Vascular epiphytes in a remnant of seasonal semideciduous forest in zona da mata of Minas Gerais, Brazil = Epífitas vasculares em um remanescente de floresta estacional semidecidual na zona da mata de Minas Gerais, Brasil

This study was performed in a remnant of Seasonal Semideciduous Forest at Fazenda Fortaleza de Sant’Anna, in the municipality of Chácara, Minas Gerais, Brazil (22.0129S, 43.8628W), in an area of ca. 1 ha, via monthly expeditions throughout the year 2012. We found 91 species of vascular epiphytes, distributed in 44 genera and 12 families. The richest families were Orchidaceae (35 spp.), Bromeliaceae (18 spp.), Polypodiaceae (10 spp.), Piperaceae (nine spp.) and Araceae (seven spp.). Two species were recorded for the first time in Minas Gerais: Rodriguezia sticta and Stelis oligantha (Orchidaceae). Rhipsalis oblonga (Cactaceae) was recollected in the state after about 100 years without records. Four species are cited in the list of endangered plants in Minas Gerais: Nematanthus crassifolius (Gesneriaceae) and Cattleya bicolor (Orchidaceae) are in the category “Vulnerable” (VU), Nidularium azureum (Bromeliaceae) and Pleurothallis pectinata (Orchidaceae) are “Critically Endangered” (CR). Nidularium azureum is also cited as CR in the Red Book of Brazilian Flora. Most species were classified as characteristic holoepiphytes and anemochory was the most frequent dispersion syndrome.


INTRODUCTION
The Atlantic Forest is one of the world hotspots of biodiversity due to the large number of plants and animals, including many endemics (MYERS et al., 2000). About 11% of its original area exists today (RIBEIRO et al., 2009), where ca. 15,800 plant species occur, a high percentage of which are threatened with extinction (STEHMANN et al., 2009).
In Minas Gerais (MG), the original forest cover remained little altered until the beginning of the nineteenth century, when the coffee crop was responsible for a great impact on the natural landscape (VALVERDE, 1958). Menini Neto et al. (2009b) highlighted that the majority of existing vegetation remnants is composed of montane or high montane forests, "campos de altitude" and "campos rupestres", which are found only in areas of difficult access.
The few studies or non-existence of biological surveys in many regions of MG hinders the evaluation of these areas and consequently, the establishment of concrete actions to conserve biodiversity (DRUMMOND et al., 2009). Specific studies concerning the epiphytic flora are concentrated in the Southern Region of Brazil, with few for the Southeastern Region (KERSTEN, 2010) and even fewer in MG (WERNECK; ESPÍRITO-SANTO, 2002;ALVES et al., 2008;MENINI NETO et al., 2009a).
To contribute to the knowledge of epiphytic flora in Minas Gerais state and to reduce the current knowledge gaps in the Southeastern Region, the present study was conducted in a remnant of Seasonal Semideciduous Forest in Zona da Mata of MG, in the municipality of Chácara, part of the "Corredor Sudeste" in an area considered of "Very High" biological importance by Drummond et al. (2005).
The aims of the study were to survey the species of vascular epiphytes, indicate the ecological category and dispersal syndromes and discuss the importance of forest remnants in the conservation of epiphytic species in the Zona da Mata of Minas Gerais.

MATERIAL AND METHODS
The study was performed in a remnant of Seasonal Semideciduous Forest that lies in Fazenda Fortaleza de Sant'Anna (FFS) (22,0129S, 43,8628W), in the Zona da Mata, MG, between the municipalities of Chácara, Coronel Pacheco, Goianá and São João Nepomuceno, in a region locally known as Serra da Babilônia (Figure 1). The forest 624 Vascular epiphytes... BARBOSA,D. E. F. et al has several watercourses that integrate the basin of Rio Paraíba do Sul. The altitude is between 800 and 900 m.s.m. and the area that surrounds the forest is occupied by crops and pasture (PREA, 2012). The climate of region is CwB according to the Köppen classification, with dry and cold winters and wet and mild summers (CETEC, 1983).
Monthly collections were conducted during 2012 (with one pilot collection in July 2011), via the "método de caminhamento" (FILGUEIRAS et al., 1994), in the region belonging to the municipality of Chácara, located about 25 km from Juiz de Fora in an area of ca. 1 ha, in gallery forest of the Rio Cágado. The plants were photographed and a "Rapid Color Guide" was published by The Field Museum of Chicago (available at: http://fm2.fieldmuseum.org/plantguides/iter_guide.a sp?type=full&id=579&link=475%20Epiphytes%20 of%20Sant'Anna.pdf). The collected specimens were herborised according to usual methodology and deposited at the CESJ Herbarium of the Universidade Federal de Juiz de Fora (acronym according to THIERS, 2012). The species were identified by comparison with the collection of the CESJ Herbarium, consultation of specialised bibliography and via consultation of experts in each family. The spelling of species and author names were determined by The International Plants Names Index (www.ipni.org). Infraspecific categories were not considered. The ecological categories of recorded species were classified according to epiphyte-phorophyte relationships based on Benzing (1990).

