Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil

Rafaela Campostrini Forzza

This study presents a list of angiosperm species in an Atlantic Forest fragment in the southern portion of Espírito Santo state, Brazil, a region that represents a collection gap within the Atlantic Forest. The studied site is a relatively small fragment of 144 ha located within a conservation unit, the Mata das Flores State Park. The site belongs to a conservation priority area for the Atlantic Forest in Espírito Santo, and is under strong anthropic pressure. Of the 239 species listed here, 21 are new records for the state, eight are endemic, and 20 figure either in the country’s or the state’s Red Lists of endangered species. Rubiaceae and Piperaceae were the families with the highest number of species. We show that small fragments that were never inventoried before can reveal a relatively large number of threatened species and that collection gaps need to be filled in order to refine our understanding about conservation priorities within the Atlantic Forest Biome.

This paper provides a floristic inventory of Angiosperms reported from six fragments of Atlantic Forest in the State of Pernambuco, northeastern Brazil. The fragments studied are of different sizes and shapes (from 12 to 380 ha) and are embedded within a matrix of sugarcane plantation. The inventory was made from 2005 to 2008, with a more intensive effort from February 2007 to May 2008 with an average of 5 days of fieldwork a month. The samples collected are available at the herbaria IPA, UFP, and ULM. Six categories of life-forms were established: terrestrial herbs and shrubs; aquatic herbs and shrubs; epiphytes and hemiepiphytes; parasites, hemiparasites and saprophytes; herbaceous and woody climbers; and treelets and trees. A checklist with 650 species, from 379 genera and 105 families of Angiosperms is presented. Fabaceae, Poaceae, Cyperaceae, Asteraceae, Euphorbiaceae, Myrtaceae, Rubiaceae, Melastomataceae, Araceae, Malvaceae, Apocynaceae, Sapindaceae and Sapotaceae presented the greatest species richness. Among the fragments, Zambana had 266 species, followed by Piedade with 236 species and Macacos with 228 species. Herbs and shrubs with 274 species, treelets and trees with 212 species and herbaceous and woody climbers with 94 species are the richest life-form categories. This floristic inventory confirms the ecological value of the fragments of Atlantic Forest located at Usina São José. Previous checklists elaborated in the northeastern Atlantic forest have underestimated plant species diversity.

A list of angiosperms from Serra do Urubu, a montane forest area in the state of Pernambuco, is here provided. Based on 14 botanical expeditions and material deposited in herbaria, 832 taxa belonging to 442 genera and 118 families have been recorded in this area, with about 90% of the taxa identified to species level. The richest families are Orchidaceae (86 spp.), Fabaceae (51 spp.) and Rubiaceae (42 spp.). Miconia and Solanum (14 spp. each), and Psychotria (13 spp.) are the richest genera. About 15% of the recorded species are endemic to the Atlantic Forest, and another 10% are disjunct between this area and the Amazon Rainforest. The results indicate that the Serra do Urubu is one of the richest areas in terms of number of species of the Atlantic Forest in the Northeast, and corroborates the Pernambuco Endemism Center.

Biota Neotropica 14(2): 1––12, 2014 www.scielo.br/bn inventory Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil Paula Leitman1,5, André Amorim2,3, Luiz Menini Neto4 & Rafaela C. Forzza1 1 Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão 915, Jardim Botânico, Rio de Janeiro, RJ, Brazil , CEP: 22460-030 2 Universidade Estadual de Santa Cruz, Departamento de Ciências Biológicas, Salobrinho, Ilhéus, BA, Brazil, CEP: 45662900 3 Centro de Pesquisas do Cacau - Herbário CEPEC, Caixa Postal 07, Itabuna, Bahia, Brazil, CEP: 45660970 4 Centro de Ensino Superior de Juiz de Fora, Campus Arnaldo Janssen - Rua Luz Interior 345, Santa Luzia, Juiz de Fora, MG, Brazil, CEP: 36030-776 5 Corresponding author: Paula Leitman, e-mail: paulaleitman@gmail.com LEITMAN, P., AMORIM, A., MENINI NETO, L., FORZZA, R.C. Epiphytic angiosperms in a –12. http://dx.doi.org/10.1590/S1676mountain forest in southern Bahia, Brazil. Biota Neotropica. 