), once accepted as cannot be confirmed here. a synonym of B. isidiza by Hale (1976). Hale (1976), Swinscow & Krog (1988), A few descriptions in the literature Elix (1994), Kurokawa & Lai (2001) and mention characters that cannot be considered Divakar & Upreti (2005) all mentioned that B. typical. Contrary to that observed here, Dodge isidiza can be found corticolous as well as (1959) described specimens of B. isidiza with a saxicolous. As seen from the material cited black lower cortex as likely to be related to B. here, such indifference to the substrate must be tabacina. The author noted marginal cilia, considered fairly unusual for the genus which he described as up to 1 mm long and Bulbothrix. Most species in the genus appear to spaced 1 mm from each other, but he did not be quite substrate specific. Nevertheless, mention the presence of basal bulbs. Swinscow Divakar & Upreti (2005) also mention that B. & Krog (1988) described B. isidiza specimens isidiza is rarely found on soil. 11
Mycosphere Doi 10.5943/mycosphere/4/1/1 Hale (1976) suspected that B. and apparently he did not notice the cilia, hypocraea could be the parental form of B. because in his key P. gillettii is mentioned isidiza, which is plausible given the among the eciliate species. Dodge gives larger morphological and chemical similarities of ascospores measurments in his key than those these two species. The presence of very mentioned in the description (18.5 × 8.0 µm), conspicuous, punctiform maculae on most and he calls the colour reaction in his key K + thalli, the ecoronate apothecia, the lower cortex yellow to reddish orange, which is the colour colour, the colour and shape of the cilia and reaction typically give for norstictic acid (the rhizines and the size of ascospores are all very specimen does, however, contain salazinic similar. acid, as confirmed here by HPLC). An Regarding the synonyms, Hale (1976) annotation label of the holotype by Hale reads suggested that P. tiliacea var. hypoleuca that he suspected that this specimen belongs to Müller Argoviensis (1894), given by Dodge Parmelia sublaevigatoides, but Hale (1976) (1959) as a synonym of Parmelia lythogeana latter confirmed that P. gillettii should be (= Hypotrachyna lythogeana), must actually be considered a synonym of B. isidiza and instead considered a synonym of B. isidiza instead. P. sublaevigatoides is synonymous with B. This is clearly a misunderstanding by Dodge. tabacina. when he studied the type material of P. Among the similar species, Bulbothrix lythogeana, he might not have observed that tabacina Hale (L! lectotype, PC! duplicate) is this species is not isidiate. The type collection the species most frequently compared to B. of P. tiliacea var. hypoleuca (Fig. 7) is poor, isidiza, differentiated only by the colour of the consisting of mixed thalli of two Bulbothrix lower cortex, which is black with partially species. One is a fragment containing few brown margins. The presence of consalazinic isidia and lacking apothecia; this specimen acid as a accessory substance was pointed out fragment is abundantly maculate, it belongs to by Divakar & Upreti (2005) as another Bulbothrix isidiza and this specimen was difference. chosen here as the lectotype. The width of the Ribeiro (1998), Eliasaro (2001) and laciniae in the lectotype specimen of P. tiliacea Jungbluth (2006) compared Bulbothrix var. hypoleuca is half of the width typical of ventricosa (TUR-V! lectotype) with B. isidiza. the holotype of B. isidiza, and it has more Bulbothrix ventricosa is distinguished by the subcrenate margins with mainly axillary cilia. variable colour of its lower cortex, more However, since this is only a very small abundant cilia, coronate apothecia, frequent specimen, and because the characters are development of laminal ciliar bulbs, and by the overall very similar, this taxon is not presence of medullary norstictic acid (Benatti considered a seperate species here. The other 2012a). fragment in the packet of the type material is Saxicolous specimens of B. isidiza are even smaller, much damaged, heavily similar to those of B. cinerea, due the laciniae parasitized, and it is uncertain to which species aspect, isidiate thalli, simple cilia and rhizines this fragment belongs. It has no maculae, it is and by the brown lower cortex. However, B. paler, has partially bulbate cilia and does not cinerea has a more greyish colour, generally have propagules or apothecia. Finally, this larger isidia with darkened apices, rhizines fragment contains norstictic acid unlike all often with bulbate bases, coronate apothecia other specimens examined here. and it contains norstictic acid in the medulla. The holotype (Fig. 6) of Parmelia Bulbothrix australiensis (US! Holotype, gillettii Dodge (1959) shows virtually no MEL isotype n.v.) was compared to B. isidiza differences compard to the type material of B. by Elix (1994). As seen, it differs by the isidiza. The main characteristics are all present, narrower and sublinear laciniae 0.5−2.0 mm including the typical width of its laciniae, the wide and by the emaculate upper cortex. The cilia, the maculae, the lower cortex colour and isidia of B. australiensis are usually much venation, non-bulbate rhizines, and the size of larger than those seen in specimens of B. ascospores. Dodge (1959) made no comments, isidiza, often up to 1.0 mm high. 12
Mycosphere Doi 10.5943/mycosphere/4/1/1 Bulbothrix subglandulifera (PC!, dense at a few random parts, ± evenly holotype) differs by much narrower laciniae distributed. Apothecia and pycnidia not found. 0.1−0.7 mm in width, frequently branched TLC/HPLC − cortical atranorin and isidia, some with small basal bulbs, rhizines chloroatranorin, medullar salazinic and with distinct readily apparent basal bulbs and consalazinic acids (see also Elix 1993b, 1994). by the smaller ascospores, which usually Distribution − Oceania: Australia (Elix measure 6.0−10.0 × 5.0−8.0 µm (see the 1993b, 1994). detailed description that follows). Comments − The holotype (Fig. 8) consists of a small thallus that is almost intact, Bulbothrix microscopica Elix. Mycotaxon 47: in excellent condition. It adheres to tree bark, 102. 