Floristic patterns of epiphytes in the Brazilian Atlantic Forest, a biodiversity hotspot

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1 bs_bs_banner Botanical Journal of the Linnean Society, 2015, 179, With figures Floristic patterns of epiphytes in the Brazilian Atlantic Forest, a biodiversity hotspot PAULA LEITMAN 1 *, ANDRÉ M. AMORIM 2,3, JERÔNIMO B. B. SANSEVERO 1,4 and RAFAELA C. FORZZA 1 1 Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão 915, Jardim Botânico, Rio de Janeiro, RJ , Brazil 2 Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Salobrinho, Ilhéus, BA , Brazil 3 Centro de Pesquisas do Cacau Herbário CEPEC, Caixa Postal 07, Itabuna, Bahia , Brazil 4 Departamento de Ciências Ambientais, Instituto de Florestas, Universidade Federal Rural do Rio de Janeiro, BR 465, Km 07, Seropédica, RJ , Brazil Received 20 January 2015; revised 6 August 2015; accepted for publication 24 August 2015 To assess the main factors driving epiphytic angiosperm distribution throughout the Brazilian Atlantic Forest, we compiled 57 floristic surveys and analysed species composition under the influence of environmental variables, space and vegetation type using canonical correspondence analysis (CCA), similarity (Sorensen) and Mantel s tests. The indicator value index (IndVal) was used to find indicator species of each Brazilian Atlantic Forest vegetation type. Group sharpness analysis was performed in order to determine the appropriate group partition level. CCA showed a separation of the epiphytic flora reflecting temperature and rainfall gradients. Mantel s test showed that environment and space were highly correlated with floristic similarity. Cluster analysis, indicating floristic similarity, resolved five groups, mainly grouped by region. Clear differentiation of the Brazilian Atlantic Forest epiphytic flora on a north south axis with a strong correlation with temperature and rainfall gradients was found. The role of space and environment on species composition varied according to distinct epiphytic species groups. In particular, for Bromeliaceae and Orchidaceae, the main factor associated with floristic similarity was space. Indicator species were found for all vegetation types apart from the Seasonal Semideciduous Forest that seemed to represent a subset of a more humid forest type The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179, ADDITIONAL KEYWORDS: environmental variables epiphytic species floristic similarity Mantel test spatial and climatic predictors. INTRODUCTION The study of variation in species distribution and diversity along elevational and latitudinal gradients is one of the main goals of biogeography. Environmental components vary across these gradients with direct effects on the distribution of organisms (Lomolino, 2001). Gentry & Dodson (1987) suggested a mid-elevation bulge on epiphyte diversity between 500 and 1000 m, where cloud concentration ensures *Corresponding author. paulaleitman@gmail.com frequent high levels of air humidity (Sudgen & Robins, 1979; Benzing, 1990). The study of Küper et al. (2004) on epiphyte diversity patterns in the Andes supported the hypothesis described above. This survey found a significant floristic dissimilarity between study areas (70%) and revealed that the composition was more influenced by elevation than by geographical proximity. Similar results were found by Menini Neto, Forzza & Zappi (2009) for areas of the Atlantic Forest of southern and south-eastern Brazil, where groups were formed according to region and elevational range. Gentry & 587

2 588 P. LEITMAN ET AL. Dodson (1987) also suggested that low temperatures are a limiting factor for epiphyte establishment at high elevations, whereas high temperatures that raise evapotranspiration levels reduce their occupation of lowlands. Fontoura, Scudeller & Costa (2012), in a study of epiphytic bromeliad distribution in the Atlantic Forest, found that latitude, minimum and mean annual temperatures and distance from the ocean were the main factors driving the dispersal of taxa. With c species of epiphytes, c. 20% of the total of the vascular plant flora, the Brazilian Atlantic Forest is a centre of epiphyte diversity in the Neotropics (Nieder, Prosperí & Michaloud, 2001; Stehmann et al., 2009; Kersten, 2010). This forest formation is located in the eastern part of the South American continent, through a wide latitudinal (from 3 S to 30 S) and elevational (from sea level up to > 2800 m) range, with significant rainfall differences, comprising a vast heterogeneity of habitats and, consequently, high biodiversity (Oliveira-Filho & Fontes, 2000). Now covering only 11% of its original area (Ribeiro et al., 2009), this biome, considered to be one of 34 world biodiversity hotspots (Mittermeier et al., 2004), includes several vegetation types, partly resulting from environmental gradients (Oliveira-Filho et al., 2005). Studies of floristic relationships between the Brazilian Atlantic Forest vegetation types have been mainly based on woody species, as a result of the greater number of floristic inventories on this functional group (Oliveira-Filho et al., 2005). Taking into account the contribution of epiphytes to the high species richness level of the Brazilian Atlantic Forest and to understand better the factors that drive species distribution, this study aims to answer the following questions. What role do environmental variables and space play in epiphytic composition throughout the Brazilian Atlantic Forest? Are there epiphytic indicator species for each of the Brazilian Atlantic Forest vegetation types? How are areas across the Brazilian Atlantic Forest grouped on the basis of their epiphytic composition? Considering suggestions from previous studies on the Andes and the Brazilian Atlantic Forest (Gentry & Dodson, 1987; Menini Neto et al., 2009; Fontoura et al., 2012), we expect to find a differentiation of the floras between southern, south-eastern and northeastern Brazil, and that temperature and rainfall influence epiphyte distribution across the biome. MATERIAL AND METHODS STUDY AREA A list of species of the epiphytic angiosperms of the Atlantic Forest was compiled from published work (Menini Neto et al., 2009), databases (Rede em epífitas da Mata Atlântica, CAPES/PNADB; L. Freitas, pers. comm.) and fieldwork. Fifty-seven areas were selected (Table 1), encompassing five Atlantic Forest