Orchids of the State Park of Serra do Tabuleiro, Southern Brazil

Lenzi, M., de Matos, J.Z., Fraga, A.M. & Crespo, M.B. 2015. Orchids of the State Park of Serra do Tabuleiro, Southern Brazil. Anales Jard. Bot. Madrid 72(2): e020. Orchidaceae show a high diversity of species in Brazil, especially in the Atlantic Forest Biome. Over the course of a 12-month study in the State Park of Serra do Tabuleiro in Southern Brazil, collections were made of orchids occurring in areas of restinga and riparian vegetation. A total of 92 orchid species were registered, belonging to three subfamilies and 51 genera. Octomeria was the best represented genus with ten species. Among all collections, two species are new records for Santa Catarina state, and 20 species is reported for the first time in the studied region. Regarding to conservation, 17 species (19%) are currently included with different threat labellings in any of the red lists of threatened plant species of Brazil. Among the total of orchids registered, 55 species (59%) are characteristic holoepiphytes, 47 species (51%) are restricted to the Atlantic Forest, 77 species (84%) occur in the riparian vegetation, and only nine species (10%) are restricted to restinga vegetation. The remarkable richness of orchids found in the present study highlights the importance for conservation the studied forest remnants. The historical of environmental degradation of the restinga vegetation can be negatively influencing the current floristic composition of the orchid community.


INTRODUCTION
Orchidaceae are usually considered to be one of the widest families of Angiosperms, with around 20000 species (Dressler, 1993). According to Barros & al. (2015), the family is well represented in Brazil with 238 genera and about 2553 species, 1636 of which are endemic to the country.
In the state of Santa Catarina, Southern Brazil, the family is still poorly known. In the most recent checklist of Orchidaceae published for that state, Klein & al. (1978) listed 295 species for the whole Florianópolis Island plus nine neighbouring municipalities.
The State Park of Serra do Tabuleiro covers an area of 87405 ha, which represents approximately 1% of the state of Santa Catarina, and is very close to Florianópolis Island. It reaches nine municipalities and several coastal islands. All these different areas comprise a great diversity of natural environments, ranging from coastal environments to inland habitats that represent five of the six phytogeographic regions found in the state. The park is still considered the southern boundary for many species with tropical distribution, thus constituting an important phytogeographic barrier (Klein, 1978;1980;. It comprises areas of Atlantic Forest (Mata Atlântica) formed by riparian and restinga vegetation.
The Atlantic Forest is considered as one of the richest biomes of the planet in biodiversity, and also one of the most severely threatened ecosystems; less than 10% of its original area remains well conserved (Galindo-Leal & Câmara, 2005). The state of Santa Catarina is totally included into this biome and at present possesses only 23.5% of its forest remnants in good estate of conservation (Fundação SOS Mata Atlântica, 2013). Studies with vascular species undertaken on plant communities growing close to water courses (riparian vegetation), although still scarce, show that they constitute very diverse ecosystems due to their high environmental heterogeneity (Kageyama & Gandara, 2000). According to Battilani & al. (2005), riparian vegetation is crucial to maintain the local ecosystem integrity and it plays an important role for conservation of high diversity sites.
Littoral plant communities, that constitute the restinga vegetation, occur on the coastal flats and possess a wide diversity of habitats (Klein, 1980;Scherer & al., 2005). Recent studies (Fraga & Peixoto, 2004, Rocha & Waechter, 2010 highlighted the species richness of orchids in this ecosystem. However, Falkenberg (1999) and Scherer & al. (2005) noted that the impact of human activities has caused strong degradation and fragmentation of the coastal environments, hampering the current understanding of patterns of both abundance and distribution of the local flora.
These factors together increase the threat on the orchid flora of the State Park of Serra do Tabuleiro and also in the state of Santa Catarina as a whole, and point out the importance to take urgent steps for the study and maintenance of biodiversity in these areas. An inventory of the orchids of the State Park of Serra do Tabuleiro may help to determine species subjected to some threat and to prepare future red lists of species of threatened flora for Santa Catarina and other regions of Brazil.
The objectives of the present study were: 1) to record the diversity of Orchidaceae in remnants of restinga and riparian vegetation in the Atlantic Forest, and 2) to update and depict the current geographic distribution of these species, threat category in red lists and their life forms, as the basic step for future studies on conservation of local biodiversity.

