Acrocarpic mosses ( Bryophyta ) of Chapada das Mesas National Park , Maranhão , Brazil

Chapada das Mesas National Park is located in southwestern Maranhão state, Brazil and comprises several forest types characteristic of the Brazilian Cerrado. We contribute to the knowledge of the distribution of Brazilian bryoflora and provide a list of moss species of Chapada das Mesas National Park. A total of 38 species of acrocarpic mosses were found, with Fissidentaceae being the richest family with 11 species. Of the species recorded, 22 are new occurrences for the state of Maranhão, and 4 of these are new records for the Northeast Region of Brazil. Most of the species recorded are broadly distributed in Brazil (66%), while restricted species represented just 10%. The most common acrocarpic moss species were Hyophila involuta (Hook.) A. Jaeger and Octoblepharum albidum Hedw.


Introduction
Chapada das Mesas National Park (CMNP) is located in the southwest region of the state of Maranhão, Brazil.It was created by presidential decree on December 2005, as a result of a historical process of community organization in the region, for the establishment of a Conservation Unit to protect the region of the Chapadas das Mesas against the advance of the agricultural frontier and other projects that could endanger its ecological value and compromise its ecotourism potential (Moraes and Lima 2007).The various vegetation types present in CMNP are Cerrado (sensu strict) and campo sujo (savanna), along with forest formations of cerradão (seasonal forest), mata seca (dry forest) and the so-called marginal forests comprising matas de galeria (gallery forests) and buritizais (palm swamps) (Moraes and Lima 2007).There are also numerous water sources in the form of 3 important river basins: Parnaíba, Araguaia/Tocantins, and São Francisco.
According to Galinkin et al. (2004), the southwestern region of Maranhão is important for the maintenance of Brazilian biodiversity because it encompasses an ecotone between 3 biomes, the Cerrado, Amazon, and Caatinga.Thus, it represents an area with high potential for sheltering high levels of richness and abundance of flora and fauna and serves as significant component of the Araguaia-Bananal ecological corridor.Although the Cerrado is recognized as one of the main centers of diversity and endemism of plant species in Brazil (Medeiros 2011), there is little information about the bryoflora of the Cerrado of Maranhão and in particular of CMNP.The destruction of the Cerrado has accelerated as this biome is being replaced by monocultures.In view this, the need to carry out inventories of the bryoflora has become extremely relevant.
Sixty species of mosses are known from the state of Maranhão (Costa and Peralta 2015).However, inventories of bryophytes around waterfalls have yet to be undertaken in the state even though a survey in Serra da Canastra National Park revealed rich moss flora in similar habitats (Carmo and Peralta 2016).
The acrocarpic growth form is evidenced in mosses that present a perichaetium produced at the apex of a main branch (La Farge-England1996).The high diversity of acrocarpic mosses in the state of Maranhão is remarkable, as shown in publications on the bryoflora of the state (Peralta et al. 2011, Vieira et al. 2017).
The great importance of CMNP for the preservation of endemic species and its maintenance as a Conservation Unit make it an interesting area for study.Therefore, we made a floristic inventory of the acrocarpic mosses of CMNP with our goal to increase knowledge about the geographic distribution of bryophytes in Brazil.

