Selaginella P.Beauv. (Selaginellaceae) in the state of Maranhão, northeastern, Brazil: A floristic survey and a new record for the Cerrado domain

Abstract This work is a floristic study of Selaginella in Maranhão. The species survey is based on collections from fieldwork conducted between April 2006 and February 2023 and specimens from Maranhão deposited at the CCAA, HBRA, MG, and SLUI herbaria. Ten species were identified: Selaginella conduplicata, S. convoluta, S. erythropus, S. flagellata, S. gynostachya S. marginata, S. minima, S. radiata, S. simplex, and S. sulcata. We report the first record of S. gynostachya for Maranhão and the Cerrado domain in Brazil. Until now, this species was only known from areas of Amazonia. We provide a map with records, an identification key, and comments about the identification and geographic distribution of Selaginella species in Maranhão state. For the new record, we also provide photos.


Introduction
Selaginella P.Beauv. is the most speciose genus in the class Lycopodiopsida (lycophytes).It is estimated that there are approximately 700 species of Selaginella; the only genus in Selaginellaceae Wilk., which has a cosmopolitan distribution (PPGI 2016).However, the highest diversity of species is mostly found in the tropics (Jermy 1990, Valdespino 1993, Fraile et al. 1995).
In Brazil, Selaginella is represented by 97 species distributed in all phytogeographic domains, and with 38 species endemic to the country (Góes-Neto et al. 2023).Most of the diversity of the genus in Brazil is in the Amazonia (53 spp.) and the Cerrado domains (11 spp.) (Góes-Neto et al. 2023).The Brazilian Cerrado is notoriously under-collected for all groups of plants, including those in protected areas.For Maranhão, recent studies have increased the number of known Selaginella from five (Góes-Neto et al. 2023) to nine species, most of which occur in the Cerrado (Almeida et al. 2020, Fernandes et al. 2022).
The objective of this work is to provide a list of the Selaginella species occurring in the state of Maranhão, and to newly document the occurrence of a species previously undocumented for the Cerrado domain in Brazil for which a corresponding illustration.Furthermore, a key to identify currently known Selaginella species as occurring in the state of Maranhão is provided, as well as a distribution map for each of these taxa.Furthermore, under each species we provide comments related to habitat and distribution, as well as morphological characters to help identify them.

Material and Methods
Maranhão has a tropical, rainy climate (Alvares et al. 2013), average annual temperature between 25 and 26° C, average annual precipitation between 1400 and 1800 mm and is one of the states in northeastern Brazil with the lowest hydric deficit (Martins & Oliveira 2011).The dry period lasts five or six months (July to November or December), when the hydric deficit is 150-300 mm, and the rainy period also lasts five or six months (January to May or June) and is most intense between February and March (IMESC 2021).
Maranhão is an extremely relevant State in terms of biodiversity, housing three different phytogeographic domains, as well as transition areas between them, such as: Amazonia, occupying around 35% of the area of the state territory; Cerrado, around 64%; and Caatinga, around 1%. Furthermore, Maranhão has a large coastal region (around 640 km), also comprising floral elements characteristic of coastal zones, as well as transition zones towards the interior, between this large coastal region, and its continental phytogeographic domains, making the State ecosystems even more interesting and complex (Ab'Saber 2002, Rebêlo et al. 2003, Almeida & Vieira 2010, Spinelli-Araujo et al. 2016, Koerber et al. 2022, Vieira et al. 2023).Areas with cocais vegetation in Maranhão (where Attalea speciosa Mart.ex Spreng., the babaçu palm, is predominant) are locations modified by humans (Oren 1988, Santos-Filho et al. 2013).
The Amazonian region of Maranhão is part of the Belém Center of Endemism, with an area of 243,000 km 2 , limited the Tocantins River to the west and the Pindaré River to the east.Less than a third of the forests in the Belém Center of Endemism are preserved, making it the most threatened area of endemism in Brazilian Amazon (Silva et al. 2005, Almeida & Viera 2010).The Cerrado in Maranhão is one of the most threatened areas in Brazil due to increased agricultural practices in the last decades, especially the cultivation of soybeans, corn and cotton (EMBRAPA, 2023).According to Castro & Martins (1999), Maranhão has the largest area of Cerrado in the Northeastern Brazil (328,366 km 2 ), corresponding to around 60% of the Cerrado in this region.Around 50% of the Brazilian Cerrado has been lost and what remains is becoming increasingly fragmented (Rodrigues et al. 2022).
This study is based on an analysis of material deposited in the CCAA, EAC, HBRA, MG, and SLUI herbaria (acronyms according to Thiers 2023) and field expeditions made between April 2006 and February 2023.The fieldwork was mainly conducted in the following protected areas and surroundings in Maranhão: Área de Proteção Ambiental Inhamum, Reserva Biológica do Gurupi, Parque Nacional Chapada das Mesas, Parque Estadual do Mirador, Reserva Extrativista Chapada Limpa, and Área de Relevante Interesse Ecológico Itamacaoca (Figure 1).
The key below to identify species in Maranhão is based on material here studied and documented, followed by corresponding taxon information.Ferreira,522,523 (CCAA).

