Abstract

We present a key to identify and an annotated list of lycophytes and ferns of the Immediate Geographical Region of São Luís, Maranhão State, which has ecotonal characteristics of Amazonian Forest, Cerrado, and Coastal Vegetation. Specimens were collected monthly between April 2020 and September 2022 in the 13 municipalities of this region. A total of 64 species were identified, including 61 species of ferns, in 18 families and 38 genera, and three species of lycophytes, in two genera and one family. The most representative families were Pteridaceae (18 species) and Polypodiaceae (nine species). The most recorded substrate of occurrence was terrestrial with 35 species (54.6%), followed by epiphytic with 15 species (23.4%), aquatic with four species (6.2%), rupicolous with three species (4.6%), and hemiepiphytic with two species (3.1%). Five species (7.8%) had more than one life form. This study expands the knowledge about the geographic distribution of fern and lycophyte species in the central region of Northern Maranhão, in Northeastern Brazil, which until now had several sampling gaps. Maranhão has a diversity that is still poorly reported and known compared to other states in South and Southeast Brazil. Therefore, floristic surveys are essential to increase what is known about the flora, especially in areas under anthropic pressure and places with few collections, such as the ecotonal areas in Maranhão.

Keywords
Floristics; Immediate Geographic Region of São Luís; Transition zone

Resumo

Apresentamos uma chave para a identificação e uma lista com detalhes das licófitas e samambaias da Região Geográfica Imediata de São Luís, Estado do Maranhão, que possui características ecotonais da Floresta Amazônica, Cerrado e Vegetação Litorânea. Os dados foram coletados mensalmente entre abril de 2020 e setembro de 2022 nos 13 municípios dessa região. Foram identificadas 64 espécies, incluindo 61 espécies de samambaias, em 18 famílias e 38 gêneros, e três espécies de licófitas, em dois gêneros e uma família. As famílias mais representativas foram Pteridaceae (18 espécies) e Polypodiaceae (nove espécies). O substrato de ocorrência mais registrado foi o terrestre com 35 espécies (54,6%), seguido do epifítico com 15 espécies (23,4%), aquático com quatro espécies (6,2%), rupícola com três espécies (4,6%) e hemiepifítico com duas espécies (3,1%). Cinco espécies (7,8%) apresentaram mais de uma forma de vida. Este estudo amplia o conhecimento sobre a distribuição geográfica de espécies de samambaias e licófitas na região central do norte do Maranhão, no Nordeste do Brasil, que até então possuía várias lacunas de amostragem. O Maranhão possui uma diversidade ainda pouco relatada e conhecida em comparação com outros estados das regiões Sul e Sudeste do Brasil. Portanto, levantamentos florísticos são essenciais para aumentar o conhecimento sobre a flora, principalmente em áreas sob pressão antrópica e locais com poucas coletas, como as áreas ecotonais do Maranhão.

Palavras-chave
Florística; Região Geográfica Imediata de São Luís; Zona de transição

Introduction

Lycophytes and ferns are seedless vascular plants that are commonly studied together because they have shared characteristics such as a life cycle with alternation of generations, free gametophytes, and reproduction through spores, have a worldwide distribution, except at the poles, and are very diverse in the tropics (Krieg and Chambers 2022KRIEG, C.P. & CHAMBERS, S.M. 2022. The ecology and physiology of fern gametophytes: A methodological synthesis. Appl. Plant Sci. 10(2): e11464. https://doi.org/10.1002/aps3.11464.
https://doi.org/10.1002/aps3.11464... ).

In Brazil, 1,412 spp. have been recorded, of which most occur in the Atlantic Forest (944 species), Amazon (578 spp.), and Cerrado (319 spp.) biomes (Ferns and Lycophytes in Flora and Funga of Brazil 2023).

Maranhão is a Brazilian state that has several areas of transitional vegetation, including an ecotonal region between the Amazonian Forest and Cerrado biomes in the central part and, to a lesser extent, an ecotonal region between Cerrado and Caatinga in the eastern part (Spinelli-Araújo et al. 2016SPINELLI-ARAÚJO, L., SILVA, G.B.S., TORRESAN, F.E., VICTORIA, D.C., VICENTE, L.E. BOLFE, E.L. & MANZATTO, C.V. 2016. Conservação da Biodiversidade do Estado do Maranhão: Cenário Atual em Dados Geospaciais. 1. ed. Embrapa Meio Ambiente, Jaguariúna, 28p.). Ecotonal areas between these biomes are floristically diverse due to the numerous habitats in places dominated by Amazonian Forest, Inundated Areas, Mangrove, Restinga, and Cerrado physiognomies (Spinelli-Araújo et al. 2016SPINELLI-ARAÚJO, L., SILVA, G.B.S., TORRESAN, F.E., VICTORIA, D.C., VICENTE, L.E. BOLFE, E.L. & MANZATTO, C.V. 2016. Conservação da Biodiversidade do Estado do Maranhão: Cenário Atual em Dados Geospaciais. 1. ed. Embrapa Meio Ambiente, Jaguariúna, 28p.; Silva-Moraes et al. 2019SILVA-MORAES, H.G., CORDEIRO, I. & FIGUEIREDO, N. 2019. Flora and floristic affinities of the Cerrados of Maranhão state, Brazil. Edinburgh J. Bot. 76:1–21.).

According to the IBGE (2017)IBGE. 2017. Divisão regional do Brasil em regiões geográficas imediatas e regiões geográficas intermediárias. Vol. 1. Ed. IBGE, Rio de Janeiro, 82p., Maranhão is divided into five Intermediate Geographic Regions and 22 Immediate Geographic Regions, formerly known as Mesoregions and Microregions, respectively. Among these, the Immediate Geographic Region of São Luís is in a transition area between the Amazon and Cerrado and has a wide variety of water bodies, including the Una, Munim, Arruda, and Boqueirão rivers that have rapids and waterfalls. This area is visited by many tourists and is under high anthropic pressure (Martins 2016MARTINS, R.F.D. 2016. Alterações Socioambientais na microbacia do Rio Una em Morros, MA. Anais do XVIII Encontro Nacional de Geógrafos (24 a 30 de julho de 2016. São Luís, MA) A construção do Brasil: geografia, ação política e democracia. http://www.eng2016.agb.org.br/resources/anais/7/1467683352_ARQUIVO_ALTERACOESSOCIOAMBIENTAISNAMICROBACIADORIOUNAEMMORROS.pdf.
http://www.eng2016.agb.org.br/resources/... ).