Study region
The State Park of Serra do Tabuleiro ( Fig. 1) is located in the central part of the coast of Santa Catarina state (Lat. 27°41′09″ S to 28°12′42″ S, Long. 48°49′20″ W to 48°25′08″ W), to SW of Florianópolis Island. The main orientation is on N-S direction and lesser in E-W direction, following the mountain ranges of Cambirela, Tabuleiro and Capivari. The altitude gradient ranges from the sea level in the coastal areas, up to over 1200 m in Serra do Tabuleiro (Klein, 1978;. The climate is characterized by mild and rainy summers, and humid and warm winters. The average annual rainfall is 1600 mm and the annual average temperature is 20.3°C (INMET, 2011).
The present study covered a total area of 34400 m 2 distributed along eight transects in eight sites (Appendix 1): two of them in restinga vegetation (20000 m 2 ), and six of them in riparian vegetation (14400 m 2 ). These transects were characterized according to their location, morphology and vegetation type, as indicated below: i) Site 1, and Site 2, (Fig. 1 & Appendix 1), both transects were located so as to avoid sites disturbed by fires that occurred in the region between 2001 and 2008, as surveyed by Pereira & al. (2009). Sampling was settled with 100 m side squares, distancing a maximum of 100 m of the beach line and totalling 20000 m 2 of area. The areas are covered by restinga vegetation, with herbaceous and woody layers. This vegetation occurs exclusively in coastal flats, which are geomorphological units constituted by marine sediments, along the Brazilian coast at altitudes varying from sea level up to 30 m towards inland the continent (Klein, 1980). According to Falkenberg (1999), the herbaceous and subshrub layers of restinga vegetation are constituted mainly by small plants that endure higher luminosity and stronger sea influence, therefore comprising plant communities closer to the sea. The shruby layer includes taller species (between 1 to 5 m in height).
ii) The other six transects ( Fig. 1 & Appendix 1) were located along both sides of several rivers and around small river islands. Site 3, and Site 8, each with an extension of 800 m and a total area of 3200 m 2 . Site 4, Site 5, Site 6, and Site 7, each with an extension of 500 m and a total area of 4000 m 2 . Morphologically, all these areas are formed by deep river valleys with an intense dissection, with very steep slopes and with a drainage network of waterfalls. The Atlantic Forest is represented on the slopes of the Serra do Tabuleiro, between 30 and 400 m altitude; forming part of a set of mountain plant communities with physiognomic variations, which is known as Floresta Ombróflia Densa and which constituting the largest part of forest diversity in the region (Klein, 1980). The riparian vegetation is a characteristic type of plant community found along the river courses, which vary according to ecological and biogeographic features of territories, their altitudes, and the dominant plant community of each site (Rodrigues & Gandolfi, 2001).

Plant survey
Field work was carried out between March and October 2010. Orchid specimens were collected from soil, rocks and phorophytes (up to 5 m in height) in restinga (herbaceous, subshrubby and shrubby layers), and in riparian vegetation. All samples were deposited in the herbaria ABH and FLOR (acronyms according to Thiers, 2015).
Geographic distributions of species were updated through the list of Klein & al. (1978) and Barros & al. (2015).
Species classification into the different categories follows the existing information from the official lists of threatened plant species for the states (Santa Catarina: Klein, 1990;Paraná: SEMA, 1995;Rio Grande do Sul: SEMA, 2014;São Paulo: SEMA, 2004;Espírito Santo: IPEMA, 2007) and the whole country ( Martinelli & Moraes, 2014). When categories of two or more lists were in conflict, the most recent (since updated) labelling was selected. Only those taxa identified to species rank were used to outline geographic distribution and threat categories.
The Ecological Category (EC) of each species was determined by direct visual observations in the field as being: (a) characteristic holoepiphyte (HLC), which occurs on phorophytes; (b) facultative holoepiphyte (HLF), based on the type of relationship with the type of substrate (phorophytes or rocks); (c) hemiepiphyte (HEM) (Benzing 1990); and (d) terrestrial (TER) (Dressler, 1981).  Thematic cartography was made with QGIS (for geographic information system and treatment of orbital images). The location of transects on the field was determined using a GPS.

