The Lichenologist 44(6): 813–826 (2012) 6 British Lichen Society, 2012

doi:10.1017/S0024282912000436

The true identity of Bulbothrix goebelii (Zenker) Hale and the

re-establishment of some of its synonyms as accepted species

M. N. BENATTI and J. A. ELIX

Abstract: The type collection of Parmelia goebelii (Bulbothrix goebelii) was discovered to be a mixture
of several different Bulbothrix species. The true identity of B. goebelii is established and problems
regarding the variability of this species discussed. The species B. papyrina, B. scortella and B. sub-
dissecta, synonymized with B. goebelii by Hale, are resurrected as valid taxa. A detailed description of
B. goebelii is presented, its lectotype is selected, and the characteristics of all four species discussed.
Key words: bulbate cilia, gyrophoric acid, isidia, lichen, lobaric acid, Parmeliaceae
Accepted for publication 15 June 2012

Introduction work (Benatti 2010), many type specimens

were examined and this resulted in the rein-
The genus Bulbothrix Hale (Hale 1974) was
terpretation of some species previously treated
based on the Series Bicornutae (Lynge) Hale
as synonyms (Hale 1976).
& Kurok. of the genus Parmelia Ach. The
Prior to his discovery and combination of
species can readily be identified by the small,
B. goebelii (Hale 1976), Hale accepted three
deeply laciniate thalli with marginal bulbate
isidiate species that he subsequently synony-
cilia (the main characteristic), cortical atra- mized with this species: B. papyrina, B.
norin (which differentiates Bulbothrix from
scortella and B. subdissecta (Hale & Kurokawa
the genus Relicina), hyaline, unicellular, ellip-
1964; Hale 1974). However, he did not dis-
soid or bicornute ascospores and bacilliform cuss the difficulties in interpreting the rela-
to bifusiform conidia. The medullary chemis-
tionships within this broader concept of B.
try is variable, containing several chemosyn-
goebelii, nor the uncertainties involved (Hale
dromes and some unknown substances. Hale
1976). More recent studies (Benatti 2010)
assembled all of the then available taxonomic
have shown that these species have different
information in a monograph of the genus
characteristics from each other. The type
(Hale 1976). Subsequently several additional
material of B. goebelii was shown to be a mix-
species have been described, mainly from the
ture of species and the fragment that is most
Neotropics (e.g., Sérusiaux 1984; Hale 1986;
consistent with the protologue is actually non-
Sipman & Aubel 1992; Elix 1993, 1995; Krog
isidiate and contains only medullary lobaric
1993; Marcelli 1993; Morales-Méndez et al. acid (Benatti 2010).
1995; Aptroot & Aubel 1999; Marcelli & Ri-
beiro 2002; Jungbluth et al. 2008; Spielmann
& Marcelli 2008), and it seemed an oppor- Materials and Methods
tune time to revise the genus. During this The morphological and anatomical characters of the
specimens were analyzed using standard stereoscopic
and compound microscopes. Anatomical sections, in-
M. N. Benatti: Instituto de Botânica, Seção de Micologia cluding those of apothecia and pycnidia when present,
e Liquenologia, Caixa Postal 68041, São Paulo / SP, CEP were cut by hand with a razor blade. The chemical
04045-972, Brazil. Email: michel_benatti@yahoo.com.br constituents were checked by spot tests with potassium
J. A. Elix: Research School of Chemistry, Building 33, hydroxide (K, 10% and 30%), sodium hypochlorite (C)
Australian National University, Canberra, A.C.T. 0200, and para-phenylenediamine (P), and also examined under
Australia. UV light (360 nm). Chemical constituents of all speci-
814 THE LICHENOLOGIST Vol. 44

mens were identified by thin-layer chromatography At least 16 ascospores (the usual content of two full
(TLC) using solvent C (Bungartz 2001), and selected asci) were measured per apothecium, but average size
specimens including all types were analyzed by HPLC. ranges were obtained from 32 ascospores. This was for
Types and additional specimens of all species cited all specimens examined that contained apothecia, in-
were studied and compared (43 specimens). The mor- cluding all types of accepted names and their synonyms.
phological terminology for lobe development follows A few mature apothecia were cut for each specimen.
that of recent publications (listed in the Introduction), A key for the nine currently known isidiate species
with two exceptions. Lacinules are adventitious, ribbon- containing C+ and KC+ substances (gyrophoric, lecanoric
like secondary outgrowths from the primary lobe mar- and lobaric acids) is presented. Other species are currently
gins or sometimes from the upper surface. Lobules are under study and this list will certainly grow. Table 1
similar, but short and rounded (Marcelli et al. 2011). compares the characteristics of the four species dis-
cussed in this paper.

