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Article • Hoehnea 47 • 2020 • https://doi.org/10.1590/2236-8906-61/2020   copy

Bryophytes of the Parque Estadual da Serra do Brigadeiro, an Atlantic Forest Remnant in Southeastern Brazil1 1 Part of the Masters’ Dissertation of the first Author

Briófitas do Parque Estadual da Serra do Brigadeiro, um remanescente de Mata Atlântica no Sudeste do Brasil

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

The objective was to present the floristic survey of the bryophytes of the Parque Estadual da Serra do Brigadeiro. It included an evaluation of the species richness, as well as information about the substrate preference of each species and its geographic distributions in Brazil. We found 208 taxa of bryophytes: one hornwort, 88 liverworts and 119 mosses. This richness represents ca. 26% of the bryoflora of Minas Gerais State and ca. 13% of that known for Brazil. Eighteen of the bryophytes species are endemic to Brazil, whereas 19 species are recorded for the first time in Minas Gerais. The bryoflora showed preference for tree bark (30%) and rock (23%) as substrates. Our data show that the Parque Estadual da Serra do Brigadeiro is an important area for the diversity conservation of Brazilian bryophytes and maintenance of endemic species of the country.

Keywords:
conservation; liverworts; Minas Gerais State; mosses; substrate

RESUMO

O objetivo foi apresentar o levantamento florístico das briófitas do Parque Estadual da Serra do Brigadeiro, incluindo uma avaliação da riqueza de espécies, bem como informações sobre a preferência de substrato de cada espécie e suas distribuições geográficas no Brasil. Encontramos 208 táxons de briófitas: um antócero, 88 hepáticas e 119 musgos. Essa riqueza representa 26% da brioflora do Estado de Minas Gerais e 13% do Brasil. Dezoito das espécies de briófitas são endêmicas do Brasil, enquanto 19 espécies são registradas pela primeira vez em Minas Gerais. A brioflora mostrou preferência pelo substrato casca de árvore (30%) e rocha (23%). Os dados obtidos mostram que o Parque Estadual da Serra do Brigadeiro é uma área importante para a conservação da diversidade de briófitas brasileiras e para a manutenção de espécies endêmicas do país.

Palavras-chaves:
conservação; hepáticas; Estado de Minas Gerais; musgos; substrato

Introduction

Bryophytes are nonvascular plants characterized by a life cycle featuring alternating haploid and diploid generations, with the gametophyte as the main life form, which helps and feeds the unbranched, unisporangiate sporophyte (Vanderpoorter & Goffinet 2009Vanderpoorter, A. & Goffinet, B. 2009. Introduction to Bryophytes. Cambridge University Press, New York, pp. 6-329.). The monophyly of the three bryophyte groups and the Setaphyta clade of liverworts and mosses as the sister to Traqueophyta has been supported (Puttick et al. 2018Puttick, M.N., Morris, J.L., Williams, Cox, C.J., Edwards D., Kenrick, P., Pressel, S., Wellman, C.H., T.A., Schneider, H., Pisani, D. & Donoghue, D.P. 2018. The interrelationships of land Plants and the nature of the ancestral Embryophyte. Current Biology 28: 733-745.), contrary to the view of three lineages of bryophytes like a paraphyletic group (Goffinet & Shaw 2009Goffinet, B., Buck, W. & Shaw, A. 2009. Morphology, anatomy and classification of the Bryophyta. In: B Goffinet& J. Shaw (eds.). Bryophyte Biology, 2 ed. Cambdrige University Press, Cambdrige, pp. 56-138. ) and hornworts as the sister to vascular plants (Qiu et al. 2006Qiu, Y.L., Li, L., Wang, B., Chen, Z., Knoop, V., Groth-Malonek, M., Dombrovska, O., Lee, J., Kent, L., Rest, J., Estabrook, G.F., Hendry, T.A., Taylor, D.W., Testa, CH.M., Ambros, M., Crandall-Stotler, B., Duff, R.J., Stech, M., Frey,W., Quandt, D. & Davis, CH.C. 2006. The deepest divergences in land plants inferred from phylogenomic evidence. Proceedings of the National Academy of Sciences 103 (42): 15511-15516.).

These three groups are represented by ca. 18, 000 species worldwide (Goffinet & Shaw 2009Goffinet, B., Buck, W. & Shaw, A. 2009. Morphology, anatomy and classification of the Bryophyta. In: B Goffinet& J. Shaw (eds.). Bryophyte Biology, 2 ed. Cambdrige University Press, Cambdrige, pp. 56-138. ). In Brazil, 1,578 taxa have been recorded (Flora do Brasil 2020, 2020), and the country has the highest rate of endemism (22%) (Flora do Brasil 2020, 2020Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. Available in http://floradobrasil.jbrj.gov.br/ (accessed on 15-VII-2020).
http://floradobrasil.jbrj.gov.br/... ).

