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Ferns and Lycophytes from the Estação Ecológica Serra Geral do Tocantins: a contribution to the flora of the Jalapão, Brazil

Abstract

This study contributes to the flora of ferns and lycophytes, also referred to as pteridophytes, from the Estação Ecológica Serra Geral do Tocantins (EESGT), which is part of the Jalapão region in Tocantins. Although Jalapão is one of the largest protected areas in the Cerrado vegetation of Northern Brazil, its biodiversity has, thus far, been poorly reported in the literature. Therefore, fieldwork was recently carried out at EESGT in different habitats. Our collections and data from digital repositories included 31 ferns and four lycophyte species belonging to 20 genera of 15 families. Despite occupying only a small fraction of the landscape, forests concentrate most pteridophyte diversity, reinforcing their importance for the conservation of this group within the Cerrado. Eleven species are new records for Tocantins, one is new for Bahia, and one was recently described (Anemia areniticola). In addition to a list of all taxa, we provide illustrations and an identification key to encourage further studies on this often-neglected component of Cerrado flora.

Key words:
Cerrado rupestre; forest; protected areas; pteridophytes; savanna

Resumo

Este estudo é uma contribuição à flora de samambaias e licófitas, também conhecidas como pteridófitas, da Estação Ecológica Serra Geral do Tocantins (EESGT), que faz parte da região do Jalapão no Tocantins. O Jalapão é uma das maiores áreas protegidas da vegetação do Cerrado do Norte do Brasil, mas com poucas informações sobre sua biodiversidade até o momento. Os trabalhos de campo foram realizados na EESGT, em diferentes habitats. Nossas coletas e dados de repositórios digitais resultaram em 31 samambaias e quatro espécies de licófitas, pertencentes a 20 gêneros de 15 famílias. Apesar de ocuparem uma pequena fração da paisagem, as florestas concentram a maior parte da diversidade de pteridófitas, reforçando sua importância para a conservação do grupo no Cerrado. Onze espécies são novos registros para o Tocantins, uma para a Bahia, e uma espécie foi recentemente descrita (Anemia arenticola). Além de uma lista com todos os táxons, também fornecemos ilustrações e uma chave de identificação para incentivar novos estudos sobre esse componente frequentemente negligenciado da flora do Cerrado.

Palavras-chave:
Cerrado rupestre; floresta; unidades de conservação; pteridófitas; savana

Introduction

Ferns and lycophytes, popularly known as pteridophytes, are cosmopolitan plant groups that encompass diverse life forms with adaptive mechanisms allowing them to inhabit various ecosystems. The greatest diversity of species occurs in the tropics (Jermy 1990Jermy AC (1990) Conservation of Pteridophytes. In: Kramer KU & Green PS (eds.) The Pteridophytes and Gymnosperms. The families and genera of vascular plants. Vol. 1. Springer, Berlin, Heidelberg. 14p. <https://doi.org/10.1007/978-3-662-02604-5_4>.
https://doi.org/10.1007/978-3-662-02604-...
; Sharpe & Mehltreter 2010Sharpe JM & Mehltreter K (2010) Ecological insights from fern population dynamics. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern Ecology. Cambridge University Press, Cambridge. Pp. 61-110.; Tryon & Tryon 1982Tryon RM & Tryon AF (1982) Ferns and allied plants: with special reference to Tropical America. Springer, New York. 896p. <https://doi.org/10.1007/978-1-4613-8162-4>.
https://doi.org/10.1007/978-1-4613-8162-...
; Zuquim et al. 2008Zuquim G, Costa FRC, Prado J & Tuomisto H (2008) Guide to the ferns and lycophytes of REBIO Uatumã - Central Amazonia. Átemma Design Editorial, Manaus. 316p.). Brazil has 1,411 species of ferns and lycophytes, of which 524 are endemics (BFG 2022BFG - The Brazil Flora Group (2022) Brazilian Flora 2020: Leveraging the power of a collaborative scientific network. Taxon 71: 178-198. <https://doi.org/10.1002/tax.12640>
https://doi.org/10.1002/tax.12640...
). Although most species of pteridophytes are found in the Amazon and Atlantic forests, the Cerrado of Central Brazil is also an important region for these plant groups, including about 320 species, in other words, 22.6% of the national flora (BFG 2022BFG - The Brazil Flora Group (2022) Brazilian Flora 2020: Leveraging the power of a collaborative scientific network. Taxon 71: 178-198. <https://doi.org/10.1002/tax.12640>
https://doi.org/10.1002/tax.12640...
). The lower species richness in the Cerrado, which is dominated by open habitats under a seasonally dry climate, reflects the ecological preference of most pteridophyte groups for moist and forested areas. Nevertheless, many species can be found in wet environments associated with water bodies, such as gallery forests and swamps (Colli et al. 2004Colli AMT, Souza SA, Salino A, Lucca ALT & Silva RT (2004) Pteridófitas do Parque Estadual de Vassununga, Santa Rita do Passa Quatro (SP), Brasil. Gleba Pé-de-Gigante. Revista do Instituto Florestal 16: 121-127.; Fernandes et al. 2022Fernandes RS, Silva LR, Oliveira SS, Ottoni FP & Pietrobom MR (2022) Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotropica 22: e20211273. <https://doi.org/10.1590/1676-0611-bn-2021-1273>.
https://doi.org/10.1590/1676-0611-bn-202...
; Kreutz et al. 2016Kreutz C, Athayde Filho FP & Sanchez M (2016) Spatial and seasonal variation in the species richness and abundance of ferns and lycophytes in gallery forests of Cerrado in Central Brazil. Brazilian Journal of Botany 39: 315-326. <https://doi.org/10.1007/s40415-015-0236-9>.
https://doi.org/10.1007/s40415-015-0236-...
; Miguez et al. 2013Miguez FA, Kreutz C & Athayde Filho FP (2013) Samambaias e Licófitas em quatro Matas de Galeria do município de Nova Xavantina, Mato Grosso, Brasil. Pesquisas, Botânica 64: 243-258.; Nunes & Labiak 2021Nunes MG & Labiak PH (2021) Ferns and lycophytes of the Cerrado State Park, Paraná, Brazil. Rodriguésia 72: e00192020. <https://doi.org/10.1590/2175-7860202172096>.
https://doi.org/10.1590/2175-78602021720...
). On the other hand, some dry-adapted lineages have successfully colonized open habitats of the Cerrado, such as species of Anemia (Hietz 2010Hietz P (2010) Fern adaptations to xeric environments. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 140-176.; Mickel 2016Mickel JT (2016) Anemia: Anemiaceae. New York Botanical Garden Press, New York. Pp. 1-182.), a genus especially diverse in Central Brazil (Mickel 2016Mickel JT (2016) Anemia: Anemiaceae. New York Botanical Garden Press, New York. Pp. 1-182.). These open habitats harbor the largest number of Cerrado endemics (Prado et al. 2015Prado J, Sylvestre LS, Labiak PH, Windisch PG, Salino A, Barros ICL, Hirai RY, Almeida TE, Santiago ACP, Kieling-Rubio MA, Pereira AFN, Øllgaard B, Ramos CGV, Mickel JT, Dittrich VAO, Mynssen CM, Schwartsburd PB, Condack JPS, Pereira JBS & Matos FB (2015) Diversity of ferns and lycophytes in Brazil. Rodriguésia 66: 1073-1083. <https://doi.org/10.1590/2175-7860201566410>.
https://doi.org/10.1590/2175-78602015664...
), as well as most new species of pteridophytes recently described for the biome (Hirai et al. 2018Hirai RY, Cruz R & Prado J (2018) A new species of Hemionitis (Pteridaceae) from central Brazil. Willdenowia 48: 371. <https://doi.org/10.3372/wi.48.48305>.
https://doi.org/10.3372/wi.48.48305...
; Labiak et al. 2018Labiak PH, Mickel JT & Matos FB (2018) Anemia paripinnata (Anemiaceae), a new species from Central Brazil. American Fern Journal 108: 1-6. <https://doi.org/10.1640/0002-8444-108.1.1>.
https://doi.org/10.1640/0002-8444-108.1....
; Mickel 2016Mickel JT (2016) Anemia: Anemiaceae. New York Botanical Garden Press, New York. Pp. 1-182.; Oliveira & Schwartsburd 2021Oliveira AGS & Schwartsburd PB (2021) Two new species of Doryopteris (Pteridaceae) from Brazil. American Fern Journal 111: 35-42. <https://doi.org/10.1640/0002-8444-111.1.35>.
https://doi.org/10.1640/0002-8444-111.1....
; Pereira & Prado 2022Pereira JBS & Prado J (2022) Two new endemic tetraploid species of the genus Isoëtes from the Brazilian Savanna. Systematic Botany 47: 301-305. <https://doi.org/10.1600/036364422X16512564801704>.
https://doi.org/10.1600/036364422X165125...
).