Key to the isidiate species of Bulbothrix containing medullary gyrophoric,

lecanoric and lobaric acids
1 Thallus containing only medullary lobaric acid (C--, KC+ rose, UV+ bluish) . . . . 2
Thallus containing mainly medullary gyrophoric or lecanoric acids, some species
containing lobaric as an accessory substance . . . . . . . . . . . . . . . . . . . . . . . . . 3
2(1) Isidia eciliate; lower cortex black, brown margins of varying widths . . B. apophysata
Isidia ciliate; lower cortex entirely pale brown to tan . . . . . . . . . . B. thomasiana
3(1) Medulla C+ and KC+ red, containing lecanoric acid. . . . . . . . . . . B. laevigatula
Medulla C+ and KC+ rose, containing gyrophoric acid, with/without accessory
lobaric acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
4(3) Laciniae narrow, 01–07 mm wide; isidia ciliate. . . . . . . . . . . . . . . . . . . . . . . . 5
Laciniae broad, 05–30 mm wide; isidia eciliate . . . . . . . . . . . . . . . . . . . . . . . . 7
5(4) Laciniae 01–03 mm wide; lower cortex mottled black and brown, ascospores
bicornute, with pointed tips, 12–18  3–4 mm . . . . . . . . . . . . . . . . B. sipmanii
Laciniae 02–07 mm wide; lower cortex black with distinct brown margins;
ascospores ellipsoid, with rounded tips, 4–10  4–6 mm . . . . . . . . . . . . . . . . . 6
6(5) Cilia and rhizines simple to partially furcate; apothecia coronate; ascospores ellipsoid,
usually 80–100  45–60 mm . . . . . . . . . . . . . . . . . . . . . . . . . B. fungicola
Cilia and rhizines densely dichotomously branched; apothecia eciliate; rounded asco-
spores almost spherical, usually 40–60  40–50 mm . . . B. pseudofungicola
7(4) Laciniae 10–30 mm wide; upper cortex emaculate; isidia becoming tortuous and
often pycnidiate when mature; amphithecium often pycnidiate when mature;
medulla containing only gyrophoric acid . . . . . . . . . . . . . . . . . . . . B. papyrina
Laciniae 05–10 mm wide; upper cortex maculate; isidia usually more or less straight
and never developing pycnidia regardless of stage; medulla containing gyrophoric
and lobaric acids (see comments under B. scortella) . . . . . . . . . . . . . . . . . . . . 8
8(7) Lower cortex brown, with darker or paler margins; ascospores (60–)70–110(–125)
 40–60 mm; usually only medullary gyrophoric acid . . . . . . . . . . B. scortella
Lower cortex black, with brown margins, occasionally with very dark brown small
spots; ascospores (50–)60–80(–90)  40–50 mm; usually gyrophoric acid com-
bined with lobaric acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. subdissecta
2012 Identity of Bulbothrix goebelii—Benatti & Elix 815

The Species c. 05–20 mm wide, shiny to opaque, smooth,

weakly papillate, rhizinate; rhizines brown to
Bulbothrix goebelii (Zenker) Hale
light brown or whitish, usually paler than the
MycoBank No: MB 341599 cortex, initially simple or furcate at the margin
Smith. Contr. Bot. 32: 14 (1976). soon becoming repeatedly dichotomously or
Basionym: Parmelia goebelii Zenker, Pharm. Waarenk.1: irregularly branched, with basal or displaced
134 (1827); type: ‘‘Auf officinellen Rinden’’ in Goebel blackened bulbs, 010–050(–060)  c. 003
‘‘Auf Stücken der Loxachina.’’, América do Sul, collec- mm, abundant, often intertwined and aggluti-
tor unknown [lectotype (here designated)—M!].
nated, evenly distributed, almost appearing
(Fig. 1) as a tomentum.
Apothecia laminal or submarginal, common,
Thallus with sublinear to subirregular laci- subplane to concave, 03–31 mm diam.,
niae, up to 87 cm wide (type composed of adnate to substipitate, margins smooth to
small fragments about 1 cm wide), coriaceous subcrenate, amphithecia smooth, without
to subcoriaceous, corticolous or saxicolous, ornamentation or occasionally unevenly pyc-
greenish grey becoming dusky grey or dusky nidiate, ecoronate; disc brown, epruinose,
green in the herbarium; upper cortex 125– imperforate, epithecium 75–150 mm; hyme-
425 mm thick, algal layer 150–550 mm nium 350–550 mm, subhymenium 150–
thick, medulla 150–1300 mm thick; lower 300 mm; ascospores rounded to subspherical,
cortex 125–325 mm thick. Laciniae aniso- 40–65(–70)  40–60 mm, epispore c. 05
tomic to isotomic dichotomously or some- mm thick.
times irregularly branched, 03–19(–31) Pycnidia laminal to submarginal, scarce
mm wide, contiguous to slightly imbricate or to common, immersed, with black ostioles;
occasionally crowded, very adnate, strongly conidia bacilliform to weakly bifusiform, 50–
attached; apices plane to involute, truncate 75  c. 075 mm.
to subtruncate; margin sinuous to crenate or Chemistry. Colour reactions: upper cortex
subirregular, flat, entire to sometimes slightly
K+ yellow, UV--; medulla K--, C--, KC--, P--,
incised, not or scarcely sublacinulate, ciliate,
UV-- (KC+ rose and UV+ light blue under
axils oval to irregular. Upper surface contin-
the hymenial discs and amphithecia). TLC/
uous, smooth, with occasional transvere
HPLC: cortical atranorin and chloroatra-
cracks in older parts, laminal ciliary bulbs
norin; medullary lobaric, oxolobaric and co-
absent; maculae absent. Adventitious lacinules
lensoic acids, concentrated in the apothecia.
absent to scarce on older parts, very short,
simple, flat, 02–12  01–05 mm, trun- Distribution. The distribution cited by Hale
cate or acute, underside concolorous with (1976) includes several different species pre-
the lower margin. Cilia black to brown, viously synonymized under B. goebelli. The
initially simple soon becoming furcate and currently confirmed distribution, based on
then dichotomous or irregularly ramified, samples we have examined, includes South
005–040(–055)  c. 003 mm, with semi- America (from unknown localities, including
immersed to emergent basal bulbs c. 005– the type collection), Peru and Brazil (states
015 mm wide, abundant along the margins, of Goiás and Minas Gerais).
separate (005–010 mm) from one another
to contiguous mainly in the axils, absent or Comments. Hale (1976) faced difficult prob-
scarce at the apices. Medulla white. Soredia, lems regarding this species complex which
pustules and isidia absent. Lower surface he resolved by including eight names as
black with small dark brown to brown occa- synonyms of B. goebelii. Following careful
sional spots, slightly shiny to opaque, smooth examination of the type collection, checking
to subrugose, moderately to densely rhizi- Hale’s previous notes together with accom-
nate; marginal zone black, indistinct from panying chemical data, we were finally able
the centre to dark or light brown, attenuated, to understand the source of the confusion.
816 THE LICHENOLOGIST Vol. 44