14(2): 1– 06032014001013 Abstract: The Atlantic Forest in southern Bahia State, Brazil, has high levels of diversity and vascular plant endemism. There have been few floristic surveys of the mountain forests there, however, especially those focusing on herbs and canopy plants, with studies of Atlantic Forest epiphytes having been limited to the southern and southeastern region of that country. The present study therefore surveyed the epiphytic angiosperms in the Serra das Lontras National Park (SLNP), the distribution of their species among genera and families, and their biogeographical patterns. Fieldwork was performed between February 2011 and March 2012. Collections were made along roads and trails and phorophytes were occasionally climbed and fallen trees and branches examined in order to sample canopy species. The study site demonstrated high epiphyte richness (256 spp.), one of the highest recorded in the Atlantic Forest. The richest families are Orchidaceae, Bromeliaceae, and Araceae, reaffirming the patterns reported in previous major reviews on epiphytes. The species exhibit high degrees of endemism (45%) to the Atlantic Forest, especially among the Bromeliaceae and Orchidaceae. One new occurrence to Brazil, four to the Atlantic Forest and 30 to Bahia state are registered. The SLNP shares more species with areas of southern and southeastern Brazil than with other northeastern states. Keywords: Atlantic forest, Araceae, Bromeliaceae, Orchidaceae, biogeographical patterns. LEITMAN, P., AMORIM, A., MENINI NETO, L., FORZZA, R.C. Angiospermas epı́fitas de uma floresta montana no sul da Bahia, Brasil. Biota Neotropica. 14(2): 1––12. http://dx.doi.org/10.1590/S167606032014001013 Resumo: A Floresta Atlântica do sul da Bahia apresenta elevados nı́veis de diversidade e endemismo de plantas vasculares. No entanto, poucos levantamentos florı́sticos foram realizados em áreas de floresta montana, especialmente para ervas e plantas de dossel. Estudos com epı́fitas estão concentrados principalmente em áreas do Sul e Sudeste do Brasil. Desta forma, o presente estudo realizou o levantamento das angiospermas epı́fitas do Parque Nacional da Serra das Lontras (PNSL) e verificou a distribuição das espécies pelas famı́lias e gêneros e seus padrões biogeográficos. As coletas foram realizadas entre fevereiro de 2011 e março de 2012 nas trilhas e estradas de acesso. Alguns forófitos foram escalados e árvores e ramos caı́dos foram examinados com o intuito de coletar espécies restritas ao dossel. A área de estudo apresentou alta diversidade de epı́fitas (256 spp.), uma das maiores já registradas para a Floresta Atlântica. As famı́lias com maior riqueza são Orchidaceae, Bromeliaceae e Araceae, reafirmando os padrões encontrados anteriormente em revisões do tema. As espécies apresentam alto grau de endemismo (45%) à Floresta Atlântica, especialmente em Bromeliaceae e Orchidaceae. São registradas uma nova ocorrência para o Brasil, quatro para a Floresta Atlântica e 30 para a Bahia. O PNSL possui mais espécies em comum com o Sul e o Sudeste do que com a região Nordeste. Palavras-chave: Floresta Atlântica, Araceae, Bromeliaceae, Orchidaceae, padrões biogeográficos. http://dx.doi.org/10.1590/S1676-06032014001013 http://www.scielo.br/bn 2 Biota Neotrop., 14(2): 1– –12, 2014 Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil Introduction Epiphytes spend most or all of their life cycles growing on other plants (phorophytes), taking advantage of their mechanical support (Benzing 1990). Epiphytes account for approximately 10% of world’s vascular flora and are found in 84 angiosperm families (Gentry & Dodson 1987, Kersten 2010). Araceae, Bromeliaceae, and Orchidaceae are the most successful epiphytic angiosperm families, and the latter is responsible for over 70% of total richness. Bromeliaceae is a typically American family, while the largest genera of Araceae and Orchidaceae (e.g., Anthurium, Epidendrum, Lepanthes, Philodendron and Pleurothallis s.l.) are likewise endemic to that continent. The Neotropical region therefore hosts the greater part of world’s epiphytic flora (. 15.500 spp.), which are mainly concentrated in Central America, the Andes, northwestern Amazonia and the Atlantic Forest (Gentry & Dodson 1987, Nieder et al. 2001). Of the 14.500 vascular plants known to inhabit the Atlantic Forest, 3.000-4.000 are epiphytes (Stehmann et al. 2009, Kersten 2010). The Atlantic Forest has large latitudinal (from 36S to 306S) and altitudinal (from sea level up to 2.890 m) extensions and significant rainfall variations – resulting in high habitat heterogeneity and an extraordinary diversity of organisms (Oliveira-Filho & Fontes 2000). Southern Bahia is considered an area of great biological importance, with elevated levels of richness and endemism in its arboreal component (Mori et al. 1983, Thomas et al. 1998, Martini et al. 2007, Thomas et al. 2009, Rocha & Amorim 2012), although surveys of humid montane forests have been scarce, especially those focusing on terrestrial and epiphytic herbs (Amorim et al. 2009, Matos et al. 2010). The recently created Serra das Lontras National Park comprises a vast remnant of montane Atlantic Forest in southern Bahia (Save Brasil et al. 2009). A preliminary survey in the park, covering only a small area, recorded 709 angiosperm species, of which 158 (22.3%) were epiphytes (Amorim et al. 2009). These authors highlighted the fact that many of the species encountered, including many epiphytes (e.g., Fuchsia regia [Vell.] Munz, Nematanthus lanceolatus [Poir.] Chautems, and Vriesea longicaulis Mez), were previously known only from mountainous areas in southern and southeastern Brazil. For the preliminary