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Identification key for lycophytes and ferns from the Picinguaba and Santa Virgínia Nuclei, Parque Estadual da Serra do Mar, Ubatuba, SP, Brazil

Chave de identificação para licófitas e samambaias dos Núcleos Picinguaba e Santa Virgínia, Parque Estadual da Serra do Mar, Ubatuba, SP, Brasil

Abstract

This work contributes to the knowledge of the fern and lycophytes diversity in the Picinguaba and Santa Virginia Nuclei, Parque Estadual da Serra do Mar (PESM), Ubatuba, São Paulo, Brazil, as well as to provide subsidies to identification of the found taxa in these areas. In total, 30 collecting expeditions were conducted and the vouchers were deposited at UEC Herbarium. We have identified 135 species distributed in 53 genera and 19 families for both areas. The most representative families were Polypodiaceae (28 species) and Dryopteridaceae (19 species), whereas Asplenium (12 species), Blechnum and Elaphoglossum (8 species each) were the most important genera. Epiphytic species predominated (62 overall), probably due to the presence of favorable habitats. Among the taxa, 41 are considered endemic from Brazil, 35 of them endemic to the Brazilian Atlantic Forest. Five species are classified as vulnerable according to the “Official list of endangered species in the State of São Paulo”: Elaphoglossum macahense (Fée) Rosenst., Anetium citrifolium (L.) Splitg., Asplenium muellerianum Rosenst., Cyathea glaziovii (Fée) Domin, and Thelypteris angustifolia (Willd.) Proctor, which emphasizes the importance of preservation areas such as the Parque Estadual da Serra do Mar. An identification key has been elaborated to help with the recognition of these groups in Picinguaba and Santa Virgínia Nuclei.

Keywords:
Floristics; taxonomy; diversity; Atlantic Rain Forest

Resumo

Este trabalho visa contribuir para o conhecimento da diversidade de licófitas e samambaias ocorrentes nos núcleos Picinguaba e Santa Virgínia do Parque Estadual da Serra do Mar (PESM), Ubatuba, SP, Brasil, bem como fornecer subsídios para a identificação dos táxons encontrados nestas áreas. Ao todo, foram realizadas 30 expedições de coleta e o material botânico encontra-se depositado no Herbário UEC. Foram identificadas 135 espécies, 19 famílias e 53 gêneros para as duas áreas. As famílias mais representativas foram Polypodiaceae (28 espécies) e Dryopteridaceae (19 espécies), enquanto Asplenium (12 espécies), Blechnum e Elaphoglossum (8 espécies cada) foram os gêneros melhor representados. As espécies epífitas predominaram (62 ao todo), provavelmente devido à presença de hábitats favoráveis. Dos táxons encontrados, 41 são considerados endêmicos do Brasil, sendo 35 deles endêmicos da Mata Atlântica brasileira; cinco espécies são classificadas como vulneráveis, conforme a “Lista oficial de espécies ameaçadas de extinção no Estado de São Paulo”: Elaphoglossum macahense (Fée) Rosenst., Anetium citrifolium (L.) Splitg., Asplenium muellerianum Rosenst., Cyathea glaziovii (Fée) Domin e Thelypteris angustifolia (Willd.) Proctor, o que ressalta a importância de áreas de preservação como o Parque Estadual da Serra do Mar, no contexto conservacionista. Uma chave de identificação foi elaborada para contribuir no reconhecimento destes grupos nos núcleos Picinguaba e Santa Virgínia.

Palavras-chaves:
florística; taxonomia; diversidade; Floresta Ombrófila Densa Atlântica

Introduction

The Atlantic Forest is a complex set of ecosystems, with significant importance for harboring a considerable portion of Brazilian biological diversity (Joly et. al., 1999Joly C.A., AIDAR. M.P.M., KLINK C.A., MCGRATH D.G., MOREIRA A.G., MOUTINHO P., NEPSTAD D.C., OLIVEIRA A.A., POTT A., RODAL M.J.N. & SAMPAIO E.V.S.B. 1999. Evolution of the Brazilian phytogeography classification systems: implications for biodiversity conservation. Ciência e cultura 51 (5-6): 331-348.). According to Forzza et al. (2012)Forzza R.C., Baumgratz J.F.A., Bicudo C.E.M., Canhos D.A.I., Carvalho jr. A.A., Coelho M.A.N., Costa A.F., Costa D.P., Hopkins M.G., Leitman P.M., Lohmann L.G., Lughadha E.N., Maia L.C., Martinelli G., Menezes M., Morim M.P., Peixoto A.L., Pirani J.R., Prado J., Queiroz L.P., Souza S., Souza V.C., Stehmann J.R., Sylvestre L.S., Walter B.M.T. & Zappi D.C. 2012. New Brazilian Floristic List Highlights Conservation Challenges. BioScience 62(1): 39-45. this vegetation presents 19,335 species of plants and fungi, which contributes substantially to the mega-diversity of the country.

However, studies reveal that only 7.9% of the Atlantic Forest remnants are larger than 100 hectares, a size that would be representative for biodiversity conservation (SOS Atlantic Forest and INPE, 2011FUNDAÇÃO SOS MATA ATLÂNTICA & INSTITUTO NACIONAL DE PESQUISAS ESPACIAIS – INPE. 2011. Atlas dos Remanescentes Florestais da Mata Atlântica. <http://mapas.sosma.org.br/>. Acesso em 30 de julho de 2011.
http://mapas.sosma.org.br/...
). These data reinforce the need to better understand and protect this forest, which is considered one of the major biodiversity hotspots of the Neotropics (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.).

