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The disjunct distribution of Cladonia dimorphoclada Robbins (Ascomycota: Cladoniaceae): first record in South America

Distribuição disjunta de Cladonia dimorphoclada Robbins (Ascomycota: Cladoniaceae): primeiro registro para a América do Sul

ABSTRACT

Previously known only from the North and Central America, the lichenized fungi Cladonia dimorphoclada Robbins is recorded for the first time in South America. The specimens were found growing on soil, in an open area at 1695 m alt., in Southern Brazil. We present a distribution map, figures, and comments.

Keywords:
Atlantic Forest; biodiversity; fungi; high altitude fields; lichen

RESUMO

Conhecida previamente apenas para América do Norte e Central, o fungo liquenizado Cladonia dimorphoclada Robbins é registrada pela primeira vez para a América do Sul. Os espécimes foram encontrados crescendo sobre solo, em áreas abertas, a 1695 m de altitude no Sul brasileiro. Nós apresentamos um mapa de distribuição, figuras e comentários.

Palavras-chave:
Biodiversidade; campos de altitude; Floresta Atlântica; fungo; líquen

Introduction

Cladonia P. Browne is one of the most frequently collected lichenized fungi, even by non-lichenologists, and thus reports about the genus have been abundant in recent literature for systematic studies (e.g.Pino-Bodas et al. 2010Pino-Bodas, R., Burgaz, A.R. & Martín, M.P. 2010. Elucidating the taxonomic rank of Cladonia subulata versus C. rei (Cladoniaceae). Mycotaxon 113: 311-326., 2011Pino-Bodas, R., Burgaz, A.R. & Martín, M.P. & Lumbsch, H.T. 2011. Phenotypical plasticity and homoplasy complicate species delimitation in the Cladonia gracilis group (Cladoniaceae, Ascomycota). Organisms, Diversity and Evolution 11: 343-355., 2012Pino-Bodas, R., Burgaz, A.R. & Martín, M.P. & Lumbsch, H.T. 2012. Species delimitations in the Cladonia cariosa group (Cladoniaceae, Ascomycota). The Lichenologist 44: 121-135., Gumboski et al. 2013Gumboski, E.L., Beilke, F. & Eliasaro, S. 2013. Cladonia dunensis sp. nov. from southern Brazil, with notes on the genus in beach dune environments. Mycotaxon 124: 333-340.. Ahti & Sipman 2013Ahti, T. & Sipman, H.J.M. 2013. Ten new species of Cladonia (Cladoniaceae, Lichenized Fungi) from the Guianas and Venezuela, South America. Phytotaxa 93: 25-39., Yanez-Ayabaca et al. 2013Yánez-Ayabaca, A., Ahti, T. & Bungartz, F. 2013. The family Cladoniaceae (Lecanorales) in the Galapagos Islands. Phytotaxa 129: 1-33), and new distribution records of various species (e.g. Burgaz & Ahti 2009Burgaz, A.R. & Ahti, T. 2009. Cladoniaceae. Flora Liquenológica Ibérica. v. 4. Sociedad Espanola de Liquenología, Madrid., Ahti & Stenroos 2012Ahti, T. & Stenroos, S. 2012. New data on nomenclature, taxonomy and distribution of some species of the lichen genus Cladonia. Botanica Complutensis 36: 31-34., Burgaz & Pino-Bodas 2012Burgaz, A.R. & Pino-Bodas, R. 2012. Notes on species of the genus Cladonia from Bosnia-Herzegovina and Croatia. Botanica Complutensis 36: 13-18., Flakus et al. 2012Flakus, A., Etayo, J., Schiefelbein, U.L.F., Ahti, T., Jablónska, A., Oset, M., Bach, K., Flakus, P.R. & Kukwa, M. 2012. Contribution to the knowledge of the lichen biota of Bolivia. 4. Polish Botanical Journal 57: 427-461., Charnei & Eliasaro 2013Charnei, A.M. & Eliasaro, S. 2013. Verticillate Cladonia species (Lichenized Ascomycota) from high-altitude environments of Serra do Mar in Southern Brazil. Hoehnea 40: 87-97., Yanez-Ayabaca et al. 2013Yánez-Ayabaca, A., Ahti, T. & Bungartz, F. 2013. The family Cladoniaceae (Lecanorales) in the Galapagos Islands. Phytotaxa 129: 1-33).

