Introduction
Heterodermia Trevis. is a genus of macrolichens in the Physciaceae (Jungbluth & Marcelli Reference Jungbluth and Marcelli2012) with c. 175 species worldwide (Lücking et al. Reference Lücking, Hodkinson and Leavitt2017). The species are most common in tropical mountain regions, occurring mostly on tree bark or twigs but some species also, or even only, occur on rock or compacted soil.
The study of the genus started with Taylor (Reference Taylor1847), who described the first species that would later be accepted in Heterodermia. Kurokawa (Reference Kurokawa1962) made a monograph of the genus but still treated it as Anaptychia Körb. Later, Kurokawa (Reference Kurokawa1998) and Trass (Reference Trass1992) provided lists of accepted species and valid combinations.
Although the difference between Anaptychia and Heterodermia was clear from the beginning, the distinction from Physcia (Schreb.) Michx. caused more problems. It was Swinscow & Krog (Reference Swinscow and Krog1976) who reported the distinguishing character, as well as providing a key to Heterodermia species for East Africa that has been used all over the tropics since. The common Physcia species that had been confused with Heterodermia for a long time was described as Physcia atrostriata Moberg and was treated in Moberg (Reference Moberg1990). Several regional revisions are available: Aptroot (Reference Aptroot1988) treated the species from the Guianas; Scutari (Reference Scutari1995) treated the species from a region in Argentina; Moberg & Nash (Reference Moberg and Nash1999) treat the species known from a larger desert region on the border of Mexico and the USA; Chen & Wang (Reference Chen and Wang2001) made one of the first local treatments for China of part of the genus with a more refined species concept; Lendemer (Reference Lendemer2009) treated the species from the USA; Moberg (Reference Moberg2011) treated the species of Heterodermia known from Central and South America, but applied a very wide species concept, accepting only 33 species which is less than currently known for even some states in Brazil; Rodriguez et al. (Reference Rodriguez, Estrabou and Quiroga2012) treated the species from a different region in Argentina; Michlig et al. (Reference Michlig, Rodríguez, Aptroot, Niveiro and Ferraro2017) described several new species within the H. comosa (Eschw.) Follman & Redon group from Argentina, some of which also occur in Brazil. In their treatment for Thailand, Mongkolsuk et al. (Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015) stressed the importance of terpenoid chemistry, the overall thallus appearance, and anatomy. In addition, they attempted to split the monophyletic genus Heterodermia into several groups, in which they formally described the genera Leucodermia Kalb and Polyblastidium Kalb. In their paper, Heterodermia s. str. are the species with a lower cortex present. They treated two further informally named species groups, but the phylogenetic position of neither the named nor the unnamed groups as shown.
From Brazil, 41 species have so far been reported (see references below under the respective species), plus a small number of subspecific taxa. For instance, Eliasaro (Reference Eliasaro1992) and Eliasaro & Fleig (Reference Eliasaro and Fleig1994) treated the species from Rio Grande do Sul. In addition, in an unpublished thesis dealing mostly with São Paulo specimens, Martins (Reference Martins2007) distinguished 17 additional, undescribed new species. Marcelli & Martins (Reference Marcelli and Martins2007) and Marcelli (Reference Marcelli2013) published some chapters from this work, but not the key or the new species. Two of the new species were described, one by Marcelli et al. (Reference Marcelli, Jungbluth, Benatti, Spielmann, Canêz, Cunha and Martins2007) and one by Benatti & Marcelli (Reference Benatti and Marcelli2017). Both were not very distinct species and they are not accepted below. Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019) accepted some of these new species and reported them from Santa Catarina, also adding three new, so far undescribed species.
Here, we revised the species of the genus Heterodermia reported from Brazil based on literature references, public databases and the examination of over 500 specimens, mostly collected by ourselves and L. S. Canêz in 15 states all over the country. Fifteen species are described as new, partly based on our own material, partly by validating and describing some of the species distinguished by Martins (Reference Martins2007). Twelve further species are new reports for Brazil. We provide a key for all accepted species now known from Brazil.
Material and Methods
We based our investigations on reports in the pertinent literature (e.g. Kurokawa Reference Kurokawa1962, Reference Kurokawa1998; Eliasaro Reference Eliasaro1992; Eliasaro & Fleig Reference Eliasaro and Fleig1994; Martins Reference Martins2007; Moberg Reference Moberg2011; Mongkolsuk et al. Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015), the observation of material and after consulting the databases of the herbaria B, CNHLH and UPS. Identification and descriptive work was carried out at the Universidade Federal de Mato Grosso do Sul using an Olympus SZX7 stereomicroscope and an Olympus BX50 compound microscope connected to a Nikon Coolpix digital camera. Sections were mounted in water, in which all measurements were also taken. The specimens from this study are mostly preserved in the herbarium CGMS.
Descriptions use and follow generally applied terms and patterns; arachnoid denotes a floccose hyphal layer at the lower surface. The algal layer is continuous, unless specifically mentioned as discontinuous.
The chemistry of all specimens was investigated by thin-layer chromatography (TLC) using solvent A (Orange et al. Reference Orange, James and White2001). As reported by Mongkulsuk et al. (Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015), this solvent gives the best results for the separation of the substances generally found in Heterodermia. For the identification of substances, we consulted Mongkolsuk et al. (Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015) and Schumm & Elix (Reference Schumm and Elix2015). Many specimens were tested with potassium hydroxide (K) on the upper lobe tips; in Heterodermia this is the best area for spot reactions since the medulla is often thin and testing the lower surface may give other results because there are often pigments present with separate reactions. The upper surface of the lobe tip reacts yellow when only atranorin and terpenoids (and sometimes dissectic acid) are present in the cortex and medulla, respectively, and the reaction becomes red when salazinic and/or norstictic acid are also present in the medulla; when a pigment was present on the lower surface, the pigment was also tested.
Total DNA was extracted from 18 selected dried specimens, all collected in Mato Grosso do Sul, Santa Catarina and Rio Grande do Sul in 2018 and 2019 (Supplementary Material Table S1, available online), employing a modification of Murray & Thompson's (Reference Murray and Thompson1980) protocol. A portion was macerated with the aid of a micropestle in 600 μl CTAB buffer (CTAB 2%, NaCl 1.4 M, EDTA (pH 8.0) 20 mM, Tris-HCl (pH 8.0) 100 mM). The resulting mixture was incubated for 15 min at 65 °C. A similar volume of chloroform:isoamilalcohol (24:1) was added and carefully mixed with the samples until their emulsion. It was then centrifuged for 10 min at 13 000 g and the DNA in the supernatant was precipitated with isopropanol. After a new centrifugation of 15 min at the same speed, the pellet was washed in 70% cold ethanol, centrifuged again for 2 min and dried. It was finally resuspended in 200 μl of ddH2O. PCR amplification was performed with the primers ITS1F and ITS4 (White et al. Reference White, Bruns, Lee, Taylor, Innis, Gelfand, Sninsky and White1990; Gardes & Bruns Reference Gardes and Bruns1993) for ITS. PCR reactions were performed under a program consisting of a hot start at 95 °C for 5 min, followed by 35 cycles at 94 °C, 54 °C and 72 °C (for 45, 30 and 45 s respectively) and a final 72 °C step for 10 min. PCR products were checked in 1% agarose gels and positive reactions were sequenced with the primer ITS4. Chromatograms were checked searching for putative reading errors, and these were then corrected. Sequences were downloaded and analyzed with Geneious. A full search for the best scoring maximum likelihood tree was performed in RAxML (Stamatakis Reference Stamatakis2006).
Results
Based on an evaluation of literature reports and examination of materials, we accept 68 different species of Heterodermia known from Brazil, 15 of which are newly described below and 10 are new records.
We adopted, following Mongkolsuk et al. (Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015), a species concept that does not allow variations in the presence or absence of major depsidones (the notable exception being H. casarettiana (A. Massal.) Trevis.). We pay special attention to the variation in phyllidia morphology. It appears that phyllidia can be used as a species character when no other secondary propagules are present. The shape of the phyllidia is different in every phyllidiate species. For example, the phyllidia in H. squamulosa (Degel.) W. L. Culb. and H. phyllalbicans M. F. Souza & Aptroot vary so much that they could be termed differently. Also, the isidia of H. crocea R. C. Harris and H. neocrocea M. F. Souza & Aptroot are quite dissimilar. The distribution of the pigments on the lower surface (in an arachnoid layer, spotted or absent) is a valuable character, as already reported by Lücking et al. (Reference Lücking, del Prado, Lumbsch, Will-Wolf, Aptroot, Sipman, Umaña and Chaves2008).
In Heterodermia, TLC is usually essential for a definite identification. However, with careful application of K most of the diagnostic substances can be detected. There have been many substances reported, and for several substances various different names or identifications are in use. For the identification of substances, we followed Schumm & Elix (Reference Schumm and Elix2015) rather than Mongkolsuk et al. (Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015) because of inconsistencies in the data shown in the latter reference. For instance, the R f value of even the major terpenoids as given in their tables 1 and 2 differ, and differ from their illustrated TLC plate, even in order of appearance. In addition, the nomenclature of the pigments differs between their text, table and plate, to the extent that identical substances may have been listed twice under different names.
