New species and new records of Peltula (Lichinales, Ascomycota lichenized) from Mato Grosso do Sul, Brazil

Marcos Junji Kitaura Jean-Marc Torres Mayara Camila Scur Aline Pedroso Lorenz Rogério Rodrigues Faria About the authors

Abstract

Peltula species occur in arid and semi-arid environments, with new species being regularly described worldwide. Lichen diversity is being studied in the diverse but poorly known Midwest region of Brazil, and new species and records are being proposed. In this paper, Peltula anthracina is proposed as new to science, and P. leptophylla and P. lingulata are reported as new records from Mato Grosso do Sul state. As it is a region highly threatened by the expansion of agricultural activities, the authors highlight the importance of the conservation of native flora to preserve lichens’ hidden diversity.

Key words
arid habitat; cyanolichen; diversity; fire forest; new species

Resumo

Espécies de Peltula ocorrem em ambientes áridos e semiáridos e espécies novas têm sido constantemente descritas em todo o mundo. Neste mesmo sentido, a diversidade de liquens está sendo estudada na diversa, porém pouco conhecida, região centro-oeste do Brasil, e espécies e registros novos têm sido descobertos. Como parte do resultado, Peltula anthracina é proposta como nova para a ciência, e P. leptophylla e P. lingulata como novos registros para o estado de Mato Grosso do Sul. Como a região é altamente ameaçada pela expansão das atividades agrícolas, os autores destacam a importância da conservação da vegetação natural para preservar a diversidade oculta dos liquens.

Palavras-chave
habitat árido; cianoliquens; diversidade; incêndios florestais; espécie nova

Introduction

Peltula Nyl. is a worldwide genus of lichenized fungi with cyanobacteria as photobiont, found in arid and semi-arid environments; and arid microclimate islands within humid areas (Wetmore 1971Wetmore CM (1971) The lichen family Heppiaceae in North America. Annals of the Missouri Botanical Garden 57: 158-209.; Büdel 1987Büdel B (1987) Review of Zur Biologie und Systematik der Flechtengattungen Heppia und Peltula im sudlichen Afrika. The Lichenologist 19: 441-442., 1995; Büdel et al. 2000Büdel B, Becker U, Follmann G & Sterflinger K (2000) Algae, fungi, and lichens on inselbergs. Ecological Studies 146: 69-90.; Schultz et al. 2000Schultz M, Porembski S & Büdel B (2000) Diversity of rock-inhabiting cyanobacterial lichens: studies on granite inselbergs along the Orinoca and the Guyana region. Plant Biology 2: 482-495.; Marques et al. 2013Marques J, Schultz M & Paz-Bermúdez G (2013) A Peltula Nyl. diversity hotspot in north-east Portugal, with one species new to science and three species new to mainland Europe. The Lichenologist 45: 483-498.; Makryi 2016Makryi TV (2016) Peltula pannarioides and P. rosulata (Peltulaceae), new lichen species from Baikal Siberia. Novosti Sistematiki Nizshikh Rastenii 50: 213-242., 2017). Nowadays, new species are constantly reported, and the number of Peltula species is still uncertain. For example, the number of Peltula was estimated at 40 species in a generic study of lichen classification (Lücking et al. 2017Lücking R, Hodkinson BP & Leavitt SD (2017) Corrections and amendments to the 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota. Bryologist 120: 58-69.). One year later, 50 species were estimated for the genus in a phylogenetic study of Peltulaceae (Kauff et al. 2018Kauff F, Bachran A, Schultz M, Hofstetter V, Lutzoni F & Büdel B (2018) Molecular data favours a monogeneric Peltulaceae (Lichinomycetes). The Lichenologist 50: 313-327.), but more than 60 taxa are accepted for the genus according to Index Fungorum and MycoBank websites.

Regarding the photobiont partner, information about the cyanobacteria is practically absent. The name of the lichens is related to mycobiont partner, and the cyanobacteria identification has been neglected within of the thallus. In this way, the photobiont are practically unknown to lichens and only the Chroococcidiopsis genus is reported to Peltula (Nübel et al. 1997Nübel U, Garcia-Pichel F & Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Applied and Environmental Microbiology 63: 3327-3332.; Komárek & Anagnostidis 1999Komárek J & Anagnostidis K (1999) Cyanoprokaryota, Part 1: Chroococcales, Süsswasserflora von Mitteleuropa, Bd 19/1. Gustav Fischer Verlag, Stuttgart. 548p.).