Bryophyte representativeness is especially high in the Atlantic forest, which harbors 87% of all taxa recorded for the country (Flora do Brasil 2020, 2020Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. Available in http://floradobrasil.jbrj.gov.br/ (accessed on 15-VII-2020).
http://floradobrasil.jbrj.gov.br/... ). This biome is recognized as a biodiversity hotspot with a high percentage of endemic species (Myers et al. 2000Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B. & Kent, J. 2000. Biodiversity hotspots for conservation priorities. Nature, 403: 853-858., Stehmann et al. 2009Stehmann, J.R., Forzza, R.C., Salino, A., Sobral, M., Costa, D.P. & Kamino, L. 2009. Plantas da Floresta Atlântica. Jardim Botânico do Rio de Janeiro, Rio de Janeiro , pp. 3-501.), including mosses and liverworts. Unfortunately, it is under intensive process of deforestation and destruction, and only ca. 28% of the native vegetation cover persists as isolated fragments in different stages of succession, with only 30% of the total vegetation cover found in protected areas, 9% of them are strictly protected and 21% of sustainable use (Rezende et al. 2018Rezende, C.L., Scarano, F.R., Assad, E.D., Joly, C.A., Metzger, J.P., Strassburg, B.B.N., Tabarelli, M., Fonseca, G.A. & Mittermeier, R.A. 2018. From hotspot to hopespot: An opportunity for the Brazilian Atlantic Forest. Perspectives in Ecology and Conservation 16 (4): 208-214.). Consequently, this bryoflora could be seriously threatened and many species could disappear without being known to science.

Several floristic surveys of bryophytes in Minas Gerais State were done in the Atlantic Forest, such as Parque Estadual de Ibitipoca (Luizi-Ponzo et al. 2013Luizi-Ponzo, A., Siviero, T., Amorim, E., Henriques, D., Rocha, L., Gomes, H., Paiva, L., Rodrigues, R., Silva, I., Silva, A., Ribeiro, G., Gomes, C. & Campeão, A. 2013. Briófitas do Parque Estadual do Ibitipoca no Herbário Prof. Leopoldo Kriegeer. In: R. Forzza, L. Neto, F.R. Salimena & D. Zappi (Org.). Flora do Parque Estadual de Ibitipoca e seu entorno, 1ed Editora UFJF, Juiz de Fora, pp. 95-122., Yano & Luizi-Ponzo 2014Yano, O. & Luizi-Ponzo, A.P. 2014. Adições à Brioflora do Parque Estadual do Ibitipoca, Minas Gerais, Brasil. Revista de Biologia Neotropical 11(2): 71-96., Siviero & Luizi-Ponzo 2015Siviero, T.S. & Luizi-Ponzo, A.P. 2015. Briófitas de diferentes fitofisionomias florestais e campestres: estudo em uma área de conservação no sudeste do Brasil-Parque Estadual do Ibitipoca. Pesquisas, Botânica 67: 101-117.), Serra Negra (Amorin et al. 2017Amorim, E.T., Carvalho, F.A., Santos, N.D. & Luizi-Ponzo, A. 2017. Distribution of Bryophytes in South-Eastern Brazil: An Approach on Floristic Similarity and Environmental Filtering. Cryptogamie Bryologie, 38: 3-17.), and Parque Nacional da Serra do Cipó (Yano & Peralta 2011aYano, O. & Peralta, D.F. 2011a. Flora da Serra do Cipó, Minas Gerais: Briófitas (Anthocerotophyta, Bryophyta e Marchantiophyta). Boletim de Botânica da Universidade de São Paulo 29: 135-211., Sousa & Câmara 2015Sousa, R.V. & Câmara, P.E.A.S. 2015. Survey of the bryophytes of a gallery forest in the National Park of Serra do Cipó, Minas Gerais, Brazil. Acta Botânica Brasílica 29: 24-29.). However, due the great size of the state, there are still large gaps in the knowledge of the brioflora of Minas Gerais State (Amorin 2013Amorin E.T. 2013. Estudo florístico e ecológico das briófitas da Serra Negra (Minas Gerais) e sua relação com outras áreas do sudeste do Brasil. Dissertação de Mestrado, Universidade Federal de Juiz de Fora, Juiz de Fora.).

The Parque Estadual da Serra do Brigadeiro (PESB) is located in one of the areas of the Atlantic Forest that still comprises large tracts of continuous forest (Plano de Manejo PESB- Parque Estadual da Serra do Brigadeiro 2007Plano de Manejo PESB - Parque Estadual da Serra do Brigadeiro. 2007. Governo do Estado de Minas Gerais. Secretaria de Estado de Meio Ambiente e Desenvolvimento Sustentável - SEMAD, pp. 1-89.). The Park has a variety of geographical, climatic and phytophysiological conditions, and, consequently, it harbors a high quality and quantity of microhabitats, with variation in the availability of nutrients (Benites et al. 2001Benites, V.M, Schaefer, C.E.G.R., Mendonça, E.S. & Martin, N.L. 2001. Caracterização da matéria orgânica e micromorfologia de solos sob Campos de Altitude no Parque Estadual da Serra do Brigadeiro (MG). Revista Brasileira de Ciência do Solo 25: 661- 674.), a key factor in the diversity patterns of bryophytes (Pócs 1982Pócs, T. 1982. Tropical Forest Bryophytes. In: A.J.E., Smith (ed.). Bryophyte Ecology. Chapman and Hall, London, New York, pp. 59-103. , Newmaster et al. 2005Newmaster, S.G., Belland, R.J., Arsenault, A., Vitt, D.H. & Stephens, T.R. 2005. The ones we left behind: Comparing plot sampling and floristic habitat sampling for estimating bryophyte diversity: estimating bryophyte diversity. Diversity and Distributions 11: 57-72.). For these reasons, the PESB harbors a diverse community of bryophytes with high numbers of endemic species, many of which have not been previously recorded for the state of Minas Gerais.