vegetation types: Dense Evergreen Forest (DEF) (17), Seasonal Semideciduous Forest (SSF) (22), Mixed Evergreen Forest (MEF) (7), Restinga (RES) (7) and Brejos de Altitude (BA) (4) distributed across a latitudinal range from 7 6 to (Fig. 1). The Atlantic Forest limits follow IBGE (2004) and the Atlantic Forest law (n ). According to Rizzini (1997) and IBGE (2012), these five forest types can be characterized as follows. DEF is coastal rain forest, with high temperatures (annual mean, 25 C) and high rainfall, distributed evenly throughout the year. RES is located in the narrow strip between the coastline and DEF, and suffers strong marine influence, high levels of insolation and temperatures, and relatively low water availability as a result of percolation; it can be divided into scrub found closer to the sea and on sand-dunes, and forest formations inland on the coastal plain (for this work, only the latter was studied). SSF is a forest formation found inland that undergoes long periods of drought during the winter (4 6 months) and intense summer rainfall within its tropical zone, and low temperatures during the winter (annual mean, < 15 C) in its subtropical zone. MEF occurs in the southernmost part of the biome and is marked by lower temperatures throughout the year (annual mean, 18 C) and evenly distributed rainfall. BA is mountain forest in the caatinga domain, occurring on the high plateaus or chapadas of north-eastern Brazil, with precipitation levels of > 1200 mm per year resulting from orographic rainfall, allowing the establishment of humid forest vegetation in the semi-arid region. FLORISTIC COMPOSITION AND ENVIRONMENTAL AND SPATIAL VARIABLES Taxa were updated according to the List of Species of the Brazilian Flora (2013). Only characteristic and facultative holoepiphytes and primary and secondary hemiepiphytes (according to Benzing, 1990) were used in the analyses, thus excluding accidental epiphytes. One thousand and sixty-eight species were registered, representing 180 genera and 22 families. For similarity analysis, singletons were excluded in order to reduce data noise (Santos et al., 2012). The species composition matrix (F) included 682 species from the 57 sites. For each study area, environmental variables were obtained (WorldClim 1.4) (Hijmans et al., 2005), with a 30-arc-s resolution, in addition to distance from the coast and geographical coordinates. From a larger set of environmental variables, correlation tests and collinearity diagnostics were performed in order to select the most significant variables and remove

3 EPIPHYTE PATTERNS IN THE ATLANTIC FOREST 589 Table 1. Atlantic Forest areas used for canonical correspondence analysis (CCA), floristic similarity, indicator value index (IndVal) and Mantel s test Area Area number Reference Latitude Longitude Vegetation Types Area size (ha) Itapuã SP 1 Musskopf (2006) Isolated fig trees on coastal plain of 2 Gonçalves & Waechter (2003) Rio Grande do Sul Estreito Augusto César 3 Rogalski & Zanin (2003) Experimental Agronomic Station 4 Giongo & Waechter (2004) Passo Fundo NF 5 Buzatto, Severo & Waechter (2008) Curitiba fragments 6 Borgo & Silva (2003) Ingá Park 7 Dettke, Orfrini & Milaneze-Gutierre (2008) Tibagi River 8 Bonnet et al. (2011) Tibagi River 9 Bonnet et al. (2011) Tibagi River 10 Bonnet et al. (2011) Ilha do Mel 11 Kersten & Silva (2001) Serra da Prata 12 Blum, Roderjan & Galvão (2011) Iguaçú River Basin 13 Kersten & Kuniyoshi (2009) São Jerônimo River 14 Kersten, Kuniyoshi & Roderjan (2009) Campo Mourão 15 Geraldino, Caxambú & Souza (2010) Cerrado de Jaguariaíva SP 16 Linsingen et al. (2006) Intervales SP, Saibadela Base 17 Ziparro et al. (2005) Cidade Universitária Armando Salles 18 Dislich & Mantovani (1998)/Groppo & de Oliveira Reserve Pirani (2005) Juréia-Itatins ES 19 Mamede et al. (2004) Bertioga 20 Martins et al. (2008) Mata da Pavuna 21 Biral & Lombardi (2012) Serra do Japi MBR 22 Lombardi et al. (2012) Fontes do Ipiranga SP 23 Laurenti-Santos (2008) Serra do Mar SP, Núcleo Curucutu 24 Garcia & Pirani (2005) Caetetus ER 25 Breier (2005) Carlos Botelho SP 26 Breier (2005) Ilha do Cardoso SP 27 Breier (2005) Mata do Baú 28 Menini Neto et al. (2009) Represa do Grama BR 29 Menini Neto et al. (2009) Ibitipoca SP 30 Menini Neto et al. (2009) RES 5566 RES SSF SSF MEF MEF 97 SSF 47.3 SSF SSF MEF RES 2760 DEF 6.30 MEF MEF MEF 30 SSF SSF SSF DEF RES SSF SSF SSF 357 DEF 2800 SSF DEF RES SSF 10 SSF DEF

4 590 P. LEITMAN ET AL. Table 1. Continued Area Area number Reference Latitude Longitude Vegetation Types Area size (ha) Serra do Brigadeiro SP 31 Leoni & Tinte (2004) Serra de São José 32 Alves & Kolbek (2009) Serra Negra 33 Salimena et al. (2013) Itatiaia NP 34 JABOT (2012) Serra dos Órgãos NP 35 JABOT (2012) Serra da Tiririca SP 36 Barros (2008) Jacarepiá SER 37 Fontoura et al. (2009) COMPERJ 38 Bonnet et al. (2012) Macaé de Cima 39 JABOT (2012)/Fontoura et al. (1997)/Costa & Wendt (2007) Paulo César Vinha SP 40 Assis, Thomaz & Pereira (2004) Santa Lúcia BS 41 Splink (2012) Vale do Rio Doce NR 42 Splink (2012) Serra das Lontras NP 43 Leitman et al. (2013) Serra Bonita PR 44 Amorim et al. (2009) updated Serra da Pedra Lascada 45 Amorim et al. (2009) updated Serra do Corcovado 46 Coelho (2013) Serra do Teimoso 47 Amorim et al. (2005) Una BR 48 Amorim et al. (2008) Serra da Fazenda Retiro 49 Cardoso et al. (2009) Serra da Itabaiana NP 50 Mendes, Gomes & Alves (2010) Tapacurá ES 51 Rodal et al. (2005) Serra Negra BR 52 Rodal & Nascimento (2002) Pico do Jabre 53 Agra, Barbosa & Stevens (2004) Serra do Bituri 54 Nascimento, Rodal & Silva (2012) Usina São José 55 Melo et al. (2011) São Vicente Férrer 56 Ferraz & Rodal (2008) Mata do Buraquinho 57 Barbosa (2008) SSF SSF 3000 DEF DEF DEF DEF 1800 RES 1250 DEF 0.2 DEF 7200 RES 4 DEF 440 DEF DEF DEF 7500 DEF 300 DEF 2500 SSF 500 DEF 9000 SSF 13 SSF 3421 SSF 81 BA 1100 BA BA SSF BA 600 DEF 471 Vegetation types and conservation units are represented by the following acronyms: BA, Brejos de Altitude; BR, Biological Reserve; BS, Biological Station; DEF, Dense Evergreen Forest; ER, Ecological Reserve; ES, Ecological Station; MBR, Municipal Biological Reserve; MEF, Mixed Evergreen Forest; NF, National Forest; NP, National Park; NR, Natural Reserve; PR, Private Reserve; RES, Restinga; SER, State Ecological Reserve; SP, State Park; SSF, Seasonal Semideciduous Forest., no information available.

