Pteridaceae in remnants of Cerrado in Maranhão state, Brazil

. The Pteridaceae is one of the most diverse families of ferns, with representatives adapted to diverse habitats ranging from aquatic to dry environments. It is the most species-rich family of ferns in the Brazilian Cerrado, although it is still poorly known in some areas of this domain in Maranhão state. Our objective was to investigate the diversity of Pteridaceae in Cerrado remnants in Maranhão. We based our study on the morphological analyses of specimens deposited in the herbaria, as well as additional new collections made by us and collaborators. Five genera comprising 15 species were recorded. Illustrations, an identification key

Pteridaceae is one of the largest families of ferns. It comprises 53 genera and 1,211 species (PPG I 2016), which is approximately 10% of the class. In Brazil, the diversity of Pteridaceae is estimated to be 24 genera and 207 species, of which 71 are endemic (Prado et al. 2020). This diversity is directly related to the fact that the life forms in this family (aquatic, epiphytic, rupicolous, terrestrial) are the most varied among ferns, the representatives of the family have adapted to a wide range of habitats (aquatic to xeric), and these adaptations differ from those found in other fern families (Schuettpelz et al. 2007).
Species of Pteridaceae are morphologically diverse. One characteristic of the group is that the sporangia, on the abaxial lamina surface, are along the veins or on the margin of the segments, and generally protected by a false indusium, or covering the entire abaxial surface (acrostichoid sori) (Tryon and Tryon 1982;Schuettpelz et al. 2007).

ANNOTATED LIST OF SPECIES
In addition to morphological characters, authors have lately started to include molecular data and phylogenetic analyses. Smith et al. (2006) recognized five monophyletic groups in Pteridaceae which could be treated as families or subfamilies: Parkeriaceae or Parkerioideae, Adiantaceae or Adiantoideae, Cryptogrammaceae, Sinopteridaceae or Cheilanthoideae, and Pteridaceae s.str. or Pteridoideae. In the PPG I (2016) classification, there are five subfamilies of Pteridaceae: Parkerioideae, Cryptogrammoideae, Pteridoideae, Vitarioideae, and Cheilanthoideae.
In Brazil, floristic and taxonomic studies specifically of the family have been conducted in various domains at the local level, for example, Prado (1992), Prado (1997), Pietrobom and Barros (2002), Nonato and Windisch (2004), Prado (2004), Prado (2005bPrado ( , 2005cPrado ( , 2005d, Maciel and Pietrobom (2010), and Prado et al. (2017). Other notable works are Winter et al. (2011) and Miranda et al. (2015), who studied Adiantum L. The greatest diversity of Pteridaceae has been recorded in the Atlantic Forest of Brazil, which is a center of endemism for ferns in South America (Tryon 1972;. In the Cerrado domain, 50 species of Pteridaceae have been recorded by Prado et al. (2020).
For the Northeast Region of Brazil, there is only one published work on Pteridaceae (Pietrobom and Barros 2002). The known diversity of the family in this region has been mainly reported in floristic inventories of ferns and lycophytes, notably by Pietrobom and Barros (2003), Santiago et al. (2004), Pietrobom and Barros (2006), Matos et al. (2010), Xavier et al. (2012), and Santiago et al. (2014).
Maranhão state is in at the transition zone between three phytogeographic domains, the Amazon, the Cerrado, and the Caatinga, and this favors greater taxonomic diversity (IBGE 2004;Muniz 2006;Stella 2011), but for Pteridaceae, only 10 genera, 33 species, and three varieties have been recorded (Prado et al. 2020;Fernandes et al. 2022). Of these species, 15 occur in the Amazon domain and 21 in areas of Cerrado (Fernandes et al. 2007(Fernandes et al. , 2010(Fernandes et al. , 2022Conceição and Rodrigues 2010;Conceição et al. 2015;Silva et al. 2017;Prado et al. 2020). This is almost half of the total number of 50 species recorded for the family in the Brazilian Cerrado domain (Prado et al. 2020).
There are no studies on specifically the Pteridaceae of Maranhão. The known diversity of the family is based on general floristic inventories of ferns and lycophytes (Bastos and Cutrim 1999;Fernandes et al. 2007Fernandes et al. , 2010Fernandes et al. , 2022Conceição and Rodrigues 2010;Conceição and Ruggieri 2010;Conceição et al. 2015;Silva et al. 2017;Silva Junior et al. 2018. These studies do not include identification keys to the genera, species and varieties, nor do they include illustrations of the taxa, complete lists of georeferenced material, or comments on life forms and habitats. The objective of our study was to investigate the diversity of Pteridaceae in Cerrado remnants in Maranhão state based on new collections, including ours, and material deposited in the Centro de Ciências Agrárias e Ambientais (CCAA) and São Paulo (SP) herbaria. An identification key, illustrations, and comments about habitat and environmental occurrence are provided for the taxa.