Despite its relevance, the bryoflora of the PESB is still poorly known. There are only three papers citing bryophytes collected in the PESB: Crum (1994)Crum, H. 1994. Sphagnum leonii. A new species from Minas Gerais. Pabstia 5: 1-5., describing a new species, Sphagnum leonii, Leoni & Tinte (2004)Leoni, L.S. & Tinte, V.A. 2004. Flora do Parque Estadual da Serra do Brigadeiro, Minas Gerais, Brasil: caracterização da vegetação e lista preliminar das espécies. Carangola, MG, Brasil: Faculdade de Filosofia, Ciências e Letras de Carangola, pp. 21-24. listing 52 species that occur in the area, and Castro et al. (2011)Castro, T.A., Leoni, L.S. & Rocha, M.J. 2011. Briófitas do Herbário “Guido Pabst”- GFJP, Carangola - MG. In: XIII Encontro Latino Americano de Iniciação Científica e IX Encontro Latino Americano de Pós-Graduação - Universidade do Vale do Paraíba, pp. 1-6. listing the herbarium specimens.

In this paper, we present a detailed floristic survey of the bryophytes of the PESB, including an assessment of species richness, as well as information on substrate preference of each species, and its geographical distributions at the national level according to Flora do Brasil 2020 (2020)Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. Available in http://floradobrasil.jbrj.gov.br/ (accessed on 15-VII-2020).
http://floradobrasil.jbrj.gov.br/... .

Materials and methods

Study site - The Parque Estadual da Serra do Brigadeiro (PESB) is a protected area under state administration, located among the municipalities of Ervália, Fervedouro, Sericita, Araponga, Miradouro, Pedra Bonita, Muriaé and Divino, in the State Minas Gerais, Brazil. The Park covers an area of 14,985 ha between the geographical coordinates 20º33' to 21º00'S and 42º40' to 40º20'W (figure 1, map was generated using ArcGIS® software). The vegetation in the Park is composed of secondary fragments inserted in the area of Atlantic Forest biome (Caiafa & Silva 2005Caiafa, A. & Silva, A. 2005. Composição florística e espectro biológico de um campo de altitude no Parque Estadual da Serra do Brigadeiro, Minas Gerais - Brasil. Rodriguésia 56: 163-173.) and has two types of vegetal formations, according with IBGE (2012)IBGE (Instituto Brasileiro de Geografia e Estatística). 2012. Manual técnico da vegetação brasileira. Rio de Janeiro.: (1) semideciduous forest from the altomontana formation and (2) high-altitude fields (campos de altitude).

Figure 1
Location of Atlantic Forest domain in Brazil and sampling areas for bryophytes in the Parque Estadual da Serra do Brigadeiro in Minas Gerais State, Brazil. 1. Trilha do Laje do Ouro. 2. Trilha do Carvão. 3. Trilha do Pico do Grama. 4. Trilha da Lajinha. 5. Trilha da Pedra do Pato. 6. Trilha do Cruzeiro do Careço. 7. Trilha do Itajurú. 8. Trilha do Avião.

Floristic surveys - Specimens were collected during four field expeditions between May 2017 and April 2018, along eight preexistent trails located in the northern, central and southern areas of the Park (approximate coordinates plotted in figure 1). Collecting effort was intended to cover the range of habitats and microhabitats (substrate type) available for bryophytes, like soil, trunks, lianas, shrubs, rocks, in both semideciduous forest and high-altitude fields, between 1000 to 1540 m of elevation, following Frahm’s recommendations (2003)Frahm, J.P. 2003. Manual of tropical bryology. Tropical Bryology 23: 1-196. . Specimens were deposited at VIC herbarium, with duplicates in SP (Acronyms follow Index Herbariorum, Thiers, 2020Thiers, B. 2020. Index Herbariorum: A Global Directory of Public Herbaria and Associated Staff. New York Botanical Garden’s Virtual Herbarium (http://sweetgum.nybg.org/science/ih/)
http://sweetgum.nybg.org/science/ih/... ).

Bryophyte identification - For the specimen identification we used keys and specialized literature for to each family (Yano & Peralta 2011aYano, O. & Peralta, D.F. 2011b. Bryophytes from Serra de São José, Tiradentes, Minas Gerais, Brasil. Boletim de Botânica da Universidade de São Paulo 21: 141-172., Frahm 1991Frahm, J.P. 1991. Dicranaceae: Campylopodioideae, Paraleucobryoideae. Flora Neotropica, Monograph 54: 1-237., Sharp et al. 1994Sharp, A.J., Crum, H. & Eckel, P. 1994. The Moss flora of Mexico. Memoirs of the New York Botanical Garden 69: 1-1113. , Yano & Carvalho 1995Yano, O. & Carvalho, A. 1995. Briófitas da Serra da Piedade, Minas Gerais, Brasil. In: Anais do IX Congresso da Sociedade Botânica de São Paulo, pp. 15-25., Gradstein, Churchill, et al. 2001Gradstein, S.R., Griffin, III D., Morales, M. & Nadkarni, N. 2001b. Diversity and habitat differentiation of mosses and liverworts in the cloud forest of Monteverde, Costa Rica. Caldasia 23: 203-212., Gradstein & Costa 2003Gradstein, S.R. & Costa D.P. 2003. The Hepaticae and Anthocerotae of Brazil. Memoirs of the New York Botanical Garden 87: 1-318., Bordin & Yano 2013Bordin, J. & Yano, O. 2013. Fissidentaceae (Bryophyta) do Brasil. Boletim do Instituto de Botânica 22: 1-72.).