5 EPIPHYTE PATTERNS IN THE ATLANTIC FOREST 591 Figure 1. Map showing the location of 57 areas of Brazilian Atlantic Forest used in canonical correspondence analysis (CCA), floristic similarity, indicator value index (IndVal) and Mantel s tests. The vegetation types are represented by the following symbols:, Brejos de Altitude;, Dense Evergreen Forest;, Mixed Evergreen Forest; +, Seasonal Semideciduous Forest;, Restinga. The arrow indicates the location of Conde s fault. redundancy (Legendre & Legendre, 1998). A resulting environmental matrix (E) included the variables elevation, evapotranspiration, mean annual temperature, variation in annual temperature, distance from the coast, annual rainfall and rainfall in the driest quarter. The space matrix (S) was calculated on the basis of geographical coordinates of the 57 study sites. The inclusion of distance between areas as a component aims to verify the contribution of space to floristic similarity.

6 592 P. LEITMAN ET AL. DATA ANALYSIS A canonical correspondence analysis (CCA) was carried out in order to analyse floristic patterns related to environmental variables and space. This test was performed with species composition (F), environment (E) and space (S) matrices (Supporting Information Table S1) using the Vegan package (Oksanen et al., 2010) in R environment (R Development Core Team, 2010). First, the floristic matrix (species occurrence/site) (T) was used to calculate similarity with Sorensen s distance. For E and S matrices, Gower s distance was used (Legendre & Legendre, 1998). The influence of E and S variables on floristic similarity (F) was tested with simple and partial Mantel s (ρ) correlations (Legendre & Legendre, 1998). This aimed to verify the correlation between environment and floristic similarity, removing the effect of space, and vice versa. This was performed for the whole floristic matrix and for the four richest families of epiphytes: Araceae, Bromeliaceae, Orchidaceae and Piperaceae. Tests of statistical significance for simple and partial Mantel s correlations were based on permutations under appropriate null models (e.g. Pillar & Duarte, 2010). This was calculated using the software MULTIV (V. Pillar, v 2.3; available at ecoqua.ecologia.ufrgs.br/multiv.html). The indicator value index (IndVal), proposed by Dufrêne & Legendre (1997), was calculated in order to investigate the existence of epiphytic indicator species for each forest type. For this, vegetation types were used as a habitat category (Table 1). This analysis was performed using the indspc package in the R environment (available at labdsv/r/labdsv). As suggested by Dufrêne & Legendre (1997), only occurrence values > 0.25 were considered. As this analysis requires a minimum of four areas of each habitat (Dufrêne & Legendre, 1997), the Estreito Augusto César (3) (Table 1), composed of deciduous seasonal forest, was treated as semideciduous seasonal forest. Floristic similarity between sites was calculated using Sorensen s distance and relationships between sites were obtained using UPGMA (unweighted pairgroup method with arithmetic mean). A group sharpness analysis was performed in order to determine the appropriate group partition level (Pillar, 1999). This procedure was based on permutations under appropriate null models using the software MULTIV (V. Pillar, v 2.3; available at: RESULTS The first axis of the CCA was correlated with latitude, longitude, mean annual temperature, variation in annual temperature and distance from the coast (Fig. 2). Mean annual precipitation, precipitation during the driest quarter and evapotranspiration were related to the second axis (Fig. 2). The first two axes explained 43% of the total variation. The northeastern DEF and SSF were positioned on the right side of the biplot, whereas areas of MEF were placed on the left, reflecting a temperature gradient (Fig. 2). South-eastern and some southern DEF and SSF appeared in the top part of the biplot, related to high levels of annual precipitation and evapotranspiration. BA emerged in two separate groups according to distance from the coast, with an area closer to the coastal lowland (56) and a group composed of three further inland areas (52 54) (Fig. 2). Areas of SSF and RES appeared dispersed on the biplot, not forming clear groupings (Fig. 2). Apart from MEF, the vegetation types did not exhibit a clear pattern in relation to the environmental gradients. Mantel s simple correlation analysis showed that environment and space were highly correlated with the floristic similarity of the area (0.53, P < 0.01) (Table 2). This pattern was also observed for the four families richer in epiphytic species (Araceae, Bromeliaceae, Orchidaceae and Piperaceae) (Table 2). However, partial Mantel test indicated that environment and space had a different effect on each family (Table 2). For the total epiphytic assembly, floristic similarity was more strongly correlated with space (0.33) than with environment (0.20) (Table 2). Bromeliaceae showed no relation between floristic distribution and environment once the effect of space was removed, whilst otherwise displaying a significant correlation with space (Table 2). A similar pattern was also observed for Orchidaceae (Table 2). For Piperaceae, the results revealed a greater correlation with environmental variables in comparison with space (Table 2). IndVal analysis yielded 38 indicator epiphytic species for the Atlantic Forest vegetation types (Table 3). Most species were indicators of MEF (22 species), followed by RES (seven), DEF (six) and BA (two) (Table 3). SSF had no indicator species. Most indicator species belonged to Bromeliaceae and Orchidaceae. Group sharpness analysis resulted in five groups (Fig. 3). The first is composed of north-eastern SSF (51), DEF (57) and BA closer to coastal lowland areas (56) (Fig. 3). The second group is composed of areas in north-eastern Brazil, predominantly of SSF. The third group combines areas of MEF and DEF in southern Brazil and the three most inland BA sites (52 54). The fourth group is composed of areas from southeastern Brazil with RES, DEF, SSF and areas of southern Bahia. The last group has a single area of DEF (Núcleo Curucutu; 57).