Documenting the diversity of pteridophytes in the Cerrado has been challenging given the low number of floristic surveys, so most biome regions still need to be sampled. One of these regions is the Jalapão, in the northeastern portion of the Cerrado, which encompasses the most significant remnants of Cerrado’s native vegetation, including an extensive mosaic of natural reserves (Alencar et al. 2020Alencar A, Shimbo JZ, Lenti F, Marques CB, Zimbres B, Rosa M, Arruda V, Castro I, Ribeiro JPFM, Varela V, Alencar I, Piontekowski V, Ribeiro V, Bustamante MMC, Sano EE & Barroso M (2020) Mapping three decades of changes in the Brazilian Savanna native vegetation using landsat data processed in the Google Earth engine platform. Remote Sensing 12: 924. <https://doi.org/10.3390/rs12060924>.
https://doi.org/10.3390/rs12060924...
). Despite some recent progress in documenting the flora of Jalapão (Antar & Sano 2019Antar GM & Sano PT (2019) Angiosperms of dry grasslands and savannahs of Jalapão, the largest conserved Cerrado area in Brazil. Rodriguésia 70: e04002017. <https://doi.org/10.1590/2175-7860201970070>
https://doi.org/10.1590/2175-78602019700...
; Proença et al. 2002Proença CEB, Sampaio AB, Silva LH, Milhomens LC, Simon, MF, Simpson PL & Farias R (2002) Relatório de Botânica. In: Arruda MB & von Behr M (eds.) Jalapão: expedição científica e conservacionista. IBAMA, Brasília. Pp. 21-28.; Santana & Simon 2022Santana JCO & Simon MF (2022) Plant diversity conservation in an agricultural frontier in the Brazilian Cerrado. Biodiversity and Conservation 31: 667-681. <https://doi.org/10.1007/s10531-022-02356-2>.
https://doi.org/10.1007/s10531-022-02356...
; Silva et al. 2017Silva DP, Amaral AG, Bijos NR & Munhoz CBR (2017) Is the herb-shrub composition of veredas (Brazilian palm swamps) distinguishable? Acta Botanica Brasilica 32: 47-54. <https://doi.org/10.1590/0102-33062017abb0209>.
https://doi.org/10.1590/0102-33062017abb...
), most inventories have been exclusively focused on angiosperms while neglecting the diversity of ferns and lycophytes.

Therefore, we aim to fill this gap by conducting a floristic survey of the Estação Ecológica Serra Geral do Tocantins, one of the largest protected areas in the Cerrado. We present an expert-vetted checklist and provide information about habitat, photographic plates, and a key for ferns and lycophytes.

Material and Methods

Study area

The Estação Ecológica Serra Geral do Tocantins (EESGT) comprises an area of 716,306 hectares (centroid 10°51’25”S, 46°41’33”W; Fig. 1). It is included within the boundaries of four municipalities in eastern Tocantins (Almas, Mateiros, Ponte Alta do Tocantins, and Rio da Conceição) and one in western Bahia (Formosa do Rio Preto), and it is part of a mosaic of protected areas in the Jalapão region. According to Köppen’s classification, the climate corresponds to type Aw (Alvares et al. 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM & Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728. <https://doi.org/10.1127/0941-2948/2013/0507>
https://doi.org/10.1127/0941-2948/2013/0...
) with dry winters, an average annual temperature of 24-26 °C, and average annual precipitation of 1,300 mm (data from Mateiros Weather Station; <https://www.snirh.gov.br/hidroweb/serieshistoricas>). Sequences of sedimentary plateaus and terraces are the dominant landforms in the landscape, where altitudes range from 400 m in the west to 730 m in the east (Villela & Nogueira 2011Villela FNJ & Nogueira C (2011) Geologia e geomorfologia da estação ecológica Serra Geral do Tocantins. Biota Neotropica 11: 217-229. <https://doi.org/10.1590/S1676-06032011000100023>.
https://doi.org/10.1590/S1676-0603201100...
).

Figure 1
Location of the Estação Ecológica Serra Geral do Tocantins (EESGT) and density of collections of vascular plants. Each hexagonal grid cell has an area of 28.9 km2, and colors represent the count of botanical records per grid cell (1192 total, 1116 angiosperms, and 76 ferns and lycophytes). Ferns and lycophytes: records from field expeditions (54 records; circles); records from digital repositories (22 records; triangles). Brazilian states: BA (Bahia), TO (Tocantins). Map produced with QGIS, version 3.10 (QGIS Development Team 2019QGIS Development Team (2019) QGIS Geographic Information System. Available at <http://qgis.org>. Access on 7 April 2021.
http://qgis.org...
).

Vegetation in EESGT is dominated by open formations of grasslands and savannas, which cover around 98% of the reserve, whereas forests represent only 2% of the area (Franke et al. 2018Franke J, Barradas ACS, Borges MA, Costa MM, Dias PA, Hoffmann AA, Orozco Filho JC, Melchiori AE & Siegert F (2018) Fuel load mapping in the Brazilian Cerrado in support of integrated fire management. Remote Sensing of Environment 217: 221-232. <https://doi.org/10.1016/j.rse.2018.08.018>.
https://doi.org/10.1016/j.rse.2018.08.01...
). According to the classification of Ribeiro & Walter (2008)Ribeiro JF & Walter BMT (2008) As principais fitofisionomias do Cerrado. In: Sano SM, Almeida SP & Ribeiro JF (eds.) Cerrado: ecologia e flora. Embrapa Cerrados, Planaltina. Pp. 151-212., vegetation types in the EESGT include savanna and grassland physiognomies (Campo limpo, Campo sujo, Cerrado ralo, Cerrado rupestre, and Vereda), as well as riverine forests (Mata ciliar and Mata de galeria), Figs. 2 and 3.

Figure 2
a-g. Vegetation types found in the Estação Ecológica Serra Geral do Tocantins (EESGT) - a. Vereda; b. Mata Ciliar at “Rio Novo”; c. Vereda; d. vegetation mosaic with Vereda in the foreground and Mata de galeria in the background; e. Mata de galeria at “Rio Verdinho”; f. “Cachoeira da Fumaça”; g. detail of Mata ciliar downstream of “Cachoeira da Fumaça” and its conspicuous water vapor during the rainy season. (Photographs: a-c, e-g. M. Figueira & B. Schindler; d. S.E. Noronha).

Figure 3
a-g. Vegetation types found in the Estação Ecológica Serra Geral do Tocantins (EESGT) - a. predominant physiognomy with a significant extension of the vegetation mosaic of Campo sujo and Cerrado ralo; b. Campo sujo in the foreground; c. transition between Campo sujo (right) and Campo limpo úmido (left) near “Lagoa da Serra”; d. Cerrado ralo; e. Cerrado ralo with large rocky blocks, Formosa do Rio Preto, Bahia; f. Campo limpo in the foreground; Cerrado ralo and testimonial hills in the background; g. Cerrado rupestre at “Morro do Fumo”. (Photographs: a-d, f-g. M. Figueira & B. Schindler; e. S.E. Noronha).

Fieldwork and botanical identification

Five expeditions were carried out between 2018 and 2022 during dry and rainy seasons, totaling 26 field days. Surveys encompassed all habitats in the EESGT (Figs. 2-3) and all life forms of vascular plants. The density of collections of all groups of vascular plants (1192 collections) sampled in the EESGT provides a measure of sampling effort (Fig. 1). After the usual herborization process (Fidalgo & Bononi 1984Fidalgo O & Bononi VLR (1984) Técnicas de coleta, preservação e herborização de material botânico. Instituto de Botânica, São Paulo. 61p.), specimens were deposited in the CEN herbarium, and duplicates were sent to herbaria CESJ and UPCB (acronyms according to Thiers, continuously updatedThiers B (continuously updated) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at <http://sweetgum.nybg.org/science/ih/>. Access on 12 September 2022.
http://sweetgum.nybg.org/science/ih/...
). A herbarium voucher was selected to represent each species in the checklist. Identification was made using taxonomic revisions and keys provided in the Flora e Funga do Brasil 2022Flora e Funga do Brasil 2022 (continuously updated) Jardim Botânico do Rio de Janeiro. Available at <https://floradobrasil.jbrj.gov.br/FB245>. Access on 12 September 2022.
https://floradobrasil.jbrj.gov.br/FB245...
(continuously updated), and by comparisons with specimens already deposited in CEN and CESJ collections. Digital images of specimens, as determined by specialists and/or nomenclatural types available in virtual herbaria of the repositories SpeciesLink (CRIA 2022CRIA (2022) Centro de Referência e Informação Ambiental. Specieslink - simple search. Available at <https://specieslink.net/search/>. Access on 12 September 2022.
https://specieslink.net/search/...
), Global Biodiversity Information Facility (GBIF 2022GBIF.org (2022) GBIF Home Page. Global Biodiversity Information Facility. Available at <https://www.gbif.org/>. Access on 12 September 2022.
https://www.gbif.org/...
), and Reflora (2022)REFLORA (2022) Reflora - Herbário Virtual. Available at <http://reflora.jbrj.gov.br/reflora/herbarioVirtual/ConsultaPublicoHVUC/ConsultaPublicoHVUC.do;jsessionid=F2131AC6CCEDF3F5209B9CE35AAAE9F3?http://reflora.jbrj.gov.br/reflora/herbarioVirtual/>. Access on 12 June 2022.
http://reflora.jbrj.gov.br/reflora/herba...
, were also consulted. When necessary, images or duplicates were sent for identification by specialists. The nomenclature of scientific names followed IPNI (2022)IPNI (2022) International Plant Names Index. The Royal Botanic Gardens, Kew, Harvard University Herbaria & Libraries, and Australian National Herbarium. Available at <http://www.ipni.org>. Access on 15 December 2022.
http://www.ipni.org...
, and the morphological terms used in the identification key followed Beentje (2010)Beentje H (2010) The Kew plant glossary: an illustrated dictionary of plant terms. Royal Botanic Gardens, Kew, Richmond, Surrey. 160p. and Lellinger (2002)Lellinger DB (2002) A modern multilingual glossary for taxonomic pteridology. Pterodologia 3 A. American Fern Society, Washington. 264p.. The order in which the species are presented in the photographic plates follows the sequence they appear in the dichotomous key.