1993. Fig. 8 which is glued to cardboard and for this study Mycobank: MB 360108 it was necessary to remove part of it from the Holotype − Australia, Queensland, Tin substrate to determine the colour of the lower Can Bay, along the foreshore of Tin Can Inlet, cortex; the piece removed was subsequently 25o54’S, 153o01’E, 1 m alt., strand vegetation, glued back onto the cardboard, along the on Rhizophora stylosa, J.A. Elix 22862, 3-VII- thallus to facilitate that other researchers can 1989 (CANB!). examine the cortex more easily. Apothecia, Thallus sublinear laciniate, dusky ascospores and conidia are still unknown for greenish grey in herbarium, up to 2.3 cm in the species. diam., submembranaceous, corticolous, upper Bulbothrix microscopica is one of the cortex 10.0−15.0 µm thick, algal layer smallest species of the genus, with very narrow 12.5−17.5 µm thick, medulla 25.0−32.5 µm laciniae, unlikely to exceed 0.5 mm wide. All thick, lower cortex 15.0−20.0 µm thick. features observed in the holotype are in Laciniae anisotomic dichotomously branched, agreement with the descriptions of Elix (1993b, 0.10.5 (0.7) mm wide, contiguous, adnate 1994), except for the colour of the lower and adpressed, with flat, truncate apices, the cortex, described as black, but which is margins flat, smooth to sinuous, entire, not actually dark brown, with margins paler than sublacinulate, the axils oval. Upper cortex the center. Due to the narrow space between smooth and continuous, laminal ciliar bulbs the internodes of the laciniae and to the narrow absent. Adventitious marginal lacinulae absent. size of these, the cilia, that are in reality Maculae absent. Cilia black, apices simple, axillary, as commonly occurs in Bulbothrix often bent downwards, 0.05–0.25 (−0.60) species with medullary salazinic acid, 0.02−0.03 mm, with sessile bulbate bases eventually cover almost the entire margin with 0.050.10 mm wide, frequent to abundant the exception only of the apices of the laciniae. along the margins spaced ca. 0.05 mm from Elix (1993b, 1994) compared B. each other to contiguous, becoming absent or microscopica to B. subtabacina (MEL! scarce at the apices of the laciniae. Soredia and holotype, CANB! isotype). As seen here, this pustules absent. Isidia frequent to abundant, species differs by wider laciniae (ca. 0.5−1.5 laminal, granular to smooth cylindrical, mm), strongly cracked and maculate upper straight, 0.050.15(0.25) ca. 0.05 mm, cortex, ciliate isidia, crenate margins, branched simple, erect, firm, concolorous or with cilia and rhizines and by the almost uniformly brownish apices, eciliate. Medulla white. black lower cortex. Lower cortex dark brown, shiny, smooth, Among the larger similar species, moderately rhizinate. Marginally brown, paler Bulbothrix tabacina (L! lectotype, PC! than in the center, attenuated, 0.2−0.7 mm duplicate) differs by wider, subirregular wide, shiny, smooth, weakly rhizinate. laciniae (1.5−5.5 mm) with rounded apices and Rhizines dark brown to black, simple, usually crenate margins, maculate upper cortex, and by without basal or displaced bulbs (some few a black lower cortex with brown margins. appear to have subtle bulbs), 0.100.30 ca. Bulbothrix isidiza (H-Nyl! holotype) also 0.03 mm, frequent, usually sparse leaving the differs by wider subirregular laciniae (2.0−5.5 lower cortex visible but occasionally more mm) with rounded apices, rugose and maculate 13
Mycosphere Doi 10.5943/mycosphere/4/1/1
Figs 4–11 – 4 Holotype of Bulbothrix imshaugii (MSC). 5 Holotype of Bulbothrix isidiza (H-Nyl). 6 Holotype of Parmelia gillettii (BM). 7 Holotype of Parmelia tiliacea var. hypoleuca (G). 8 Holotype of Bulbothrix microscopica (CANB). Scale bars = 1 cm (4, 5, 6, 7, 8). 14
Mycosphere Doi 10.5943/mycosphere/4/1/1 upper cortex, and by a light brown lower cortex ca. 0.10 (−0.15) mm wide, scarce along the with brown rhizines. margins becoming frequent at the crenae and Most closely related is another small axils spaced ca. 0.05−0.10 mm from each species, Bulbothrix australiensis (US! other, solitary or in small groups becoming Holotype, MEL isotype n.v.) which has slightly absent at the apices and adjacent parts of the wider sublinear laciniae (0.5−2.0 mm), laciniae. Soredia and isidia absent. Pustules in elongated and eventually branched isidia that the form of irregular wrinkles or twisted and are often more than 1.0 mm tall; it also has a villous dactyloid structures, laminal, intact or pale brown lower cortex and rhizines with dark erumpent, sometimes disintegrating into coarse basal bulbs. Bulbothrix linteolocarpa Marcelli granules. Medulla white. Lower cortex black, (SP!, holotype) is also similar to B. with random dark brown spots at the transition microscopica due its narrow laciniae (ca. for the center, shiny, smooth to subrugose, 0.2−0.5 mm wide), emaculate upper cortex, weakly papillate, moderately rhizinate. sinuous and frequently ciliate margins, and Marginal zone brown, attenuated, ca. 1.0−6.0 medullar salazinic acid. However, unlike B. mm wide, shiny, smooth to subrugose, microscopica, it is not isidiate, and its cilia and papillate becoming rhizinate in the ransition for rhizines vary from simple to furcate, the the center. Rhizines black, simple to rhizines always developing from basal bulbs. occasionally furcate, without basal or displaced bulbs, 0.100.40 ca. 0.04 mm, usually Bulbothrix pustulata (Hale) Hale. Phytologia frequent but scarcer when near the margins, 28(5): 480. 1974. Figs 9−10. evenly distributed. Apothecia concave, adnate, Mycobank MB 341608 0.3−1.7 mm in diam., laminal, ecoronate, Basyonym − Parmelia pustulata Hale. margin smooth, amphithecia initially smooth Contributions from the United States National becoming subrugose and pustulate. Disc Herbarium 43: 140. 1964. brown, epruinose, imperforate, epithecium Holotype − Burundi, Ngozi, bamboo- 10.012.5 µm high, hymenium 37.5−55.5 µm thickets, 2100 m, on bamboo, leg. Deuse s.n. high, subhymenium 25.0−30.0 µm high. (US!, isotypes at LG and O nv.). Ascospores ellipsoid to oval, 9.0−14.0 × Thallus subirregular sublaciniate, dusky 6.0−8.0 µm, epispore ca. 1.0 µm. Pycnidia not grey in herbarium, fragments up to 9.3 cm in found. diam., fragile membranaceous, corticolous, TLC/HPLC − cortical atranorin, upper cortex 7.5−12.5 µm thick, algal layer medullar salazinic acid (see also Hale & 20.0−32.5 µm thick, medulla 100.0−125.0 µm Kurokawa 1964, Hale 1976, Sérusiaux 1984). thick, lower cortex 5.0−10.0 µm thick. Distribution − Africa: Burundi (Hale & Laciniae irregularly to occasionally Kurokawa 1964, Hale 1976, Sérusiaux 1984), ±anisotomic dichotomously branched, (1.5−) Rwanda (Sérusiaux 1984, Bock et al. 2007), 2.65.5 mm wide, imbricate becoming Tanzania (Krog 2000). crowded at the center, weakly adnate and Comments − The holotype (Fig. 9) is loosely adpressed, with flat, subrotund to fragmented, with various parts heavily subtruncate apices, the margins flat, smooth to damaged, but overall nevertheless reasonably crenate or occasionally irregular, entire to preserved. Several sections of the margins and slightly incised, not sublacinulate, the axils apices of laciniae are so damaged that it is oval to irregular. Upper cortex smooth to difficult to find any bulbate cilia, although subrugose, usually with many irregular cracks these are present. Despite the poor condition of that eventually become more accentuated at the the material, the pustules are easily noticed. older parts, sometimes flaking off the cortex, Although not cited in the protologue of laminal ciliar bulbs absent. Adventitious the species, Sérusiaux (1984) mentioned three marginal lacinulae absent. Maculae absent. isotypes, one in LG, the other in O, and another Cilia black, apices simple or occasionally in the Follmann herbarium, those unfortunately double, and short and curved, 0.05–0.25 (– could not be located or obtained on loan. 0.40) ca. 0.03 mm, with sessile bulbate bases According to Sérusiaux (1984), the type 15