Fig. 1. Bulbothrix goebelii. A, type collection; B, lectotype; C, detail of a Bulbothrix goebelii thallus showing the
apothecia under UV light (Spielmann et al. 2573, SP). Scales: A–C ¼ 1 cm. Incolour online.
2012 Identity of Bulbothrix goebelii—Benatti & Elix 817

The type collection of B. goebelii is a mix- smaller and more rounded than those de-
ture of small fragments of four different spe- scribed by Hale (1976) [40–65(–70) 
cies of Bulbothrix. A significant portion com- 40–60 mm vs. 80–100  40–60 mm] and
prises fragments of a fertile species which are among the smallest found in the genus.
lacks isidia and contains lobaric, oxolobaric Since Hale’s concept of B. goebelii (1976)
and colensoic acids (HPLC and TLC in comprised multiple morphologically and
solvent C). This specimen best fits the proto- chemically similar species, it was necessary
logue of Zenker (1827), and has been chosen to restudy and compare the synonyms and
as the lectotype of B. goebelii. As such, B. related specimens to determine whether or
goebelii could well be the primary, non- not they represent B. goebelii s. str. or other
isidiate counterpart of B. apophysata (Hale species (Benatti 2010).
& Kurok.) Hale (US! holotype, TNS! isotype). Other species similar to B. goebelii con-
It appears that the lobaric acid is concentrated taining medullary gyrophoric acid include
in the apothecia given that the medullary B. atrichella (Nyl.) Hale (H-NYL 35233!
spot tests on the laciniae are negative. lectotype, duplicates at FH-Tuck! and M!), a
The second most prominent component species which differs from B. goebelii by being
of the mixture is a sterile, isidiate species, distinctly maculate, in having black rhizines
with a black to dark brown lower cortex, without bulbs and somewhat larger ellipsoid
brown margins and black rhizines which ascospores (c. 60–80  40–50 mm). Bul-
contain medullary gyrophoric, lecanoric and bothrix semilunata (Lynge) Hale (S! holotype)
lobaric acids. This fragment is entirely con- differs in having narrower laciniae (c. 02–05
sistent with B. subdissecta (Nyl.) Hale and mm wide), coronate apothecia and larger bi-
its latter synonym B. lobarica Jungbluth et al. cornute, crescent-shaped ascospores c. 120–
( Jungbluth et al. 2008). The mixture of these 230 mm long. Bulbothrix coronata (Fée) Hale
two species probably caused Hale (1976) to (G! lectotype) can be distinguished from B.
interpret B. goebelii as an isidiate species con- goebelii by the coronate apothecia and the
taining gyrophoric acid, which was subse- larger ellipsoid ascospores 60–100  40–
quently followed by other authors. 60 mm.
The third species present in the mixture Additional specimens examined. South America, un-
consists of a fragment with rounded lobes, known collector, fragment numbers 5 and 6 (G, together
dense maculae, unbranched cilia and rhizines, with the type material of B. coronata). Peru: Dept. San
a brown lower cortex and medulla with a K+ Martin: Prov. San Martin, Tarapoto, NE of Hotel de
yellow ! red reaction (salazinic acid), and is Turistas, c. 6 30 0 S, c. 76 20 0 W, alt. 350 m, 12 iii 1981,
R. Santesson & G. Thor P71:24 (S).—Brazil: Goiás:
probably identical with B. hypocraea (Vain.) Água Fria Municipality, Repeater Station of Telebrası́lia
Hale. Another very small isidiate fragment de Roncador, alt. 1200m, 1992, G. Hatschbach, M.
on a sliver of bark above the previous species, Hatschbach & E. Barbosa 58330 (C); ibid, Serra Dourada
has a brown lower cortex (a different shade of Municipality, 120 km NW of Goiânia, 50 10 0 W,
16 04 0 S, c. 850 m alt., 1990, T. H. Nash 29337
brown from the major isidiate thallus), con- (CANB); ibid.,, Alto Paraı́so de Goiás Municipality,
tains gyrophoric acid, and is most likely a Chapada dos Veadeiros, 1991, M. P. Marcelli & O.
fragment of B. scortella (Nyl.) Hale. Yano 11126 (SP). Minas Gerais: Catas Altas Municipal-
The apothecia represent the most striking ity, Parque Natural do Caraça, 1265 m alt., 20 06 0 0600 S,
43 29 0 12900 W, 2006, A. A. Spielmann, L. S. Canêz
feature of B. goebelii: they concentrate lobaric & M. P. Marcelli 2260, 2261 (SP); ibid., 1260 m alt.,
acid which reacts KC+ (violet) pink and 20 06 0 01300 S, 43 29 0 09000 W, 2006, A. A. Spielmann,
emits a strong blue fluorescence under UV L. S. Canêz & M. P. Marcelli 2573 (SP).
light. These reactions were not observed in
any other part of the thalli, which were nega- Bulbothrix papyrina (Fée) Hale
tive to all colour tests. MycoBank No: MB 341606
The ascospores of the lectotype and the Phytologia 28(5): 480 (1974).
other specimens of B. goebelii studied are Basionym: Parmelia papyrina Fée, Essai sur les crypt.
des écorces exot. offic. suppl.: 121 (1837); type: South
818 THE LICHENOLOGIST Vol. 44