survey there was no effort focused on this habit, which presents peculiarities that hinder their sampling, including the height they occur on the phorophyte and the small sizes of some groups (e.g., Peperomia and Pleurothallis s.l.). We therefore sought to inventory the composition of epiphytic angiosperms in the Serra das Lontras National Park to investigate their distributions into genera and families and their biogeographical patterns to increase our knowledge of this group in the park and in northeastern Brazil. Material and methods Serra das Lontras National Park (SLNP) is located in southern Bahia State (Figure 1), Brazil, in the municipalities of Arataca, São José da Vitória, and Una (156079-156159S and 396159-396259W). The park comprises approximately 11.000 hectares at altitudes that vary from 400 to 1.000 m. Located 30 km from the coast, the mountains act as a first barrier to humid air masses moving inland from the ocean, resulting in http://www.scielo.br/bn mean annual precipitation rates of 1.300-1.600 mm, without a marked dry season, and a mean annual temperature of 246C (classified as Af in the Koppen system) (Peel et al. 2007, Amorim et al. 2009, Nacif et al. 2009). Situated in the Atlantic Forest domain, the SLNP comprises a vegetation mosaic of anthropogenic areas mixed with wellpreserved submontane forests (with canopies .30 m) at lower altitudes and cloud forests above 800 m with smaller trees with twisted trunks bearing bryophytes (Stadtmüller 1987). A total floristic inventory of the SLNP has been underway for the last eight years, and preliminary results have already been published (Amorim et al. 2009; Save Brasil et al. 2009). Visits to the area were made every two months, from February/ 2011 to March/2012 to survey the epiphytic angiosperms. Collections were made along roads and trails in order to cover the largest possible areas, and some living phorophytes were occasionally climbed and fallen trees examined to collect canopy species. Accidental epiphytes were not considered in this survey. Informations on the type of epiphytism (characteristic holoepiphyte, facultative holoepiphyte, hemiepiphyte) were obtained from local observations and complemented with informations from literature. This was done in order to have more accurate data, since many facultative species might have been seen only as epiphytes in the area or might occur as terrestrial or rupiculous in parts of the park that were not visited. All fertile material was deposited at the RB and CEPEC herbaria, while sterile specimens were incorporated into the exsitu collection at the Rio de Janeiro Botanical Garden. Specimens collected during the general floristic inventory, as well as those from the present survey, were identified to the species level, when possible, with the help of specialists and specific literature (e.g., the Flora Neotropica). Nomenclature and species concepts follow the List of Species of the Brazilian Flora - LSBF (2013). Distribution and endemism data were obtained from the LSBF for taxa identified to the species level. A Rapid Color Guide, published by The Field Museum, was prepared and images on most species can be seen at www. fm2.fieldmuseum.org/plantguides/guideimages.asp?ID=545. Results The Serra das Lontras National Park shows high epiphyte richness, with a total of 256 species identified, representing 87 genera and 18 families (Table 1) – making it one of the richest sites for epiphytic angiosperms in the Atlantic Forest. Of the published checklists, only Macaé de Cima in Rio de Janeiro State reported more epiphyte species (275 spp.) (Fontoura et al. 1997). The most important families encountered were Orchidaceae (106 spp.), Bromeliaceae (64 spp.), Araceae (31 spp.), and Piperaceae (14 spp.). Together, these families encompassed more than 80% of the epiphyte flora at SLNP. The species distributions within the families were very unequal, however, with 11 families being represented by less than five species. The richest genera were Vriesea (22 spp.), Peperomia and Stelis (14 spp. each), Anthurium (13 spp.), Aechmea and Philodendron (12 spp. each), Epidendrum (11 spp.), and Hohenbergia (10 spp.). The species distributions within the genera were very unequal, with half of them (43 genera) being represented by only a single species, and 82% by less than five species. With many ornamental species, 10 epiphytes registered for the SLNP are cited on the Red Book of Brazilian Flora http://dx.doi.org/10.1590/S1676-06032014001013 Biota Neotrop., 14(2): 1––12, 2014 3 Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil Figure 1. Map showing the location of the studied area (Serra das Lontras National Park); in gray is the Atlantic Forest limits. N.P. - National Park; B.R. - Biological Reserve/Mapa de localização da área de estudo (Parque Nacional da Serra das Lontras); em cinza está demarcado o limite da Floresta Atlântica. (Martinelli & Moraes 2013). Of this total, three are ‘‘Critically endangered’’, five are ‘‘Endangered’’, and two are ‘‘Vulnerable’’. Four are considered to be ‘‘Data Deficient’’ (Table 1). Discussion The high numbers of species observed in Araceae, Bromeliaceae, Orchidaceae, and Piperaceae were consonant with global patterns of epiphytic distribution among angiosperm families, as reported by Madison (1977) and Gentry & Dodson (1987). Similar results were reported for the http://dx.doi.org/10.1590/S1676-06032014001013 Neotropical region (e.g., Sudgen & Robins 1979, Gentry & Dodson 1987, Wolf & Flamenco-S 2003, Küper et al. 2004) and the tropical and subtropical Atlantic Forest (e.g., Fontoura et al. 1997, Borgo & Silva 2003, Giongo & Waechter 2004, Kersten & Silva 2001, Buzatto et al. 2008, Martins et al. 2008, Menini Neto et al. 2009, Mania & Monteiro 2010). Table 2 compares the SLNP and other Atlantic Forest areas with high epiphyte richness. The elevated numbers of species of Bromeliaceae, Araceae, and Gesneriaceae is notable, representing the highest epiphyte richness ever recorded for these families in the Atlantic Forest. Vriesea, Stelis, Anthurium, http://www.scielo.br/bn 4 Biota Neotrop., 14(2): 1– –12, 2014 Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil Table 1. Epiphytic Angiosperms registered for Serra das Lontras National Park, Bahia, Brazil. 1 *New occurence to Bahia state; ** New occurence to the Atlantic Forest; *** New occurence to Brazil. 2 AA – André M. Amorim; AF – André P. Fontana; AJ – Alessandra B. Jardim; JJ – Jomar G. Jardim; JP – José Lima da Paixão; ML – Márdel M. Lopes; PF – Pedro Fiaschi; PL – Paula Leitman; RB – Rafael X. Borges; RP – Ricardo O. Perdiz; WT – Wm. Wayt Thomas. 3 Epi – Characteristic Holoepiphyte; Fac – Facultative Holoepiphyte; Hep – Hemiepiphyte. 4 CAF – CerradoAtlantic Forest; Di – Disjunct distribution Amazon-Atlantic Forest; En – Endemic to Atlantic Forest; WD – Wide distribution; O – Other; ‘‘-’’ – not applicable. 5 CR – Criticaly endangered; DD – Data deficient; EN – Endangered; VU – Vulnerable. Family Acanthaceae Araceae Specie1 Voucher2 Habit3 Distribution4 Clistax bahiensis Profice & Leitman Anthurium boudetii Nadruz * Anthurium gladiifolium Schott Anthurium gracile (Rudge) Lindl. ** Anthurium intermedium Kunth Anthurium jilekii Schott Anthurium pentaphyllum (Aubl.) G.Don AA 5301 AA 6399 AA 5770 PL 211 PL 165 PL 547 AA 5770a ML 1473 AA 6610 PL 417 JJ 4919 PL 324 JJ 4389 JJ 4337 JJ 4886 JP 956 AA 6580 JJ 4898 ML 1449 AA 5960 JJ 4896 AA 6727 AA 6599 PL 202 PL 287 AA 5296 PL 119 PL 561 JJ 4842 PL 428 AA 5298 AA 5960a AA 6568 AA 5280 AA 5265 PL 338 AA 5275 PL 424 PL 378 PL 309 AA 6594 PL 262 PL 395 AA 7217 PL 129 ML 1484 ML 1491 PL 141 JJ 4680 JJ 5431 Hep Fac Epi Epi Fac Hep Hep En En En WD En O WD Hep Fac Epi Epi Epi Epi Epi Hep Hep Hep Hep Hep Hep Fac Hep Hep Hep Hep Hep Hep Hep Hep Hep Epi Hep WD WD WD WD En En WD WD O WD WD En En Di Di WD Di Di WD Hep Hep Hep Hep Hep Fac Fac Fac Fac Fac Fac Fac Fac Epi Epi Epi Epi Epi WD En En En O En En En En En CAF Di En En En En - Anthurium scandens (Aubl.) Engl. Anthurium solitarium Schott Anthurium sp. 1 Anthurium sp. 2 Anthurium sp. 3 Anthurium sp. 4 Anthurium sp. 5 Heteropsis oblongifolia H.B.K. Monstera adansonii Schott Philodendron cordatum Kunth Philodendron edmundoi G.M.Barroso * Philodendron fragrantissimum (Hook.) G.Don Philodendron hederaceum (Jacq.) Schott Philodendron insigne Schott Philodendron ornatum Schott Philodendron pedatum (Hook.) H.B.K. Philodendron propinquum Schott Philodendron recurvifolium Schott Philodendron rudgeanum Schott Philodendron surinamense (Miq.) Engl. Philodendron aff. williamsii Hook. f. Rhodospatha latifolia Poepp. Rhodospatha oblongata Poepp. Stenospermation spruceanum Schott Syngonium vellozianum Schott Araliaceae Begoniaceae Bromeliaceae Oreopanax capitatus (Jacq.) Decne. & Planch. Begonia convolvulacea A.DC. Begonia fruticosa (Klotzsch) A.DC. Begonia aff. itaguassuensis Brade Begonia radicans Vell. Begonia grisea A.DC. ** Aechmea burlemarxii E. Pereira Aechmea conifera L.B.Sm. * Aechmea froesii (L.B.Sm.) Leme & J.A.Siqueira Aechmea gustavoi J.A.Siqueira & Leme Aechmea multiflora L.B.Sm. Aechmea nudicaulis Griseb. Aechmea patentissima (Mart. ex Schult. & Schult. f.) Baker Aechmea subintegerrima (Philcox) Leme Aechmea tentaculifera Leme et al. Aechmea turbinocalyx Mez Aechmea viridostigma Leme & H.Luther Aechmea sp. Threat category5 CR Continued on next page http://www.scielo.br/bn http://dx.doi.org/10.1590/S1676-06032014001013 Biota Neotrop., 14(2): 1––12, 2014 5 Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil Table 1. Continued. Specie1 Voucher2 Habit3 Distribution4 Billbergia euphemiae E.Morren Billbergia saundersii Bull Canistrum camacaense Martinelli & Leme Canistrum montanum Leme Guzmania lingulata (L.) Mez Hohenbergia augusta (Vell.) E.Morren * Hohenbergia brachycephala L.B.Sm. Hohenbergia capitata Schult. & Schult.f. Hohenbergia edmundoi L.B.Sm. & Read Hohenbergia minor L.B.Sm. Hohenbergia sp. 1 Hohenbergia sp. 2 Hohenbergia sp. 3 Hohenbergia sp. 4 Hohenbergia sp. 5 Lymania azurea Leme Neoregelia azevedoi Leme Neoregelia