The Serra do Mar (a mountain range within the Atlantic Forest Domain) is located mainly in the Southeastern region of Brazil. It is a primary center of diversity and endemism for lycophytes and ferns (Tryon, 1986Tryon, R. M. 1986. Some new names and new combinations in Pteridaceae. American Fern Journal 76(4): 184-186.), probably because of regional relief features. As amply documented in several previous studies, mountainous areas have favorable environmental conditions for the development of these two groups of plants (see Holttum, 1938Holttum R.E. 1938. The ecology of tropical pteridophytes. In: Manual of Pteridology (F. Verdoorn & A.H.G. Alston, eds.) Springer Netherlands, Plant Sciences, p. 420-450.; Page, 1979Page C.N. 1979. The diversity of ferns: an ecological perspective. In: Dyer A.F. (ed.). The experimental biology of ferns. Academic Press, London, UK, p. 9-56.; Tryon 1986Tryon, R. M. 1986. Some new names and new combinations in Pteridaceae. American Fern Journal 76(4): 184-186.; Roos, 1996Roos M. 1996. Mapping the world’s pteridophyte diversity – systematics and floras. In: Pteridology in Perspective, ed. J. M. Camus, M. Gibby and R. J. Johns. Kew, UK: Royal Botanic Gardens, p. 29–42., and Moran, 2008Moran R.C. 2008. Biogeography of ferns and lycophytes. In: The Biology and Evolution of Ferns and Lycophytes (C. Haufler & T.A Ranker, eds.) Cambridge University Press, p. 369-396.).

Recently, Prado et al. (2015)Prado, J, Sylvestre L. S., Labiak P. H., Windisch P. G., Salino A., Barros I. C. L., Hirai R. Y., Almeida T. E., Santiago A. C. P., Kieling-Rubio M. A., Pereira A. F. N., Øllgaard B., Ramos C. G. V., Mickel J. T., Dittrich V. A. O., Mynssen C. M., Schwartsburd P. B., Condack J. P. S., Pereira J. B. S., Matos F. B. 2015. Diversity of ferns and lycophytes in Brazil. Rodriguésia 66(4): 1073-1083. reported 883 species of ferns and lycophytes in the Brazilian Atlantic Rain Forest. This number surpasses Amazon (with 503 species), Cerrado (269 species), Caatinga (26 species), Pantanal (30 species), and Pampa (eight species). In the Atlantic Rain Forest of São Paulo there are 603 species, distributed in 115 genera and 33 families of ferns and lycophytes. According to Prado (1998)Prado, J. 1998. Pteridófitas do Estado de São Paulo. In: Bicudo, C.E.M. & Shepherd G. (Eds.). Fungos macroscópicos e plantas do Estado de São Paulo (Série Biodiversidade do Estado de São Paulo). São Paulo: FAPESP 2: 49-61., the highest diversity of ferns and lycophytes within this area is found at Serra da Mantiqueira, Serra da Bocaína, Serra do Japi, and Vale do Ribeira.

For similar areas to the current study (i.e., Atlantic Forest mountain slopes in the state of São Paulo), there are the works by Custódio-Filho (1989)Custódio FILHO A. 1989. Flora da Estação Ecológica de Boracéia – Listagem de espécies. Revista do Instituto Florestal 1: 161-199., Prado & Labiak (2001Prado J. & Labiak P.H. 2001. Pteridófitas. In: M. C. H. Mamede, I. Cordeiro & L. Rossi, Flora vascular da Serra da Juréia, Município de Iguape, São Paulo, Brasil. Boletim do Instituto de Botânica 15: 83-86., 2009Prado J. & Labiak P.H. 2009. Pteridófitas da Reserva Biológica de Paranapiacaba. In: M.I.M.S. Lopes; M. Kirizawa; M.M.R.F.de Melo. (Org.). Patrimônio da Reserva Biológica do Alto da Serra de Paranapiacaba: A Antiga Estação Biológica do Alto da Serra. São Paulo: Editora Secretaria do Meio Ambiente de São Paulo, p. 269-290.); Athayde-Filho et al. (2003)Athayde-Filho F.P., PEREIRA. V.S., SMIDT E.C. & NONATO F.R. 2003. Pteridófitas do Parque Estadual da Ilha Anchieta (PEIA). Bradea 12: 55-66., Prado (2004)Prado J. 2004. Pteridófitas do Maciço da Juréia. In: W. Duleba & O.A.V. Marques (orgs.) Estação Ecológica Juréia – Itatins: ambiente físico, flora e fauna. 1a. ed. FAPESP, Instituto Butantan, Holos, Ribeirão Preto, p. 139-151., Boldrin & Prado (2007)Boldrin A.H.L. & Prado J. 2007. Pteridófitas terrestres e rupícolas do Forte dos Andradas, Guarujá, São Paulo, Brasil. Boletim de Botânica da Universidade de São Paulo 25: 1-69., Salino & Almeida (2008)Salino, A. & Almeida, T.E. 2008. Pteridófitas do Parque Estadual do Jacupiranga, SP, Brasil. Acta Botanica Brasilica 22: 983-991., and Mazziero et al. (2015)MAZZIERO.F.F.F.; LABIAK, P.H. & PACIENCIA, M.L.B. 2015. Checklist of ferns and lycophytes from the Parque Estadual Turístico do Alto Ribeira, Iporanga, São Paulo, Brazil. Check List 11: 1791.. However, there are no identification keys for the ferns and lycophytes from the Atlantic Forest in northeastern São Paulo.

The Picinguaba and Santa Virgínia Nuclei are located in the Parque Estadual da Serra do Mar, municipalities of Ubatuba, São Luís do Paraitinga, and Cunha, protecting a very well preserved area of Atlantic Forest at northeastern São Paulo. These places harbor a rich flora of lycophytes and ferns and the main objective of this paper is to provide an identification key for determining the species of these groups in these areas.

Material and Methods

Study area: The “Parque Estadual da Serra do Mar” (State Park) represents the largest continuous area of well preserved Atlantic Forest in Brazil, with almost 315 000 ha (3.159 m2) and covering areas from two states, São Paulo and Rio de Janeiro, in the southeast region of the country. This park is divided into 10 conservation units, among them Picinguaba and Santa Virginia.

The Santa Virginia Nucleus (SVN) belongs to the municipalities of São Luís do Paraitinga (70% of its area), Cunha (20%), and Ubatuba (10%), at coordinates 23°17’–23°24'S and 45°03'–45°11'W, spanning about 5,000 ha (57 m2) of predominantly Montane Dense Ombrophilous Forest (Veloso et al., 1991Veloso H.P., Rangel FILHO A.L.R. & Lima J.C.A. 1991. Classificação da Vegetação Brasileira, Adaptada a um Sistema Universal. IBGE, Departamento de Recursos Naturais e Estudos Ambientais.). Altitudes vary from 850 to 1,100 m, with an average annual temperature of 17° C, and average annual rainfall of 2,300 mm (Salemi, 2009Salemi L.F. 2009. Balanço de água e de nitrogênio em uma microbacia coberta de pastagens no litoral norte do Estado de São Paulo. 2009. Dissertação de Mestrado, Universidade de São Paulo, Piracicaba.).