America, on bark of Cinchona sp., locality and collector the apices of the laciniae. Medulla white. Sor-
unknown (G!—holotype). edia and pustules absent. Isidia scarce to fre-
Synonyms: Parmelia granatensis Nyl. Flora 68: 613
(1885); type: Colombia, Nova Granata, Socorro, alt. quent or abundant in older parts, laminal to
1200 m, 1863, A. Lindig s.n. (H-NYL 35170!—lectotype, occasionally submarginal, granular to mostly
as in Hale 1976). smooth cylindrical, straight when young to
Parmelia addenda Vain. Hedwigia 46: 169 (1907); tortuous when mature, 005–070  c. 005–
type: Thailand, Sinus Bengalensis, ad corticem Arecae
catechu prope Lem Dan, in insula Koh Chang, 1900,
010 mm, simple to sparsely branched, erect
J. Schmidt X, (C!—lectotype; TUR-V!—duplicate as to partially procumbent, firm to caducous,
in Hale 1976). concolorous or with brownish apices, eciliate,
Parmelia acariospora Zahlbr. Denks. der Akad. der Wiss. often partially pycnidiate when mature. Lower
in Wie, Math.-Naturwiss Klasse 83: 169 (1909); type: surface black, shiny, smooth to subrugose, e
Brazil, Prov. São Paulo, in itiniere S. Amaro-Barra
Mansa in districtu urbis Itapecerica, 800–900 m, June papillate, densely rhizinate. Marginal zone
1901, Schiffner s. n., (W!—lectotype; W!, US!—dupli- brown to light brown, becoming darker to-
cates as in Hale 1976). wards the centre, attenuated, c. 05–40 mm
wide, shiny, smooth to subrugose, e papil-
(Fig. 2) late, becoming partially rhizinate nearer to
the centre. Rhizines black to partially brown
Thallus sublinear laciniate, pale dusky brown or with whitish apices, initially simple or
in the herbarium, up to 97 cm diam., sub- furcate but soon becoming richly dichoto-
membranaceous to subcoriaceous, cortico- mously or irregularly branched, often with
lous; upper cortex 150–225 mm thick, algal subtle, basal blackish bulbs, 005–050 
layer 250–375 mm thick, medulla 650– c. 003–005 mm, frequent to abundant, par-
875 mm thick, lower cortex 100–175 mm tially intertwined and agglutinated at some
thick. Laciniae anisotomic, dichotomously parts, evenly distributed.
or trichotomously to irregularly branched, Apothecia laminal or submarginal, com-
(03–)10–24 (–31) mm wide, contiguous mon, subconcave to subplane or plane, 03–
to slightly imbricate, adnate and adpressed 32 mm diam., sessile to adnate or substi-
to occasionally undulate on older parts, apices pitate, margins smooth to occasionally sub-
plane, truncate to subtruncate, margin smooth crenate, amphithecia smooth, without orna-
and slightly sinuous to subcrenate or irregular, mentations or occasionally subrugose and
flat to slightly involute, entire to slightly in- unevenly pycnidiate, ecoronate. Disc light
cised, rarely sublacinulate, axils oval to irre- brown, epruinose, imperforate, epithecium
gular. Upper surface continuous, smooth to 50–125 mm; hymenium 300–450 mm, sub-
subrugose, with occasional fissures, laminal hymenium 100–300 mm. Ascospores sub-
ciliar bulbs absent. Maculae absent, only rounded to ellipsoid or oval, (50–)60–
scars left by eroded isidia. Adventitious mar- 105  40–60(–85) mm, epispore c. 075
ginal lacinules absent to scarce or scattered mm.
in older parts, short, simple to furcate or Pycnidia submarginal or on the isidia, very
irregularly branched, flat, 02–17  01–06 scarce to common, immersed, with black
mm, truncate or acute, underside concolo- ostioles. Conidia bacilliform, 40–60  c. 05
rous with the lower margin. Cilia black, apices mm.
initially simple or furcate and soon becoming
subdichotomously or irregularly ramified at Chemistry. Colour reactions: upper cortex
the axils (very brittle and absent in part), K+ yellow, UV--; medulla K--, C+ rose to
005–025(–040)  c. 003 mm, with semi- reddish rose, KC+ rose to reddish rose, P--,
immersed to immersed bulbate bases c. 005– UV-- or + weakly pale bluish. TLC: cortical
010 mm wide, frequent throughout the atranorin; medullary gyrophoric acid (also
margins, spaced 005–010 mm from each mentioned by Hale as he erroneously inter-
other to abundant and contiguous at the axils preted it as a synonym of B. goebelii, see Hale
and some random parts, becoming sparse at 1976).
2012 Identity of Bulbothrix goebelii—Benatti & Elix 819

Fig. 2. Bulbothrix papyrina (holotype); B, Parmelia acariospora (lectotype); C, Parmelia addenda, (lectotype);
Parmelia granatensis (lectotype). Scales: A–D ¼ 1 cm. In colour online.
820 THE LICHENOLOGIST Vol. 44

