The scaly tree ferns ( Cyatheaceae-Polypodiopsida ) of Brazil

A synopsis of all scaly tree fern species (Cyatheaceae) occurring in Brazil is presented. We recognize 51 species in three genera [Sphaeropteris one species, Alsophila four species (one subspecies, two varieties), and Cyathea 45 species (one variety)] with 17 taxa being endemic to Brazil. One hybrid endemic to Brazil is recognized. Further included are fi ve species that have not yet been recorded in Brazil, but are expected here because they are found in adjacent countries and occur literally on the border with Brazil. We present the fi rst key covering the family for the whole territory of Brazil.


Introduction
Brazil covers a landmass of 8.5 million km² and encompasses several major fl oral regions: Amazonian lowland rainforest, Cerrado (evergreen tree savannah), Caatinga (dry scrub vegetation), Pantanal (swamp forests) and the Mata Atlântica (Atlantic rainforest) (Forzza et al. 2010).Its most extensive mountain range is the Planalto Central in the east but its highest peak (Pico da Neblina, 2994 m) is found at the northern border to Venezuela, which forms the southern limit of the Guayana Highlands.Because of this vast variety of habitats, the fl ora of Brazil is one of the most diverse on earth and contains many endemics (Forzza et al. 2010).Vegetation types that are almost exclusive to Brazil are the Cerrado, the Caatinga and the Mata Atlântica, which all have suff ered severe degradation since colonial times ( The family Cyatheaceae contains ca.600 species distributed throughout the wet tropics and the temperate southern hemisphere (Lehnert 2009).Th e Neotropics alone harbor ca.210 species, with centers of endemism located in the Greater Antilles, southern Mexico plus Central America and the Andes (Tryon & Gastony 1975).Tryon and Gastony (1975) do not include Brazil as a center of endemism even though they fi nd 37% (9 of 24) of the tree fern species to be endemic.Th ere are confl icting accounts on the number of species in Brazil, resulting from diff erent approaches and species concepts.Revisionary works on the family (Gastony 1973;Stolze 1974;Tryon 1976;Windisch 1977;1978;Barrington 1978;Conant 1983) Schwartsburd et al. 2015).Also, the family has never been treated systematically for the whole country.
In the following, we present a revised list of the Brazilian Cyatheaceae and provide the first synoptical key for the scaly tree ferns of the country.16 spores per sporangia, whereas the Gymnosphaera clade has retained the ancestral condition with 64 spores per sporangia.Other diagnostic features are not found in all species of each clade, thus do not serve as synapomorphies.Since ranks are arbitrary (Judd et al. 2007) and groups not supported by synapomorphies should best be avoided in a natural classification (Christenhusz & Chase 2014), we adhere to a three genera solution for the Cyatheaceae with the genera Sphaeropteris, Alsophila and Cyathea for the time being.Recognizeable monophyla that correspond to subgenera and sections (i.e., Fourniera J.Bommer ex E.Fourn., Schizocanea J.Sm. ex Hook., Sarcopholis Holttum and Gymnosphaera sensu Holttum 1963), we simply refer to as clades.Similarly, we here advocate the usage of the terms "Cnemidaria C.Presl clade" and "Hymenophyllopsis (K.I.Goebel) Christenh.clade" instead of referring to these distinct subunits as subgenera of Cyathea s.str.because the polyphyletic remainder of the genus cannot be further split up satisfactorily in morphologically defined subgenera.

Results
We report 51 species and one hybrid of scaly tree ferns for Brazil and further five species are to be expected from the country with high probability.Seventeen taxa are considered endemic for the country, all being restricted to the Atlantic rainforest.