Approximately 115 species of Cladonia are known from Brazil (e.g. Vainio 1887Vainio, E.A. 1887. Monographia Cladoniarum universalis. I. Acta Societatis pro Fauna et Flora Fennica 4: 1-509., 1894Vainio, E.A. 1894. Monographia Cladoniarum universalis. II. Acta Societatis pro Fauna et Flora Fennica 10: 1-498., Ahti et al. 1992, Fleig et al. 1995Fleig M., Ahti, T. & Stenroos, S. 1995. A família Cladoniaceae (liquens) no Rio Grande do Sul, Brasil. Napaea 11: 1-29., Ahti & Marcelli 1995Ahti, T. & Marcelli., M.P. 1995. Taxonomy of the Cladonia verticillaris complex in South America. In: E.E. Farkas, R. Lücking & V Wirth (eds.). Scripta Lichenologica -Lichenological Papers Dedicated to Antonín Vezda. Bibliotheca Lichenologica, pp. 5-26., Ahti 2000Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx.,Stenroos et al. 2002Stenroos, S., Hyvonen, J., Myllys, L., Thell, A. & Ahti, T. 2002. Phylogeny of the genus Cladonia s.lat. (Cladoniaceae, Ascomycetes) inferred from molecular, morphological, and chemical data. Cladistics 18: 237-278., Gumboski & Eliasaro 2011Gumboski, E.L. & Eliasaro, S. 2011. Cladonia litoralis (Cladoniaceae), a new species from southern Brazil. The Bryologist 114: 665-667., Gumboski et al. 2013Gumboski, E.L. & Eliasaro, S. 2011. Cladonia litoralis (Cladoniaceae), a new species from southern Brazil. The Bryologist 114: 665-667.) and distributed in various environments. However, the lichenized mycota in many Brazilian regions remain poorly studied, in terms of inventories and ecology.

Previously, Cladonia dimorphoclada was only known from the Eastern United States (e.g.Ahti 1973Ahti, T. 1973. Taxonomic notes on some species of Cladonia, subsect. Unciales. Annales Botanici Fennici 10: i63-184., Flenniken 1999Flenniken, D.G. 1999. The macrolichens in West Virginia: a regional manual of over 275 species illustrated in color. Publ. by the Author, Wooster, Ohio., Hansen & Freeman 2003Hansen, C.J. & Freeman, J.D. 2003. A catalog and brief history of the lichen flora of Alabama. Evansia 2G: 59-1G1., Thomson 2003Thomson, J.W. 2003. Lichens of Wisconsin. Universidade de Wisconsin, Madison., Harris 2004Harris, R.C. 2004. A preliminary list of the lichens of New York. Opuscula Philolichenum 1: 55-74.), and also rarely found in southern Mexico, and western Cuba (Ahti 2000Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx.). In this paper, we report the occurrence of C. dimorphoclada for the first time in South America, more precisely from the Southern region of Brazil.

Material and methods

Specimens were examined using standard techniques, stereomicroscope, and light microscope. Sections of the thallus and apothecia were mounted in water. Chemical analyses were done according to Huneck & Yoshimura (1996)Huneck, S. & Yoshimura, I. 1996. Identification of Lichen Substances. Springer-Verlag, Berlin, Heidelberg. and Orange etal. (2001)Orange, A., James, P.W. & White, F.J. 2001. Microchemical Methods for the Identification of Lichens. British Lichen Society, London.. The distribution map (figure 1) was produced in QGIS Software 2.0.1, according to a tutorial developed by Calegari et al. (2016)Calegari, B.B., Delapieve, M.L. & Sousa, L.M. 2016. Tutorial para preparação de mapas de distribuição geográfica. Boletim, Sociedade Brasileira de Ictiologia 118: 15-30..