Study Area
The Cerrado vegetation in Maranhão are in the eastern and center-south parts of the state and cover 216,688 km 2 , which corresponds to 65% of the land area of Maranhão (IBGE 2004;Sano et al. 2008). This vegetation has zones that are in contact with the Amazon Forest, the Restinga, and the Caatinga, occurring at elevations from the coast of the Atlantic Ocean to around 700 m in the Chapadões, in the municipality of Alto Parnaíba in the southern part of the state (Sano et al. 2007;Moraes 2014;Silva-Moraes et al. 2018).
The Cerrado vegetation in the state comprises the following formations: savanna (also known as Campo Cerrado, Campo Sujo do Cerrado, and Campo Limpo de Cerrado); forest (also known as Cerradão); and pioneer formations, represented by mangroves and restingas on the coast (IBGE 2011;Spinelli-Araújo et al. 2016).

Methods
Our study is mainly based on an analysis of specimens from the CCAA herbarium of the Universidade Federal do Maranhão (UFMA), and the SP herbarium of the Instituto de Pesquisas Ambientais (IPA), as well as recent collections made by us and our collaborators from the Laboratório de Sistemática Vegetal, Centro de Ciências Agrárias e Ambientais at UFMA. The recent collections were made in Parque Nacional Chapada das Mesas, Reserva Extrativista Chapada Limpa, and Mata da Itamacaoca between September 2019 and April 2020. Figure 1 shows the locations and municipalities where all the collections were made.
The collected material was processed on techniques for ferns (Silva 1984;Windisch 1992) and deposited in CCAA. Some duplicates were sent to Museu Paraense Emílio Goeldi (MG) and SP for identification or confirmation of the determinations.
For the species studied, taxonomic and ecological comments are provided based on the material examined and the literature. The geographic distribution of each species follows the classification by Labiak and Prado (1998): (1) pantropical, species that occur in all tropical regions of the world; (2) Neotropical, species that occur in tropical and/or subtropical regions of America, including the southern United States; (3) species exclusive to South America; and (4) species endemic to Brazil. For geographic distribution of species, we used Moran and Riba (1995), Smith and Lellinger (1995), Mickel and Smith (2004), Labiak and Prado (2007), Kessler et al. (2017), Prado et al. (2017), and Prado et al. (2022). Flora e Funga do Brasil (2022) was used for the geographic distributions in Brazil.

Results
We identified 15 taxa of Pteridaceae from Cerrado remnants in Maranhão state. These included 15 species distributed in five genera: Adiantum L., Ceratopteris Brongn., Cheilanthes Sw., Pityrogramma Link, and Vittaria Sm. Adiantum was the most diverse, with 11 species. One species of this genus, Adiantum sp., has an unusual morphology with poorly formed, or aborted, spores and is probably an undescribed hybrid. Additional research is needed to better understand this material. The data has already been added to Flora e Funga do Brasil (2022).
Most species have a Neotropical distribution (10 species), one is pantropical, one is exclusive to South America (Adiantum sinuosum Gardner), and two are endemic to Brazil (Adiantum intermedium Sw. and Cheilanthes pohliana Mett.).
Information on each taxon is provided in alphabetical order by genus, then species, following the key.  (Prado and Hirai 2020). In the study area, 11 species of Adiantum have been recorded. Adiantum is terrestrial, or rarely rupicolous, and can be easily recognized by the presence of veins on the false indusia, sporangia on the revolute margin of the lamina, and trilete spores (Prado and Hirai 2020). Identification. Adiantum deflectens has an erect rhizome, 1-pinnate lamina, flabellate, articulate pinnae with denticulate sterile margins, and an oblong to lunate false indusium. Adiantum delicatulum Mart., which also occurs in the Northeast Region in the Caatinga domain, is similar to A. deflectens because of its 1-pinnate lamina and flabellate, articulate pinnae; however, it can be differentiated by its ciliate, sterile pinna margins and rounded false indusium (Kessler et al. 2017).

