Diversity and conservation of Pottiaceae (Pottiales) in the Atlantic Rainforest

The taxonomy, diversity and conservation status of all species of the family Pottiaceae in the Atlantic Rainforest of Rio de Janeiro State in southeastern Brazil are presented. The Atlantic Rainforest is a globally recognized biodiversity hotspot. The treatments are based on field expeditions and studies of herbarium collections. Twenty eight species from 18 genera are discussed. A key to the genera and species is provided, with comments on their distributions and altitudinal ranges, with illustrations and evaluation of the conservation status.


Introduction
The family Pottiaceae (belonging to the order Pottiales) was created by Schimper (1855) and, comprises 77 genera and 1457 species (Zander 1993; extrapolated from Crosby et al. 1999).The family is diverse in tropical America, especially in humid regions, and includes 55 genera and 361 species (about 250 valid species, extrapolated from Gradstein et al. 2001).Thirty-three genera and 64 species are recognized in Brazil (Costa et al. 2011;Costa 2014a).Zander (1993) considered South America to be one of the centers of morphological diversity to Pottiaceae.
According to Zander (1996), Pottiaceae is the largest moss family in terms of the number of genera (77); 22 are considered critical, as they are rare and contain only one to three species.Three of these genera occur in Brazil (Erythrophyllopsis, Ganguleea, and Hymenostyliella), with only one species each, being found in sub-mountainous areas, on riverbank rocks, and on the vertical faces of granitic rocks along riversides.
Pottiaceae is among the 12 largest moss families in Brazil according to Costa et al. (2011) and Costa (2014a), with 33 genera and 64 species, although several genera (e.g., Barbula, Didymodon, Syntrichia, Trichostomum, Tortula, and Weissia), will require thorough regional revisions that should result in reductions in the number of recognized species.These taxa are found in open and often rather dry habitats, with their greatest diversity occurring in the montane regions.

Historical Background
Publications focusing on Brazilian mosses are very extensive, comprising almost 400 titles.The earliest paper, by Christian Friedrich Hornschuch, can be found in the Flora Brasiliensis (Vol. 1, part 2, 1840) describing 194 species collected in the states of Rio de Janeiro and Minas Gerais.Numerous new species for Brazil were described at the end of the 19th century/beginning of the 20th century by Müller (1898;1900;1901) based on the collections of Glaziou (Rio de Janeiro), Puiggari (São Paulo: Apiahy), Lindman (Rio Grande do Sul), Dusén (Serra do Itatiaia), Ule (southern Brazil and Amazonia).More recent contributions are cited in the Brazilian checklist published by Costa et al. (2011).
Although there have been many studies mentioning species of Pottiaceae in Brazil, the overwhelming majority are floristic inventories or new records for different states, and there has been only a single taxonomic treatment for the genus Streptopogon (Costa 2012) and new synonyms (Costa 2014b).Various authors list a total of ca. 15 genera and ca.45 species of Pottiaceae in Rio de Janeiro State, although Costa et al. (2011) and Costa (2014a) recently reduced the total number of taxa previously recognized there by approximately 60%.Rio de Janeiro State now includes 28 recognized species; three taxa have been excluded as they are considered poorly known (with no material available to study or supporting records).There is no general key available for the genera and species of Pottiaceae known to Rio de Janeiro State or Brazil.
The bryoflora of Rio de Janeiro State is reasonably wellknown in comparison with other Brazilian states (Costa et al. 2005a;2011).Eighteen genera and 28 species of Pottiaceae are recognized in the Atlantic Rainforest of Rio de Janeiro State in this study, representing 5% of the total number of moss taxa recorded for that state, 44% of the Pottiaceae taxa recorded for Brazil, and 8% of the taxa known for tropical America (Costa 2014a, Gradstein et al. 2001).These percentages demonstrate the importance of the diversity of this family in the Atlantic Rainforest of southeastern Brazil and confirm Zander's (1977) inclusion of the family among the main moss families found in floristic inventories in the Neotropics.

