Species diversity of the genus Riccia L. (Marchantiales, Ricciaceae) in Maranhão state, Brazil

Ricciaceae is a little-known liverwort family in northeastern Brazil. Fieldwork in 4 localities in Maranhão state yielded 4 species of Riccia , with 2 taxa, R. mauryana and R. weinionis , representing new state records. This paper describes the species diversity of the genus Riccia in Maranhão state, and provides descriptions, ecological notes, and illustrations for each species.


Introduction
Riccia L. is the most species-rich genus within the order Marchantiales.It comprises approximately 150 species globally; 53 species occur in tropical America (Bischler-Causse et al. 2005) and 36 in Brazil (Costa and Peralta 2015), corresponding to 67% of the tropical American species of Riccia and 24% of the world species diversity (Söderström et al. 2016).Most species are terrestrial and occur in both natural and disturbed habitats (such as gardens and along trails), often on soil in open areas.
Studies on the genus Riccia in Brazil have been carried out by Vianna (1985), who treated the genus Riccia in a revision of the Marchantiales for Rio Grande do Sul State and reported 11 species; Gradstein and Costa (2003), who cited 29 species for Brazil and provided a key to all the species; Bischler-Causse et al. (2005), who treated 32 species of Brazil in the Flora Neotropica Monograph for Marchantiidae; and Ayub et al. (2014), who reported 22 species for Rio Grande do Sul State (including new records for Brazil and for that state).
The northeastern region of Brazil is considered to have low bryophyte diversity, with their richness being concentrated in the Atlantic Rainforest area, in addition to a low endemicity rate (just 2 species: Riccia erythro-carpa Jovet-Ast and R. subdepilata Jovet-Ast) (Gradstein and Costa 2003).
The present paper provides an overview of the genus Riccia for Maranhão state, incorporating new records into the liverwort flora and analyzing the distributions of those taxa, and represents the first effort directed towards filling in information gaps about this genus in northeastern Brazil.

Methods
Specimens were collected in 4 different municipalities: Anapurus and Chapadinha in eastern Maranhão state, and Carolina and Estreito in southern Maranhão state (Fig. 1).These municipalities are predominantly covered by Cerrado vegetation (Silva et al. 2008, IBGE 2017).Samples were collected mainly during the rainy season, between 2016 and 2017, following the methodology proposed by Yano (1989).The specimens were preserved in dry and wet form (ex situ in a greenhouse).Preserved specimens were subsequently deposited in the CCAA herbarium of the Federal University of Maranhão, with duplicates in herbarium RB at the Rio de Janeiro Botanical Garden.