The Picinguaba Nucleus (PN) is located in the Municipality of Ubatuba, at coordinates 23°31’–23°34'S and 45°02'–45°05'W, and consists of about 47,500 ha (4,75 m2), according to SMA (1996). There are different types of vegetations in PN: Pioneer Formations with Marine Influence (Dunes); Pioneer Formations with Fluvial Influence (Caxetal); Pioneer Formations with Fluvial-Marine Influence (Mangrove); Lowland Dense Ombrophilous Forest (Restinga Forest); Submontane Dense Ombrophilous Forest; and Montane Dense Ombrophilous Forest (Assis, 1999Assis M.A. 1999. Florística e caracterização das comunidades vegetais da Planície Costeira de Picinguaba, Ubatuba/SP. Tese de Doutorado, Universidade Estadual de Campinas, Campinas.). The altitude varies from sea level up to 1,340 m, with an annual average temperature of 22° C, and average annual rainfall exceeding 2,200 mm (Setzer 1966Setzer, J. 1966. Atlas climatológico do estado de São Paulo. Comissão Interestadual da Bacia do Paraná-Paraguai; CESP, São Paulo.).

The study areas covers four different vegetation types in Atlantic Forest, designated according to Veloso et al. (1991)Veloso H.P., Rangel FILHO A.L.R. & Lima J.C.A. 1991. Classificação da Vegetação Brasileira, Adaptada a um Sistema Universal. IBGE, Departamento de Recursos Naturais e Estudos Ambientais. as: Lowland Dense Ombrophilous Forest, (Figure 1 - B, C, D, E, F), Submontane Dense Ombrophilous Forest (Figure 1 - G, H, I, J), Montane Dense Ombrophilous Forest (Figure 1 - K, L, M, N) and Alluvial Dense Ombrophilous Forest (Figure 1 - A). According to observations by Assis (1999)Assis M.A. 1999. Florística e caracterização das comunidades vegetais da Planície Costeira de Picinguaba, Ubatuba/SP. Tese de Doutorado, Universidade Estadual de Campinas, Campinas., this last area is treated as Restinga Forest in the scope of the Biota FAPESP, Project, nº 03/12595-7.

Figure 1
Location of the study areas in the Parque Estadual da Serra do Mar. A= Restinga; B, C, D, E, F= Lowlands Rain Forest; G, H, I, J= Submontane Rain Forest; K, L, M, N= Montane Rain Forest. (Google Earth in 17 Nov 2015).

Sampling design: The lycophyte and fern of the Picinguaba and Santa Virginia Nuclei was investigated along trails, roads, and plots found in these areas. We conducted 23 collecting expeditions in the Picinguaba Nucleus, from 2008 to 2011.Eleven of these expeditions were made to the “Casa da Farinha” (Figure 1 - B, C, D, E), seven to the “Fazenda Capricórnio” (Figure 1 - F, G, H, I, J), and five to the “Praia da Fazenda” areas (Figure 1 - A). Seven expeditions with the same purpose were undertaken in Santa Virginia Nucleus (Figure 1 - K, L, M, N), totaling 30 collecting expeditions in both Nuclei.

The collected material was prepared according to the methodology indicated by Silva (1989)Silva A.T. 1989. Pteridófitas. In: O. Fidalgo & V.L.R. Bononi (coords.). Técnicas de coleta, preservação e herborização de material botânico. Manual nº 04. 2 ed. São Paulo, Instituto de Botânica, p. 32 –34.. Herbarium vouchers were deposited at UEC. We adopted the classification system by Smith et al. (2006Smith A.R., Pryer K.M., Schuettpelz E. KORALL P., SCHNEIDER, H. & WOLF P.G. 2006. A classification for extant ferns. Taxon 55: 705-731., 2008Smith A.R., Pryer K.M., Schuettpelz E., Korall P., Schneider H. & Wolf P.G. 2008. Fern Classification. In: T.A. Ranker & C.H. Haufler (eds.). Biology and evolution of ferns and Lycophytes. Cambridge University, Cambridge, p. 417-467.), with changes by Christenhusz et al. (2011)Christenhusz J. M. M., ZHANG XIAN-CHUN & SCHNEIDER H. 2011. A linear sequence of extant families and genera of lycophytes and ferns. Phytotaxa 19: 7–54..

For the geographic distribution, we adopted four basic categories: Pantropical (species of the tropical zones), Tropical America (species of the tropical and subtropical America, including South of the USA), South America (only in South America), and Endemics from Brazil. The distribution of the endemic species was based on Prado et al. (2015)Prado, J, Sylvestre L. S., Labiak P. H., Windisch P. G., Salino A., Barros I. C. L., Hirai R. Y., Almeida T. E., Santiago A. C. P., Kieling-Rubio M. A., Pereira A. F. N., Øllgaard B., Ramos C. G. V., Mickel J. T., Dittrich V. A. O., Mynssen C. M., Schwartsburd P. B., Condack J. P. S., Pereira J. B. S., Matos F. B. 2015. Diversity of ferns and lycophytes in Brazil. Rodriguésia 66(4): 1073-1083.. The habitat and growth are reported as guilds of the life forms, according to Paciencia (2008)Paciencia, M.L.B. 2008. Diversidade de pteridófitas em gradientes de altitude na Mata Atlântica do Estado do Paraná, Brasil. Tese de Doutorado. Universidade de São Paulo, São Paulo, 229p..

The identification key here presented was prepared through the observation of the morphological features of adult plants recorded from Picinguaba and Santa Virginia Nuclei. This key prioritizes the morphological features that are easily observed in the field as well as on herbarium specimens. Therefore, the intention was to develop a key containing the maximum set of possible macroscopic features and to avoid the practice of cutting herbarium specimens.