Figure 1
Distribution map of Cladonia dimorphoclada. Green circles: previous records. Red star: new record.

Results and Discussion

Cladonia dimorphoclada Robbins in Sandstede, Cladon. Exs. 1882. 1929.

Figure 2

Description. Primary thallus not seen. Podetia 1.0-5.0 cm tall, 0.4-2.0 mm thick, pale yellowish green, somewhat branched, branching type irregular, anisotomic dichotomy and trichotomy, often with many short outgrowths; axils closed; apices slightly acute, rather slender, erect; not melanotic at base; surface slightly shiny, dull at the base, pruinose near tips, smooth to slightly rough, areolate but not cracked. Podetial wall 130-250 μm thick, cortex rudimentary, 7-12(-25) μm thick, medulla intermixed with irregular bundles of stereome, medulla 110-240 μm thick, bundles of stereome 65-100 μm in diam., inner surface rough to slightly arachnoid. Conidiomata not seen. Hymenial disks apical, immature.

Figure 2
Cladonia dimorphoclada found in Southern Brazil. a. Podetia (JOI). b. Anatomical section of a podetial showing the stereome intermixed with medulla. c. Detail of an anatomical section showing the rudimentary cortex (black arrow). Scale bar: a = 1 cm; b,c = 200 μm.

Chemistry. Spot tests: K-, C-, KC- or KC+ yellow, P-, UV-. TLC and NMR: Usnic acid only.

Distribution and ecology: according to Ahti (2000)Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx., in the United States Cladonia dimorphoclada occurs mainly on sandy soils, in Mexico on sandstone rocks, and in Cuba on the coastal white sand. In Brazil, specimens were found growing on top of a rocky outcrop in an open field (figure 3).

Figure 3
Habitat where Cladonia dimorphoclada was found in Southern Brazil, Municipality of Urubici, São Joaquim National Park.

Cladonia dimorphoclada can be differentiated from other Brazilian Cladoniae by the few branched thalli with closed axils, the presence of a rudimentary cortex and stereome intermixed with medulla, and the production of usnic acid as the only secondary compound.

Species with similar morphology and chemistry are Cladonia substellata Vain., C. spinea Ahti, C. uncialis (L.) Weber ex F.H. Wigg. and C. vareschi Ahti. However, C. substellata has moderately to very branched podetia with pale gray necrotic base (Vainio 1887Vainio, E.A. 1887. Monographia Cladoniarum universalis. I. Acta Societatis pro Fauna et Flora Fennica 4: 1-509., Ahti 2000Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx.); C. spinea form densely branched cushions and present six chemotypes where only usnic acid is constant (Ahti 2000Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx.); C. uncialis has a richly branched podetia with a well-developed cortex (Ahti 2000Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx., Burgaz & Ahti 2009Burgaz, A.R. & Ahti, T. 2009. Cladoniaceae. Flora Liquenológica Ibérica. v. 4. Sociedad Espanola de Liquenología, Madrid.); and C. vareschi has moderately branched podetia with a slender cortex and well-delimited stereome (Ahti 1986Ahti, T. 1986. New species and nomenclatural combinations in the lichen genus Cladonia. Annales Botanici Fennici 23: 205-220., 2000Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx.).