Distribution. The names Parmelia addenda, Thallus sublinear to linear laciniate, pale
P granatensis and P. acariospora were all cited dusky, greenish or olivaceous grey in the her-
for the following locations: Asia (Thailand), barium, up to 65 cm diam., subcoriaceous
Carribean (Guadalupe, Martinique), and to submembranaceous and fragile, cortico-
South America (Brazil, Colombia) (Fée 1837; lous; upper cortex 125–150 mm thick, algal
Nylander 1885; Vainio 1907, 1915; Zahl- layer 200–275 mm thick, medulla 375–
bruckner 1909; Lynge 1914). Based on type 500 mm thick; lower cortex 125–200 mm
specimens and additional materials, the spe- thick. Laciniae isotomic to anisotomic di-
cies is confirmed for Asia (Thailand) and chotomously, trichotomously or irregularly
South America (Colombia and Brazil, Mato branched, 03–12(–16) mm wide, contigu-
Grosso and São Paulo states). ous to slightly imbricate or rarely crowded in
the centre, very adnate and appressed, apices
Comments. The type material is a small but
plane, truncate to subtruncate; margin smooth
entire thallus which has been significantly
and sinuous to subcrenate or subirregular,
damaged and has few isidia. Few pycnidia flat, entire to incised, partially sublacinulate,
were seen in this specimen and they are par-
axils oval to irregular. Upper surface continu-
ticularly rare on the isidia; conidia were not
ous and smooth, with occasional irregular
observed. The apothecia are well developed
fissures in older parts, laminal ciliar bulbs
and contain mature ascospores. Occasionally,
absent. Maculae weak, punctiform, laminal,
the pycnidia may also occur, scattered on the
sparse to e frequent, amidst scars left by
amphithecia. The pycnidiate isidia are a com-
eroded isidia. Adventitious marginal or lami-
mon, but variable feature in this species and
nal lacinules sparse to frequent, especially on
may be dependent upon the stage of isidial
older parts, sometimes growing amidst the
development. The upper surface is more
isidia, short, simple to furcate or irregularly
densely isidiate than those of other species branched, flat, 03–20  01–03(–05) mm,
of this group.
truncate or acute, underside concolorous with
For comparisons with B. scortella and B.
the lower margin. Cilia black to brown or occa-
subdissecta, see below. sionally whitish, apices initially simple soon
Additional specimens examined. Brazil: Mato Grosso: becoming furcate and then subdichotomously
Santa Anna da Chapada, in margine silvae minus densa, branched, 005–015(–025)  c. 003 mm,
9 iii 1894, G. O. Malme s. n. (UPS); Santa Anna da Cha-
pada, 1894, G. O. Malme 2435 (LD); Santa Anna da
with semi-immersed to immersed bulbate
Chapada, 625–1100 m alt., 1894, G. O. Malme 2509b bases c. 005–010(–015) mm wide, fre-
(US); ibid., between Jaciara and São Vicente, km 313 quent to abundant along the margins, spaced
da BR-364, c. 100 km ESE de Cuiabá, 750 m alt., 1980, 005–010 mm from each other to contigu-
M. P. Marcelli 9148 (SP).
ous in the axils, becoming sparse or absent
at the apices or random parts of the laciniae.
Bulbothrix scortella (Nyl.) Hale Medulla white. Soredia and pustules absent.
MycoBank No: MB 341610 Isidia sparse to frequent, laminal, granular
Phytologia 28(5): 480 (1974). to smooth cylindrical, straight to slightly
Basionym: Parmelia scortella Nyl. Flora 68: 615 (1885); tortuous, 005–035(–050)  c. 005 mm,
type: [United States of America], America Septentriona- simple to sparsely branched, erect to procum-
lis, Texas, 1850, C. Wright [FH-Tuck!—lectotype (Hale bent in part, firm to caducous, concolorous or
1976); H-NYL!—duplicate].
Synonyms: Parmelia njalensis Dodge, Ann. Miss. Bot. with pale brownish apices, eciliate. Lower sur-
Gard. 46: 65 (1959); type: Sierra Leone, Kori, Njala, face brown to dark brown, occasionally almost
on bark of Funtumia africana, Deighton M5642 (BM!— blackish in random spots, shiny to opaque,
holotype).—Parmelia marginalis Lynge. Ark. för Bot. smooth to subrugose, densely rhizinate.
13(13): 112 (1914); type: Brazil, Mato Grosso, 1914, Marginal zone brown to dark brown and in-
Brasiliae civit. Matto Grosso, Santa Anna da Chapada, in
margine silvae, ad corticem, 21-II-1894, Malme 2393 distinct or somewhat darker than the centre
(S!—holotype). and attenuated, c. 05–15 mm wide, shiny,
smooth, partially papillate, weakly to densely
(Fig. 3A–C) rhizinate. Rhizines cream to light or dark
2012 Identity of Bulbothrix goebelii—Benatti & Elix 821