Additional data search

To complement the list obtained from our field expeditions, an additional search for taxa was carried out in GBIF (<https://www.gbif.org/>) and SpeciesLink (<https://specieslink.net/search/>). Searches of botanical records were conducted in September 2022, as follows: First, municipalities in Tocantins (Almas, Mateiros, Ponte Alta do Tocantins, and Rio da Conceição) and Bahia (Formosa do Rio Preto) were included in accordance with data in the repository SpeciesLink. Second, SpeciesLink and GBIF repository records located within the EESGT area plus a 5 km buffer were retained. Third, all retrieved records were checked individually for the precision of geographic coordinates and/or mistakes to ensure they corresponded to genuine collections made in the study area. Finally, locality notes containing the terms “Jalapão”, “Estação Ecológica Serra Geral do Tocantins”, “estação ecológica”, “ESEC”, “fumaça”, “Rio Balsa”, “vila dos Prazeres”, and “Rio Peixinho”, among others, were considered, even if geographic coordinates were absent or mistaken. Records obtained from online databases were checked case-by-case for taxonomic identity. When confirmation was not possible, specimens were disregarded.

Detection of new occurrence records

We also checked for new occurrence records for Bahia and Tocantins. A taxon could be considered a new record if it was not previously mentioned for Bahia and Tocantins in Flora e Funga do Brasil 2022Flora e Funga do Brasil 2022 (continuously updated) Jardim Botânico do Rio de Janeiro. Available at <https://floradobrasil.jbrj.gov.br/FB245>. Access on 12 September 2022.
https://floradobrasil.jbrj.gov.br/FB245...
(continuously updated). In addition, a bibliographic search was conducted for relevant floristic surveys, taxonomic reviews, and regional floras, as well as searches in GBIF and SpeciesLink databases, to make sure that collections comprise genuine new occurrence records.

Results and Discussion

Field expeditions at EESGT resulted in 54 collections of 29 species of ferns and four lycophytes. Secondary data from online repositories included 22 records and two species not recorded in our field surveys (Fig. 1). A total of 35 species belonging to 15 families and 20 genera are compiled for the EESGT (see Tab. 1 for all species and authors), including one taxon identified at the genus level (Blechnum sp.). Species are illustrated in photographic plates (Figs. 4-12), and can be determined with the help of the dichotomous key presented below.

Table 1
Checklists of Ferns and Lycophytes recorded at the Estação Ecológica Serra Geral do Tocantins. New occurrence records: TO = Tocantins; BA = Bahia. (*) = second record for Tocantins. Substrate: Rup = rupicolous; Ter = Terrestrial. Physiognomies sensuRibeiro & Walter (2008)Ribeiro JF & Walter BMT (2008) As principais fitofisionomias do Cerrado. In: Sano SM, Almeida SP & Ribeiro JF (eds.) Cerrado: ecologia e flora. Embrapa Cerrados, Planaltina. Pp. 151-212. CUm = Campo úmido; CRu = Cerrado rupestre; MC = Mata ciliar; MG = Mata de galeria; Ve = Vereda.

Figure 4
a-f. Lycophytes of Estação Ecológica Serra Geral do Tocantins (EESGT) - a. Palhinhaea camporum - erect stem and detail of pendent strobili; b-c. Lycopodiella longipes - b. erect strobili; c. prostrate stem; d-e. Selaginella radiata - d. habit; e. detail of the discolored laminar surface; f. S. flexuosa - habit with prostrate stem. (Photographs: M. Figueira & B. Schindler).

Figure 5
a-f. Ferns of Estação Ecológica Serra Geral do Tocantins (EESGT) - a-b. Dicranopteris flexuosa - a. dichotomous ramifications; b. gem detail with accessory pinnae (arrow); c-d. Schizaea elegans - c. lamina; d. detail of sporangiophores on the margin; e-f. Anemia areniticola - e. habit; f. detail of sporangiophores on basal pinnae (arrow). (Photographs: M. Figueira & B. Schindler).

Species recorded comprise different life forms, ranging from small rupicolous taxa, such as Anemia spp., Cheilanthes pohliana, and Mineirella eriophora, to forest dwelling tree ferns (Cyathea spp.). Most listed pteridophytes comprised terrestrial species (18 spp.), followed by rupicolous taxa (12 spp.), while five species were classified as both rupicolous and terrestrial. No epiphytic species were found in the area. Although epiphytes are common in rainforests, they seem to be rare in sites located in regions with seasonal climates (Fernandes et al. 2010Fernandes RS, Conceição GM, Costa JM & Paula-Zárate EL (2010) Samambaias e licófitas do município de Caxias, Maranhão, Brasil. Boletim do Museu Paraense Emílio Goeldi Ciências Naturais 5: 345-356.; Lehn et al. 2020Lehn CR, Gonzatti F & Arana MD (2020) Samambaias e licófitas dos Cerros do Tigre e Palomas, província biogeográfica do Pampa, estado do Rio Grande do Sul, Brasil. Hoehnea 47: e762019. <https://doi.org/10.1590/2236-8906-76/2019>.
https://doi.org/10.1590/2236-8906-76/201...
; Miguez et al. 2013Miguez FA, Kreutz C & Athayde Filho FP (2013) Samambaias e Licófitas em quatro Matas de Galeria do município de Nova Xavantina, Mato Grosso, Brasil. Pesquisas, Botânica 64: 243-258.; Xavier et al. 2012Xavier SRS, Barros ICL & Santiago ACP (2012) Ferns and lycophytes in Brazil’s semi-arid region. Rodriguésia 63: 483-488. <https://doi.org/10.1590/S2175-78602012000200021>.
https://doi.org/10.1590/S2175-7860201200...
). However, epiphytic ferns have been registered in Cerrado gallery forests. For example, Oliveira & Arcela (2014)Oliveira RP & Arcela V (2014) Distribuição vertical e valor de importância das epífitas vasculares da Reserva Biológica do Guará, Brasília, DF. Heringeriana 8: 20-31. <https://doi.org/10.17648/heringeriana.v8i1.93>.
https://doi.org/10.17648/heringeriana.v8...
found several individuals belonging to four species of Polypodiaceae in a survey of epiphytes in a gallery forest sampled in Distrito Federal.

Pteridophyte occurrence in different habitats within the EESGT

Although open formations, consisting of grasslands and savannas, dominate the landscape within the EESGT, the largest number of species were recorded in forests and humid environments (Tab. 1), predominantly in the understory, where pteridophytes occupy several microenvironments. A predominance of pteridophytes in wet forests (Mata de galeria and Mata cCiliar) has been reported in other studies in the Cerrado (Colli et al. 2004Colli AMT, Souza SA, Salino A, Lucca ALT & Silva RT (2004) Pteridófitas do Parque Estadual de Vassununga, Santa Rita do Passa Quatro (SP), Brasil. Gleba Pé-de-Gigante. Revista do Instituto Florestal 16: 121-127.; Fernandes et al. 2022Fernandes RS, Silva LR, Oliveira SS, Ottoni FP & Pietrobom MR (2022) Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotropica 22: e20211273. <https://doi.org/10.1590/1676-0611-bn-2021-1273>.
https://doi.org/10.1590/1676-0611-bn-202...
; Kreutz et al. 2016Kreutz C, Athayde Filho FP & Sanchez M (2016) Spatial and seasonal variation in the species richness and abundance of ferns and lycophytes in gallery forests of Cerrado in Central Brazil. Brazilian Journal of Botany 39: 315-326. <https://doi.org/10.1007/s40415-015-0236-9>.
https://doi.org/10.1007/s40415-015-0236-...
; Miguez et al. 2013Miguez FA, Kreutz C & Athayde Filho FP (2013) Samambaias e Licófitas em quatro Matas de Galeria do município de Nova Xavantina, Mato Grosso, Brasil. Pesquisas, Botânica 64: 243-258.; Nunes & Labiak 2021Nunes MG & Labiak PH (2021) Ferns and lycophytes of the Cerrado State Park, Paraná, Brazil. Rodriguésia 72: e00192020. <https://doi.org/10.1590/2175-7860202172096>.
https://doi.org/10.1590/2175-78602021720...
). Compared to those studies, the species number reported here is relatively low, considering the expanded size of the EESGT.