7 EPIPHYTE PATTERNS IN THE ATLANTIC FOREST 593 Figure 2. Diagram obtained by canonical correspondence analysis showing the ordination on the first two axes of 57 areas of Brazilian Atlantic Forest based on occurrence records of epiphytic angiosperms. The vegetation types are represented by the following symbols:, Brejos de Altitude;, Dense Evergreen Forest;, Mixed Evergreen Forest; +, Seasonal Semideciduous Forest;, Restinga. Spatial and environmental variables: Alt, altitude; Dist_coast, distance from the coast; Evap, evapotranspiration; Lat, latitude; Long, longitude; Prec, precipitation; Prec_dq, precipitation during the driest quarter; Temp, mean annual temperature; Var_Temp, variation in annual temperature. Table 2. Mantel s test based on occurrence records for epiphytic angiosperms of 57 Atlantic Forest areas, using all species and only the richest families ρ(f.e + S) ρ(f.es) ρ(f.se) All species 0.53** 0.20** 0.33** Araceae 0.36** 0.16** 0.18** Bromeliaceae 0.33** ** Orchidaceae 0.40** 0.15* 0.24** Piperaceae 0.40** 0.24** 0.13 F - species composition; E environment; S space. ρ(f.es) controlling for spatial effects; ρ(f.se) controlling for environmental effects. *P < 0.05, **P < DISCUSSION The Brazilian Atlantic Forest occurs across a wide latitudinal range with significant environmental variation (Oliveira-Filho & Fontes, 2000). Habitat heterogeneity has been suggested as one of the main factors associated with the elevated species richness and high levels of species endemism and rarity found in this biome (Scarano, 2009; Caiafa & Martins, 2010; Bergamin, Müller & Mello, 2012). The large proportion of epiphytic angiosperms registered in a single area (36% of the total species) corroborates this. Studies on tree communities have indicated that their composition is strongly influenced by environmental factors, demonstrating a clear pattern separating the Atlantic Forest vegetation types (e.g. DEF and SSF) (Oliveira-Filho & Fontes, 2000; Oliveira- Filho et al., 2005, 2013; Nettesheim et al., 2010). For epiphytes, however, these separations were not

8 594 P. LEITMAN ET AL. Table 3. IndVal analysis of the four vegetation types of the Atlantic Forest based on occurrence records of epiphytic angiosperms for 57 Atlantic Forest areas Family Species Vegetation types IndVal P Bromeliaceae Tillandsia juncea (Ruiz & Pav.) Poiret BA Orchidaceae Cattleya labiata Lindl. BA Araceae Philodendron propinquum Schott DEF Orchidaceae Dichaea cogniauxiana Schltr. DEF Begoniaceae Begonia fruticosa (Klotzsch) A.DC. DEF Rubiaceae Hillia parasitica Jacq. DEF Araceae Syngonium vellozianum Schott DEF Orchidaceae Epidendrum paranaense Barb.Rodr. DEF Orchidaceae Campylocentrum grisebachii Cogn. MEF Bromeliaceae Billbergia nutans H.H.Wendl. ex Regel MEF Cactaceae Lepismium lumbricoides (Lem.) Barthlott MEF Orchidaceae Capanemia superflua (Rchb.f.) Garay MEF Orchidaceae Acianthera hatschbachii (Schltr.) Chiron & van den Berg MEF Orchidaceae Leptotes unicolor Barb.Rodr. MEF Orchidaceae Acianthera hygrophila (Barb.Rodr.) Pridgeon & M.W.Chase MEF Piperaceae Peperomia catharinae Miq. MEF Piperaceae Peperomia trineura Miq. MEF Gesneriaceae Sinningia douglasii (Lindl.) Chautems MEF Bromeliaceae Aechmea distichantha Lem. MEF Bromeliaceae Aechmea recurvata (Klotzsch) L.B.Sm. MEF Bromeliaceae Vriesea platynema Gaudich. MEF Orchidaceae Acianthera sonderiana (Rchb.f.) Pridgeon & M.W.Chase MEF Cactaceae Rhipsalis floccosa Salm-Dyck ex Pfeiff. MEF Cactaceae Rhipsalis camposportoana Loefgr. MEF Orchidaceae Capanemia australis (Kraenzl.) Schltr. MEF Bromeliaceae Vriesea reitzii Leme & A.F.Costa MEF Cactaceae Lepismium warmingianum (K.Schum.) Barthlott MEF Orchidaceae Anathallis paranaensis (Schltr.) Pridgeon & M.W.Chase MEF Orchidaceae Anathallis dryadum (Schltr.) F.Barros MEF Orchidaceae Brasiliorchis picta (Hook.) R.B.Singer et al. MEF Piperaceae Peperomia tetraphylla (G.Forst.) Hook. & Arn. MEF Bromeliaceae Vriesea procera (Mart. ex Schult. & Schult.f.) Wittm. RES Urticaceae Coussapoa microcarpa (Schott) Rizzini RES Orchidaceae Brassavola tuberculata Hook. RES Orchidaceae Epidendrum latilabre Lindl. RES Bromeliaceae Vriesea gigantea Gaudich. RES Bromeliaceae Vriesea rodigasiana E.Morren RES Gesneriaceae Codonanthe gracilis (Mart.) Hanst. RES Vegetation types are represented by the following acronyms: BA, Brejos de Altitude; DEF, Dense Evergreen Forest; MEF, Mixed Evergreen Forest; RES, Restinga. Figure 3. Similarity tree (Sorensen s coefficient) obtained by the analysis of epiphytic species (except singletons) of 57 areas of Brazilian Atlantic Forest. The vegetation types are represented by the following symbols:, Brejos de Altitude;, Dense Evergreen Forest;, Mixed Evergreen Forest;, Seasonal Semideciduous Forest;, Restinga. Dotted line indicates group partitioning. clear. The absence of a floristic pattern could have resulted from the combination of environmental and space effects on the similarity of epiphytic species composition. SSF areas emerged scattered throughout both CCA and similarity analyses, revealing a greater proximity with geographically closer areas. IndVal revealed no indicator species for SSF, showing that, for epiphytes, this vegetation type