Fig. 3. A, Bulbothrix scortella (lectotype); B, Parmelia marginalis (holotype); C, Parmelia njalensis (holotype); D,
Bulbothrix subdissecta (lectotype). Scales: A–D ¼ 1 cm. In colour online.
822 THE LICHENOLOGIST Vol. 44

brown, occasionally blackish or with whitish Small pieces of a Punctelia species are inter-
apices, usually paler than the lower cortex, mixed with these fragments.
initially simple or furcate soon becoming Bulbothrix scortella is distinguished from B.
richly dichotomously branched, usually with goebelii by the presence of sparse to frequent
subtle basal or displaced blackish bulbs, isidia, medullary gyrophoric acid and the
010–060  c. 003–005 mm, abundant and brown colour of the lower cortex. It is the
tomentum-like, evenly distributed. only species of this group that has a brown
Apothecia laminal or submarginal, common, lower cortex with tan margins, rather than
subconcave to plane, 02–26 mm diam., black with brown margins (Moore 1968),
adnate to sessile, margins smooth to partially although most specimens examined here often
subcrenate, amphithecia smooth, occasion- have darker brown margins.
ally with sparse isidia, ecoronate. Disc light By contrast, both B. papyrina and B. sub-
brown, epruinose, imperforate; epithecium dissecta have a black lower cortex and brown
75–100 mm, hymenium 350–450 mm, margins, further differentiated by the width
subhymenium 350–500 mm. of the laciniae (in the case of B. papyrina),
Ascospores subglobose to ellipsoid or oval, the presence/absence of cortical maculae,
sometimes with weakly acuminate apices, the size and shape of the isidia and the me-
(55–)70–110(–125)  40–50(–60) mm, dullary chemistry (all B. papyrina specimens
epispore 05–10 mm. examined contain only gyrophoric acid as
Pycnidia submarginal, sparse, immersed, a medullary substance). No intermediate
with black ostioles. Conidia bacilliform to specimens with variable lower surface colour
weakly bifusiform, some appearing weakly were found, as was observed in specimens
sublageniform, (40–)50–70  c. 075 mm. of B. ventricosa (Hale & Kurok.) Hale or B.
viatica Spielmann & Marcelli (Benatti 2012).
Chemistry. Colour reactions: upper cortex For comparisons with B. subdissecta, see
K+ yellow, UV--; medulla K--, C+ rose to
below and Table 1.
reddish rose, KC+ rose to reddish rose, P--,
UV--. TLC/HPLC: cortical atranorin; medul- Additional specimens examined. Malaysia: Sabah:
lary gyrophoric acid [also mentioned by Hale Sungei Bating road, about 15 mi NW of Sandakan,
c. 10 m alt., 1965, M. E. Hale 30598, 30599, 30600
(1976) as he erroneously interpreted it as a (US).—South Africa: Cape Prov.: District Knysna, 6 mi
synonym of B. goebelii ]. The lectotype also N of town, 1953, O. Almborn 2664 (LD); ibid., Wynberg
contains traces of medullary lecanoric, lobaric District, Kirstenbosch, 1953, O. Almborn 1381 (US).—
and oxolobaric acids, possibly contaminants. USA: Florida: Lake County, Leesburg, 1967, B. J. Moore
4104 (DUKE). North Carolina: Brunswick County, Smith
Distribution. The names Parmelia scortella, Island, Bald Head, 1959, W. L. Culberson 8064 (DUKE).
P. njalensis and P. marginalis were cited for Georgia: Hancock County, Piedmont, 33o50 0 N, 83o48 0 W,
1992, F. H. M. Crew s. n. (DUKE).—Cuba: about half-
the following localities: Asia (Japan), Africa way up Loma Del Gato, Sierra Maestra, Oriente, 1959,
(Sierra Leone), USA, South America (Vene- H. A. Imshaug 24952 (US).—Dominican Republic:
zuela and Brazil) (Nylander 1885, 1890; Province La Vega: vicinity of Piedra Blanca, near Good-
Lynge 1914; Vainio 1915; Dodge 1959; rich rubber grove, 200–500 m, 1947, H. A. Allard 16829
(US).—Brazil: Mato Grosso: km 313 of BR-364 high-
McCullough 1964; Moore 1968). Here the way, between Jaciara and São Vicente, c. 100 km ESSE
species is confirmed for Asia (Malaysia), of Cuiabá, 750 m alt., 1980, M. P. Marcelli 8441, 9131,
Africa (South Africa), USA (states of Florida, (SP). Minas Gerais: Tiradentes Municipality, base of the
Georgia and North Carolina), Caribbean São José Mountain Range, 1993, M. P. Marcelli, T. Ahti
& O. Yano 25677 (SP). São Paulo: Santa Rita do Passa
(Cuba, Hispaniola) and South America
Quatro Municipality, fazenda Vassununga, km 259 of the
(Brazil, states of Mato Grosso, Minas Gerais Anhanguera Highway, 760 m alt., 1978 , M. P. Marcelli &
and São Paulo). B. L. Morretes 15629 (SP).

Comments. The lectotype of Parmelia scor- Bulbothrix subdissecta (Nyl.) Hale

tella (Fig. 8) consists of four fragments from
25 to 65 cm in diam., the largest of the frag- MycoBank No: MB 341615
ments almost comprising an entire thallus. Phytologia 28(5): 481 (1974).
2012 Identity of Bulbothrix goebelii—Benatti & Elix 823

Table 1. Comparative diagnostic characteristics of Bulbothrix goebelii, B. papyrina, B. scortella and B. subdissecta.
The data refer to the most typical range found.

Lower cortex Medullar

Species Laciniae width Propagules colour substance(s) Ascospore sizes

B. goebelii 10–30 mm Absent Black centre, Lobaric acid 40–70  40–60 mm

brown margins
B. papyrina 10–30 mm Isidiate Black centre, Gyrophoric 60–105  40–60 mm
(pycnidiate) brown margins acid
B. scortella 05–15 mm Isidiate Brown centre Gyrophoric 70–125  40–60 mm
(unornamented) and margins acid*
B. subdissecta 05–15 mm Isidiate Black centre, Gyrophoric and 60–90  40–50 mm
(unornamented) brown margins lobaric acids

* At the present, it is uncertain if other substances are, or are not, in fact, produced by B. scortella, how much
variability there is, or if contaminants are possibly involved.