In Heterodermia, atranorin and zeorin are always present and thus are not diagnostic. Norstictic acid (K+ yellow → orange-red), with or without connorstictic (or rarely only connorstictic), salazinic (K+ yellow → blood red), or dissectic acid (a green spot high in solvent A) are occasionally present, and their presence is effective at species level. Dissectic acid was found in species belonging to three different groups and was not restricted to (and characteristic of) one subgroup as mentioned by Mongkolsuk et al. (Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015). Pigments are also diagnostic, even though the certain identification of the emodin derivatives is not always possible. The pigments are clustered in chemosyndromes and there are only three different main chemosyndromes that can be distinguished by colour and K reaction.
Usually, additional terpenoids are also present. In solvent A, they are well separated and from top to bottom of the plate they are: T1 (6α-acetoxyhopane-22-ol, above atranorin), zeorin, T2 (spathulene, 16β-acetoxyhopane-22-ol, below zeorin), T3 (6α,16β-diacetoxyhopane-22-ol), T4 (16β-acetoxyhopane-6α, 22-diol), T5 (6α-acetoxyhopane-16β, 22-diol, always a very narrow band), japonene and leucotylin (a usually vague round spot very low on the plate).
Phylogeny
The focus of this paper is on species, not on deeper nodes in the phylogeny. However, species are classified in genera, and the generic division of the group is in flux and as yet unsettled. In order to test the validity of the split genera and to some extent our species concept, we sequenced 18 of our more recent specimens (see Supplementary Material Table S1 & Fig. S1, available online) and added these results to publicly available sequences. In the cladogram constructed from ITS only, four of the five groups found by Mongkolsuk et al. (Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015) could be recognized (see Supplementary Material Fig. S1). In a concatenated tree based on ITS and mtSSU, the pattern is much less clear, and in fact none of the groups, and none of the split genera are monophyletic. It is not a good sign when the more information that is added, the more confused the pattern becomes, and in any case Heterodermia s. str. is paraphyletic. Therefore, we do not accept the split genera introduced by Mongkolsuk et al. (Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015), who also did not present any cladograms supporting their division. We do informally recognize an additional group, the H. dactyliza-group, which is morphologically and ecologically well characterized, and has been a source of confusion to some previous authors: sometimes specimens belonging to this group are included inside the H. obscurata-group, sometimes they belong to Leucodermia.
A problem with the current phylogeny of Heterodermia s. lat. is that the identification or even the concept of many species varies among authors. All our specimens with the same identification clustered together but, for example, specimens called H. microphylla (Kurok.) Skorepa from other parts of the world identified as such do not cluster with them, suggesting that different but similar species are involved.
Key to the species of Heterodermia in Brazil
Key to the groups
1 Thallus with lower cortex………1. Heterodermia sensu stricto
Thallus without lower cortex, or lower cortex along the margins only………2
2(1) Cilia commonly white, lobes either linear and rarely branched or short and pulvinate………3
Cilia commonly black, thallus usually sympodially branched………4
3(2) Lobes linear and little branched………2. Heterodermia leucomelos group (Leucodermia)
Lobes canaliculate, thallus almost pulvinate………3. Heterodermia comosa group
4(2) Lobes dichotomously branched, remaining discrete, tips incurved, lower surface with marginal cortex, upper cortex generally over 200 μm thick………4. Heterodermia dactyliza group
Lobes generally sympodially branched, often confluent, tips not incurved, lower surface without cortex, upper cortex generally under 150 μm thick………5. Heterodermia japonica/obscurata group (including Polyblastidium)
1. Key to Heterodermia s. str.
1 Thallus with isidia or phyllidia………2
Thallus with soredia or without vegetative propagules………6
2(1) Thallus with isidia………3
Thallus with phyllidia………4
3(2) Thallus K+ yellow → red, with salazinic acid………H. antillarum (Vain.) Swinscow & Krog
Thallus K+ yellow, without salazinic acid………H. isidiophora (Vain.) D. D. Awasthi
4(2) Thallus K+ yellow, without depsidones………H. lepidota Swinscow & Krog
Thallus K+ yellow → orange-red or red, with depsidones………5
5(4) Thallus K+ yellow → red, with salazinic acid………H. phyllalbicans M. F. Souza & Aptroot
Thallus K+ yellow → orange-red, with norstictic and dissectic acid………H. dissecta (Kurok.) D. D. Awasthi
6(1) Thallus with soredia………7
Thallus without soredia………10
7(6) Thallus K+ yellow → orange-red or red, with depsidones………8
Thallus K+ yellow, without depsidones………9
8(7) Thallus K+ yellow → orange-red, with norstictic acid………H. pseudospeciosa Kurok.
Thallus K+ yellow → red, with salazinic acid………H. albicans (Pers.) Swinscow & Krog
9(7) Lobes elongated, spores over 30 μm long………H. speciosa (Wulf.) Trevis.
Lobes short, spores under 30 μm long………H. tremulans (Müll. Arg.) Culb.
10(6) Medulla with yellow pigment………H. rugulosa (Kurok.) Wetmore
Thallus without yellow pigment………11
11(10) Thallus with pseudocyphellae………H. diademata (Taylor) D. D. Awasthi
Thallus without pseudocyphellae………12
12(11) Thallus with dissectic acid………H. dissecticodiademata M. F. Souza & Aptroot
Thallus without dissectic acid………H. major (Nyl.) Trevis.
2. Key to the H. leucomelos group
1 Thallus with phyllidia………H. borphyllidiata (Kalb & Meesim) M. F. Souza & Aptroot
Thallus without phyllidia………2
2(1) Lower surface with brown to brick red colour………3
Lower surface without pigment or with yellow or pink colour………4
3(2) Lower surface brown, K−………H. fertilis Moberg
Lower surface brick red, K+ red………H. vulgaris (Vain.) Follm. & Redón
4(2) Lower surface without pigment or with pink pigment………5
Lower surface with yellow, K+ greenish yellow pigment………8
5(4) Lobes ending in curls………H. circinalis (Zahlbr.) W. A. Weber
Lobes remaining flattened………6
6(5) Thallus K+ yellow → red, with salazinic acid………H. leucomelos (L.) Poelt
Thallus K+ yellow, without depsidones………7
7(6) Thallus with tubercles………H. sublinearis M. P. Marcelli & M. F. N. Martins
Thallus without tubercles………H. boryi (Fée) Kr. P. Singh & S. R. Singh
8(4) Thallus K+ yellow → red, with salazinic acid………H. caneziae M. F. Souza & Aptroot
Thallus K+ yellow, without depsidones………H. lutescens (Kurok.) Follm.
3. Key to the H. comosa group
1 Upper surface with cilia………2
Upper surface without cilia………10
2(1) Lower surface with soredia………3
Lower surface without soredia………5
3(2) Soralia lip-shaped………H. macrosoraliata M. P. Marcelli & M. F. N. Martins
Soralia not lip-shaped………4
4(3) Lower surface with pigment………H. sorediosa Michlig et al.
Lower surface without pigment………H. namaquana Brusse
5(2) Lower surface with orange pigment………H. neocomosa M. P. Rodríguez et al.
Lower surface without pigment………6
6(5) Lower surface veined………H. mobergiana Michlig et al.
Lower surface not veined………7
7(6) Thallus with helmet-shaped lobes………H. comosa (Eschw.) Follm. & Redon
Thallus without helmet-shaped lobes………8
8(7) Thallus K+ yellow → red, with norstictic and salazinic acid………H. cubensis (Kurok.) Trass
Thallus K+ yellow, without norstictic and/or salazinic acid………9
9(8) Cilia partly with black tips………H. stellata (Vain.) W. A. Weber
Cilia white………H. spinigera (Kurok.) Moberg
10(1) Thallus with lip-shaped soralia………11
Thallus without soralia………13
11(10) Thallus with norstictic acid………H. allardii (Kurok.) Trass
Thallus without norstictic acid………12
12(11) Thallus closely appressed, without cilia………Heterodermia sp. 1
Thallus pulvinate to ascending, with marginal cilia………H. galactophylla (Tuck.) W. Culb.