Cladonia apodocarpa Robbins and C. robbinsii A. Evans also present disjunct distribution between North America and temperate South America (Ahti 2000Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx.), somewhat like C. dimorphoclada. Cladonia apodocarpa was recorded in North America (e.g.Evans 1947Evans, A.W. 1947. The Cladoniae of Vermont. The Bryologist 50: 221-246., Harris 2004Harris, R.C. 2004. A preliminary list of the lichens of New York. Opuscula Philolichenum 1: 55-74.) and Uruguay (Ahti 2000Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx.), and C. robbinsii was recorded in North America (e.g. Flenniken 1999Flenniken, D.G. 1999. The macrolichens in West Virginia: a regional manual of over 275 species illustrated in color. Publ. by the Author, Wooster, Ohio., Thomson 2003Thomson, J.W. 2003. Lichens of Wisconsin. Universidade de Wisconsin, Madison., Harris 2004Harris, R.C. 2004. A preliminary list of the lichens of New York. Opuscula Philolichenum 1: 55-74.) and South America, in Chile (Galloway & Quilhot 1998Galloway, D.J. & Quilhot, W. 1998. Checklist of Chilean lichen-forming and lichenicolous fungi. Gayana Botanica 55: 111-185., Ahti 2000Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx.), Uruguay and Southern Brazil (Fleig et al. 1995Fleig M., Ahti, T. & Stenroos, S. 1995. A família Cladoniaceae (liquens) no Rio Grande do Sul, Brasil. Napaea 11: 1-29., Ahti 2000Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx.).

Material examined: BRAZIL. Santa Catarina: Municipality of Urubici, Parque Nacional de São Joaquim, Campo de Santa Bárbara, in exposed site, rocky outcrop, near an old cemetery, 1695 m alt., 1-II-2012, leg. A.A. Spielmann & L.S. Canêz 9978 (CGMS, JOI).

Acknowledgements

We are grateful to Dr. Teuvo Ahti (Finland) for valuable discussions with the first author about the species identity. We also thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico -CNPq (Process 478705/2010-7) for funding the field trips and sampling for L.S. Canêz and A.A. Spielmann.

