Bulbothrix meizospora (Nyl.) Hale. Phytologia 28(5): 480. 1974.

Benatti, Michel N., 2012, A review of the genus Bulbothrix Hale: the species with medullary salazinic acid lacking vegetative propagules, MycoKeys 5, pp. 1-30 : 13-16

Bulbothrix meizospora (Nyl.) Hale. Phytologia 28(5): 480. 1974. Figures 11-14

Parmelia tiliacea var. meizospora Nyl. Synopsis Methodica Lichenum 1: 383. 1860. [Basionym]

Parmelia meizospora (Nylander) Nyl. Flora 52: 292. 1869. [Synonyms]

Parmelia amplectens Stirton. Scottish Naturallist 4: 201. 1878.

Bulbothrix vainioi Jungbluth, Marcelli & Elix. Mycotaxon 104: 59. 2008.

Holotype.

India, Nilgherries Montains, Watt s.n. (H-NYL 35107!).

Description.

Thallus subirregular laciniate to sublaciniate, dark dusky gray in the herbarium, up to 7.3 cm diam., subcoriaceous to submembranaceous, corticolous (rarely on rocks or soil); upper cortex 15.0−20.0 µm thick, algal layer 25.0−35.0 µm thick, medulla 85.0−110.0 µm thick, lower cortex 15.0−20.0 µm thick. Laciniae irregularly to almost anisotomically dichotomously branched, 1.6-6.1 mm wide, contiguous to slightly imbricate, becoming crowded at the center, ± adnate and adpressed, with flat to slightly involute, subrounded to subtruncate or rarelytruncate apices; margins flat to slightly involute, crenate to or irregular, entire, rarely sublacinulate; axils oval to irregular. Upper cortex smooth and continuous at younger parts, becoming rugose and irregularly cracked at older parts; laminal ciliary bulbs absent. Adventitious marginal lacinulae absent to scarce on older parts, short, 0.2-0.8 × ca. 0.1-0.3 mm, plane, simple; apices truncate; lower side concolorous with the lower marginal zone. Maculae weak, punctiform, laminal or in the amphithecium, usually common but hard to see on darkened specimens (such as the type). Cilia black, without or with simple or double apices, short and bent downwards, 0.05-0.30 (−0.60) × 0.03−0.05 mm, with semi-immerse to emerse bulbate bases 0.10-0.30 mm wide (these partially enlarged or occasionally absent), often withered and becoming reniform at the axils, scarce along the margins but more frequent at the crenae and axils, spaced 0.05−0.15 mm from each to occasionally contiguous, solitary or in small groups, becoming absent at the apices and adjacent parts of the laciniae. Soredia, Isidia and Pustulae absent. Medulla white. Lower cortex black, occasionally dark brown at the transition from the margins to the center, slightly shiny to opaque, smooth to rugose, moderately rhizinate. Marginal zone black and indistinct from the center to brown or dark brown and attenuate, 0.5−4.0 mm wide, opaque to slightly shiny, smooth to rugose, weakly papillate, scarcely rhizinate at the transition to the center. Rhizinae black, occasionally dark brown close to the margins, initially simple to rarely furcate, without basal or displaced bulbs, 0.10-0.40 (−0.70) × ca. 0.05 mm, usually frequent but varying from scarce to abundant at a few parts or near the margins, evenly distributed. Apothecia urceolate to concave or subconcave, partially becoming fissured and folded when old, adnate to subpedicelate, 0.8−6.2 mm diam., laminal to submarginal, ecoronate; margin smooth; amphitecia smooth becoming subrugose, without ornamentations. Disc light to dark brown, epruinose, imperforate; epithecium 10.0-20.0 µm high; hymenium 50.0−80.0 µm high; subhymenium 15.0−37.5 µm high. Ascospores ellipsoid to oval or rounded, (10.0−) 12.5−19.0 (−22.0) × (7.5−) 9.0−11.0 (−14.0) µm; epispore (0.5−) 1.0−1.5 µm. Pycnidia frequent, laminal to submarginal, immerse, with black ostioles. Conidia baciliform to weakly or distinctly bifusiform (4.0−) 5.0−9.0 × 0.75 µm.

TLC/HPLC: cortical atranorin and chloroatranorin, medullary salazinic and consalazinic acids (see also Hale 1976).

Distribution.