Adiantum deflectens
Distribution and ecology. Neotropical. In Brazil, it is recorded in AL, BA, CE, DF, ES, GO, MA, MG, MS, MT, PA, PB, PE, PI, RJ, RN, RO, SE, SP, and TO. It occurs in ravines, on the margins of trails, and in the interior of secondary forests (Fernandes et al. 2007). This species is very common in the study area and has been recorded as terrestrial and sometimes rupicolous, on the margin of riparian forests, trails or in rock crevices, in the shade and areas exposed to light. Identification. Adiantum intermedium is characterized by its falcate pinnules, which are glabrous on both surfaces or have sparse scales on the veins abaxially, and glabrous false indusium (Prado 2005c). On the specimens analyzed, the pinnules are slightly glaucous abaxially and the false indusium is oblong to linear-lunate.

Adiantum intermedium
In the study area, the species is most similar to Adiantum tetraphyllum Willd. because of its 2-pinnate lamina and pinnules with a slightly falcate apex. However, A. tetraphyllum has a moderately long-creeping rhizome, pinnules with numerous scales abaxially, and a false indusium with trichomes, while A. intermedium has a short-creeping rhizome, pinnules that are glabrous or have a few sparse scales abaxially, and a glabrous false indusium.  margins of streams, in ravines, and on clayey soils (Prado 2005c). In the study areas, this species was recorded as terrestrial and rupicolous, on rock walls and the margins of riparian forests, in partial shade. Identification. Adiantum latifolium is characterized by its long-creeping rhizome, lamina glabrous on both surfaces and glaucous abaxially, 1-3 pairs of lateral pinnae, 10-16 pairs of pinnules per pinna, pinnules with a rounded or acute apex, and rachis with scales and trichomes. Adiantum latifolium is similar to Adiantum argutum Splitg., which also occurs in Maranhão, due to its longcreeping rhizome, 2-pinnate lamina, and petiole and rachis with scales with a pectinate base (Prado and Lellinger 2002). However, A. argutum mainly differs by its pinnules with setiform scales abaxially, which are on the veins, and conspicuously biserrate, sterile pinnule margins (Kessler et al. 2017).