Mycosphere Doi 10.5943/mycosphere/4/1/1 material of B. pustulata was collected in 1958 Sérusiaux (1984) referred to the by P. Deuse, a Belgian botanist working in pustules of B. pustulata as dactyls in the sense Rwanda and Burundi. The chemistry was of Swinscow & Krog (1978). However, the studied by Ramaut (1965 in Sérusiaux 1984), publication by Swinscow & Krog (1978) and the material sent to M.E. Hale. Sérusiaux focuses on Dirinaria (Tuck.) Clem. a genus in (1984) mentioned that the collection at LG was the Physciaceae and the structures observed in large and that the material was divided into Parmeliaceae may in fact not be identical to isotypes, subsequently sent to the O and those of the Physciaceae. Here, the term Follmann herbaria, though Hale (1964) and “dactyls” as used by Swinscow & Krog (1988) Hale & Kurokawa (1976) did not make any is considered inappropriate for structures mention of isotypes, perhaps unaware of their observed in B. pustulata. The term pustule existence. Hale concluded that the species appears more adequate because these structures should be really rare, noting that J. Lambinon, do not fit well the definition of “a nodular to who collected much in the region, found only cylindrical to clavate body, somewhat one other poor specimen, and a few kilometers resembling a swollen isidium...”. from the type locality, on the same substrate: Among other large laciniate Bulbothrix bamboo stalks in secondary woods inside species containing medullary salazinic acid, B. forests in mountainous regions. tabacina (L! lectotype, PC! duplicate) was This is one of the only two Bulbothrix compared to B. pustulata by Hale & Kurokawa species which are known to form pustules, the (1964), and as seen it differs by the continuous, other being B. oliveirae A. Fletcher. Agreeing smooth and maculate cortex, and by the with general observances of Hale & Kurokawa formation of simple laminal isidia rather than (1964), Hale (1976) and Sérusiaux (1984), the pustules. Bulbothrix meizospora (Nyl.) Hale thallus of B. pustulata is membranaceous, (H-Nyl! holotype) differs by the absence of brittle and rough, with the upper cortex easily pustules or vegetative propagation, and by the flaking off, the irregular subrotund laciniae has larger ascospores 12.022.0 9.012.0 µm. wide inconspicuously ciliate crenae, and the Bulbothrix isidiza (H-Nyl! holotype) differs by inflated pustules have an irregular appearance the maculate subrugose cortex, by the or are sometimes similar to isidioid dactyls, formation of simple or sparsely branched small breaking apically, but not forming true soredia isidia, and by the pale brown lower cortex with (Fig. 10). brown rhizines. Bulbothrix hypocraea (TUR- Hale & Kurokawa (1964) did not V! lectotype, BM! duplicate) differs by the mention apothecia on the original description, smooth and maculate upper cortex, light brown but latter Hale (1976) mentioned rudimentary lower cortex with brown, bulbate rhizines, and sessile apothecia, up to 1.5 mm in diam., by the absence of vegetative propagules or however he did not find ascospores. Sérusiaux pustules. (1984) mentioned some adnate apothecia, up to As previously stated, Bulbothrix 2 mm in diam., for the LG isotype, with eroded oliveirae (NY!, holotype) is the only other margins and brown discs, containing ellipsoid species in the genus that form pustules. It ascospores 14.0−16.0 × 8.0 to 9.0 µm. The differs from B. pustulata by more narrow, apothecia in the holotype are few in number, sublinear laciniae (ca. 0.5−1.0 mm wide), but the more developed ones contain asci with smooth upper cortex, dichotomously branched mature ascospores. As seen, the size of the cilia and rhizines, and by the presence of ascospores are slightly smaller than those medullary gyrophoric acid as main substance. mentioned by Sérusiaux (1984) and similar to In direct comparison, the pustules of B. those of B. tabacina, which looks like B. oliveirae are more rounded, like smooth pustulata in morphology and chemistry, and "bubbles" or "pellets". When these “pellets” with that it must somehow be related, as break off, the thallus becomes deeply eroded supposed by Hale (1976). There are no exposing thus even its lower cortex, which in pycnidia in the holotype of B. pustulata. turn appears covered by granules, fragments
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Mycosphere Doi 10.5943/mycosphere/4/1/1 derived from the breakdown of the cortex due becoming absent or scarce at the apices of the to the erosion of the “pellets”. In B. pustulata laciniae. Soredia and pustules absent. Isidia these structures are more “uplifted”, abundant, laminal, granular to smooth occasionally resembling very rough and cylindrical, straight to slightly tortuous, retorted actyls. They are in fact are similar to 0.050.30 ca. 0.05 mm, simple to often those seen in specimens of Parmotrema branched, erect to procumbent, firm to madilynae Fletcher and thalli of B. pustulata caducous, concolorous or with brownish may resemble to some extend very small thalli apices, partially ciliate with small bulbs. of P. madylinae, even though this species has Medulla white. Lower surface pale brown, bulbate cilia and contains different medullary sometimes slightly darker at a few random substances. Unlike the pustules of B. oliveirae, parts, shiny, smooth to subrugose, weakly to those of B. pustulata do not erode quite as moderately rhizinate. Marginal zone brown deeply, thus not leaving the cortex lower indistinct from the center to sometimes slightly exposed. darker, shiny, smooth, weakly rhizinate. Rhizines pale to dark brown, simple, usually Bulbothrix subglandulifera (Hue) Hale. with bulbate bases, 0.100.70 0.030.05 mm, Phytologia 28(5): 481. 1974. Fig. 11 frequent becoming scarcer near the margins, Mycobank MB 341616 evenly distributed. Apothecia concave, adnate Basionym − Parmelia subglandulifera to subpedicellate, 0.3−2.6 mm in diam., Hue. Nouvelles Archives du Muséum Paris, laminal, ecoronate, margin subcrenate to série 3(1): 144. 