13(10) Lower surface with pigment………H. hypochracea (Vain.) Swinscow & Krog
Lower surface without pigment………14
14(13) Thallus K+ yellow → orange-red, with norstictic acid, marginal cilia forming a dense mat……… ………H. barbifera (Nyl.) Kr. P. Singh
Thallus K+ yellow, without norstictic acid………15
15(14) Apothecia with cilia………H. trichophora (Kurok.) Trass
Apothecia without cilia………16
16(15) Apothecia laminal………H. palpebrata (Tayl.) Trass
Apothecia terminal………H. podocarpa (Bél.) D. D. Awasthi
4. Key to the H. dactyliza group
1 Lower surface with yellow pigment………H. flavodactyliza M. F. Souza & Aptroot
Lower surface without yellow pigment………2
2(1) Thallus K+ yellow, without depsidones………H. dactyliza (Nyl.) Swinscow & Krog
Thallus K+ yellow → orange-red or red, with depsidones………3
3(2) Thallus K+ yellow → orange-red, with norstictic acid………H. nigromarginata M. F. Souza & Aptroot
Thallus K+ yellow → red, with salazinic acid………Heterodermia sp. 2
5. Key to the H. japonica/obscurata group
1 Thallus with isidia or phyllidia………2
Thallus with soredia or without vegetative propagules………9
2(1) Thallus with isidia………3
Thallus with phyllidia………5
3(2) Lower surface without pigment………H. corallophora (Tayl.) Skorepa
Lower surface with pigment………4
4(3) Isidia partly decorticate………H. neocrocea M. F. Souza & Aptroot
Isidia corticate………H. crocea R. C. Harris
5(2) Lower surface with yellow pigment………6
Lower surface without pigment………7
6(5) Yellow pigment present as tiny spots………H. flavulifera M. F. Souza & Aptroot
Yellow or orange pigment present in an arachnoid layer………H. flavosquamosa Aptroot & Sipman
7(5) Thallus K+ yellow → orange-red, with norstictic acid………H. appendiculata (Kurok.) Swinscow & Krog
Thallus K+ yellow, without norstictic acid………8
8(7) Phyllidia partly ecorticate, partly granular………H. microphylla (Kurok.) Skorepa
Phyllidia corticate, dorsiventral………H. squamulosa (Degel.) W. L. Culb
9(1) Thallus with soredia………10
Thallus without soredia………18
10(9) Lower surface with yellow or orange pigment………11
Lower surface without yellow or orange pigment………14
11(10) Yellow pigment K+ green………H. casarettiana (A. Massal.) Trevis.
Yellow or orange pigment K+ red to purple………12
12(11) Yellow pigment present as tiny spots………H. delicatula M. P. Marcelli & M. F. N. Martins
Yellow or orange pigment present in arachnoid layer………13
13(12) Lower pigment bright yellow………H. subcitrina Moberg
Lower pigment ochraceous to orange………H. obscurata (Nyl.) Trevis.
14(10) Thallus K+ yellow, without depsidones………15
Thallus K+ yellow → orange-red or red, with depsidones………16
15(14) Lower cortex absent………H. japonica (Sâto) Swinscow & Krog
Lower surface with a thin false cortex without rhizines………H. spathulifera Moberg
16(14) Thallus K+ yellow → red, with salazinic acid………H. hypocaesia (Yasuda ex Räsänen) D. D. Awasthi
Thallus K+ yellow → orange-red, with norstictic acid………17
17(16) Soralia labriform………H. labiata M. P. Marcelli & M. F. N. Martins
Soralia irregular………H. propagulifera (Vain.) Dey
18(9) Lower surface with yellow to orange pigment………19
Lower surface without pigment………25
19(18) Thallus with depsidones, K+ yellow → orange-red or red, rarely only yellow………20
Thallus without depsidones, always K+ yellow………23
20(19) Yellow or orange pigment K+ red to purple………21
Yellow pigment K+ green………H. amphilacinulata M. F. N. Martins & M. P. Marcelli
21(20) Thallus K+ yellow, with dissectic acid………H. dissecticoflabellata M. F. Souza & Aptroot
Thallus K+ yellow → orange-red, with norstictic acid………22
22(21) Yellow pigment present as tiny spots………H. dendritica (Pers.) Poelt
Yellow or orange pigment present in an arachnoid layer………H. corcovadensis (Kurok.) Elix
23(19) Yellow or orange pigment K+ red to purple………24
Yellow pigment K+ green………H. lamelligera (Taylor) Trass
24(23) Secondary lobes without pseudocyphellae; main lobes over 1 mm wide………H. flabellata (Fée) D. D. Awasthi
Secondary lobes with pseudocyphellae; main lobes under 1 mm wide………H. minor M. F. Souza & Aptroot
25(18) Thallus K+ yellow → orange-red or red, with depsidones………26
Thallus K+ yellow, without depsidones………27
26(25) Thallus K+ yellow → red, with salazinic acid………H. spielmannii M. F. Souza & Aptroot
Thallus K+ yellow → orange-red, with norstictic acid………H. africana (Kurok.) M. F. Souza & Aptroot
27(25) Ascospores over 35 μm………H. magellanica (Zahlbr.) Swinscow & Krog
Ascospores under 35 μm………H. hypoleuca (Ach.) Trevis.
Taxonomy
New species
Heterodermia amphilacinulata M. F. N. Martins & M. P. Marcelli sp. nov.
MycoBank No.: MB 839878
Similar to H. flabellata but with the yellow pigment K+ green.
Type: Brazil, São Paulo State, municipality of São Bento do Sapucaí, corticolous, 15 July 1998, Marcelli 28792, Gugliotta & Maziero (SP—holotype).
(Fig. 1A)
Holotypes of new species of Heterodermia. A, H. amphilacinulata. B, H. caneziae. C & D, H. delicatula (D, lower surface showing the pigment in spots). E, H. dissecticodiademata. Scales = 5 mm. In colour online.
Thallus greyish white, loosely adnate, up to 15 cm in width, 225–450 μm thick; upper cortex 225–250 μm thick, lower cortex lacking. Lobes with anisotomic dichotomous ramifications, 3.0–6.0 × 0.7–1.2 mm, flat to slightly convex. Soredia, phyllidia and isidia absent. Medulla white. Lower surface ecorticate with yellow arachnoid pigment. Cilia 1.0–3.0 × 0.1–0.2 mm, mostly black, simple when young, soon becoming squarrosely branched, projecting outwards and forming a mat.
Apothecia 1.0–4.5 mm diam., laminal to submarginal; margin lacinulate with lower side of the lacinules having yellow pigment; disc concave, epruinose, brown; ascospores ellipsoid, 39–50 × 19–24 μm, sporoblastidia 1 to 4.
Chemistry
Atranorin, zeorin, 6α,16β-diacetoxyhopane-22-ol (T3), 6α-acetoxyhopane-16β, 22-diol (T5), hybocarpone, demethylhybocarpone. Thallus K+ yellow; yellow pigment K+ green.
Etymology
Named after the lacinulae that are present on the amphithecium.
Distribution and ecology
Known only from São Paulo State, in Atlantic rainforest and the Cerrado.
Discussion
This is similar to H. flabellata, but with the yellow pigment K+ green. It has the same chemistry as H. casarettiana (A. Massal.) Trevis. and they can be considered a species pair.
Additional specimen examined
Brazil: São Paulo State: Mogi-Guaçu Municipality, corticolous, 1995, Marcelli 29373, Marbach, Ribeiro & Luchi (SP).
Heterodermia caneziae M. F. Souza & Aptroot sp. nov.
MycoBank No.: MB 839879
Similar to H. lutescens but with salazinic acid.
Type: Brazil, Rio Grande do Sul State, Vacaria, Fazenda da Estrela, corticolous, 12 January 2004, Canêz 988 & Spielmann (CGMS—holotype).
(Fig. 1B)
Thallus pale ochraceous grey, rather loosely hanging to subfruticose, up to 6.5 cm wide, 150–200 μm thick; upper cortex 50–75 μm thick, lower cortex lacking. Lobes with dichotomous ramifications, leaving large interspaces, not laterally overlapping, 3.0–6.0 × 0.8–1.2 mm, flat to slightly concave. Soredia, phyllidia and isidia absent. Medulla white. Lower surface ecorticate, but with a broad corticate margin, with K+ greenish yellow pigment. Cilia rather abundant, black, 0.2 × 2–5 mm, mostly simple, some sparingly dichotomously branched.
Apothecia unknown.
Chemistry
Atranorin, zeorin, salazinic acid, and the unknown lutescens pigment. Thallus K+ yellow; pigment K+ greenish yellow.
Etymology
Named after our colleague and esteemed teacher Luciana da Silva Canêz.
Distribution and ecology
Known only from Rio Grande do Sul, in Atlantic rainforest.
Discussion
This species is similar to H. lutescens (Kurok.) Follmann but with salazinic acid.
Heterodermia delicatula M. P. Marcelli & M. F. N. Martins sp. nov.
MycoBank No.: MB 839888
Similar to H. obscurata but the pigment on the lower surface is restricted to tiny spots.
Type: Brazil, São Paulo, Ubatuba, Parque Estadual da Serra do Mar, corticolous, 17 March 2006, Martins 578 & Jungbluth (SP—holotype).
Thallus greenish to whitish grey, loosely adnate to elevated, up to 7.5 cm in width, 110–135 μm thick; upper cortex 10–60 μm thick, algal layer subcontinuous, 20–60 μm, lower cortex lacking. Lobes with sympodial to irregular ramifications, leaving large interspaces to laterally overlapping, 1.5–3.0 × 1.0–2.0 mm, flat to slightly convex. Soredia farinose, in labriform soralia at the end of secondary lobes, whitish grey. Phyllidia and isidia absent. Medulla white. Lower surface ecorticate with yellow arachnoid pigment in tiny spots. Cilia 1.0–3.0 × 0.1–0.2 mm, mostly black, simple when young, soon becoming squarrosely branched, projecting outwards.