It can be argued that the low species richness reported here resulted from undersampling. Indeed, the vast area of the EESGT represents a challenge to comprehensive sampling. However, we were still able to conduct an intensive search for ferns and lycophytes in widely distributed sites within the EESGT, including 15 collection sites located in wet habitats highly suitable for pteridophytes (Mata ciliar, Mata de galeria, Vereda, Campo úmido; Figs. 2; 3c). Therefore, we believe that our sampling effort was adequate and enabled the collection of representative samples of local flora. A more likely explanation for the low diversity of pteridophytes in the EESGT, compared to other surveys in the Cerrado, is the paucity of suitable habitats. Grasslands and savannas on deep sandy soils, the dominant habitat in the EESGT, are poor in pteridophyte species, possibly owing to a lack of moisture during the dry season. On the other hand, more suitable microhabitats, including wet forests and rocky outcrops (Cerrado rupestre), where most species were found, comprise only a small fraction of the landscape.

One spot of high diversity of pteridophytes in the area was the “Cachoeira da Fumaça”, a waterfall of the Balsas River located on the southwestern edge of the EESGT (red cell in Figs. 1 and 2f-g), which alone contributed 11 species to the list. That waterfall continuously sends water towards the forest downstream in a gorge, producing a moist environment where several typical ombrophilous species, including ferns, thrive. Pteridophyte diversity in this locality includes large-sized tree ferns, such as Cyathea spp. (Fig. 12), as well as rupicolous (Blechnum sp., Danaea leprieurii; Fig. 10; Selaginella spp., Fig. 4) and terrestrial species (Lindsaea spp., Fig. 9; Meniscium maxonianum, Fig. 11f-g; Schizaea elegans, Fig. 5c-d). As far as we know, “Cachoeira da Fumaça” is the only locality where Cyathea myriotricha (Fig. 13a-b) and Cyclodium meniscioides (Fig. 11a-c) were recorded throughout the entirety of Tocantins state. This habitat sharply contrasts with the seasonally dry grasslands surrounding it, making the site an island of humidity, even during the dry season. The high number of species recorded in the “Cachoeira da Fumaça” is probably associated with this unique and heterogeneous microclimate related to humidity and shade (forest stratification) gradients, as well as the diversity of substrates and high abundance of litter. Indeed, the high species richness of ferns is associated with environmental heterogeneity in Cerrado gallery forests (Kreutz et al. 2016Kreutz C, Athayde Filho FP & Sanchez M (2016) Spatial and seasonal variation in the species richness and abundance of ferns and lycophytes in gallery forests of Cerrado in Central Brazil. Brazilian Journal of Botany 39: 315-326. <https://doi.org/10.1007/s40415-015-0236-9>.
https://doi.org/10.1007/s40415-015-0236-...
).

On the other hand, species like Lycopodiella longipes, Palhinhaea camporum, Pityrogramma calomelanos, and Telmatoblechnum serrulatum (Figs. 4; 10) were strongly associated with open vegetation on seasonally flooded hydromorphic soils, such as “Campos úmidos and Veredas”, typical of habitats found along watercourses and springs in the EESGT (Fig. 2). However, these same species were reported in similarly poorly-drained environments in other regions (Athayde Filho & Agostinho 2005Athayde Filho FP & Agostinho AA (2005) Pteridoflora de duas veredas no município de Campinápolis, Mato Grosso, Brasil. Pesquisas, Botânica 56: 145-160.; Fernandes et al. 2022Fernandes RS, Silva LR, Oliveira SS, Ottoni FP & Pietrobom MR (2022) Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotropica 22: e20211273. <https://doi.org/10.1590/1676-0611-bn-2021-1273>.
https://doi.org/10.1590/1676-0611-bn-202...
; Zambiase et al. 2016Zambiase RM, Resende ILM, Kreutz C & Athayde Filho FP (2016) Análise ecoflorística de samambaias e licófitas em mata de galeria inundável e vereda, Quirinópolis, Goiás, Brasil. Pesquisas, Botânica 69: 169-181.), as well as Veredas of the EESGT (Silva et al. 2017Silva DP, Amaral AG, Bijos NR & Munhoz CBR (2017) Is the herb-shrub composition of veredas (Brazilian palm swamps) distinguishable? Acta Botanica Brasilica 32: 47-54. <https://doi.org/10.1590/0102-33062017abb0209>.
https://doi.org/10.1590/0102-33062017abb...
).

We also highlight a few species able to tolerate the dry and nutrient-poor soils of Cerrado environments. For example, Anemia, Cheilanthes, and Mineirella species were found in open habitats and on rocky outcrops and can be classified as xeromorphic (Figs. 5; 6). These small-sized ferns were often found in arenitic slopes and outcrops (Cerrado rupestre) growing on sandy soil in pockets and crevices (Fig. 3). To compensate for the xeric conditions, these species have efficient mechanisms for obtaining nutrients, the ability to dry out and become latent during the dry season, and the ability to resprout during the wet season from underground rhizomes that can withstand fire (Benzing 2004Benzing DH (2004) CHAPTER 9 - Vascular Epiphytes. In: Lowman MD & Rinker HB (eds.) Forest canopies. 2nd ed. Academic Press, San Diego. Pp. 175-211. <http://dx.doi.org/10.1016/B978-012457553-0/50014-9>
http://dx.doi.org/10.1016/B978-012457553...
; Goetz et al. 2012Goetz MNB, Fraga LL & Schmitt JL (2012) Florística e aspectos ecológicos de samambaias e licófitas em um parque urbano do Rio Grande do Sul, Brasil. Pesquisas, Botânica 63: 165-176.; Hietz 2010Hietz P (2010) Fern adaptations to xeric environments. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 140-176.). The occurrence of these genera in habitats generally less favorable to ferns can be facilitated by apogamy (Hietz 2010Hietz P (2010) Fern adaptations to xeric environments. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 140-176.; Moran 2012Moran RC (2012) História natural das samambaias. TECC Editora, Florianópolis. 264p.). Other studies report the occurrence of these genera in similar environments elsewhere (Santos-Silva et al. 2023Santos-Silva DL, Prado J & Eisenlohr PV (2023) Living on the edge: composition, biogeography, and conservation of ferns in rocky environments of Southern Amazonia. Brazilian Journal of Botany 46: 227-239. <https://doi.org/10.1007/s40415-022-00866-5>.
https://doi.org/10.1007/s40415-022-00866...
; Castro-Aguiar et al. 2022Castro-Aguiar PH, Fernandes RS & Prado J (2022) Pteridaceae in remnants of Cerrado in Maranhão state, Brazil. Check List 18: 1263-1278. <https://doi.org/10.15560/18.6.1263>
https://doi.org/10.15560/18.6.1263...
; Fernandes et al. 2014Fernandes JH, Kreutz C & Athayde Filho FP (2014) Samambaias em formações de Cerrado rupestre da Bacia do Rio das Mortes, Mato Grosso, Brasil. Pesquisas, Botânica 65: 217-231.; Lehn et al. 2020Lehn CR, Gonzatti F & Arana MD (2020) Samambaias e licófitas dos Cerros do Tigre e Palomas, província biogeográfica do Pampa, estado do Rio Grande do Sul, Brasil. Hoehnea 47: e762019. <https://doi.org/10.1590/2236-8906-76/2019>.
https://doi.org/10.1590/2236-8906-76/201...
; Mickel 2016Mickel JT (2016) Anemia: Anemiaceae. New York Botanical Garden Press, New York. Pp. 1-182.; Ponce & Scataglini 2021Ponce MM & Scataglini MA (2021) Phylogenetic position of South American Cheilanthes (Cheilanthoideae, Pteridaceae): advances in the generic circumscription and segregation of the new genus Mineirella. Journal of Systematics and Evolution 60: 1-15. <https://doi.org/10.1111/jse.12723>.
https://doi.org/10.1111/jse.12723...
; Xavier et al. 2012Xavier SRS, Barros ICL & Santiago ACP (2012) Ferns and lycophytes in Brazil’s semi-arid region. Rodriguésia 63: 483-488. <https://doi.org/10.1590/S2175-78602012000200021>.
https://doi.org/10.1590/S2175-7860201200...
).

Figure 12
a-h. Ferns of Estação Ecológica Serra Geral do Tocantins (EESGT) - a-b. Cyathea myriotricha - a. detail of fiddlehead and petiole; b. abaxial surface of pinna; c-e. C. pungens - c. detail of fiddlehead; d. petiole; e. abaxial surface of pinna; f-h. C. delgadii - f. detail of fiddlehead; g. petiole; h. abaxial surface of pinna. (Photographs: M. Figueira & B. Schindler).