1899. Holotype: Madagascar, revolute, amphitecia smooth sometimes in littore occidental, corticolam, leg. Grandidier becoming weakly isidiate. Disc dark brown, s.n. (PC!). epruinose, imperforate, epithecium 10.015.0 Thallus sublinear laciniate, pale dusky m high, hymenium 60.0−75.0 µm high, grey in herbarium, up to 2.5 cm in diam., subhymenium 40.0−50.0 µm high. Ascospores subcoriaceous, corticicolous, upper cortex rounded to ellipsoid or oval, 6.0−10.0 (−11.0) 17.5−22.5 µm thick, algal layer 20.0−32.5 µm × 5.0−7.0 (−8.0) µm, epispore 0.5−1.0 (−1.5) thick, medulla 95.5−120.0 µm thick, lower µm. Pycnidia laminal, scarcet, immerse, with cortex 17.5−20.0 µm thick. Laciniae black ostioles. Conidia bacilliform to weakly anisotomic dichotomously to irregularly bifusiform 5.0−7.0 × ca. 0.75 µm. branched, contiguous to slightly imbricate, TLC/HPLC − cortical atranorin, 0.41.3 (1.9) mm wide, adnate and adpressed, medullary salazinic acid (see also Hale 1976). with flat, subtruncate to truncate apices, the Distribution − Africa: Madagascar margins flat, slightly sinuous to crenate or (Hue 1899). subirregular, entire to slightly incised, Additional specimen examined − occasionally sublacinulate, the axils oval or Madagascar, côte ouest, leg. Grandidier s.n. irregular. Upper cortex smooth and continuous, (PC). occasionally with a few irregularly cracks, Comments − The holotype (Fig. 11) is a laminal ciliar bulbs absent. Adventitious much fragmented thallus on pieces of bark. It is marginal lacinulae scarce on random parts, reasonably preserved, although several parts of short, 0.20.8 0.10.2 mm, plane, simple to the laciniae are damaged, and the medulla is irregularly branched, apices truncate or acute, stained by oxidized salazinic acid. There is a lower side concolorous to the lower marginal large amount of isidia covering parts of the zone. Maculae weak to distinct, punctiform, cortex, and some apothecia in good condition laminal. Cilia black to brown, apices simple or containing mature ascospores. The material has absent, 0.05–0.40 ca. 0.03−0.05 mm, with only a few pycnidia, nevertheless these contain sessile bulbate bases 0.050.20 mm wide, conidia. frequent along the margins but more abundant Hue (1899) mentions that B. at the crenae and axils spaced ca. 0.05 mm subglandulifera can be characterized by isidia from each other eventually becoming that eventually became soredioid. The material contiguous, solitary or in small groups studied here shows granular isidia with some 17
Mycosphere Doi 10.5943/mycosphere/4/1/1
Figs 9–11 – Holotype of Bulbothrix pustulata (US). 10 Detail of the upper cortex of the holotype. 11 Holotype of Bulbothrix subglandulifera (PC). Scale bars= 1 cm (9, 10), and 5 mm (11).
18
Mycosphere Doi 10.5943/mycosphere/4/1/1 similarity to soredia, but these are nevertheless slightly branched isidia, an usually pale brown young and still poorly developed true isidia and lower cortex, brown simple rhizines with basal even the largest isidia always remain corticate; or displaced bulbs, and by the presence of they do not become sorediate. The "marginal medullary salazinic acid. For description and dark glands" mentioned by Hue (1899) are in comments on this species and some other fact bulbate bases of cilia, which have not yet recent combinations, see Benatti 2012b. apically differentiated into distinct cilia. Contrary to what Hue (1899) observed the Bulbothrix subtabacina (Elix) Elix. unusually large measurments of the laciniae Mycotaxon 47: 127. 1993. Fig. 12 can also not be confirmed here, as he gave MB 360133 measurements approximately three times the Basionym – Parmelia subtabacina Elix. width seen here. Australian Journal of Botany 27: 875. 1979. The species was treated as a synonym Holotype – On tree in pocket of of B. isidiza by Hale (1976). However, among rainforest, Long Beach, 3 km east of Batemans the synonyms, it is unique in having ascospores Bay, New South Wales, Australia, 3542’S, usually smaller than 10 µm (quite uncommon 15013’E, alt. 6 m., 19-III-1977, leg. J.A. Elix for the salazinic group), besides other 2951 (MEL!, isotype at CANB!). apparently constant differences. Bulbothrix Thallus sublinear laciniate, dark dusky isidiza (H-Nyl! holotype) differs by the wider greenish grey in herbarium, up to 4.5 cm in subirregular laciniae (ca. 1.5−5.0 mm wide) diam., submembranaceous, corticolous, upper with rounded apices, generally simple isidia, cortex 7.5−10.0 µm thick, algal layer rhizines without bulbate bases, and larger 10.0−15.0 µm thick, medulla 32.5−50.0 µm ascospores, usually 11.0−16.0 × 5.0−9.0 µm. thick, lower cortex 5.0−7.5 µm thick. Laciniae Among other species, Bulbothrix anisotomic dichotomously to ±irregularly australiensis is somewhat similar to B. branched, contiguous to slightly imbricate, subglandulifera, however differs by the 0.41.1 (1.5) mm wide, adnate and adpressed, emaculate thallus, usually simple and larger with subplane, subtruncate to truncate apices, isidia (0.5−1.0 mm high), and by the darker the margins flat, smooth and sinuous to brown colour of the lower cortex. Bulbothrix partially subirregular, entire to slightly incised, cinerea (Kalb pers. herb!, holotype) has a occasionally sublacinulate, the axils oval or similar pale brown lower cortex and rhizines irregular. Upper cortex smooth, almost entirely with dark bulbate bases, but differs by its irregularly cracked (most commmon at the saxicolous habit, coriaceous, dark and center) except by the distal parts, laminal ciliar emaculate thallus, generally simple (sometimes bulbs absent. Adventitious marginal lacinulae dilated or lobulated) isidia, the ascospores scarce and occasional, short, 0.20.3 ca. 0.1 10.0−14.0 × 6.0−8.5 µm, and by the presence mm, plane, simple, apices truncate, lower side of medullary norstictic acid. concolorous with the lower marginal zone. Maculae weak to distinct, easily visible at the Bulbotrix subscortea (Asahina) Marcelli & distal parts, punctiform, laminal. Cilia black to Benatti. Mycosphere 3(1): 48. 2012. brown, apices initially simple becoming furcate Mycobank MB 519638 and finally dichotomously branched, 0.05–0.25 Basionym – Parmelia subscortea ca. 0.03−0.04 mm, with semi-immerse to Asahina. Journal of Japanese Botany 32: 99. sessile bulbate bases 0.050.10 mm wide, 1957. abundant along the margins spaced 0.05−0.10 Holotype – Taiwan, Keitau, saxicolous, mm from each other, becoming absent or leg. Y. Asahina 3324, 24-XII-1933 (TNS!). scarce at the apices of the laciniae. Soredia and For image see Benatti (2012b) Pustulespustules absent (parts where there are Bulbothrix subscortea is characterized much detachment of isidia expose the medulla by the broad (ca. 1.0–5.5 mm wide) subirregular in a way similar to that of rudimentary soralia). laciniae, emaculate upper cortex, frequent Isidia abundant, laminal, granular or smooth marginal cilia with simple apices, simple to cylindrical, straight to tortuous, 0.050.15 19