Apothecia unknown.
Chemistry
Atranorin, zeorin, 6α-acetoxyhopane-22-ol (T1), 6α,16β-diacetoxyhopane-22-ol (T3), leucotylin, 7-chloroemodin, and other emodin derivatives. Thallus K+ yellow; pigment K+ violet.
Etymology
Named after the fragile thallus.
Distribution and ecology
Known only from the states of Paraná, São Paulo and Santa Catarina, in Atlantic rainforest and the Cerrado.
Discussion
This species is similar to H. obscurata (Nyl.) Trevis. but the pigment on the lower surface is restricted to tiny spots.
Additional specimens examined
Brazil: São Paulo State: same details as the type, Martins & Jungbluth 576, 583, 584; Parque Estadual da Cantareira, vi 2000, Benatti s. n.; Ilha Comprida, 2004, Canêz et al. 1267; Botucatu, 2006, Martins et al. 1245 (all in SP herbarium). Paraná: 2020, Aptroot & Souza 82129 (on leaves), 82178 & 82187 (all CGMS). Also reported from Santa Catarina State by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia dissecticodiademata M. F. Souza & Aptroot sp. nov.
MycoBank No.: MB 839889
Similar to H. diademata but with dissectic acid.
Type: Brazil, Rio Grande do Sul, Porto Alegre, near the Laguna Guaíba lake, corticolous, 27 September 2014, Cáceres 22247 & Aptroot (CGMS—holotype; ABL—isotype).
Holotypes of new species of Heterodermia. A, H. dissecticodiademata (lower surface). B, H. dissecticoflabellata. C, H. flavodactyliza. Scales = 5 mm. In colour online.
Thallus mineral grey with pink coloration towards the lobe tips, loosely adnate, up to 8.5 cm in width, 250–350 μm thick; upper cortex c. 35 μm thick, lower cortex c. 35 μm thick. Lobes with a sympodial ramification, laterally overlapping, leaving almost no open spaces, in most parts of the thallus completely confluent, up to 1.5 cm long, 2.0–3.5 mm wide, flat to slightly concave or convex, tips crenulate, without pseudocyphellae. Soredia, phyllidia and isidia absent, but central part of the thallus with minute secondary lobules that occasionally extend to the apothecium margins. Medulla white. Lower surface pale ochraceous, some lobe tips pinkish. Rhizines abundant, whitish to pale ochraceous or partly grey, on the marginal lobes simple, c. 0.50 × 0.05 mm, on the central part of the thallus becoming sparsely branched and up to 2 mm long, not projecting outwards.
Apothecia common, covering most of the thallus, cupulate, often almost closed and elongate in outline, up to 3.5 mm diam., laminal; margin grey, c. 1 mm wide, incurved, crenulate; disc deeply concave, epruinose, pale brown; ascospores 8 per ascus, fusiform to citriform, brown, 1-septate, thick-walled, 25–29 × 11–13 μm, without sporoblastidia.
Chemistry
Atranorin, dissectic acid, zeorin, 6α,16β-diacetoxyhopane-22-ol (T3), 6α-acetoxyhopane-16β, 22-diol (T5), japonene. Thallus K+ yellow.
Etymology
A fertile species with dissectic acid.
Distribution and ecology
Known only from Rio Grande do Sul State, in urban areas, and Santa Catarina State, in the Atlantic rainforest biome.
Discussion
This species is similar to H. diademata, but with dissectic acid. Heterodermia verdonii Elix is also similar and has the same chemistry but has copious pseudocyphellae. The decomposition of dissectic acid may cause the pinkish colour on the lobe tips.
Additional specimen examined
Brazil: Santa Catarina: Riqueza Municipality, Spielmann s. n. (CGMS).
Heterodermia dissecticoflabellata M. F. Souza & Aptroot sp. nov.
MycoBank No.: MB 839890
Similar to H. flabellata, but contains dissectic acid.
Type: Brazil, Mato Grosso do Sul, Bonito, Fazenda Marambaia, corticolous on Myrsine, 30 October 2018, Aptroot 77031 & Souza (CGMS—holotype; ABL—isotype). GenBank Nos: OK058284 (ITS) and OK058302 (mtSSU).
(Fig. 2B)
Thallus mineral grey, rather tightly adnate, up to 6.5 cm wide, 180–250 μm thick; upper cortex 100–125 μm thick, lower cortex lacking. Lobes with anisotomic ramifications, leaving large interspaces, not laterally overlapping, 3.5–4.0 × 1.5–2.5 mm, flat to slightly convex. Soredia, phyllidia and isidia absent. Medulla white. Lower surface ecorticate with yellow arachnoid pigment. Cilia 0.5–0.9 × 0.1–0.2 mm, mostly black but often with whitish base, simple, projecting outwards.
Apothecia 1.7–2.0 mm, laminal to submarginal; margin dentate; disc concave, epruinose, brown; ascospores 8 per ascus, ellipsoid, distinctly curved, 1-septate, thick-walled, 25–30 × 13–15 μm, without sporoblastidia, lumina angular.
Chemistry
Atranorin, dissectic acid, zeorin, 6α,16β-diacetoxyhopane-22-ol (T3), 16β-acetoxyhopane-6α, 22-diol (T4), leucotylin, 7-chloroemodin, and probably chloroskyrin. Thallus K+ yellow; pigment K+ purple.
Etymology
The name refers to the similarity with H. flabellata but containing dissectic acid.
Distribution and ecology
Known only from Mato Grosso do Sul and Minas Gerais, in Atlantic rainforest.
Discussion
This species is very similar to H. flabellata but it contains dissectic acid.
Additional specimens
Brazil: Mato Grosso do Sul: Jardim, 2018, Aptroot 77474; Campo Grande, 2019, Aptroot 79034. Minas Gerais: Itatiaia, 2009, Spielmann 7651 (all CGMS).
Heterodermia flavodactyliza M. F. Souza & Aptroot sp. nov.
MycoBank No.: MB 839891
Similar to H. dactyliza but with orange, K+ violet pigment on the lower surface.
Type: Brazil, Minas Gerais, Caraça, corticolous, 2 April 2006, Spielmann 2925 (SP—holotype).
(Fig. 2C)
Thallus mineral grey, tightly adnate, more than 6.5 cm wide, 325–400 μm thick; upper cortex 100–165 μm thick, lower cortex lacking. Lobes with anisotomic ramifications, contiguous but not confluent, without interspaces, not laterally overlapping, 3.0–6.0 × 1.0–1.7 mm, flat to slightly convex. Soredia, phyllidia and isidia absent. Medulla white. Lower surface mostly ecorticate with yellow arachnoid pigment, with corticate margins of 0.2 mm wide. Cilia black, projecting outwards, rather sparse, simple, 0.5–1.2 × 0.2 mm.
Apothecia 4.0–6.0 mm, laminal to submarginal; margin dentate; disc concave, epruinose, brown; ascospores 8 per ascus, ellipsoid, distinctly curved, 1-septate, thick-walled, 30–37 × 13–16 μm, with 2–4 sporoblastidia.
Chemistry
Atranorin, zeorin, emodin and 5,7-dichloroemodin. Thallus K+ yellow; pigment K+ purple.
Etymology
The name refers to the similarity with H. dactyliza, but with a yellow-orange pigment on the lower surface.
Distribution
Known only from Minas Gerais, in the Atlantic rainforest biome.
Discussion
This species is similar to H. dactyliza (Nyl.) Swinscow & Krog but with an orange, K+ violet pigment on the lower surface.
Heterodermia flavulifera M. F. Souza & Aptroot sp. nov.
MycoBank No.: MB 839892
Similar to H. flavosquamosa but with spotted pigment.
Type: Brazil, Rio Grande do Sul, Vacaria, Fazenda da Estrela, saxicolous, 10 January 2004, Canêz 1056 (CGMS—holotype).
(Fig. 3A)
Holotypes of new species of Heterodermia. A, H. flavulifera. B, H. labiata. C, H. macrosoraliata. Scales = 5 mm. In colour online.
Thallus greenish to whitish grey, loosely adnate to elevated, up to 7.0 cm in width, 200–250 μm thick; upper cortex 30–60 μm thick, lower cortex lacking. Lobes with sympodial to irregular ramifications, leaving interspaces, laterally overlapping, 4.0–6.0 × 1.0–1.5 mm, flat to slightly convex. Soredia and isidia absent. Phyllidia copious in the centre of the thallus, flat to upright, dissected, c. 0.2–0.5 mm. Medulla brown. Lower surface ecorticate with yellow spotted pigment. Cilia 1.5–2.0 × 0.1–0.2mm, mostly black, simple when young, soon becoming dichotomously branched, projecting outwards.
Apothecia 2.0–5.0 mm, laminal to submarginal; margin with phyllidia; disc concave, epruinose, black; ascospores ellipsoid, 1-septate, thick-walled, 37–42 × 18–21 μm, without sporoblastidia, lumina spade-shaped.