In Brazil, 16 species of Peltula have already being reported, and most of the records were collected in states near the Atlantic Ocean (Tab. 1). In the Midwest region, only Peltula euploca (Ach.) Poelt, P. obscurans (Nyl.) Gyeln., and P. tortuosa (Ach.) Wetmore have been reported (Fleig & Riquelme 1991Fleig M & Riquelme I (1991) Liquens de Piraputanga, Mato Grosso do Sul, Brasil. Acta Botanica Brasilica 5: 3-12.; Aptroot & Spielmann 2020Aptroot A & Spielmann A (2020) New lichen species and records from the Serra da Bodoquena, Mato Grosso do Sul, Brazil, the westernmost Atlantic rain forest. Archives for Lichenology 16: 1-26.).

Table 1
Species of Peltula reported in Brazil. In bold, the species reported to Mato Grosso do Sul state.

This paper aims to contribute to the knowledge of Peltula biodiversity in Mato Grosso do Sul, Brazil. One new species and two new records are proposed using an integrative approach, utilizing morphological, anatomical, and phylogenetic analyses.

Material & Methods

The lichen collection deposited at the Universidade Federal de Mato Grande do Sul Herbarium (CGMS) was revised, and the Peltula species were selected for study. Students from the Federal University of Mato Grosso do Sul collected most of the specimens during expeditions carried out in the Corumbá and Ladário municipalities on the geographical boundaries between Brazil and Bolivia. Both municipalities are located in the Pantanal biome, a seasonally floodable tropical savannah characterized by 25.1 °C of mean annual temperature and 1,070.0 mm of mean annual precipitation (Soriano 1997Soriano BMA (1997) Caracterização climática de Corumbá-MS. EMBRAPA-CPAP. Boletim de Pesquisa 11: 1-25.), and a climate type Aw (Peel et al. 2007Peel MC, Finlayson BL & McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11: 1633-1644. <https://doi.org/10.5194/hess-11-1633-2007>).

Initially, anatomical and morphological studies were performed and the fungal barcode sequences, the Internal Transcribed Spacer (nuITS) region, were generated for all specimens, according to Kitaura et al. (2018)Kitaura MJ, Scur MC, Spielmann AA and Lorenz AP (2018) A revision of Leptogium (Collemataceae, lichenized Ascomycota) from Antarctica with a key to species. The Lichenologist 50: 467-485. <http://dx.doi.org/10.1017/S0024282918000269>. The obtained sequences were compared to those deposited at GenBank. The dataset was initially constituted of sequences of the Peltula and Lichinella from Kauff et al. (2018)Kauff F, Bachran A, Schultz M, Hofstetter V, Lutzoni F & Büdel B (2018) Molecular data favours a monogeneric Peltulaceae (Lichinomycetes). The Lichenologist 50: 313-327., including other species available in GenBank, as: P. africana (Jatta) Swinscow & Krog (MN103150), P. auriculata Büdel, M. Schultz & A. Gröger (DQ832329), P. euploca (MK811928), P. radicata Nyl. (MN103151, and MN103152), and P. umbilicata (Vain.) Swinscow & Krog (DQ832333). After the preliminary analyses, the dataset was reduced to the Peltula clades in which the analyzed species were positioned (Tab. S1, available on supplementary material <https://doi.org/10.6084/m9.figshare.19300175.v1>). Trichoglossum hirsutum (Pers.) Boud. (AY789314) was settled as outgroup.

The alignments were performed in Geneious v9.1.2 (Kearse et al. 2012Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P & Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649. <http://dx.doi.org/10.1093/bioinformatics/bts199>) with the MAFFT v7.308 algorithm (Katoh et al. 2002Katoh K, Misawa K, Kuma K & Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059-3066. <http://dx.doi.org/10.1093/nar/gkf436>). Additionally, the Gblocks web server (<http://molevol.cmima.csic.es/castresana/Gblocks_server.html>) was used to exclude unreliably aligned sites. Phylogenetic trees were estimated using the Bayesian (BA), and Maximum Likelihood (ML) approaches. The nucleotide substitution and site heterogeneity models were inferred following the Bayesian Inference Criterion in jModelTest2 (Darriba et al. 2012Darriba D, Taboada GL, Doallo R & Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. <http://dx.doi.org/10.1038/nmeth.2109>; Guindon & Gascuel 2003Guindon S & Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52: 696-704. <http://dx.doi.org/10.1080/10635150390235520>). The BA was performed in Beast v.1.8.0 (Drummond et al. 2012Drummond AJ, Suchard MA, Xie D & Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969-1973. <http://dx.doi.org/10.1093/molbev/mss075>) using GTR+I+G model, and the Yule speciation process was set prior to one run with a chain length of 10,000,000 generations sampled every 1,000 steps. The first 25% of the generated trees was discarded as burn-in, and maximum clade credibility trees were built with treeannotator. All values of effective sample sizes were checked for >200 in tracer (Rambaut et al. 2018Rambaut A, Drummond AJ, Xie D, Baele G & Suchard MA (2018) Posterior summarization in bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901-904. <https://doi.org/10.1093/sysbio/syy032>). ML trees were built with the RaxML v.7.2.8 (Stamatakis 2014Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313. <http://dx.doi.org/10.1093/bioinformatics/btu033>) plugin in Geneious v9.1.2, with 1,000 bootstrap replications and the remaining settings as default. FigTree v1.4.2 (<http://tree.bio.ed.ac.uk/software/figtree/>) was used to edit the trees and check for incongruences between the trees produced by the BA and ML methods. Support values of BA above 0.95 and bootstrap values of ML above 70 were considered significant for the hypotheses of phylogenetic relationships between the species examined.