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(0.25) ca. 0.05 mm, simple to slightly that they end up masking the true maculae. branched, occasionally aggregate, erect, firm to Because of this, the maculae are often more caducous, concolorous to the upper cortex, easily seen in the distal portions of the laciniae, commonly ciliate. Medulla white. Lower where isidia are few or absent. surface black, with small dark brown spots, The isidia apparently detach in large shiny, smooth, moderately rhizinate. Marginal quantities as small blocks, leaving deep marks zone variable, black and indistinct from the in the upper cortex, essentially causing the center to brown and attenuated 0.5−1.5 mm thallus to be covered in small holes. wide, shiny, smooth, rhizinate. Rhizines black, Eventually, these marks are large enough to initially simple soon becoming furcate and then expose medullary hyphae, in appearance dichotomously or irregularly branched, without somewhat similar to pseudocyphellae seen in bulbate bases (some have a slight swelling, but Punctelia species but also resembling eroded it is uncertain if that are very subtle bulbs), soralia (true soredia, however, were not seen in 0.100.50 ca. 0.03 mm, ± sparse leaving the any part). The isidia of B. subtabacina are lower cortex visible, evenly distributed. similar to those seen in the holotype of B. Apothecia and pycnidia not found. fungicola (S!) because they are generally TLC/HPLC − cortical atranorin and simple and short, often only small ciliar bulbs chloroatranorin, medullary salazinic acid (see that have not yet developed into cilia can be also Elix & Stevens 1979, Elix 1994). observed. Distribution − Oceania: Australia (Elix Usually, Bulbothrix species containing & Stevens 1979, Elix 1993b, Elix 1994). medullary salazinic acid such as B. hypocraea Comments − The holotype (Fig. 12) of (TUR-V! lectotype, BM! duplicate), B. isidiza this species consists of a thallus that is still (H-Nyl! holotype), B. meizospora (Nylander) almost completely intact; additionally the Hale (H-Nyl! holotype) or B. tabacina (L! packet also contains a small fragment, also of lectotype, PC! duplicate) have much wider excellent condition. Both specimens are glued laciniae (usually three or four times the width to cardboard (it was necessary to remove a part of those from B. subtabacina) with a more from the substrate to study its lower cortex). irregular branching pattern and rounded apices. No apothecia or pycnidia could be found on Curiously, the overall aspect of B. subtabacina either one of the thalli. The isotype, obviously resemble those containing medullary not a fragment of the holotype, seems to be gyrophoric, lecanoric or lobaric acids. instead a complete small thallus, maybe Bulbothrix tabacina was compared to collected together. It is slightly less cracked B. subtabacina by Elix & Stevens (1979). It than the holotype specimen, although its center differs by wider laciniae (1.5−5.5 mm wide) appears just as fragmented. Like the holotype, with rounded apices, a continuous upper the isotype lacks apothecia and pycnidia, but it cortex, eciliate isidia, and by the usually simple is much more isidiate. cilia and rhizines. Elix (1994) also compared B. As described by Elix & Stevens (1979) subtabacina to B. microscopica (CANB!, and Elix (1994), the thalli present a very holotype), which differs by the narrower, half- frequent cracked upper cortex, more than size laciniae (0.10.5 mm wide), emaculate commonly seen for other species of the genus, upper cortex, and by the simple cilia and the center so fissured as looking areolate in rhizines. some parts. The eroded parts that the authors have referred are the result of the combination Bulbothrix tabacina (Montagne & Bosch) of cracks with the strong marks left by blocks Hale. Phytologia 28:481. 1974. Fig. 13−16 of detached isidia. MB 341619 The species is maculate, but it is Basionym − Parmelia tabacina difficult to see in the material examined, due to Montagne & Bosch. Sylloge generum the large amount of isidia on the upper cortex, specierumque cryptogamarum: 327. 1856. and the numerous marks left when they break Synonyms − Parmelia meizospora var. off. The marks are so abundant in some parts isidiosa Müller Argoviensis. Flora 67: 620. 20
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1884 (nomem nudum). to tortuous, 0.050.60 ca. 0.05 (0.15) mm, Parmelia meizosporoides Dodge. simple to sometimes sparsely branched, erect Annals of the Missouri Botanical Garden 46: to procumbent, firm to caducous, concolorous 83. 1959. with the upper cortex, brownish or with Parmelia ochrovestita Zahlbruckner. brownish apices, eciliate. Medulla white. Annales de Cryptogamie Exotique. 1: 200. Lower surface black, with some occasional 1928. small dark brown spots in the transition area to Parmelia sublaevigatoides Dodge. the margins (these spots rarely more extensive, Annals of the Missouri Botanical Garden 46: stretching between the margin and center), 88. 1959. slightly shiny to opaque, smooth to subrugose, Lectotype: Indonesia, Java, in cortice venate, weakly papillate, moderately rhizinate. arborum, leg. Junghuhn s.n. (L!, isolectotype at Marginal zone pale to dark brown and PC!). attenuated, 1.0−3.0 (−6.0) mm wide, rarely Thallus sublinear to subirregular laciniate to black and indistinct from the center, shiny, sublaciniate, pale grey to dusky greenish grey smooth to subrugose, papillate becoming in herbarium, up to 7.3 cm in diam., rhizinate in the transition to the center. submembranaceous to subcoriaceous, Rhizines black, pale to dark brown or with corticolous or rarely saxicolous, upper cortex whitish apices when near the margins, simple 10.0−15.0 µm thick, algal layer 12.5−20.0 µm to rarely irregularly branched, without basal or thick, medulla 45.0−100.0 µm thick, lower displaced bulbs, 0.100.70 ca. 0.030.05 cortex 10.0−12.5 µm thick. Laciniae irregularly mm, frequent, often scarce near the margins, to partially anisotomic dichotomously but somewhat randomly scattered and in some branched, (0.6−) 1.64.1 (5.4) mm wide, parts abundant, often appearing from venations contiguous to imbricate becoming partially and warts, ±evenly distributed. Apothecia crowded at the center, slightly adnate and subplane to concave or urceolate, adnate to adpressed, with flat, subrotund to subtruncate substipiate, 0.3−5.2 mm in diam., laminal to or rarely truncate apices, the margins flat, submarginal, ecoronate, margin smooth to smooth and sinuous to crenate or subirregular, subrugose and subcrenate, amphithecia smooth entire to slightly incised, occasionally to subrugose eventually becoming isidiate. sublacinulate, the axils oval or irregular. Upper Disc pale to dark brown, epruinose, cortex smooth and continuous, occasionally imperforate, epithecium 5.07.5 m high, subrugose with variable irregular cracks on hymenium 35.0−50.0 µm high, subhymenium older parts, laminal ciliar bulbs absent. 