In the state of Maranhão, the first study of lycophytes and ferns was done by Bastos & Cutrim (1999). They carried out a floristic survey in the Sacavém Forest Reserve in São Luís and reported the occurrence of 35 species, all of which were new records for the state. Subsequent works recorded species already known for the flora of Maranhão, as well as species commonly found in anthropic sites (Conceição & Ruggieri 2010; Conceição et al. 2015; Silva et al. 2017SILVA, G.S., SILVA, D.L.S., OLIVEIRA, R.R. & CONCEIÇÃO, G.M. 2017. Licófitas e Samambaias no Cerrado do Leste do Maranhão, Brasil. Acta Bras. 1:13–16.; Silva Junior et al. 2018SILVA JUNIOR, W.R., FERNANDES, R.S. & FERREIRA, A.W.C. 2018. First record of the exotic fern Pteris tripartita Sw. (Pteridaceae) for the Maranhão state, Northeastern Brazil. Biod. Int. J. 2:161–163.). A few surveys were conducted in protected areas, but generally, a low number of species was found (Fernandes et al. 2007, 2010; Conceição & Rodrigues 2010).

According to Flora and Funga of Brazil (2023)FLORA E FUNGA DO BRASIL 2023. (http://floradobrasil.jbrj.gov.br). Acesso em: 21/01/2023.
http://floradobrasil.jbrj.gov.br... , 100 species of lycophytes and ferns occur in the state of Maranhão. However, studies of ferns and lycophytes in Maranhão suggest that there is a higher number of species. In a survey conducted only in forest fragments in the Amazonian portion of Maranhão, Silva Junior et al. (2020)SILVA JUNIOR, W.R., FERREIRA, A.W.C., ILKIU-BORGES, A.L. & FERNANDES, R.S. 2020. Ferns and lycophytes of remnants in Amazônia Maranhense, Brazil. Biota Neotrop. 20:e20200972. speciesLink 2023. (https://specieslink.net/). (Last access 21/01/2023).
https://specieslink.net/... reported 64 species, of which 24 were new records for the state. Additionally, in a study in the Chapada das Mesas region, a Cerrado-Amazon transition area, Fernandes et al. (2022)FERNANDES, R.S., SILVA, L.R., OLIVEIRA, S.S., OTTONI, F.P. & PIETROBOM, M.R. 2022. Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotrop. 22:e20211273. recorded 89 species, 26 of which were also new records for Maranhão. Further, this study provided a compilation of the known species in the state, which resulted in an estimated number of 151 species.

The objective of the present research was to carry out a comprehensive floristic survey of lycophytes and ferns in the thirteen municipalities of the Immediate Geographical Region of São Luís, Maranhão, a transition area between the Amazonian Forest, Cerrado, and Coastal Vegetation biomes and to provide an identification key for all taxa found.

Material and Methods

1. Study area

The state of Maranhão has a tropical rainy climate, AW (humid with moderate water deficit) (Köppen 1948KÖPPEN, W.P. 1948. Climatologia: com un estudio de los climas de la tierra. Vol 1. Ed. Fondo de Cultura Econômica, México, 478p.), with an average annual temperature between 25°–26° C and an average annual precipitation between 1,400–1,800 mm; it is one of the northeastern states with the lowest water deficit (Martins & Oliveira 2011MARTINS, M.B. & OLIVEIRA, T.G. 2011. Amazônia Maranhense: Diversidade e Conservação. Ed. MPEG, Belém, 328p.). The dry season lasts five to six months, from July to December when there is a water deficit of 150–300 mm (Golfari 1980GOLFARI, L. 1980. Zoneamento ecológico para reflorestamento da área de influência da Serra de Carajás. Rev. Comp. Vale do Rio Doce 1:3–18.), and the most intense rainy season is between January and June (Brasil 1986BRASIL. 1986. Levantamento exploratório-reconhecimento de solos do estado do Maranhão. EMBRAPA/SNLCS, Bol. Pesq. 35:522.). The Immediate Geographic Region of São Luís (Figure 1) encompasses the Municipalities: of Alcântara, Axixá, Bacabeira, Cachoeira Grande, Icatu, Morros, Paco do Lumiar, Presidente Juscelino, Raposa, Rosário, Santa Rita, São José de Ribamar, and São Luís. It is an area containing predominantly Amazonian Forest vegetation in transition with Coastal Vegetation, with some Cerrado enclaves (Spinelli-Araújo et al. 2016SPINELLI-ARAÚJO, L., SILVA, G.B.S., TORRESAN, F.E., VICTORIA, D.C., VICENTE, L.E. BOLFE, E.L. & MANZATTO, C.V. 2016. Conservação da Biodiversidade do Estado do Maranhão: Cenário Atual em Dados Geospaciais. 1. ed. Embrapa Meio Ambiente, Jaguariúna, 28p.; IBGE 2017IBGE. 2017. Divisão regional do Brasil em regiões geográficas imediatas e regiões geográficas intermediárias. Vol. 1. Ed. IBGE, Rio de Janeiro, 82p.).

2. Data collection

Field expeditions were carried out monthly between April 2020 and September 2022. The specimens were georeferenced with a GPS and photographed with a digital camera in the environment where they occurred (Figures 2−4). To locate plants in the field, the free-walking method was used (Filgueiras et al. 1994FILGUEIRAS, T.S., BROCHADO, A.L., NOGUEIRA, P.E. & GUALA, G.F. 1994. Caminhamento: um método expedito para levantamentos florísticos qualitativos. Cad. Geoc.12:39–43.). Collecting and processing specimens followed standard techniques for vascular plants (Silva 1989SILVA, A.T. 1989. Pteridófitas. In: BONONI, V.L.R. & FIDALGO, O. (eds.). Técnicas de coleta, preservação e herborização de material botânico. Instituto de Botânica, São Paulo, p.33–34.; Bridson & Forman 1998BRIDSON, D. & FORMAN, L. 1998. International Herbarium Handbook. Ed 3. Royal Botanic Gardens, Kew, 334p.).