Our classification follows Söderström et al. (2016)Söderström, L., Hagborg, A., Konrat, M., Bartholomew-Began, S., Bell, D., Briscoe, L., Brown, E., Cargill, D.C., Costa, D.P., Crandall-Stotler, B.J., Cooper, E., Dauphin, G., Engel, J., Feldberg, K., Glenny, D., Gradstein, S.R., He, X., Hentschel, J., Ilkiu-Borges, A.L., Katagiri, T., Konstantinova, N.A., Larraín, J., Long, D., Nebel, M., Pócs, T., Puche, F., Reiner-Drehwald, E., Renner, M., Sass-Gyarmati, A., Schäfer-Verwimp, A., Segarra-Moragues, J., Stotler, R.E., Sukkharak, P., Thiers, B., Uribe, J., Váňa, J., Wigginton, M., Zhang, L. & Zhu, R.L. 2016. World checklist of hornworts and liverworts. PhytoKeys 59: 1-828. for Anthocerotophyta and Marchantiophyta and Goffinet et al. (2009)Goffinet, B., Buck, W. & Shaw, A. 2009. Morphology, anatomy and classification of the Bryophyta. In: B Goffinet& J. Shaw (eds.). Bryophyte Biology, 2 ed. Cambdrige University Press, Cambdrige, pp. 56-138. for Bryophyta. The taxa are listed in alphabetical order by families, genera, and species, indicating endemic species and those recorded for the first time for Minas Gerais State. Distribution data was obtained from Flora do Brasil 2020 (2020)Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. Available in http://floradobrasil.jbrj.gov.br/ (accessed on 15-VII-2020).
http://floradobrasil.jbrj.gov.br/... , as well as from Santos et al. (2017)Santos, E.D., Carmo, D. & Peralta, D.F. 2017. Bryophytes of the cloud forest of Pico do Marumbi State Park, Paraná, Brazil. Check List 13: 959-986. , Carmo & Peralta (2016)Carmo, D.M. & Peralta, D.F. 2016. Survey of bryophytes in Serra da Canastra National Park, Minas Gerais, Brazil. Acta Botânica Brasílica 30: 254-265., Costa & Peralta (2015)Costa, D.P., Santos, N.D., Rezende, M.A., Buck, W.R. & Schäfer-Verwimp, A. 2015. Bryoflora of the Itatiaia National Park along an elevation gradient: diversity and conservation. Biodiversity and Conservation 24: 2199-2212., Machado et al. (2015)Machado, P.S., Amorim, E.T., Siviero, T.S., Gomes, H.C.S. & Luizi-Ponzo A.P. 2015. Novas ocorrências de espécies de Anthocerotophyta e Marchantiophyta para o estado de Minas Gerais, Brasil. Pesquisas, Botânica 67: 51-64. , Yano & Luizi-Ponzo (2014)Yano, O. & Luizi-Ponzo, A.P. 2014. Adições à Brioflora do Parque Estadual do Ibitipoca, Minas Gerais, Brasil. Revista de Biologia Neotropical 11(2): 71-96., Yano & Peralta (2011a)Yano, O. & Peralta, D.F. 2011a. Flora da Serra do Cipó, Minas Gerais: Briófitas (Anthocerotophyta, Bryophyta e Marchantiophyta). Boletim de Botânica da Universidade de São Paulo 29: 135-211., and Gradstein & Costa (2003)Gradstein, S.R. & Costa D.P. 2003. The Hepaticae and Anthocerotae of Brazil. Memoirs of the New York Botanical Garden 87: 1-318..

Species classification according to substrate types follows Robbins (1952)Robbins, R.G. 1952. Bryophyte ecology of a dune area in New Zealand. Vegetation Acta Geobotanica 4: 1-31.: (1) corticolous, species that grow on living trunks and branches; (2) epiphyllous, those that grow on leaves; (3) epixylic, on dead or decaying trunk; (4) rupicolous, on stones; and (5) terrestrial, on the ground.

Results

We collected and analyzed 514 specimens, corresponding to 208 species of bryophytes: one hornwort, 88 liverworts (20 families, 41 genera) and 119 mosses (32 families, 63 genera), (table 1). These taxa comprise 208 species, three varieties and one subspecies.

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Table 1
List of bryophytes found in the Parque Estadual da Serra do Brigadeiro, Minas Gerais State, Brazil, with their substrate. Voucher information corresponds to the collecting series of Libia Mayerly Cifuentes (LMC).

The best represented liverworts families were Lejeuneaceae, with 35 species (36%), Plagiochilaceae, with 10 (11%), and Lepidoziaceae, with six (6%), whereas the best represented moss families were Leucobryaceae, with 16 species (13%), Sematophyllaceae, with 12 (10%), and Pilotrichaceae, with nine (7%). The most representative genera in liverworts were Plagiochila and Lejeunea, with 10 species each; in mosses, the most speciose genera were Campylopus, with 10 species, and Fissidens, with nine, (table 1).

Regarding substrate colonization, 70% of the species were found in only one type of substrate: tree bark (63 taxa), rocks (49), soil (20), decayed wood (six), and live leaves (nine). The remaining species were found in two to four types of substrates.

