<i>Ephebe brasiliensis</i> (Ascomycota, Lichinaceae): an overlooked freshwater lichenized fungus

Gumboski, Emerson Luiz; Gerlach, Alice da Cruz Lima; Spielmann, Adriano Afonso; Canêz, Luciana da Silva; Marcelli, Marcelo Pinto

doi:10.1590/2175-7860201970086

Abstract

Ephebe brasiliensis is a semi-aquatic fruticose cyanolichen that occurs in freshwater environments from Brazil (Minas Gerais and São Paulo states) and Uruguay. Although this species may be locally abundant and has "wide" distribution, it has been poorly studied and is still misunderstood with respect to their distribution and ecological characteristics. Herein, E. brasiliensis is reported for the first time in Southern Brazil.

Key words: Atlantic Forest; biodiversity; cyanobacteria; cyanolichen; Stigonema

Resumo

Ephebe brasiliensis é um cianolíquen fruticoso e semiaquático que ocorre em ambientes de água doce do Brasil e Uruguai. Embora essa espécie possa ser localmente abundante e apresente uma ampla distribuição geográfica, ela ainda é pouco estudada e permanece incompreendida. Nesse artigo, E. brasiliensis é registrada pela primeira para o Sul do Brasil.

Palavras-chave: Floresta Atlântica; biodiversidade; cianobactéria; cianolíquen; Stigonema

Lichens with cyanobacteria as the main photobiont are commonly known as cyanolichens and correspond to a small group gathering approximately 12% of lichen-forming fungal species (Rikkinen 2003).

The most well-known genera of cyanolichens in Brazil are Leptogium (Ach.) Gray (e.g., Müller Argoviensis 1891; Marcelli 1992; Osorio 1997; Spielmann 2006; Kitaura & Marcelli 2012, 2013; Kitaura et al. 2013a,b, 2014; Benatti et al. 2013), Collema F. H. Wigg., and Coccocarpia Pers. (e.g., Müller Argoviensis 1891; Degelius 1974; Osorio 1977; Fleig 1990; Spielmann 2006; Eliasaro et al. 2009; Gumboski & Eliasaro 2011), still with unreported/undiscovered species for many localities. In fact, genera with large thalli, which are frequently collected by non-lichenologists, such as Sticta (Schreb.) Ach. (p.p.) and Peltigera Willd, present many dubious citations and need revision (see Vitikainen 1998; Moncada et al. 2014).

Other cyanolichens recorded in Brazil are also still poorly known in relation to their taxonomy, ecology, and mainly their actual distribution within of the country. These include Peltula Nyl., Jenmania W. Wächt., Leprocollema Vain., Pyrenopsis (Nyl.) Nyl. and Ephebe Fr., whose species are recorded for few localities, most often only in very succinct species list (e.g., Vainio 1890; Osorio & Homrich 1978; Fleig 1995; Spielmann et al. 2007). Overall, the actual distribution and ecological features of these taxa are poorly understood.

The knowledge about semi-aquatic lichens (which remain submerged for a substantial amount of time) is even more incipient in Brazil. Even though many crustose lichens from freshwater and marine habitats were reported in Europe and USA (e.g., Verrucaria Schrad.; Orange et al. 2009; Peltigera hydrothyria Miadl. & Lutzoni; Brodo et al. 2001), only informal observations indicated that this fascinating group of lichens also occurs in freshwater and marine habitats in Brazil (author's personal field experience, unpublished data). This is the first attempt at the semi-aquatic lichens from Brazil. Many questions about these lichens still remain unclear, and we suggest the following references for more information (e.g., Hawkswoth 2000; Shearer et al. 2007; Nash 2008).