The key does not present families or genera. We avoided presenting our results in the traditional way, because we believe that the users of this key could be enthusiasts in the study of lycophytes and ferns and they are familiarized with the common morphological features of the different groups. Unlike keys that separate different groups, the present paper pays attention to the morphological structures that are similar between species, even if they are phylogenetically distant.

Results and Discussion

We found 135 species distributed in 53 genera and 19 families of ferns and lycophytes for the two areas (Table 1). The most representative families were Polypodiaceae, with 28 species, and Dryopteridaceae, with 19 species. The genera with more species were Asplenium (12 species), followed by Blechnum and Elaphoglossum (eight species each).

Table 1
Species of ferns and lycophytes found in the Biota Gradiente Funcional area (EA= endemic of the Atlantic Forest, exclusively; EB= Endemic of Brazil, not exclusively of the Atlantic Rain Forest). RF = Restinga Forest; LF = Lowlands Rain Forest; SF = Submontane Rain Forest; MF = Montane Rain Forest. T = terrestrial; R = rupicolous; E = epiphyte; H = hemiepiphyte; S = scandent; Sb = subarborescent A = arborescent.

Among the guilds of life forms, the epiphytes were predominant, with 62 species overall (Figure 2). According to Madison (1977)Madison, M. 1977. Vascular epiphytes: Their systematic occurrence and salient features. Selbyana 2: 1-13., the high diversity of epiphytes in neotropical forests is favored by an abundance of favorable habitats, especially in montane regions. In these regions, these groups of plants represent about 50% of the total flora (Kelly et al., 1994Kelly, D.L.; Tanner, E.V.J.; Lughadha Nic, E.M. & Kapos, V. 1994. Floristic and biogeography of a rain forest in the Venezuelan Andes. J Biogeogr 21: 421–440.), due, primordially, to the forest structure and water availability (Grubb & Withimore, 1966Grubb, P.J. & Withimore, T.C. 1966. A comparison of montane and Lowland Rain forest in Ecuador, II. The climate and its Effects on the Distribution and Physiognomy of the Forest. J Ecol 54: 303-333.).

Figure 2
Species number per different life forms in the Picinguaba and Santa Virginia Nuclei.

The high degree of endemism for south and southeastern Brazil (Tryon & Tryon, 1982Tryon, R.M. & Tryon, A.F. 1982. Ferns and allied plants, with special reference to tropical America. Springer-Verlag, New York. 857p.; Prado & Silvestre, 2010Prado, J. & Sylvestre, L.S. 2010. As samambaias e licófitas do Brasil. In: Forzza, R.C.; Baumgratz, J.F.A.; Bicudo, C.E.M.; Canhos, D.A.I.; Carvalho, Jr. A.A.; Coelho, M.A.N.; Costa, A.F.; Costa, D.P.; Hopkins, M.G.; Leitman, P.M.; Lohmann, L.G.; Lughadha, E.N.; Maia, L.C.; Martinelli, G.; Menezes, M.; Morim, M.P.; Peixoto, A.L.; Pirani, J.R.; Prado, J.; Queiroz, L.P.; Souza, S.; Souza, V.C.; Stehmann, J.R.; Sylvestre, L.S.; Walter, B.M.T. & Zappi, D.C. (Org.). Catálogo de plantas e fungos do Brasil. Rio de Janeiro: Andrea Jakobsson Estúdio; Jardim Botânico do Rio de Janeiro. Pp. 69-74.) can be exemplified in this work, which presents about 30.37% (41 spp.) of the taxa considered endemic from Brazil. About 85% (35 spp.) of these are endemic to the Atlantic Rain Forest (Figure 3).

Figure 3
Species number found in PESM area, separated by geographic distribution class.

Two invasive exotic species, Macrothelypteris torresiana (Gaudich.) Ching and Nephrolepis cordifolia (L.) C. Presl, were found in the study area. These species are common in various other sites of the Atlantic Forest (Zenni & Ziller, 2011Zenni R.D. & Ziller S.R. 2011. An overview of invasive plants in Brazil. Revista Brasileira de. Botânica 34(3): 431-446.).

In total, five species are considered endangered in the vulnerable category, according to “Lista oficial de espécies ameaçadas de extinção no Estado de São Paulo” (Resolução SMA nº 48/2004): Anetium citrifolium (L.) Splitg., Asplenium muellerianum Rosenst., Cyathea glaziovii (Fée) Domin, Elaphoglossum macahense (Fée) Rosenst., and Thelypteris angustifolia (Willd.) Proctor. This factor stresses the importance of the Picinguaba and Santa Virgínia Nuclei for the conservation of biodiversity in the State of São Paulo.

This forest is lush and diverse, with humidity and relief suitable for the development of ferns and lycophytes. Thus, the present paper contributes to the knowledge of these groups and highlights the importance of the permanent preservation of these areas.

The key presented ahead is the first one for a broad area covered by the Atlantic Rain Forest in Brazil. It constitutes an important tool for the identification of ferns and lycophytes from the northeastern portion of the state of São Paulo.

Acknowledgments

The first author is grateful to the CNPq for the scholarship and Biota FAPESP Program for financial support. We also thank Fernando B. Matos for English corrections to improve the manuscript.