The species descriptions included most of the characteristics used by Wetmore (1971)Wetmore CM (1971) The lichen family Heppiaceae in North America. Annals of the Missouri Botanical Garden 57: 158-209., and the anatomical sections were made through free hand (Kitaura et al. 2018Kitaura MJ, Scur MC, Spielmann AA and Lorenz AP (2018) A revision of Leptogium (Collemataceae, lichenized Ascomycota) from Antarctica with a key to species. The Lichenologist 50: 467-485. <http://dx.doi.org/10.1017/S0024282918000269>). Furthermore, we added details for the apothecia tissues when present, like subhymenium, hypothecium, parahymenium tissue, proprium and thalline exciples (Kitaura et al. 2018Kitaura MJ, Scur MC, Spielmann AA and Lorenz AP (2018) A revision of Leptogium (Collemataceae, lichenized Ascomycota) from Antarctica with a key to species. The Lichenologist 50: 467-485. <http://dx.doi.org/10.1017/S0024282918000269>), but chemical tests were not made. The lichen substances are usually lacking in Peltulaceae (Kauff et al. 2018Kauff F, Bachran A, Schultz M, Hofstetter V, Lutzoni F & Büdel B (2018) Molecular data favours a monogeneric Peltulaceae (Lichinomycetes). The Lichenologist 50: 313-327.).

Results

Phylogenetic analyses

In the present study, seven nuITS sequences were generated: five from P. anthracina, one from P. leptophylla and one from P. lingulata. The generated sequences were compared with other Peltula sequences available in GenBank (James et al. 2006James TY, Kauff F, Schoch C, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüßler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DD, Humber RA, Morton JB, Sugiyama J, Rossman A, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsura K, Langer E, Lanfer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW & Vilgalys R (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443: 818-822.; Kauff et al. 2018Kauff F, Bachran A, Schultz M, Hofstetter V, Lutzoni F & Büdel B (2018) Molecular data favours a monogeneric Peltulaceae (Lichinomycetes). The Lichenologist 50: 313-327.; Marthinsen et al. 2019Marthinsen G, Rui S & Timdal E (2019) OLICH: a reference library of DNA barcodes for Nordic lichens. Biodiversity Data Journal 7: e36252.), resulting in one prior dataset constituted of 55 sequences and 789 bp (base pairs), and the final dataset with 30 sequences and 685 bp (Tab. S1, available on supplementary material <https://doi.org/10.6084/m9.figshare.19300175.v1>).

The phylogenetic trees of BA and ML approaches were congruent and retained the main phylogenetic relationships revealed by the six-locus analysis of Kauff et al. (2018)Kauff F, Bachran A, Schultz M, Hofstetter V, Lutzoni F & Büdel B (2018) Molecular data favours a monogeneric Peltulaceae (Lichinomycetes). The Lichenologist 50: 313-327. (Fig. S1, available on supplementary material <https://doi.org/10.6084/m9.figshare.19300175.v1>; Fig. 1). The new species, Peltula anthracina, is phylogenetically close to P. clavata (Kremp.) Wetmore (MF766348) and P. lingulata (Vain.) Swinscow & Krog (MF766360 and LSC3364).

Figure 1
Bayesian Maximum Clade Credibility tree based on the nuITS dataset showing the phylogenetic relationships among Peltula species. Branches with posterior probabilities (PP) > 0·95 are in bold. Sequences obtained in this study are in bold.

The P. leptophylla sequence from Mato Grosso do Sul clustered with the other P. leptophylla sequence from Mexico, and the P. lingulata sequence from Mato Grosso do Sul clustered with the P. lingulata sequence from South Africa (Kauff et al. 2018Kauff F, Bachran A, Schultz M, Hofstetter V, Lutzoni F & Büdel B (2018) Molecular data favours a monogeneric Peltulaceae (Lichinomycetes). The Lichenologist 50: 313-327.).

New species

Peltula anthracina Kitaura, sp. nov. Fig. 2a-d

Figure 2
a-d. Peltula anthracina – a. distribution of the P. anthracina squamules; b. detail of the squamule with immerse apothecia; c. transversal section of the thallus, with upper cortex (Uc), photobiont (Pt), medullar region (Mr), and lower cortex (Lc); d. diametral section of the apothecia, highlighting the subhymenia (Sh) and asci with innumerous ascospores (arrow). (a-b. stereomicroscope images; c-d. light microscope images).

