Bryophyte flora of the Apodi Plateau , Ceará , Brazil

In the state of Ceará, bryophytes have been mainly sampled in humid and sub-humid enclaves, remnants of Atlantic rain forest, while studies in the Caatinga Domain are practically non-existent. The present work aimed to survey the floristic composition of bryophytes of the Apodi Plateau, a region predominantly covered by Caatinga. Collections were conducted as part of the field activities of the Program for Research in the Biodiversity of the Semiarid region of Brazil (PPBio). The briological material was collected in 2014, in the Apodi Plateau located within the territory of Ceará state. Fifty-nine bryophyte species were found: 27 liverworts Marchantiophyta distributed in seven families and 11 genera, and 32 mosses Bryophyta distributed in 14 families and 26 genera. Among the species found, 25 were new records for the state of Ceará and Riccia subplana is reported for the first time for the Northeast region of Brazil. Twenty-three are new records for the Caatinga Domain. Taxonomic comments are provided for the new records for the state of Ceará and for Caatinga, as well as an illustration of the species Weisiopsis bahiensis.


Introduction
The northeastern region of Brazil occupies an area of 1,540,827 km 2 (Nimer 1989), and has a semiarid climate in approximately 800,000 km 2 , corresponding to 10% of the Brazilian territory (Ab'Sáber 1974). The relief has altitudes mostly below 500 m, among surfaces that reach 1,000 m in the Borborema, Araripe and Ibiapaba plateaus, up to 1,200 m in the Diamantina plateau. This altitudinal variation associated with the position in the relief, where the increasing altitude causes forced convective rains and lower temperatures, leads to the occurrence of different types of vegetation. The xerophilous Caatinga vegetation is dominant in the semiarid area, presenting physiognomic and floristic variations (Romariz Rodriguésia 70: e00692018. 2019Ferri 1980;Andrade-Lima 1981;Sampaio 1995;Rizzini 1997).
The different physiognomies of the Caatinga hold a diversified biological heritage, with rare and endemic taxa (Giulietti et al. 2004) and an invaluable richness of plant and animal species (MMA 2004). In contrast to other semiarid regions of the world, the biological diversity of the Caatinga is extremely significant (Luetzelburg 1974;Andrade-Lima 1981;Araújo Filho & Carvalho 1997) and adds biological and economic value to Brazil. Despite such remarkable characteristics, the Caatinga is one of the least known domains in the country. This situation is a consequence of the belief that the Domain has a very low diversity, no endemic species, and vegetation that is strongly modified by anthropic actions (Giulietti et al. 2004). It is noteworthy that this vegetation is one of the most affected by human interference in Brazil; in 2008, approximately 45% of its original coverage had already been deforested (MMA 2010). According to Castelletti et al. (2004), the last intact native vegetation remnants are extremely fragmented.
The Northeast region of Brazil ranks third in number of bryophyte species, behind the South and Southeast regions (Costa & Peralta 2015). As for the bryophyte flora of the state of Ceará, this is still partially known. Most studies on the flora of Ceará have focused on flowering plants, for they represent the predominant vegetation. There are still few reports of bryophytes in Ceará, especially due to the lack of collections in native vegetation, although bryophytes can be found even in the most inhospitable places (Brito & Pôrto 2000). The best explored areas to date are quite small and, considering the extension of the state, it is unlikely that the results obtained portray the real situation of the bryophyte flora of Ceará. The main areas sampled until present are humid and sub-humid enclaves, remnants of Atlantic rain forest (Oliveira & Alves 2007;Oliveira & Bastos 2009, 2010aSiqueira et al. 2011).
There are no works specifically addressing the bryophytes growing in the Caatinga in Ceará. The few studies carried out so far were floristic surveys in humid environments, in high altitudes such as the Ibiapaba Plateau (Oliveira & Bastos 2009, 2010a and the Guaramiranga mountain (Yano & Pôrto 2006). In this context, the Apodi Plateau, located in the eastern side of Ceará, represents a relevant area to the study of bryophytes growing in the Caatinga, taking into account the lack of works in the region. The knowledge of the bryophyte flora of the Apodi Plateau is fundamental to understand the diversity of the ecosystem as a whole, aiming at environmental valuation and support to appropriate management measures.
The present study aimed to carry out a floristic survey of the bryophytes of the Apodi Plateau, within the limits of the territory of the state of Ceará.