Distribution and ecology.
Neotropical. In Brazil, this species is widely distributed and recorded in AC, AL, AM, AP, BA, CE, DF, ES, GO, MA, MG, MS, MT, PA, PB, PE, PI, PR, RJ, RO, RR, SC, and SP. Adiantum latifolium is usually terrestrial in Terra firme forests (Miranda et al. 2015;Prado et al. 2017) and occurs on slopes, in the interior of forests, and on the margins of trails (Pietrobom and Barros 2002). In the study area, it has been recorded as terrestrial and rupicolous, on the margin and within riparian forests, and in rock crevices, in partial sun or shade.
Adiantum lucidum (Cav.) Sw., Syn. Fil.: 121. 1806. Figure 2C Material examined. Identification. Adiantum lucidum can be recognized by its pinnae that are in 10-13 pairs per frond, lanceolate, rounded on the acroscopic side and cuneate on the basiscopic side, with scattered scales abaxially and a few similar scales adaxially, veins usually free, sometimes anastomosing, two sori per pinna, one on each side of the pinna and not reaching the pinna apex, and false indusium with reddish-brown trichomes ). In the A. lucidum specimens analyzed, two forms were observed: a 1-pinnate lamina with 8-18 pinna pairs and a 1-pinnate lamina with 1-pinnate basal pinna pair. This morphological variation has been recorded by other authors, such as Kessler et al. (2017).
The most similar species to Adiantum lucidum that also occurs in Maranhão state is A. dolosum Kunze because of the 1-pinnate lamina with scales on both surfaces, petiole and rachis with scales, and false indusia in continuous lines on both sides of the pinnae. However, A. lucidum differs by having more than 8 pairs of pinnae, with an asymmetric base and main veins free, while A. dolosum has 3-5 pairs of pinnae, with a symmetric base and veins regularly anastomosed (Kessler et al. 2017).
Distribution and ecology. Neotropical. In Brazil, this species is re the states of AM, AP, BA, CE, ES, MA, MG, MT, PA, PE, and RO. It is common in secondary vegetation and disturbed forests . In the study area, A. lucidum is terrestrial and rupicolous in riparian forests, on stream banks, in shady ravines, or on the sides of trails. Identification. Adiantum pulverulentum is characterized by its short-creeping rhizome, 2-pinnate lamina, conform terminal pinna, rachis with lanceolate scales with a pectinate base and arachnoid scales, and one linear or lunate false indusium per pinnule that is glabrous or has trichomes and is on the acroscopic side of the pinnule.

Adiantum petiolatum
The main characteristic that differentiates this species from the others that have a 2-pinnate lamina in the study area is the presence of one linear or lunate false indusium along the acroscopic side of the pinnule Identification. Adiantum serratodentatum is characterized by its long-creeping rhizome, 2-pinnate lamina, with conspicuous idioblasts present on both pinnule surfaces and sparse scales on the veins abaxially, and rachis with lanceolate scales with a pectinate base and arachnoid scales.
Adiantum serratodentatum is distinct from the other species of the genus that have a 2-pinnate lamina in the study area and grow in the Cerrado by generally more ascending pinnae and more coriaceous (Kessler et al. 2017).

Distribution and ecology.
Neotropical. In Brazil, this species is recorded in the states of AM, AP, BA, GO, MA, MG, MS, MT, PA, PE, PR, RJ, RR, and SP. It is terrestrial and has been recorded in open vegetation and semideciduous forests (Tryon and Stolze 1989;Kessler et al. 2017), as well as on the margins of trails and in the interior of the Cerradão (Arantes et al. 2010;Fernandes et al. 2010). In the study area, it has been collected as terrestrial in riparian forests and on the margins of trails, in shady or partially exposed environments.

Distribution and ecology.
Exclusive to South America. In Brazil, this species is recorded in DF, GO, MA, MG, MT, PA, and TO. It generally occurs on sandy, rocky soil between rock outcrops and is also frequently near the base of shrubs, mainly in the Cerrado (Labiak and Prado 2007 Identification. This specimen is characterized by its long-creeping rhizome, 2-pinnate lamina, terminal pinna that is larger than the lateral pinnae, 1 or 2 pairs of lateral pinnae, pinnules that have lanceolate scales with a pectinate base abaxially and are glabrous adaxially, and oblong, glabrous false indusia. It is probably a hybrid involving A. latifolium, since it has a long-creeping rhizome, 2-pinnate lamina, and glabrous false indusium. However, more fieldwork and morphological studies are needed to confirm its parents. In the material examined, the sporangia are malformed (aborted). The failure to form sporangia is a very common characteristic of Adiantum hybrids.

Distribution and ecology.
In the Cerrado in Maranhão, the species has been recorded in Terra firme forest, Capoeira, and near a watercourse.

Ceratopteris Brongn.
Ceratopteris is pantropical and comprises six species (PPG I 2016; Kessler et al. 2017), of which two occur in Brazil . In the study area, only one species was recorded. Identification. Ceratopteris thalictroides can be recognized by its non-inflated petioles, 2-or 3-pinnate sterile lamina, with alternate proximal pinnae, and sporangia with a well-developed annulus.
Ceratopteris pteridoides (Hook.) Hieron., which also occurs in Maranhão state, is similar to C. thalictroides but can be differentiated by its simple sterile lamina, opposite basal pinnae, frequently inflated petiole, and poorly developed sporangia with a vestigial or no annulus (Moran 1995a).