Eighteen of the bryophyte species are endemic to Brazil, including 13 species of mosses and five liverworts, whereas 19 species (10%) are recorded for the first time in the Minas Gerais State (Flora do Brasil 2020 (2020)Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. Available in http://floradobrasil.jbrj.gov.br/ (accessed on 15-VII-2020).
http://floradobrasil.jbrj.gov.br/... , Carmo & Peralta 2016Carmo, D.M. & Peralta, D.F. 2016. Survey of bryophytes in Serra da Canastra National Park, Minas Gerais, Brazil. Acta Botânica Brasílica 30: 254-265., Costa & Peralta 2015Costa, D.P., Santos, N.D., Rezende, M.A., Buck, W.R. & Schäfer-Verwimp, A. 2015. Bryoflora of the Itatiaia National Park along an elevation gradient: diversity and conservation. Biodiversity and Conservation 24: 2199-2212., Machado et al. 2015Machado, P.S., Amorim, E.T., Siviero, T.S., Gomes, H.C.S. & Luizi-Ponzo A.P. 2015. Novas ocorrências de espécies de Anthocerotophyta e Marchantiophyta para o estado de Minas Gerais, Brasil. Pesquisas, Botânica 67: 51-64. , Yano & Luizi-Ponzo 2014Yano, O. & Luizi-Ponzo, A.P. 2014. Adições à Brioflora do Parque Estadual do Ibitipoca, Minas Gerais, Brasil. Revista de Biologia Neotropical 11(2): 71-96., Yano & Peralta 2011aYano, O. & Peralta, D.F. 2011a. Flora da Serra do Cipó, Minas Gerais: Briófitas (Anthocerotophyta, Bryophyta e Marchantiophyta). Boletim de Botânica da Universidade de São Paulo 29: 135-211., Gradstein & Costa 2003Gradstein, S.R. & Costa D.P. 2003. The Hepaticae and Anthocerotae of Brazil. Memoirs of the New York Botanical Garden 87: 1-318.) (table 1).

Discussion

Bryophyte species richness and Brazilian distribution - The high bryophyte species diversity in the mountain ecosystems of the Neotropics has been related to the large variety of microhabitats and conditions of constant humidity that facilitate the co-occurrence of numerous species (Frahm 2003Frahm, J.P. 2003. Manual of tropical bryology. Tropical Bryology 23: 1-196. , Gradstein et al. 2008). The bryophytes found in this survey of the PESB correspond to ca. 26% of the species estimated for the State of Minas Gerais and 13% of those known for Brazil (Flora do Brasil 2020, 2020Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. Available in http://floradobrasil.jbrj.gov.br/ (accessed on 15-VII-2020).
http://floradobrasil.jbrj.gov.br/... ). In our list, we added 189 species to those previously recorded by Leoni & Tinte (2004)Leoni, L.S. & Tinte, V.A. 2004. Flora do Parque Estadual da Serra do Brigadeiro, Minas Gerais, Brasil: caracterização da vegetação e lista preliminar das espécies. Carangola, MG, Brasil: Faculdade de Filosofia, Ciências e Letras de Carangola, pp. 21-24.. The difference in species number is large, and the number of families and genera recorded are different, with 53 families and 105 genera versus 26 families and 40 genera listed in Leoni & Tinte (2004)Leoni, L.S. & Tinte, V.A. 2004. Flora do Parque Estadual da Serra do Brigadeiro, Minas Gerais, Brasil: caracterização da vegetação e lista preliminar das espécies. Carangola, MG, Brasil: Faculdade de Filosofia, Ciências e Letras de Carangola, pp. 21-24.. In their list, these authors included the endemic species Sphagnum leoni, whose type locality is the PESB, and included also six other species that are doubtful records for Brazil.

Our results indicate a high diversity of bryophytes in the PESB. Yano & Peralta (2011a)Yano, O. & Peralta, D.F. 2011b. Bryophytes from Serra de São José, Tiradentes, Minas Gerais, Brasil. Boletim de Botânica da Universidade de São Paulo 21: 141-172. found 237 species in the Parque Estadual da Serra do Cipó, Luizi-Ponzo et al. (2013)Luizi-Ponzo, A., Siviero, T., Amorim, E., Henriques, D., Rocha, L., Gomes, H., Paiva, L., Rodrigues, R., Silva, I., Silva, A., Ribeiro, G., Gomes, C. & Campeão, A. 2013. Briófitas do Parque Estadual do Ibitipoca no Herbário Prof. Leopoldo Kriegeer. In: R. Forzza, L. Neto, F.R. Salimena & D. Zappi (Org.). Flora do Parque Estadual de Ibitipoca e seu entorno, 1ed Editora UFJF, Juiz de Fora, pp. 95-122. found 209 taxa in Parque Estadual de Ibitipoca, Amorim et al. (2017)Amorim, E.T., Carvalho, F.A., Santos, N.D. & Luizi-Ponzo, A. 2017. Distribution of Bryophytes in South-Eastern Brazil: An Approach on Floristic Similarity and Environmental Filtering. Cryptogamie Bryologie, 38: 3-17. recognized 92 species of the Serra Negra, and Carmo & Peralta (2016)Carmo, D.M. & Peralta, D.F. 2016. Survey of bryophytes in Serra da Canastra National Park, Minas Gerais, Brazil. Acta Botânica Brasílica 30: 254-265. recorded 289 species in Parque Nacional da Serra da Canastra.