Methods
Study area.CMNP has an area of 161,000 ha divided between 2 administrative areas.The larger area (140,000 ha) covers parts of the municipalities of Carolina and Estreito, while the smaller (19,000 ha) covers the part of municipality of Riachão.The relief is characterized by the presence of sandstone hills with elevations between 250 m and 524 m (Fig. 1).
According to the Köppen climate classification, the climate of the region is Tropical Humid, with high temperatures throughout the year.There are 2 well-defined seasons: a dry summer from May to October and a rainy winter from November to April.The average annual mean temperature is 26.1 °C, with a minimum temperature of 25.2 °C in January to September and a maximum of 36 °C in July and August.Annual rainfall ranges from 1,250 to 1,500 mm per year (Lima et al. 2007).
The CMNP is almost entirely on yellow latosol soil with a characteristic deep profile, along with the constant presence of sedimentary sands, which are characteristic of these tabular reliefs.The main types of soils found in the region of CMNP are quartz sands, cambisols, and redyellow latosols (Martins et al. 2017).
There are numerous springs within CMNP which supply 3 important watersheds: Parnaíba, Araguaia/Tocantins, and São Francisco.The Farinha River, one of the larger rivers of CMNP, is a tributary of the south bank of the Tocantins River, which is a very important water source for the entire central region of the country (Marques and Amorim 2014).
Sampling, herborization and identification.Authorization for the collection and transport of specimens was approved by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio number 50981).
Our collection expeditions were carried out during both the dry and rainy seasons and were focussed on areas near waterfalls, but also covered other areas and substrates.We gave special attention to the habitats most favorable for the colonization by bryophytes, such as waterfalls and the vegetation along stream banks.We collected and herborized the samples according to Frahm (2003), with the specimens being collected manually or with a knife and/or spatula and placed in brown paper bags.Data on substrate colonization follow the bryocenological groups of Robbins (1952), and included corticicolous (Co), epixilous (Epx), epiphyllous (Epf), rupicolous (Ru), and terricolous (Te).
The classification system adopted is that of Goffinet et al. (2009).Brazilian geographical distributions were categorized according to Valente and Pôrto (2006), who considered bryophytes that occur in 1 to 4 Brazilian states as "restricted"; those occurring in 5 to 9 states as "moderately distributed"; and those occurring in 10 or more Brazilian states as "broadly distributed".The geographical distributions follow Forzza et al. (2010), Costa et al. (2011), Costa and Peralta (2015) and Carmo and Peralta (2016).
Diagnostic characterization of new records and remarkable species are provided here in alphabetical order.Barbula indica (Hook.)Spreng.(Fig. 5) Recognized by oval to elliptical leaves; margins plane or weakly recurved at mid-leaf; apex acute to rounded, costae percurrent or subpercurrent, laminal cells quadrate and strongly pluripapillose.Habitat: soil and rocks.Brazilian range: AC, AM, PA, BA, PE, RN, SE, DF, GO, MS, MT, ES, MG, RJ, SP, PR, RS.

Calymperes afzelli
Sw. (Fig. 7) Recognized by cancellinae ending in acute angles, costae percurrent to long-excurrent, spiny-papillose costa on adaxial surface, many propagules at the tip of costa.Grout (Fig. 8) Recognized by hyaline hair point, basal portion of leaves hyaline and strong transition of ribbed costae with lamina in cross section.Habitat: soil and rocks.Brazilian range: RO, RR, BA, DF, MT, MS, MG, SP, PR.

Fissidens ornatus
Leucobryum laevifolium Broth.(Fig. 14) Plants whitish to pale green in color, leaves grouped, costa reaching almost the leaf width, percurrent, smooth; outer walls of cells convex in crosssection of the apex region.Straight leaves differentiate this species from L. martianum, which has falcate leaves.Habitat: roots and tree trunks.Brazilian range: AM, MG, MT, RJ, RS, SC, SP.
Ochrobryum subulatum Hampe (Fig. 16) Plants small, forming lax to dense tufts, yellowish green in color.Differs from O. gardneri, the most common species of the genus, because of its linear lanceolate leaves with long acuminate apexes.Habit: rocks and tree trunks.Brazilian range: AC, AM, PA, RO, RR, TO, AL, PE, DF, GO, MT, SP.
Philonotis sphaerocarpa (Hedw.)Brid.(Fig. 18) Recognized by salient costae on adaxial surface, acuminate apex and small cells at base of lamina.Growing in tufts on rocky cliffs and banks of waterfalls.This is the first citation for the state of Maranhão.Habitat: rocks.Brazilian range: AM, BA, CE, MT, RJ, SC, SP.
Syrrhopodon prolifer Schwägr.(Fig. 21) Plants dark-green in color, straight contorted when dry, linear-lingulate blades, margins entire at base, costa often spinose near leaf apex.Habitat: soil and rocks.Brazilian range: AC, AM, AP, PA, RO, TO, AL, BA, CE, PE, PI, SE, DF, GO, MT, ES, MG, RJ, SP, PR, RS, SC.Hampe (Fig. 22) Similar to S. prolifer and often misidentified as such.Distinguishable by red to dark green color, wide lamina and cancelinae cells forming a concave region that always produces a wide-spreading habit to the leaves.Habitat: decomposing tree trunks and rocks.Brazilian range: MG, RJ, SP, RS, SC.