The material was processed at the Orchid Studies Laboratory at the Federal University of Maranhão, Campus Cidade Universitária Dom Delgado de São Luís, and deposited in the HABIT, SLUI, and SP (acronyms according to Index Herbariorum 2023) herbaria.

Identifications were made using specialized literature (e.g., Tryon & Stolze 1994TRYON, R.M. & STOLZE, R.G. 1994. 22. Marsileaceae – 28. Isoëtaceae. In: Pteridophyta of Peru. Fieldiana, Bot. 32(Part 6):1–190.; Moran & Riba 1995MORAN, R.C. & RIBA, R. 1995. Flora Mesoamericana. Psilotaceae a Salviniaceae. Universidade Nacional Autônoma do México, México, v.1, 470p.; Mickel & Smith 2004MICKEL, J.T. & SMITH, A.R. 2004. The Pteridophytes of Mexico. Mem. New York Bot. Gard. 88:1–1054p.; Prado & Moran 2008PRADO, J. & MORAN, R.C. 2008. Revision of the neotropical species of Triplophyllum (Tectariaceae). Brittonia 60103–130.; Arantes et al. 2010ARANTES, A.A., PRADO, J. & RANAL, M.A. 2010. Polypodiaceae e Pteridaceae da Estação Ecológica do Panga, Uberlândia, Estado de Minas Gerais, Brasil. Revta. Brasil. Bot. 33:167–183.; Zuquim et al. 2011ZUQUIM, G., COSTA, F.R.C., PRADO, J. & TUOMISTO, H. 2011. Guia de Samambaias e Licófitas da REBIO Uatumã. 2nd ed. INPA, Manaus, 316p.; Maciel 2016MACIEL, S. 2016. Nephrolepis (Lomariopsidaceae – Polypodiopsida) na Amazônia brasileira. Rodriguésia 67:77–84.; Prado et al. 2017PRADO, J., HIRAI, R.Y & MORAN, R.C. 2017. Fern and lycophyte flora of Acre state, Brazil. Biota Neotrop. 17:e20170369.; Silva et al. 2017SILVA, G.S., SILVA, D.L.S., OLIVEIRA, R.R. & CONCEIÇÃO, G.M. 2017. Licófitas e Samambaias no Cerrado do Leste do Maranhão, Brasil. Acta Bras. 1:13–16.; Salino et al. 2018SALINO, A., ARRUDA, A.J. & ALMEIDA, T.E. 2018. Ferns and lycophytes from Serra dos Carajás, an Eastern Amazonian Mountain range. Rodriguésia 69:1417–1434.; Prado & Hirai 2020PRADO, J. & HIRAI, R.Y. 2020. Adiantum (Pteridaceae) in Brazil: Key to the species and illustrations. Biota Neotrop. 20:e20201119.; Silva Junior et al. 2020SILVA JUNIOR, W.R., FERREIRA, A.W.C., ILKIU-BORGES, A.L. & FERNANDES, R.S. 2020. Ferns and lycophytes of remnants in Amazônia Maranhense, Brazil. Biota Neotrop. 20:e20200972. speciesLink 2023. (https://specieslink.net/). (Last access 21/01/2023).
https://specieslink.net/... ; Fernandes et al. 2022FERNANDES, R.S., SILVA, L.R., OLIVEIRA, S.S., OTTONI, F.P. & PIETROBOM, M.R. 2022. Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotrop. 22:e20211273.). The classification of high taxa follows PPG I (2016) and the authors’ abbreviations follow the International Plant Names Index (IPNI 2023IPNI 2023. International Plant Name Index. (http://www.ipni.org/). (last access 21/01/2023).
http://www.ipni.org/... ). The geographical distribution of the species was verified using Flora and Funga of Brazil (2023) and current articles of surveys of fern and lycophyte species in Maranhão (Silva Junior et al. 2020SILVA JUNIOR, W.R., FERREIRA, A.W.C., ILKIU-BORGES, A.L. & FERNANDES, R.S. 2020. Ferns and lycophytes of remnants in Amazônia Maranhense, Brazil. Biota Neotrop. 20:e20200972. speciesLink 2023. (https://specieslink.net/). (Last access 21/01/2023).
https://specieslink.net/... ; Fernandes et al. 2022FERNANDES, R.S., SILVA, L.R., OLIVEIRA, S.S., OTTONI, F.P. & PIETROBOM, M.R. 2022. Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotrop. 22:e20211273.).

The classification of the substrate(s) of occurrence of the taxa found follows Lellinger (2002)LELLINGER, D.B. 2002. A modern multilingual glossary for taxonomic pteridology. Pteridologia 3A. American Fern Society, Washington, 263p. and Zuquim et al. (2011)ZUQUIM, G., COSTA, F.R.C., PRADO, J. & TUOMISTO, H. 2011. Guia de Samambaias e Licófitas da REBIO Uatumã. 2nd ed. INPA, Manaus, 316p., with modifications according to Flora and Funga of Brazil (2023): terrestrial, epiphytic, hemiepiphytic, rupicolous, and aquatic. The environments of occurrence were subdivided into urban, swamp, Cerrado, terra firme Amazonian Forest, free-floating, and gallery forest according to observations made in the field. Table 1 contains the full list of the taxa found, organized by families, genera, and species/varieties, as well as information about the substrate and environment of occurrence, voucher(s) plus an identification key and images of some species/varieties, are also provided. The map of the study area was made using the software QGIS 3.22.14 and SIRGAS 2000 datum and IBGE data (2018).

To recognize the lycophytes and ferns found in this region an identification key is presented and it keys out each taxon at the level of species/varieties. In this work, the data presented in the identification key and Table 1 are complementary since in the Flora and Funga of Brazil (2023) there are no identification keys for families of lycophytes and ferns. The respective family of each taxon belongs can be found in Table 1.

Results

A total of 64 species were recognized, including 61 fern species, in 18 families and 38 genera, and three lycophyte species, in two genera and one family (Table 1). The most recorded substrate was terrestrial with 35 species (54.6%), followed by epiphytic with 15 species (23.4%), aquatic with four species (6.2%), rupicolous with three species (4.6%), and hemiepiphytic with two species (3.1%). Five species (7.8%) occurred in more than one type of substrate, terrestrial/rupicolous and epiphytic/terrestrial, and one species colonized three types of substrates: epiphytic, terrestrial, and rupicolous (see Table 1).