Study area
The Apodi Plateau is located in the eastern side of the state of Ceará, also extending into the territory of Rio Grande do Norte (Fig. 1). In general, the natural vegetation is represented by hyperoxerophilic Caatinga, which is part of the dominant landscape of the ecosystem of the Apodi Plateau, associated to secondary forests with varied herbaceous strata. According to Filho et al. (2001), different types of vegetation coverage can be observed in the region: Savanna (Cerrado); Forested savanna (Cerradão), currently named as xeromorphic tropical subcaducifolia forest; Carrasco; and a seasonal dense Ombrophilous Forest remnant, probably resulting from great environmental heterogeneity throughout many geological periods (Giulietti et al. 2004). Fernandes (1990) believes that the presence of a forest such as Cerradão in the state of Ceará was driven by climate change through geological time, which also caused progressions and regressions of this forest into the central region of Brazil. The predominant climate of the region is Hot Sub-humid Tropical, the soil is Yellow Dystrophic Latosol, and the mean annual precipitation and temperature is 1,061 mm and 25 o C, respectively.

Collections of botanical material
Collections were part of the field activities of the Program for Research in the Biodiversity of the Semiarid region of Brazil (PPBio). Briological material was collected in 2014, in the Apodi Plateau located within the territory of Ceará, according to specialized techniques described in Frahm (2003). The material was collected manually or with the aid of a knife and stored in Kraft paper bags. In the field, altitudes and geographical coordinates were recorded at all points of collection with the aid of a GPS. The following data were also recorded: date and site of collection, type of ecosystem, habit, growth form, colonized substrate (bryocenological group), and other relevant ecological and/or taxonomic observations. Samples were identified in the Plant Taxonomy Laboratory of the Universidade Estadual de Feira de Santana. For the macro and microscopic analysis, morpho-anatomical characteristics of gametophytes and sporophytes were observed with the aid of a stereomicroscope and an optical microscope. The classification system used was the one of Crandall-Stotler et al. (2009) for liverworts, and Goffinet et al. (2009) for mosses. The geographical distribution of the species in Brazil was based on the BFG (2018). In order to identify species, the following works were used: Buck (1998), Bordin & Yano (2013), Costa (2016), Frahm (1991), Gradstein & Costa (2003), Lemos-Michel (2001), Sharp et al. (1994), Yano & Peralta (2007) and Zander (1993).
Vouchers of the identified material were deposited in the collection of the Herbarium of the Universidade Estadual de Feira de Santana (HUEFS).

Results
Fifty-nine bryophyte species were recorded, consisting of 27 liverworts -Marchantiophytadistributed in seven families and 11 genera, and 32 mosses -Bryophyta -distributed in 14 families and 26 genera (Tab. 1). Among the species found, 25 are new records for Ceará, and Riccia subplana Steph. is reported for the first time to the Northeast region of Brazil. Twenty-one are new occurrences for the Caatinga Domain.
A list of all the new records for the state of Ceará, for the Caatinga, and for the Northeast region, with taxonomic comments for each species, is provided in the list below, in alphabetical order of families. An illustration of Weisiopsis bahiensis (Müll. Hal.) Broth. is provided because this is a species with restricted distribution in Brazil, cited only for the states of Bahia (site where the type was collected) and Piauí, and because there are few illustrations of the species available in the literature.
It is characterized by creeping habit, green to brown coloration, entire and imbricate underleaves, oblong-orbicular leaves with rectangular lobules, which have an apical tooth consisting of 1-2 cells. It was collected on rotting log. It is one of the most common epiphytic liverworts in the Amazon forest and is reported here for the first time for the Caatinga Domain and for the state of Ceará. Brazilian geographical distribution: North (AC, AM, PA, RR), Northeast (AL, BA, PE), Southeast (ES, MG, RJ).
It is distinguished by inflated, spherical lobules present in some parts or in the whole plant, and perianths with four horns. It was found on live bark. This is the first record for the Caatinga Domain. Brazilian geographical distribution:   Dauphin (2003). It is characterized by the presence of caducous leaves and frequent reduced lobules. It was found on live bark. This is the first record for the Caatinga Domain and for the state of Ceará.  Gradstein & Costa (2003).
The striking features of this species are the leaf lobes with strongly involute margins. It was found growing on rotting log. This is the first occurrence for the Caatinga. Brazilian geographical distribution: Northeast (BA, CE), Southeast (ES, MG, SP). Spruce, J. Bot. 19: 36. 1881. The illustrations of this species is in Bastos & Yano (2004), as L. filipes Spruce.