Results
Riccia L., Sp. pl., ed. 1, 1138Sp. pl., ed. 1, . 1753. .Thalli forked, in rosettes or gregarious patches, prostrate and dorsiventral, terrestrial or aquatic (floating), usually with a deep median groove, green, grayish-green, yellow-green or glaucous, ventral surface usually with scales and rhizoids.Ventral scales usually in 1-2 rows or absent, imbricate, lunulate, purple or hyaline, sometimes extending beyond the margins of the thalli.Epidermal region with air chambers in 1-3 layers.Monoecious or dioecious.Antheridia and archegonia scattered and embedded in the thallus, chambers open through ostioles.Capsule embedded in the thallus, disintegrating at maturity.Spores sometimes in tetrads, large, brown to black, distal and proximal faces with areoles, ridges, spines or smooth.
The species are delimited morphologically by characteristics of thalli (cross section), scales (color and arrangement), and spores (shape, ornamentation, size).Description.Thalli in gregarious patches, dorsal surface light to grayish-green and ventral surface pale-green to brownish, forked 2-3 times, lobes 5-15 mm long, 2-3 mm wide, rounded apically, margins narrow and hyaline, 2-3 cells wide, with a deep median groove.Epidermal cells green and ovate-rounded when intact, and lunulate when not intact; without pores.Ventral scales hyaline to rose, imbricate, lunulate.Lobes in cross section 2-6 times as wide as high, 0.6-0.8mm high, dorsal margin acute, ascending or concave, recurved and acute; ventral margin convex; dorsal tissues with large cells in 5-7 cell layers, with thickened walls or with thick and it is usually found forming mats on limestone substrates (such as pavements), but forms rosettes on partially flooded sites.We observed scales varying in color depending on the degree of thallus decomposition and habitat humidity.In dry habitats, it is possible to observe scales more pinkish than hyaline, while in humid habitats the scales are always hyaline.Quite common and widespread in Brazil (in the states of Bahia, Ceará, Espírito Santo, Goiás, Maranhão, Mato Grosso, Mato Grosso do Sul, Paraíba, Paraná, Pernambuco, Rio Grande do Sul, Rio de Janeiro, Santa Catarina, and São Paulo).This species grows in abundant populations along the margin of ravines near water in Maranhão state, often being encountered partially submerged along stream margins.The species sampled and described in this paper are all from the Cerrado Biome, and likely represent only a small portion of the bryophyte diversity of Maranhão, a state which occurs in the transitional zones between 3 different Brazilian biomes (Amazonian, Caatinga, and Cerrado).Riccia has its highest diversity often observed in areas with dry seasons (Bischler-Causse et al. 2005), such as the Cerrado.Beside this, according to Jovet-Ast (1991, 1993), species distributions are still incomplete because of the strong seasonality (disappearing dur-ing the dry season) of the species.Most of the studies and collection efforts in the state focused in the Cerrado biome (see Conceição et al. 2010, Santos and Conceição 2010, Peralta et al. 2011, Varão et al. 2011, speciesLink Network 2018).Therefore, information from other biomes in the state are scarce, and the genus is probably sub-sampled.Thus, additional floristic and taxonomic studies related to the genus will still be necessary in different under-collected regions of the state, including in the Amazonian and Caatinga biomes from where few collections are currently held in the Brazilian herbaria (speciesLink Network 2018).

Riccia vitalii
Collecting in these 2 biomes will almost certainly add new records to the liverwort bryoflora of Maranhão state.The Caatinga biome is unique to Brazil and very distinct from the Amazonian and Atlantic Forest biomes.We expect to find Riccia species in the Caatinga biome because of its semiarid climatic conditions including high temperatures and high luminosity, as observed by Reis (2015) for Pernambuco.Our results suggest the need for additional fieldwork to better understand the distribution and ecology of the genus Riccia in northeastern Brazil, since the species richness distribution is necessary to understand spatial patterns of biodiversity, to establish conservation strategies, or to predict future patterns of biodiversity under global change (Ricklefs 2004, Algar et al. 2009).
rounded apically, margins narrow and hyaline, 1-2 cells wide, median groove absent.Epidermal cells light green and rounded, with pores bounded by 4 cells.Ventral scales hyaline, conspicuous, semi-lunulate.Lobe in cross section 2-3 times as wide as high, 0.3 mm high, dorsal margin rounded Material examined.Brazil: Maranhão: Carolina, Parque Nacional Chapada das mesas, near to Farinha river, right margin, rupicolous, exposed to the sun, 06°59ʹ37ʺ S, 047°09ʹ57ʺ W, 194 m a.s.l., J.A.S.Silva, 12 March 2017,  73, 75, 79 (CCAA); Estreito, Parque Nacional Chapada das Mesas, left bank of the river, on rocks in front of the waterfall, exposed to the sun, 06°59ʹ39ʺ S, 047°09ʹ56ʺ W, 192 m a.s.l., J.A.S.Silva, 12 March 2017, 85 (CCAA).Rio Grande do Norte, Rio Grande do Sul).It is quite common in Brazil and found on humid soils or rocky surfaces, forming large mats.When dry, the scales fold over the dorsal surface of the thallus -which is easily observed in the field and useful for distinguishing R. vitalii from other species of Riccia.