Key to the Ferns and Lycophytes of Estação Ecológica Serra Geral de Tocantins, Brazil

  • 1. Plants with microphylls, leaves with one vein, usually up to 1 cm long 2

    • 2. Microphylls inserted in numerous series, without ligule; plants homosporous 3

      • 3. Stem erect; strobili pendulous, at the apex of the lateral branches Palhinhaea camporum (Fig. 4a)

      • 3’. Stem prostrate; strobili erect, at the apex of an erect branch Lycopodiella longipes (Fig. 4b-c)

    • 2’. Microphylls inserted in four series, with ligule; plants heterosporous 4

      • 4. Rhizophores restricted to stem base; stem decumbent to erect; discolored leaf surface Selaginella radiata (Fig. 4d-e)

      • 4’. Rhizophores distributed up to the basal half of the stem; stem prostrate to suberect; concolor leaf surface Selaginella flexuosa (Fig. 4f)

  • 1’. Plants with megaphylls, leaves multinerved, longer than 3 cm and reaching several meters in length 5

    • 5. Laminae branched dichotomously, with a bud and accessory pinnae between the bifurcations Dicranopteris flexuosa (Fig. 5a-b)

    • 5’. Laminae entire or regularly pinnate, without bud and accessory pinnae between the bifurcations 6

      • 6. Sporangiophores present (pinnae or modified portions of the laminae) 7

        • 7. Laminae flabelliform; sporangiophores located on the margin of the laminae Schizaea elegans (Fig. 5c-d)

        • 7’. Laminae of other shapes; sporangiophores located in a modified basal pinnae 8

        • 8. Abaxial surface of the laminae lanose; fertile pinnae horizontal or oblique, not fully erect 9

          • 9. Fertile pinnae shorter than the sterile; sterile pinnae glabrescent or sparsely lanose on the adaxial surface Anemia areniticola (Fig. 5e-f)

          • 9’. Fertile pinnae longer than the sterile; sterile pinnae densely lanose on the adaxial surface Anemia trichorhiza (Fig. 6a-b)

            Figure 6
            a-e. Ferns of Estação Ecológica Serra Geral do Tocantins (EESGT) - a-b. Anemia trichorhiza - a. habitat; b. laminae and detail of sporangiophores on basal pinnae (arrow); c. A. humilis - habitat and detail of laminae decreasing basiscopically (arrow); d. A. presliana - habitat and detail of laminae not decreasing basiscopically (arrow); e. A. andersonii - detail of lamina. (Photographs: M. Figueira & B. Schindler).

        • 8’. Abaxial surface of the laminae hirsute; fertile pinnae erect 10

          • 10. Laminae with ≤ 10 pairs of pinnae; petiole of fertile pinnae approximately the same length as the sterile 11

            • 11. Sterile laminae decreasing basiscopically Anemia humilis (Fig. 6c)

            • 11’. Sterile laminae not decreasing basiscopically Anemia presliana (Fig. 6d)

          • 10’. Laminae with ≥ 10 pairs of pinnae; petiole of fertile pinnae longer than the sterile Anemia andersonii (Fig. 6e)

  • 6’. Sporangiophores absent 12

    • 12. Sporangia on the margin of the laminae 13

      • 13. Sori conical, with involucres immersed in laminar tissue 14

        • 14. Laminae dimorphic Trichomanes pinnatum (Fig. 7a)

          Figure 7
          a-g. Ferns of Estação Ecológica Serra Geral do Tocantins (EESGT) - a. Trichomanes pinnatum - detail of conical sori on the margin of pinnae; b. T. pilosum - detail of conical sori on the margin of pinnae; c. T. cristatum - detail of conical sori on the margin of pinnae; d-e. Mineirella eriophora - d. habit; e. detail of the abaxial surface of the laminae; f-g. Cheilanthes pohliana - f. habit; g. detail of the abaxial surface of the lamina. (Photographs: a-b, d-g. M. Figueira & B. Schindler; c. Felipe Gonzatti).

        • 14’. Laminae monomorphic 15

          • 15. Laminae deltoid, arched or curved Trichomanes pilosum (Fig. 7b)

          • 15’. Laminae linear and erect Trichomanes cristatum (Fig. 7c)

      • 13’. Sori of other formats 16

        • 16. Laminae pinnatifid, ovate-pentagonal or pentagonal, lanose abaxially Mineirella eriophora (Fig. 7d-e)

        • 16’. Laminae 1-3 pinnate or more, glabrous or the indument of other types 17

          • 17. Pinnule hirsute, slightly revolute, sori encircling all margin Cheilanthes pohliana (Fig. 7f-g)

          • 17’. Pinnule never hirsute, flat or sinuose, never revolute, sori only on the upper margin (acroscopic) 18

            • 18. Indusia opening toward the costa or segment apex (pseudo-indusia) 19

              • 19. Laminae 1-pinnate, pinnae glabrous Adiantum deflectens (Fig. 8a-b)

                Figure 8
                a-f. Ferns of Estação Ecológica Serra Geral do Tocantins (EESGT) - a-b. Adiantum deflectens - a. habit; b. detail of pinnae; c-d. A. serratodentatum - c. lamina; d. detail of pinnules with scales and sori; e-f. A. sinuosum - e. lamina; f. detail of pinnules with sori. (Photographs: a-b. V.A.O. Dittrich; c-f. M. Figueira & B. Schindler).

              • 19’. Laminae 1-3 pinnate or more at the base, glabrous or with scales 20

                • 20. Pinnules flat, scales on abaxial surface Adiantum serratodentatum (Fig. 8c-d)

                • 20’. Pinnules slightly sinuate, glabrous on both surfaces Adiantum sinuosum (Fig. 8e-f)

            • 18’. Indusia opening toward the lamina margin 21

              • 21. Distal pinnules conspicuously smaller in size towards apex of pinnae; spores monolete Lindsaea quadrangularis (Fig. 9a-b)

                Figure 9
                a-h. Ferns of Estação Ecológica Serra Geral do Tocantins (EESGT) - a-b. Lindsaea quadrangularis - a. lamina; b. detail of pinnules with sori; c-d. L. divaricata - c. lamina; d. detail of pinnules with sori; e-f. L. stricta - e. lamina; f. detail of pinnae with sori; g-h. L. lancea - g. habit; h. detail of pinnae with sori. (Photographs: M. Figueira & B. Schindler).

              • 21’. Distal pinnules of equal or slightly reduced size towards the apex of the pinnae (or laminae 1-pinnate); spores trilete 22

                • 22. Laminae often 1-pinnate, rarely 2-pinnate or more; indusium lacerate Lindsaea stricta (Fig. 9e-f)

                • 22’. Laminae 2-pinnate or more; indusium entire 23

                  • 23. Petiole and rachis sub-terete Lindsaea divaricata (Fig. 9c-d)

                  • 23’. Petiole and rachis angulose Lindsaea lancea (Fig. 9g-h)

  • 12’. Sporangia superficial on the laminae, on the veins or parallel to the main vein 24

    • 24. Sporangia forming synangium or sori linear and parallel to the costa 25

      • 25. Petioles with pulvinus; rachis alate; synangia on the veins Danaea leprieurii (Fig. 10a-b)

        Figure 10
        a-e. Ferns of Estação Ecológica Serra Geral do Tocantins (EESGT) - a-b. Danaea leprieurii - a. rhizome, lamina, and details of pulvinus (arrow); b. rachis and detail of veins; c. Blechnum sp. - abaxial surface of lamina with sori; d. Telmatoblechnum serrulatum - abaxial surface of lamina with sori; e. Pityrogramma calomelanos - abaxial surface of lamina with whitish-farinose indument. (Photographs: M. Figueira & B. Schindler).

      • 25’. Petioles without pulvinus; rachis non-alate or absent; sori parallel to the main vein 26

        • 26. Laminae pinnatifid, margin inconspicuously denticulate Blechnum sp. (Fig. 10c)

        • 26’. Laminae pinnate, margin serrate Telmatoblechnum serrulatum (Fig. 10d)

  • 24’. Sporangia forming rounded or oblong sori, or spread on the laminae 27

    • 27. Abaxial surface of the laminae with a whitish, farinose indument Pityrogramma calomelanos (Fig. 10e)

    • 27’. Abaxial surface of the laminae lacking a farinose indument 28

      • 28. Veins anastomosing 29

        • 29. Pinnae with crenate to toothed margin Cyclodium meniscioides (Fig. 11a-b)

          Figure 11
          a-h. Ferns of Estação Ecológica Serra Geral do Tocantins (EESGT) - a-b. Cyclodium meniscioides - a. lamina; b. detail of pinnae venation and sori; c-d. Meniscium arborescens - c. lamina; d. detail of pinnae venation and sori; e-f. M. maxonianum - e. lamina; f. detail of pinnae venation and sori; g. Metaxya parkeri - lamina and sori detail; h. Nephrolepis biserrata, lamina and sori detail. (Photographs: M. Figueira & B. Schindler).