The Municipalities with the highest number of species were Axixá (32 spp.), Cachoeira Grande (27 spp.), and Morros (12 spp.), while the municipalities with the lowest number of species were Paço do Lumiar (4 spp.) and Raposa (3 spp.) (see Table 1). Although this region is an Amazonian-Cerrado ecotone, most of the species are Amazonian since they are associated with the vegetation close to the watercourses in these municipalities.

Each taxon from the studied region can be identified at the level of genus, species, and/or variety using the key below, and its respective family, plus other information, can be found in Table 1.

Identification key to the lycophyte and fern species in the Immediate Geographic Region of São Luís

• 1

  Plant leaves microphylls (with one medial vein), acicular ............2

• 1

  Plant leaves megaphylls (complex venation), simple (entire), decompound (pinnate or more divided), or scale-like ................. 4

• 2

  Plants prostrate, strobili erect ................................................................................................................. Pseudolycopodiella meridionalis

• 2

  Plants erect, strobili pendant ..................................................... 3

• 3

  Microphylls densely arranged; lateral branches ascending or suberect ................................................................................................................................................ Palhinhaea camporum (Fig. 3B)

• 3

  Microphylls sparse; lateral branches recurved downward ………………………..........…........... Palhinhaea cernua (Fig. 3B)

• 4

  Leaves scale-like; sporangia fused, forming a synangium ............................................................................................ Psilotum nudum

• 4

  Leaves simple or decompound; sporangia not fused, grouped in sori, sporocarps, or spikes ......................................................... 5

• 5

  Plants arborescent .......................................................................... 6

• 5

  Plants herbaceous ..................................................................... 7

• 6

  Sori with globose indusia ..................................... Cyathea delgadoi

• 6

  Sori lacking indusia ........................................ Cyathea microdonta

• 7

  Lamina translucid, thin, with one or two layers of cells; stomata absent; sporangia with oblique annulus .......................................... 8

• 7

  Lamina not translucid, with several layers of cells; stomata present; sporangia with apical or longitudinal annulus, or the annulus consisting of a slightly thickened lateral patch .............. 11

• 8

  Leaves entire, <3 cm long; true roots absent; false veinlets present in the lamina parallel to the true veins .......................................... 9

• 8

  Leaves pinnate, >3 cm long; true roots present; false veinlets absent or, when present, perpendicular to the true veins .............................................................................................................. 10

• 9

  Leaves with palmate venation; margin of the indusium without darkened cells ........................................................................................................................... Didymoglossum nummularium (Fig. 2A)

• 9

  Leaves with flabellate venation; margin of the indusium with darkened cells ......................... Didymoglossum punctatum

• 10

  Lamina lacking false veinlets ................................................................................................ Trichomanes hostmannianum (Fig. 3F)

• 10

  Lamina with false veinlets, these perpendicular to the true veins .................................................................................................................................................. Trichomanes pinnatum

• 11

  Plants aquatic, fixed to a substrate or free-floating .................... 12

• 11

  Plants terrestrial, epiphytic, hemiepiphytic, or rupicolous ................................................................................................... 15

• 12

  Plants aquatic, with roots fixed to a substrate …….................. 13

• 12

  Plants aquatic, free-floating ............................................... 14

• 13

  Lamina 4-foliolate; sporangia generally between 5−20, grouped into sporocarps ….............................. Marsilea polycarpa (Fig. 3G)

• 13

  Lamina 1–3-pinnate; sporangia numerous >20, grouped into grooves on lamina margins ……........................................................................................ Ceratopteris thalictroides (Fig. 4E)

• 14

  Adaxial surface of the floating lamina with conspicuous papillae; apex of lamina slightly incised .............................................................................................................. Salvinia auriculata (Fig. 4F)

• 14

  Adaxial surface of the floating lamina with minute papillae or papillae absent; apex of lamina round ........................................................................................................... Salvinia radula

• 15

  Sporangia sessile; annulus not interrupted by the pedicel of the sporangium, apical to subapical, or oblique ............................. 16

• 15

  Sporangia pedicellate; annulus interrupted by the pedicel of the sporangium ….................................................................. 20

• 16

  Sporangia with oblique annulus ................................................................................................................. Metaxya parkeri (Fig. 4A)

• 16

  Sporangia with apical to subapical annulus ....................... 17

• 17

  Plants with indefinite growth, reaching several meters long, scandent/climbing ….................................................................... 18

• 17

  Plants with defined growth, reaching up to 50 cm long......... 19

• 18

  Pinnules continuous with the petiolule .................................................................................................................. Lygodium venustum

• 18

  Pinnules articulate with the petiolule .......................................................................................................... Lygodium volubile

• 19

  Leaves with dichotomously divided or flabellate lamina ...................................................................................... Schizaea elegans

• 19

  Leaves with linear lamina ........................................................................................................ Actinostachys pennula (Fig. 3D)

• 20

  Petiole articulate with the rhizome ........................................... 21

• 20

  Petiole continuous with the rhizome ................................... 29

• 21

  Leaves with 1-pinnate or pinnatisect lamina ................................ 22

• 21

  Leaves with simple lamina .................................................. 25

• 22

  Lamina 1-pinnate; rachis not sulcate adaxially ....................................................................................... Pecluma plumula (Fig. 2D)

• 22

  Lamina pinnatisect; rachis sulcate adaxially ........................ 23

• 23

  Sorus borne on a receptacle formed on the tip of the single veinlet included in the areole ...............................… Serpocaulon triseriale

• 23

  Sorus borne on a receptacle formed on the tips of two parallel veinlets in the areole ………..............…….....……………... 24

• 24

  Sori distributed in two rows between the margin and costa of the segments ...................................................... Phlebodium aureum

• 24

  Sori distributed in more than two rows between the margin and costa of the segments ................ Phlebodium decumanum

• 25

  Rhizomes short-creeping, with clathrate scales; sori arranged in two or more rows between the costa and margin of the lamina ............................................................................................................... 26