The genus Ephebe (Lichinaceae) is widespread, currently with 13 species (Lücking et al. 2017) and is characterized by the black to brownish black fruticose thallus with the cyanobacteria Stigonema determining the appearance of the whole thallus. This species branches are terete, its hymenium never covered by photobiont filaments, and occurs in semi-aquatic freshwater habitats (Vainio 1890; Henssen 1963; Schultz & Büdel 2002). In South America only two, poorly known species have been recorded: Ephebe ocellata Henssen, recorded in Argentina (Calvelo & Liberatore 2002) and Chile (Henssen 1963; Galloway & Quilhot 1998), and E. brasiliensis (Vain.) Henssen, reported to Brazil (Vainio 1890; Müller Argoviensis 1895; Henssen 1963; Aptroot 2002) and Uruguay (Osorio 1975).

Ephebe brasiliensis was currently only known for two localities in Brazil, the type locality in the state of Minas Gerais (Vainio 1890; Henssen 1963; Aptroot 2002) and in the state of São Paulo (Henssen 1963), as well as one single locality in Uruguay (Osorio 1975) (Fig. 1). These localities are over 1000 km apart in a North-South line, and the wide range of environments between them demonstrates the lack of information about the species distribution. This report records now Ephebe brasiliensis in Southern Brazil and aim to contribute with information about its distribution, taxonomy, and ecological features.

Figure 1
Distribution of Ephebe brasiliensis in Brazil and Uruguay. Already known records are in black circles, the new records are in red triangles.

Specimens were collected using a knife, stored in paper bags, and dried at room temperature. They were examined using standard stereoscope (20-40×) and light microscope (100-1000×) techniques. Freehand sections of the thalli were mounted in water. The spot tests (K, C, KC and P), observations under UV light, and thin layer chromatography (TLC) using solvent system C were conducted according to Huneck & Yoshimura (1996) and Orange et al. (2001). The distribution map (Fig. 1) was produced in QGIS Software 2.0.1, according to a tutorial developed by Calegari et al. (2016).

Ephebebrasiliensis (Vain.) A. Henssen, Symb. Bot. Upsal. 18(1): 56. 1963.

≡ Ephebeia brasiliensis Vain., Acta Soc. Fauna Fl. Fenn. 7: 245. 1890. Brazil, Minas Gerais state, Catas Altas, Caraça, 1885, Vainio (Holotype: TUR; Isotype: BM, UPS). fide Henssen (1963).

= Ephebe uleana Müll. Arg., Hedwigia 34: 27. 1895. Brazil, Minas Gerais state, Catas Altas, Caraça, 1892, Ule (Isotypes: HBG, UPS). fide Henssen (1963). Fig. 2

Figure 2
Ephebe brasiliensis - a. habitat with submerged thalli; b. thallus not submerged attached to rock. Scale bar: 1 cm.

Description. Thallus fruticose, caespitose, black to bluish black, shiny when wet and somewhat olive opaque when dry, up to 3 cm tall in the field, up to 1.5 cm tall when dry, something gelatinous when wet and brittle when dry, homoiomerous, ecorticate; branches terete, (90-)105-180 µm thick, solid, surface smooth to somewhat rough, branching mainly anisotomic-dicotomic, sometimes trichotomic and rarely tetracotomic, apices usually curved, frequently with up to 6 tiny branches. Photobiont with true branching. Ascomata and pycnidia not found.

Chemistry. Spot tests: K-, C-, KC-, P-, UV-. No substances detected by TLC.

Substrate and ecology. Most specimens were found on rocks in montane water streams, with at least a thin layer of freshwater (Fig. 3). Specimens from the state of Santa Catarina were found in semi-aquatic conditions (Fig. 2a), while some specimens, including those from the state of Rio Grande do Sul, were found submersed up to 0.4 m. Nevertheless, they can survive out of the water during dry periods (Fig. 2b). Locally, this species is abundant, forming a large population that can occupy several square meters.

Figure 3
Habitat of Ephebe brasiliensis found in Rio Grande do Sul state, Municipality of Cambará do Sul, National Park Serra Geral.