        • 29’. Pinnae with entire, wavy or slightly crenate margin 30

          • 30. Abaxial surface of the laminae with glandular trichomes Meniscium maxonianum (Fig. 11c-d)

          • 30’. Abaxial surface of the laminae with acicular trichomes Meniscium arborescens (Fig. 11e-f)

    • 28’. Veins free 31

      • 31. Laminae 1-pinnate 32

        • 32. Pinnae chartaceous, apex long-attenuate to caudate, margins serrate; sori without indusium, one or usually several sori on each side of the costae Metaxya parkeri (Fig. 11g)

        • 32’. Pinnae membranous, apex acute, acuminate or emarginate, margin entire to slightly serrate; sori with circular to semicircular indusium, uniseriate on each side of the costae Nephrolepis biserrata (Fig. 11h)

      • 31’. Laminae 2-pinnate or more divided 33

        • 33. Petiole inermous Cyathea myriotricha (Fig. 12a-b)

        • 33’. Petiole aculeate 34

          • 34. Pinnules pinnatipartite; indusium absent Cyathea pungens (Fig. 12c-e)

          • 34’. Pinnules pinnatisect; indusium present Cyathea delgadii (Fig. 12f-h)

Our results suggest strong habitat specificity with different pteridophyte assemblages occupying various habitat types in the EESGT. One exception is Selaginella radiata, which was recorded growing in sunny, dry rocky outcrops, and in shady and humid places, an ecological observation also reported by Góes-Neto et al. (2016)Góes-Neto LAA, Pallos J & Salino A (2016) Flora das cangas da Serra dos Carajás, Pará, Brasil: Selaginellaceae. Rodriguésia 67: 1177-1180. <https://doi.org/10.1590/2175-7860201667514>.
https://doi.org/10.1590/2175-78602016675...
.

Overall, we found the highest richness in wet forests on non-flooded soils, whereas comparatively less species were found in open and/or flooded habitats. Habitats with high light incidence, low humidity, seasonally dry microclimates, and sites occurring on poorly-drained soils may represent ecological barriers that prevent colonization by many pteridophyte groups. According to Kessler (2010)Kessler M (2010) Biogeography of ferns. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 22-60., environmental conditions can limit the coexistence of different species in the same habitat.

New occurrence records

The 35 species of pteridophytes found in the EESGT represent a considerable fraction of the total number of species recorded for Tocantins and add 11 species to the state’s list (Tab. 1). New Cerrado records include the first record for the family Marattiaceae with the occurrence of Danaea leprieurii, which was only registered to the Amazonian domain (Flora e Funga do Brasil 2022Flora e Funga do Brasil 2022 (continuously updated) Jardim Botânico do Rio de Janeiro. Available at <https://floradobrasil.jbrj.gov.br/FB245>. Access on 12 September 2022.
https://floradobrasil.jbrj.gov.br/FB245...
(continuously updated); Salino & Lima 2017Salino A & Lima LV (2017) Flora das cangas da Serra dos Carajás, Pará, Brasil: Marattiaceae. Rodriguésia 68: 861-863. <https://doi.org/10.1590/2175-7860201768315>.
https://doi.org/10.1590/2175-78602017683...
). Another highlight is the record of a recently described species, Anemia areniticola cited only for Pará and Maranhão (Pereira et al. 2022Pereira JBS, Nunes MG & Labiak PH (2022) Novelties in the Anemia elegans clade (Anemiaceae), with a new species and nothospecies from Brazil. Systematic Botany 47: 840-845. <https://doi.org/10.1600/036364422X16573019348364>.
https://doi.org/10.1600/036364422X165730...
). In addition to new records, we report the second record of Anemia andersonii, A. trichorhiza (B. Schindler et al. 382), and Cyathea pungens from Tocantins.

In the dataset obtained from digital repositories, we found occurrence records of Metaxya lanosa A.R. Sm. & Tuomisto (L.G. Sousa VIC 48791) and M. rostrata (Humb. & Bonpl. ex Willd.) C. Presl (J. Cordeiro et al. 2637), two species that occur in central and western Amazonia (Cárdenas et al. 2016Cárdenas GG, Tuomisto H & Lehtonen S (2016) Newly discovered diversity in the tropical fern genus Metaxya based on morphology and molecular phylogenetic analyses. Kew Bulletin 71: 5. <https://doi.org/10.1007/s12225-016-9618-9>
https://doi.org/10.1007/s12225-016-9618-...
). After examining images of these collections, we preferred not including these species in our checklist since we were not confident in their identifications. A careful examination of the herbarium material would be required to confirm they identity. The specimen M. rostrata abovementioned was collected at the “Cachoeira da Fumaça”, the same locality where we collected a plant identified as M. parkeri based on the work of Cárdenas et al. (2016)Cárdenas GG, Tuomisto H & Lehtonen S (2016) Newly discovered diversity in the tropical fern genus Metaxya based on morphology and molecular phylogenetic analyses. Kew Bulletin 71: 5. <https://doi.org/10.1007/s12225-016-9618-9>
https://doi.org/10.1007/s12225-016-9618-...
. We do not rule out that these collections could be conspecific. In any case, we recommend a more detailed revision of the material of Metaxyaceae collected in Tocantins, a group that is most diverse in Amazonia.

Prado et al. (2015)Prado J, Sylvestre LS, Labiak PH, Windisch PG, Salino A, Barros ICL, Hirai RY, Almeida TE, Santiago ACP, Kieling-Rubio MA, Pereira AFN, Øllgaard B, Ramos CGV, Mickel JT, Dittrich VAO, Mynssen CM, Schwartsburd PB, Condack JPS, Pereira JBS & Matos FB (2015) Diversity of ferns and lycophytes in Brazil. Rodriguésia 66: 1073-1083. <https://doi.org/10.1590/2175-7860201566410>.
https://doi.org/10.1590/2175-78602015664...
reported an increase of 210% in the number of species for Tocantins comparing the List of Flora of Brazil 2010 (20 spp.) with the 2015 version (69 spp.). According to the BFG (2022)BFG - The Brazil Flora Group (2022) Brazilian Flora 2020: Leveraging the power of a collaborative scientific network. Taxon 71: 178-198. <https://doi.org/10.1002/tax.12640>
https://doi.org/10.1002/tax.12640...
, 82 species are reported for the state. Despite this recent progress in botanical knowledge of Tocantins, the current figures are underestimated. For example, Goiás, a state similar in size to Tocantins but with much better documented flora, has 260 species of ferns and lycophytes. In contrast, Distrito Federal, with an area 50 times smaller, has 148 documented species (BFG 2022BFG - The Brazil Flora Group (2022) Brazilian Flora 2020: Leveraging the power of a collaborative scientific network. Taxon 71: 178-198. <https://doi.org/10.1002/tax.12640>
https://doi.org/10.1002/tax.12640...
). Therefore, increasing collection efforts in Tocantins is essential to improve the state’s floristic knowledge and contribute to new species discovery. Increasing occurrence data on ferns and lycophytes in the region would also result in a better understanding of the biogeographic context of Tocantins flora. For example, additional pteridophyte records could provide further evidence for the influence of the Amazon on the flora of riparian forests of the Cerrado (Martins et al. 2013Martins SV, Brito-Ibrahim ER, Eisenlohr PV, Oliveira-Filho AT & Silva AF (2013) A vegetação de ipucas no Tocantins: estudo de caso e relações florísticas com remanescentes do Cerrado e da Amazônia. In: Felfili JM, Eisenlohr PV, Melo MMRF, Andrade LA & Meira Neto JAA (eds.) Fitossociologia no Brasil - métodos e estudos de casos. Ed. UFV, Viçosa. Pp. 460-478.; Oliveira-Filho & Ratter 2000Oliveira-Filho AT & Ratter JA (2000) Padrões florísticos das matas ciliares da região do Cerrado e a evolução das paisagens do Brasil Central durante o Quaternário Tardio. In: Rodrigues RR & Leitão Filho HF (eds.) Matas ciliares: conservação e recuperação. EDUSP, São Paulo. Pp. 73-89.), such as records of the Amazon-centered species Danaea leprieurii and Selaginella radiata in the EESGT.

Anemia trichorhiza, a species that inhabits rocky outcrops on the slopes of the Serra Geral, is classified as vulnerable (CNCFlora 2023CNCFlora (2023) Anemia trichorhiza in Lista Vermelha da Flora Brasileira versão 2012.2. Centro Nacional de Conservação da Flora. Available at <http://cncflora.jbrj.gov.br/portal/pt-br/profile/Anemiatrichorhiza>. Access on 23 May 2023.
http://cncflora.jbrj.gov.br/portal/pt-br...
) and was the single new occurrence record to Bahia reported here.

