Synopsis of Orchidaceae from Serra do Urubu : an area of montane forest , Pernambuco State , Brazil

(Synopsis of Orchidaceae from Serra do Urubu: an area of montane forest, Pernambuco State, Brazil). This study provides a survey of Orchidaceae species in an area of montane Atlantic Forest in the State of Pernambuco, Brazil. The study area comprises two conservation units (RPPN Frei Caneca and RPPN Pedra D’Anta), forming together the Serra do Urubu, which is located in the border of the Borborema plateau. Orchidaceae is represented in this study area by 81 species and 50 genera. Epidendrum L. (10 spp.) and Habenaria Willd. (four spp.) are the most representative genera. The subtribes Laeliinae (22 spp.) and Pleurothallidinae (14 spp.) together represent about half of the number of species. The high number of orchid species distinguishes Serra do Urubu as one of the richest areas for the family in the Atlantic Forest in northeastern Brazil. Our study also provides 18 new records of species to Pernambuco as well as reporting on about 40% of the species and 60% of the genera cited to the State. Campylocentrum pernambucense, Cattleya labiata, Cattleya granulosa, Phragmipedium sargentianum and Zygostates bradei are cited as endangered, 14 species are endemic to the Atlantic Forest, and other seven have distributions restricted to northeastern Brazil. All these facts reinforce the importance of this area as well as management strategies for the conservation of Orchidaceae.


Introduction
The Atlantic Forest biome is the second largest forested formation in South America, but due to the high level of deforestation, and the high number of endemic species, it is considered one of the world's hotspots in biodiversity (Mittermeyer et al. 2004).
More than 20,000 species of Angiosperms have been recorded for the Atlantic Forest, and ca.8,000 (40%) are considered endemic to this formation (Myers et al. 2000).
Historical factors point out the northern portion of such ecosystem as the most endangered mainly because it is composed of small and isolated fragments in a matrix of sugarcane (Ranta et al. 1998).The Atlantic Forest north of Rio São Francisco [also known as Pernambuco Endemism Center (Prance 1982)] has been far less studied than the southern portion.Furthermore, due to the several new taxa which have been recently described (Alves-Araújo & Alves 2011, 2012a, 2012b, Amorim & Alves 2012, Melo & Alves 2012, Araújo & Alves 2013, Amorin et al. 2013, Costa-Lima & Alves 2013, Lourenço et al. 2013, Terra et al. 2013, Costa-Lima et al. 2014, Pessoa & Alves 2014, Pessoa et al. 2014a, 2014b), the Pernambuco Endemism Center is pontentially much more diverse than it is currently known.
In the State of Pernambuco only 4.6% of the original Atlantic Forest remains (Secretaria de Ciência, Tecnologia e Meio Ambiente 1994), and the only two surveys of the family in these forest fragments were carried out by Siqueira-Filho & Felix (2006) and Pessoa & Alves (2012).According to Stehmann et al. (2009), Orchidaceae is very well represented in the Atlantic Forest, with ca.1400 species (Barros et al. 2014).They also stressed that from the 180 species cited for the State of Pernambuco, 90% of them occur in the forest fragments of this ecosystem.
The aim of this study was to provide a survey of the Orchidaceae species in a montane area of Atlantic Forest in Pernambuco State, northeastern Brazil.Our survey includes an identification key, pictures or illustrations, and comments on geographical distribution, ecology as well as main characters of the species.

Material and methods
The study area comprises two conservation units: Reserva Particular do Patrimônio Natural (RPPN) Frei Caneca and Reserva Particular do Patrimônio Natural (RPPN) Pedra D'Anta.Both areas are located in the Serra do Urubu (8°42'S and 35°50'W), within the municipalities of Lagoa dos Gatos, São Benedito do Sul and Jaqueira, in the eastern border of the Borborema plateau (Pernambuco State, northeastern Brazil).
The climate is considered tropical wet and dry (Aw sensu Köppen), with an annual average precipitation of 1200 mm, and mean temperatures between 18-30 °C (LAMEPE/ITEP).The site comprises Montane Dense Ombrophilous Forest based on the types of vegetation proposed by Veloso (1992).