Chemistry
Atranorin, zeorin, 16β-acetoxyhopane-6α, 22-diol (T4), emodin and 5,7-dichloroemodin. Thallus K+ yellow; pigment K+ purple.
Etymology
Bearing yellow spots.
Distribution and ecology
Known only from Rio Grande do Sul, in Atlantic rainforest.
Discussion
This species is similar to H. flavosquamosa but with a spotted pigment.
Additional specimen examined
Brazil: Rio Grande do Sul: same locality and date as the type, corticolous, Canêz 1028 (CGMS).
Heterodermia labiata M. P. Marcelli & M. F. N. Martins sp. nov.
MycoBank No.: MB 839893
Similar to H. japonica but with norstictic acid and labriform soralia.
Type: Brazil, São Paulo, Parque Estadual das Fontes do Ipiranga, corticolous, 24 August 2000, Marcelli 34718 & Andrade (SP—holotype).
(Fig. 3B)
Thallus greenish grey, loosely adnate to elevated, up to 5.5 cm in width, 175–200 μm thick; upper cortex 10–60 μm thick, algal layer subcontinuous, 25–45 μm thick, lower cortex lacking. Lobes with sympodial to irregular ramifications, leaving large interspaces to laterally overlapping, 1.5–3.0 × 1.0–2.0 mm, flat to slightly convex. Soredia farinose, in labriform soralia at the ends of secondary lobes, whitish grey. Phyllidia and isidia absent. Medulla white. Lower surface ecorticate without pigment. Cilia 1.0–3.0 × 0.1–0.2 mm, mostly black, simple when young, soon becoming squarrosely branched, projecting outwards.
Apothecia unknown.
Chemistry
Atranorin, norstictic acid, zeorin and 6α,16β-diacetoxyhopane-22-ol (T3). Thallus K+ yellow → orange-red.
Etymology
Named after the labiate soralia.
Distribution and ecology
Known only from São Paulo, in urban areas and Atlantic rainforest.
Discussion
This species is similar to H. japonica but with norstictic acid and labriform soralia.
Additional specimens examined
Brazil: São Paulo: same locality and date as the type, Marcelli & Andrade 34694; ibid., 2006, Martins 375 & 376; Ubatuba, Parque Estadual da Serra do Mar, 2006, Martins & Jungbluth 556 (all in SP).
Heterodermia macrosoraliata M. P. Marcelli & M. F. N. Martins sp. nov.
MycoBank No.: MB 839894
Similar to H. galactophylla but with cilia on the upper surface, and with norstictic acid.
Type: Brazil, São Paulo, Pratânia, Fazenda Palmeira da Serra, corticolous, 7 May 2006, Martins 1134 & Kitaura (SP—holotype).
(Fig. 3C)
Thallus greenish to whitish grey, pulvinate to loosely adnate, up to 2.5 cm in width, 110–250 μm thick; upper cortex 35–110 μm thick, lower cortex lacking, algal layer discontinuous. Lobes spathulate, with few irregular ramifications, laterally overlapping, 2.0–3.5 mm wide, flat to convex, ending in large soralia on the lower surface becoming up to 2.0 mm. Soredia granular, in large and well-developed soralia with greenish coloration, which dominate the thallus aspect. Phyllidia and isidia absent. Medulla white. Upper surface with white cilia. Lower surface ecorticate, white, without corticate margin. Cilia 0.1–1.2 × 0.1 mm, mostly whitish, simple.
Apothecia unknown.
Chemistry
Atranorin, norstictic acid and zeorin. Thallus K+ yellow → orange-red.
Etymology
Named after the large soralia.
Distribution and ecology
Known only from São Paulo and Santa Catarina, in the Cerrado and Atlantic rainforest.
Discussion
This species is similar to H. galactophylla but with cilia on the upper surface, and norstictic acid present. It was described as ‘Heterodermia manuelensis’ by Martins (Reference Martins2007).
Additional specimens examined
Brazil: São Paulo: same locality and date as the type, Martins & Kitaura 1131, 1132 & 1174 (all in SP). Also reported from Santa Catarina State by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia minor M. F. Souza & Aptroot sp. nov.
MycoBank No.: MB 839895
Similar to H. flabellata but main lobes less than 1 mm wide and secondary lobes with pseudocyphellae.
Type: Brazil, Mato Grosso, Cuiabá, Chapada dos Guimarães, corticolous, 12–19 September 2020, Aptroot 81780 & Souza (CGMS—holotype; ABL—isotype).
(Fig. 4A)
Holotypes of new species of Heterodermia. A, H. minor. B, H. neocrocea. C & D, H. nigromarginata (D, lower surface showing the black margins). Scales = 5 mm. In colour online.
Thallus mineral grey, rather tightly adnate, up to 5 cm wide, 200–250 μm thick; upper cortex 100–125 μm thick, lower cortex lacking. Lobes with anisotomic ramifications, leaving interspaces, barely laterally overlapping, 1.5–2.5 × 0.7–0.9 mm, flat to slightly convex. Secondary lobes (lobes in the central part of the thallus) divergent (curved outwards), mostly ending in a white pseudocyphella. Soredia, phyllidia and isidia absent. Medulla white. Lower surface ecorticate with yellow-orange arachnoid pigment. Cilia 0.3–0.6 × 0.1 mm, mostly black, simple, projecting outwards.
Apothecia unknown.
Chemistry
Atranorin, zeorin, 6α,16β-diacetoxyhopane-22-ol (T3) and 7-chloroemodin. Thallus K+ yellow; pigment K+ purple.
Etymology
The name refers to the small size, compared to the only other Heterodermia species with pseudocyphellae, the large H. major.
Distribution and ecology
Known only from Mato Grosso State, in Cerrado forest.
Discussion
This species is similar to H. flabellata but the main lobes are less than 1 mm wide and the secondary lobes end in pseudocyphellae.
Additional specimen examined
Brazil: Mato Grosso: same locality and date as the type, Souza & Aptroot 88 (CGMS).
Heterodermia neocrocea M. F. Souza & Aptroot sp. nov.
MycoBank No.: MB 839896
Similar to H. crocea but with granular, partly decorticate isidia.
Type: Brazil, Santa Catarina, Urubici, saxicolous, 19 July 2019, Aptroot 79672 (CGMS—holotype; ABL—isotype).
(Fig. 4B)
Thallus mineral grey, loosely adnate, up to 3.0 cm in width, 150–200 μm thick; upper cortex 25–50 μm thick, lower cortex lacking. Lobes with sympodial to irregular ramifications, leaving large interspaces, 1.5–2.5 × 0.8–1.2 mm, flat to slightly convex. Isidia simple to mostly branched, mostly marginal, partly decorticate, resembling polysidiangia, whitish grey, 0.1–0.2 mm wide and high. Soredia and phyllidia absent. Medulla white. Lower surface ecorticate with yellow arachnoid pigment. Cilia 0.7–2.0 × 0.1 mm, sparse, black, mostly simple, rarely sparingly squarrosely branched, projecting outwards.
Apothecia unknown.
Chemistry
Atranorin, zeorin, 16β-acetoxyhopane-6α-22-diol (T4), emodin and 5,7-dichloroemodin. Thallus K+ yellow; pigment K+ purple.
Distribution and ecology
Known only from Santa Catarina, in Atlantic rainforest.
Etymology
A new species similar to H. crocea.
Discussion
This is similar to H. crocea but with smaller, granular, partly decorticate isidia.
Heterodermia nigromarginata M. F. Souza & Aptroot sp. nov.
MycoBank No.: MB 839897
Similar to H. dactyliza but with norstictic acid and black margins on the lower surface.
Type: Brazil, Minas Gerais, Caraça, saxicolous, 5 April 2006, Canêz 1975 (CGMS—holotype).
Thallus ochraceous grey, loosely adnate, up to 9.0 cm wide, 250–300 μm thick; upper cortex 100–165 μm thick, lower cortex lacking. Lobes with irregularly dichotomic ramifications, leaving large interspaces, occasionally laterally overlapping, 1.5–2.5 × 0.6–0.9 mm, convex. Soredia, phyllidia and isidia absent. Medulla white. Lower surface ecorticate, without yellow pigment, with black corticate margins of 0.2 mm wide. Cilia 0.5–1.2 × 0.1–0.2 mm, black, mostly simple or irregularly branched, projecting outwards.
Apothecia unknown.
Chemistry
Atranorin, norstictic acid, 6α-acetoxyhopane-22-ol (T1), zeorin, 6α,16β-diacetoxyhopane-22-ol (T3) and japonene. Thallus K+ yellow → orange-red.
Etymology
Named after the black margins on the lower surface.
Distribution and ecology
Known only from the states of Minas Gerais and Bahia, in the Atlantic rainforest biome.
Discussion
This species is very similar to H. dactyliza but it contains norstictic acid and the lower surface has black margins.
Additional specimen examined
Brazil: Bahia State: Chapada Diamantina, Palmeiras Municipality, saxicolous, 2017, Cáceres 40911 & Aptroot (ISE, ABL).