Overall, our sampling effort, which focused on a single protected area, resulted in a significant improvement in the knowledge of pteridophytes in an otherwise poorly known region, highlighting, in turn, the need for additional botanical surveys that include all groups of vascular plants to fill biodiversity gaps, particularly in Tocantins state. Our results also highlight the importance of forest formations and wet habitats as critical environments for the conservation of pteridophytes within the Cerrado. Despite occupying a small fraction of the landscape, these habitats concentrate most pteridophyte diversity. We expect that the checklist presented here, which represents the first compilation of pteridophytes for a protected area in the Jalapão region, will encourage further studies on this often-neglected component of the Cerrado flora.

Acknowledgements

We thank EESGT managers (ICMBio) Ana Carolina S. Barradas, Marco A. Borges, and Maximo M. Costa, for all technical and logistical support; all rangers, especially Walter B. Silva, who accompanied us on all expeditions, always sharing his valuable regional knowledge; taxonomists Luiz Góes-Neto, Alexandre Salino, and Felipe Gonzatti, for all the help essential to accomplish accurate identifications; and staff at herbarium CEN, including Aécio A. Santos, Valdeci F. Gomes (Dudu) and Sérgio E. Noronha, for assistance in the field. MFS thanks CNPq (Proc. 305570/2021-8) and ICMBio, for an authorization for plant collections (SISBIO 61941-1).

Data availability statement

In accordance with Open Science communication practices, the authors inform that all data associated with herbarium specimens cited in this study is publicly available in the repository SpeciesLink (CRIA 2022CRIA (2022) Centro de Referência e Informação Ambiental. Specieslink - simple search. Available at <https://specieslink.net/search/>. Access on 12 September 2022.
https://specieslink.net/search/...
).