9 EPIPHYTE PATTERNS IN THE ATLANTIC FOREST 595 Figure 3. See caption on previous page.

10 596 P. LEITMAN ET AL. appears to be a subset of more humid and diverse forests. This result was also found by Forzza et al. (2014), in a comparison between epiphytes from some areas of Atlantic Forest, in which 24 of the 41 registered species were shared between SSF and DEF. Concerning the woody component, SSF is also composed of DEF species more adapted to seasonality (Oliveira-Filho & Fontes, 2000). It seems apparent that, during a warmer and moister past, the expansion of the forest allowed epiphytes to extend their range. Similarity between areas tends to be inversely proportional to the distance between them. This involves environmental differentiation and species dispersal capacity (Nekola & White, 1999). However, considering the high environmental heterogeneity of the Brazilian Atlantic Forest, areas that are geographically closer may exhibit contrasting environmental conditions (see Scarano, 2002). Thus, the understanding of the effects of space and environment on epiphytic species composition is an important step towards understanding the driving factors of their biogeography. For Bromeliaceae, areas that are geographically closer share more species, differing vegetation types and environmental conditions (Table 2). Furthermore, it appears that dispersal limits can be a determining factor for the distribution of this group in the Brazilian Atlantic Forest, where closer areas show higher similarity, even when under environmental conditions showing discrepancy. This may be related to the capacity of the family to adapt to different habitats, exemplified by the ability to occupy different forest layers, where the same species can be found epiphytically, terricolously and rupicolously (Benzing, 1990; Forzza et al., 2014). Meanwhile, for Piperaceae, floristic composition shows a stronger relation to environmental conditions. Hence, the effects of space and environment on species assembly show differing patterns, indicating that particular plant groups respond in different ways to these factors. The areas in southern Bahia are grouped with the montane areas of south-eastern Brazil. This sharing of species has been observed for other high-elevation areas of southern Bahia in surveys of angiosperm, fern and lycophyte diversity (e.g. Amorim et al., 2009; Matos, Amorim & Labiak, 2010). This floristic similarity was also found by L. Menini Neto (pers. comm.), who suggested that this separation from other northeastern areas seems to be related to a discontinuity of DEF, which is replaced by SSF in the state of Bahia, near the city of Conde. The interruption of the more humid vegetation was recognized by that researcher as the Conde fault (Fig. 1). Similarities among sites based on data for frogs (Bertoluci et al., 2007) and harvestmen (Pinto da Rocha & Silva, 2005) reflect differences inherent to distinct geomorphological formations. For epiphytes, this was also found to be true, with areas of the same mountain range appearing together, or at least in the same cluster (e.g. southern Bahia range, Serra do Mar, Serra da Borborema). The sites located north of the Conde fault formed distinct groups (1, 2 and part of 5), with low similarity levels among them. The BA areas were separated into two groups: hinterland sites, west of the Borborema plateau (52 54), and the area closer to the coast (56). The latter emerged grouped with areas of coastal lowlands (51 and 57), a pattern that was also found by Rodal (2002) and Ferraz et al. (2004) for the tree and shrub components. This division reflects diminishing rainfall levels towards the semi-arid caatinga and a history of connections with different forest formations (e.g. Amazon) (Santos et al., 2007). The group formed by was placed together with areas of southern Brazil. This relation, however, presented low similarity and these areas are composed of species with broad Atlantic Forest distributions. The Núcleo Curucutu (NC) appeared separated from other sites because it shares species with the two main groups (4 and 5). This was also found by Abreu, Menini Neto & Konno (2011) on a study of Orchidaceae from caatinga, cerrado, Atlantic Forest and southern Brazilian campos (grasslands), where NC was positioned as a sister group to all Atlantic Forest areas. The NC protected area comprises a wide elevational range of DEF and therefore it appears to bring together the flora from both regions, where southern species dwell in the higher parts of the park. Increasing latitudinal range within the comparisons seems to diminish the influence of elevation over the general distribution pattern of epiphytes. Fontoura et al. (2012) also found a low contribution of elevation to epiphytic Bromeliaceae, suggesting that this may be stronger at regional scales. As pointed out by Oliveira-Filho & Fontes (2000), the influence of elevation over climate (e.g. increase in solar radiation, acceleration of air masses, promotion of cloud concentration) is far more complex than a simple gradient. The vegetation type with the largest number of indicator species was MEF, which also exhibits the highest levels of IndVal. This highlights the existence of an epiphytic flora better adapted to low temperatures. Our results match the findings of Oliveira-Filho et al. (2013) for trees, where MEF includes large numbers of non-endemic species, which probably dwell at higher elevations in areas located in lower latitudes. As found for DEF, southern areas of SSF are closely related to MEF in their epiphytic components, as was also found for the arboreal component (Oliveira-Filho et al., 2013). Most species identified as indicators of BA (Table 3) are shared with biomes other than Atlantic Forest, such as caatinga and cerrado, indicating floristic elements adapted to drier environments. All indicator

11 EPIPHYTE PATTERNS IN THE ATLANTIC FOREST 597 species of BA belong to Bromeliaceae and Orchidaceae, families with several physiological adaptations that enable them to cope with water shortage (Benzing, 1990). RES areas were dispersed throughout the CCA, placed near geographically close areas. RES and the south-eastern DEF have a distinct arboreal composition, as a direct consequence of edaphic differences between these two environments (Assis et al., 2011). As soil composition is not a determining factor for epiphyte establishment and persistence, the pattern described above is not applicable to this group. Despite the fact that RES has indicator species with certain fidelity to this vegetation type, many can be commonly found in DEF forest areas [e.g. Aechmea nudicaulis Griseb., Codonanthe gracilis (Mart.) Hanst., Peperomia glabella (Sw.) A.Dietr., Vriesea procera (Mart. ex Schult. & Schult.f.) Wittm. and V. rodigasiana E.Morren]. The data corroborate the results of Araújo (2000) for RES of Rio de Janeiro, where 60% of the flora are shared with DEF. The results make evident a north south distinction of the epiphytic