Basionym: Parmelia subdissecta Nyl, Jour. Linnean Soc., isidia, short, simple to furcate, dichotomous
London 20: 51 (1884); type: Malaysia, Malacca, Tanjong, or irregularly branched, flat, 03–24  01–
on cocoa-palms, 9 November 1866, A. C. Maingay 2865
(H-NYL!—holotype; BM!—isotype). 03 mm, truncate or acute, underside con-
Synonym: Bulbothrix lobarica Jungbluth, Marcelli & colorous with the lower margin. Cilia black
Elix, Mycotaxon 104: 57 (2008); type: Brazil, São Paulo, to occasionally brown or whitish, apices
Itirapina Municipality, Estação Experimental do Instituto initially simple but soon becoming furcate,
Florestal, 22 15 0 S 47 49 0 W, 770 m alt., along the trail
inside cerradão next to Pedregulho, on a tree trunk, 24
trifurcate and then dichotomous or irregu-
March 2004, L. S. Canêz, P. Jungbluth & A. A. Spiel- larly branched, 005–020(–025)  002–
mann 1174 (SP!—holotype). 003 mm, with semi-immersed to immersed
bulbate bases c. 005(–010) mm wide, abun-
(Fig. 3D) dant along the margins, separate (005 mm)
Thallus sublinear laciniate, pale dusky green from one another to contiguous, becoming
to grey in the herbarium, fragments up to 48 sparse or absent at the apices of the laciniae.
cm diam., subcoriaceous to submembrana- Medulla white. Soredia and pustules absent.
ceous and fragile, corticolous; upper cortex Isidia frequent, laminal to rarely marginal,
100–175 mm thick, algal layer 150–250 granular to smooth cylindrical, straight to
mm thick, medulla 200–525 mm thick, lower slightly twisted 005–025(–035)  c. 005
cortex 75–250 mm thick. Laciniae aniso- mm, simple to rarely sparsely branched,
tomic dichotomously or trichotomously to ir- erect to partially procumbent, firm to cadu-
regularly branched, (03–)04–12 mm wide, cous, with concolorous or brownish apices,
contiguous to slightly imbricate, very adnate eciliate. Lower surface black, occasionally with
and adpressed, apices plane, truncate to sub- dark brown spots, shiny, smooth to sub-
truncate, margin smooth and sinuous to sub- rugose, weakly papillate, densely rhizinate.
crenate or subirregular, flat, entire to incised, Marginal zone brown to light brown, attenu-
partially sublacinulate, axils oval to irregular. ated, c. 02–15 mm wide, shiny, smooth,
Upper surface continuous and smooth, with weakly papillate, partially rhizinate. Rhizines
occasional irregular or transverse fissures in black to brown or light brown especially close
older parts, laminal ciliar bulbs absent. Mac- to the margins, occasionally with whitish
ulae weak to distinct, punctiform, laminal, apices, initially simple soon becoming fur-
intermixed with scars left by eroded isidia. cate and then dichotomously or irregularly
Adventitious marginal or rarely laminal laci- branched, with subtle basal or displaced black-
nules frequent to absent, often present on ish bulbs in part, 010–030(–040)  003–
older parts, sometimes intermixed with the 005 mm, abundant almost forming a tomen-
824 THE LICHENOLOGIST Vol. 44