Literature cited

  • Ahti, T. 1973. Taxonomic notes on some species of Cladonia, subsect. Unciales Annales Botanici Fennici 10: i63-184.
  • Ahti, T. 1986. New species and nomenclatural combinations in the lichen genus Cladonia Annales Botanici Fennici 23: 205-220.
  • Ahti, T. 2000. Cladoniaceae. Flora Neotropica 78. Organization for Flora Neotropica and New York Botanical Garden, Bronx.
  • Ahti, T. & Marcelli., M.P. 1995. Taxonomy of the Cladonia verticillaris complex in South America. In: E.E. Farkas, R. Lücking & V Wirth (eds.). Scripta Lichenologica -Lichenological Papers Dedicated to Antonín Vezda. Bibliotheca Lichenologica, pp. 5-26.
  • Ahti, T. & Stenroos, S. 2012. New data on nomenclature, taxonomy and distribution of some species of the lichen genus Cladonia Botanica Complutensis 36: 31-34.
  • Ahti, T. & Sipman, H.J.M. 2013. Ten new species of Cladonia (Cladoniaceae, Lichenized Fungi) from the Guianas and Venezuela, South America. Phytotaxa 93: 25-39.
  • Ahti, T., Stenroos, S. & Xavier-Filho, L. 1993. The lichen family Cladoniaceae in Paraiba, Pernambuco and Sergipe, Northeast Brazil. Tropical Bryology 7: 55-70.
  • Burgaz, A.R. & Ahti, T. 2009. Cladoniaceae. Flora Liquenológica Ibérica. v. 4. Sociedad Espanola de Liquenología, Madrid.
  • Burgaz, A.R. & Pino-Bodas, R. 2012. Notes on species of the genus Cladonia from Bosnia-Herzegovina and Croatia. Botanica Complutensis 36: 13-18.
  • Calegari, B.B., Delapieve, M.L. & Sousa, L.M. 2016. Tutorial para preparação de mapas de distribuição geográfica. Boletim, Sociedade Brasileira de Ictiologia 118: 15-30.
  • Charnei, A.M. & Eliasaro, S. 2013. Verticillate Cladonia species (Lichenized Ascomycota) from high-altitude environments of Serra do Mar in Southern Brazil. Hoehnea 40: 87-97.
  • Evans, A.W. 1947. The Cladoniae of Vermont. The Bryologist 50: 221-246.
  • Flakus, A., Etayo, J., Schiefelbein, U.L.F., Ahti, T., Jablónska, A., Oset, M., Bach, K., Flakus, P.R. & Kukwa, M. 2012. Contribution to the knowledge of the lichen biota of Bolivia. 4. Polish Botanical Journal 57: 427-461.
  • Fleig M., Ahti, T. & Stenroos, S. 1995. A família Cladoniaceae (liquens) no Rio Grande do Sul, Brasil. Napaea 11: 1-29.
  • Flenniken, D.G. 1999. The macrolichens in West Virginia: a regional manual of over 275 species illustrated in color. Publ. by the Author, Wooster, Ohio.
  • Galloway, D.J. & Quilhot, W. 1998. Checklist of Chilean lichen-forming and lichenicolous fungi. Gayana Botanica 55: 111-185.
  • Gumboski, E.L. & Eliasaro, S. 2011. Cladonia litoralis (Cladoniaceae), a new species from southern Brazil. The Bryologist 114: 665-667.
  • Gumboski, E.L., Beilke, F. & Eliasaro, S. 2013. Cladonia dunensis sp. nov. from southern Brazil, with notes on the genus in beach dune environments. Mycotaxon 124: 333-340.
  • Hansen, C.J. & Freeman, J.D. 2003. A catalog and brief history of the lichen flora of Alabama. Evansia 2G: 59-1G1.
  • Harris, R.C. 2004. A preliminary list of the lichens of New York. Opuscula Philolichenum 1: 55-74.
  • Huneck, S. & Yoshimura, I. 1996. Identification of Lichen Substances. Springer-Verlag, Berlin, Heidelberg.
  • Orange, A., James, P.W. & White, F.J. 2001. Microchemical Methods for the Identification of Lichens. British Lichen Society, London.
  • Pino-Bodas, R., Burgaz, A.R. & Martín, M.P. 2010. Elucidating the taxonomic rank of Cladonia subulata versus C. rei (Cladoniaceae). Mycotaxon 113: 311-326.
  • Pino-Bodas, R., Burgaz, A.R. & Martín, M.P. & Lumbsch, H.T. 2011. Phenotypical plasticity and homoplasy complicate species delimitation in the Cladonia gracilis group (Cladoniaceae, Ascomycota). Organisms, Diversity and Evolution 11: 343-355.
  • Pino-Bodas, R., Burgaz, A.R. & Martín, M.P. & Lumbsch, H.T. 2012. Species delimitations in the Cladonia cariosa group (Cladoniaceae, Ascomycota). The Lichenologist 44: 121-135.
  • Stenroos, S., Hyvonen, J., Myllys, L., Thell, A. & Ahti, T. 2002. Phylogeny of the genus Cladonia s.lat. (Cladoniaceae, Ascomycetes) inferred from molecular, morphological, and chemical data. Cladistics 18: 237-278.
  • Thomson, J.W. 2003. Lichens of Wisconsin. Universidade de Wisconsin, Madison.
  • Vainio, E.A. 1887. Monographia Cladoniarum universalis. I. Acta Societatis pro Fauna et Flora Fennica 4: 1-509.
  • Vainio, E.A. 1894. Monographia Cladoniarum universalis. II. Acta Societatis pro Fauna et Flora Fennica 10: 1-498.
  • Yánez-Ayabaca, A., Ahti, T. & Bungartz, F. 2013. The family Cladoniaceae (Lecanorales) in the Galapagos Islands. Phytotaxa 129: 1-33

Publication Dates

  • Publication in this collection
    Oct-Dec 2018

History

  • Received
    04 Apr 2018
  • Accepted
    08 Aug 2018
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