Floristic similarity of lycophytes and ferns in the Amazonia/Cerrado transition zone in the central region of northern Maranhão state, Brazil

Floristic similarity studies make it possible to compare species richness between different phytophysiognomies and to assess whether species are typical of a phytophysiognomies or if they are common to two or more phytophysiognomies. The Immediate Geographic Region of São Luís (IGR), in the central region of northern Maranhão, is characterized by the presence of Amazonia, Cerrado, and coastal vegetation phytophysiognomies. The objectives of this work were to verify if the fern and lycophyte species in the IGR are similar to those in another Amazonia and Cerrado phytophysiognomies in Maranhão and Brazil. Sixty-three species of lycophytes and ferns were identified, with a predominance of individuals in the families Pteridaceae and Polypodiaceae. A similarity analysis indicated the study area has a greater affinity with the Amazonia. This is the first floristic similarity study that emphasizes ferns and lycophytes in Maranhão. However, the scarcity of floristic surveys in Maranhão and other ecotonal areas in Brazil hindered a more complex analysis of the floristic similarity of these phytophysiognomies.


INTRODUCTION
Lycophytes and ferns are seedless vascular plants, that reproduce through spores, and occur in two distinct lineages that are estimated to have 11,916 species, although this number increases each year [1]. These plants are more diverse in equatorial regions of the planet, with a decrease in species richness towards the poles [2].
The diversity of lycophytes and ferns in Brazil is estimated to be 1,412 species. Of these, 525 species are endemic [3]. The biomes with the greatest number of species are the Atlantic Forest (944 species), Amazonia (578 species) and Cerrado (319 species), and these biomes have different physiognomies and water bodies, providing ideal habitats for the diversification and proliferation of species [3].
The state of Maranhão is in the Northeast Region of Brazil, has large areas of the Amazonia and Cerrado, and also contains a small portion of the Caatinga, which has resulted in several transition areas where there is contact between species from different biomes [4]. Maranhão is estimated to have 151 species of lycophytes and ferns [3,4], but this number is low because the state still has vast areas with no data about these groups [4,5].
Floristic similarity surveys make it possible to compare species richness between different phytophysiognomies and their transition areas, as well as to assess, among other things, whether species are typical of a phytophysiognomies or if they are common in two or more phytophysiognomies. Based on similarity studies, more information can be obtained to delimit priority areas for preservation and conservation of species [6,7].
There are few studies about the floristic similarity of lycophytes and ferns in Brazil; some works have been conducted in the Northeast [8,9], Southeast [10], and South [11] regions. In Maranhão, in addition to the lack of floristic studies of lycophytes and ferns, there have been no studies focused on the floristic similarity of these groups.
Thus, this work aimed to verify if the species of lycophytes and ferns in the Immediate Geographic Region of São Luís, a transitional area between Amazonia, Cerrado, and coastal vegetations are similar to those in other areas of the Amazonia or Cerrado in Maranhão state, Brazil.

Study Area
The state of Maranhão has a tropical rainy climate (AW), according to the classification by Köppen (1948) [12], with average temperatures between 25º and 26ºC and annual precipitation between 1,400-1,800 mm [13]. The presente study was carried out in the Immediate Geographic Region of São Luís (Figure 1), which has 13 Municipalities: Alcântara, Axixá, Bacabeira, Cachoeira Grande, Icatu, Morros, Paço do Lumiar, Presidente Juscelino, Raposa, Rosário, Santa Rita, São José do Ribamar, and São Luís. This region is in the central area of the northern part of the state. It has Amazonia, Cerrado, and coastal vegetation phytophysiognomies, as well as transitional areas between them. The rainy period occurs between January and June and the dry period is between July and December, with a variation of one month, more or less [14,15].

Data collecting
Floristic data were collected during field expeditions between April 2020 and September 2022. The fern and lycophyte species were georeferenced and photographed. The specimens were located using the walking method [16] and processed according to standard techniques used for this type of material [17,18].
The specimens were mounted in the Orchid Study [19]).

Floristic similarity analysis
We used data from articles about floristic surveys of lycophytes and ferns carried out in areas of the Amazonia, Cerrado, or transition areas between them, in Maranhão and other locations in Brazil (Table 1). These papers were selected based on searching online platforms of the Portal de Periódicos CAPES and Scielo using the following terms: lycophytes and ferns Amazonia, lycophytes, and ferns Cerrado, lycophytes and ferns, Cerrado. Only works published between 2018 and 2022 were included. We chose papers about surveys of ferns and lycophytes in the Amazonia or Cerrado biomes with a minimum of 10 species. We used these works cited in Table 1 for comparison with our study because they already use the most recent concept about the recorded taxa in our sampled area, thus facilitating the analysis. Data were compared using the Jaccard similarity index and a mean association cluster analysis (UPGMA), with internal support calculated through 5000 bootstrap simulations, using the software Paleontological Statistics-PAST [29].