Specimens examined: BRAZIL. RIO GRANDE DO SUL: Municipality of Cambará do Sul, National Park Serra Geral, Tigre Preto, 14.III.2014, A. Gerlach & M. Akkerman 1484 (ICN); Fortaleza Canion, on submerse rock on stream, 05.V.2007, L.S. Canêz, A.A. Spielmann, P. Jungbluth & M.J. Kitaura 2488 (CGMS). SANTA CATARINA: Municipality of São Bento do Sul, APA Rio Vermelho/Humboldt, Araucaria forest, rural area, on rocks submerged in the river, 26°15'23.26"S, 49°16'48.84"W, 16.II.2013, E. Gumboski 4240 (JOI); 12.III.2013, E. Gumboski 4282, 4288 (JOI), 31.X.2013, E. Gumboski 4896 (JOI). MINAS GERAIS: Municipality of Catas Altas, Parque Natural do Caraça, 27.VII.2010, A. Gerlach 274 (ICN); 20°05'38.7" S, 43°30'00.3" W, Cascudos Stream, on submerse sedimentar rock, 27.III.2006, L.S. Canêz, A.A. Spielmann & M.P. Marcelli 1477 (CGMS).

In Brazil, Ephebe brasiliensis is a freshwater lichen that can be recognized even when it is sterile. It is characterized by the black to bluish black fruticose thallus, containing Stigonema species as photobiont, with (90-)105-180 µm thick branches. According to Vainio (1890) and Henssen (1963), the species have lecanorine apothecia, lateral to terminal, up to 0.5 mm diam., with 16-spored asci, ascospores simple, colorless, ellipsoid, 9-16 × 4-7 µm (immature in asci). The conidia are cylindrical, 2.5-3 × 1 µm. This species can be found on rocks, submerged or not, in semi-aquatic or aquatic environments.

As previously known, lichens are excellent environmental bio monitors (e.g., Cislaghi & Nimis 1997; Nash 2008). Therefore, we recommend that Ephebe brasiliensis would be included as a key species for future biomonitoring and water quality investigations due to its occurrence in conserved areas (i.e. National Parks).

Future studies are important for conservation strategies of the species, and we postulate that E. brasiliensis probably presents an even wider distribution in South America.

The first author thanks Dr. Matthias Schultz (University of Hamburg, Germany) for taxonomic confirmation of specimens from Santa Catarina.