Mosses presented a greater number of species than liverworts. This fact is common in high mountain ecosystems rather than in lowlands (Gradstein et al. 2001bGradstein, S.R., Griffin, III D., Morales, M. & Nadkarni, N. 2001b. Diversity and habitat differentiation of mosses and liverworts in the cloud forest of Monteverde, Costa Rica. Caldasia 23: 203-212.) and this is consistent with results provided in other studies in high altitude areas (Yano & Peralta 2011aYano, O. & Peralta, D.F. 2011b. Bryophytes from Serra de São José, Tiradentes, Minas Gerais, Brasil. Boletim de Botânica da Universidade de São Paulo 21: 141-172., 2011bYano, O. & Peralta, D.F. 2011b. Bryophytes from Serra de São José, Tiradentes, Minas Gerais, Brasil. Boletim de Botânica da Universidade de São Paulo 21: 141-172., Luizi-Ponzo et al. 2013Luizi-Ponzo, A., Siviero, T., Amorim, E., Henriques, D., Rocha, L., Gomes, H., Paiva, L., Rodrigues, R., Silva, I., Silva, A., Ribeiro, G., Gomes, C. & Campeão, A. 2013. Briófitas do Parque Estadual do Ibitipoca no Herbário Prof. Leopoldo Kriegeer. In: R. Forzza, L. Neto, F.R. Salimena & D. Zappi (Org.). Flora do Parque Estadual de Ibitipoca e seu entorno, 1ed Editora UFJF, Juiz de Fora, pp. 95-122., Carmo & Peralta 2016Carmo, D.M. & Peralta, D.F. 2016. Survey of bryophytes in Serra da Canastra National Park, Minas Gerais, Brazil. Acta Botânica Brasílica 30: 254-265.). The predominance of mosses is explained by Costa et al. (2015)Costa, D.P., Santos, N.D., Rezende, M.A., Buck, W.R. & Schäfer-Verwimp, A. 2015. Bryoflora of the Itatiaia National Park along an elevation gradient: diversity and conservation. Biodiversity and Conservation 24: 2199-2212. as a result of their life forms and the morphology of their gametophyte, which increases the ability to colonize open environments, such as rock outcrops, exposed soils, and banks; these microhabitats are abundant in the PESB, due to the wide altitudinal range of the area.

Lejeuneaceae was the best represented family in terms of species number, with 36% of the species. This comes as no surprise, as Lejeuneaceae is the largest family of liverworts in Brazil and in the tropics (Gradstein et al. 2001bGradstein, S.R., Griffin, III D., Morales, M. & Nadkarni, N. 2001b. Diversity and habitat differentiation of mosses and liverworts in the cloud forest of Monteverde, Costa Rica. Caldasia 23: 203-212., Gradstein & Costa 2003Gradstein, S.R. & Costa D.P. 2003. The Hepaticae and Anthocerotae of Brazil. Memoirs of the New York Botanical Garden 87: 1-318.). Another well-represented family was Leucobryaceae (11%), a group reported by Yano & Peralta (2011a)Yano, O. & Peralta, D.F. 2011b. Bryophytes from Serra de São José, Tiradentes, Minas Gerais, Brasil. Boletim de Botânica da Universidade de São Paulo 21: 141-172., Siviero & Luizi-Ponzo (2015)Siviero, T.S. & Luizi-Ponzo, A.P. 2015. Briófitas de diferentes fitofisionomias florestais e campestres: estudo em uma área de conservação no sudeste do Brasil-Parque Estadual do Ibitipoca. Pesquisas, Botânica 67: 101-117. and Carmo & Peralta (2016)Carmo, D.M. & Peralta, D.F. 2016. Survey of bryophytes in Serra da Canastra National Park, Minas Gerais, Brazil. Acta Botânica Brasílica 30: 254-265. as having the greatest richness in high altitude areas in Minas Gerais State. The predominance of Leucobryaceae has been attributed to the acrocarpous growth habit of their gametophyte. Furthermore, they have hyalocysts cells in the leaves and alar cells at the basal angles of the leaves (Campylopus), which can store large amounts of water and thus can thrive in more exposed areas (Frahm 2003Frahm, J.P. 2003. Manual of tropical bryology. Tropical Bryology 23: 1-196. ), a common habitat in the PESB.

On the other hand, 10% of the species found in the Park are endemic to Brazil (Flora do Brasil 2020 (2020)Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. Available in http://floradobrasil.jbrj.gov.br/ (accessed on 15-VII-2020).
http://floradobrasil.jbrj.gov.br/... , Costa & Peralta 2015Costa, D.P., Santos, N.D., Rezende, M.A., Buck, W.R. & Schäfer-Verwimp, A. 2015. Bryoflora of the Itatiaia National Park along an elevation gradient: diversity and conservation. Biodiversity and Conservation 24: 2199-2212.). Some endemic species in the PESB are Aptychopsis estrellae, Sphagnum gracilescens, Riccardia regnellii, Rhacocarpus inermis var. inermis, Polytrichum angustifolium and Bryum subapiculatum (figure 2) (Flora do Brasil 2020 (2020)Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. Available in http://floradobrasil.jbrj.gov.br/ (accessed on 15-VII-2020).
http://floradobrasil.jbrj.gov.br/... , Costa & Peralta 2015Costa, D.P. & Peralta, D.F. 2015. Bryophytes diversity in Brazil. Rodriguésia 66: 1063-1071., Machado et al. 2015Machado, P.S., Amorim, E.T., Siviero, T.S., Gomes, H.C.S. & Luizi-Ponzo A.P. 2015. Novas ocorrências de espécies de Anthocerotophyta e Marchantiophyta para o estado de Minas Gerais, Brasil. Pesquisas, Botânica 67: 51-64. , Yano & Luizi-Ponzo 2014Yano, O. & Luizi-Ponzo, A.P. 2014. Adições à Brioflora do Parque Estadual do Ibitipoca, Minas Gerais, Brasil. Revista de Biologia Neotropical 11(2): 71-96., Gradstein & Costa 2003Gradstein, S.R. & Costa D.P. 2003. The Hepaticae and Anthocerotae of Brazil. Memoirs of the New York Botanical Garden 87: 1-318.). For that reason, we assume that the PESB offers microhabitats of high quality and quantity, with moisture and nutrients available for these species; these variables have been pointed as determinants of diversity patterns in this group (Pócs 1982Pócs, T. 1982. Tropical Forest Bryophytes. In: A.J.E., Smith (ed.). Bryophyte Ecology. Chapman and Hall, London, New York, pp. 59-103. , Newmaster et al. 2005Newmaster, S.G., Belland, R.J., Arsenault, A., Vitt, D.H. & Stephens, T.R. 2005. The ones we left behind: Comparing plot sampling and floristic habitat sampling for estimating bryophyte diversity: estimating bryophyte diversity. Diversity and Distributions 11: 57-72.).