Asia: India ( Nylander 1860, Stirton 1878, Hale 1976a, Divakar and Upreti 2005), Pakistan ( Hale 1976a), Nepal ( Hale 1976a, Kurokawa 1993), and Thailand ( Wolseley et al. 2002). Africa: Camarões ( Hale 1976a), Kenya ( Swinscow and Krog 1988), and Tanzania ( Krog 2000). South America: Brazil - State of São Paulo ( Marcelli 1993, Jungbluth 2006). Accordingly to Elix (1994), the species was erroneously cited for Australia ( Knight 1882), and does not occur in that region. Here it is cited as new for Malawi.

Additional specimens examined.

India, Mussoorie, northwest Himalaya, 7000 ft., leg. R. R. Stewart s.n., VII-1931 (NY 12298). Idem, Nilgherries Montains, Watt s.n. (lectotype of Parmelia amplectens , BM!, duplicate at GLAM!). Pakistan, Lower Topa, Murree hills, on bark of Pinus excelsa, leg. S. H. Iqbal 835, 11-VII-1967 (US). Malawi, Cholo Mt., dead branchlets of rain-forest trees, 1200 m alt., leg. L. J. Brass s.n. 24-IX-1946 (NY 17788). Brazil, São Paulo State, Itirapina Municipality, Estação Experimental de Itirapina, IF, leg. P. Jungbluth, L. S. Canêz & A. A. Spielmann PJ881, 26-III-2004. Idem, Santa Rita do Passa Quatro Municipality, Fazenda Vassununga, km 259 of the Anhanguera Highway, leg. M. P. Marcelli & B. L. Morretes 15653, 03-VI-1978 (SP). Idem, São Manuel Municipality, Fazenda Palmeira da Serra, non official particular cerrado (savannah) reserve, on tree trunk, leg. M. P. Marcelli & S. B. Barbosa 35693, 03-VI-2003 (SP). Idem, Botucatu Municipality, beside the highway that connects the city to the highway Castello Branco (SP-280), km 3, private cerradão forest inside Fazenda Morro do Ouro, 22°53'S, 48°26'W, 804 m alt, on a tree trunk, leg. M. P. Marcelli & S. B. Barbosa 35696, 4-VI-2003 (holotype of Bulbothrix vainioi , SP!).

Comments.

The holotype (Fig. 11) consists of a single thallus on bark. It is partially detached from the substrate and in poor condition. Part of the upper cortex is absent, the medulla is much stained by oxidized salazinic acid, and the thallus is brittle and fragile. There are several apothecia in different stages of maturation, some of them also damaged, though they have ascospores. The thallus has many pycnidia, some containing conidia.

Nylander wrote on a label with the type specimen voucher "ascospores 14.0-18.0 × 7.0-11.0 mm", but mentioned as measures 14.0-21.0 × 8.0-11.0 mm at the work in which he described Parmelia tiliacea var. meizospora ( Nylander 1860), and as 11.0-21.0 × 8.0-11.0 mm in the work that raised the variety to the rank of species ( Nylander 1869).

Nylander (1885) mentioned bifusiform conidia for Indian material, measuring 5.0 × 0.5−0.7 µm (he was one of the first authors to note bifusiform conidia in Bulbothrix ). Divakar and Upreti (2005) and Jungbluth (2006) also mentioned bifusiform conidia for Bulbothrix meizospora .

Hale (1976a) mentioned that the size of ascospores was variable in the species, and that is confirmed by the material cited below, in which ascospores may have any measure starting from 12.0−15.0 × 7.0−10.0 µm up to 12.0−22.,0 × 8.0−12.,0 µm. Marcelli (1993) and Jungbluth (2006) mentioned ascospores 12.0−16.5 × 8.0−10.0 µm. Ascospores under 12.0 µm are usually quite rare and look not fully developed.

Cilia in Bulbothrix meizospora are usually infrequent, and a portion of them in a same thalli apices might not present apices, while some others do not have bulbs. Often the bulbs become withered or reniform, which is more evident in the axillary cilia.

Regarding the presence and intensity of cortical maculae, Swinscow and Krog (1988) and Marcelli (1993) cited specimens of Bulbothrix meizospora with absence of cortical macules, while Hale (1976a) and Divakar and Upreti (2005) mentioned that the species can be weakly to moderately maculate, and Jungbluth (2006) mentioned distinct maculae.

Apparently, as mentioned by Benatti (2010), there are no Bulbothrix species with varaible presence of maculae, but that are are always either emaculate such as Bulbothrix continua (Lynge) Hale, or always maculate as Bulbothrix hypocraea (Vainio) Hale. What seems to happen is that certain species, such as Bulbothrix meizospora , have variable maculae intensity, more subtle and scarce in some thalli (which makes it difficult to see them) and somewhat more evident in others.