References

Aptroot A (2002) New and interesting lichens and lichenicolous fungi in Brazil. Fungal Diversity 9: 15-45.
Benatti MN, Kitaura MJ, Marcelli MP & Cunha IPR (2013) Cianoliquens dos gêneros Coccocarpia, Collema e Leptogium do Parque Estadual da Cantareira, SP, Brasil, depositados no herbário SP. Hoehnea 40: 131-141.
Brodo IM, Duran Sharnoff S & Sharnoff S (2001) Lichens of North America. Yale University Press, New Haven & London. 795p.
Calegari BB, Delapieve ML, Sousa LM (2016)Tutorial para preparação de mapas de distribuição geográfica. Boletim, Sociedade Brasileira de Ictiologia 118: 15-30.
Calvelo S & Liberatore S (2002) Catálogo de los líquenes de la Argentina. Kurtziana 29: 7-170
Cislaghi C & Nimis PL (1997) Lichens, air pollution and lung cancer. Nature 387: 463-464.
Degelius G (1974) The lichen genus Collema with special reference to the extra European species. Symbolae Botanicae Upsalienses 20: 1-215.
Eliasaro S, Veiga PW, Donha CG & Nogueira L (2009)Inventário de macroliquens epífitos sobre árvores utilizadas na arborização urbana em Curitiba, Paraná, Brasil: Subsídio para biomonitoramento urbano. Biotemas 22: 1-8.
Fleig M (1990) Liquens da Estação Ecológica de Aracuri. Novas ocorrências no Rio Grande do Sul. Iheringia Série Botânica 40: 121-125.
Fleig M (1995) Lichens from "Casa de Pedra" and surroundings, Bagé, Rio Grande do Sul, Brazil. In: Daniels FJA, Schulz M,Peine J. (eds.) Flechten Follman. Contributions to lichenology in honour of Gerhard Follman. Geobotanical and Phytotaxonomical study group. Botanical Institute, University of Cologne, Cologne Pp. 415-426.
Galloway DJ & Quilhot W (1998) Checklist of Chilean lichen-forming and lichenicolous fungi. Gayana Botanica 55: 111-185.
Gumboski EL & Eliasaro S (2011) Checklist of lichenized fungi of Santa Catarina state (Brazil). Mycotaxon 115: 535.
Hawksworth DL (2000) Freshwater and marine lichen-forming fungi. In: Hyde KD, Hoand WH & Pointing SB (eds) Aquatic mycology across the Millennium. Fungal Diversity 5: 1-7.
Henssen A (1963) Eine Revision der Flechtenfamilien Lichinaceae und Ephebaceae. Symbolae Botanicae Upsalienses 18: 1-123.
Huneck S & Yoshimura I (1996) Identification of Lichen Substances. Springer-Verlag, Berlin, Heidelberg. 101p.
Kitaura MJ & Marcelli MP (2012) The Leptogium juressianum complex in southeastern Brazil. Mycotaxon 120: 215-221.
Kitaura MJ & Marcelli MP (2013) A revision of Leptogium species with spherical-celled hairs (section Mallotium p.p.). The Bryologist 116: 15-27.
Kitaura MJ, Marcelli MP, Hora BR & Jungbluth P (2013a) A new non-isidiate Leptogium species with transverse septate ascospores from Southeastern Brazil. Mycosphere 4: 986-992.
Kitaura MJ, Marcelli MP, Jungbluth P & Hora BR (2013b) Five supposedly well-known species of Leptogium section Mallotium. Mycosphere 4: 520-530.
Kitaura MJ, Kaffer MI, Marcelli MP & Martins SMA (2014) A new hairy Leptogium (Section Mallotium) from Rio Grande do Sul, Brazil. Hoehnea 41: 303-306.
Lücking R, Hodkinson BP & Leavitt SD (2017) The 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota - Approaching one thousand genera. The Bryologist 119: 361-416.
Marcelli MP (1992) Ecologia liquênica nos manguezais do sul-sudeste brasileiro. Bibliotheca Lichenologica 47: 1-310.
Moncada B, Lücking R. & Suárez A (2014) Molecular phylogeny of the genus Sticta (lichenized Ascomycota: Lobariaceae) in Colombia. Fungal Diversity 64: 205-231.
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Nash TH (2008) Lichen biology. 2ª ed. Cambridge University Press, Cambridge 486p.
Orange A, James PW & White FJ (2001) Microchemical Methods for the Identification of Lichens. British Lichen Society, London. 101p.
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Osorio HS (1975) Contribution to the lichen flora of Uruguay. VIII. Additions and corrections. Comunicaciones Botánicas del Museo de Historia Natural de Montevideo 4: 1-12.
Osorio HS (1977) Contribution to the lichen flora of Brazil II. Lichens from Guarapuava, Paraná state. Dusenia 10: 101-102.
Osorio HS (1997) Contribution to the lichen flora of Brazil. XXXIV. Lichens from Laguna, Santa Catarina state. Comunicaciones Botánicas del Museo de Historia Natural de Montevideo 6: 1-4.
Osorio HS & Homrich M (1978) Contribution to the lichen flora of Brazil IV. Lichens from southern Rio Grande do Sul. The Bryologist 81: 452-454.
Rikkinen J (2003) Ecological and evolutionary role of photobiont-mediated guilds in lichens. Symbiosis 34: 99-110.
Schultz M & Büdel B (2002) Key to the genera of the Lichinaceae. Lichenologist 34: 39-62.
Spielmann AA (2006) Checklist of lichens and lichenicolous fungi of Rio Grande do Sul (Brazil). Caderno de Pesquisa Série Biologia 18: 7-125.
Spielmann AA, Osorio HS & Marcelli MP. (2007) Jenmania osorioi is added to the flora of Brazil. Comunicaciones Botánicas, Museo de Historia Natural y Anthroplogía [Montevideo] 6(134): 1-3.
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.
Vitikainen O (1998) Taxonomic notes on Neotropical species of Peltigera. In: Marcelli MP & Seaward MRD (eds). Lichenology in Latin America: history, current knowledge and applications. CETESB, São Paulo. Pp. 135-139.