• 25

  Rhizomes long-creeping, scales not clathrate; sori arranged in only one row between the costa and margin of the lamina .... 27

• 26

  Areoles in 8–18 rows between the costa and margin of the lamina ….............................…….. Campyloneurum brevifolium (Fig. 2C)

• 26

  Areoles in 7–8 rows between the costa and margin of the lamina …………..........…………... Campyloneurum phyllitidis

• 27

  Sori varying from round to oblong ...................................................................................................... Microgramma persicariifolia

• 27

  Sori round ................................................................................. 28

• 28

  Lamina venation visible adaxially; rhizome scales with ciliate margins .......................................... Microgramma lycopodioides

• 28

  Lamina venation not visible adaxially; rhizome scales with dentate margins ….............. Microgramma percussa (Fig. 4B )

• 29

  Sori pseudoacrostichoid or totally acrostichoid ....................... 30

• 29

  Sori marginal, submarginal, or between the veins ……...... 33

• 30

  Venation reticulate, areoles irregular to round, without included veinlets …………………………...….…….........................….... 31

• 30

  Venation areolate, areoles regular, in pairs, with the transverse veins producing excurrent veins that run toward the margin of the leaf ……………………............................................ 32

• 31

  Sori present along all pinnae of the fertile fronds …….............................................................................. Acrostichum danaeifolium

• 31

  Sori present only on the distal pinnae of the fertile fronds ................................................................... Acrostichum aureum

• 32

  Pinnae with serrate margins; sporangia glabrous .............................................................................................. Meniscium serratum

• 32

  Pinnae with crenulate margins; sporangia with paraphyses on the pedicel ………….....…….............. Meniscium hostmannii

• 33

  Rhizome scales clathrate ............................................................ 34

• 33

  Rhizome scales not clathrate .............................................. 38

• 34

  Sori with indusia ................................ Asplenium serratum (Fig. 3C)

• 34

  Sori lacking indusia ........................................................... 35

• 35

  Sori submarginal, parallel to the margin of the lamina ............... 36

• 35

  Sori arranged along the laminar tissue abaxially on the veins or between the veins ............................................................ 37

• 36

  Leaves linear (2−3 mm wide), with one row of areoles between the costa and margin of the lamina …………................. Vittaria lineata

• 36

  Leaves linear-elliptic (0.8−1.5 cm wide), with two to five rows of areoles between the costa and margin of the lamina ..................................................................................... Ananthacorus angustifolius

• 37

  Rhizomes long-creeping; leaves elliptic; sori on and between veins ………….................................………..….. Polytaenium citrifolium

• 37

  Rhizomes short-creeping; leaves oblanceolate; sori only on veins …............................................. Polytaenium guayanense

• 38

  Base of the petiole (cross-section) with two vascular bundles ........................................................................................................ 39

• 38

  Base of the petiole (cross-section) with one, three, or more vascular bundles ................................................................. 43

• 39

  Leaves 2-pinnate-pinnatifid; costa without grooves adaxially ……………………...................…... Macrothelypteris torresiana

• 39

  Leaves 1-pinnate-pinnatifid; costa sulcate adaxially ............ 40

• 40

  Furcate or stellate hairs present on the rachis and scales of the rhizome ..................................................................................... 41

• 40

  Furcate or stellate hairs absent on the rachis and scales of the rhizome ............................................................................... 42

• 41

  Venation free; sporangia glabrous ................... Goniopteris tristis

• 41

  Venation anastomosing; sporangia with setiform hairs ........................................................... Goniopteris poiteana (Fig. 2F)

• 42

  Rhizomes short-creeping; petiole and rachis pubescent .................................................................................... Christella hispidula

• 42

  Rhizomes long-creeping; petiole and rachis glabrous ……………...………………….……... Cyclosorus interruptus

• 43

  Sori linear, borne on the two sides of the costa; indusium opening introrsely .…..........................……. Telmatoblechnum serrulatum

• 43

  Sori round to linear, borne in a submarginal or median position on the lamina; indusium absent, present and opening extrorsely, or a false indusium present and formed by a revolute, modified (thin) lamina margin …......................................................... 44

• 44

  Sori with reniform indusium .......................................................... 45

• 44

  Sori indusium several shapes (not reniform) or false indusium present and formed by a revolute, modified (thin) lamina margin ............................................................................. 46

• 45

  Scales on the petiole base bicolor (blackish and light brown), with ciliate margins; sori submarginal ......……… Nephrolepis brownii

• 45

  Scales on the petiole base concolor (orangish), with entire margins; sori median ........................ Nephrolepis biserrata

• 46

  Sterile and fertile leaves dimorphic; sterile pinnae lanceolate and fertile pinnae linear …................ Cyclodium meniscioides (Fig. 3E)

• 46

  Sterile and fertile leaves monomorphic ............................. 47

• 47

  Sori circular, protected by a true indusium (formed abaxially) .................................................................................................... 48

• 47

  Sori linear, circular to oblong, covered by a true indusium or by a false indusium formed by a revolute, modified (thin) lamina margin ..................................................................................49

• 48

  Rhizomes erect; veins anastomosing; indusium glabrous ............................................................................................... Tectaria incisa

• 48

  Rhizomes creeping; veins free; indusium pubescent ......................................................................... Triplophyllum funestum

• 49

  Leaves more than 1.5 m long; lamina coriaceous ...................................................................... Pteridium esculentum var. harpianum

• 49

  Leaves up to 1 m long; lamina chartaceous or membranaceous ….......................................................................................... 50

• 50

  Indusia present, linear, abaxial ................................................. 51

• 50

  Indusia absent or with marginal false indusia ...................... 54

• 51

  Petiole alate; terminal pinna with non-prolonged apex …........... 52

• 51

  Petiole not alate; terminal pinna with prolonged apex ............ 53

• 52

  Laminae 2-pinnate; rachis reddish brown ......................................................................................................... Lindsaea divaricata

• 52

  Laminae 1-pinnate; rachis paleaceous to dark brown ……………...…......…………............... Lindsaea falcata (Fig. 2B)

• 53

  Rhizomes long-creeping; apical pinnule with entire margins.............................................. Lindsaea guianensis var. guianensis