Heterodermia phyllalbicans M. F. Souza & Aptroot sp. nov.
MycoBank No.: MB 839898
Similar to H. albicans but with phyllidia instead of soredia.
Type: Brazil, Mato Grosso do Sul, Campo Grande, corticolous, 20 November 2019, Aptroot 80466 & Souza (CGMS—holotype; ABL—isotype).
(Fig. 5A)
Holotypes of new species of Heterodermia. A, H. phyllalbicans. B & C, H. spielmannii (B, field picture when wet). D, H. sublinearis. Scales = 5 mm. In colour online.
Thallus mineral grey, tightly to loosely adnate, up to 10.0 cm in width, 100–150 μm thick; upper cortex 25–50 μm thick, lower cortex 25–50 μm thick. Lobes with sympodial to irregular ramifications, often laterally overlapping, 1.5–2.5 × 0.8–1.2 mm, flat to slightly concave. Phyllidia mostly marginal, whitish grey, becoming granular. Soredia and isidia absent. Medulla white. Lower surface corticate, pale ochraceous in colour. Rhizines 0.1–0.4 × 0.1 mm, pale ochraceous to black, mostly simple, rarely sparingly dichotomously branched.
Apothecia regularly present, sessile, 0.5–1.0 mm, laminal; margin with soredia; disc concave, epruinose, brown; ascospores ellipsoid, 1-septate, thick-walled, 20–24 × 11–13 μm, without sporoblastidia, lumina spade-shaped.
Chemistry
Atranorin, salazinic acid, zeorin, often 6α,16β-diacetoxyhopane-22-ol (T3), and sometimes also 16β-acetoxyhopane-6α, 22-diol (T4). Thallus K+ yellow → red.
Etymology
The name refers to the species being similar to H. albicans but with phyllidia.
Distribution and ecology
Known only from Mato Grosso do Sul State, in Cerrado forest.
Discussion
This species is most similar to H. albicans but it has phyllidia instead of soredia.
Additional specimens examined
Brazil: Mato Grosso do Sul: same locality as the type, 2020, Aptroot & Souza 80836–80839 & 80864; Terenos, 2010, Spielmann 8090 (all CGMS).
Heterodermia spielmannii M. F. Souza & Aptroot sp. nov.
MycoBank No.: MB 839899
Similar to H. hypoleuca but with salazinic acid.
Type: Brazil, Rio Grande do Sul, Piratini, corticolous, 21 July 2011, Spielmann 9351 (CGMS—holotype).
Thallus mineral grey, rather tightly adnate, up to 6.0 cm wide, 101–250 μm thick; upper cortex 30–50 μm thick, lower cortex lacking. Lobes with anisotomic ramifications, occasionally leaving large interspaces, mostly laterally overlapping, 1.0–2.0 × 0.7–1.0 mm, convex, lobe tips widening, flabellate. Soredia, phyllidia and isidia absent. Medulla white. Lower surface ecorticate without yellow pigment. Cilia 1.0–2.5 × 0.1–0.2 mm, black, mostly perpendicularly branched, projecting outwards.
Apothecia 1.0–6.0 mm, laminal; margin dentate, often convoluted; disc concave, pruinose, brown; ascospores 8 per ascus, ellipsoid, distinctly curved, 1-septate, thick-walled, 30–35 × 13–16 μm, without sporoblastidia or rarely with one sporoblastidium, lumina angular.
Chemistry
Atranorin, zeorin and salazinic acid. Thallus K+ yellow → red.
Etymology
Named after our colleague and esteemed teacher, Adriano Afonso Spielmann.
Distribution and ecology
Known only from Rio Grande do Sul, in the Pampa biome.
Discussion
This species is similar to H. hypoleuca but with salazinic acid.
Heterodermia sublinearis M. P. Marcelli & M. F.N. Martins sp. nov.
MycoBank No.: MB 839900
Similar to H. boryi but with tubercles on the upper surface.
Type: Brazil, São Paulo, Campos do Jordão, terricolous, 24 November 1994, Marcelli 27567 & Luchi (SP—holotype).
(Fig. 5D)
Thallus pale ochraceous grey, rather loosely hanging to subfruticose, up to 18 cm wide, 115–130 μm thick; upper cortex 40–80 μm thick, lower cortex lacking. Lobes with dichotomous ramifications, leaving large interspaces, not laterally overlapping, 4.0–7.0 × 0.5–1.0 mm, flat to slightly concave, with occasional tubercles of 0.2–0.6 mm diam. Soredia, phyllidia and isidia absent. Medulla white. Lower surface ecorticate, but with a broad corticate margin, without pigment. Cilia rather copious, black, 0.2 × 2–4 mm, mostly simple, some sparingly dichotomously branched.
Apothecia rare, sessile to stalked, 0.7–2.2 mm, subterminal; margin lacinulate; disc concave, pruinose, brown; ascospores 8 per ascus, ellipsoid, 1-septate, thick-walled, 35–45 × 15–19 μm, with 2–7 sporoblastidia.
Chemistry
Atranorin and zeorin. Thallus K+ yellow.
Distribution and ecology
Known only from the states of São Paulo and Minas Gerais, in Atlantic rainforest.
Discussion
This species is similar to H. boryi but with tubercles on the upper surface.
Additional specimens examined
Brazil: São Paulo State: same locality as the type, 1991, Marcelli 12313. Minas Gerais: Parque Estadual do Ibitipoca, corticolous, 1993, Marcelli et al. 24384 (all SP).
Species newly reported from Brazil
In this and the following section, ‘Species already reported from Brazil’, and in Supplementary Material Table S1 (available online), abbreviations of two capital letters outside brackets refer to federal states in Brazil, and are as follows: AL = Alagoas; AP = Amapá; BA = Bahia; CE = Ceará; DF = Distrito Federal; GO = Goiás; MG = Minas Gerais; MS = Mato Grosso do Sul; MT = Mato Grosso; PA = Pará; PE = Pernambuco; PR = Paraná; RJ = Rio de Janeiro; RO = Rondônia; RS = Rio Grande do Sul; SC = Santa Catarina; SE = Sergipe; SP = São Paulo. In the text, states are listed from northwest to southeast, in the order usually followed in floristic literature in Brazil.
Heterodermia barbifera (Nyl.) Kr. P. Singh — Database records: SP, Sipman 41068, 41120 (B).
Heterodermia crocea R. C. Harris — Specimen examined: PE, Cáceres & Aptroot 21958 (ISE). Database record: SC (B).
Heterodermia cubensis (Kurok.) Trass — Database record: MG, Henschen (UPS).
Heterodermia hypocaesia (Yasuda ex Räsänen) D. D. Awasthi — Specimen examined: MS, Aptroot & Souza 80792 (CGMS).
Heterodermia lamelligera (Taylor) Trass — Specimen examined: MS, Aptroot 82645 (CGMS).
Heterodermia major (Nyl.) Trevis. — Specimens examined: MG, Canêz 12; RS, 11 specimens examined including Aptroot 79646, Canêz 4467 and Spielmann 15 (all CGMS). This species differs from H. diademata, with which it has often been confused and synonymized, mostly by the absence of pseudocyphellae.
Heterodermia mobergiana Michlig et al. — Specimens examined: MT, Souza & Aptroot 101; MG, Spielmann 7655; PR, Aptroot & Souza 82018; SC, Aptroot 79697; RS, 13 specimens examined including Aptroot 79321, Canêz 266 and Spielmann 681 (all CGMS). This species has been only recently described and differentiated from H. comosa. Many old reports of H. comosa may refer to H. mobergiana, which is the most common species of the H. comosa group in Brazil.
Heterodermia pseudospeciosa (Kurok.) W. L. Culb. — Specimens examined: MT, Souza & Aptroot 36 (CGMS); MS, Aptroot & Souza 80803 (CGMS); SP, Cáceres & Aptroot 13690 (ISE); RS, Cáceres & Aptroot 22200 (ISE). Database records: MG (UPS), RJ (NY). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia rugulosa (Kurok.) Wetmore — Specimen examined: SP, Canêz 2452 (CGMS).
Heterodermia spinigera (Kurok.) Trass — Specimen examined: RS, Canêz 4459 (CGMS).
Species already reported from Brazil
One reference per state per species is given.
Heterodermia africana (Kurok.) M. F. Souza & Aptroot comb. et stat. nov. MycoBank No.: MB 839901. Basionym: Anaptychia magellanica var. africana Kurok., Journal of the Hattori Botanical Laboratory 37, 604 (1973). — Reported from SP (Martins Reference Martins2007).
Heterodermia albicans (Pers.) Swinscow & Krog — Reported from AP (Cáceres & Aptroot (Reference Cáceres and Aptroot2016), specimen is H. tremulans); PE (Moreira de Barros & Xavier Filho Reference Moreira de Barros Barros and Filho L1972); AL (Menezes et al. Reference Menezes, Xavier-Leite, Aptroot and Cáceres2013); MS (Osorio Reference Osorio1992); SP (Kalb Reference Kalb1982c); PR (Osorio Reference Osorio1977b); RS (Spielmann Reference Spielmann2006). Database record: RJ (LSU). Additional state records: MT, Aptroot & Souza 81542 & 81965 (CGMS); SC, Canêz 1413 (CGMS).