Distribution and ecology.
Pantropical. In Brazil, this species is recorded in the states of AL, AM, AP, BA, CE, ES, GO, MA, MG, MS, MT, PA, PB, PE, RJ, RN, RO, RS, SC, SE, and SP. It is found in aquatic habitats, such as lagoons, creeks, and swampy areas, and is usually rooted in mud (Moran 1995a). In the Cerrado in Maranhão, it has been recorded in periodically flooded environments, riparian forests, near Mauritia flexuosa L.f. forests, and isolated or together with populations of Marsilea L. in an open environment.

Cheilanthes Sw.
Cheilanthes is pantropical (Ponce and Arana 2016;Ponce et al. 2022) and comprises around 70 species . There are approximately 40 species in South America (Ponce and Arana 2016), of which 13 species have been recorded in Brazil . Only one species was recorded in the study area.
The genus is recognized by its lamina covered with trichomes on both surfaces, concolor rhizome scales, and sori restricted to the margin of the lamina and covered by a recurved lamina margin that forms a false indusium without veins (Kessler et al. 2017).
Distribution and ecology. Endemic to Brazil. This species has been recorded in the states of GO, MA, MG, MT, PA, and TO. It tolerates dry environments and generally colonizes rocks (Tryon and Tryon 1982;Ponce and Scataglini 2018). In the study area, it grows on large, exposed rock walls.

Pityrogramma Link.
Pityrogramma is pantropical and comprises 20 species (Mickel and Smith 2004;PPG I 2016;Kessler et al. 2017;Prado et al. 2017). In Brazil, it is represented by four species and two varieties (Prado and Hirai 2022a). In the Cerrado in Maranhão, only one species was recorded. The genus is terrestrial and can be easily recognized by the white to yellowish wax on the abaxial laminar tissue. The wax is produced by glandular trichomes. Identification. Pityrogramma calomelanos var. calomelanos can be recognized by its 2-pinnate-pinatifid lamina, chartaceous, ascendant pinnules, and farinose abaxial surface with dense, white farina (wax). Pityrogramma calomelanos var. aureoflava, which also occurs in the Brazilian Cerrado (Prado and Hirai 2022a), is similar to P. calomelanos var. calomelanos by the characters mentioned but differs by having yellowish wax on the abaxial surface of the pinnules (Tryon 1962). It is very common in the neotropical region and mainly occurs in disturbed areas, on the margins of roads, slopes, forests, and riverbanks, and rarely in forests (Moran 1995b;Kessler et al. 2017). In the study area, it has been found as terrestrial or rupicolous in ravines, rocky areas, and near water courses, in open, sunny areas.