Barbula arcuata
Type: INDIA.Griffith 27 (holotype: BM!).Fig. 1(D-H) Barbula arcuata has a sclerodermis and central strand; the leaves are linear-lanceolate, with apex obtuse, denticulate, with entire margins; the costa is broad, up to 1/3 of the width of the base, its cells are smooth, rectangular, and show guide cells in cross section, epidermal cells only on the ventral surface, and stereids on the dorsal surface.Peristome without teeth.According to its distribution, this taxon is apparently rare in Brazil and only one old collection is known from Rio de Janeiro State.It was reported for the first time in Brazil by Schäfer-Verwimp (1992) in Goiás State, being cited now the second time in the country and for the first in the northern and southeastern regions.
Distribution, habitat and conservation: Widespread globally.In Brazil, reported from AM, GO, MG, RJ and SP.On hu-mid soils along river banks, sometimes submerged, or on moist rocks, 0-900 m, in the Amazon Forest, Savanna, and Atlantic Rainforest (LC).  1 (I-L).This species was reported for the first time in Brazil by Schäfer-Verwimp (1991) in Espírito Santo State, appearing to that author to be quite common from southeastern to northeastern Brazil, as was corroborated by the present study.According to Zander (1979), Barbula indica sensu strictu has leaves narrowly oval to elliptical, with planar margins or weakly recurved at mid-leaf, with small, green, obovoid propagula occurring in masses in the leaf axils, characteristics found in the Brazilian specimens examined.This species appears to be quite common in southeastern and northeastern Brazil.
Distribution, habitat and conservation: Pantropical.In Brazil, reported from AC, AM, BA, DF, ES, GO, MG, MS, MT, PA, PE, RJ, RS, SE and SP.On sandy soils, shady rocks, road banks, steep slopes, 0-1600 m, in the Amazon Forest, Atlantic Rainforest, Savanna (Gallery Forest), Pantanal (seasonally inundated), and Restinga (LC).BM!).Fig. 2 (E-I).According to Vital & Pursell (1992), this species occurs at moderate elevations in Mexico, the West Indies, Central America, and the South American Andes, as well as northeastern and southeastern Brazil -representing an extensive range for the species.
Distribution, habitat and conservation: Tropical America.In Brazil, reported from BA, CE, ES, RJ and SP.Occurs in urban areas, on the ground, or along stream margins on calcareous soils, or shady river banks, 0-540 m, in the Atlantic Rainforest (LC).
Representative specimens examined: BRAZIL.H!, isotype: BM!).Fig. 2 (J-N).This monotypic genus was described by Zander (1989) from the Himalayas of India and Nepal.The Brazilian collections of Schäfer-Verwimp (1992) and Schäfer-Verwimp & Giacontti (1993) were the first records for the Southern Hemisphere, being cited now from Itatiaia (Serra da Mantiqueira) and Nova Friburgo (Serra do Mar) in Rio de Janeiro State.Considered a rare moss, with leaves narrowing toward the base, sporophyte lateral, and capsule plicate without peristome.
Distribution, habitat and conservation: Southeastern Brazil, the Himalayas of India and Nepal.In Brazil, reported from RJ and SP.On shady rocks along riverbanks and on the vertical faces of riverside granitic rocks, 160-700 m, in the Atlantic Rainforest (VU).Gallischen Naturwiss.Ges.1871-72: 354.1873.Gymnostomum involutum Hook., Musci Exot.2: 154.1819.Type: NEPAL.Gardner s.n (holotype: BM!).Fig. 3 (A-E).Easily recognized when dry by the strongly rolled-up leaf margins.The propagula vary in shape and size, and considerable differences were observed in the dentations of the upper leaf margins (Zander 1994) in the Brazilian collections studied.
Distribution, habitat and conservation: Widespread globally.In Brazil, reported from AL, AM, BA, CE, DF, ES, GO, MG, MS, MT, PA, PB, PE, PI, PR, RJ, RO, RR, RS and SP.On shady soils, old stone walls in urban areas, or rocks, 0-1400 m, in the Amazon Forest, Atlantic Rainforest, Caatinga (dry land vegetation), and Savanna (Gallery Forest), being very common in urban areas (LC).(holotype not located).Fig. 4 (O-R).This species is characterized by cirrhate leaves, with papilose laminal cells, and papillae low and hemispherical.There are seven varieties described for this taxon, but only one was cited by Zander (1972) for Brazil, Leptodontium viticulosoides var.panamense (Lor.)R.H. Zander (reported from BA, MG, RJ, RS, SC and SP, between 0-1850 m) with many synonymizations done by him, for example, Lepto- dontium excelsum (Sull.)Britt., L. serrae (Müll.Hal.) Par., and L. ulocalyx (Müll.Hal.) Mitt.There are two collections from Rio Grande do Sul State (Cambará do Sul) housed at NY herbarium and identified as var.panamense; examinations confirmed that they do in fact belong to this variety, differing from the typical variety (var.viticulosoides) by the papillae and spores.Allen (2002) cited L. viticulosoides var.panamense as a synonym of L. ulocalyx (Müll.Hal.) Mitt. a species synonymized by Zander (1972)   (holotype: PC!).Fig. 5 (H-L).A robust species, similar to the genus Pseudosymblepharis Broth., but the leaves are bordered along nearly 2-3 their length by enlarged, bulging, hyaline cells that are denticulate above, and with the upper and basal cells distinctly different.Schäfer-Verwimp & Giacontti (1993) recorded this genus for the first time in southern Brazil, being here cited for the second time for that country, and for the first time in the southeastern region.