flora, influenced by temperature in its latitudinal distribution and by rainfall in its longitudinal distribution, as pointed out by previous studies on arboreal strata (Leitão Filho, 1987; Oliveira-Filho & Ratter, 1995; Oliveira-Filho & Fontes, 2000; Oliveira-Filho et al., 2005). Similarity patterns found in the present work coincide with the endemism centres of several groups of organisms in the Atlantic Forest, such as butterflies (Brown & Freitas, 2000), harvestmen (Pinto da Rocha & Silva, 2005), moths (Ferro & Melo, 2011) and termites (Cancello et al., 2014). CONCLUSIONS The environmental variables that most influence the distribution of epiphytic angiosperms across the Brazilian Atlantic Forest are temperature and rainfall, with a clear differentiation of the flora along a north south axis. However, when analysing the richest families separately, it becomes clear that not all groups respond in the same way to these variables. Floristic similarities for species of Bromeliaceae and Orchidaceae were more associated with space than with environmental conditions. Piperaceae follows the general pattern, although the distribution of this family is also significantly correlated with environment. Therefore, the role of space and environment on species composition varies according to distinct epiphytic species groups. SSF represents a subset of DEF and MEF more adapted to seasonality. RES is also more similar to areas geographically closer. Except for SSF, all other Brazilian Atlantic Forest vegetation types have indicator epiphytic angiosperm species. The epiphytic flora of MEF has the largest number of indicator species and indicator values. This flora is more adapted to low temperatures and temperature variation throughout the year. Well-preserved forest areas host larger epiphyte diversity, as shown by Barthlott et al. (2001). The long history of occupation of the Atlantic Forest has reduced forested areas (Ribeiro et al., 2009) and, consequently, epiphyte habitat (Pifano et al., 2007). Studies regarding community similarity help in our understanding of large-scale ecological processes and in improving landscape and regional planning, as pointed out by Zurita & Bellocq (2010). Combining information on diversity and endemism centres and similarity patterns for different biota elements of the Atlantic Forest will help manage its remnants and allow decision makers to manage it more appropriately. ACKNOWLEDGEMENTS We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico, Fundação de Amparo à Pesquisa do Estado da Bahia, Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro and Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior for fieldwork financial support and masters and doctoral scholarships (PL and JBBS, respectively). RCF and AMA are CNPq research fellows. We also thank Luis Menini Neto for providing initial floristic surveys database, Leandro Freitas for improving the initial project idea and Daniela Zappi for English revision. REFERENCES Abreu N, Menini Neto L, Konno TUP Orchidaceae das Serras Negra e do Funil, Rio Preto, Minas Gerais, e similaridade florística entre formações campestres e florestais do Brasil. Acta Botanica Brasílica 25: Agra MF, Barbosa MRV, Stevens WD Levantamento florístico preliminar do Pico do Jabre, Paraíba, Brasil. In: Porto KC, Cabral JJP, Tabarelli M, eds. Brejos de altitude em Pernambuco e Paraíba: história natural, ecologia e conservação. Brasília: Ministério do Meio Ambiente, Alves RJV, Kolbek J Summit vascular flora of the Serra de São José, Minas Gerais, Brasil. Check List 5: Amorim AMA, Fiaschi P, Jardim JG, Thomas WW, Clifton B, Carvalho AMV The vascular plants of a forest fragment in southern Bahia, Brazil. Sida 25: Amorim AMA, Jardim JG, Lopes MMM, Fiaschi P, Borges RAX, Perdiz RO, Thomas WW Angiosper-

12 598 P. LEITMAN ET AL. mas em remanescentes de floresta montana no sul da Bahia, Brasil. Biota Neotropica 9: Amorim AMA, Thomas WW, Carvalho AMV, Jardim JG Floristics of the Una Biological Reserve, Bahia, Brasil. Memoirs of the New York Botanical Garden 100: Araújo DSD Análise florística e fitogeográfica das restingas do Estado do Rio de Janeiro. Unpublished DPhil Thesis, Universidade Federal do Rio de Janeiro. Assis AM, Thomaz LD, Pereira OJ Florística de um trecho de floresta de restinga no município de Guarapari, Espírito Santo, Brasil. Acta Botanica Brasílica 18: Assis MA, Magalhães E, Prata B, Pedroni F, Sanchez M Florestas de restinga e de terras baixas na planície costeira do Sudeste do Brasil: vegetação e heterogeneidade ambiental. Biota Neotropica 11: Barbosa MRV Floristic composition of a remnant of Atlantic Coastal Forest in João Pessoa, Paraíba, Brasil. Memoirs of the New York Botanical Garden 100: Barros AAM Análise florística e estrutural do Parque Estadual da Serra da Tiririca, Niterói e Maricá, Rio de Janeiro, Brasil. Unpublished DPhil Thesis, Jardim Botânico do Rio de Janeiro. Barthlott W, Schmit-Neuerburg V, Nieder J, Engwald S Diversity and abundance of vascular epiphytes: a comparison of secondary vegetation and primary montane rain forest in the Venezuelan Andes. Plant Ecology 152: Benzing DH Vascular epiphytes. New York: Cambridge University Press. Bergamin RS, Müller S, Mello RSP Indicator species and floristic patterns in different forest formations in southern Atlantic rainforest of Brazil. Community Ecology 13: Bertoluci J, Brassaloti RA, Ribeiro Júnior JW, Vilela VMFN, Sawakuchi HO Species composition and similarities among anuran assemblages of forest sites in southeastern Brazil. Scientia Agricola 64: Biral L, Lombardi JA Flora vascular da Mata da Pavuna, Botucatu, SP, Brasil. Rodriguésia 63: Blum CT, Roderjan CV, Galvão F Composição florística e distribuição altitudinal de epífitas vasculares da floresta ombrófila densa na Serra da Prata, Morretes, Paraná, Brasil. Biota Neotropica 11: Bonnet A, Cunha CF, Curcio GR, Resende AS, Gonçalves FLA, Uhlmann A Epífitos vasculares e sua distribuição na paisagem. In: Prado RBP, Cardoso EC, Bonnet A, eds. Monitoramento da revegetação do Comperj: etapa inicial. Brasilia: Embrapa. Bonnet A, Curcio GR, Lavoranti OJ, Galvão F Flora epifítica vascular em três unidades vegetacionais do Rio Tibagi, Paraná, Brasil. Rodriguésia 62: Borgo M, Silva SM Epífitos vasculares em fragmentos de floresta ombrófila mista, Curitiba, Paraná, Brasil. Revista Brasileira de Botânica 26: Breier TB O epifitismo vascular em florestas do Sudeste do Brasil. Unpublished DPhil Thesis, Universidade Estadual de Campinas. Brown KS, Freitas AV Atlantic Forest butterflies: indicators for landscape conservation. Biotropica 32: Buzatto CR, Severo BMA, Waechter JL Composição florística e distribuição ecológica de epífitos vasculares na Floresta Nacional de Passo Fundo, Rio Grande do Sul. Iheringia (Série Botânica) 63: Caiafa A, Martins F Forms of rarity of tree species in the southern Brazilian Atlantic rainforest. Biodiversity and Conservation 19: Cancello EM, Silva RR, Vasconcellos A, Reis YT, Oliveira LM Latitudinal variation in