The Serra do Urubu is mainly covered by forest with some exposed rocky outcrops and has an altitude of 600-750 m ASL.The lower elevation areas (300-400 m) are occupied by sugarcane crops.
The fieldwork was carried out from December 2010 to May 2013, covering eleven months of each year with the exception of February.The samples were submitted to the usual taxonomic procedures (Mori et al. 1985) and then deposited at the UFP herbarium, with duplicates sent to NY and RB, among other herbaria.
The morphological terminology follows Harris & Harris (2001) and Gonçalves & Lorenzi (2007).The data on geographical distribution of the species follows Barros et al. (2014) and Govaerts et al. (2014).Basionyms, whenever necessary, are provided after the accepted name as well as new synonyms.

Results and Discussion
Orchidaceae is represented in Serra do Urubu by 81 species and 50 genera.Epidendrum L. (10 spp.) and Habenaria Willd.(four spp.) are the most speciesrich genera.The subtribes Laeliinae (22 spp.) and Pleurothallidinae (14 spp.) represent together almost half of the total number of species found in the area.The diversity of orchid species in Serra do Urubu ranks the area as one of the richest for the family in the Atlantic Forest in northeastern Brazil (Pessoa & Alves 2011, Pessoa & Alves 2012, Marinho & Azevedo 2013, Coelho & Amorim 2014).
This study provides 18 new records of species to the State of Pernambuco.The results also encompass about 40% of the species and 60% of the genera cited to the State by Barros et al. (2014).The forested portion of Serra do Urubu is more speciesrich (65 spp.) than the rock outcrops (17 spp.), and only five species share both habitats.According to Barros et al. (2014), among the species found in the area, 14 are considered endemic to the Atlantic Forest, and seven are known only in northeastern Brazil, including a recently described one, Specklinia integripetala E.Pessoa & F. Barros (Pessoa et al. 2014a).Campylocentrum pernambucense Hoehne, Cattleya labiata Lindl., Cattleya granulosa Lindl., Phragmipedium sargentianum (Rolfe) Rolfe and Zygostates bradei (Schltr.)Garay are cited as endangered by the Ministério do Meio Ambiente (2008( ), Biodiversitas (2008) ) and Martinelli & Moraes (2013).These facts reinforce the value of the area for Orchid conservation.
When the data are compared to a lowland Atlantic Forest area in Pernambuco State [Usina São José, Pessoa & Alves (2012)], it is clear that both sites do not share the same compostion of the orchid flora (only 11 shared species).Around 80% of the species from the montane forest are not found in the lowland forest, which shows a strong split pattern in the orchid flora locally.
Seventeen species cited by Siqueira-Filho & Felix (2006) for the same area were not found during our field trips nor located at the indicated herbaria.Due to the lack of vouchers to corroborate the occurrence of these species in the area, they were ruled out from the present study.1a This epiphyte differs from Acianthera hygrophyla by the peduncle of the inflorescence longer than the subtending leaf.It occurs in forested areas and it is endemic to the Atlantic Forest of Brazil (States of Pernambuco, Alagoas, Bahia, Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo, Paraná, Santa Catarina and Rio Grande do Sul) (Barros et al. 2014, Govaerts et al. 2014).
Examined material: BRAZIL.Pernambuco: Jaqueira, RPPN Frei Caneca, 11-III-2011, fl 1b This epiphyte differs from Acianthera glumacea by the peduncle of the inflorescence shorter than the subtending leaf.It occurs in forested areas and it is endemic to the Atlantic Forest of Argentina and Brazil (States of Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo, Paraná, Santa Catarina and Rio Grande do Sul) (Barros et al. 2014, Govaerts et al. 2014) 2a This epiphyte is easily recognized among the Pleurothallidinae in the area by the long peduncle (> 1.0 cm long), from where the purplish flowers arise successively from the same point.It occurs in forested areas, and it is widely distributed in the Neotropics, including Brazil (Barros et al. 2014, Govaerts et al. 2014).