Heterodermia allardii (Kurok.) Trass — Reported from MG and SP (Moberg Reference Moberg2011).
Heterodermia appendiculata (Kurok.) Swinscow & Krog — Reported from MG (Aptroot Reference Aptroot2002).
Heterodermia borphyllidiata (Kalb & Meesim) M. F. Souza & Aptroot comb. nov. MycoBank No.: MB 839902. Basionym:Leucodermia borphyllidiata Kalb & Meesim, Phytotaxa 235, 33 (2015). — Reported from MG (Mongkolsuk et al. (Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015), as Leucodermia borphyllidiata).
Heterodermia boryi (Fée) Kr. P. Singh & S. R. Singh — Reported from AL (Oliveira Júnior et al. Reference Oliveira Junior, Aptroot, Cavalcante, Košuthová and Cáceres2020); BA (Kalb Reference Kalb1982b); PR (Osorio Reference Osorio1977a); RS (Spielmann Reference Spielmann2006). Additional state records: MT, Souza & Aptroot 4 (CGMS); MG, Canêz 1869 (CGMS).
Heterodermia casarettiana (A. Massal.) Trevis. — Reported from PA (Brako et al. Reference Brako, Dibben and Amaral1985); PE (Moreira de Barros & Xavier Filho Reference Moreira de Barros Barros and Filho L1972); MG (Aptroot Reference Aptroot2002); SP (Martins Reference Martins2007), PR (Osorio Reference Osorio1977b); RS (Spielmann Reference Spielmann2006). Database records: RJ (B), MT (UPS). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia circinalis (Zahlbr.) W. A. Weber — Reported from SP (Martins Reference Martins2007).
Heterodermia comosa (Eschw.) Follmann & Redon — Reported from PA (Mongkolsuk et al. Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019); BA (Moreira Barros & Xavier Filho Reference Moreira de Barros Barros and Filho L1972); MT (Kurokawa Reference Kurokawa1962); MG (Aptroot Reference Aptroot2002); RJ (Cengia Sambo Reference Cengia1940); SP (Marcelli Reference Marcelli and Galloway1991); SC (Marcelli Reference Marcelli1992); RS (Spielmann Reference Spielmann2006). Database record: DF (LSU). This species was until recently taken in a wide sense (Michlig et al. Reference Michlig, Rodríguez, Aptroot, Niveiro and Ferraro2017), and most of the records above may refer to Heterodermia mobergiana.
Heterodermia corallophora (Tayl.) Skorepa — Reported from MG (Kurokawa Reference Kurokawa1962); RJ (Zahlbruckner Reference Zahlbruckner1902); SP (Marcelli Reference Marcelli and Galloway1991); PR (Osorio Reference Osorio1977b); RS (Spielmann Reference Spielmann2006). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia corcovadensis (Kurok.) Elix — Reported from RJ (Kurokawa Reference Kurokawa1962). Additional state records: MG, Canêz 1816, 1818 (CGMS); RS, Canêz 3768 (CGMS).
Heterodermia dactyliza (Nyl.) Swinscow & Krog — Reported from BA (Aptroot & Cáceres Reference Aptroot and Cáceres2018); MG (Aptroot Reference Aptroot2002). Database records: PA (UPS), RJ (UPS).
Heterodermia dendritica (Pers.) Poelt — Reported from MG (Aptroot Reference Aptroot2002). Database records: GO (ASU), RJ (B), SP (B). Additional state record: RS, Canêz 4464 (CGMS).
Heterodermia diademata (Taylor) D. D. Awasthi — Reported from PA (Brako et al. Reference Brako, Dibben and Amaral1985); MT (Lynge Reference Lynge1924); MS (Aptroot & Spielmann Reference Aptroot and Spielmann2020); RJ (Cengia Sambo Reference Cengia1940); SP (Martins Reference Martins2007); RS (Spielmann Reference Spielmann2006). Since the species was often confused with Heterodermia major, some of the records above may refer to this species.
Heterodermia dissecta (Kurok.) D. D. Awasthi — Reported from PE (Cáceres Reference Cáceres2007); AL (Menezes et al. Reference Menezes, Xavier-Leite, Aptroot and Cáceres2013).
Heterodermia fertilis Moberg — Reported from MG (Moberg Reference Moberg2011).
Heterodermia flabellata (Fée) Awasthi — Reported from PA (Brako et al. Reference Brako, Dibben and Amaral1985); PE (Moreira de Barros & Xavier Filho Reference Moreira de Barros Barros and Filho L1972); MS (Aptroot & Spielmann Reference Aptroot and Spielmann2020); MG (Aptroot Reference Aptroot2002); SP (Martins Reference Martins2007); SC (Kurokawa Reference Kurokawa1962); RS (Spielmann Reference Spielmann2006). Additional state record: PR, Aptroot & Souza 82268 (CGMS). Database records: MT (UPS), RJ (UPS).
Heterodermia flavosquamosa Aptroot & Sipman — Reported from SP (Martins Reference Martins2007); RS (Spielmann Reference Spielmann2006). Additional state record: MS, Aptroot 80517 (CGMS). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia galactophylla (Tuck.) W. Culb. — Reported from PA (Brako et al. Reference Brako, Dibben and Amaral1985); AL (Oliveira Júnior et al. Reference Oliveira Junior, Aptroot, Cavalcante, Košuthová and Cáceres2020); SE (Cáceres et al. Reference Cáceres, Nascimento, Aptroot and Lücking2014); MT (Mongkolsuk et al. Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015); MG (Kalb Reference Kalb1984); RJ (Cengia Sambo Reference Cengia1940); SP (Marcelli Reference Marcelli1992); SC (Marcelli Reference Marcelli1992); RS (Spielmann Reference Spielmann2006). Additional state record: PR, Aptroot & Souza 82170 (CGMS).
Heterodermia hypochracea (Vain.) Swinscow & Krog — Reported from SP (Martins Reference Martins2007); PR (Eliasaro et al. Reference Eliasaro, Gerlach and Gumboski2012); RS (Spielmann Reference Spielmann2006).
Heterodermia hypoleuca (Ach.) Trevis. — Reported from MT (Lynge Reference Lynge1924); MG (Vainio Reference Vainio1890); RJ (Cengia Sambo Reference Cengia1940); SC (Müller Reference Müller1891a); RS (Spielmann Reference Spielmann2006).
Heterodermia isidiophora (Vain.) D. D. Awasthi — Reported from RS (Benatti & Marcelli Reference Benatti and Marcelli2017). Database record: MG (UPS). Additional state record: RJ, Spielmann 10084 (CGMS). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia japonica (M. Sâto) Swinscow & Krog — Reported from RO (Aptroot & Cáceres (Reference Aptroot and Cáceres2014), specimen is H. obscurata); AL (Oliveira Júnior et al. Reference Oliveira Junior, Aptroot, Cavalcante, Košuthová and Cáceres2020); SE (Cáceres et al. Reference Cáceres, Nascimento, Aptroot and Lücking2014); BA (Marcelli Reference Marcelli1992); MT (Lynge Reference Lynge1924); MS (Lynge Reference Lynge1924); RJ (Mongkolsuk et al. Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015); SP (Marcelli Reference Marcelli1992); SC (Marcelli Reference Marcelli1992); RS (Spielmann Reference Spielmann2006). Database record: GO (UPS). Additional state records: PE, Cáceres & Aptroot 22023 (ISE); MG, Canêz 1821, 1824 (CGMS); PR, Aptroot & Souza, 6 specimens including 82005 (all CGMS).
Heterodermia lepidota Swinscow & Krog — Reported from SP (Martins Reference Martins2007).
Heterodermia leucomelos (L.) Poelt — Reported from PA (Müller Reference Müller1891b); PE (Moreira de Barros & Xavier Filho Reference Moreira de Barros Barros and Filho L1972); AL (Nusbaumer et al. Reference Nusbaumer, Cáceres, Aptroot, Gibertoni, Horak, Studer, Nusbaumer and Spichiger2015); MG (Vainio Reference Vainio1890); RJ (Cengia Sambo Reference Cengia1940); SP (Nagaoka & Marcelli Reference Nagaoka and Marcelli1989); SC (Müller Reference Müller1891a); RS (Spielmann Reference Spielmann2006).
Heterodermia lutescens (Kurok.) Follm. — Reported from AL (Oliveira Júnior et al. Reference Oliveira Junior, Aptroot, Cavalcante, Košuthová and Cáceres2020); MG (Aptroot Reference Aptroot2002); RJ (Mongkolsuk et al. Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015); SP (Martins Reference Martins2007); RS (Spielmann Reference Spielmann2006). Database records: GO (UPS), PR (UPS). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia magellanica (Zahlbr.) Swinscow & Krog — Reported from MG (Aptroot Reference Aptroot2002); SP (Martins Reference Martins2007); PR (Eliasaro et al. Reference Eliasaro, Gerlach and Gumboski2012); RS (Spielmann Reference Spielmann2006). Database record: RJ (B). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia microphylla (Kurok.) Skorepa — Reported from BA (Aptroot & Cáceres Reference Aptroot and Cáceres2018); MS (Fleig & Riquelme Reference Fleig and Riquelme1991); RJ (Mongkolsuk et al. Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015); SP (Mongkolsuk et al. Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015); RS (Spielmann Reference Spielmann2006). Additional state records: MG, Canêz 1864 (CGMS); PR, Aptroot & Souza 82151; SC, Aptroot 78408 (all CGMS).