Discussion
Even if the five non-confirmed taxa are included, Brazil has relatively few scaly tree fern species given its size (51-56 spp. on 8.5 million km²).Adjacent countries may have almost twice the diversity on a far smaller area.Peru has 83 spp.(Lehnert 2011a) on 1.28 million km², Ecuador has 86 spp.(M.Lehnert unpubl.res.) on 0.28 million km² and Colombia probably 110 spp.(M.Lehnert unpubl.res.) on 1.14 million km².With 46 spp., Bolivia has a diversity of scaly tree ferns comparable to that of Brazil (51-56 spp.) but fewer endemics (one spp. vs. 17 spp.).On 1.1 million km² of the Bolivian territory, suitable tree fern habitat is found mainly in the northern lowlands and the wet mointain forests of the so-called Yungas, both of which are contiguous with identical vegetation types in Peru.Generally, most tree ferns grow in the mountains between 1000 and 3000 m, with narrowly distributed (i.e.rare and endemic) species occurring mainly on sandstone and in the tree line ecotone.The low elevation of the mountains in the moister Atlantic coast may be seen as the main factor for the relatively low tree fern diversity in Brazil; another is the weak orographic and geologic structure of the mountain range.The result is a relatively homogenic strip of mountain forest, in which the most prominent feature that structures the habitats is the latitudinal temperature gradient.
The Brazilian species of Amazonia and the Guayana shield are all shared with the neighboring countries, and this is not surprising because these ecosystems are not delimited by national borders.On the other hand the Mata Atlantica, which harbors all Brazilian endemics, reaches only with small extensions into Paraguay, Argentina and Uruguay (Forzza et al. 2010).In a way, Brazilian tree fern endemics are synonymous with Mata Atlantica endemics.In total 17 species of Cyatheaceae are endemic to the Atlantic rainforest, which is 80 % of their diversity encountered here: Only Cyathea delgadii, C. microdonta, C. poeppigii, C. uleana and C. villosa are not restricted to this vegetation type.Given the strong fragmentation and low percentage of protected area of this vegetation type, all 17 endemic species should be categorized at least as near threatened (NT) according to the IUCN categories (IUCN 2012, 2014), with some species that are currently known from only ten or fewer localities (i.e. Alsophila capensis, Cyathea atrocastanea, C. praecincta) also as vulnerable (VU).For the rest of the Brazilian Cyatheaceae, only least concern (LC) can be given because they are widespread and further distributed in other countries.In the case of the Guayana Highland endemics, the small ranges are in remote areas that are already classified as nature reserves and protected indigenous territories, thus they could be considered as not yet threatened (LC or NT).However, given the scarcity of collections and reported field observations from that area, a general classification as data deficient (DD) seems most adviseable.
Naturally occurring hybrids may be the reason for the observed weak morphological differences between some Brazilian taxa of scaly tree ferns.Some currently recognized species have been assumed to be hybrids or of hybridogenic origin (Conant & Cooper-Driver 1980;Lehnert & Weigand 2013).However, based on observations in the field only Cyathea ×stella-matutina seems to be confirmable at present to be a true hybrid (Schwartsburd et al. 2015).Therefore, we are not considering more hybrid taxa in the following taxonomic treatment and key.More field work and especially genetic and karyological studies are required for the solution of this topic, which will deserve a publication on its own.
Plant material herbaria was revised for this study: AAU, B, BM, COL, CUZ, F, FLOR, GH, GOET, HUT, JOI, K, MBM, MBML, MG, MICH, MO, NY, P, RB, S, SP, U, UC, UFP, UPCB, US, W and Z. Online resources were used for checking typifications (plants.jstor.org,apps.kew.org,science.mnhn.fr, ww2.bgbm.org)and references for the species (www.ipni.org,www.tropicos.org,see supplementary material for detailed synonymy and references).Species of the Gymnosphaera Blume clade (Korall et al. 2007; Christenhusz et al. 2011) are currently treated under the genus Alsophila R.Br.(sensu Conant 1983), which may continue to be the nomenclaturally parsimonious solution in a phylogenetically supported classification.Previous phylogenetic studies (e.g.Korall et al. 2007; Janssen et al. 2008; Korall & Pryer 2014) have found the genus Sphaeropteris Bernh.(with non-marginate petiole scales) to be sister to the remainder of the Cyatheaceae, which all have marginate petiole scales.Within this clade, three monophyla are consistently retrieved, which contain the type species of the genera Alsophila, Gymnosphaera and Cyathea Sm., respectively, but their relationship to each other was ambiguous and weakly supported in most of the previous studies (Moran et al. 2008; Korall & Pryer 2014).Now with an ampler and broader sampling (M Lehnert et al. unpubl.res.), the topology with the Cyathea clade (with non-setose petiole scales; psilate to baculate spore ornamentation if present) being sister to the Alsophila and Gymnosphaera clades (both with setate petiole scales; crested to ridged spore ornamentation) slowly emerges to most likely reflect natural relationships.Species of the Alsophila clade are separated morphologically only by having come up with 25 species for the whole country while local floras report even more for a single state (e.g., 29 species for Santa Catarina; Sehnem 1978).Quite recently, some new species have been described (Fernandes 2000; Labiak & Matos 2009), reinstated (Lehnert 2011b; Lehnert & Weigand 2013; Schwartsburd et al. 2015) or reported from the country (Lehnert 2006; 2011b; Carvalho et al. 2012; Almeida & Salino 2015).The 'Catálogo de Plantas e Fungos do Brasil' (Forzza et al. 2010) reports 41 species with 21 endemics for the family.However, this latest work needs to be updated regarding the generic concept (Christenhusz et al. 2011; Lehnert 2012) and the number of species (Carvalho et al. 2012; Prado et al. 2015;