Vittaria Sm.
Vittaria is pantropical ) and comprises around seven species (PPG I 2016;Schuettpelz et al. 2016). In Brazil, it is represented by three species (Schuettpelz et al. 2022). Only one species was recorded in the study area.
The genus is epiphytic or sometimes rupicolous and easily recognized by the narrow, linear fronds (~2-3 mm wide) and linear sori that are parallel to the margins of the lamina. The scales on the rhizome are clathrate and reddish brown.  Figure 2F Material examined.  (Windisch and Nonato 1999;Silva Junior et al. 2020). In the study area, this species has been found as an epiphyte on live tree trunks, near the margin of a trail, and as on rocks near a waterfall, in the shade and sun.
On the other hand, when we observed species that occur in two domains in Maranhão-like the Cerrado and Amazon-this can be justified by the presence of transition areas in the state between these biomes. Such species are: Adiantum deflectens, A. latifolium, A. lucidum, A. petiolatum, A. pulverulentum, A. terminatum, Ceratopteris thalictroides, Pityrogramma calomelanos var. calomelanos, and Vittaria lineata (Silva Júnior et al. 2020;Fernandes et al. 2022).
One collection of Adiantum (Adiantum sp.) is probably a hybrid, as suggested by its unusual morphology and malformed (aborted) sporangia. However, additional study is needed to determine the probable parents of this taxon. There is a confirmed hybrid, Adiantum × moranii J. Prado (Prado 2005a) in Brazil, and other specimens that may be hybrids are known for the genus (Prado and Hirai 2020). The preferred environments of hybrids in the genus are forest fragments, disturbed vegetation formations, and stream banks that are usually affected by flooding (Moran and Watkins 2002). The specimen collected was in a secondary forest, near a watercourse.
One important occurrence for the Cerrado in Maranhão is the genus Cheilanthes, which has species that are tolerant to dry environments (Tryon and Tryon 1982;Ponce and Scataglini 2018). In the Brazilian Cerrado, five species of the genus have been recorded. In our study, and in other areas of Cerrado in Brazil, Cheilanthes pohliana has been recorded in rocky areas, generally in rock crevices (Fernandes et al. 2014;Della et al. 2019).
The diversity of epiphytic ferns in the Polypodiaceae and Nephrolepidaceae in the Cerrado in Maranhão is low (Conceição and Rodrigues 2010;Silva et al. 2017). In the study area, one epiphytic species of Pteridaceae, Vittaria lineata, was recorded growing on a live tree trunk in a riparian forest near a waterfall. The occurrence there of this species is like due to adaptations of the leaves, such as laminae covered by a thick cuticle, which allow it to survive long periods of drought (Dubuisson et al. 2009). According to Ribeiro and Walter (1998), in the Brazilian Cerrado, epiphytic species are usually more diverse than in riparian forests, where the relative humidity in the interior is high during dry periods of the year.
Of the 15 taxa recorded in this study, 14 species occur in Parque Nacional Chapada das Mesas (Fernandes et al. 2022) and three occur in Reserva Extrativista Chapada Limpa, which are both protected areas (conservation units) of Cerrado in Maranhão. Adiantum intermedium, A. terminatum, A. tetraphyllum, Adiantum sp., Cheilanthes pohliana, and Vittaria lineata are notable for having been recorded only in Parque Nacional Chapada das Mesas. The greater number of species in this park is related to more diverse environments and because more fieldwork has been conducted there (Fernandes et al. 2022). Despite that only three species were recorded in Reserva Extrativista Chapada Limpa, this number is greater than that recorded in other protected areas: Área de Preservação Ambiental do Inhamum, with two species (Fernandes et al. 2007); and Parque Estadual do Mirador, with only one species (Conceição and Rodrigues 2010).
For the Cerrado domain in Maranhão, studies that have included Pteridaceae species are floristic works that were conducted mainly in the Caxias microregion in eastern Maranhão (Fernandes et al. 2007(Fernandes et al. , 2010Conceição et al. 2015;Silva et al. 2017). For the southern Maranhão, three studies have been published on the ferns or lycophytes: Conceição and Rodrigues (2010), Almeida et al. (2020), and Fernandes et al. (2022). The first study was conducted in Parque Estadual do Mirador, which is the largest conservation unit in the state (766,781 ha) (Maranhão 2009), and only seven species (one Pteridaceae) of ferns and lycophytes were recorded there. The second study was only on the lycophytes in Parque Nacional Chapada das Mesas and recorded six species. The third study was a floristic survey of ferns and lycophytes in Parque Nacional Chapada das Mesas, and the Pteridaceae had the greatest number of species.
Although species of Pteris L. (P. denticulata Sw.) and Adiantopsis Fée [A. chlorophylla (Sw.) Fée, and A. radiata (L.) Fée] are mentioned in the Flora of Brazil for the Cerrado in Maranhão , these species were not found in the study area of this floristic survey.
Our results show that the Cerrado in Maranhão harbors a diverse flora of Pteridaceae, with representatives that occur in diverse habitats and have various life forms. Although the most representative fern family in floristic studies in Maranhão is Pteridaceae, the diversity of this group is still undersampled in the state because collection sites in the Cerrado are few. Additional fieldwork is needed to fill information gaps in the Cerrado and other phytogeographic domains in Maranhão.