References

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  • Prado J. & Labiak P.H. 2009. Pteridófitas da Reserva Biológica de Paranapiacaba. In: M.I.M.S. Lopes; M. Kirizawa; M.M.R.F.de Melo. (Org.). Patrimônio da Reserva Biológica do Alto da Serra de Paranapiacaba: A Antiga Estação Biológica do Alto da Serra. São Paulo: Editora Secretaria do Meio Ambiente de São Paulo, p. 269-290.
  • Prado J. 2004. Pteridófitas do Maciço da Juréia. In: W. Duleba & O.A.V. Marques (orgs.) Estação Ecológica Juréia – Itatins: ambiente físico, flora e fauna. 1a. ed. FAPESP, Instituto Butantan, Holos, Ribeirão Preto, p. 139-151.
  • Prado, J, Sylvestre L. S., Labiak P. H., Windisch P. G., Salino A., Barros I. C. L., Hirai R. Y., Almeida T. E., Santiago A. C. P., Kieling-Rubio M. A., Pereira A. F. N., Øllgaard B., Ramos C. G. V., Mickel J. T., Dittrich V. A. O., Mynssen C. M., Schwartsburd P. B., Condack J. P. S., Pereira J. B. S., Matos F. B. 2015. Diversity of ferns and lycophytes in Brazil. Rodriguésia 66(4): 1073-1083.
  • Prado, J. & Sylvestre, L.S. 2010. As samambaias e licófitas do Brasil. In: Forzza, R.C.; Baumgratz, J.F.A.; Bicudo, C.E.M.; Canhos, D.A.I.; Carvalho, Jr. A.A.; Coelho, M.A.N.; Costa, A.F.; Costa, D.P.; Hopkins, M.G.; Leitman, P.M.; Lohmann, L.G.; Lughadha, E.N.; Maia, L.C.; Martinelli, G.; Menezes, M.; Morim, M.P.; Peixoto, A.L.; Pirani, J.R.; Prado, J.; Queiroz, L.P.; Souza, S.; Souza, V.C.; Stehmann, J.R.; Sylvestre, L.S.; Walter, B.M.T. & Zappi, D.C. (Org.). Catálogo de plantas e fungos do Brasil. Rio de Janeiro: Andrea Jakobsson Estúdio; Jardim Botânico do Rio de Janeiro. Pp. 69-74.
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Identification key for lycophytes and ferns species found in Biota Gradient Functional areas (Picinguaba and Santa Virgínia Nuclei)

  • 1. Arborescent plants (tree ferns)

    • 2. Petiole base with black, tapered and rigid spines; thickly coated with filamentous setae scales

      • 3. Aphlebias present; petiole base persistent on the stem ................. Alsophila setosa

      • 3. Aphlebias absent; petiole base deciduous leaving a scar on the stem ................. Alsophila sternbergii

    • 2. Petiole base with spines with the same coloration of this, conical, acute apex or absents; lanceolate scale scattered or concentrated in proximal portion, setae present or absent

      • 4. Petiole scales whitish or bicolor (i.e., whitish at margins and brown at center)

        • 5. Petiole base deciduous leaving a scar on the stem, scales with black setae ................. Cyathea hirsuta

        • 5. Petiole base persistent on the stem, scales without setae

          • 6. Petiole scales concolor (whitish) ................. Cyathea leucofolis

          • 6. Petiole scales bicolor (whitish and brown) ................. Cyathea dichromatolepis

      • 4. Petiole scales brown

        • 7. Petiole base deciduous leaving a scar on the stem, indusium globose ................. Cyathea delgadii

        • 7. Petiole base persistent on the stem, indusium absent

          • 8. Secondary veins predominantly forked; costae and costules only with inflated scales ................. Cyathea phalerata

          • 8. Secondary veins predominantly simple; costae and costules with plan and inflated scales (bullate scales)

            • 9. Petiole with spines at base; sori with paraphyses longer than the sporangia ................. Cyathea atrovirens

            • 9. Petiole without spines (with small round projections); sori with paraphyses shorter than the sporangia ................. Cyathea glaziovii

  • 1. Herbaceous plants (climbers, epiphytes, hemiepiphytes, terrestrial, rupicolous, or subarborescent)

    • 10. Leaves with a single vein (microphylls) and with a minute ligule; stems with rhizophores

      • 11. Stems articulate; lateral and axillary microphylls with base auriculate................. Selaginella sulcata

      • 11. Stems not articulate, lateral and axillary microphylls not auriculate at base

        • 12. Microphylls with ciliate margins ................. Selaginella macrostachya

        • 12. Microphylls without ciliate margins

          • 13. Lateral microphylls oval; dorsal microphylls asymmetric ................. Selaginella muscosa

          • 13. Lateral microphylls oblong or oblong-elliptic; dorsal microphylls symmetric ................. Selaginella flexuosa

    • 10. Leaves with more than one vein (megaphylls), without ligule; rhizome or stem with adventitious roots, without rhizophores

      • 14. Lamina undivided (or only fertile leave undivided in Cochlidium serrulatum), without segments (not pinnate)

        • 15. Sori round, oblong or ovate; venation anastomosing with free veins included in the areoles

          • 16. Stem scales not clathrate

            • 17. Lamina without scales ................. Microgramma geminata

            • 17. Lamina with scales

              • 18. Scales present only on the adaxial surface ................. Microgramma vacciniifolia

              • 18. Scales present on both surfaces

                • 19. Sterile leaf linear-lanceolate ................. Microgramma percussa

                • 19. Sterile leaf ovate ................. Microgramma tecta

          • 16. Stem scales clathrate

            • 20. Sori oblong or ovate, longer than wide ................. Pleopeltis astrolepis

            • 20. Sori round

              • 21. One row of sori between two lateral veins ................. Niphidium crassifolium

              • 21. Two rows of sori between two lateral veins

                • 22. Lateral veins abaxially prominent

                  • 23. Stem scales brown, ovate, sub-globose ................. Campyloneurum nitidum

                  • 23. Stem scales slightly bicolor (brown and light-brown), lanceolate ................. Campyloneurum minus

                • 22. Lateral veins abaxially not prominent

                  • 24. Rhizome with peltate scales; lamina margins revolute ................. Campyloneurum angustifolium

                  • 24. Rhizome with scales basifix, cordate; lamina margins flat

                    • 25. Lamina linear, rigid and bright................. Campyloneurum rigidum

                    • 25. Lamina lanceolate, flexible, opaque ................. Campyloneurum lapathifolium

          • 15. Sori not round, oblong or oval; veins free or if anastomosing without free veins included in the areoles

            • 26. Sori acrostichoid

              • 27. Lamina elliptic, oblong or ovate

                • 28. Apex of the lamina round ................. Elaphoglossum lingua

                • 28. Apex of the lamina acuminate or acute

                  • 29. Stem scales yellow or light brown, ovate ................. Elaphoglossum minutum

                  • 29. Stem scales black, fimbriate, with irregular process and cilia ................. Elaphoglossum luridum

              • 27. Lamina lanceolate

                • 30. Lamina without scales on laminar tissue (present only on the petiole, costae, and margins) ................. Elaphoglossum decoratum

                • 30. Lamina with scales on laminar tissue (including petiole and costae) or lamina glabrous

                  • 31. Lamina glabrous or with scales, the scales not similar to those of the petiole

                    • 32. Veins free near the margins of the lamina ................. Elaphoglossum macahense