Figure 2
Some endemic species of Brazil found in the Parque Estadual da Serra do Brigadeiro in Minas Gerais State, Brazil. Aptychopsis estrellae (Hornsch.) Ångström, Sphagnum gracilescens Müll. Hal., Riccardia regnellii (Aongström.) Hell, Rhacocarpus inermis (Müll. Hal.) Lindb. var. inermis, Polytrichum angustifolium Mitt. and Bryum subapiculatum Hampe.

Substrate colonization - In the PEBS, most bryophytes showed substrate type preferences,with a greater number of species found in tree bark (63 taxa). This predominance could be related to heterogeneous conditions, such as the varied sizes of the phorophytes and the physical characteristics of bark -with more available colonization niches- (Bates 1992Bates, J.W. 1992. Influence of chemical and physical factors on Quercus and Fraxinus epiphytes at Loch Sunart, western Scotland: a multivariate analysis. Journal of Ecology 80: 163-179., Frahm 2003Frahm, J.P. 2003. Manual of tropical bryology. Tropical Bryology 23: 1-196. , Batista et al. 2018Batista, W.V.S.M., Pôrto, K.C. & Santos, N.D. 2018. Distribution, ecology, and reproduction of bryophytes in a humid enclave in the semiarid region of northeastern Brazil. Acta Botânica Brasílica 32(2): 303-313.), combined with forest conditions of temperature, luminosity, and humidity (Batista & Santos 2016). In works done in the Atlantic Forest, Germano & Pôrto (2005)Germano, S.R. & Pôrto K.C. 2006. Bryophyte communities in Atlantic forest remnant, state of Pernambuco, Brazil. Cryptogamie, Bryologie 27: 153-163., Sousa & Câmara (2015)Sousa, R.V. & Câmara, P.E.A.S. 2015. Survey of the bryophytes of a gallery forest in the National Park of Serra do Cipó, Minas Gerais, Brazil. Acta Botânica Brasílica 29: 24-29. and Siviero & Luizi-Ponzo (2015)Siviero, T.S. & Luizi-Ponzo, A.P. 2015. Briófitas de diferentes fitofisionomias florestais e campestres: estudo em uma área de conservação no sudeste do Brasil-Parque Estadual do Ibitipoca. Pesquisas, Botânica 67: 101-117. also observed a greater number of corticicolous species and they also point to the reasons stated above.

The preference for substrate types has been attributed to the low humidity and to the need of occupying specialized microhabitats, to take advantage of their particular conditions (Batista et al. 2018Batista, W.V.S.M., Pôrto, K.C. & Santos, N.D. 2018. Distribution, ecology, and reproduction of bryophytes in a humid enclave in the semiarid region of northeastern Brazil. Acta Botânica Brasílica 32(2): 303-313.). The annual average rainfall in the PEBS (1,300 mm/year) and it is characterized by a rainy period, during the months of November to March, which is the warmest, and by a dry period, from April to October (Plano de Manejo PESB- Parque Estadual da Serra do Brigadeiro 2007), so the preference for substrate types in bryophytes species of the PESB could be an important strategy for this climate conditions.

The frequency of species on rocky substrates (49 taxa) could be due to the abundant naked surfaces, mainly in the rocky outcrops and streams. In the Atlantic Forest numerous taxa grew on rocks and few species occurred on soil, probably as a result of the existence of a litter on the forest ground that makes difficult growth of the bryophytes (Santos & Costa 2008Santos, N.D. & Costa, D.P. 2008. A importância de reservas particulares do patrimônio natural para a conservação da brioflora da Mata Atlântica: um estudo em El Nagual, Magé, RJ, Brasil. Acta Botânica Brasílica 22: 359-372.). In addition, a lower percentage of species growing in rocks and soil in the Atlantic Forest of northeastern Brazil was explained due to a minor heterogeneity in these substrates in contrast with tree bark (Batista et al. 2018Batista, W.V.S.M., Pôrto, K.C. & Santos, N.D. 2018. Distribution, ecology, and reproduction of bryophytes in a humid enclave in the semiarid region of northeastern Brazil. Acta Botânica Brasílica 32(2): 303-313.).