25.0−30.0 µm high. Ascospores ellipsoid to Adventitious marginal lacinulae absent to oval, 9.0−15.0 (−16.5) × 5.0−8.0 (−10.0) µm, scarce on random parts, short, 0.21.3 0.1– epispore 0.5−1.5(−2.0) µm. Pycnidia scarce, 0.4 mm, plane, simple to irregularly branched, laminal to submarginal, on central parts of the apices truncate, lower side concolorous to the thalli, with brown to black ostioles. Conidia lower marginal zone. Maculae weak to distinct, (not found on the type) weakly bifusiform, punctiform, laminal. Cilia black to occasionally 4.06.0 ca. 1,0 m. brown, apices simple to rarely double, TLC/HPLC − cortical atranorin, occasionally bent downwards, 0.050.30 medullary salazinic acid (see also Hale 1976; (0.40) 0.030.04 mm, with semi-immersed there are also labels of Kurokawa dated 1960 to sessile bulbate bases ca. 0.050.15 (0.20) and Aptroot dated 1985 together with the type mm wide, scarce to frequent along the margins material). The holotype of P. meizosporoides spaced 0.50.10 (0.15) mm from each other also contain cortical chloroatranorine and to rarely contiguous, solitary or in small groups medullary consalazinic acid, with traces of in the crenae and axils, usually absent or scarce norstictic acid (this last one possibly a on the apices of the laciniae. Soredia and contaminant). pustules absent. Isidia frequent, laminal, Distribution − Oceania: Australia (Hale usually breaking off together in small packets, 1976, Elix 1994), Polynesia (Louwhoff & Elix smooth, cylindrical or rarely granular, straight 2000), Rarotonga (Louwhoff & Elix 2002a). 21
Mycosphere Doi 10.5943/mycosphere/4/1/1 Asia: India (Hale 1976, Divakar & Upreti 38º37’E, 800-900 m, leg. R. Santesson 23422, 2005), Indonesia (Zahlbruckner 1928, as the 11-I-1971 (US). Uganda, Monte Eglon, alt. synonym Parmelia ochrovestita, Junghuhn 1290 m, collector unknown XII-1914 (BM!, 1855, Montagne 1856, Hale 1976),Philippines holótipo de Parmelia sublaevigatoides). (Hale 1976), Malaysia (Hale 1976), Nepal, Madagascar, Andrangolaoka, Imerina, leg. (Hale 1976, Kurokawa 1993), Sri Lanka Hildebrandt s.n., XI-1880 (FH!, holotype of (Awasthi 1976), Taiwan (Hale 1976, Parmelia meizosporoides Dodge). Mexico, Kurokawa & Lai 2001). Africa: Angola (Hale Chiapas, 2 km north of highway 190 on road to 1976), Congo (Dodge 1959, as the synonym P. Puebla Nueva west of Chiapas, Chiapa de sublaevigatoides), Ethiopia (Swinscow & Krog Corzo, pine pasture, on conifers, ca. 1070 m, 1988), Guinea (Hale 1976), Madagascar leg. M.E. Hale & T.R. Soderstrom 21067, 23- (Dodge 1959, as the synonym P. III-1960 (US). Idem, Veracruz, 46 km meizosporoides, Hale 1976, Aptroot 1990), southwest of junction of highway 140 and 155, Malawi, Mozambique, South Africa (Dodge northeast of Huatusco, hillside, scattered trees 1959, as the synonym P. sublaevigatoides), in coffee plantation, ca. 1020 m, leg. M.E. Hale Kenia (Swinscow & Krog 1988), Uganda & T.R. Soderstrom 19475, 13-III-1960 (US). (Dodge 1959, as the synonym P. Porto Rico, Distr. Arecibo, trail at end of Hwy sublaevigatoides, Swinscow & Krog 1988), 625, just outside of Observatório de Arecibo, Tanzania (Dodge 1959, as the synonym P. ca. 18o 22’N, 66o 45’W, 265-295 m, humid sublaevigatoides, Hale 1976, Swinscow & forest in limestone mogotes, leg. R.C. Harris Krog 1988). North America: Mexico (Hale 27598, 12-I-1992 (NY). Venezuela, Táchira, 1976, Sipman & Wolf 1998). Caribbean: Cuba, Via Rubio, Bramón, 800−1100 m, leg. M.E. Haiti, Dominican Republic, Trinidad and Hale & M. López Figueiras 45724 p. max. p., Tobago (Hale 1976), South America: Chile 24-III-1975 (US). Brazil, São Paulo, São Paulo (Galloway & Quilhot 1998), Guyana (Feuerer Municipality, Parque Estadual da Cantareira, 2008), Uruguay (Osório 1992), Venezuela on tree branches in the woods, leg. M.N. (Hale 1976, López-Figueiras 1986, Marcano et Benatti 1410, VI-2000 (SP); idem, Mogi- al. 1996) and Brazil Rio Grande do Sul Guaçu Municipality, Reserva Biológica de (Canêz 2005) and São Paulo (Hale 1976, Mogi-Guaçu, Fazenda Campininha, on tree Osorio 1989, Marcelli 1990, 1991, 1993, thin twig, leg. M.P. Marcelli & M. Falco Jungbluth 2006). This species is being cited for 33065, 2-IV-1999 (SP); idem, on tree trunk in Porto Rico for the first time. the woods, leg. M.P. Marcelli & M. Falco Additional selected specimens 34325, 14-IX-2000 (SP). examined:New Caledonia, Mission Tejé, 1909, Comments − The holotype (Fig. 13) is leg. G. Giamuier s.n. (DUKE). Papua New dark brown, and the medullary acid is oxidized, Guinea, MacDonald´s Corner, near Port the medulla completely stained with a rusty Moresby, on bark of rubber trees, leg. S.L. brown tint. It consists of two larger and one Thrower 2719, 30-VI-1976 (US). Indonesia, small fragments, all on bark, not glued to the Java, corticola, in horto botanico cardboard. The fragments are quite brittle. Buitenzorgensi, ad Pandanum Bidur Jungh., There are a few pycnidia, but no conidia were leg. Overeem 335 (W!, holotype of Parmelia found in them. The apothecia are poorly ochrovestita). Malaysia, Pahang State, oak- developed, and in almost all the hymenia are dipterocarp forest, elev. About 1300 m, vicinity damaged. The duplicate consists of a fragment of Frazier´s Hill, leg. M.E. Hale 30134 4-III- in the same poor conditions, also with the 1965 (DUKE). South Africa, Pietersburg hymenial discs of the apothecia completely District, Bem Lavin Nature Reserve, near darkened and making it impossible to examine Louis Trichardt, 23 29 BB, bushveld of mixed the ascospores. Although I cannot be sure if legume trees, leg. W.R. Buck 13405, 12-I-1986 this fragment is really a duplicate, it was the (NY). Tanzania, Tanga Province, Usambara only B. tabacina specimen located at PC; there Mts., Amani, Road towards SW, on the trunk is no collector’s name, however the fragment of a tree (Leguminosae) in a field, 5º8’S, do appear to have the same age and is in the 22
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Figs 12–16 – 12 Holotype of Bulbothrix subtabacina (MEL). (US). 13 Lectotype of Bulbothrix tabacina (L). 14 Holotype of Parmelia meizosporoides (FH). 15 Holotype of Parmelia sublaevigatoides (BM). 16 Hlotype of Parmelia ochrovestita (W). Scale bars = 1 cm (12, 13, 14, 15, 16).