Bot. Estado São Paulo 1: 22. 1938.Figure 1e This epiphyte is easily recognized among the species of the genus in the area by its cylindrical leaves and shorter inflorescence (< 0.8 cm long).It occurs in forested areas and it is endemic to the Atlantic Forest of northeastern Brazil (States of Paraiba, Pernambuco, Alagoas and Sergipe) (Barros et al. 2014, Govaerts et al. 2014) 1f This epiphyte differs from Cattleya labiata by the 2-leaved, cylindrical pseudobulbs and sepals greenish to yellowish with brown spots.It occurs in forested areas and it is endemic to the Brazilian Atlantic Forest (States of Rio Grande do Norte, Paraíba, Pernambuco, Alagoas, Bahia and Espírito Santo) (Barros et al. 2014, Govaerts et al. 2014).It is cited as endangered by the Ministério do Biodiversitas (2008), Meio Ambiente (2008) and Martinelli & Moraes (2013).It is rarely found in the Serra do Urubu.

1833. Figure 2k
This epiphyte differs from Dichaea pendula by its articulated linear-oblong leaves, and non-geniculated peduncle of the inflorescence.It occurs in forested areas and it is widely distributed in the Neotropics (Govaerts et al. 2014).In Brazil, it has a disjunct distribution between the Amazon and Atlantic Forests (States of Amazonas, Pará, Amapá, Rondônia, Mato Grosso, Paraíba, Pernambuco, Alagoas and Sergipe) (Barros et al. 2014).

Figure 1h
This epiphyte resembles an Epidendrum, but differs from the species of that genus in the area by its pinkish flowers with the column basally adnate with the lip.It occurs in forested areas and it is widely distributed in the Neotropics (Govaerts et al. 2014).In Brazil, it has a disjunct distribution between the Amazon and Atlantic Forests (States of Amazonas, Amapá, Pará, Maranhão, Ceará, Paraíba, Pernambuco, Alagoas, Sergipe, Bahia and Espírito Santo) (Barros et al. 2014).
29. 1760.Figure 2n This epiphyte differs from E. strobiliferum by its linear-oblong leaves and linear petals.It occurs in forested areas and it is widely distributed in the Neotropics (Govaerts et al. 2014).In Brazil, it has a disjunct distribution between the Amazon and Atlantic Forests (States of Amazonas, Amapá, Roraima, Ceará, Pernambuco, Bahia, Rio de Janeiro, Minas Gerais, Espírito Santo, São Paulo, Paraná, Santa Catarina and Rio Grande do Sul) (Barros et al. 2014) 1n This epiphyte differs from E. ramosum by its lanceolate to elliptical leaves and oblanceolate petals.It occurs in forested areas and it is widely distributed in the Neotropics (Govaerts et al. 2014).In Brazil, it has a disjunct distribution between the Amazon and Atlantic Forests (States of Acre, Amazonas, Amapá, Pará, Roraima, Rondônia, Mato Grosso, Goiás, Maranhão, Pernambuco, Alagoas, Minas Gerais, São Paulo and Paraná) (Barros et al. 2014).
Examined material: BRAZIL.Pernambuco: Lagoa dos Gatos, RPPN Pedra D'Anta, 17-XII-2010, fl., E. Pessoa et al. 420 1r This terrestrial herb differs from species such as H. pratensis and H. trifida, which also have 2-lobed petals and a 3-lobed lip, by its ovate sepals and anterior lobe of the lip longer than the posterior one.It occurs on rock outcrops and it is endemic to Brazil (States of Paraíba, Pernambuco Bahia, Distrito Federal, Goiás, Minas Gerais, and São Paulo) (Barros et al. 2014, Govaerts et al. 2014).
Examined material: BRAZIL.Pernambuco: Jaqueira, RPPN Frei Caneca, 3-IX-2013, fl., A. Melo 1197 (UFP).Lindl., Gen. Sp. Orchid Pl. 316. 1835.Figure 1s This terrestrial herb differs from the other Habenaria species found in the area by its entire petals and lip.It occurs on rock outcrops and it is known from Argentina, Paraguay and Brazil, where it is widely distributed (Barros et al. 2014, Govaerts et al. 2014) 1t This terrestrial herb differs from H. trifida by its posterior lobe of the petals elliptical, mid-lobe of the lip rhomboid, and shorter spur (< 3.0 cm long).It occurs on rock outcrops and it is endemic to Brazil (States of Maranhão, Rio Grande do Norte, Paraíba, Pernambuco, Sergipe, Alagoas, Bahia, Mato Grosso, Goiás and Santa Catarina) (Barros et al. 2014, Govaerts et al. 2014).