Distribution, habitat and conservation: Tropical America.In Brazil, reported from GO, MG, PR, RJ, RS and SP.On rocks, soil, or tree trunks, 0-2000 m, in the Atlantic Rainforest, Savanna, and Steppe (LC).19.Pseudosymblepharis schimperiana (Paris) H.A. Crum, Bryologist. 55: 139. 1952.Syrrhopodon schimperiana Paris, Index Bryol.1254.1898.Type: MEXICO.Veracruz, Orizaba, 1853, Müller s.n.(holotype: BM!).Fig. 5 (M-P).According to Crum (1952), Paris (1898) changed the original name of this species to Syrrhopodon schimperianus because Syrrhopodon circinatus had already been used by Mitten (1869).For this reason, Pseudosymblepharis circinata (Schimp.)Broth.was replaced by Crum (1952) as a new combination based on Syrrhopodon schimperianus Paris.Pseudosymblepharis cavernarum is only known from the type collection (endemic to southeastern Brazil), and the original material exhibits leaves ovate-lanceolate, contorted above, upper laminal cells quadrate, thick-walled, pluripapillose (papillae bulging over lumen), sheathing cells elongated, thick-walled, and porous, laminal cells of sheath long-rectangular, smooth, thin-walled, cells at shoulder hyaline, extending along margin with inner cells typical of limb in a "v"; these are distinctive features of P. schimperiana and considered by Costa (2014b) as conspecific with it.Schäfer-Verwimp (1996) cited the genus and the species as a new record for Brazil, but commented that it could have been reported earlier as Tortella or Trichostomum -and studies of the collections from different Brazilian herbaria have confirmed that possibility.In Brazil P. schimperiana is similar to Trichostomum tenuirostris (Hook.& Tayl.)Lindb.by their narrow leaf bases; however, the upper basal cells near the costa are not porous in Trichostomum.There is one specimen housed at the NY herbarium identified as Trichostomum aureum Bartr.n. sp. that is a nomen nudum because it was never described by Bartram, being only a herbarium name.Zander studied this collection in 1986 (label information) and identified it as P. schimperiana.
Distribution, habitat and conservation: Tropical America, Africa.In Brazil, reported from AL, DF, GO, MG, MS, MT, PE, PR, RJ, RS, SC and SP.On soil, rocks, tree trunks, and rotten wood, also in urban areas, 0-2500 m, in the Atlantic Rainforest, Savanna (Gallery Forest), Steppe, and Restinga (LC).Guerra, Ros & Carrión 1992, G!). Fig. 7 (F-H).Small plants (< 4 mm), with leaves oblong-lanceolate, margins revolute and bordered by 1-2 rows of thick-walled cells, apex smooth in a hyaline hair-point, and peristome very long and twisted (2-3 times).Cano & Gallego (2008) found several syntypes of T. muralis var.longipila housed at the E, NY, O, and PC herbaria, identified as Tortula longipila Dusén from Rio Negro (AM), and selected the specimen at NY as the lectotype.Tortula muralis var.longipila can be distinguished from var. muralis by its long hair-point, capsule with annulus disposed in only one row, and by upper and middle laminal cells with low papillae, while in T. muralis the papillae are taller.However, all of these characteristics are considered by those authors to be included within the natural variability of T. muralis, and they considered it a synonym of that taxon.I agree with these authors because the Brazilian collections showed the same variability.
Distribution, habitat and conservation: Widespread globally.In Brazil, reported from PE, PR, RJ, RS, SC and SP.On soil, rocks, or cement walls, 0-1400 m, in the Atlantic Rainforest and Savanna (LC).Müll. Hal., Bull. Herb. Boissier 6: 92. 1898.Type: BRASILIEN.Serra do Itatiaia, Mont Serrat, 1894, Ule 1814 (holotype: R!; isotype: HBG).Fig. 7 (I-L).The records of Syntrichia fragilis for Goiás and Mato Grosso by Egunyomi &Vital (1984) andGuarim Neto &Yano (1985), respectively, are based on misidentifications, and actually refer to T. weisioides.Trichostomum weisioides is very similar to T. arboreum (Mitt.)R.H. Zander and can be distinguished only by leaves lingulate and short--mucronate.These two taxa may be synonymous.This species is known only from the type collection in Rio de Janeiro State.As it commonly grows as an epiphyte (rarely on the ground) mixed in with other bryophytes, it can easily be overlooked.