crispata Leme Neoregelia kerryi Leme Neoregelia pauciflora L.B.Sm. Neoregelia wilsoniana M.B.Foster Nidularium innocentii Lem. Nidularium procerum Lindm. AA 5752 JP 976 AA 5751 AA 5269 RB 591 PL 149 PL 439 AA 6602 JJ 4920 PL 158 PL 398 PL 134 PL 307 PL 391 PL 305 JJ 5316 AA 6624 AA 5991 AA 5807 AA 6590 PL 267 AA 6696 WT 14093b PL 435 AA 6597 AA 5351 AA 5820 AA 6391 JJ 4895 AA 6086 PL 208 AA 5303 PL 380 JP 965 JP 975 RB 590 PL 489 AA 5797 AA 6758 AA 6646 PL 368 AA 6759 PL 301 PL 205 PL 150 PL 345 AA 6097 AA 6688 PL 289 PL 114 PL 181 PL 442 JJ 4401 PL 230 PL 200 Fac Epi Fac Epi Fac Fac Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Fac Epi Epi Fac Fac En En En En WD En En En En En En En En En En En En En Epi Epi Fac Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi En En En WD CAF CAF CAF En En En En En En En En En Di O En En En En O En En WD O En Family Cactaceae Portea filifera L.B.Sm. Portea nana Leme Quesnelia clavata Amorim & Leme Racinaea spiculosa (Griseb.) M.A.Spencer & L.B.Sm. Tillandsia geminiflora Brong. Tillandsia sprengeliana Klotzsch ex Mez Tillandsia stricta Sol. Vriesea breviscapa (E.Pereira & I.A.Penna) Leme Vriesea dictyographa Leme Vriesea drepanocarpa (Baker) Mez Vriesea duvaliana E.Morren Vriesea ensiformis (Vell.) Beer Vriesea flammea L.B.Sm. Vriesea guttata Linden & André * Vriesea longiscapa Ule Vriesea longisepala A.F.Costa Vriesea paratiensis E.Pereira Vriesea procera (Mart. ex Schult. & Schult.f.) Wittm. Vriesea regnelli Mez Vriesea rhodostachys L.B.Sm. Vriesea rodigasiana E.Morren Vriesea ruschii L.B.Sm. Vriesea simplex (Vell.) Beer Vriesea tijucana E. Pereira Vriesea vagans (L.B.Sm.) L.B.Sm. * Vriesea sp. 1 Vriesea sp. 2 Vriesea sp. 3 Vriesea sp. 4 Epiphyllum phyllanthus (L.) Haw. Lepismium cruciforme (Vell.) Miq. Rhipsalis floccosa Salm-Dyck ex Pfeiff. Threat category5 EN EN EN EN DD DD Continued on next page http://dx.doi.org/10.1590/S1676-06032014001013 http://www.scielo.br/bn 6 Biota Neotrop., 14(2): 1– –12, 2014 Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil Table 1. Continued. Family Clusiaceae Cyclanthaceae Gesneriaceae Lentibulariaceae Marcgraviaceae Melastomataceae Voucher2 Habit3 Distribution4 Threat category5 Rhipsalis hileiabaiana (N.P.Taylor & Barthlott) N. Korotkova & Barthlott Rhipsalis lindbergiana K.Schum Rhipsalis neves-armondii K.Schum Rhipsalis oblonga Loefgr. Clusia panapanari (Aubl.) Choisy Asplundia gardneri (Hook,) Harling PL 521 Epi CAF DD PL 367 PL 513 ML 1019 AA 7205 PL 213 Epi Epi Epi Hep Hep O En En O WD Asplundia maximiliani Harling Evodianthus funifer (Poit.) Lindm. Thoracocarpus bissectus (Vell.) Harling Codonanthe cordifolia Chautems Codonanthe gracilis (Mart.) Hanst. Codonanthe uleana Fritsch Columnea sanguinea (Pers.) Hanst. Nematanthus albus Chautems Nematanthus corticola Schrad. Nematanthus lanceolatus (Poir.) Chautems Utricularia jamesoniana Oliv. ** PL 506 ML 1464 PL 427 JJ 4892 PL 411 AA 7221 RB 622 JJ 4907 JP 973 AA 5276 JJ 4908 Hep Hep Hep Epi Epi Epi Epi Epi Epi Fac Epi En WD WD CAF En WD WD En En CAF O Marcgravia coriacea Vahl AA 6679 Hep WD Marcgravia polyantha Delpino Bertolonia alternifolia Baumgratz et al. JJ 4697 AJ 170 Hep Epi CAF En Bertolonia bullata Baumgratz et al. Bertolonia ovata DC. AA 5979 WT 14581 JJ 4921 WT 14112 PF 2811 FF 1447 AA 5806 PL 412 PL 361 Epi Epi En En Epi Hep En WD Hep Hep Hep Epi Epi WD O CAF En En AF 2682 Epi Di PL 251 AA 5809 PL 376 Fac Epi Epi WD WD En RP 536 JJ 4677 PL 225 JJ 5383 AF 2666 AF 2688 JJ 4385 PL 244 PL 355 JJ 4922 AA 6626 PL 354 AA 5816 Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi En En En CAF O En Di En En CAF Pleiochiton blepharodes (DC.) Reginato & Goldenberg Ficus arpazusa Casar. Moraceae Onagraceae Orchidaceae Specie1 Ficus castellviana Dugand Ficus hirsuta Schott Fuchsia regia (Vand. ex Vell.) Munz Acianthera auriculata (Lindl.) Pridgeon & M.W.Chase Acianthera capanemae (Barb.Rodr.) Pridgeon & M.W.Chase * Acianthera hygrophila (Barb.Rodr.) Pridgeon & M.W.Chase * Anathallis rubens (Lindl.) Pridgeon & M.W.Chase Anathallis sclerophylla (Lindl.) Pridgeon & M.W.Chase Baptistonia gutfreundiana (Chiron & V.P.Castro) Chiron & V.P.Castro Baptistonia truncata (Pabst) Chiron & V.P.Castro * Brachionidium restrepioides Hoehne & Pabst Bulbophyllum micropetaliforme J.E.Leite Bulbophyllum napellii Lindl. Camaridium carinatum (Barb.Rodr.) Hoehne Camaridium cf. micranthum M.A. Blanco Catasetum cf. hookeri Lindl. Catasetum purum Nees & Sinnings Cirrhaea cf. seidelii Pabst Coppensia flexuosa (Sims) Campacci Coppensia hookeri (Rolfe) F.Barros & L.Guimarães Dichaea brevicaulis Cogn. Dichaea cogniauxiana Schltr. CR VU Continued on next page http://www.scielo.br/bn http://dx.doi.org/10.1590/S1676-06032014001013 Biota Neotrop., 14(2): 1––12, 2014 7 Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil Table 1. Continued. Specie1 Voucher2 Habit3 Distribution4 Dichaea pendula (Aubl.) Cogn. Elleanthus brasiliensis (Lindl.) Rchb.f. Elleanthus crinipes Rchb.f. Elleanthus hymenophorus (Rchb.f.) Rchb.f. *** Elleanthus linifolius