Habenaria petalodes
Examined material: BRAZIL.Pernambuco: Jaqueira, RPPN Frei Caneca, 17-VIII-2010, fl., M.A. Chagas 20 (UFP).Kunth, Nov. Gen. Sp. 1: 330. 1816.Figure 3a This terrestrial herb differs from H. pratensis by its posterior lobe of the petals oblong to linear, mid-lobe of the lip linear-oblong, and longer spur (> 3.0 cm long).It occurs on rock outcrops and it is widely distributed in the Neotropics and also in Brazil (Barros et al. 2014, Govaerts et al. 2014) 2r This epiphyte differs from Nitidobulbon nasutum by its discolorous leaves and shorter acute sepals (< 2.0 cm long).It occurs in forested areas, and it is known from Belize, Nicaragua, French Guyana, Guyana, Suriname, Venezuela, Ecuador, Peru, Bolivia and Brazil (States of Amazonas, Amapá, Pará, Roraima and Bahia) (Barros et al. 2014, Govaerts et al. 2014) 3c This epiphyte differs from J. teretifolia by its sessile inflorescence and purple flowers.It occurs in forested areas and it is widely distributed in the Neotropics (Govaerts et al. 2014); in Brazil, it is found in the Amazon and Atlantic Forests (States of Amazonas, Pará, Roraima, Ceará, Pernambuco, Alagoas, Sergipe, Bahia, Espírito Santo, Rio de Janeiro, São Paulo, Paraná and Santa Catarina) (Barros et al. 2014).2s This epiphyte differs from J. globosa by its longpedunculate inflorescence and yellowish to orangish flowers.It occurs in forested areas and it is widely distributed in the Neotropics (Govaerts et al. 2014); in Brazil, it is found in the Amazon and Atlantic Forests (States of Amazonas, Roraima, Bahia, Minas Gerais, Espírito Santo, Rio de Janeiro and São Paulo) (Barros et al. 2014)

Figure 2t
This epiphyte is easily distinguished from the other Pleurothallidinae in the area by its lepanthiform sheaths.It occurs in forested areas and it is widely distributed in the Neotropics (Govaerts et al. 2014); in Brazil, it grows in the Amazon and Atlantic Forests (States of Pernambuco, Espírito Santo, Rio de Janeiro, São Paulo, Paraná and Santa Catarina) (Barros et al. 2014).
Examined material: BRAZIL.Pernambuco: Jaqueira, RPPN Frei Caneca, 30-V-2012, fl. e fr., E. Pessoa et 4a This terrestrial herb can be confused vegetatively in the area with Malaxis excavata, but can be easily recognized by its racemose inflorescence and 2-lobed lip.It occurs in forested areas and it is pantropical and widely distributed in Brazil (Barros et al. 2014, Govaerts et al. 2014).
Pl. 2: 673.1891 ≡ Microstylis excavata Lindl., Edwards's Bot.Reg.24: 51.1838.Figure 3d This terrestrial herb can be confused vegetatively in the area with Liparis nervosa, but it can be easily recognized by its umbellate inflorescence and acute lip.It occurs in forested areas and it is widely distributed in the Neotropics (Govaerts et al. 2014) 3e This epiphyte differs from Mormolyca rufescens by its pseudo-petiolate leaves and papillose mid-lobe of the lip.It occurs in forested areas and it is known from French Guyana, Guyana, Suriname, Venezuela, Colombia, Ecuador, Peru and Brazil (States of Amazonas, Pará, Bahia, Espírito Santo, Rio de Janeiro, São Paulo, Paraná and Santa Catarina) (Barros et al. 2014, Govaerts et al. 2014) Barb. Rodr., Gen. Sp. Orchid. 2: 198. 1882.Figure 3f This epiphyte can be confused in the area with Mormolyca rufescens and Mapinguari desvauxianus, but it differs by its inflorescences twice as long as the length of the pseudobulb.It occurs in forested areas, and it is known from French Guyana and Brazil (States of Amazonas, Pará, Ceará, Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo, Paraná and Santa Catarina) (Barros et al. 2014, Govaerts et al. 2014) 4b This epiphyte differs from Camaridium carinatum by its pseudo-petiolate apical leaf, withish flowers and longer sepals (> 3.5 cm long).It occurs in forested areas and it is known from Venezuela, Colombia, Ecuador, Peru and Brazil (States of Roraima, Pernambuco, Bahia, Espírito Santo, Rio de Janeiro, Minas Gerais, São Paulo, Paraná and Santa Catarina) (Barros et al. 2014, Govaerts et al. 2014).