23
Mycosphere Doi 10.5943/mycosphere/4/1/1 same condition as the lectotype. By the differs from B. tabacina by being strictly description of Montagne & Bosch (Montagne saxicolous, with a frequently cracked 1856), it is probable that the thallus was emaculate upper cortex, having narrower (ca. already on a very advanced stage of medullary 0.5−3.0 mm wide) and sublinear laciniae with substance deterioration at the type of its usually truncate apices, smaller and blackened collection. isidia, and by cilia with larger bulbs, which Bulbothrix tabacina is one of the most sometimes do elongate into cilia. widely distributed species of the genus, cited Regarding the accepted synonyms of B. for many tropical countries of almost all tabacina, Parmelia meizosporoides (Fig. 14) continents. According to Hale (1976), this is was considered by Hale (1976) a synonym of one of the species in the genus that can very Bulbothrix tabacina; this is confirmed here. easily be collected. Junghuhn (1855) cited a The name Parmelia meizosporoides Dodge specimen from Java Island (Indonesia) one (1959) resulted from a validated description for year before the publication of the species by the species (nomem nudum) called P. Montagne & Bosch (1856), mentioning the meizospora f. isidiosa Argoviensis by Müller species and the page where it would be (1884). In fact, in the work the name is only eventually found (in his descriptiom, Junghuhn mentioned in a list, and only Zahlbruckner describes the medulla as reddish brown, of a (1930) cited P. meizospora f. isidiosa in the similar colour as tobacco, due to discoloration synonymy of Parmelia amazonica Nyl. caused by oxidized salazinic acid). The species Dodge (1959) described Parmelia may well be found on twigs as well as on tree meizosporoides with negative medullary trunks. reactions, however, the holotype (FH!) actually The ascospore measurements cited by reacts to the K test, and contains medullary Hale (1976), Swinscow & Krog (1988), Elix salazinic acid as seen in TLC/HPLC. The type (1994) and Kurokawa & Lai (2001) are all in material is saxicolous, and besides the accordance with those given here, varying ascospores were described as not exceeding 10 between 9.0−15.0 × 5.0−8.0 µm to 12.0−15.0 × µm long, these were found to measure 7.0−10.0 µm, although no pseudosepta, as 9.013.0 (15.0) 4.06.5 (7.5) µm, with mentioned by Swinscow & Krog (1988), were epispore 1.01.5 µm. The holotype of found in any specimen. Swinscow & Krog Parmelia meizosporoides has clear medullae, (1988) described the species as emaculate in better condition than the holotype of having marginal cilia that are not always Bulbothrix tabacina. Dodge already mentioned bulbate and occasionally bearing phylidia. the bulbate cilia, indicating that the margins of None of these observations can be confirmed the thallus were “papillate”. The specimen was here. described with more sublinear laciniae ca. 1 cm Swinscow & Krog (1988) and Elix wide, but has laciniae 1.5−4.0 mm wide. (1994) mentioned saxicolous specimens of B. The holotype (Fig. 15) of Parmelia tabacina, but have accepted B. decurtata as a ochrovestita (Zahlbruckner 1928) is probably synonym. However, the saxicolous specimens the same species as Bulbothrix tabacina, but it of B. tabacina studied here display the same displays a number of atypical features. characteristics as the corticolous specimens, Although it shares all of the morphological and these all differ from the characters variation seen in other specimens of B. observed in B. decurtata (see description and tabacina, the holotype of Parmelia comments there). Unlike argued by Swinscow ochrovestita is characterized by more & Krog (1988), and comparing the materials sublinear, more narrow laciniae (1.0−3.0 mm studied, B. decurtata is not accepted here as a wide.), it is pale greyish, and its lower cortex synonym of B. tabacina. Instead the has elongate, attenuated pale brown margins. differences of the two species agree well with The whole thallus gradually becomes darker those already pointed out by Hale & Kurokawa towards it center where it eventually become (1964). Bulbothrix decurtata (Hale & completely blackened. The isidia are very Kurokawa) Hale (LD!, isotype at US!) thus abundant, covering large portions of the 24
Mycosphere Doi 10.5943/mycosphere/4/1/1 thallus, they are thus not quite like the laciniae than B. tabacina (1.5−4.5 × 1.0−2.5 relatively scarce isidia seen on most other mm wide), the material studied (Benatti 2012a) specimens of B. tabacina. showed that the variation is similar in both Studies of the holotype specimen (Fig. species. She also described specimens with an 16) of Parmelia sublaevigatoides Dodge emaculate surface, but they actually have weak (1959) also suggest that this taxon should be and sparse maculae. considered a synonym of B. tabacina. Its Hale (1976) compared Bulbothrix laciniae are slightly narrower than usual laevigatula (Nyl.) Hale (H-Nyl 35653!, (although in accordance with the minimum duplicate at PC!) to B. tabacina, and this found), and they are also more sublinear often species differs by the narrow, sublinear with subtruncate apices. However, the dichotomously branched laciniae (ca. 0.5−2.0 specimen is clearly small and undeveloped. mm wide), dichotomously branched cilia and The material bears no apothecia or pycnidia. rhizines, and by the presence of medullary Dodge mentioned P. sublaevigatoides in his lecanoric acid. key as not isidiate, however, the material has Jungbluth (2006a) and Jungbluth et al. sparse isidia, smaller than commonly found in (2008) compare B. cassa Jungbluth, Marcelli & the specimens of B. tabacina. Due to the Elix (SP!, holotype) to B. tabacina. Bulbothrix immature condition of the holotype it appears cassa is morphologically similar, differing by that laciniae and isidia did not yet reach their the brown lower córtex and by the presence of maximum width and size. a medullary fatty acid instead of salazinic acid. Dodge (1959) cited medullary chemical Bulbothrix subtabacina (holotype at reactions as negative for this species. However, MEL!, isotype at CANB!) differs by the more the thallus clearly contains medullary salazinic linear, dichotomous, and narrow laciniae acid, with its typical K + reaction, confirmed (0.5−1.0 mm wide) with truncate apices, very also by TLC/HPLC (this has been annotated on cracked upper cortex, commonly ciliate isidia the label already by T.D.V. Swinscow and by the dichotomously branched cilia and mentioning the mistake by Dodge, although no rhizines. indication is given by which method the presence of salazinic acid was confirmed). The Nomina Inquirenda upper cortex of the specimen does not react K− as mentioned by Dodge, but it is clearly K + Parmelia demangei Harmand, Annales yellow due to the presence of atranorin. Cryptogamae Exotiques 1: 327. 