                    • 32. Veins anastomosing near the margins of the lamina ................. Elaphoglossum macrophyllum

                  • 31. Lamina with scales, the scales similar to those of the petiole

                    • 33. Scales of the lamina linear-lanceolate ................. Elaphoglossum horridulum

                    • 33. Scales of the lamina oblong-lanceolate or lanceolate ................. Elaphoglossum chrysolepis

            • 26. Sori not acrostichoid (sporangia forming lines parallel to the veins, costae, and margins or immersed, or on the surface forming coenosorus)

              • 34. Venation free

                • 35. Lamina shorter than 5 cm long; sporangia forming coenosorus; spores with chlorophyll

                  • 36. Hydathodes inconspicuous on the adaxial surface of the lamina; sori restricted to the distal pat of the lamina ................. Cochlidium serrulatum

                  • 36. Hydathodes conspicuous on the adaxial surface of the lamina; sori not restricted to the distal pat of the lamina ................. Cochlidium punctatum

                • 35. Lamina bigger than 5 cm long; sporangia linear; spores without chlorophyll

                  • 37. Lamina > 4 cm wide; sori parallel to the lateral veins ................. Asplenium serratum

                  • 37. Lamina < 3 cm wide; sori parallel to the costa ................. Blechnum lanceola

              • 34. Venation anastomosing, without free veins included in the areoles

                • 38. Lamina with only one row of areoles between the margin and costa ................. Radiovittaria stipitata

                • 38. Lamina with several rows of areoles between the margin and costa ................. Anetium citrifolium

      • 14. Lamina divided (pinnate, 2-pinnate or more divided, pinnatifid, pinnatisect, or dichotomous)

        • 39. Lamina with 1 or 2 cell layers in thickness, translucid

          • 40. Indusium bivalve, receptacle not extended beyond the margins of the involucre

            • 41. Lamina glabrous

              • 42. Lamina 1-pinnate-pinnatisect, petiole not winged ................. Hymenophyllum asplenioides

              • 42. Lamina 2 or 3-pinnate-pinnatissect, petiole winged

                • 43. Terminal segments long (caudate), plants > 10 cm long ................. Hymenophyllum caudiculatum

                • 43. Terminal segments shorts (not caudate), plants < 10 cm long ................. Hymenophyllum polyanthos

            • 41. Lamina with hairs

              • 44. Rachis fully winged; fronds with stellate hairs on the petiole, rachis, veins, and margins of the lamina (except on the laminar tissue between veins and margins) ................. Hymenophyllum hirsutum

              • 44. Rachis irregular winged; fronds with stellate hairs on the entire blade (including the laminar tissue) ................. Hymenophyllum rufum

          • 40. Indusium tubular and bilabiate, receptacle long beyond involucre margins

            • 45. Plants terrestrial; rhizome erect or short-creeping; fronds fasciculate

              • 46. Lamina deltoid and 3 or 4-pinate-pinnatisect, rachis without wings ................. Abrodictyum rigidum

              • 46. Lamina lanceolate and 1-pinate-pinatissect, rachis with narrow wings ................. Trichomanes cristatum

            • 45. Plants epiphytes; rhizome long-creeping; fronds not fasciculate

              • 47. False veins present in the laminar tissue

                • 48. Indusium included in the lamina; false veins parallel to the margin of the lamina ................. Didymoglossum krausii

                • 48. Indusium exserted; false veins not parallel to the margin of the lamina

                  • 49. Plants up to 5 cm long; margins of the lamina with furcate and stellate hairs, restricted to sinus ................. Didymoglossum reptans

                  • 49. Plants up to 2 cm long; margins of the lamina with only furcate hairs ................. Didymoglossum hymenoides

              • 47. False veins absent in the laminar tissue

                • 50. Venation catadromous ................. Trichomanes polypodioides

                • 50. Venation anadromous

                  • 51. Petiole not winged ................. Polyphlebium angustatum

                  • 51. Petiole winged

                    • 52. Stem and petiole with brown hairs ................. Vandenboschia radicans

                    • 52. Stem and petiole with black hairs ................. Polyphlebium pyxidiferum

        • 39. Lamina with more than 2 cell layers in thickness, not translucid

          • 53. Petiole base persistent in the stem, forming phyllopodium

            • 54. Lamina dichotomously divided

              • 55. Sori rounded or oblong ................. Pleopeltis pleopeltifolia

              • 55. Sori linear ................. Pleopeltis furcata

            • 54. Lamina pinnate, 2-pinnate or more divided

              • 56. Petiole cylindrical, not sulcate

                • 57. Veins simple ................. Pecluma sicca

                • 57. Veins forked

                  • 58. Proximal segments reduced (auriculate) ................. Pecluma paradiseae

                  • 58. Proximal segments not reduced ................. Pecluma recurvata

              • 56. Petiole sulcate

                • 59. Venation free

                  • 60. Scales abundant on the laminar tissue ................. Pleopeltis hirsutissima

                  • 60. Scales absent on the laminar tissue ................. Pecluma chnoophora

                • 59. Venation anastomosing

                  • 61. Lamina pinnatisect

                    • 62. Stem dark-brown to black, pruinose ................. Serpocaulon catharinae

                    • 62. Stem light brown to yellow, without waxy deposits

                      • 63. Lamina without hairs, scales presents in the costae ................. Serpocaulon latipes

                      • 63. Lamina with hyaline hairs ................. Serpocaulon laetum

                  • 61. Lamina 1-pinnate

                    • 64. Medial pinnae not adnate ................. Serpocaulon fraxinifolium

                    • 64. Medial pinnae with the acroscopic side slightly adnate ................. Serpocaulon meniscifolium

      • 53. Phyllopodium absent

        • 65. Sori linear

          • 66. Sori marginal or submarginal

            • 67. Sori submarginal, protected by an abaxial indusium

              • 68. Pinnules 2 or 3 times forked ................. Lindsaea virescens var. virescens

              • 68. Pinnules not forked (pinnate or more divided)

                • 69. Rachis and secondary rachis quadrangular ................. Lindsaea quadrangularis subsp. quadrangularis