Ecuador 9: 238.1978 ≡ Spiranthes cuspidata Lindl., Gen. Sp.Orchid.Pl.: 471.1840.Figure 4c This terrestrial herb differs from Sacoila lanceolata by having leaves when in bloom and by the yellowish-white flowers.It occurs in forested areas and it is known from Guyana, Suriname, Venezuela, Colombia, Ecuador, Peru, Bolivia, Paraguay, Argentina and Brazil (States of Mato Grosso, Goiás, Distrito Federal, Espírito Santo, Rio de Janeiro, Minas Gerais, São Paulo, Paraná, Santa Catarina and Rio Grande do Sul) (Barros et al. 2014, Govaerts et al. 2014) 4d This epiphyte differs from Mapinguari desvauxianus by its sub-sessile leaves and smooth, not papillose mid-lobe of the lip.It occurs in forested areas, and it is known from Belize, Guatemala, Honduras, Trinidad and Tobago, French Guyana, Guyana, Suriname, Venezuela, Colombia, Ecuador, Peru and Brazil, where it is widely distributed (Barros et al. 2014, Govaerts et al. 2014).

Figure 3h
This epiphyte differs from Heterotaxis discolor by its concolorous leaves and longer acuminate sepals (> 2.5 cm long).It occurs in forested areas and it is widely distributed in the Neotropics (Govaerts et al. 2014); in Brazil, it is found in the Amazon and Atlantic Forests (States of Amazonas, Roraima, Mato Grosso, Bahia and Espírito Santo) (Barros et al. 2014).It is a new record for the State of Pernambuco.However it was not recollected during this survey.
Examined material: BRAZIL.Pernambuco: Jaqueira, RPPN Frei Caneca, 9-VII-1999, fl., J.A. Siqueira-Filho & J.A. Vicente 984 (UFP).Barb. Rodr., Gen. Sp. Orchid. 2: 223. 1882.Figure 4e This epiphyte is easily distinguished from the orchids in the area by its pendulous inflorescence and flowers with a clawed lip.It occurs in forested areas and it is endemic to Brazil (States of Ceará and Minas Gerais) (Barros et al. 2014, Govaerts et al. 2014).It is a new record for the State of Pernambuco.Schltr., Anexos Mem. Inst. Butantan, Secc. Bot. 1: 53. 1922.Figure 3i This rupiculous herb can be confused vegetatively in the area with Brassavola tuberculata, but it is easily distinguished by its congested fascicle and shorter sepals (< 1.0 cm long).It occurs on rock outcrops and it is endemic of Brazil (States of Bahia, Rio de Janeiro, São Paulo and Rio Grande do Sul) (Barros et al. 2014, Govaerts et al. 2014) 4f This terrestrial herb is easily distinguished from other species in the area by its variegated leaves and the apically 2-lobed spur.It occurs in forested areas and it is pantropical and widely distributed in Brazil (Barros et al. 2014, Govaerts et al. 2014).
Examined material: BRAZIL.Pernambuco: Jaqueira, RPPN Frei Caneca, 30-V-2012, fl., E. Pessoa 4h This terrestrial herb is easily recognized among the species in the area by its undulated petals, calceolate lip, and a conspicuous shield-like staminode.It occurs on rock outcrops and it is endemic to the Atlantic Forest of northeastern Brazil (States of Pernambuco, Alagoas and Bahia) (Barros et al. 2014, Govaerts et al. 2014).It is cited as endangered by the Ministério do Meio Ambiente (2008) and Biodiversitas (2008).It is rarely found in the Serra do Urubu.
