Introduction
Brazil, the fifth largest country in the world, is also considered one of the most diverse countries on the planet. Two of the three major tropical rainforest blocks in the Neotropics are located in Brazil: the Atlantic rainforest and the Amazon (Whitmore Reference Whitmore1998). They are both regarded as biodiversity hotspots (Myers et al. Reference Myers, Mittermeier, Mittermeier, Fonseca and Kent2000), the Amazon being the largest in surface area. In Brazil, the Amazon covers c. 4 100 000 km2, of which around 3·4 million km2 remain forested.
The three major forest ecosystems of Brazil, the Amazonian ‘terra firme’ forest, the Atlantic forest and the ‘planalto’ forests (Cerrado), in spite of their geographical proximity, exhibit considerable diversity and marked floristic differences (Leitão Filho Reference Leitão-Filho1987; Whitmore Reference Whitmore1998). Thus, it is also expected that differences in the lichen biota between these vegetation types will be found (Cáceres Reference Cáceres2007; Cáceres et al. Reference Cáceres, Lücking and Rambold2008), which emphasizes the need for specific lichen diversity studies in each region. In contrast to the Atlantic rainforest and the ‘planalto’ forests, a good estimate of the lichen diversity in the Brazilian Amazon is still unavailable, although some recent efforts have been made to increase the knowledge of the lichenized mycota of this vast region (Kalb Reference Kalb2004, Reference Kalb2009; Frisch et al. Reference Frisch, Kalb and Grube2006; Frisch & Kalb Reference Frisch and Kalb2009). Therefore, a larger inventory work is currently being undertaken in two areas of Amazonian Brazil in the states of Pará and Rondônia. The present paper presents results from the study undertaken at the Ferreira Penna Research Station [http://www.museu-goeldi.br/ecfpn], which covers an area of 33 000 ha within the Caxiuanã National Forest (330 000 ha) in the state of Pará and is under the administration of the Museu Paraense Emílio Goeldi (MPEG; Lisboa Reference Lisboa1997, Reference Lisboa2002). The foliicolous lichens at Ferreira Penna Research Station were treated in an earlier paper (Lücking & Cáceres Reference Lücking, Cáceres and Lisboa2002), and a first list of corticolous species focusing on Graphidaceae is being published separately (Cáceres et al. Reference Cáceres, Santos Viera, Santos De Jesus, Lücking and Lisboa2012). Here we formally introduce two new species and four new combinations.
Material and Methods
The material used for this study was collected by the first author during a one-week field trip in January 2009, to the Ferreira Penna Research Station. The Caxiuanã National Forest (Floresta Nacional or FloNa) is situated in the municipalities of Melgaço and Portel (1°37′S, 51°19′W and 1°54′S, 51°58′W and limits south of 2°15′S, 51°15′W and 2°15′S, 51°56′W) in the administrative micro-region of Furos de Breves, in the bay of Caxiuanã between the Xingu and Tocantins rivers, occupying an area of c. 300 000 ha. The area includes several vegetation types, including non-flooded (terra firme forest with islands of savanna-like and secondary forest) and flooded forest (várzea and igapó), as well as abundant aquatic vegetation, the terra firme forest being the predominant type (Lisboa Reference Lisboa1997, Reference Lisboa2002).
Thallus morphology of the collected lichens was examined using Leica EZ4 and LEICA MS5 dissecting microscopes. Sections of thalli and ascomata were cut by hand with a razor blade and examined with squash preparations in water, KOH and Lugol's solution, using a ZEISS Axioskop 2 compound microscope. TLC was performed using standard techniques with solvent C. Type material and duplicates are deposited at ISE, MPEG, and F.
The Taxa
Ampliotrema megalostoma (Müll. Arg.) M. Cáceres & Lücking comb. nov.
MycoBank No: MB 800583
Ocellularia megalostoma Müll. Arg., Hedwigia 31: 283 (1892); type: Brazil, Trail s. n. (BM!—holotype)
(Fig. 1A)
Fig. 1. General habit of the Brazilian lichen species studied. A, Ampliotrema megalostoma; B, Graphis brachylirellata; C, Malmidea leucogranifera; D, Ocellularia conformalis; E, Redingeria microspora; F, Sarcographa megistocarpa. Scale=1 mm. In colour online.
Notes. Ampliotrema megalostoma is a very typical Ampliotrema, closely resembling A. auratum (Tuck.) Kalb in the large apothecia with yellow-pruinose disc, but differing in the larger, transversely septate ascospores (40–80×9–15 µm and 11–17-septate in A. megalostoma versus 14–22×8–10 µm and submuriform in A. auratum). The ascospores are similar to those of A. lepadinoides (Leight.) Kalb, but that species has smaller apothecia with orange-pruinose discs, and the ascospores are usually larger (up to 150 µm in A. lepadinoides).
Specimens examined. Brazil:Pará: Municipality of Melgaço, Estação Científica Ferreira Penna, 400 km west of Belém, on trail behind the station, 2009, Cáceres 6012 (F, ISE), 9716, 9724, 9737, 9747 (ISE).
Graphis brachylirellata M. Cáceres & Lücking sp. nov.