                • 69. Rachis and secondary rachis not quadrangular

                  • 70. Rachis and secondary rachis paleaceous, winged paleaceous; pinnules semilunate ................. Lindsaea lancea var. lancea

                  • 70. Rachis and secondary rachis reddish brown, winged paleaceous contracting with rachis color; pinnules not semilunate ................. Lindsaea divaricata

            • 67. Sori marginal, protected by an adaxial indusium formed by the revolute margin of the lamina

              • 71. Lamina not fully pinnate ................. Doryopteris concolor

              • 71. Lamina pinnate

                • 72. Lamina 1-pinnate ................. Pteris splendens

                • 72. Lamina 2-3-pinnate

                  • 73. Venation free ................. Pteris deflexa

                  • 73. Venation anastomosing ................. Pteris decurrens

          • 66. Sori not marginal and not submarginal

            • 74. Sori parallel and adjacent to the costa

              • 75. Plants with indeterminate growth, climbing ................. Salpichlaena volubilis

              • 75. Plants with determinate growth, not climbing

                • 76. Fertile and sterile fronds monomorphic

                  • 77. Proximal pinnae gradually reduced toward the lamina base

                    • 78. Plants herbaceous; stem stoloniferous; petiole with lanceolate and brownish scales ................. Blechnum polypodioides

                    • 78. Plants sub-arborescent; stem not stoloniferous; petiole with linear to linear-lanceolate and blackish scales ................. Blechnum brasiliense

                  • 77. Proximal pinnae not reduced or only slightly reduced toward the lamina base

                    • 79. Fronds entire ................. Blechnum lanceola

                    • 79. Fronds pinnate

                      • 80. Proximal pinnae petiolulate ................. Blechnum gracile

                      • 80. Proximal pinnae sessile or adnate ................. Blechnum occidentale

                • 76. Fertile and sterile fronds dimorphic

                  • 81. Petiole base with concolor scales ................. Blechnum cordatum

                  • 81. Petiole base with bicolor scales

                    • 82. Stem erect, subarborescent with scales, the scales blackish or brown in the center and golden near the margin ................. Blechnum schomburgkii

                    • 82. Stem scandent with scales, the scales blackish or brown in the center and light brown near the margin ................. Blechnum acutum

            • 74. Sori not parallel to the costa

              • 83. Sori in both sides of the secondary vein, at least in the proximal veins

                • 84. Lateral pinnae entire ................. Diplazium riedelianum

                • 84. Lateral pinnae divided ................. Diplazium cristatum

              • 83. Sori only in one side of the secondary veins

                • 85. Venation anastomosing near the lamina margin ................. Hemidictyum marginatum

                • 85. Venation free

                  • 86. Lamina 2-4-pinnate at base

                    • 87. Rachis with proliferous buds ................. Asplenium radicans

                    • 87. Rachis without proliferous buds

                      • 88. Plants epiphyte; fronds pendulous; stem with linear scale; green lamina ................. Asplenium scandicinum

                      • 88. Plants terrestrial; fronds erects; stem with lanceolate scale; bluish-green lamina .................Asplenium pseudonitidum

                  • 86. Lamina 1-pinnate at base

                    • 89. Stem long-creeping with coloration conspicuously green ................. Hymenasplenium triquetrum

                    • 89. Stem erect or decumbent with coloration little evident

                      • 90. Lamina margin entire to weakly crenate ................. Asplenium oligophyllum

                      • 90. Lamina margin weakly or deeply incised (serrate)

                        • 91. Apex of the segments mucronate

                          • 92. Petiole green and glabrous ................. Asplenium mucronatum

                          • 92. Petiole greyish with linear-lanceolate scales ................. Asplenium mullerianum

                        • 91. Apex of the segments not mucronate

                          • 93. Pinnae acroscopically with an auricle overlapping the rachis ................. Asplenium auriculatum

                          • 93. Pinnae acroscopically without auricle or, if it is present, not overlapping the rachis

                            • 94. Proximal pinnae gradually reduced (1/2 the length of medial or smaller)

                              • 95. Fronds erect; petiole long about 1/3 of the lamina length ................. Asplenium claussenii

                              • 95. Fronds pendulous; petiole short about 1/10 of the lamina length ................. Asplenium pteropus

                            • 94. Proximal pinnae not gradually reduced or only slightly reduced

                              • 96. Apex of the lamina without proliferous buds ................. Asplenium raddianum

                              • 96. Apex of the lamina with proliferous buds ................. Asplenium kunzeanum

        • 65. Sori not linear

          • 97. Sori acrostichoid

            • 98. Venation anastomosing

              • 99. Fronds 2-4 m long; spores trilete ................. Acrostichum danaeifolium

              • 99. Fronds smaller than 2 m long; spores monolete

                • 100. Pinnae articulate to the rachis ................. Mickelia scandens

                • 100. Pinnae not articulate to the rachis

                  • 101. Sterile pinna with basiscopic side excavate; veins joined by a submarginal vein (inconspicuous in dry material) ................. Olfersia cervina

                  • 101. Sterile pinna with basiscopic and acroscopic sides conform; veins conspicuously areolate ................. Bolbitis serratifolia

            • 98. Venation free

              • 102. Lamina 1-pinnate; pinnae entire articulate with the rachis ................. Lomariopsis marginata

              • 102. Lamina 1-3-pinnate-pinnatisect; pinnae pinnate or more divided not articulate to the rachis

                • 103. Stem scales with entire margins and recurved base; proximal pinnae 3-pinnate-pinnatisect ................. Polybotrya cylindrica

                • 103. Stem scales with eroded margins to slightly denticulate and base not recurved; proximal pinnae pinnate-pinnatisect ................. Polybotrya semipinnata

          • 97. Sori not acrostichoid

            • 104. Sporangia gathered in synangium or in spikes

              • 105. Plants terrestrial; rhizome fleshy and protected by amilaceous stipules; sporangia in synangium ................. Danaea geniculata

              • 105. Plants climbing; rhizome long-creeping without stipules; sporangia in spikes ................. Lygodium volubile

            • 104. Sporangia not gathered in synangium or spikes

              • 106. Pair of fertile pinnae modified in spike; sporangia pyriform with apical annulus

                • 107. Terminal pinna conform; equilateral pinna base; anastomosing veins ................. Anemia phyllitidis