Edited by

Editor de área: Dr. Anibal de Carvalho Junior

Publication Dates

Publication in this collection
20 Dec 2019
Date of issue
2019

History

Received
03 Apr 2018
Accepted
26 June 2018

This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

[1] Aptroot A (2002) New and interesting lichens and lichenicolous fungi in Brazil. Fungal Diversity 9: 15-45.

[2] Benatti MN, Kitaura MJ, Marcelli MP & Cunha IPR (2013) Cianoliquens dos gêneros Coccocarpia, Collema e Leptogium do Parque Estadual da Cantareira, SP, Brasil, depositados no herbário SP. Hoehnea 40: 131-141.

[3] Brodo IM, Duran Sharnoff S & Sharnoff S (2001) Lichens of North America. Yale University Press, New Haven & London. 795p.

[4] Calegari BB, Delapieve ML, Sousa LM (2016)Tutorial para preparação de mapas de distribuição geográfica. Boletim, Sociedade Brasileira de Ictiologia 118: 15-30.

[5] Calvelo S & Liberatore S (2002) Catálogo de los líquenes de la Argentina. Kurtziana 29: 7-170

[6] Cislaghi C & Nimis PL (1997) Lichens, air pollution and lung cancer. Nature 387: 463-464.

[7] Degelius G (1974) The lichen genus Collema with special reference to the extra European species. Symbolae Botanicae Upsalienses 20: 1-215.

[8] Eliasaro S, Veiga PW, Donha CG & Nogueira L (2009)Inventário de macroliquens epífitos sobre árvores utilizadas na arborização urbana em Curitiba, Paraná, Brasil: Subsídio para biomonitoramento urbano. Biotemas 22: 1-8.

[9] Fleig M (1990) Liquens da Estação Ecológica de Aracuri. Novas ocorrências no Rio Grande do Sul. Iheringia Série Botânica 40: 121-125.

[10] Fleig M (1995) Lichens from "Casa de Pedra" and surroundings, Bagé, Rio Grande do Sul, Brazil. In: Daniels FJA, Schulz M,Peine J. (eds.) Flechten Follman. Contributions to lichenology in honour of Gerhard Follman. Geobotanical and Phytotaxonomical study group. Botanical Institute, University of Cologne, Cologne Pp. 415-426.

[11] Galloway DJ & Quilhot W (1998) Checklist of Chilean lichen-forming and lichenicolous fungi. Gayana Botanica 55: 111-185.

[12] Gumboski EL & Eliasaro S (2011) Checklist of lichenized fungi of Santa Catarina state (Brazil). Mycotaxon 115: 535.

[13] Hawksworth DL (2000) Freshwater and marine lichen-forming fungi. In: Hyde KD, Hoand WH & Pointing SB (eds) Aquatic mycology across the Millennium. Fungal Diversity 5: 1-7.

[14] Henssen A (1963) Eine Revision der Flechtenfamilien Lichinaceae und Ephebaceae. Symbolae Botanicae Upsalienses 18: 1-123.

[15] Huneck S & Yoshimura I (1996) Identification of Lichen Substances. Springer-Verlag, Berlin, Heidelberg. 101p.

[16] Kitaura MJ & Marcelli MP (2012) The Leptogium juressianum complex in southeastern Brazil. Mycotaxon 120: 215-221.

[17] Kitaura MJ & Marcelli MP (2013) A revision of Leptogium species with spherical-celled hairs (section Mallotium p.p.). The Bryologist 116: 15-27.