MycoBank No: MB 800584
Differing from G. mexicana in the striate lirellae, thicker excipulum, septate ascospores, and stictic acid chemistry.
Type: Brazil, Pará, Municipality of Melgaço, Estação Científica Ferreira Penna, 400 km west of Belém, on trail behind the station, 31 January 2009, Cáceres 6015 (ISE—holotype; F—isotype).
(Fig. 1B)
Thallus corticolous, up to 5 cm diam., 50–100 µm thick, continuous; surface smooth to uneven, matt, pale yellowish grey; prothallus absent. Thallus in section with thin, cartilaginous upper cortex and irregular algal layer and medulla encrusted with large clusters of calcium oxalate crystals.
Apothecia rounded to very shortly lirelliform, straight, unbranched, prominent, with thin to thick complete thalline margin, 0·7–1·0 mm long and broad, 0·3–0·4 mm high; disc concealed; proper margin thick, labia striate; thalline margin thin to thick, usually completely covering the labia, yellowish white, but sometimes abraded to expose black labia. Excipulum apically crenulate, completely carbonized, 100–200 µm wide, black; laterally covered by corticate algiferous thallus including large clusters of calcium oxalate crystals, laterally above the hymenium with short, thick periphysoids; hypothecium prosoplectenchymatous, 20–30 µm high, yellowish; hymenium 250–300 µm high, colourless, clear; epithecium indistinct. Paraphyses unbranched; asci fusiform, 150–200×30–40 µm. Ascospores 1 per ascus, fusiform, 19–25-septate, 120–150×25–30 µm, 4–5 times as long as wide, colourless, I+ violet-blue.
Secondary chemistry. Stictic and constictic acids, traces of cryptostictic acid.
Notes. This species is characterized by the unusual combination of short, almost rounded, massively carbonized ascomata with striate labia, large, transversely septate ascospores, and stictic acid. It resembles Graphis mexicana (Hale) Lumbsch et al. and related species (Mangold et al. Reference Mangold, Martín, Kalb, Lücking and Lumbsch2008), but these differ by the lack of chemical substances, entire labia, muriform ascospores, and the comparatively thin excipulum. The new species also resembles a Carbacanthographis, particularly due to the periphysoids (Staiger Reference Staiger2002), but the ascospores are distinctly amyloid and we could not see wart-like ornamentation in the periphysoids covering the inner part of the labia. We therefore place the new species in Graphis, pending molecular studies. The most similar species in Carbacanthographis is C. crassa (Müll. Arg.) Staiger & Kalb, which is comparable in the massive lirellae and chemistry, but has warty periphysoids and muriform, non-amyloid ascospores (Staiger Reference Staiger2002).
Malmidea leucogranifera M. Cáceres & Lücking sp. nov.
MycoBank No: MB 800585
Differing from M. granifera in the light brown apothecial disc and hypothecium.
Type: Brazil, Pará, Municipality of Melgaço, Estação Científica Ferreira Penna, 400 km west of Belém, on trail behind the station, 31 January 2009, Cáceres 9740 (ISE—holotype; F—isotype); same locality and date, Cáceres 9706, 9708, 9715 (ISE—paratype).
(Fig. 1C)
Thallus crustose, corticolous, continuous, 20–50 mm across and 30–70 µm thick, densely verrucose, green-grey; medulla pale yellow, K+ dark yellow. Photobiont chlorococcoid; cells 4–7 µm diam.
Apothecia sessile, rounded to irregular, 0·5–1·0 mm diam. and 250–350 µm high; disc plane, orange-brown; margin thin but distinct, not prominent, cream-coloured. Excipulum externally paraplectenchymatous with small cells and loose hyphal ends, 20–50 µm broad, hyaline, internally with medullary layer composed of loosely arranged, periclinal hyphae with constricted septa, 40–60 µm broad, encrusted with hydrophobic granules, nubilous but dissolving in KOH (without visible colour reaction). Hypothecium 20–30 µm high, orange-brown, K−. Epithecium indistinct. Hymenium 80–100 µm high, colourless. Asci 70–90×15–20 µm. Ascospores 8 per ascus, non-septate, broadly ellipsoid, 12–16×7–10 µm, 1·6–2·0 times as long as broad.
Pycnidia not observed.
Secondary chemistry. Two unknown substances (xantholepinones?), pale yellow medullary pigment.
Notes. This new species is closely related to Malmidea badimioides (Cáceres & Lücking) Cáceres & Kalb (Kalb et al. Reference Kalb, Rivas Plata, Lücking and Lumbsch2011), but differs in the pale yellow, K+ intensifying instead of white, K− medulla. The apothecial margin is also thinner on average and never pure white as in M. badimioides. In addition, the green K+ reaction of the medullary layer in the excipulum of M. badimioides was not observed in M. leucogranifera. The new species differs from M. granifera (Ach.) Kalb et al. (Kalb et al. Reference Kalb, Rivas Plata, Lücking and Lumbsch2011) mainly in the light orange-brown, rather than brown-black hypothecium and apothecial disc.
Ocellularia conformalis (Kremp.) M. Cáceres & Lücking comb. nov.