Species richness
A total of 92 taxa of Orchidaceae were identified, which belong to 51 genera distributed in three subfamilies, 11 tribes and 13 subtribes (Table 1). Subfamily Epidendroideae was the most representative with 41 genera (80%), followed by Orchidioideae with seven genera (16%), Vanilloideae with two genera (4%) ( Table 1). Of the 92 recorded taxa, three were not identified at the species rank: Campylocentrum sp., Pelexia sp. and Vanilla sp. (probably an exemplar of V. dietschiana Edwall), as well as an adult plant of small size (±110 cm) that showed flower remnants insufficient for identification.
Octomeria was the best represented genus with 10 species, followed by Epidendrum with six especies; Bifrenaria and Stelis each with five species; Anathallis and Maxillaria each with four species; Gomesa, Pabstiella and Polystachya each with three species; Acianthera, Brasiliorchis, Campylocentrum, Christensonella, Dichaea, Dryadella, Phymathidium and Vanilla each with two species. The remaining 33 genera were represented by one species (Table 2).

Geographic distribution and conservation of endangered species
With regard to the geographic distribution in the states of Brazil, all the specimens recorded to species rank (n=89) occur in two or more states of the country ( Table 2). Some species (n=6; 7%) can be found in at least four phytogeographic domains, as is the case of E. secundum, L. nervosa, O. grandiflora, O. maculata, P. concreta and S. lanceolata. However, the Atlantic Forest (MA) has the largest number of exclusive species (n=47; 53%). Out of 89 taxa identified to species rank, 33 species (37%) are distributed through the state of Santa Catarina, but they do not reach the southern state of Rio Grande do Sul (Table 2).
Based on available checklists (Klein & al., 1978;Barros & al., 2015) and data from herbaria, of a total of 89 taxa identified to species rank, two species are recorded for the first time in the state of Santa Catarina, and 20 species are new for the municipalities of Palhoça and Santo Amaro da Imperatriz (Table 2), which are partially included within the limits of the State Park of Serra do Tabuleiro (Fig. 1).