tum, often intertwined with one another and and laminal adventitious lacinules amidst
the cilia, evenly distributed. the isidia, similar to those of B. scortella. Cilia
Apothecia (very sparse and juvenile in the vary from being simple to dichotomously
holotype) laminal or submarginal, sparse to branched. While in some thalli dichotomous
common, e plane, 03–14 mm diam., ad- cilia are best developed in the axils, in others
nate, margins smooth, amphithecia smooth, the cilia are more densely branched all along
without ornamentation, ecoronate. Disc dark the margins apart from the apices of laciniae.
brown, epruinose, imperforate; epithecium Although there is considerable variation, the
100–150 mm, hymenium 300–350 mm, rhizines in B. subdissecta are usually paler
subhymenium 200–250 mm. Ascospores ellip- than the lower cortex, except for the type
soid to oval, 50–80(–90)  40–50 mm, and several other specimens where black rhi-
epispore c. 1.0 mm. zines predominate. As mentioned by Hale
Pycnidia laminal to submarginal, sparse, (1976), the Asian populations tend to have a
immersed, with black ostioles. Conidia bacil- black lower surface with black, more sparsely
liform to weakly or evidently bifusiform, branched rhizines compared to specimens
(40–)50–60  05–10 mm. from the Americas.
Bulbothrix scortella differs from B. subdis-
Chemistry. Colour reactions: upper cortex
secta in having a predominantly brown lower
K+ yellow, UV--; medulla K--, C+ rose to
cortex and larger ascospores (80–120 
reddish rose, KC+ rose to reddish rose, P--,
40–60 mm versus 50–80  40–50 mm).
UV+ faint bluish (sometimes weak, almost
Other characters mostly overlap, and molec-
UV--). TLC/HPLC: cortical atranorin; me-
ular studies are probably needed to confirm
dullary gyrophoric, lecanoric, lobaric, oxolo-
the integrity of these two species.
baric, ehiascic (trace) acids (see also Hale
Bulbothrix apophysata is morphologically very
1976). similar to B. subdissecta and differs mainly in
Distribution. The names Parmelia subdis- containing medullary lobaric acid rather than
secta and Bulbothrix lobarica were all cited for gyrophoric acid. Bulbothrix fungicola (Lynge)
the following locations: Asia (Philippines, Hale (S!, lectotype) differs in having nar-
Malaysia), Caribbean (Hispaniola), Central rower laciniae, small ciliate isidia with tiny
America (Panama) and South America bulbs, simple to partially furcate cilia and
(French Guiana, Brazil) (Nylander & Crom- rhizines, coronate apothecia and larger as-
bie 1884; Vainio 1909; Jungbluth 2006; cospores (80–100  40–60 mm) and by
Jungbluth et al. 2008). Based on type speci- the presence of only gyrophoric acid in the
mens and additional materials, the species is medulla.
confirmed for Asia (Philippines), Central Bulbothrix laevigatula (Nyl.) Hale (H-NYL
America (Dominican Republic and Panama) 35653! holotype, PC! isotype) is quite similar
and South America (Peru and Brazil, Goiás, to B. subdissecta, but differs in containing
Mato Grosso, and São Paulo states). medullary lecanoric acid. Like Hale (1976),
we could not find other clearly distinct mor-
Comments. The holotype is a small thallus phological differences between the species.
on tree bark and is in good condition. There
are very few apothecia which do not exceed Additional specimens examined. Philippines: Quezon
Prov.: Luzon, c. 300 m alt., Chuan logging area, Sierra
03 mm in width, all with poorly developed Madre, about 15 km east of Pagbilao, 1964, M. E. Hale
hymenia, as well as a few pycnidia. The & J. Banaag 26915 (LD).—Dominican Republic: in
duplicate is similar but has better developed ravine in Sabana de la Rosa near km 28 on Duarte High-
apothecia containing ascospores. way, 1947, H. A. Allard 15955 (US).—Panama: Canal
The upper surface of most specimens of B. Zone, F. Drayton Trail, Barro Colorado Island, 50–150 m,
1977, M. E. Hale 47710 (US).—South America: ‘‘Auf
subdissecta is maculate, and even when there officinellen Rinden’’, unknown collector (mixed part of
are scars left by eroded isidia, they are often the type collection of Bulbothrix goebelii, M!).—Peru:
incorporated within the maculae. In addi- Dept. San Martı́n: Tingo Marı́a, 625–1100 m alt., 1949/
tion, this species often develops marginal 1950, H. A. Allard 22581a (US).—Brazil: Mato Grosso:
2012 Identity of Bulbothrix goebelii—Benatti & Elix 825

Buriti, Chapada dos Guimarães, near the MT-305 High- Jungbluth, P. (2006) A famı́lia Parmeliaceae ( fungos
way, 1980, 600 m alt., M. P. Marcelli 8356 (SP). Goiás: liquenizados) em fragmentos de cerrados do Estado de
Rio Verde, between Jataı́ and Rio Verde, BR-060, 485 São Paulo. M.Sc. Dissertation, Instituto de Botâ-
km before Rio Verde, 780 m alt., 1980, M. P. Marcelli nica, São Paulo.
8028, 8041 (SP); ibid., Alto Paraı́so de Goiás, Chapada Jungbluth, P., Marcelli, M. P. & Elix, J. A. (2008) Five
dos Veadeiros, near the GO-118 (BR-010) Highway, new species of Bulbothrix (Parmeliaceae) from cer-
1250 m alt., 1991, M. P. Marcelli & O. Yano 11106 rado vegetation in São Paulo State, Brazil. Myco-
(SP); ibid., Fazenda Palmital, beside the GO-118 (BR- taxon 104: 51–63.
010) Highway, c. 10 km from Alto Paraı́so beside the Krog, H. (1993) Parmelina enormis (Hale) Hale is Bulbo-
Highway, 1560 m alt., 1991 M. P. Marcelli & O. Yano thrix enormis (Hale) Krog comb. nov. Lichenologist
11109A (SP). 25: 299–300.
Lynge, B. (1914) Die Flechten der ersten Regnellschen
The authors wish to thank the curators of BM (Scott Expedition. Die Gattungen Pseudoparmelia gen. nov.
LaGreca), C (Eric Hansen), CANB (Brendan Lepschi), und Parmelia Ach. Arkiv för Botanik 13: 1–172.
DUKE (Kathleen Pryer), FH (Donald Pfister), G McCullough, H. A. (1964) Foliose and fruticose lichens
(Philippe Clerc), H (Leena Myllys), L (Erik Smets), of the Piedmont Upland of Alabama. Bryologist 67:
LD (Arne Thell), LWG (Tariq Husain), M (Andreas 226–233.
Beck), PC (Bruno Dennètiere), S (Anders Tehler), Marcelli, M. P. (1993) Pequenas Parmelia s .lat. (lı́quens:
TNS (Yoshihito Ohmura), TUR (Seppo Huhtinen), Ascomycotina) ciliadas dos cerrados brasileiros. Acta
US (Rusty Russell), UPS (Anders Nordin) and W Botanica Brasilica 7: 25–70.
(Uwe Passauer) for the loans of the type specimens and Marcelli, M. P. & Ribeiro, C. H. (2002) Twenty-one
additional material, and Richard Harris and an anony- new species of Parmeliaceae (lichenized fungi) from
mous reviewer for critical revision of the manuscript. southeastern Brazil. Mitteilungen aus dem Institut für
Allgemeine Botanik Hamburg 30–32: 125–155.
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