Identification key to the Selaginella species in Maranhão
Identification.Selaginella erythropus is characterized by the dark red to reddish stem, patent to ascendent lateral microphylls that are ovate in the most basal portion, and become ovate-lanceolate, lanceolate or slightly falcate towards the apex of the branch, acroscopic margin that is hyaline and ciliate along the basal portion and denticulate along the apical portion, and basiscopic margin that is greenish, narrowly hyaline, and entire or denticulate to serrulate along the apical portion.
Habitat and distribution.Costa Rica, Colombia, Ecuador, Peru, Brazil (Bahia, Ceará, Distrito Federal, Goiás, Maranhão, Mato Grosso, Mato Grosso do Sul, Minas Gerais, Pará, Paraíba, Piauí, Rio Grande do Norte, Rio de Janeiro, and Tocantins) and Bolivia.In the study area, it grows in closed gallery forests in sandy soils and on rocks near waterfalls.Identification.Selaginella flagellata is characterized by the longaristate dorsal microphylls, with an arista that is often half the length of the microphyll and an asymmetric base that sometimes forms a short external auricle, and axillary microphylls with conspicuously hyaline margins that are ciliate at the base and turn denticulate towards the apex.Sterile individuals of the species can be identified by the stem apex which is usually flagelliform.

Selaginella flagellata
Habitat and distribution.Mexico, Guatemala, Honduras, Nicaragua, Costa Rica, Panama, Colombia, Venezuela, Trinidad and Tobago, Guyana, Suriname, French Guiana, Ecuador, Peru, Brazil (Acre, Amapá, Amazonas, Maranhão, Mato Grosso, Pará, Piauí, Rondônia, and Tocantins) and Bolivia.In the study area, this species grows in closed gallery forests, in sandy ravines, and almost always in shady areas.Identification.Selaginella minima is 1-9 cm tall and has totally dimorphic microphylls along the length of its stem.The margins of the lateral and dorsal microphylls and sporophylls have 2 to 5 rows of idioblasts that give the border of the leaves a whitish appearance.The dorsal microphylls are ovate and have an asymmetric (the internal base tends to be truncate and the external base forms a poorly differentiated external auricle) or oblique base, margins that are serrate to finely serrate or short-ciliate along the proximal half and finely serrate along the distal half, with an internal side that is serrate to finely serrate, and an apex that is acute to acuminate.In addition, rarely, there are scattered, short trichomes on the upper surface of the lateral microphylls, mainly towards the basiscopic half of the lamina (see the illustration of this species in Mickel et al. 2004 Identification.Selaginella simplex is a small, delicate plant that reaches 5 cm long.It can also be characterized by the ovate to ovate-elliptic lateral microphylls with a rounded base, acroscopic base sometimes overlapping the stem, acroscopic margin greenish, narrowly hyaline, denticulate at the base, serrulate towards the apex, basiscopic margin greenish, narrowly hyaline, serrulate mainly along the upper middle, and lower surface of the lateral microphylls occasionally with idioblasts.The dorsal microphylls are around 1.0 mm apart and have margins that are greenish, narrowly hyaline and denticulate, an upper surface without idioblasts or stomata, and an acuminate to long-acuminate apex.
(Góes- Neto et al. 2015)ts in the upper surface of the axillary microphylls and the denticulate to ciliate-denticulate margins of the lateral microphylls are variable characteristics that must be carefully observed(Cremers & Boudrie 2007).Selaginella gynostachya, a species recently recorded for Brazil(Góes- Neto et al. 2015), resembles S. karowtipuensis Valdespino (which occurs in Guyana).However, the latter differs because it has dorsal microphylls with a subcordate to rounded base, idioblasts in the upper surface of the lateral microphylls and dorsal microphylls with a long-acuminate to short-aristate apex, while S. gynostachya has dorsal microphylls with a sub-truncate to rounded base, lacks idioblasts in the upper surface of the lateral microphylls, and has elliptic to ovate-elliptic or widely ovate dorsal microphylls with an acute to short-acuminate apex.This is the first record of this species for the Brazilian Cerrado and Maranhão.Previous records are all from areas in Amazonia, Brazil (Flora e Funga do Brasil 2023).Habitat and distribution.Venezuela, Guyana, French Guiana, and Brazil.In Brazil, this species was known only from Amazonia, in Pará (Flora e Funga do Brasil 2023), and it is now also known to occur in the Cerrado in Maranhão.In the study area, S. gynostachya grows in closed gallery forests near water courses and on rocks near waterfalls.Uruguay.In the study area, it grows in the interior of gallery forests and on rocky outcrops exposed to light near waterfalls.
Habitat and distribution.Mexico, Costa Rica, Panama, Venezuela,  Trinidad and Tobago, Ecuador, Brazil (Bahia, Goiás, Maranhão, Mato  Grosso, Pará, Pernambuco, and Sergipe)and Bolivia.It occurs in gallery forests in sandy, wet ravines and on wet rocks near waterfalls.