DISCUSSION
The richness of orchid species found in the present study can be considered high when compared to other studies on Orchidaceae in different regions of Brazil. In the Southern region, Rocha & Waechter (2006) studied terrestrial orchids in the area of restinga vegetation and found 42 species distributed in 24 genera. In the same area, Buzatto & al. (2007) cited 50 species and 35 genera from an area of riparian vegetation. In the Southeast region, Fraga & Peixoto (2004) cited 73 species distributed in 41 genera, in the restinga vegetation; and Cunha & Forzza (2007) in an area covered by Atlantic Forest and restinga vegetations found 26 species in 18 genera. In other regions, Pansarin & Pansarin (2008) recorded 125 species in an area mesophytic-semideciduous forest, and Menini-Neto & al. (2009) cited 89 species in three areas of Atlantic Forest, montane forest and semi-deciduous forest at different altitudes.
For the state of Santa Catarina, no recent floristic surveys on Orchidaceae are available and those extant are outdated, a fact that makes further precise comparisons extremely difficult. Nonetheless, if the results are compared to that of Klein & al. (1978), it is noticeable that the species richness found here appears to be not very much representative. However, some relevant factors must be considered for a better understanding of the results. The studied area was limited to a few remnants of herbaceous and shrubby restinga vegetation still found in the region, and the sampling in riparian vegetation was restricted by up to five meters in height on the phorophytes. In fact, our study though performed in the same region covered a smaller area when compared to that of Klein & al. (1978), which was much wider in both geographic and ecologic terms. However, we report 20 new records for the same region of the study, demonstrating that there is still a great diversity. Undoubtedly, if the studied area were greater, including other types of vegetation, and also the canopy of the forest, the number of species recorded probably would be much greater. The State Park of Serra do Tabuleiro was created to preserve an area that had already undergone processes of environmental deface, generated by logging, agriculture and urbanizing activities. Certainly, when taken into account the study of Orchidaceae by Fraga & Peixoto (2004) and Rocha & Waechter (2006), made in areas of restinga vegetation in the state of Rio Grande do Sul, also in southern Brazil, the specific diversity found in our study is extremely low. The fragmentation and haphazard occupation of coastal areas are identified by those authors as negative factors for the conservation of restinga vegetation and for orchids themselves. According to Rocha & Waechter (2006), when performed in a short period of time studies on herbaceous terrestrial species in the restinga vegetation probably underestimate the total specific richness of Orchidaceae. This mainly occurs because of the difficulty to observe many species that often are represented by tiny and isolated individuals, with low frequency and/or without leaves during anthesis.
Orchids occur in up to two phytogeographic domains, although the great majority is found only in Atlantic Forest. It is believed that for species of Atlantic Forest there would be a continuum in their distributions in the N-S direction (Klein, 1980). However, this is not always the rule. Some species such as P. falcifolium, P. nummularia and S. parvifolia occur without gaps up to the state of São Paulo, and they only reappear in the state of Santa Catarina to the south. It is also possible that the lack of detailed studies on Orchidaceae in the states of Paraná and Santa Catarina make difficult a more accurate phytogeographic understanding of their distribution patterns. Furthermore, our results show that 37% of the studied species are found continuously from the northern states southwards to Santa Catarina, but they do not reach the state of Rio Grande do Sul (in the very South of Brazil). According to Klein (1978;1980), Serra do Tabuleiro is the most important phytogeographic barrier in southern Brazil impeding that many plants species can move in a north-south direction. In fact, Orchidaceae are among the leading families that are not able to cross this geographic boundary, so that one-third of the orchid species growing in the north, disappear in the southern part of that mountain range (Klein, 1980).
Although up to seventeen of the studied species are listed on any of the Brazilian regional red lists of endangered species list, only one of them is included in the most recent list of endangered species of the Brazilian flora, published by Ministério do Meio Ambiente (MMA, 2015). Nonetheless, at a local scale a number of those species (as well as others not included in the lists) can be in serious concern. It is therefore urgent to generate regional and local lists as an effective conservation tool for threatened species. Provided that many changes have occurred in the last 18 years that affected areas of natural vegetation through the whole country, it can be assumed that the threat degree for many species should also change. Galindo-Leal & Câmara (2005) suggested that the entire Biome of Atlantic Forest is seriously threatened. According to a survey of Fundação SOS Mata Atlântica  (Benzing 1990) and TER=terrestrial (Dressler 1981). Characteristic holoepiphyte (HLC) were not exclusive in restinga vegetation.
(2013), the deforestation rate in the state of Santa Catarina increased up to 7% between 2000 and 2005. Although a reduction in that rate was recorded between 2008 and 2010, deforestation continues to be a significant threat in the state. In relation to the forest remnants of 2008, currently 0.17% (3626 ha) of forests have already been lost, the restinga vegetation being the most seriously affected with 0.10% (75 ha) of its cover deforested (Fundação SOS Mata Atlântica, 2013).
The characteristic holoepiphyte was the most common ecologic category among the studied specimens and this agrees with other studies on Orchidaceae in Brazil (Barros, 2004;Fraga & Peixoto, 2004;Cunha & Forzza, 2007;Buzzato & al., 2007;Menini-Neto & al., 2009, Medeiros & Jardim, 2011. According to Benzing (1990), Orchidaceae are well known for their success in tree colonization, being orchids about two out of three epiphytes on every tree. However, many of them behave as facultative holoephiphytes, commonly also found growing on rocks on the banks of rivers and in small river islands, as demonstrated by the present study. Similarly, Falkenberg (2003) describes that the epiphytic habitats can easily be compared to the rocky habitats since both share a similar ecological situation, and in many cases epiphytic species can even grow best on rocks, if light conditions are satisfactory.
In terms of conservation, it is of paramount importance to preserve all diversity of vegetation types found in the State Park of Serra do Tabuleiro this would ensure the maintenance of different habitats suitable for colonization and perpetuation of orchid populations. Conservation figures such as 'plant micro-reserves' (cf. Laguna, 2001;Laguna & al., 2004) would be useful for that purpose, since they are small plots that require active management to maintain vegetation spots unchangeable along time, therefore avoiding community (and also species) successional replacement. This is especially relevant in the riparian vegetation, in which most species are found, including several threatened species. Indeed, the orchid community from the restinga vegetation shows lower diversity rates when compared to riparian vegetation. However, the history of environmental degradation endured by the studied coastal area of the State Park of Serra do Tabuleiro may be influencing negatively the current floristic composition of Orchidaceae in the restinga vegetation.