Heterodermia namaquana Brusse — Reported from SP (Martins Reference Martins2007). Additional state record: MG, Canêz 1867 (CGMS). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia neocomosa M. P. Rodríguez et al. — Reported from MS (Michlig et al. Reference Michlig, Rodríguez, Aptroot, Niveiro and Ferraro2017).
Heterodermia obscurata (Nyl.) Trevis. — Reported from PA (Brako et al. Reference Brako, Dibben and Amaral1985); CE (Alves Reference Alves2014); AL (Oliveira Júnior et al. Reference Oliveira Junior, Aptroot, Cavalcante, Košuthová and Cáceres2020); PE (Moreira de Barros & Xavier Filho Reference Moreira de Barros Barros and Filho L1972); SE (Cáceres et al. Reference Cáceres, Nascimento, Aptroot and Lücking2014); BA (Aptroot & Cáceres Reference Aptroot and Cáceres2018); MG (Aptroot Reference Aptroot2002); RJ (Zahlbruckner Reference Zahlbruckner1902); SP (Marcelli Reference Marcelli1992); PR (Osorio Reference Osorio1977b); SC (Marcelli Reference Marcelli1992); RS (Spielmann Reference Spielmann2006). Additional state records: RO, Cáceres & Aptroot 11009 (ISE); MT, Souza & Aptroot 5, 43 and Aptroot & Souza 81963 (CGMS); MS, Aptroot & Souza 80471, 80823, 80965 (CGMS).
Heterodermia palpebrata (Tayl.) Trass — Reported from Brazil but state not indicated (Meyen & Flotow Reference Meyen and Flotow1843).
Heterodermia podocarpa (Bél.) D. D. Awasthi — Reported from PA (Brako et al. Reference Brako, Dibben and Amaral1985); PE (Moreira de Barros & Xavier Filho Reference Moreira de Barros Barros and Filho L1972); MT (Lynge Reference Lynge1924); MG (Kalb Reference Kalb1982a); RJ (Müller Reference Müller1891b); SP (Martins Reference Martins2007); SC (Müller Reference Müller1891a); RS (Spielmann Reference Spielmann2006).
Heterodermia propagulifera (Vain.) Dey — Reported from SP (Marcelli Reference Marcelli and Galloway1991); RS (Spielmann Reference Spielmann2006). Additional state records: MT, 5 specimens including Souza & Aptroot 21, 143; MG, Canêz 1805, 1817, 1865, Spielmann 7632, 7675; PR, Aptroot & Souza 82075; SC, Canêz 2901 (all CGMS).
Heterodermia sorediosa Michlig et al. — Reported from AL (Oliveira Júnior et al. Reference Oliveira Junior, Aptroot, Cavalcante, Košuthová and Cáceres2020). Additional state record: MS, Aptroot 79049 (CGMS).
Heterodermia spathulifera Moberg & Purvis — Reported from Brazil but state not indicated (Moberg Reference Moberg2011); according to the database in UPS the specimens are from MG and SP.
Heterodermia speciosa (Wulf.) Trevis. — Reported from PA (Brako et al. Reference Brako, Dibben and Amaral1985); CE (Alves Reference Alves2014); AL (Oliveira Júnior et al. Reference Oliveira Junior, Aptroot, Cavalcante, Košuthová and Cáceres2020); BA (Marcelli Reference Marcelli1992); MS (Fleig & Riquelme Reference Fleig and Riquelme1991); MG (Aptroot Reference Aptroot2002); RJ (Vainio Reference Vainio1890); SP (Marcelli Reference Marcelli1992); SC (Marcelli Reference Marcelli1992); RS (Spielmann Reference Spielmann2006). Additional state records: MT, Souza & Aptroot 36 and Aptroot & Souza 81544 (CGMS).
Heterodermia squamulosa (Degel.) W. L. Culb. — Reported from SP (Marcelli Reference Marcelli1992); PR (Eliasaro et al. Reference Eliasaro, Gerlach and Gumboski2012); RS (Spielmann Reference Spielmann2006). Database record: RJ (LSU), MS (UPS). Additional state records: MT, 5 specimens including Souza & Aptroot 105 and Aptroot & Souza 81582 (CGMS). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia stellata (Vain.) W. A. Weber — Reported from MG (Mongkolsuk et al. Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015); SP (Martins Reference Martins2007). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia subcitrina Moberg — Reported from Brazil but state not indicated (Moberg Reference Moberg2011); according to the database in UPS the specimen is from RS.
Heterodermia tremulans (Müll. Arg.) Culb. — Reported from CE (Aptroot & Cáceres Reference Aptroot and Cáceres2016); PE (Moreira de Barros & Xavier Filho Reference Moreira de Barros Barros and Filho L1972); AL (Oliveira Júnior et al. Reference Oliveira Junior, Aptroot, Cavalcante, Košuthová and Cáceres2020); BA (Aptroot & Cáceres Reference Aptroot and Cáceres2018); MS (Aptroot & Spielmann Reference Aptroot and Spielmann2020); MG (Kurokawa Reference Kurokawa1962); RJ (Mongkolsuk et al. Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015); SP (Mongkolsuk et al. Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015); PR (Eliasaro et al. Reference Eliasaro, Gerlach and Gumboski2012); RS (Spielmann Reference Spielmann2006). Additional state records: AP, Cáceres & Aptroot 27215 (ISE); MT, Aptroot & Souza 81660 (CGMS). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia trichophora (Kurok.) Trass — Reported from RJ (Moberg Reference Moberg2011); SP (Moberg Reference Moberg2011); PR (Eliasaro et al. Reference Eliasaro, Gerlach and Gumboski2012); RS (Spielmann Reference Spielmann2006).
Heterodermia vulgaris (Vain.) Follm. & Redón — Reported from AL (Oliveira Júnior et al. Reference Oliveira Junior, Aptroot, Cavalcante, Košuthová and Cáceres2020); MS (Osorio Reference Osorio1992); MG (Moberg Reference Moberg2011); RJ (Mongkolsuk et al. Reference Mongkolsuk, Meesim, Poengsungnoen, Buaruang, Schumm and Kalb2015); SP (Marcelli Reference Marcelli and Galloway1991); PR (Osorio Reference Osorio1977a); RS (Spielmann Reference Spielmann2006). Database record: DF (LSU). Also reported from SC by Reginaldo & Gumboski (Reference Reginaldo and Gumboski2019).
Heterodermia sp. 1. — About to be described from SC (Reginaldo & Gumboski Reference Reginaldo and Gumboski2019).
Heterodermia sp. 2. — About to be described from SC (Reginaldo & Gumboski Reference Reginaldo and Gumboski2019).
Further species described from Brazil
The species mentioned below have been described from Brazil but are still not validly published. Their tentative identity is given below.
H. kalbii M. F. N. Martins & M. P. Marcelli, ined.: probably = H. magellanica.
H. velata M. P. Marcelli & M. N. Benatti, ined.: probably = H. obscurata.
Discussion
Heterodermia species are very unevenly dispersed over Brazil (Fig. 6). Not a single species is known from most of the Amazonian states, and from two states just one species is recorded. In the Northeast Region, more species occur but mostly in the Atlantic rainforest. Most species occur in the Southeast and South Regions of the country, including Mato Grosso and Mato Grosso do Sul. Based on our data, the states of Minas Gerais, São Paulo and Rio Grande do Sul are richest in species, each state containing (with a large overlap of species) more than half of the total Heterodermia mycota of the country.
Map of Brazil with an indication of the number of recorded Heterodermia species per state. Geographic coordinate system: SIRGAS 2000.
Acknowledgements
The first author thanks the CNPq for the support from a student grant. We thank Milton Martins and Marcelo Marcelli for the permission to publish nomenclatural novelties and relevant descriptions from Martins’ thesis, and for giving us access to original data including photocopies of TLC plates. We also thank Felix Schumm for sending us his unpublished book on Heterodermia, as well as many pictures. This study is partly financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001, who provided a visiting professorship to the second author. We thank Pablo Alvaredo for DNA extraction and sequencing of the specimens and Wellington Fava for downloading sequences and constructing cladograms. Jean Marc Torres helped with TLC. Lidiane Alves kindly prepared the map. The authors are very grateful to the referees for their constructive and informed comments.
Author ORCIDs
André Aptroot, 0000-0001-7949-2594; Adriano Spielmann, 0000-0003-0137-0807.
Supplementary Material
To view Supplementary Material for this article, please visit https://doi.org/10.1017/S0024282921000499