On the other hand, epiphyllous species were scarce at our study site (nine taxa), and were represented only by liverworts: eight species of Lejeuneaceae and Bazzania stolonifera (table 1). The greatest representativeness of Lejeuneaceae in this substrate is a common condition in tropical forests (Pócs 1982Pócs, T. 1982. Tropical Forest Bryophytes. In: A.J.E., Smith (ed.). Bryophyte Ecology. Chapman and Hall, London, New York, pp. 59-103. , Siviero & Luizi-Ponzo 2015Siviero, T.S. & Luizi-Ponzo, A.P. 2015. Briófitas de diferentes fitofisionomias florestais e campestres: estudo em uma área de conservação no sudeste do Brasil-Parque Estadual do Ibitipoca. Pesquisas, Botânica 67: 101-117.), because content the most specialized epiphyllous species among all the bryophytes, and these have vegetative and reproductive structures for water-storing and anchoring on the leaves (Pócs 1982Pócs, T. 1982. Tropical Forest Bryophytes. In: A.J.E., Smith (ed.). Bryophyte Ecology. Chapman and Hall, London, New York, pp. 59-103. ). Another important attribute of the epiphyllous bryophytes is the heterogeneous occurrence pattern in the forest environment - they are strategically positioned in locations with specific microclimatic conditions (Alvarenga & Porto 2007Alvarenga, L.D.P. & Pôrto, K.C. 2007. Patch size and isolation effects on epiphytic and epiphyllous bryophytes in the fragmented Brazilian Atlantic forest. Biological Conservation 134: 415-427. ). So, low occurrence of epiphyllous species in a general inventory like this one is highly probable, because we mainly sample the easily accessible places (near to pre-existent trails) and these are more readily impacted by different anthropic pressures, such as deforestation, wood extraction, unsustainable tourism (Plano de Manejo PESB - Parque Estadual da Serra do Brigadeiro 2007Plano de Manejo PESB - Parque Estadual da Serra do Brigadeiro. 2007. Governo do Estado de Minas Gerais. Secretaria de Estado de Meio Ambiente e Desenvolvimento Sustentável - SEMAD, pp. 1-89.).

In the fragmented Brazilian Atlantic Forest, the opening of the canopy was considered a cause of reduction and local extinction of epiphyllous bryophyte communities, as it can alter humidity, temperature, and light conditions in the lower forest (Alvarenga & Porto 2007Alvarenga, L.D.P. & Pôrto, K.C. 2007. Patch size and isolation effects on epiphytic and epiphyllous bryophytes in the fragmented Brazilian Atlantic forest. Biological Conservation 134: 415-427. ). Epiphyllous dependence on the microclimate conditions created by vegetation, and consequent susceptibility to environmental disturbances has been repeatedly pointed out (Gradstein 1997Gradstein, S.R. 1997. The taxonomic diversity of epiphyllous bryophytes. Abstracta Botanica 21(1): 15-19., Costa 1999Costa, D.P. 1999. Epiphytic bryophyte diversity in primary and secondary lowland rainforest in southeastern Brazil. Bryologist 102: 320-326., Alvarenga & Porto 2007Alvarenga, L.D.P. & Pôrto, K.C. 2007. Patch size and isolation effects on epiphytic and epiphyllous bryophytes in the fragmented Brazilian Atlantic forest. Biological Conservation 134: 415-427. , Alvarenga et al. 2009Alvarenga, L.D.P., Pôrto, K.C. & Silva, M.P.P. 2009. Relations between regional-local habitat loss and metapopulation properties of epiphyllous bryophytes in the Brazilian Atlantic forest. Biotropica 41(6): 682-691.).

Then, it is advisable to do studies focused on the specific habitats that these plants occupy, such as humid and shady places within the forest (Gradstein et al. 2001Gradstein, S.R., Griffin, III D., Morales, M. & Nadkarni, N. 2001b. Diversity and habitat differentiation of mosses and liverworts in the cloud forest of Monteverde, Costa Rica. Caldasia 23: 203-212.), because epiphyllous are good indicators of the state of conservation of the area.

Conclusions

The data obtained in this study show that the Parque Estadual da Serra do Brigadeiro (PESB) is an important area for conservation of the diversity of Brazilian bryophytes and for the conservation and maintenance of species that are endemics, rare or have a moderate distribution in Brazil.

Our floristic survey of the bryophytes in the PESB contributes to the knowledge of the floristic diversity of the Park with the verification of their distribution, endemism and substrate types. It also contributes with the enrichment of the collection of bryophytes in the VIC Herbarium, where the samples are available for future studies on other aspects of Brazilian bryophytes.

  • 1
    Part of the Masters’ Dissertation of the first Author

Acknowledgements

We thank the CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nivel Superior), for providing scholarships by the first Author and Instituto Estadual de Florestas de Minas Gerais (IEF), by permitted sampling. We thank the director of the Parque Estadual da Serra do Brigadeiro, Mr. José Roberto Mendes de Oliveira, and other Park staff, for logistics, transport and assistance during sampling. Thanks so much to Park staff Francisco Javier Oliveira Ramos and Rosmeri Menendes de Paula, who assisted in the collection and transport. We greatly appreciate the help of Nayara Smith and Julio Lanazca Vargas during field work, the contributions of Rodrigo Bernal to the manuscript and Michael Alejandro Castro Bonilla by the map elaboration.

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Publication Dates

  • Publication in this collection
    20 Nov 2020
  • Date of issue
    2020

History

  • Received
    03 June 2020
  • Accepted
    11 Sept 2020
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