• 53

  Rhizomes short-creeping; apical pinnule with crenulate to serrate margins .............................................. Lindsaea pallida

• 54

  Indusia absent …….................................................................... 55

• 54

  False indusia marginal ........................................................ 56

• 55

  Laminae 2-pinnate-pinnatifid; rachis glabrous; lamina with whitish farina abaxially .................................. Pityrogramma calomelanos

• 55

  Laminae 1-pinnate; rachis pubescent; lamina without whitish farina abaxially ............................... Hemionitis rufa (Fig. 2E)

• 56

  Sporangia borne on the abaxial surface of the lamina and protected by a false indusium that lacks veins; sori with paraphyses or not ………....................................................................................... 57

• 56

  Sporangia borne on the adaxial surface of a revolute lamina margin, forming a false indusium with veins …................. 60

• 57

  Sori without paraphyses …………… Adiantopsis radiata (Fig. 4C)

• 57

  Sori with paraphyses …………………………..………..... 58

• 58

  Laminae variegated on the adaxial surface, with whitish details ............................................................................... Pteris ensiformis

• 58

  Laminae not variegated ….................................................... 59

• 59

  Laminae 1-pinnate; veins free …….......................... Pteris vittata

• 59

  Laminae 2-pinnate-pinnatifid; veins partially areolate ................................................................................. Pteris tripartita

• 60

  Laminae 1-pinnate ..................................................................... 61

• 60

  Laminae 2-pinnate ............................................................... 62

• 61

  Pinnae flabellate; veins free ……..................... Adiantum deflectens

• 61

  Pinnae lanceolate; veins irregularly anastomosing …............................................................................... Adiantum dolosum

• 62

  Rhizomes, petioles, and rachis completely covered with scales; sori 1 or 2(3) per pinnule …………....…. Adiantum pulverulentum

• 62

  Rhizomes, petioles, and rachis with sparse scales; sori more than 3 per pinnule ................................................................ 63

• 63

  Laminae glabrous abaxially; false indusium glabrous ............................................................................ Adiantum latifolium (Fig. 4D)

• 63

  Laminae with septate hairs abaxially; false indusium with septate hairs ……................................ Adiantum terminatum

Discussion

The total number of fern and lycophyte species collected during this survey was 41.7% of the species recorded for the state of Maranhão (Silva Junior et al. 2020SILVA JUNIOR, W.R., FERREIRA, A.W.C., ILKIU-BORGES, A.L. & FERNANDES, R.S. 2020. Ferns and lycophytes of remnants in Amazônia Maranhense, Brazil. Biota Neotrop. 20:e20200972. speciesLink 2023. (https://specieslink.net/). (Last access 21/01/2023).
https://specieslink.net/... ; Fernandes et al. 2022FERNANDES, R.S., SILVA, L.R., OLIVEIRA, S.S., OTTONI, F.P. & PIETROBOM, M.R. 2022. Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotrop. 22:e20211273.; Flora and Funga of Brazil 2023). It is the third largest study in number of taxa recorded for Maranhão State (Figures 3 and 4).

Some taxa presented in this study represent new records for Maranhão State or new records for the Northeast Region of Brazil. These novelties are highlighted in Table 1 with one or two stars, respectively. Although this list is similar to the list presented by Silva Junior et al. (2023)SILVA JUNIOR, W.R., PRADO, J., FERREIRA, A.W.C. & OLIVEIRA, H.C. 2023. Floristic similarity of lycophytes and ferns in the Amazonia/Cerrado transition zone in the central region of northern Maranhão state, Brazil. Sci. Plena 19(6):e061201. DOI: 10.14808/sci.plena.2023.061201.
https://doi.org/10.14808/sci.plena.2023.... these results were not previously highlighted by the authors as being new records. Additionally, in the present list, Adiantopsis radiata (L.) Fée is another novelty not previously recorded by Silva Junior et al. (2023)SILVA JUNIOR, W.R., PRADO, J., FERREIRA, A.W.C. & OLIVEIRA, H.C. 2023. Floristic similarity of lycophytes and ferns in the Amazonia/Cerrado transition zone in the central region of northern Maranhão state, Brazil. Sci. Plena 19(6):e061201. DOI: 10.14808/sci.plena.2023.061201.
https://doi.org/10.14808/sci.plena.2023.... .

The first study to record fern species in the Immediate Geographic Region of São Luís was presented by Bastos & Cutrim (1999). It was conducted in Sacavém Park in São Luís. Although the present study was not carried out in the same place as Bastos & Cutrim (1999), we found all the species reported by them in other parts of the study area, except for Adiantum raddianum C.Presl and Lindsaea stricta (Sw.) Dryand. Another study that recorded fern species in the study region is Silva Junior et al. (2018)SILVA JUNIOR, W.R., FERNANDES, R.S. & FERREIRA, A.W.C. 2018. First record of the exotic fern Pteris tripartita Sw. (Pteridaceae) for the Maranhão state, Northeastern Brazil. Biod. Int. J. 2:161–163., who reported the occurrence of Pteris tripartita Sw. (an introduced fern species in Brazil) in the municipality of São José de Ribamar. In the present study, this species was also collected in the municipality of São Luís.