                • 107. Terminal pinna pinnatifid; pinna base not equilateral; free veins ................. Anemia mandioccana

              • 106. Pair of fertile pinnae not modified in spike; sporangium globose with oblique, lateral or vertical annulus

                • 108. Sporangium with oblique annulus

                  • 109. Fronds 3-4-pinnate-pinnatifid; rhizome erect and stout with golden hairs, 4-10 mm long; plants subarborescent ................. Lophosoria quadripinnata

                  • 109. Fronds dichotomously divided (pinnae furcate); rhizome creeping with scales or hairs (up to 4 mm long); plants herbaceous

                    • 110. Buds protected by hairs; veins 2-4-furcate ................. Gleichenella pectinata

                    • 110. Buds protected by scales; veins one time furcate

                      • 111. Axes scales patent; segments > 1.5 cm long ................. Sticherus nigropaleaceus

                      • 111. Axes scales appressed; segments <1.5 cm long ................. Sticherus bifidus

                • 108. Sporangium pedicelate with annulus vertical interrupted by the pedicel

                  • 112. Spores with chlorophyll

                    • 113. Petiole and lamina glabrous, lacking brown setae ................. Cochlidium serrulatum

                    • 113. Petiole and lamina conspicuous with brown setae and hyaline hairs

                      • 114. Stem scales clathrate ................. Melpomene pilosissima

                      • 114. Stem scales not clathrate

                        • 115. Segments veins pinnate ................. Terpsichore chrysleri

                        • 115. Segments veins simple or only one in the acroscopic branch ................. Moranopteris achilleifolia

                  • 112. Spores without chlorophyll

                    • 116. Sporangia sparse on the abaxial lamina surface protected by whitish wax ................. Ptyrogramma calomelanos

                    • 116. Sporangium gathered in defined sori and the lamina lacking white wax

                      • 117. Lamina 2-pinnate; sori oblong

                        • 118. Fronds large (1-2 m long); sori abaxial ................. Didymochlaena truncatula

                        • 118. Fronds small (not exceed 1 m long); sori marginal ................. Adiantum windischii

                      • 117. Lamina 1-pinnate, sori round, not elongate

                        • 119. Pinnae articulate to the rachis

                          • 120. Indusium reniform; lamina glabrous abaxially ................. Nephrolepis cordifolia

                          • 120. Indusium orbicular; lamina with scales and/or hairs abaxially, the scales fimbriate, the hairs catenate

                            • 121. Costa adaxially with hairs catenate ................. Nephrolepis biserrata

                            • 121. Costa adaxially without hairs or with sparse scales ................. Nephrolepis rivularis

                        • 119. Pinnae not articulate to the rachis

                          • 122. Costa not sulcate adaxially

                            • 123. Veins anastomosing ................. Tectaria incisa

                            • 123. Veins free

                              • 124. Petiole with two vascular bundles at base; lamina pubescent, the hairs acicular and septate ................. Macrothelypteris torresiana

                              • 124. Petiole with more than vascular bundles at base; lamina pubescent, the hairs catenate or clavate

                                • 125. Rachis adaxially with two prominent edges; clavate hairs on the adaxial surface of the axis ................. Lastreopsis amplissima

                                • 125. Rachis adaxially lacking prominent edges, catenate hairs on the adaxial axis

                                  • 126. Rachis and costae lacking scales ................. Ctenitis deflexa

                                  • 126. Rachis and costae with clathrate scales ................. Ctenitis submarginalis

                          • 122. Costa sulcate adaxially

                            • 127. Veins clavate at apex, ending before the lamina margin; lamina with internal glands punctuated and translucent

                              • 128. Lamina 1-pinnate-pinatissect ................. Stigmatopteris caudata

                              • 128. Lamina 1-pinnate, entire pinnae with crenate margin ................. Stigmatopteris heterocarpa

                            • 127. Veins not clavate at apex, ending at margin of the lamina; lamina without internal glands

                              • 129. Lamina 3 or 4 pinnate; indusium double (adaxially formed by the green laminar tissue and abaxially scarious and slender); spores trilete ................. Saccoloma brasiliense

                              • 129. Lamina 2-pinnate; indusium single or absent; spores monolete

                                • 130. Lamina 1-pinnate; venation anastomosing, meniscioid

                                  • 131. Pedicel of the sporangium with setiform hairs ................. Thelypteris longifolia

                                  • 131. Pedicel of the sporangium without setiform hairs

                                    • 132. Lamina glabrous abaxially; capsule of the sporangium with setiform hairs ................. Thelypteris angustifolia

                                    • 132. Lamina pubescent abaxially; capsule of the sporangium glabrous ................. Thelypteris salzmannii

                                • 130. Lamina 1-pinnate-pinnatifid or 1-pinnate-pinnatisect; venation free or only the proximal veins of the adjacent segments anastomosing (not meniscioid)

                                  • 133. Proximal pinna greater than or with the same size of the medial ones, or reduced, with proximal veins of the adjacent segments joining in the sinus or below the sinus (subg. Cyclosorus) ................. Thelypteris interrupta

                                  • 133. Proximal pinnae smaller than the medial ones, gradually or abruptly reduced, with proximal veins of the adjacent segments joining to the margin above the sinus (subg. Amauropelta)

                                    • 134. Glandular hairs absent on the laminar tissue and/or veins, costa and margins ................. Thelypteris eriosora

                                    • 134. Glandular hairs present on the laminar tissue and/or veins, costa, and margins

                                      • 135. Costa of the segments lacking scales abaxially; aerophores absent ................. Thelypteris opposita

                                      • 135. Costae of the segments with inconspicuous fimbriate scales; aerophores present on the base of the pinnae abaxially ................. Thelypteris metteniana

Publication Dates

  • Publication in this collection
    2016

History

  • Received
    03 Dec 2015
  • Reviewed
    16 Aug 2016
  • Accepted
    13 Sept 2016
Instituto Virtual da Biodiversidade | BIOTA - FAPESP Departamento de Biologia Vegetal - Instituto de Biologia, UNICAMP CP 6109, 13083-970 - Campinas/SP, Tel.: (+55 19) 3521-6166, Fax: (+55 19) 3521-6168 - Campinas - SP - Brazil
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