Examined material: BRAZIL.Pernambuco: Jaqueira, RPPN Frei Caneca, 29-V-2012, fl., E. Pessoa et 4i This epiphyte differs from Myoxanthus exasperatus by its lateral sepals by being completely connate.It occurs in forested areas and it is widely distributed in the Neotropics (Govaerts et al. 2014); in Brazil, it has a disjunct distribution between the Amazon and Atlantic Forests (States of Pará, Roraima and Ceará) (Barros et al. 2014).It is a new record for the State of Pernambuco.
Examined material: BRAZIL.Pernambuco: Jaqueira, RPPN Frei Caneca, 20-IX-2011, fl., B.S. Amorim 1087 (UFP).Barb. Rodr., Gen. Sp. Orchid. 2: 273. 1882.Figure 3o This terrestrial herb is easily recognized among the species in the area by its ovate, conduplicate leaves distributed along the stem, flowers without a spur, and column free.It occurs in forested areas, and it is known from Venezuela and Brazil (States of Amazonas, Bahia, Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo, Paraná, Santa Catarina and Rio Grande do Sul) (Barros et al. 2014, Govaerts et al. 2014) 3p This epiphyte is easily recognized among the species in the area by its 2-leaf pseudobulbs and 1-flowered inflorescence.It occurs in forested areas and it is known from Venezuela, Colombia, Ecuador, Peru, Bolivia and Brazil (States of Roraima, Maranhão, Bahia, Espírito Santo, Rio de Janeiro, Minas Gerais, São Paulo, Paraná, Santa Catarina and Rio Grande do Sul) (Barros et al. 2014, Govaerts et al. 2014) 4p This terrestrial or rupiculous herb is easily recognized among the species in the area by its plicate leaves and big white flowers (sepals > 6.0 cm long).It occurs on rock outcrops and it is known from French Guyana, Guyana, Suriname, Venezuela, Colombia, Peru, Bolivia and Brazil (States of Amazonas, Roraima, Amapá, Pará, Mato Grosso, Pernambuco, Sergipe, Bahia and Espírito Santo) (Barros et al. 2014, Govaerts et al. 2014).
This hemi-epiphyte differs from V. aff.pompona by the texture (membranaceous) and shape (elliptic) of the leaf blades and the length of the internodes (< 7.0 cm long).The identity of the collected specimen is still obscure due to the lack of flowers, but based on vegetative and fruit characters, it appears to belong to the V. mexicana group.It is found in forested areas.
1829. Figure 3t This hemi-epiphyte differs from V. aff.mexicana by its coriaceous, oblong leaves, and longer internodes (> 9.0 cm long).It occurs in forested areas and it is widely distributed in the Neotropics (Govaerts et al. 2014); in Brazil, it is cited to the Amazon and Atlantic Forests (States of Amazonas, Amapá, Tocantins, Rondônia, Paraíba, Pernambuco, Mato Grosso and Minas Gerais) (Barros et al. 2014).
Additional material: BRAZIL.Pernambuco: São Lourenço da Mata, Estação Ecológica de Tapacurá, 17-XI-2010, fl., E. Pessoa et al. 403 4t This epiphyte is easily recognized among the species in the area by its flowers with serrate sepals.It occurs in forested areas and it is endemic to the Brazilian Atlantic Forest (States of Pernambuco, Alagoas, São Paulo, Paraná and Santa Catarina) (Barros et al. 2014, Govaerts et al. 2014).It is cited as endangered by Biodiversitas (2008).There are large populations of this species in the Serra do Urubu.
. It is a new record for the State of Pernambuco.
(Barros et al. 2014)4)or the State of Pernambuco and another case of disjunction between the Amazon and Atlantic Forests.This epiphyte can be confused vegetatively in the area with E. linifolius, but it differs by its floral bracts covering only the base of the pedicellate ovary, and pinkish flowers.It occurs in forested areas, and it is widely distributed in the Neotropics(Govaerts et al. 2014), including Brazil (States of Ceará, Pernambuco, Bahia, Distrito Federal, Mato Grosso do Sul, Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo, Paraná, Santa Catarina and Rio Grande do Sul )(Barros et al. 2014).
. It is a new record for the State of Pernambuco.
. It is a new record for the State of Pernambuco.
. It is a new record for the State of Pernambuco.
. It is a new record for the State of Pernambuco.