Trichostomum weisioides
Distribution, habitat and conservation: Endemic to Brazil, being reported from DF, GO, MT and RJ.On soil and tree trunks, 500-1500 m, in Savanna (Gallery Forest) and Atlantic Rainforest (DD).Müll. Hal.,Syn. Musc. Frond. 1: 664.1849.Type: INSULA ANTILLARUM ST.TOMAS.1841, Breutel s.n.(isotypes: MO!, NY!).Fig. 7 (M-O).Weissia breutelii differs from the other two Brazilian Weissia species (W.controversa Hedw.and W. jamaicensis (Mitt.)Grolle) by having bulging-mammilose leaf cells on the ventral surface but smooth on the dorsal surface.This was also observed by Allen (2002) among Central America plants.The Brazilian collections of W. glazioui from the states of Rio de Janeiro, Rio Grande do Sul, and São Paulo are all very old, and were made by Hampe, Luisier, Puiggari, and Loefgren. According to Hampe (1879), W. glazioui is characterized by leaves involute, canaliculated, narrow, with the basal laminal cells being thin-walled.This author also noted that this species is very similar to Weissia canaliculata.The collection of W. canaliculata housed at the NY herbarium has a label by Zander with the following observation: "near Acta bot.bras.29(3): 354-374.2015.