Type: Brazil, Mato Grosso do Sul State: Corumbá Municipality, Pantanal from Paraguay subregion, RPPN Rumo ao Oeste, Gaiba Bay, 17°44’18.10”S, 57°41’27.80”W, 91 m alt. 28.XI.2010. T.H. Stephanello et al. 384 (holotype CGMS). MycoBank: 839130

The epithet refers to the color of charcoal, or blackish as the charcoal. The color of the thallus is black as most of the Peltula species. We highlighted the importance of forest conservation, and we repudiate the destruction of the biomes from Mato Grosso do Sul through fire, which has literally transformed the native vegetation into charcoal.

Thallus peltate to squamulose, black under fluorescent light, matt, opaque, greenish-black under the stereomicroscope. Squamules 0.3–0.6 mm, simple or overlapping, 1–5(–8) squamules, simple to irregular branched, plane to concave, upper cortex smooth to the naked eye and 20x magnification; apices rounded to irregular, plane, without ornamentation; lateral margins irregular, plane to ascending, without ornamentation. Isidia and lobules absent. Thallus attached by canaliculus, adpressed on substrata, constituted cylindrical hyphae and cyanobacteria, cyanobacteria between the squamules. Apothecia immersed to adnate, 0.3–0.6 mm diam., laminal, one per squamule, disc concave, brownish; margin of apothecia and amphithecia concolorous with thallus, without ornaments. Pedicel absent. Pycnidia absent.

Anatomy. Thallus 110–225 µm, cortex subparaplectenchymatous, 15–25 µm thick, 3–5 (–7) layers of irregular cells; cells 2.5–5.0 µm diam. Medullar layer with clusters of cyanobacteria, usually near the upper cortex, green, spherical, up to 7.5 µm diam., central part hollow, scattered hyphae with some cyanobacteria. Apothecia with hymenium 75 µm thick; subhymenium and hypothecium indistinct, 25 µm thick; proper exciple absent; thalline exciple with subparaplectenchymatous cortex and cyanobacteria, apothecia cortex like the thallus cortex. Asci 45–50 × 10 µm, clavate, numerous ascospores per ascus, apices acute. Ascospores spherical, 2.5–4.0 µm diam., simple, hyaline.

Examined material: Corumbá municipality, Pantanal from Paraguay subregion, RPPN Rumo ao Oeste, Gaiba Bay, 17°44’18.10”S, 57°41’27.80”W, 91 m alt. 28.XI.2010. Leg. T.H. Stephanello et al. 382, 383, 386, 385 (paratypes CGMS).

Peltula anthracina is characterized by the thallus with simple to overlapping squamules, subparaplectenchymatous cortex, constituted with 3–5 layers of isodiametric cells, and immersed to adnate apothecia. The thalline exciple is composed of subparaplectenchymatous cortex.

Peltula clavata and P. lingulata are genetically close to P. anthracina. Peltula michroacanensis (de Lesd.) Wetmore is not genetically close but has a squamulose thallus without ornaments as well as P. anthracina. Therefore, the upper cortex is not developed in the first species (Wetmore 1971Wetmore CM (1971) The lichen family Heppiaceae in North America. Annals of the Missouri Botanical Garden 57: 158-209.), whereas it has 3–5 layers of isodiametric cells in the second species.

The thallus of Peltula obscurans var. deserticola (Zahlbr.) Wetmore is squamulose and has 105–240 µm thick, whereas P. anthracina has peltate and squamulose thallus with 110–225 µm thick. The cortex of P. obscurans var. deserticola is not developed and the P. anthracina cortex is subparaplectenchymatous.

Peltula leptophylla (Vain.) Büdel & M. Schultz, The Lichenologist: 324, 2018.

Basionym: Heppia leptophylla Vain., Acta Soc. Flora Fauna Fenn. 7(1): 216, 1890. Type: Brazil, Rio de Janeiro: “supra rupem graniticam litoralem, 1885, leg. E. Vainio n. 135”, (holotype UPS (L-013539), isotype TUR-VAIN 12474 (Lich. Bras. Exs. 1891)).

Examined material: Corumbá municipality, Pantanal from Paraguai subregion, RPPN Rumo ao Oeste, Guaiba Bay, saxicolous, 17°44’18.10”S, 57°41’27.80”W, 91 m alt., 28.XI.2010, leg., T.H. Stefanello et al. 379, pr. p. (CGMS, GenBank accession MW267848).

Peltula leptophylla is characterized by squamulose thallus, 1.0–1.5 mm long., crenulate and laciniate (Vainio 1890Vainio EA (1890) Étude sur la classification et la morphologie des lichens du Brésil, I. Acta Societatis pro Fauna et Flora Fennica 7: 1-247.).