Bulbothrix setschwanensis (Zahlbruckner) Hale was compared to Bulbothrix meizospora by Hale (1976a) and Divakar and Upreti (2005). It differs by the more constantly bulbate cilia with distinct apices that appear more abundantly at the margins, and by the pale brown lower cortex.

Bulbothrix sensibilis (Steiner & Zahlbruckner) Hale was compared by Swinscow and Krog (1988), and differs from Bulbothrix meizospora only by the smaller ascospores, which vary from 7.0-9.0 × 4.0−7.0 to 8.0−12.0 × 6.0-8.0 mm, as cited by Zahlbruckner (1926), Hale (1976a), and Swinscow and Krog (1988) and as seen in the present work. Hale (1976a) used the laciniae aspect and width to differentiate the species, I found that these features are not very helpful in the case of these two species, with only the tendency of smaller sizes to be more common in Bulbothrix sensibilis .Although Hale (1976a) used the shape and width of the laciniae for differentiation, comparisons between Bulbothrix sensibilis and B meizospora gave almost identical measurements, with slight variations in width, the specimens of Bulbothrix sensiblis frequently tending to have narrower, more often sublinear laciniae. Besides the sole significative difference of ascospore sizes, recent analyses of DNA sequences corroborate the distinction of the species ( Divakar et al. 2010).

Bulbothrix hypocraea (Vainio) Hale was compared to Bulbothrix meizospora by Jungbluth (2006). It differs by having a distinctly maculate upper cortex, narrower and sublinear laciniae (ca.1.0−3.0 mm wide), a pale brown lower cortex and smaller ascospores (usually 7.0−14.0 × 5.0−8.0 µm).

Recognition of Bulbothrix meizospora as a Bulbothrix species can sometimes be difficult, as commented already by Marcelli (1993), due to the relatively large size of the thalli when compared to other species of the genus, and because the bulbs are not very evident in the cilia or sometimes partially absent. Notably Canoparmelia amazonica (Nylander) Hale, present in the same habitats, was compared by Marcelli (1993) to Bulbothrix meizospora , suggesting that in certain circumstances they could be mistaken in field. Canoparmelia amazonica can be distinguished by the complete absence of marginal cilia and by the presence of medullary protocetraric acid.

The type material (Fig. 12) of Parmelia amplectens Stirton (BM! lectotype, GLAM! duplicate) has cilia with more distinct bulbs and somewhat longer apices, and it is difficult to recognize maculae due its poor condition. However, the further characteristics agree with those of Bulbothrix meizospora as accepted by Hale (1976a). Stirton (1878) described ellipsoid ascospores 15.0−18.0 × 9.0−12.0 µm and cylindr ical straight conidia 6.0 × 0.7 µm, which are also in agreement with measurements obtained here from the type (ascospores 12.0−19.0 × 10.0−12.0 µm; conidia nearly identical) and those normally found in Bulbothrix meizospora . The lectotype is a relatively large thallus (about 10 cm wide) in poor condition, the cortex and several of the marginal ciliary bulbs badly damaged. It is less brownish than the duplicate, but also with the medulla stained by oxidized salazinic acid, and several apothecia have lost their hymenia. The duplicate is composed of two larger fragments a few cm wide and several smaller fragments, and it is very dusky brown.

Bulbothrix vainioi (Figs 13-14)Jungbluth, Marcelli and Elix was described by Jungbluth et al. (2008) based on specimens with ascospores over 12 µm long included by Hale (1976a) provisionally in Bulbothrix sensibilis . However, apparently they overlooked the possibility that their material could belong to Bulbothrix meizospora , the ascospores with the minimum common diameter for that species. As was checked here, all specimens assigned to Bulbothrix vainioi are morphologically identical with Bulbothrix meiospora and have the same chemistry. Consequently Bulbothrix vainioi is not a species similar to Bulbothrix sensibilis with larger ascospores, as the authors assumed, but typical Bulbothrix meizospora with ascospores 12.0−16.0 µm long, a size range well inside the limits found for this species, and with the same cilia.

Hale (1976a) and Divakar and Upreti (2005) mentioned that thalli of Bulbothrix meizospora can occasionally be found on rocks, and rarely on soil. Divakar and Upreti (2005) mentioned pycnidia usually confined to peripheral areas of laciniae, but in the holotype and other material studied they can be seen all over the thallus.