RESULTS AND DISCUSSION
We identified 63 taxa ( Table 2): 60 fern species in 18 families and 37 genera, and three lycophyte species in one family (Lycopodiaceae) and two genera. There was a predominance of individuals in the families Pteridaceae and Polypodiaceae, with 17 and 9 species, respectively, while the most abundant genera were Adiantum L. (5 spp.) and Lindsaea Dryand. ex sm. (4 spp.).
Only two species occurred exclusively in the Cerrado portion of the state, Actinostachys pennula (Sw.) Hook. and Schizaea elegans (Vahl) Sw., which are in the family Schizaeaceae. Hemionitis rufa (L.) Sw and Pecluma plumula (Willd.) M.G. Price were collected in the transition zone between the Amazonia and Cerrado; they do not occur in other areas of the Cerrado but do grow in the Amazonia portion. For these species, we observed the phenomenon of poikiloidry, which was also seen in Microgramma percussa (Cav.) de la Sota during the dry period. The three species of lycophytes occurred in marshy areas and veredas, which are sunny and humid places throughout the year, in addition to occasionally growing along roadsides. However, it was noted that Pseudolycopodiella meridionalis (Underw. & Loyd) Holub is less frequent than the other lycophytes. It only occurs in veredas, where the soil is partially wet, unlike Palhinhaea camporum (B. Øllg. & P.G. Windisch) Holub and Palhinhaea cernua (L.) Franco & Vasc. that were observed in dry and humid environments. Acrostichum aureum L. was the only species that tolerated the salinity of coastal vegetation areas, and generally occurs on mangrove edges, in contrast to Acrostichum danaeifolium Langsd. & Fisch. that was observed only in areas further inland and is mainly associated with swamps. Pteridaceae and Polypodiaceae commonly stand out as the most diverse families in studies carried out in the Amazonia and Cerrado biomes in other Brazilian states [23,30,32] and Maranhão [4,5]. These families have wide geographic distributions in Brazil, individuals that occupy different habitats, and are highly morphologically variable [3].
Among the life forms observed, terrestrial stands out, with 34 species, followed by epiphytic with 15 species, aquatic with four species, rupicolous with three species, and hemiepiphytic with two species. Four species were observed with two life forms (terrestrial/rupicolous and epiphytic/terrestrial) and one species had three life forms (epiphytic, terrestrial, and rupicolous) ( Table 2).
The similarity analysis (cophenetic correlation: 0.98) had two major clusters (1 and 2) and several subgroups in group 1 (Figure 2). Group 1 comprises mostly areas that are predominantly Amazonian vegetation and some areas transitioning to Cerrado vegetation, while group 2 comprises areas where Cerrado vegetation is dominant and there is little influence of Atlantic Forest vegetation. Within group 1, subgroup A stands out and is represented by Chapada das Mesas National Park and its surroundings, which have Cerrado vegetation. However, although this area is predominantly Cerrado, due to its proximity to the Amazonia biome in Maranhão it shares species in common between the two biomes. Group 1 also has subgroup B, which contains studies carried out in areas of the Amazonia, subgroup C (ARM) stands out in relation to the other subgroups in this part of the dendrogram. Although the study (ARM) was carried out in areas of the Amazonia in Maranhão, it lists a smaller number of species compared to the other works of subgroup B, except for the survey of the present study (IGR).
Subgroup E has two studies that were carried out in large areas with vegetation typical of the Amazonia. This subgroup formed because a study by Oliveira et al. (2021) [31] included a large area of the Tapajós River Basin, which contains Amazon National Park, as well as the study area of Menezes and Labiak (2020) [30]. These study areas mainly have Campinaranas, upland forests, partially flooded forests (such as floodplains and igapós), and secondary forests, which are suitable environments for ferns and lycophytes.
Subgroup F includes a study by Salino et al. (2018) [25] that was carried out in Serra dos Carajás. Of the studies used in the floristic similarity analysis, this study by Salino et al. [25] has the most species. Despite that it was carried out in a mountainous region, 70% of the recorded species were found in forested areas. This subgroup also includes data from the Immediate Geographic Region of São Luís (IGR). Although this is a transition region between the Amazonia and Cerrado biomes, its vegetation type comprises species found more frequently in the Amazonia biome. The two study areas do not have similar vegetation formations because in Serra dos Carajás (SC) there is more high-altitude vegetation and rocky places [35], and in the IGR there is Terra Firme Forest, marshes, riparian forest, and gallery forest. Despite the topographical differences, the similarity between SC and IGR species seems to be linked to greater water availability throughout the year, which favors the life cycle of ferns and lycophytes.

CONCLUSION
This is the first floristic similarity study that emphasizes ferns and lycophytes in Maranhão, state. However, the scarcity of floristic surveys in Maranhão and other ecotonal areas in Brazil made more complex analyses of floristic similarity and threats of the species difficult. Even with recent efforts that resulted in publications of floristic surveys of these plants in areas of the Amazonia and Cerrado in Maranhão, additional data are needed. Floristic similarity studies can contribute to more precisely delimiting the distributions of the most species-rich areas of biomes and determining which transition areas between biomes are the most relevant to preserve and conserving species. In this similarity study, the species found were mostly Amazonia. The prevalence of Amazonia species is probably because ferns and lycophytes need water for the gametophytic phase to complete the reproductive cycle of the alternation of generations. 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 reproduce. Even in Cerrado areas in Maranhão, most species occur in gallery forests, which have a more humid environment throughout the year.