The species was described originally by Vainio (1890)Vainio EA (1890) Étude sur la classification et la morphologie des lichens du Brésil, I. Acta Societatis pro Fauna et Flora Fennica 7: 1-247. from a specimen collected in Rio de Janeiro, but the first generated sequence belongs to a Mexican specimen (Kauff et al. 2018Kauff F, Bachran A, Schultz M, Hofstetter V, Lutzoni F & Büdel B (2018) Molecular data favours a monogeneric Peltulaceae (Lichinomycetes). The Lichenologist 50: 313-327.).

Peltula leptophylla has been reported for the first time to Mato Grosso do Sul state.

Peltula lingulata (Vain.) Swinscow & Krog, Norweg. J. Agric. Sci. 26(3): 220, 1979.

Basionym: ≡Heppia lingulata Vain., Beih. Nova Hedwigia 37: 43, 1898. Type: Uganda and Democratic Republic of the Congo: the Ruwenzori mountains, located on the border, “In rupe gneissacea ad Mbuyuri”, s/d (holotype TUR?).

Examined material: Ladário, Band’Alta farm, 19°10’59.00”S, 57°32’19.70”W, 208 m. alt., exposed, on lateritic bench, 4.IX. 2010. L.S. Canêz et al. 3364 (CGMS 31717, GenBank accession MW267847).

Peltula lingulata is characterized by tongue-shape squamules, with 0.3–0.4 × 1.0–2.0 mm (Vainio 1898Vainio E (1898) Lichenes a G.F. Scott-Elliot in viciniis montis Ruwenzori in Africa centrali annis 1893-1894 collecti. Hedwigia 37: 39-44.).

The Peltula lingulata type was collected originally in Ruwenzoni mountains, without more information, and described for the African continent. The first generated sequence belongs to a South African specimen.

The P. lingulata already was reported for Brazil in the state of Rio Grande do Sul (Fleig 1995Fleig M (1995) Lichens from “Casa de Pedra” and surroundings, Bagé, Rio Grande do Sul, Brazil. In: Daniëls FJA, Schulz M & Peine J (eds.) Flechten Follmann. Contributions to Lichenology in Honour of Gerhard Follmann. Geobotanical and Phytotaxonomical Study Group, Botanical Institute, University of Cologne, Cologne. Pp. 415-426.), but this is the first record for the state of Mato Grosso do Sul.

Discussion

Phylogenetic studies have altered the circumscriptions, taxonomy, known distribution, and species numbers of inconspicuous cyanolichens (Ertz et al. 2017Ertz D, Poulsen RS, Charrier M & Søchting U (2017) Taxonomy and phylogeny of the genus Steinera (Arctomiales, Arctomiaceae) in the subantarctic islands of Crozet and Kerguelen. Phytotaxa 324: 201-238.; Fryday et al. 2017Fryday AM, Ertz D & Jørgensen PM (2017) Insights into the genus Austrella (Pannariaceae, Peltigerales), including a new species from the Falkland Islands. The Lichenologist 49: 57-65.; Park et al. 2018Park CH, Hong SG & Elvebakk A (2018) Psoroma antarcticum, a new lichen species from Antarctica and neighbouring areas. Polar Biology 41: 1083-1090.; Liu et al. 2018Liu L, Razaq A, Atri NS, Bau T, Belbahri L, Bouket AC, Chen L, Deng C, Ilyas S, Khalid AN, Kitaura MJ, Kobayashi T, Li Y, Lorenz AP, Ma Y, Malysheva E, Malysheva V, Nuytinck J, Qiao M, Saini MK, Scur MC, Sharma S, Shu L, Spirin V, Tanaka Y, Tojo M, Uzuhashi S, Valério-Júnior C, Verbeken A, Verma B, Wu R, Xu J, Yu Z, Zeng H, Zhang B, Banerjee A, Beddiar A, Bordallo J, Dafri A, Dima B, Krisai-Greilhuber I, Lorenzini M, Mandal R, Morte A, Sarathi Nath PS, Papp V, Pavlík J, Rodríguez A, Ševcíková H, Urban A, Voglmayr H & Zapparoli G. (2018) Fungal Systematics and Evolution: FUSE 4. Sydowia 70: 211-286.). Groups that have been classified according to morphological characters often do not correspond to phylogenetic patterns. An example is Peltulaceae, which was proposed with three genera, Peltula, Phyllopeltula and Neoheppia, separated mainly by the thalli type, but which proved to be monogeneric after a six-loci analysis. In this sense, Kauff et al. (2018)Kauff F, Bachran A, Schultz M, Hofstetter V, Lutzoni F & Büdel B (2018) Molecular data favours a monogeneric Peltulaceae (Lichinomycetes). The Lichenologist 50: 313-327. underlined that new species of Peltula should be carefully proposed with a clear connection between the defined operational taxonomic units (OTU) and the morphological analyses. Therefore, Peltula anthracina is proposed here as new to science based on an integrative approach through morphological, anatomical and molecular analyses.