MycoBank No: MB 800586
Thelotrema conformale Kremp., Nuovo Giorn. Bot. Ital. 7: 19 (1875); type: Malaysia (Borneo), Beccari 12 (M!—holotype).
(Fig. 1D)
Notes. This species is placed here in Ocellularia because of the carbonized excipulum and columella. Externally it resembles a Stegobolus due to the broad, split columella and the psoromic acid chemistry (Frisch et al. Reference Frisch, Kalb and Grube2006), but in molecular phylogenetic analysis it clusters close to Ocellularia pyrenuloides Zahlbr. and is apparently not closely related to either Stegobolus or Ocellularia s. str. (Rivas Plata et al. Reference Rivas Plata, Mason-Gamer, Ashley, Lücking and Lumbsch2012).
Specimens examined. Brazil:Pará: Municipality of Melgaço, Estação Científica Ferreira Penna, 400 km west of Belém, on trail behind the station, 2009, Cáceres 6004, 6033 (F, ISE).
Redingeria microspora (Zahlbr.) M. Cáceres & Lücking comb. nov.
MycoBank No: MB 800587
Leptotrema microsporum Zahlbr., Sitzungsber. Kaiserl. Akad. Wiss. Wien, Math.-Naturwiss. Klasse 111: 392 (1902).—‘Thelotrema' microsporum Zahlbr., Cat. Lich. Univ. 2: 625 (1923); orth. error; Thelotrema microsporoides Zahlbr., Cat. Lich. Univ. 2: 625 (1923) [nom. nov., non T. mi crosporum Mont.].
(Fig. 1E)
Notes. Redingeria microspora is somewhat intermediate between the genera Melanotrema [e.g. M. astrolucens (Sipman) Frisch], Redingeria, and Stegobolus [e.g. S. metaphoricus (Nyl.) Frisch], but clusters within Redingeria in molecular phylogenetic analysis (Rivas Plata et al. Reference Rivas Plata, Mason-Gamer, Ashley, Lücking and Lumbsch2012), which is consistent with its Redingeria-like thallus and ascospores as defined by Frisch et al. (Reference Frisch, Kalb and Grube2006). The latter authors placed the species in synonymy with Stegobolus metaphoricus, but this is clearly contradicted by the molecular phylogeny. The two species have indeed several characters in common, but differ both in apothecial morphology (lirellate in S. metaphoricus versus more rounded in R. microspora) and thallus surface colour and structure (yellow-green and uneven in S. metaphoricus versus grey and minutely grainy in R. microspora).
The name Thelotrema microsporoides is apparently based on a mishap. Zahlbruckner (Reference Zahlbruckner1923) listed his original species, Leptotrema microsporum, under Thelotrema, indicating T. microsporum Mont. as competing homonym, and therefore introduced the superfluous new name, T. microsporoides.
Specimens examined. Brazil:Pará: Municipality of Melgaço, Estação Científica Ferreira Penna, 400 km west of Belém, on trail behind the station, 2009, Cáceres 6030, 9113 (F, ISE).
Sarcographa megistocarpa (Leight.) M. Cáceres & Lücking comb. nov.
MycoBank No: MB 800588
Platygrapha megistocarpa Leight., Trans. Linn. Soc. London 27: 178 (1869)—Phaeographis megistocarpa (Leight.) Müll. Arg., Flora 65: 336 (1882); type: Sri Lanka, Thwaites s. n. (BM!— holotype; G!—isotype).
(Fig. 1F)
Notes. This species is very closely related to Sarcographa ramificans (Kremp.) Staiger (Reference Staiger2002), having primarily lirellate ascomata and comparatively long, multiseptate ascospores. However, the species lacks chemistry, contrary to S. ramificans which contains the stictic acid chemosyndrome, and the ascomata are usually broader and more prominent and become somewhat stromatic with age.
Specimens examined. Brazil:Pará: Municipality of Melgaço, Estação Científica Ferreira Penna, 400 km west of Belém, on trail behind the station, 2009, Cáceres 6008, 6020, 6042 (F, ISE).
The first author thanks the Moore Foundation and IEB for funding the field trip to the Ferreira Penna Scientific Station in the Caxiuanã National Forest, Pará, Brazil, and supporting the study of crustose lichens in the Brazilian Amazon, and the CNPq for a research grant. The workshop at the Universidade Federal de Sergipe in Itabaiana, Brazil, during which the material was studied, was financed by a grant from the National Science Foundation: Neotropical Epiphytic Microlichens – An Innovative Inventory of a Highly Diverse yet Little Known Group of Symbiotic Organisms (DEB 715660 to The Field Museum; PI R. Lücking). The systematic studies of Graphidaceae have been and are being funded by the following grants: Phylogeny and Taxonomy of Ostropalean Fungi, with Emphasis on the Lichen-forming Thelotremataceae (DEB 0516116 to The Field Museum; PI H. T. Lumbsch; Co-PI R. Lücking), and ATM – Assembling a Taxonomic Monograph: The Lichen Family Graphidaceae (DEB-1025861 to The Field Museum; PI T. Lumbsch, CoPI R. Lücking).