Weissia breutelii
Weissia breutelii and I here are reducing to synonyms of it" (sic), although the synonym was not published by him.According to Hampe (1874), Hymenostomum striatum is very similar to W. canaliculata by the capsule being gymnostomous (without a peristome) and angled-striate, and Zander (1993) replaced Hymenostomum striatum with W. glazioui.Weissia glazioui was only known from the type collection, being endemic to southeastern Brazil; the original material exhibits the same characteristics of the plants, leaves and cells as W. breutelii will, being considered here as conspecific with it.As these synonyms were not published.Costa (2014b) agreed with both authors and these two taxa were synonymized with W. breutelii.

Excluded records or doubtful reports
The following three taxa are considered poorly known because no material was available to study.(Itatiaia) in Brazil, this collection could not be studied and no other material has been found to confirm this species for Brazil.

Distribution
Many of the species 28.5% (eight taxa) demonstrated wide distributions in Brazil, occurring in a number of different biomes (Amazonia Rainforest, Savanna, and Atlantic Rainforest), while others were restricted to the mountainous regions of southeastern and southern Brazil (25%, seven taxa).Four taxa (14%) are restricted to southeastern Brazil, occurring in mountainous sites in the Atlantic Rainforest.Five taxa (18%) can be encountered in Savanna and Atlantic Rainforest, which seems to be a common geographical distribution for the family.A total of fifteen taxa (53.5%) occur only in the Atlantic Rainforest in Brazil, which is considered the main biome for this family in Brazil.

Conservation status
According to Costa et al. (2005b) the bryoflora of Rio de Janeiro State includes 125 taxa that are vulnerable (VU), 25 endangered (EN), and 153 insufficient data (DD).Rio de Janeiro is considered one of the centers of diversity and endemism in Brazil (Guedes-Bruni & Lima 1997, Rocha et al. 2003, Gradstein & Costa 2003), with high numbers of taxa with distributions predominantly restricted to the southeastern region of the country, or endemic.According to Rocha et al. (2003), although the remaining forests fragments in the state are protected, they still suffer strong anthropogenic pressure due to deforestation (agriculture and pasture), urbanization, the illegal commerce of animals and plants, and the introduction of exotic species.
Habitat fragmentation is a major threat to the bryoflora, especially for species with limited ranges (endemics).The Atlantic Rainforest in southeastern Brazil is under severe pressure (e.g., from agriculture and industrial development) and relentless human interference (population expansion).The protection and conservation of bryophytes represents a new and unfamiliar concept for Brazil, and there are no specific laws protecting these plants.Critical studies have only been undertaken in two states, Pernambuco (Pôrto & Germano 2002) and Rio de Janeiro (Costa et al. 2005a;Costa & Faria 2008;Costa & Santos 2009).

LC-Least Concern:
The majority of the species (20 taxa) are included within this category because: they have widespread distributions in the country; they are known from new collections; they occur in different vegetation types; are found inside protected areas (Conservation Areas); or their distributions have expanded since their initial descriptions.

VU-Vulnerable:
Five taxa are included in this category because they are restricted to the Atlantic Rainforest in Brazil: Ganguleea angulosa: VU B2ab (i, ii, iii), area of occupancy 2,000 km 2 , occurring in less than 10 locations.The species occurs in southeastern Brazil and the Himalayas (India and Nepal).In Brazil, it is restricted to the Montane and Upper Montane Atlantic Rainforest of Rio de Janeiro and São Paulo states, with few herbarium records.Some sub-populations are protected in the Itatiaia National Park.
Type: EUROPA.Faxis muris, tectis, regulis [Linn.Sp.Pl. 2. p. 1581.n. 8. Bryum tegulare humile pillosum & incanum Dill.H.M. 355.t.45.f.14], (lectotype designated by 2, occurring in less than 10 locations.This species occurs in Tropical America, but is only known from the Atlantic Rainforest of southeastern and southern Brazil at high elevations in the following conservation areas: Itatiaia National Park; Serra dos Órgãos National Park; Caparaó State Park; and Serra Geral State Park.VU B2ab (i, ii, iii), area of occupancy 2,000 km 2 , occurring in less than 10 locations.This species is widespread globally, although it is known from only one collection from the Upper Montane Atlantic Rainforest of Rio de Janeiro State, in the Itatiaia National Park in Brazil (Agulhas Negras, ca.2500 m).VU B1ab (i, ii, iii, iv), extent of occurrence 20,000 km 2 , occurring in less than 10 locations.This taxon occurs in Tropical America, Tanzania and Brazil, where it is restricted to the Upper Montane Atlantic Rainforest of Serra da Mantiqueira and Serra dos Órgãos, with sub-populations protected in the Itatiaia National Park and Desengano State Park.VU B1ab (i, ii, iii, iv), extent of occurrence 20,000 km 2 , occurring in less than 10 locations.This species occurs in Tropical America, but it is only known from the Atlantic Rainforest of southeastern Brazil (Rio de Janeiro and São Paulo states), with few herbarium records.Some sub-populations are protected in the following conservation areas: Itatiaia National Park; Desengano State Park; and Serra do Mar State Park.