The P. anthracina specimens were preliminarily determined as P. auriculata (Canêz et al., personal communication), but they do not have the characteristic of ear-shape squamules. Furthermore, P. auriculata have thallus with olive-brown color 200–300(–500) µm thick, and the upper cortex is composed of globose hyphal cells 0–5 µm (one layer of cells) thick (Schultz et al. 2000Schultz M, Porembski S & Büdel B (2000) Diversity of rock-inhabiting cyanobacterial lichens: studies on granite inselbergs along the Orinoca and the Guyana region. Plant Biology 2: 482-495.), whereas P. anthracina has a thallus colored black to greenish black, 110–225 µm thick, and the upper cortex composed by subparaplectenchymatous cells that are 15–25 µm (3–5 layers of cells) thick. Peltula clavata has a thallus minutely subfruticose and the surface covered by scattered minute isidia (Wetmore 1971Wetmore CM (1971) The lichen family Heppiaceae in North America. Annals of the Missouri Botanical Garden 57: 158-209.), whereas P. anthracina has a thallus peltate to squamulose and the upper surface without ornaments; and Peltula lingulata is characterized by a subfruticose squamulose thallus tongue-shaped, which differs from the squamulose thallus of P. anthracina. The generated sequences of P. anthracina also resulted in a distinct lineage that separated from the P. clavata (MF766348), P. lingulata (MF766360 and LSC3364) and P. auriculata lineages, corroborating the morphological and anatomical analysis.

The species were found in a wet region but with arid microclimatic features in which Peltula species are typically found. The Pantanal is a dynamic ecosystem with different phytophysiognomies that are shaped and influenced by a flood regime, where seasons are well-defined by wet (October-April) and dry (May-September) seasons. This region is influenced by the Amazon, Atlantic Forest, Cerrado and Chaco, where high biodiversity is found for different groups of animals, plants (Nunes da Cunha et al. 2007Nunes da Cunha C, Junk WJ & Leitão-Filho HF (2007) Woody vegetation in the Pantanal of Mato Grosso, Brazil: a preliminary typology. Amazoniana 19: 159-184.; Junk et al. 2014Junk WJ, Piedade MTF, Lourival R, Wittmann F, Kandus P, Lacerda LD, Bozelli RL, Esteves FA, Nunes da Cunha C, Maltchik L, Schöngart J, Schaeffer-Novelli Y & Agostinho AA (2014) Brazilian wetlands: their definition, delineation, and classification for research, sustainable management, and protection. Aquatic Conservation Marine and Freshwater Ecossystems 24: 5-22.), and possibly lichenized fungi. However, the dry season and mostly the anthropogenic activities associated with extensive agriculture has suggested that the Pantanal biome, though an elevated occurrence of fires, (Oliveira-Junior et al. 2020) is associated with changes in the vegetation shape, structure, and composition (Araújo et al. 2017Araújo FDC, Tng DYP, Apgaua DMG, Coelho PA, Pereira DGS & Santos RM (2017) Post-fire plant regeneration across a closed forest-savanna vegetation transition. Forest Ecology and Management 400: 77-84.).

With this study, the number of Peltula species has doubled for the Mato Grosso do Sul, and new field studies should reveal even greater lichen biodiversity for the region. Therefore, the conservation of natural vegetation is key to preserving the diversity of lichens, and ecological studies are key to understanding the response of these organisms to climate change in which the Pantanal of Mato Grosso do Sul is undergoing.

Acknowledgements

All the authors thank the anonymous reviewers, for improving this manuscript considerably. This work was supported in part by the Fundação Universidade Federal de Mato Grosso do Sul - UFMS/MEC - Brazil. Marcos J. Kitaura was supported in part by the Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (FUNDECT - Chamada 04/2019), and by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq); and Jean-Marc Torres and Mayara Camila Scur by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) - Finance Code 001.