The most representative family was Pteridaceae with 17 species, which was also reported in two other studies carried out in Maranhão, one in areas of the Amazonian Forest (Silva Junior et al. 2020SILVA JUNIOR, W.R., FERREIRA, A.W.C., ILKIU-BORGES, A.L. & FERNANDES, R.S. 2020. Ferns and lycophytes of remnants in Amazônia Maranhense, Brazil. Biota Neotrop. 20:e20200972. speciesLink 2023. (https://specieslink.net/). (Last access 21/01/2023).
https://specieslink.net/... ) and another in areas of Cerrado (Fernandes et al. 2022FERNANDES, R.S., SILVA, L.R., OLIVEIRA, S.S., OTTONI, F.P. & PIETROBOM, M.R. 2022. Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotrop. 22:e20211273.). The family Pteridaceae is one of the most diverse in Brazil and their genera have wide geographic distribution, because of it, it has been reported as one of the commonest in studies of ferns in Brazil (e.g., Maciel & Pietrobom 2010MACIEL, S. & PIETROBOM, M.R. 2010. Pteridaceae (Polypodiopsida) do Campo Experimental da Embrapa Amazônia Oriental, município de Moju, estado do Pará, Brasil. Acta Bot. Brasil. 24:12–23.; Winter et al. 2011WINTER, S.L.S., SYLVESTRE, L.S. & PRADO, J. 2011. O gênero Adiantum (Pteridaceae) no estado do Rio de Janeiro, Brasil. Rodriguésia 62:663–681.; Miranda et al. 2015MIRANDA, C., ILKIU-BORGES, A.L. & MACIEL, S. 2015. Avencas (Adiantum L. – Pteridaceae) do município de Acará, Pará, Brasil. Biota Amaz. 5:26–30.; Menezes & Labiak 2020MENEZES, E.A. & LABIAK, P.H. 2020. Sinopse de Licófitas e Samambaias do Parque Nacional da Amazônia, Pará, Brasil. Rodriguésia 71e02032018.; Silva Junior et al. 2020SILVA JUNIOR, W.R., FERREIRA, A.W.C., ILKIU-BORGES, A.L. & FERNANDES, R.S. 2020. Ferns and lycophytes of remnants in Amazônia Maranhense, Brazil. Biota Neotrop. 20:e20200972. speciesLink 2023. (https://specieslink.net/). (Last access 21/01/2023).
https://specieslink.net/... ; Fernandes et al. 2022FERNANDES, R.S., SILVA, L.R., OLIVEIRA, S.S., OTTONI, F.P. & PIETROBOM, M.R. 2022. Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotrop. 22:e20211273.; Flora and Funga of Brazil 2023).

Adiantum (Pteridaceae) had the highest number of species (five). This was expected since it has species that colonize various environments and is often the most diverse genus in studies that report the occurrence of Pteridaceae (Maciel & Pietrobom 2010MACIEL, S. & PIETROBOM, M.R. 2010. Pteridaceae (Polypodiopsida) do Campo Experimental da Embrapa Amazônia Oriental, município de Moju, estado do Pará, Brasil. Acta Bot. Brasil. 24:12–23.; Winter et al. 2011WINTER, S.L.S., SYLVESTRE, L.S. & PRADO, J. 2011. O gênero Adiantum (Pteridaceae) no estado do Rio de Janeiro, Brasil. Rodriguésia 62:663–681.; Miranda et al. 2015MIRANDA, C., ILKIU-BORGES, A.L. & MACIEL, S. 2015. Avencas (Adiantum L. – Pteridaceae) do município de Acará, Pará, Brasil. Biota Amaz. 5:26–30.; Silva Junior et al. 2020SILVA JUNIOR, W.R., FERREIRA, A.W.C., ILKIU-BORGES, A.L. & FERNANDES, R.S. 2020. Ferns and lycophytes of remnants in Amazônia Maranhense, Brazil. Biota Neotrop. 20:e20200972. speciesLink 2023. (https://specieslink.net/). (Last access 21/01/2023).
https://specieslink.net/... ; Oliveira et al. 2021OLIVEIRA, M.H.V., TORKE, B.M. & ALMEIDA, T.E. 2021. An inventory of the ferns and lycophytes of the Lower Tapajós River Basin in the Brazilian Amazon reveals collecting biases, sampling gaps, and previously undocumented diversity. Brittonia 73:459–480.; Fernandes et al. 2022FERNANDES, R.S., SILVA, L.R., OLIVEIRA, S.S., OTTONI, F.P. & PIETROBOM, M.R. 2022. Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotrop. 22:e20211273.).

Another genus of Pteridaceae that exhibited peculiarities in the study area was Acrostichum L. because its two species occur in different environments. Acrostichum aureum occurs exclusively in coastal areas and is associated mainly with mangroves, while A. danaeifolium was observed in swamps that were further away from coastal vegetation.

The second most representative family was Polypodiaceae, with nine taxa. Polypodiaceae are poorly represented in inventories of ferns that have been carried out in Maranhão (Silva Junior et al. 2020SILVA JUNIOR, W.R., FERREIRA, A.W.C., ILKIU-BORGES, A.L. & FERNANDES, R.S. 2020. Ferns and lycophytes of remnants in Amazônia Maranhense, Brazil. Biota Neotrop. 20:e20200972. speciesLink 2023. (https://specieslink.net/). (Last access 21/01/2023).
https://specieslink.net/... ; Fernandes et al. 2022FERNANDES, R.S., SILVA, L.R., OLIVEIRA, S.S., OTTONI, F.P. & PIETROBOM, M.R. 2022. Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotrop. 22:e20211273.). However, the number of new records of this family is increasing for the state as revealed by Silva Junior et al. (2020)SILVA JUNIOR, W.R., FERREIRA, A.W.C., ILKIU-BORGES, A.L. & FERNANDES, R.S. 2020. Ferns and lycophytes of remnants in Amazônia Maranhense, Brazil. Biota Neotrop. 20:e20200972. speciesLink 2023. (https://specieslink.net/). (Last access 21/01/2023).
https://specieslink.net/... .

The municipalities of Axixá, Cachoeira Grande, and Morros had the highest number of fern and lycophyte species. This is probably because they have several water bodies, such as swamps and tributaries of the Munim River, as well as upland and gallery forests with continuous vegetation and greater humidity throughout the year, which favor the physiology and reproduction of ferns. On the other hand, in the municipalities with the fewest species (Paço do Lumiar and Raposa) there are not many areas with native vegetation due to a greater amount of urbanization.

In the study region, only three fern species occurred specifically in the Cerrado vegetation: Actinostachys pennula (Sw.) Hook., Pteridium esculentum var. harpianum, and Schizaea elegans (Vahl) Sw. This vegetation has a dry period between July and December, showing that these species are more tolerant to water stress. The three species of lycophytes occurred in swampy areas and veredas, which are sunny and humid environments throughout the year. However, it was noted that Pseudolycopodiella meridionalis (Underw. & Loyd) Holub is less common than the other two species of lycophytes.