C.Presl Encyclia fimbriata A.C.Bastos et al. PL 353 PL 549 AF 2673 AA 4960 AA 4983 WT 14604 PL 326 AF 2659 AA 6581 PL 463 PL 432 AA 6413 ML 539 JP 971 AA 6412 AA 5810 AF 2685 JJ 4901 JJ 4904 AA 4448 PL 413 PL 191 WT 14594 AF 2675 PL 555 AF 2684 AF 2654 WT 14097 JJ 4912 ML 1023 AA 5329 JJ 4379 PL 154 JJ 4681 PL 374 PL 314 PL 316 Epi Epi Epi Epi Epi Epi WD O CAF WD WD En Fac Epi Epi Fac Epi Epi Epi Epi Fac Epi Epi Epi Epi Fac Epi Epi Epi CAF En O WD Di O WD WD WD CAF En WD CAF En Di En Epi Epi Epi Epi Epi WD O En Di CAF Epi Epi Epi Epi Epi Epi Epi Epi Epi En Di Di WD En En Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi Di WD O O En En WD En Di En CAF WD - Family Encyclia patens Hook. Encyclia unaensis Fowlie Epidendrum armeniacum Lindl. Epidendrum densiflorum Lindl. Epidendrum latilabre Lindl. * Epidendrum macrocarpum Rich. Epidendrum nocturnum Jacq. Epidendrum ochrochlorum Barb.Rodr. Epidendrum paranaense Barb.Rodr. Epidendrum ramosum Jacq. Epidendrum saximontanum Pabst Epidendrum secundum Jacq. Epidendrum sp. Gomesa recurva Barb.Rodr. Grandiphyllum pohlianum (Cogn.) Docha Neto * Heterotaxis brasiliensis (Brieger & Illg) F.Barros Houlletia brocklehurstiana Lindl. Jacquiniella globosa (Jacq.) Schltr. Koellensteinia graminea Rchb.f. Lankesterella longicollis (Cogn.) Hoehne * Lockhartia lunifera Rchb.f. Masdevallia infracta Lindl. Maxillaria bradei Schltr. ex Hoehne * Maxilaria candida Lodd. ex Lindl. * Maxillaria leucaimata Barb.Rodr. Maxillaria ochroleuca Lodd. ex Lindl. Maxilaria aff. ringens Rchb.f. Maxillaria spiritusanctensis Pabst Maxilaria aff. splendens Poepp. & Endl. Maxilaria sp. Maxillariella robusta (Barb. Rodr.) M.A.Blanco & Carnevali * Mormolyca rufescens (Lindl.) M.A.Blanco Nitidobulbon nasutum (Rchb.f.) Ojeda & Carnevali Octomeria concolor Barb.Rodr. * Octomeria crassifolia Lindl. Octomeria decumbens Cogn. Octomeria geraensis Barb.Rodr. * Octomeria grandiflora Lindl. Octomeria tricolor Rchb.f. Octomeria sp. Ornithidium rigidum (Barb.Rodr.) M.A.Blanco & Ojeda * Pabstiella bradei (Schltr.) Luer * Pabstiella ramphastorhyncha (Barb. Rodr.) L. Kollmann Pabstiella aff. trifida (Lindl.) Luer Pleurothallis ruscifolia (Jacq.) R.Br. Pleurothallis sp. JJ 4683 AA 4970 PL 464 AF 2657 PL 400 PL 265 PL 226 JJ 4665 PL 493 RP 301 PL 377 PL 360 AF 2658 PF 2821 PL 222 Threat category5 EN DD VU Continued on next page http://dx.doi.org/10.1590/S1676-06032014001013 http://www.scielo.br/bn 8 Biota Neotrop., 14(2): 1– –12, 2014 Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil Table 1. Continued. Family Specie1 Voucher2 Habit3 Distribution4 Polycycnis silvana F.Barros Polystachya estrellensis Rchb.f. Promenaea silvana F.Barros & Cath. Promenaea xanthina Lindl. Prosthechea bueraremensis (Campacci) Campacci Prosthechea calamaria (Lindl.) W.E.Higgins * Prosthechea fragans (Sw.) W.E.Higgins Prosthechea pachysepala (Klotzsch) Chiron & V.P.Castro Prosthechea pygmaea (Hook.) W.E.Higgins AA 5805 RP 294 JJ 4815 RP 330 AF 2662 AF 2674 AA 5361 RP 335 WT 14101 ML 549 AA 5355 PL 399 AF 2672 WT 14096 AF 2651 PL 494 AA 6588 PL 532 WT 14102 PL 256 AA 5746 PL 135 PL 430 PL 175 PL 359 PL 431 PL 519 JJ 4713 WT 14103 ML 1187 PL 221 RP 69 PL 310 AA 7264 AF 2665 JJ 4346 PL 100 AA 6649 WT 14541 ML 1020 JJ 4798 AA 5952 AA 5946 MJ 840 AA 6357 PL 548 PL 421 AA 6681 AA 5287 AA 5800 AA 5741 JJ 4851 AA 4962 Epi Fac Epi Epi Epi Epi Epi Epi Epi En WD En En En En WD CAF WD Fac Epi Epi Fac Epi WD Di WD WD O Epi Epi Epi Epi Epi WD WD O En Epi Epi Epi Epi Epi Epi Epi Epi Epi Epi O En Di Di En - Epi Epi Epi Fac Epi Epi Fac Fac Fac Fac En WD WD En WD O WD O Fac Epi Fac Fac Fac Fac Fac Fac Fac Fac Epi Epi Hep Hep WD WD WD WD WD En WD CAF WD WD WD En Di En Prosthechea vespa (Vell.) W.E.Higgins * Rhetinantha notylioglossa (Rchb.f.) M.A.Blanco Scaphyglottis fusiformis (Griseb.) Schultes * Scaphyglottis modesta (Rchb.f.) Schltr. Scaphyglottis reflexa Lindl. Sobralia cf. sessilis Lindl. Specklinia grobyi Batem. ex Lindl. Stelis aprica Lindl. Stelis caespitosa Lindl. ** Stelis deregularis Barb.Rodr. Stelis aff. fraterna Lindl. Stelis intermedia Poepp. & Endl. * Stelis megantha Barb.Rodr. * Stelis papaquerensis Rchb.f. * Stelis pauciflora Lindl. * Stelis ruprechtiana Rchb.f. * Stelis sp. 1 Stelis sp. 2 Stelis sp. 3 Stelis sp. 4 Piperaceae Rubiaceae Solanaceae http://www.scielo.br/bn Stelis sp. 5 Trichopilia santoslimae Brade * Xylobium colleyi (Bateman ex Lindl.) Rolfe * Xylobium variegatum (Ruiz & Pav.) Mansf. * Zygopetalum crinitum Lodd. * Zygopetalum cf. maxillare Lodd. Peperomia alata Ruiz & Pav. Peperomia corcovadensis Gardner * Peperomia elongata Kunth Peperomia emarginella (Sw.) C.DC. Peperomia hernandiifolia (Vahl) A.Dietr. Peperomia macrostachya (Vahl) A.Dietr. Peperomia magnoliifolia (Jacq.) A.Dietr. Peperomia obtusifolia (L.) A.Dietr. Peperomia pilicaulis C.DC. Peperomia pseudoestrelensis C.DC. Peperomia serpens (Sw.) Loud Peperomia tenella (Sw.) A.Dietr. Peperomia tetraphylla (G.Forst.) Hook. & Arn. Peperomia urocarpa Fisch. & C.A.Mey. Hillia parasitica Jacq. Notopleura bahiensis C.M.Taylor Schradera polycephala DC. Dyssochroma viridiflorum (Sims) Miers Threat category5 CR http://dx.doi.org/10.1590/S1676-06032014001013 Biota Neotrop., 14(2): 1––12, 2014 9 Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil Table 2. Comparison of species richness for the main families and genera with epiphytic habit between Serra das Lontras National Park and other surveys carried at the Atlantic Forest. 