RESULTS
Ninety one species of vascular epiphytes were recorded in Fazenda Fortaleza de Sant'Anna, belonging to 44 genera and 12 families (Table 1).
Rodriguezia sticta M.W.Chase and Stelis oligantha Barb. Rodr. were recorded for the first time in MG. The record of Nidularium azureum Leme (Bromeliaceae) must be highlighted, since it is an endemic species to the region and known only from a few collections from the type-locality (Coronel Pacheco, neighbouring municipality to Chácara), and Rhipsalis oblonga Loefgr. (Cactaceae), recollected after about 100 years without any collection in MG.
According to Carvalho-Silva and Guimarães (2008), Peperomia is predominant in Dense Ombrophilous Forests, and less frequent in Seasonal Forests, in which humidity levels are low, as confirmed by Menini Neto et al. (2009b), who found it to be the most representative genus of epiphytes in a Riverine Forest in the Zona da Mata of MG. However, Cervi and Borgo (2007) found Peperomia to be the most representative genus in a fragment of Seasonal Semideciduous Forest, similar to the results of this study. Surprisingly, Pleurothallis s.l. is the other genus notable for its richness in the Fazenda Fortaleza de Sant'Anna, since it is most speciose in cloud forests (Montane and High Montane Dense Ombrophilous Forests) of the Andes and in the Atlantic Forest (LUER, 1986). Thus, the large number of recorded species in the Fazenda Fortaleza de Sant'Anna is unexpected, suggesting an ombrophilous component in the studied area, probably due to the humidity provided by the Rio Cágado.
In general, the specific richness can be considered low in comparison with studies performed in the Dense Ombrophilous Forest, such as those of Breier (2005) (161 spp.), Petean (2009) (159 spp.) and Blum et al. (2011) (278 spp.), which is an expected result taking into account the climatic factors of this vegetation physiognomy, such as high temperature and humidity, as well as precipitation distributed evenly throughout the year, which favour the occurrence of epiphytic plants. Furthermore, the size of the area might be important in this comparison, since the studies of Breier (2005) and Blum et al. (2011) were performed in larger areas (10.24 and 6.3 ha, respectively), whereas only the area studied by Petean (2009) was 1 ha, as in the present study.
If compared with the same type of forest physiognomy (Seasonal Semideciduous Forest), the surveys conducted by Rogalski and Zanin (2003) (70 spp.), Giongo and Waechter (2004)  However, the richness of Fazenda Fortaleza de Sant'Anna is lower than that observed by Bianchi et al. (2012) (127 spp.) in an area of similar extent (1 ha), reinforcing the theory that ecotones demonstrate a high species richness (KERSTEN, 2010).
Four species are cited in the red list of plants threatened with extinction in MG (BIODIVERSITAS, 2007): Nematanthus crassifolius (Gesneriaceae) and Cattleya bicolor (Orchidaceae) in the category "Vulnerable" (VU); Nidularium azureum (Bromeliaceae) and Pleurothallis pectinata (Orchidaceae) as "Critically Endangered" (CR) (cited as Acianthera pectinata (Lindl.) Pridgeon & M.W.Chase). Prior to this record, P. pectinata was only collected twice in MG, according to Abreu et al. (2007), in the 1950s (in Ferros) and in 1969. Since then, there are no records of the species in MG, reinforcing its critical status of conservation. Nidularium azureum is also cited in the Red Book of Brazilian Flora as CR (Forzza et al. 2013), due to reduced area of occurrence and, until this record, only one known population in the municipality of Coronel Pacheco, neighbor to Chácara.
The records of Rodriguezia sticta and Stelis oligantha (Menini Neto et al., 2013), apart from the rediscovery of Rhipsalis oblonga, which has not been collected within the state in the past 100 years, represent an important contribution to the knowledge of MG flora. All three species are considered to be threatened with extinction in the state, due to their restricted distribution, with only a few specimens having been observed (especially the latter two species), and their occurrence in a locality without the protection of a conservation unit.
Rodriguezia sticta was previously known only from Espírito Santo and Rio de Janeiro states, in Seasonal Semideciduous Forest and Dense Ombrophilous Forest (BARROS et al., 2014). It is a Stelis oligantha is previously cited in São Paulo and Rio de Janeiro, occurring typically in Dense Ombrophilous Forest (BARROS et al., 2014). No record of this species was found on the site SpeciesLink (www.splink.org.br), suggesting that it is a rare species. However, its reduced size and difficult observation in the field, allied to a great number of unidentified or misidentified Stelis specimens in herbaria collections (L. MENINI NETO, pers. obs.) do not permit a more accurate conclusion.
Rhipsalis oblonga is found in eastern Brazil, occurring from southern Bahia to São Paulo in gallery forest or Dense Ombrophilous Forest and is absent from MG according to Zappi et al. (2014). However, on the SpeciesLink internet site, there are two specimens from MG in the herbarium of the Smithsonian Museum (US); one collected in 1915 and another without collection date, both lacking a specific locality. Therefore, we confirm the existence of this species in MG, but its rare occurrence must be emphasised, because only one specimen was found in Fazenda Fortaleza de Sant'Anna.
A high biodiversity occurs in the Atlantic Forest, despite the intensive fragmentation of its vegetation, and actions to conserve those remnants are essential. Thus, to provide subsidies to implement these actions it is necessary to perform floristic surveys in this phytogeographic domain, which currently are scarce regarding epiphytic plants, especially in MG, where there are few published studies that address the subject and the epiphytic flora is mostly unknown.
This study shows that a small area of this forest remnant shows a higher specific richness than expected for a Semideciduous Forest in a region with a strong anthropogenic intervention (crops and pasture), increasing the knowledge of the MG flora with two new records (R. sticta and S. oligantha) and the rediscovery of a species that was not collected within the last 100 years (R. oblonga), as well as the collection of N. azureum, previously known only from the type-locality.
The existence in the FFS of species threatened with extinction in MG as well as globally (with the presence of the microendemic species, N. azureum) highlights the importance of the maintenance of forest remnants in the Zona da Mata of MG and the relevance of surveys in areas not protected by conservation units.