References

  • Aptroot A & Cáceres MES (2018) New species and new records of lichens from inselbergs and surrounding Atlantic rain forest in the Chapada Diamantina (Bahia, Brazil). Herzogia 31: 359-373.
  • Aptroot A, Feuerstein SC, Cunha-Dias IPR, Nunes ARL, Honorato ME & Cáceres MES (2017a) New lichen species and lichen reports from Amazon forest remnants and Cerrado vegetation in the Tocantina Region, northern Brazil. The Bryologist 120: 320-328.
  • Aptroot A, Gumboski EL & Cáceres MES (2017b) Ocean view: a first assessment of the littoral, crustose lichen biota of south Brazil. The Lichenologist 49: 597-605.
  • Aptroot A & Spielmann A (2020) New lichen species and records from the Serra da Bodoquena, Mato Grosso do Sul, Brazil, the westernmost Atlantic rain forest. Archives for Lichenology 16: 1-26.
  • Araújo FDC, Tng DYP, Apgaua DMG, Coelho PA, Pereira DGS & Santos RM (2017) Post-fire plant regeneration across a closed forest-savanna vegetation transition. Forest Ecology and Management 400: 77-84.
  • Büdel B (1987) Review of Zur Biologie und Systematik der Flechtengattungen Heppia und Peltula im sudlichen Afrika. The Lichenologist 19: 441-442.
  • Büdel B (1995) The lichen genus Neoheppia Mycotaxon 54: 137-145.
  • Büdel B, Becker U, Follmann G & Sterflinger K (2000) Algae, fungi, and lichens on inselbergs. Ecological Studies 146: 69-90.
  • Cáceres MES, Aptroot A & Lücking R (2017a) Lichen fungi in the Atlantic rain forest of Northeast Brazil: the relationship of species richness with habitat diversity and conservation status. Brazilian Journal of Botany 40: 145-156.
  • Cáceres MES, Júnior MN, Santos LA, Pereira TA & Aptroot A (2017b) New records to Brazil and Southern Hemisphere of corticolous and saxicolous lichens from the semiarid region in Ceará. Iheringia, Série Botânica 27: 239-245.
  • Cáceres MES, Nascimento ELL, Aptroot A & Lücking R (2014) Liquens brasileiros: novas descobertas evidenciam a riqueza no norte e nordeste do país. Boletim do Museu de Biologia Mello Leitão 35: 101-119.
  • Darriba D, Taboada GL, Doallo R & Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. <http://dx.doi.org/10.1038/nmeth.2109>
  • Drummond AJ, Suchard MA, Xie D & Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969-1973. <http://dx.doi.org/10.1093/molbev/mss075>
  • Ertz D, Poulsen RS, Charrier M & Søchting U (2017) Taxonomy and phylogeny of the genus Steinera (Arctomiales, Arctomiaceae) in the subantarctic islands of Crozet and Kerguelen. Phytotaxa 324: 201-238.
  • Fleig M (1995) Lichens from “Casa de Pedra” and surroundings, Bagé, Rio Grande do Sul, Brazil. In: Daniëls FJA, Schulz M & Peine J (eds.) Flechten Follmann. Contributions to Lichenology in Honour of Gerhard Follmann. Geobotanical and Phytotaxonomical Study Group, Botanical Institute, University of Cologne, Cologne. Pp. 415-426.
  • Fleig M & Riquelme I (1991) Liquens de Piraputanga, Mato Grosso do Sul, Brasil. Acta Botanica Brasilica 5: 3-12.
  • Fryday AM, Ertz D & Jørgensen PM (2017) Insights into the genus Austrella (Pannariaceae, Peltigerales), including a new species from the Falkland Islands. The Lichenologist 49: 57-65.
  • Guindon S & Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52: 696-704. <http://dx.doi.org/10.1080/10635150390235520>
  • James TY, Kauff F, Schoch C, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüßler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DD, Humber RA, Morton JB, Sugiyama J, Rossman A, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsura K, Langer E, Lanfer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW & Vilgalys R (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443: 818-822.
  • Junk WJ, Piedade MTF, Lourival R, Wittmann F, Kandus P, Lacerda LD, Bozelli RL, Esteves FA, Nunes da Cunha C, Maltchik L, Schöngart J, Schaeffer-Novelli Y & Agostinho AA (2014) Brazilian wetlands: their definition, delineation, and classification for research, sustainable management, and protection. Aquatic Conservation Marine and Freshwater Ecossystems 24: 5-22.
  • Kauff F, Bachran A, Schultz M, Hofstetter V, Lutzoni F & Büdel B (2018) Molecular data favours a monogeneric Peltulaceae (Lichinomycetes). The Lichenologist 50: 313-327.
  • Katoh K, Misawa K, Kuma K & Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059-3066. <http://dx.doi.org/10.1093/nar/gkf436>
  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P & Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649. <http://dx.doi.org/10.1093/bioinformatics/bts199>