The most observed species in the study area were Nephrolepis biserrata (Sw.) Schott, Phlebodium decumanum (Willd.) J.Sm., and Telmatoblechnum serrulatum (Rich.) Perrie, D.J.Ohlsen & Brownsey, which occur in more than eight municipalities. Nephrolepis biserrata was observed mainly as epiphytic or rupicolous. Pteris ensiformis Burm. f. was found in three municipalities in the study area. It is native to Asian countries and considered naturalized in Brazil. Its main use is for ornamental purposes due to its variegated leaves (Costa et al. 2020COSTA, F.S.N., MOREIRA, F.F. & SYLVESTRE, L.S. 2020. Samambaias e licófitas em um afloramento rochoso costeiro no Estado do Rio de Janeiro, Brasil. Hoehnea 47:1–7.; Freitas et al. 2021FREITAS, A.P., SOUZA, M.C. & MILANEZE-GUTIERRE, M.A. 2021. Samambaias de um fragmento florestal urbano no estado do Paraná, Brasil. Pesquisas, Bot. 75:223–235.). Macrothelypteris torresiana (Gaud.) Ching is also naturalized and widely distributed in Brazil (Hirai et al. 2016HIRAI, R.Y., GISSI, D.S. & PRADO, J. 2016. Criptógamos do Parque Estadual das Fontes do Ipiranga, São Paulo, SP, Brasil. Pteridophyta: 22. Thelypteridaceae e lista atualizada dos táxons. Hoehnea 43:39–56.). Exotic species of ferns are commonly recorded in natural areas in the state of Maranhão (Silva Junior et al. 2018SILVA JUNIOR, W.R., FERNANDES, R.S. & FERREIRA, A.W.C. 2018. First record of the exotic fern Pteris tripartita Sw. (Pteridaceae) for the Maranhão state, Northeastern Brazil. Biod. Int. J. 2:161–163.; Silva Junior et al. 2020SILVA JUNIOR, W.R., FERREIRA, A.W.C., ILKIU-BORGES, A.L. & FERNANDES, R.S. 2020. Ferns and lycophytes of remnants in Amazônia Maranhense, Brazil. Biota Neotrop. 20:e20200972. speciesLink 2023. (https://specieslink.net/). (Last access 21/01/2023).
https://specieslink.net/... ), indicating human influence and the need for environmental monitoring because exotic fern species can negatively affect the native flora (Silva Junior et al. 2018SILVA JUNIOR, W.R., FERNANDES, R.S. & FERREIRA, A.W.C. 2018. First record of the exotic fern Pteris tripartita Sw. (Pteridaceae) for the Maranhão state, Northeastern Brazil. Biod. Int. J. 2:161–163.).

This set of data from the Immediate Geographical Region of São Luís was the subject of some floristic similarity analysis by Silva Junior et al. (2023)SILVA JUNIOR, W.R., PRADO, J., FERREIRA, A.W.C. & OLIVEIRA, H.C. 2023. Floristic similarity of lycophytes and ferns in the Amazonia/Cerrado transition zone in the central region of northern Maranhão state, Brazil. Sci. Plena 19(6):e061201. DOI: 10.14808/sci.plena.2023.061201.
https://doi.org/10.14808/sci.plena.2023.... . In this similarity study, the species found were mostly Amazonian. The prevalence of Amazonian species is probably because ferns and lycophytes mostly occur in wet environments. In the Cerrado, the effect of the dry season is more noticeable than in the Amazonia, which makes it difficult for ferns and lycophytes to colonize. Even in Cerrado areas in Maranhão, most species occur in gallery forests, which have a more humid environment throughout the year (Silva Junior et al. 2023SILVA JUNIOR, W.R., PRADO, J., FERREIRA, A.W.C. & OLIVEIRA, H.C. 2023. Floristic similarity of lycophytes and ferns in the Amazonia/Cerrado transition zone in the central region of northern Maranhão state, Brazil. Sci. Plena 19(6):e061201. DOI: 10.14808/sci.plena.2023.061201.
https://doi.org/10.14808/sci.plena.2023.... ).

Conclusion

This study increased what is known about the composition of fern and lycophyte flora in the central region of Northern Maranhão, which was a poorly known area. Maranhão has an extensive ecotonal zone between the Amazon and Cerrado biomes, and there is a lack of studies of lycophytes and ferns in this region. The number of records of these plants is constantly increasing in Maranhão (Silva Junior et al. 2020SILVA JUNIOR, W.R., FERREIRA, A.W.C., ILKIU-BORGES, A.L. & FERNANDES, R.S. 2020. Ferns and lycophytes of remnants in Amazônia Maranhense, Brazil. Biota Neotrop. 20:e20200972. speciesLink 2023. (https://specieslink.net/). (Last access 21/01/2023).
https://specieslink.net/... ; Fernandes et al. 2022FERNANDES, R.S., SILVA, L.R., OLIVEIRA, S.S., OTTONI, F.P. & PIETROBOM, M.R. 2022. Ferns and lycophytes in Chapada das Mesas National Park and surroundings, Maranhão state, Brazil. Biota Neotrop. 22:e20211273.; Silva Júnior et al. 2023SILVA JUNIOR, W.R., PRADO, J., FERREIRA, A.W.C. & OLIVEIRA, H.C. 2023. Floristic similarity of lycophytes and ferns in the Amazonia/Cerrado transition zone in the central region of northern Maranhão state, Brazil. Sci. Plena 19(6):e061201. DOI: 10.14808/sci.plena.2023.061201.
https://doi.org/10.14808/sci.plena.2023.... ), as seen by the results of this study. This mosaic of biomes promotes a variety of environments conducive to the propagation of lycophytes and ferns that need to be studied before they disappear.

Acknowledgments

The authors thank the following: the Graduate Program in Biodiversity, Environment, and Health at the State University of Maranhão for the opportunity to carry out this research; the funding agency Fundação de Amparo à Pesquisa e do Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA) for the Editais Universais 00430/2015, 01312/2019, and BM-01024/21 (45379/2021); the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the funding to carry out research in Maranhão and the master’s scholarship given to the first author; and Dr. Francisca Helena Muniz, Curator of the Rosa Mochel Herbarium (SLUI), for her help in depositing specimens and sending duplicates to the SP herbarium. Nathan Smith for revising the English language.

Data Availability

Supporting data are available at <https://data.scielo.org/dataset.xhtml?persistentId=doi:10.48331/scielodata.PWWYNZ>.

References

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