Lejeunea aphanes
The diagnostic feature of the species is the underleaf that grows attached to the stem and which is difficult to visualize due to its very thin cell walls which are usually collapsed. It was collected on live bark. This is the first record for the Caatinga Domain and for the state of Ceará. Brazilian geographical distribution: Northeast (BA).  Heinrichs (2002).

Lejeunea oligoclada
It is distinguished by leaves that are longer than wider, with 15 to 50 teeth, two long teeth at the apex, and dentate ventral margin. This is the first occurrence for the Caatinga Domain and for the state of Ceará. Brazilian geographical distribution: North (AM, PA), Northeast (BA, RN), Southeast (ES, MG, RJ, SP).
The dichotomous branching pattern, weakly dentate leaves with a high shoulder and with longdecurrent and entire ventral base are diagnostic characteristics of the species. Heinrichs et al. (1998)  It is characterized by the numerous white spots, which are idioblastic cells visible through the epidermis, densely areolated distal spore surface and with tuberculated angles. It was collected on soil. This is the first citation for the state of Ceará. Brazilian geographical distribution: Northeast (BA), Midwest (MS, MT), Southeast (SP), South (PR, RS, SC).
It is characterized by stems 6-7 mm long, round apex, entire margin, absence of papillae or cilia, and presence of pink scales. It was collected on soil. The species has a disjunct distribution and had been recorded only for the Amazon forest and Rio Grande do Sul in Brazil (Ayub et al. 2014). It was found on soil. This is the first citation for the  Sharp et al. (1994).
It is distinguished by the ligulate-lanceolate leaves, equally arranged in the stem, with acute to acuminate apex, rhomboid-hexagonal cells, entire and bordered margins, and long-excurrent costa ending in a wing tip. It was found on soil. It is endemic to Brazil and this is the first record for the state of Ceará. Brazilian geographical distribution: Northeast (BA, PE), Midwest (GO, MS), Southeast (RJ, SP).
It is characterized by the robust size of the gametophytes, up to 10 cm long, narrow leaves, 6.5 mm long, with serrate margins. It was found on soil. This is the first record for the Caatinga Domain and for the state of Ceará. Brazilian geographical distribution: Northeast (BA, PE), Midwest (DF), Southeast (ES, MG, RJ, SP), South (PR, RS, SC).
It is characterized by dimorphic leaves with unipapillose cells, filamentous propagules in the median region of the leaf, and cancellinae ending in acute angles. It was collected on live bark. This is the first record for the Caatinga Domain and for the state of Ceará. Brazilian The illustrations of this species is in Buck (1998).
It is distinguished by gametophytes with cylindrical branches and blackish apex, weakly concave and triangular-ovate leaves, with gradually acuminate and never piliferous apex, cordate base, crenulated margin, costa extending up to 1/2 of the leaf, and sub-quadratic and smooth alar cells. It was found on live bark. This is the first record for the Caatinga Domain and for the state of Ceará.  Sharp et al. (1994).
It is characterized by leaves with fragile and brittle apex, and marginal elongated basal cells contrasting with the rounded hexagonal cells of the lamina. It was found on live bark. This is the first record for the Caatinga Domain and for the state of Ceará. Brazilian geographical distribution: North (AM, PA, RO), Northeast (BA, PE, SE), Midwest (MT), Southeast (RJ, SP).
It is distinguished by the glossy, green to brown coloration, densely tomentose gametophytes, oblong and smooth leaves with abruptly acuminate apex. It was found on rock. This is a new record for the Caatinga Domain and for the state of Ceará.  Sharp et al. (1994) It is characterized by elliptic ovate leaves with flat or weakly curved margins in the medial portion, presence of masses of green, ovoid propagules, with three or more cells, produced in the axils of the leaves. It was found on rock. This is the first record for the state of Ceará. Brazilian  Buck (1998).
Gametophytes with erect-patent, ecostate, flat stem leaves, with gradually acuminate apex, weakly inflated and yellow-orange alar cells, quadrate supra alar cells, few in number (2-3), measuring 1/2 of the length of the alar cells. It was collected on live logs. This is the first occurrence for the state of Ceará. Brazilian geographical distribution: North (AM, PA, TO), Northeast (BA, MA, RN), Midwest (DF, GO, MS, MT), Southeast (ES, MG, RJ, SP).