termite species richness and abundance along the Brazilian Atlantic Forest hotspot. Biotropica 46: Cardoso DBOS, França F, Novais JS, Ferreira MHS, Santos RM, Carneiro VMS, Gonçalves JM Composição florística e análise fitogeográfica de uma floresta semidecídua na Bahia, Brasil. Rodriguésia 60: Coelho MM Composição florística e aspectos ecológicos em remanescentes de florestas montanas no eixo Almadina- Barro Preto, sul da Bahia, Brasil. MSc Thesis, Universidade Estadual de Feira de Santana. Costa A, Wendt T Bromeliaceae na região de Macaé de Cima, Nova Friburgo, Rio de Janeiro, Brasil. Rodriguésia 58: Dettke GA, Orfrini AC, Milaneze-Gutierre MA Composição florística e distribuição de epífitas vasculares em remanescente alterado de floresta estacional semidecidual no Paraná, Brasil. Rodriguésia 59: Dislich R, Mantovani W Flora de epífitas vasculares da Reserva da Cidade Universitária Armando de Salles Oliveira (São Paulo, Brasil). Boletim de Botânica da Universidade de São Paulo 17: Dufrêne M, Legendre P Species assemblages and indicator species: the need for flexible asymmetrical approach. Ecological Monographs 67: Ferraz EMN, Araújo EL, Silva SI Floristic similarities between lowland and montane areas of Atlantic Forest in Northeastern Brazil. Plant Ecology 174: Ferraz EMN, Rodal MJN Floristic characterization of a remnant of ombrophilous montane forest at São Vicente Férrer, Pernambuco, Brazil. Memoirs of the New York Botanical Garden 100: Ferro VG, Melo AS Diversity of tiger moths in a Neotropical hotspot: determinants of species composition and identification of biogeographic units. Journal of Insect Conservation 15: Fontoura T, Rocca MA, Schilling AC, Reinert F Epífitas da floresta seca da Reserva Ecológica Estadual de Jacarepiá, Sudeste do Brasil: relações com a comunidade arbórea. Rodriguésia 60: Fontoura T, Scudeller VV, Costa AF Floristics and environmental factors determining the geographic distribution of epiphytic bromeliads in the Brazilian Atlantic Rain Forest. Flora 9:

13 EPIPHYTE PATTERNS IN THE ATLANTIC FOREST 599 Fontoura T, Sylvestre LS, Vaz AMSF, Vieira CM Epífitas vasculares, hemiepífitas e hemiparasitas da Reserva Ecológica de Macaé de Cima. In: Lima HC, Guedes-Bruni RR, eds. Serra de Macaé de Cima: diversidade florística e conservação em Mata Atlântica. Rio de Janeiro: Jardim Botânico do Rio de Janeiro, Forzza RC, Pifano DS, Oliveira-Filho AT, Meireles LD, Faria PL, Salimena FR, Mynssen CM, Prado J Flora vascular da Reserva Biológica da Represa do Grama, Minas Gerais, e sua relação florística com outras florestas do sudeste brasileiro. Rodriguésia 65: Garcia RJF, Pirani JR Análise florística, ecológica e fitogeográfica do Núcleo Curucutu, Parque Estadual da Serra do Mar (São Paulo, SP), com ênfase nos campos junto à crista da Serra do Mar. Hoehnea 32: Gentry AH, Dodson CH Diversity and biogeography of Neotropical vascular epiphytes. Annals of the Missouri Botanical Garden 74: Geraldino CHL, Caxambú MG, Souza DC Composição florística e estrutura da comunidade de epífitas vasculares em uma área de ecótono em Campo Mourão, PR, Brasil. Acta Botanica Brasílica 24: Giongo C, Waechter JL Composição florística e estrutura comunitária de epífitos vasculares em uma floresta de galeria na Depressão Central do Rio Grande do Sul. Revista Brasileira de Botânica 27: Gonçalves CN, Waechter JL Aspectos florísticos e ecológicos de epífitos vasculares sobre figueiras isoladas no norte da planície costeira do Rio Grande do Sul. Acta Botanica Brasílica 17: Groppo M, Pirani JR Levantamento florístico das espécies de ervas, subarbustos, lianas e hemi-epífitas da mata da Reserva da Cidade Universitária Armando de Salles Oliveira, São Paulo, SP, Brasil. Boletim de Botânica da Universidade de São Paulo 23: Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: IBGE Mapa de biomas do Brasil, primeira aproximação. Rio de Janeiro: IBGE. Available at [accessed June 2015]. IBGE Manual técnico da vegetação brasileira, 2nd edn. Rio de Janeiro: Instituto Brasileiro de Geografia e Estatística IBGE. JABOT Jardim Botânico do Rio de Janeiro. Available at [accessed August 2012]. Kersten R, Kuniyoshi, YS Conservação das florestas na bacia do Alto Iguaçu, Paraná - avaliação da comunidade de epífitas vasculares em diferentes estágios serais. Floresta 39: Kersten R, Kuniyoshi YS, Roderjan CV Epífitas vasculares em duas formações ribeirinhas adjacentes na bacia do rio Iguaçu Terceiro Planalto Paranaense. Iheringia (Série Botânica) 64: Kersten R, Silva SM Composição florística e estrutura do componente epifítico vascular em floresta da planície litorânea na Ilha do Mel, Paraná, Brasil. Revista Brasileira de Botânica 24: Kersten RA Epífitas vasculares: histórico, particiação taxonômica e aspectos relevantes, com ênfase na Mata Atlântica. Hoehnea 37: Küper W, Kreft H, Nieder J, Köster N, Barthlott W Large-scale diversity patterns of vascular epiphytes in Neotropical montane rain forests. Journal of Biogeography 31: Laurenti-Santos AC Composição florística e estrutura da comunidade de epífitas vasculares associadas a trilhas no Parque Estadual das Fontes do Ipiranga, São Paulo, SP, Brasil. MSc Thesis, Instituto de Botânica da Secretaria de Estado do Meio Ambiente. Legendre P, Legendre L Numerical ecology, 2nd edn. Amsterdam: Elsevier. Leitão Filho HF Considerações sobre a florística de florestas tropicais e subtropicais do Brasil. IPEF 35: Leitman P, Amorim A, Menini Neto L, Forzza RC Epiphytic angiosperms in a mountain forest in southern Bahia, Brazil. Biota Neotropica 14: Leoni LS, Tinte VA Flora do Parque Estadual da Serra do Brigadeiro, estado de Minas Gerais, Brasil: caracterização da vegetação e lista preliminar das espécies. Carangola: Gráfica São José. Linsingen L, Sonehara JS, Uhlmann A, Cervi A Composição florística do Parque Estadual do Cerrado de Jaguariaíva, Paraná, Brasil. Acta Biológica Paranaensia 35: List of Species of the Brazilian Flora Rio de Janeiro Botanical Garden. Available at [accessed April 2013] Lombardi JA, Carvalho CS, Biral L, Saka MN Vascular flora of Serra do Japi Biological Reserve, Jundiaí, southeastern Brazil. Rodriguésia 63: Lomolino MV Elevation gradients of species-density: historical and prospective views. Global Ecology and Biogeography 10: Mamede MCH, Cordeiro I, Rossi L, Melo MMRF, Oliveira RJ Mata Atlântica. In: Marques OAV, Duleba W, eds. Estação ecológica Juréia-Itatins: ambiente físico, flora e fauna. Ribeirão Preto: Holos, Martins SE, Rossi L, Sampaio PSP, Magenta MAG Caracterização florística de comunidades vegetais de restinga em Bertioga, SP, Brasil. Acta Botanica Brasílica 22: Matos F, Amorim AM, Labiak P The ferns and lycophytes of a montane tropical forest in southern Bahia, Brazil. Journal of the Botanical Research Institute of Texas 4: Melo A, Amorim BS, García-González J, Souza JAN, Pessoa EM, Mendonça E, Chagas M, Alves-Araújo A, Alves M Updated floristic inventory of the angiosperm of the Usina São José, Igarassu, Pernambuco, Brazil. Revista Nordestina de Biologia 20: 3 26.