References

  • Alencar A, Shimbo JZ, Lenti F, Marques CB, Zimbres B, Rosa M, Arruda V, Castro I, Ribeiro JPFM, Varela V, Alencar I, Piontekowski V, Ribeiro V, Bustamante MMC, Sano EE & Barroso M (2020) Mapping three decades of changes in the Brazilian Savanna native vegetation using landsat data processed in the Google Earth engine platform. Remote Sensing 12: 924. <https://doi.org/10.3390/rs12060924>.
    » https://doi.org/10.3390/rs12060924
  • Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM & Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728. <https://doi.org/10.1127/0941-2948/2013/0507>
    » https://doi.org/10.1127/0941-2948/2013/0507
  • Antar GM & Sano PT (2019) Angiosperms of dry grasslands and savannahs of Jalapão, the largest conserved Cerrado area in Brazil. Rodriguésia 70: e04002017. <https://doi.org/10.1590/2175-7860201970070>
    » https://doi.org/10.1590/2175-7860201970070
  • Athayde Filho FP & Agostinho AA (2005) Pteridoflora de duas veredas no município de Campinápolis, Mato Grosso, Brasil. Pesquisas, Botânica 56: 145-160.
  • Beentje H (2010) The Kew plant glossary: an illustrated dictionary of plant terms. Royal Botanic Gardens, Kew, Richmond, Surrey. 160p.
  • Benzing DH (2004) CHAPTER 9 - Vascular Epiphytes. In: Lowman MD & Rinker HB (eds.) Forest canopies. 2nd ed. Academic Press, San Diego. Pp. 175-211. <http://dx.doi.org/10.1016/B978-012457553-0/50014-9>
    » http://dx.doi.org/10.1016/B978-012457553-0/50014-9
  • BFG - The Brazil Flora Group (2022) Brazilian Flora 2020: Leveraging the power of a collaborative scientific network. Taxon 71: 178-198. <https://doi.org/10.1002/tax.12640>
    » https://doi.org/10.1002/tax.12640
  • Cárdenas GG, Tuomisto H & Lehtonen S (2016) Newly discovered diversity in the tropical fern genus Metaxya based on morphology and molecular phylogenetic analyses. Kew Bulletin 71: 5. <https://doi.org/10.1007/s12225-016-9618-9>
    » https://doi.org/10.1007/s12225-016-9618-9
  • Castro-Aguiar PH, Fernandes RS & Prado J (2022) Pteridaceae in remnants of Cerrado in Maranhão state, Brazil. Check List 18: 1263-1278. <https://doi.org/10.15560/18.6.1263>
    » https://doi.org/10.15560/18.6.1263
  • CNCFlora (2023) Anemia trichorhiza in Lista Vermelha da Flora Brasileira versão 2012.2. Centro Nacional de Conservação da Flora. Available at <http://cncflora.jbrj.gov.br/portal/pt-br/profile/Anemiatrichorhiza>. Access on 23 May 2023.
    » http://cncflora.jbrj.gov.br/portal/pt-br/profile/Anemiatrichorhiza
  • Colli AMT, Souza SA, Salino A, Lucca ALT & Silva RT (2004) Pteridófitas do Parque Estadual de Vassununga, Santa Rita do Passa Quatro (SP), Brasil. Gleba Pé-de-Gigante. Revista do Instituto Florestal 16: 121-127.
  • CRIA (2022) Centro de Referência e Informação Ambiental. Specieslink - simple search. Available at <https://specieslink.net/search/>. Access on 12 September 2022.
    » https://specieslink.net/search/
  • Fernandes JH, Kreutz C & Athayde Filho FP (2014) Samambaias em formações de Cerrado rupestre da Bacia do Rio das Mortes, Mato Grosso, Brasil. Pesquisas, Botânica 65: 217-231.
  • Fernandes RS, Conceição GM, Costa JM & Paula-Zárate EL (2010) Samambaias e licófitas do município de Caxias, Maranhão, Brasil. Boletim do Museu Paraense Emílio Goeldi Ciências Naturais 5: 345-356.
  • Fernandes RS, Silva LR, Oliveira SS, Ottoni FP & Pietrobom MR (2022) Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotropica 22: e20211273. <https://doi.org/10.1590/1676-0611-bn-2021-1273>.
    » https://doi.org/10.1590/1676-0611-bn-2021-1273
  • Fidalgo O & Bononi VLR (1984) Técnicas de coleta, preservação e herborização de material botânico. Instituto de Botânica, São Paulo. 61p.
  • Flora e Funga do Brasil 2022 (continuously updated) Jardim Botânico do Rio de Janeiro. Available at <https://floradobrasil.jbrj.gov.br/FB245>. Access on 12 September 2022.
    » https://floradobrasil.jbrj.gov.br/FB245
  • Franke J, Barradas ACS, Borges MA, Costa MM, Dias PA, Hoffmann AA, Orozco Filho JC, Melchiori AE & Siegert F (2018) Fuel load mapping in the Brazilian Cerrado in support of integrated fire management. Remote Sensing of Environment 217: 221-232. <https://doi.org/10.1016/j.rse.2018.08.018>.
    » https://doi.org/10.1016/j.rse.2018.08.018
  • GBIF.org (2022) GBIF Home Page. Global Biodiversity Information Facility. Available at <https://www.gbif.org/>. Access on 12 September 2022.
    » https://www.gbif.org/
  • Góes-Neto LAA, Pallos J & Salino A (2016) Flora das cangas da Serra dos Carajás, Pará, Brasil: Selaginellaceae. Rodriguésia 67: 1177-1180. <https://doi.org/10.1590/2175-7860201667514>.
    » https://doi.org/10.1590/2175-7860201667514
  • Goetz MNB, Fraga LL & Schmitt JL (2012) Florística e aspectos ecológicos de samambaias e licófitas em um parque urbano do Rio Grande do Sul, Brasil. Pesquisas, Botânica 63: 165-176.
  • Hietz P (2010) Fern adaptations to xeric environments. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 140-176.
  • Hirai RY, Cruz R & Prado J (2018) A new species of Hemionitis (Pteridaceae) from central Brazil. Willdenowia 48: 371. <https://doi.org/10.3372/wi.48.48305>.
    » https://doi.org/10.3372/wi.48.48305
  • IPNI (2022) International Plant Names Index. The Royal Botanic Gardens, Kew, Harvard University Herbaria & Libraries, and Australian National Herbarium. Available at <http://www.ipni.org>. Access on 15 December 2022.
    » http://www.ipni.org
  • Jermy AC (1990) Conservation of Pteridophytes. In: Kramer KU & Green PS (eds.) The Pteridophytes and Gymnosperms. The families and genera of vascular plants. Vol. 1. Springer, Berlin, Heidelberg. 14p. <https://doi.org/10.1007/978-3-662-02604-5_4>.
    » https://doi.org/10.1007/978-3-662-02604-5_4
  • Kessler M (2010) Biogeography of ferns. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 22-60.
  • Kreutz C, Athayde Filho FP & Sanchez M (2016) Spatial and seasonal variation in the species richness and abundance of ferns and lycophytes in gallery forests of Cerrado in Central Brazil. Brazilian Journal of Botany 39: 315-326. <https://doi.org/10.1007/s40415-015-0236-9>.
    » https://doi.org/10.1007/s40415-015-0236-9
  • Labiak PH, Mickel JT & Matos FB (2018) Anemia paripinnata (Anemiaceae), a new species from Central Brazil. American Fern Journal 108: 1-6. <https://doi.org/10.1640/0002-8444-108.1.1>.
    » https://doi.org/10.1640/0002-8444-108.1.1
  • Lehn CR, Gonzatti F & Arana MD (2020) Samambaias e licófitas dos Cerros do Tigre e Palomas, província biogeográfica do Pampa, estado do Rio Grande do Sul, Brasil. Hoehnea 47: e762019. <https://doi.org/10.1590/2236-8906-76/2019>.
    » https://doi.org/10.1590/2236-8906-76/2019
  • Lellinger DB (2002) A modern multilingual glossary for taxonomic pteridology. Pterodologia 3 A. American Fern Society, Washington. 264p.
  • Martins SV, Brito-Ibrahim ER, Eisenlohr PV, Oliveira-Filho AT & Silva AF (2013) A vegetação de ipucas no Tocantins: estudo de caso e relações florísticas com remanescentes do Cerrado e da Amazônia. In: Felfili JM, Eisenlohr PV, Melo MMRF, Andrade LA & Meira Neto JAA (eds.) Fitossociologia no Brasil - métodos e estudos de casos. Ed. UFV, Viçosa. Pp. 460-478.
  • Mickel JT (2016) Anemia: Anemiaceae. New York Botanical Garden Press, New York. Pp. 1-182.
  • Miguez FA, Kreutz C & Athayde Filho FP (2013) Samambaias e Licófitas em quatro Matas de Galeria do município de Nova Xavantina, Mato Grosso, Brasil. Pesquisas, Botânica 64: 243-258.
  • Moran RC (2012) História natural das samambaias. TECC Editora, Florianópolis. 264p.
  • Nunes MG & Labiak PH (2021) Ferns and lycophytes of the Cerrado State Park, Paraná, Brazil. Rodriguésia 72: e00192020. <https://doi.org/10.1590/2175-7860202172096>.
    » https://doi.org/10.1590/2175-7860202172096
  • Oliveira AGS & Schwartsburd PB (2021) Two new species of Doryopteris (Pteridaceae) from Brazil. American Fern Journal 111: 35-42. <https://doi.org/10.1640/0002-8444-111.1.35>.
    » https://doi.org/10.1640/0002-8444-111.1.35
  • Oliveira RP & Arcela V (2014) Distribuição vertical e valor de importância das epífitas vasculares da Reserva Biológica do Guará, Brasília, DF. Heringeriana 8: 20-31. <https://doi.org/10.17648/heringeriana.v8i1.93>.
    » https://doi.org/10.17648/heringeriana.v8i1.93
  • Oliveira-Filho AT & Ratter JA (2000) Padrões florísticos das matas ciliares da região do Cerrado e a evolução das paisagens do Brasil Central durante o Quaternário Tardio. In: Rodrigues RR & Leitão Filho HF (eds.) Matas ciliares: conservação e recuperação. EDUSP, São Paulo. Pp. 73-89.
  • Pereira JBS, Nunes MG & Labiak PH (2022) Novelties in the Anemia elegans clade (Anemiaceae), with a new species and nothospecies from Brazil. Systematic Botany 47: 840-845. <https://doi.org/10.1600/036364422X16573019348364>.
    » https://doi.org/10.1600/036364422X16573019348364
  • Pereira JBS & Prado J (2022) Two new endemic tetraploid species of the genus Isoëtes from the Brazilian Savanna. Systematic Botany 47: 301-305. <https://doi.org/10.1600/036364422X16512564801704>.
    » https://doi.org/10.1600/036364422X16512564801704
  • Ponce MM & Scataglini MA (2021) Phylogenetic position of South American Cheilanthes (Cheilanthoideae, Pteridaceae): advances in the generic circumscription and segregation of the new genus Mineirella Journal of Systematics and Evolution 60: 1-15. <https://doi.org/10.1111/jse.12723>.
    » https://doi.org/10.1111/jse.12723
  • Prado J, Sylvestre LS, Labiak PH, Windisch PG, Salino A, Barros ICL, Hirai RY, Almeida TE, Santiago ACP, Kieling-Rubio MA, Pereira AFN, Øllgaard B, Ramos CGV, Mickel JT, Dittrich VAO, Mynssen CM, Schwartsburd PB, Condack JPS, Pereira JBS & Matos FB (2015) Diversity of ferns and lycophytes in Brazil. Rodriguésia 66: 1073-1083. <https://doi.org/10.1590/2175-7860201566410>.
    » https://doi.org/10.1590/2175-7860201566410
  • Proença CEB, Sampaio AB, Silva LH, Milhomens LC, Simon, MF, Simpson PL & Farias R (2002) Relatório de Botânica. In: Arruda MB & von Behr M (eds.) Jalapão: expedição científica e conservacionista. IBAMA, Brasília. Pp. 21-28.
  • QGIS Development Team (2019) QGIS Geographic Information System. Available at <http://qgis.org>. Access on 7 April 2021.
    » http://qgis.org
  • REFLORA (2022) Reflora - Herbário Virtual. Available at <http://reflora.jbrj.gov.br/reflora/herbarioVirtual/ConsultaPublicoHVUC/ConsultaPublicoHVUC.do;jsessionid=F2131AC6CCEDF3F5209B9CE35AAAE9F3?http://reflora.jbrj.gov.br/reflora/herbarioVirtual/>. Access on 12 June 2022.
    » http://reflora.jbrj.gov.br/reflora/herbarioVirtual/ConsultaPublicoHVUC/ConsultaPublicoHVUC.do;jsessionid=F2131AC6CCEDF3F5209B9CE35AAAE9F3?http://reflora.jbrj.gov.br/reflora/herbarioVirtual/
  • Ribeiro JF & Walter BMT (2008) As principais fitofisionomias do Cerrado. In: Sano SM, Almeida SP & Ribeiro JF (eds.) Cerrado: ecologia e flora. Embrapa Cerrados, Planaltina. Pp. 151-212.
  • Salino A & Lima LV (2017) Flora das cangas da Serra dos Carajás, Pará, Brasil: Marattiaceae. Rodriguésia 68: 861-863. <https://doi.org/10.1590/2175-7860201768315>.
    » https://doi.org/10.1590/2175-7860201768315
  • Santana JCO & Simon MF (2022) Plant diversity conservation in an agricultural frontier in the Brazilian Cerrado Biodiversity and Conservation 31: 667-681. <https://doi.org/10.1007/s10531-022-02356-2>.
    » https://doi.org/10.1007/s10531-022-02356-2
  • Santos-Silva DL, Prado J & Eisenlohr PV (2023) Living on the edge: composition, biogeography, and conservation of ferns in rocky environments of Southern Amazonia. Brazilian Journal of Botany 46: 227-239. <https://doi.org/10.1007/s40415-022-00866-5>.
    » https://doi.org/10.1007/s40415-022-00866-5
  • Sharpe JM & Mehltreter K (2010) Ecological insights from fern population dynamics. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern Ecology. Cambridge University Press, Cambridge. Pp. 61-110.
  • Silva DP, Amaral AG, Bijos NR & Munhoz CBR (2017) Is the herb-shrub composition of veredas (Brazilian palm swamps) distinguishable? Acta Botanica Brasilica 32: 47-54. <https://doi.org/10.1590/0102-33062017abb0209>.
    » https://doi.org/10.1590/0102-33062017abb0209
  • Thiers B (continuously updated) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at <http://sweetgum.nybg.org/science/ih/>. Access on 12 September 2022.
    » http://sweetgum.nybg.org/science/ih/
  • Tryon RM & Tryon AF (1982) Ferns and allied plants: with special reference to Tropical America. Springer, New York. 896p. <https://doi.org/10.1007/978-1-4613-8162-4>.
    » https://doi.org/10.1007/978-1-4613-8162-4
  • Villela FNJ & Nogueira C (2011) Geologia e geomorfologia da estação ecológica Serra Geral do Tocantins. Biota Neotropica 11: 217-229. <https://doi.org/10.1590/S1676-06032011000100023>.
    » https://doi.org/10.1590/S1676-06032011000100023
  • Xavier SRS, Barros ICL & Santiago ACP (2012) Ferns and lycophytes in Brazil’s semi-arid region. Rodriguésia 63: 483-488. <https://doi.org/10.1590/S2175-78602012000200021>.
    » https://doi.org/10.1590/S2175-78602012000200021
  • Zambiase RM, Resende ILM, Kreutz C & Athayde Filho FP (2016) Análise ecoflorística de samambaias e licófitas em mata de galeria inundável e vereda, Quirinópolis, Goiás, Brasil. Pesquisas, Botânica 69: 169-181.
  • Zuquim G, Costa FRC, Prado J & Tuomisto H (2008) Guide to the ferns and lycophytes of REBIO Uatumã - Central Amazonia. Átemma Design Editorial, Manaus. 316p.

Edited by

Area Editor: Dra. Claudine Mynssen

Publication Dates

  • Publication in this collection
    01 Dec 2023
  • Date of issue
    2023

History

  • Received
    16 Mar 2023
  • Accepted
    23 July 2023
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