Trichostomum brachydontium Bruch.
Highly variable with leaves sometimes being slender with a tapering tip.Leaves held at an angle of up to 45° or are recurved away from stem when moist, but crisp and incurved when dry, margins normally plane, but may be narrowly recurved.Habitat: decomposing tree trunks and rocks.Brazilian range: PA, RO, BA, PE, ES, PR.
Trichostomum tenuirostre (Hook.& Taylor) Lindb.(Fig. 23) Shoot tips usually dull green in color, and brown or almost black below.Leaves spread and wavy, crisp when dry, tips usually acute and margins plane.The species is very similar in appearance to T. brachydontium, but T. brachydontium is typically yellow-green in color and often grows in drier places.Habitat: rocks and tree trunks.Brazilian range: AM, PA, RO, RR, BA, CE, PI, SE, DF, GO, MT, MG, SP, RS.

Discussion
The species richness of acrocarpic mosses found in the CMNP is highly consistent with published information on the bryophyte flora of the Cerrado.There is a high diversity of species in this phytogeographical domain, as found by Câmara (2008) who recorded 26 species of acrocarpic mosses in a survey in the IBGE Ecological Reserve in Brasília, Distrito Federal.Carmo and Peralta (2016) found 28 species of mosses, including 16 acrocarpic species, in a study in Serra da Canastra National Park.In another study, Rios et al. (2016) found 16 species in an area between several Cerrado physiognomies in the state of Goiás.In the Cerrado of Maranhão state, Oliveira et al. (2018) found 20 species of acrocarpic mosses.Our results, as well as those of previous studies, demonstrate the high species richness of acrocarpic mosses in the Cerrado and the high floristic potential of bryophyte species in CMNP.The importance of floristic surveys in conservation is reinforced.Floristic analysis allows comparisons within and between forest formations in space and time, generate data on the richness and diversity of an area, as well as enable the formulation of theories, test hypotheses, and produce results that will serve as the basis for other studies (Myers et al. 2000).In this way, with our results, we hope to collaborate with the management of the CMNP.
Calymperaceae was one of the most representative families, which can be explained by the broad distribution of this family in the tropics (Gradstein et al. 2001).The high representativeness of this family is demonstrated in floristic surveys at tropical region (Cerqueira et al. 2015, Oliveira et al. 2018).The composition being dominated by Acrocarpic mosses dominate the bryophyte flora on rocky outcrops (Silva and Germano 2013, Silva et al. 2014a, 2014b), where roughly 74% of the species are acrocarpic.The most species-rich families in the studies by Silva and Germano (2013) and Silva et al. (2014aSilva et al. ( , 2014b) ) were Leucobryaceae, Bryaceae, and Pottiaceae; in our study, these families were also highly species rich, which reflects the great availability in the study area of exposed habitats, where these families are typically found.These families are adapted for sunny substrates (Richards 1984).
The large number of species in our study belonging to the rupicolous bryocenological group is correlated to the availability of rocky substrata near waterfalls, where there are numerous rocky cliffs.Our results corroborate the findings of Carmo and Peralta (2016).The predominance of rupicolous community contrasts with tropical forests where corticicolous bryophytes predominate (Richards 1984, 1988, Gradstein and Pócs 1989).
In CMNP, 57% of the bryophyte species are acrocarpic species.Most of the acrocarpic moss species found, 25 species or, are broadly distributed (Table 1).These species (e.g., Hyophila involuta, Octoblepharum albidum, and Calymperes palisotii) are generalists and can easily occupy several types of substrates.
Nine species are moderately distributed (24%) and 4 species are restricted (10%).The occurrence of these 4 species reinforces the importance of CMNP as a conservation unit with diverse vegetation types in Cerrado and areas transitioning to Amazon Forest and Caatinga.The rich mosses flora is favored by conditions, such as humidity and a variety of substrates.

Figure 1 .
Figure 1.Geographic location of CMNP in Brazil and the state of Maranhão.

Figure 3 .
Figure 3. Distribution pattern of species in Brazilian states.