1 N.P. – National Park; S.P. – State Park; N.R. – Natural Reserve. ‘‘-’’ – Information not available. 1 Serra das Lontras N.P., BA Macaé de Cima, RJ Upper Iguaçu River Basin, PR Prata Moutain Range, PR Ibitipoca S.P., MG Carlos Botelho S.P., SP Ilha do Cardoso S.P., SP Vale do Rio Doce N.R., ES Taxon Present study Kersten & Kunyioshi 2006 Blum et al. 2011 Menini Neto et al. 2009 Breier et al. 2005 Breier et al. 2005 Coelho 2010 Total area Total epiphytic Angiosperms Orchidaceae Bromeliaceae Araceae Piperaceae Cactaceae Gesneriaceae Vriesea Peperomia Stelis Anthurium Philodendron Aechmea Epidendrum Hohenbergia 11,000ha 256 Fontoura et al. 1997; Costa & Wendt 2007 7,000ha 275 254 6.3ha 204 1,923.5ha 181 10.24ha 121 10.24ha 136 22.000ha - 103 62 29 15 7 7 22 15 14 13 12 11 11 9 184 45 5 5 7 6 18 5 4 10 4 10 0 147 39 9 24 12 3 11 22 6 2 7 9 4 0 103 38 14 14 9 5 18 14 7 6 6 5 12 0 66 22 9 3 7 2 7 3 5 5 4 1 6 0 42 27 13 8 11 6 12 7 1 3 8 5 4 0 72 33 11 6 1 3 15 5 1 3 7 3 8 0 22 4 12 - Study area Aechmea, and Hohenbergia also exhibited their greatest epiphytic species diversity in the SLNP. It is interesting that Hohenbergia was among the richest genera in the study area, as this genus does not commonly figure among the most species rich taxa in epiphyte surveys. The greatest diversity of this genus is encountered in southern Bahia, where 21 of its 25 Atlantic Forest species occur (Martinelli et al. 2008, Forzza et al. 2013). In addition to H. brachycephala and H. minor, both endemic to Bahia, H. edmundoi, a poorly-known species from Bahia for which no habitat information was available (Smith & Downs 1979, Forzza et al. 2013), was found in a submontane forest in the SLNP; H. augusta, previously considered to be restricted to southeastern Brazil, was also collected. These results reaffirm the importance of southern Bahia State in the distribution and taxonomy of this genus. Vriesea (Tillandsioideae) and Aechmea (Bromelioideae) represent 12% and 7%, respectively, of the total number of species in the Atlantic Forest (Forzza et al. 2013). Fontoura et al. (2012) reported that Bromelioideae taxa were encountered 1.6 times more frequently in local surveys of epiphytic species in the Atlantic Forest than representatives of Tillandsioideae. This proportion was lower in the SLNP, where Vriesea is very diverse, with almost the same numbers of species being encountered in each subfamily (34 spp. Bromelioideae x 30 spp. Tillandsioideae). Another family that demonstrated elevated richness in the SLNP was Araceae, with one third of the 65 species known to the Atlantic Forest being encountered there (Coelho et al. 2013). The most diversified genera of this family were likewise http://dx.doi.org/10.1590/S1676-06032014001013 well represented in the park, with more than half of the species of Anthurium and Philodendron known from Bahia being encountered in the SLNP. Additionally, two new occurrence records for Bahia State (A. boudetii and P. edmundoi), one for the Atlantic Forest domain (A. gracile), and five morphotypes of Anthurium reinforce the importance of additional studies in mountainous areas there to improve our knowledge of the distribution of this family within the state. In contrast to the high endemism levels of Bromeliaceae and Orchidaceae, representatives of Araceae exhibit wide (and sometimes disjunct) distributions (Coelho et al. 2013). Orchidaceae is responsible for approximately 70% of the global epiphytic flora, and is always among the top families in every floristic study of that habit (Benzing 1990, Kersten 2010, Zotz 2013). Most orchid diversity is found in the tropics, especially in mountainous areas (Dressler 1993). The majority of the orchid taxa encountered in the SLNP is relatively small (e.g., Acianthera, Anathallis, Brachionidium, Jacquiniella, Lankesterella, Octomeria, Pabstiella, Pleurothallis, Promenaea, Specklinia, and Stelis) and commonly neglected in floristic surveys – and therefore poorly represented in scientific collections (Dressler 2005). As the present study focused on epiphytes (and ex-situ cultivation was undertaken), high numbers of species were included on the final list – with 22 new occurrences for Bahia State (Table 1). Northeastern Brazil represents one of the 10 areas in the world considered most likely to have undescribed species, and where models predict a 30% increase in known diversity (Joppa et al. 2011). Since initiating preliminary studies of the flora of the SLNP (Amorim et al. 2009), six new epiphyte species have http://www.scielo.br/bn 10 Biota Neotrop., 14(2): 1– –12, 2014 Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil been described for the area: Bertolonia alternifolia, B. bullata, Clistax bahiensis, Encyclia fimbriata, Quesnelia clavata, and Vriesea longisepala, and one is about to be published. The present survey found other possible taxonomic novelties, and recent studies in neighboring areas encountered several new species with epiphytic habits (e.g., Amorim & Leme 2009, Leme & Kollmann 2011, Costa et al. 2012, Reginato et al. 2013) – emphasizing the need of further investigations of this group in southern Bahia. The present study expands the distribution of many taxa, with one new occurrence for Brazil (Elleanthus hymenophorus (Rchb.f.) Rchb.f.), four for the Atlantic Forest biome, and 30 for Bahia State (Table 1). Utricularia jamsoniana Oliv., a species previously known only from altitudinal regions of Central America and northern South America (Taylor 1989), was encountered in a cloud forest in the highest area of the park (Peito de Moça and Javi mountain ranges). Over half (16 spp.) of these new records were known only from collections in strictly southern and southeastern regions. The epiphytic flora of the SLNP shares more species with southern and southeastern Brazil (71 spp.) than with northeastern states (five species – four Aechmea and one Hohenbergia). This same pattern was found for ferns and lycophytes on a nearby mountainous area in the Serra Bonita Private Reserve, with almost a quarter of the surveyed species being previously restricted to southeastern Brazil (Matos et al. 2010). Almost half of the 221 taxa identified to species level in the present study are endemic to the Atlantic Forest (100 spp. - 45%) (Table 1), and most of them belong to Bromeliaceae and Orchidaceae (44 and 32 species respectively). These two families exhibit high degrees of endemism in the Atlantic Forest, with 80% of Bromeliaceae and 63% of Orchidaceae being restricted to this domain (Martinelli et al. 2008, Stehmann et al. 2009). These high levels of endemism may be related to limited connections with the other major South American forest formation in the Amazon (Mori et al. 1981). These two forests are separated by an open area known as the ‘‘dry diagonal’’ (Prado & Gibbs 1993) that acts as a barrier to species dispersion, especially less droughttolerant taxa. On the other hand, 60 species showed broad distributions in Brazil or the Neotropical region, and 24 had disjunct distributions between the Atlantic and Amazon forests (Table 1); 19 species also occur in the ‘‘Cerrado’’ (Brazilian savanna) region, suggesting that dry formations do not act as barriers to all epiphyte taxa, especially those with broader ecophysiological tolerances (Oliveira-Filho & Ratter 1995, Ibisch et al. 1996). Deciduous and semi-deciduous seasonal forest patches and gallery forests that crisscross the Cerrado may offer dispersal pathways for many species and establish tenuous connections between these two major forest formations (Leitão Filho 1987, Oliveira-Filho & Ratter 1995). All of the 10 species cited on the Red Book of Brazilian Flora (Martinelli & Moraes 2013) as threatened belong to Bromeliaceae and Orchidaceae, two very ornamental families. The five bromeliads are restricted to Northeast Brazil, and four of them are endemic to Bahia. On the other hand, the orchids indicated as threatened are new occurrences to the state. These results reinforce the importance of the park as a conservation unit and the relevance of floristic surveys, especially for often neglected groups such as epiphytes. Recent floristic studies in mountainous areas in southern Bahia have revealed large http://www.scielo.br/bn numbers of new species and new occurrences of epiphytes – pointing to the need for further investigations of this group. Acknowledgments We thank FAPESB, FAPERJ and CAPES for fieldwork financial support. Paula Leitman thank CNPq and CAPES for master’s scholarship. Rafaela C. Forzza and André Amorim are CNPq research fellows. We also thank the specialists who helped identifying the species - Alain Chautems, Andrea Costa, Charlotte Taylor, Claudio Nicoletti Fraga, Daniela Zappi, Daniele Monteiro, Eliane de Lima Jacques, Elton Leme, Elsie Franklin Guimarães, João Renato Stehmann, Ludovic Kollmann, Marcus Nadruz, Nigel Taylor, Ricardo Perdiz, Sheila Profice & Simon Mayo – and fieldwork helpers – José Lima Paixão, Carlinhos, Lukas Daneu and Ricardo Perdiz. References AMORIM, A.M.A. & LEME, E.M.C. 2009. Two new species of Quesnelia (Bromeliaceae: Bromelioideae) from the Atlantic Rainforest of Bahia, Brazil. Brittonia 61(1): 14-21. doi: http:// dx.doi.org/10.1007/s12228-008-9049-5 AMORIM, A.M.A., JARDIM, J.G., LOPES, M.M.M., FIASCHI, P., BORGES, R.A.X., PERDIZ, R.O. & THOMAS, W.W. 2009. Angiospermas em remanescentes de Floresta Montana no sul da Bahia, Brasil. 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Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil

Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil

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