Discussion
The 59 bryophyte species found in the Apodi Plateau correspond to 30% of the total number species registered in the state of Ceará. This number can be considered high when compared to other surveys carried out in Caatinga areas, such as those where were conducted the studies by Porto et al. (1994) in Caruaru county, where 17 species were registered, and Porto & Bezerra (1996), who reported 13 bryophyte species for the municipality of Agrestina, also in Pernambuco.
Among the liverworts, the most representative families were Lejeuneaceae (12 spp.) and Plagiochilaceae (4 spp.). As for mosses, the families with the highest number of species were Bryaceae and Pottiaceae (4 spp.). In the present study, it was observed that the majority of the most frequent species have adaptations to thrive in restrictive environmental conditions, such as xeric environments, being considered generalists or typically adapted to solar incidence, such as Frullania caulisequa (Nees) Nees, Riccia vitallii Jovet-Ast, Bryum argenteum Broth., Octoblepharum albidum Hedw., Campylopus savannarum (Müll. Hal.) Mitt. and Hyophilla involuta (Hook.) A. Jaeger (Ochi 1980;Frahm 1991;Gradstein et al. 2001). As regards the family Lejeuneaceae, this is one of the largest families of liverworts and, although better represented in humid forests, they occur also quite frequently in open and xeric environments (Gradstein 1994;Gradstein et al. 2001). The Lejeuneaceae species recorded in this study present a considerable wide tolerance or are pioneers. In Brazil, they have also been found in disturbed forests, savannas, sandbanks, Caatinga and even plantations and pastures (Gradstein & Costa 2003;Forzza et al. 2010).
The results of this study reinforce the importance of the Apodi Plateau for the preservation of bryophyte species in Caatinga areas and for the recognition of hot spots in order to guide conservation efforts to areas with high diversity of species and endemism (Kier et al. 2009). According to Costa & Peralta (2015), Brazil has 242 endemic bryophyte species, of which only one is cited for the state of Ceará. The present study report three new records of endemic Brazilian species for the state   Weisiopsis bahiensis seems to have some inconsistencies in the information available in literature. According to the original work (Müller 1855, as Pottia bahiensis Müll. Hal.) The species type is from the state of Bahia, however, at the BFG (2018) platform, it is cited only for the state of Piauí, which is probably wrong.  cited W. bahiensis from Oeiras, Goiás state, although Oeiras is actually located in Piauí state. Crosby et al. (1999) ranked it as a species for which no new information could be found in the post-1962 literature, however, Gradstein et al. (2001) considered this species as valid. Costa (2016) is the most recent citation of this species in Brazil, however, as well as Yano et al. (2009), with herbarium samples collected in 1978. Therefore, this work represents a rediscovery of W. bahiensis in nature and the third record in Brazil and in the world.
The high number of new species reported for the state of Ceará and for the Caatinga Domain underscores the importance of continuous floristic surveys, especially in areas to which there is a gap of knowledge such as the Apodi Plateau, part of the Caatinga Domain in the Semiarid region of Brazil.