14 600 P. LEITMAN ET AL. Mendes K, Gomes P, Alves M Floristic inventory of a zone of ecological tension in the Atlantic Forest of northeastern Brazil. Rodriguésia 61: Menini Neto L, Forzza RC, Zappi D Angiosperm epiphytes as conservation indicators in forest fragments: a case study from southeastern Minas Gerais, Brazil. Biodiversity and Conservation 18: Mittermeier RA, Gil PR, Hoffmann M, Pilgrim J, Brooks T, Mittermeier CG, Lamoreux J, Fonseca GAB Hotspots revisited: earth s biologically richest and most endangered terrestrial ecoregions. Mexico City: CEMEX. Musskopf EL Composição florística e distribuição ecológica de epífitos vasculares no Parque Estadual de Itapuã, Viamão, Rio Grande do Sul. MsC Thesis, Universidade Federal do Rio Grande do Sul. Nascimento LM, Rodal MJN, Silva AG Florística de uma floresta estacional no Planalto da Borborema, nordeste do Brasil. Rodriguésia 63: Nekola J, White P The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26: Nettesheim F, Menezes L, Carvalho D, Conde M, Araujo D Influence of environmental variation on Atlantic Forest tree-shrub-layer phytogeography in southeast Brazil. Acta Botanica Brasílica 24: Nieder J, Prosperí J, Michaloud G Epiphytes and their contribution to canopy diversity. Plant Ecology 153: Oksanen J, Blanchet FG, Kindt R, Legendre P, O Hara RG, Simpson GL, Solymos P, Stevens MHH, Wagner H Vegan: community ecology package. R package version Available at package=vegan Oliveira-Filho AT, Budcke JC, Jarenkow JA, Eisenlohr PV, Neves DRM Delving into the variations in tree species composition and richness across South American subtropical Atlantic and pampean forests. Journal of Plant Ecology 6: Oliveira-Filho AT, Fontes MAL Patterns of floristic differentiation among Atlantic forests in southeastern Brazil and the influence of climate. Biotropica 32: Oliveira-Filho AT, Ratter JA A study of the origin of central Brazilian forests by the analysis of plant species distribution patterns. Edinburgh Journal of Botany 52: Oliveira-Filho AT, Tameirão-Neto E, Carvalho WAC, Werneck M, Brina AE, Vidal CV, Rezende SC, Pereira JAA Análise florística do compartimento arbóreo de áreas de Floresta Atlântica sensu lato na região das Bacias do Leste (Bahia, Minas Gerais, Espírito Santo e Rio de Janeiro). Rodriguésia 56: Pifano DS, Valente ASM, Castro RM, Pivari MOD, Salimena FRG, Oliveira Filho AT Similaridade entre os habitats da vegetação do Morro do Imperador, Juiz de Fora, Minas Gerais, com base na composição de sua flora fanerogâmica. Rodriguésia 58: Pillar VD How sharp are classifications? Ecology 80: Pillar VD, Duarte LDS A framework for metacommunity analysis of phylogenetic structure. Ecology Letters 13: Pinto da Rocha R, Silva MB Faunistic similarity and historic biogeography of the harvestmen of southern and southeastern Atlantic rain forest of Brazil. Journal of Arachnology 33: R Development Core Team R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142: Rizzini CT Tratado de fitogeografia do Brasil: aspectos ecológicos, sociológicos e florísticos. Rio de Janeiro: Âmbito Cultural Edições Ltda. Rodal MJN Montane forests in northeast Brazil: a phytogeographical approach. Botanische Jahrbücher für Systematik 124: Rodal MJN, Lucena MFA, Andrade KVSA, Melo AL Mata do Toró: uma floresta estacional semidecidual de terras baixas no nordeste do Brasil. Hoehnea 32: Rodal MJN, Nascimento LM Levantamento florístico da floresta serrana da Reserva Ecológica de Serra Negra, microrregião de Itaparica, Pernambuco, Brasil. Acta Botanica Brasílica 16: Rogalski JM, Zanin EM Composição florística de epífitos vasculares no estreito de Augusto César, floresta estacional decidual do Rio Uruguai, RS, Brasil. Revista Brasileira de Botânica 26: Salimena FRG, Matozinhos CN, Abreu NL, Ribeiro JHC, Souza FS, Menini Neto L Flora Fanerogâmica da Serra Negra, Minas Gerais, Brasil. Rodriguésia 64: Santos AMM, Cavalcanti DR, Silva JMC, Tabarelli M Biogeographical relationships among tropical forests in northeastern Brazil. Journal of Biogeography 34: Santos RM, Oliveira-Filho AT, Eisenlohr PV, Queiroz LP, Cardoso DBOS, Rodal MJN Identity and relationships of the Arboreal Caatinga among other floristic units of seasonally dry tropical forests (SDTFs) of northeastern and Central Brazil. Ecology and Evolution 2, doi: /ece3.91. Scarano FR Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic Rainforest. Annals of Botany 90: Scarano FR Plant communities at the periphery of the Atlantic rain forest: rare species bias and its risk for conservation. Biological Conservation 142: Splink SpeciesLink network. Available at [accessed August 2012].