1928. Bulbothrix isidiza (H-Nyl! holotype) MB 397447 was compared to B. decurtata by Hale (1976) Holotype − Indochina, leg. Demange 37 and is probably the most similar species in both (P, accordingly to Hale 1976a, n.v.). morphology and medullary chemistry. Comments − The type material was not However, thalli of B. isidiza tend to be mor located at P or PC. This species is accepted as a densely isidiate than those of B. tabacina, and synonym of B. isidiza by Hale (1976). As the lower cortex is pale brown from the described by Harmand (1928) Parmelia margins to the center, with little variation in demangei has a ± orbicular whitish thallus ca. 5 tone. Marcelli (1993) and Canêz (2005) cited cm in diameter, membranaceous, smooth and B. tabacina specimens with a brown lower somewhat shiny, with scattered or grouped cortex with darker parts, but these are in fact laminal isidia 0.2−0.4 mm high, sinuous and specimens of B. isidiza. incised-lobed laciniae 1.0−3.0 mm wide, that Bulbothrix ventricosa (TUR-V! are very irregularly lacinulate, has crenate lectotype) can be differentiated by the constant margins, rounded to sometimes subtruncate formation of laminal ciliar bulbs, denser isidia, apices, rounded axils, dark olive green lower a lower cortex of variable colour (often mixed cortex with dense dark brown simple to brown and black tones), and by the presence of branched rhizines 0.5 to 1.0 × 0.06 mm, both medullary norstictic acid. Althought Jungbluth upper and lower cortices ca. 9 µm thick, the (2006) mentioned that B. ventricosa had wider medulla and algal layer ca. 60 m thick. He 25
Mycosphere Doi 10.5943/mycosphere/4/1/1 described two reactions: K + yellow (possibly demangei, it is possible to make just a few the upper cortex, due to atranorin) and K + comments about this species. The taxon is yellow → blood red (typical for medullary possibly a synonym of B. isidiza and not one of salazinic acid). P. demangei. The author described the laciniae Harmand (1928) described the "rhizines as "all visibly coated (perhaps by rhizines? He usually triming the edge of the thallus having does not mention eyelashes…) followed up the the appearance of cilia." His comment that it edges." Although it is unclear as which was "a sterile lichen which appears to have character he actually means, it is quite possible been collected with the bark, without a precise that he meant bulbous marginal cilia. location." As a lacinulate lichen with an olive As with P. demangei, it is possible to lower cortex (a colour commonly seen in make just a few comments about this species, Pseudoparmelia thalli) it may be a synonym, but P. recurviscens seems more likely to be a but could also be a morphologically distinct synonym of B. isidiza than of P. demangei. species similar to B. isidiza. However, from the Harmand (1928) described the laciniae and the description alone, this is impossible to tell and lacinulae "all visibly covered (by rhizines thus it will be necessary to first locate the type perhaps? he did not mention cilia) following up material. the edges." Although it is unclear to which character this statment refers, it is quite Parmelia recurviscens Harmand, Annales possible that he meant the bulbate marginal Cryptogamae Exotiques 1: 326. 1928. cilia. MB 398151 Holotype − Indochina, leg. Demange 36 Acknowledgements (P, accordingly to Hale 1976a, n.v.). The author wishes to thank the curators Comments − The type material was not of BM (Scott LaGrecca), CANB (Brendan located at P or PC. This species is also Lepschi), DUKE (Kathleen Pryer), H (Leena accepted as a synonym of B. isidiza (Nylander) Myllys), HUFSCAr, L (Gerard Thijsse), LD Hale by Hale (1976). As described by (Arne Thell), MEL (Josephine Milne), MSC Harmand (1928) Parmelia recurviscens has a (L. Alan Prather), NY (Barbara Thiers), PC membranaceous to subcoriaceous greyish (Bruno Dennetière), TNS (Yoshihito Ohmura), thallus, with a slightly pinkish tone in the and US (Rusty Russell) for loans or access to center, a somewhat shiny smooth surface, type specimens and additional material, John scarce isidia disposed in small clusters, 0.3 to A. Elix for HPLC data on the species 4.0 (could be a typo, 0.4?) mm high, laciniae secondary metabolites, Frank Bungartz for the 2.0–5.0 mm wide, subrotund or elongated, English review, comments, and suggestions, irregularly lacinulate to crenate and lobulate, and the reviewers for critical revision of the incised, slightly imbricate, with rounded or manuscript. subtruncate apices and angular axils, a densely rhizinate, castaneous brown lower cortex, black References rhizines 0.3−1.0 mm long, both upper and lower cortices ca. 9 µm thick, algae layer ca. Aptroot A 1990 – Lichens of Madagascar: new 45 µm thick, medullae ca. 66 µm thick, and interesting records and species. apothecia 0.30−0.35 mm in diam., concave, Cryptogamie, Bryologie et Lichenologie disc castaneous brown, smooth, margin 11(4) 401–408. denticulate, containing 8 ascospores per ascus, Asahina Y. 1957 – Lichenologische Notizen simple, hyaline, oval, 12.0 × 6.0−6.5 µm. (124-125). Journal of Japanese Botany Again, he described two reactions: K + yellow 32(4) 97–100. (possibly the upper cortex, due to atranorin) Awasthi DD. 1976 – Lichen genus Parmelia in and K + yellow→ blood red (typical for India I – Subgenera Parmelia and medullary salazinic acid). Amphigymnia. Biological Memoirs 1(1-2) The only comment made by Harmand 155–229. (1928) was "uncertain locality". As with P. Benatti MN, Marcelli MP. 2010 – Four 26
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