  • Kitaura MJ, Scur MC, Spielmann AA and Lorenz AP (2018) A revision of Leptogium (Collemataceae, lichenized Ascomycota) from Antarctica with a key to species. The Lichenologist 50: 467-485. <http://dx.doi.org/10.1017/S0024282918000269>
  • Komárek J & Anagnostidis K (1999) Cyanoprokaryota, Part 1: Chroococcales, Süsswasserflora von Mitteleuropa, Bd 19/1. Gustav Fischer Verlag, Stuttgart. 548p.
  • Liu L, Razaq A, Atri NS, Bau T, Belbahri L, Bouket AC, Chen L, Deng C, Ilyas S, Khalid AN, Kitaura MJ, Kobayashi T, Li Y, Lorenz AP, Ma Y, Malysheva E, Malysheva V, Nuytinck J, Qiao M, Saini MK, Scur MC, Sharma S, Shu L, Spirin V, Tanaka Y, Tojo M, Uzuhashi S, Valério-Júnior C, Verbeken A, Verma B, Wu R, Xu J, Yu Z, Zeng H, Zhang B, Banerjee A, Beddiar A, Bordallo J, Dafri A, Dima B, Krisai-Greilhuber I, Lorenzini M, Mandal R, Morte A, Sarathi Nath PS, Papp V, Pavlík J, Rodríguez A, Ševcíková H, Urban A, Voglmayr H & Zapparoli G. (2018) Fungal Systematics and Evolution: FUSE 4. Sydowia 70: 211-286.
  • Lücking R, Hodkinson BP & Leavitt SD (2017) Corrections and amendments to the 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota. Bryologist 120: 58-69.
  • Makryi TV (2016) Peltula pannarioides and P. rosulata (Peltulaceae), new lichen species from Baikal Siberia. Novosti Sistematiki Nizshikh Rastenii 50: 213-242.
  • Makryi TV (2017) Peltula daurica (Peltulaceae), a new lichen species from Dauria (Transbaikal Territory). Novosti Sistematiki Nizshikh Rastenii 51: 191-203.
  • Marques J, Schultz M & Paz-Bermúdez G (2013) A Peltula Nyl. diversity hotspot in north-east Portugal, with one species new to science and three species new to mainland Europe. The Lichenologist 45: 483-498.
  • Marthinsen G, Rui S & Timdal E (2019) OLICH: a reference library of DNA barcodes for Nordic lichens. Biodiversity Data Journal 7: e36252.
  • Nübel U, Garcia-Pichel F & Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Applied and Environmental Microbiology 63: 3327-3332.
  • Nunes da Cunha C, Junk WJ & Leitão-Filho HF (2007) Woody vegetation in the Pantanal of Mato Grosso, Brazil: a preliminary typology. Amazoniana 19: 159-184.
  • Oliveira-Júnior JF, Teodoro PE, Silva Junior CA, Baio FHR, Gava R, Capristo-Silva GF & Costa MS (2020) Fire foci related to rainfall and biomes of the state of Mato Grosso do Sul, Brazil. Agricultural and Forest Meteorology 282-283: 107861.
  • Park CH, Hong SG & Elvebakk A (2018) Psoroma antarcticum, a new lichen species from Antarctica and neighbouring areas. Polar Biology 41: 1083-1090.
  • Peel MC, Finlayson BL & McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11: 1633-1644. <https://doi.org/10.5194/hess-11-1633-2007>
  • Rambaut A, Drummond AJ, Xie D, Baele G & Suchard MA (2018) Posterior summarization in bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901-904. <https://doi.org/10.1093/sysbio/syy032>
  • Schultz M & Aptroot A (2008) Notes on poorly known, small cyanobacterial lichens from predominantly wet tropical to subtropical regions. Sauteria 15: 433-458.
  • Schultz M, Porembski S & Büdel B (2000) Diversity of rock-inhabiting cyanobacterial lichens: studies on granite inselbergs along the Orinoca and the Guyana region. Plant Biology 2: 482-495.
  • Soriano BMA (1997) Caracterização climática de Corumbá-MS. EMBRAPA-CPAP. Boletim de Pesquisa 11: 1-25.
  • Spielmann AA (2006) Checklist of lichens and lichenicolous fungi of Rio Grande do Sul (Brazil). Caderno de Pesquisa Série Biologia 18: 7-125.
  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313. <http://dx.doi.org/10.1093/bioinformatics/btu033>
  • Vainio EA (1890) Étude sur la classification et la morphologie des lichens du Brésil, I. Acta Societatis pro Fauna et Flora Fennica 7: 1-247.
  • Vainio E (1898) Lichenes a G.F. Scott-Elliot in viciniis montis Ruwenzori in Africa centrali annis 1893-1894 collecti. Hedwigia 37: 39-44.
  • Wetmore CM (1971) The lichen family Heppiaceae in North America. Annals of the Missouri Botanical Garden 57: 158-209.
  • Zahlbruckner A (1909) Lichenes (Flechten). In: Schiffner V (ed.) Ergebnisse der botanischen expedition der kaiserlichen Akademie der Wissenschaften nach Südbrasilien, 1901, 2. Band. Denkschriften der Kaiserlichen Akademie der Wissenschaften 83: 85-211.

Supplementary Material

See supplementary material at <https://doi.org/10.6084/m9.figshare.19300175.v1>

Publication Dates

  • Publication in this collection
    01 Apr 2022
  • Date of issue
    2022

History

  • Received
    28 Nov 2020
  • Accepted
    12 Apr 2021
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