[18] Kitaura MJ, Marcelli MP, Hora BR & Jungbluth P (2013a) A new non-isidiate Leptogium species with transverse septate ascospores from Southeastern Brazil. Mycosphere 4: 986-992.

[19] Kitaura MJ, Marcelli MP, Jungbluth P & Hora BR (2013b) Five supposedly well-known species of Leptogium section Mallotium. Mycosphere 4: 520-530.

[20] Kitaura MJ, Kaffer MI, Marcelli MP & Martins SMA (2014) A new hairy Leptogium (Section Mallotium) from Rio Grande do Sul, Brazil. Hoehnea 41: 303-306.

[21] Lücking R, Hodkinson BP & Leavitt SD (2017) The 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota - Approaching one thousand genera. The Bryologist 119: 361-416.

[22] Marcelli MP (1992) Ecologia liquênica nos manguezais do sul-sudeste brasileiro. Bibliotheca Lichenologica 47: 1-310.

[23] Moncada B, Lücking R. & Suárez A (2014) Molecular phylogeny of the genus Sticta (lichenized Ascomycota: Lobariaceae) in Colombia. Fungal Diversity 64: 205-231.

[24] Müller Argoviensis J (1891) Lichenes Schenckiane a cl. Dr. H. Schenck, Bonnensi, in Brasiliae orientalis prov. Santa Catharina, Paraná, Rio de Janeiro, Minas Geraes et Pernambuco lecti. Hedwigia 30: 219-234.

[25] Müller Argoviensis J (1895) Lichenes exotici, III. Hedwigia 34: 27-38.

[26] Nash TH (2008) Lichen biology. 2ª ed. Cambridge University Press, Cambridge 486p.

[27] Orange A, James PW & White FJ (2001) Microchemical Methods for the Identification of Lichens. British Lichen Society, London. 101p.

[28] Orange A, Hawksworth DL, McCarthy PM & Fletcher A (2009) Verrucaria. In: Smith CW, Aptroot A, Coppins BJ, Flechter A, Gilbert OL, James PW & Wolseley PA (eds.) The lichens of Great Britain and Ireland, 2^nd ed. British Lichen Society, London. Pp. 931-957.

[29] Osorio HS (1975) Contribution to the lichen flora of Uruguay. VIII. Additions and corrections. Comunicaciones Botánicas del Museo de Historia Natural de Montevideo 4: 1-12.

[30] Osorio HS (1977) Contribution to the lichen flora of Brazil II. Lichens from Guarapuava, Paraná state. Dusenia 10: 101-102.

[31] Osorio HS (1997) Contribution to the lichen flora of Brazil. XXXIV. Lichens from Laguna, Santa Catarina state. Comunicaciones Botánicas del Museo de Historia Natural de Montevideo 6: 1-4.

[32] Osorio HS & Homrich M (1978) Contribution to the lichen flora of Brazil IV. Lichens from southern Rio Grande do Sul. The Bryologist 81: 452-454.

[33] Rikkinen J (2003) Ecological and evolutionary role of photobiont-mediated guilds in lichens. Symbiosis 34: 99-110.

[34] Schultz M & Büdel B (2002) Key to the genera of the Lichinaceae. Lichenologist 34: 39-62.

[35] Spielmann AA (2006) Checklist of lichens and lichenicolous fungi of Rio Grande do Sul (Brazil). Caderno de Pesquisa Série Biologia 18: 7-125.

[36] Spielmann AA, Osorio HS & Marcelli MP. (2007) Jenmania osorioi is added to the flora of Brazil. Comunicaciones Botánicas, Museo de Historia Natural y Anthroplogía [Montevideo] 6(134): 1-3.

[37] 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.

[38] Vitikainen O (1998) Taxonomic notes on Neotropical species of Peltigera. In: Marcelli MP & Seaward MRD (eds). Lichenology in Latin America: history, current knowledge and applications. CETESB, São Paulo. Pp. 135-139.

Ephebe brasiliensis (Ascomycota, Lichinaceae): an overlooked freshwater lichenized fungus