Floristic composition of a Neotropical inselberg from Espírito Santo state , Brazil : an important area for conservation

Our study on granitic and gneissic rock outcrops on Pedra dos Pontões in Espírito Santo state contributes to the knowledge of the vascular flora of inselbergs in southeastern Brazil. We registered 211 species distributed among 51 families and 130 genera. Orchidaceae, Bromeliaceae and Polypodiaceae were the most representative families. Concerning vegetative habit, herbs were predominant and about the preference for substrates, holorupicolous species and epiphytes were most speciose. The richest rocky habitat type was woody thicket, with 122 exclusive species. In total, 27 of the species registered in our study are cited on official lists of endangered plant species from Espírito Santo state and Brazil. In addition, two new records of angiosperms for Espírito Santo flora and two new species were recorded for the area. Our data demonstrates the importance of the area for conservation of unique biodiversity that serves as a sanctuary for a rich rupicolous flora composed of endemic and endangered species, some of which are new to science.


INTRODUCTION
The rocky outcrops or inselbergs (from German, insel = island, berg = mountain) are landscape elements consisting mainly of granitic and gneissic rocks, which abruptly stand out amid a predominantly flat landscape (Bremer & Sander 2000).However, in floristic and ecological terms, inselberg refers to all granitic and gneissic rock outcrops, which are home to a specific, distinct type of vegetation different from that of the surroundings (Burke 2003; Barbará et al. 2009;Couto et al. 2016;Manhães et al. 2016).
Inselbergs form isolated ecosystems possessing strong environmental filters (e.g., total or partial absence of soil, low water retention, nutrient scarcity, difficulty in affixing roots, exposure to wind and heat) that allow these areas to support a highly specialized flora with sometimes high levels of diversity and endemism (Larson et al. 2000;Porembski & Barthlott 2000;Porembski 2007).Among the major regions recognized worldwide for this type of vegetation, southeastern Brazil stands out (Porembski 2007).In this context, the inselbergs situated in southern portion of Espírito Santo state are worth mentioning, recognized by Martinelli (2007) as a priority area for floristic studies and the creation of protected areas.This fact demonstrates the need for a greater effort for recording the biodiversity of these environments, as knowledge of this biota is essential for proposing actions for their management, use, restoration, and conservation.
Floristic inventories carried out on inselbergs in Espírito Santo are scarce.One study worth mentioning is Esgario et al. (2009) survey of inselbergs at Alto Misterioso, in mid-west region of Espírito Santo, where 172 species, including 10 new to science, were recorded.
Thus, the goal of this current study is to present for the first time a list of vascular plants that grow on rocky outcrops of Pedra dos Pontões, Mimoso do Sul, and to document occurrence of endemic and endangered species in order to reinforce the need for preservation of this priority area for conservation within Espírito Santo.

Study site
Pedra dos Pontões (20°56ʹ43ʺ S -20°56ʹ27ʺ S, 041°32ʹ21ʺ W -041°34ʹ05ʺ W, WGS84) is a montane inselberg (Couto et al. 2016) located in Mimoso do Sul municipality, in the southern portion of Espírito Santo (Figure 1).It is well known for its scenic beauty, standing out from the landscape where it can be seen for tens of kilometers, even though set in a mountainous region, typical of the region.
The site covers approximately 350 ha with an altitude gradient ranging from 700 to 1400 m (Couto et al. 2013).The vegetation cover consists of a mosaic of rock outcrops and forest vegetation in a transition area between seasonal semideciduous montane forest and dense rainforest (Couto et al. 2016).These native vegetation are inserted in an anthropogenic matrix mainly developed for agricultural activities on small, family-operated, rural farms, where the main activity is cultivation of mountain-grown coffee (Coffea arabica L.), interspersed with fruit-growing (banana), monoculture of eucalyptus and small areas intended for raising livestock (Couto et al. 2013).This is also an important area for recharging water to the Muqui do Sul River hydrographic micro-basin, a contributor to the Itabapoana basin, which supplies water to hundreds of rural properties in Mimoso do Sul municipality.
The climate of the region, according to Köppen classification, is type Cwb (subtropical, moderately humid), mesothermal humid, with rainy summers and dry winters, water deficit during the period from May to September (cold, dry season) and a precipitation surplus between December and March (hot, rainy season).The average annual rainfall (based on 30 years of historical data) is 1,375 mm with an average temperature of 21°C (Couto et al. 2016).
The inselbergs' vegetation is well preserved, with four major sectors being recognized (Figure 2): sector 1 -Garden of Pontões (Jardim dos Pontões): composed of more flat and undulating areas with the presence of some cavities (caves) and high inaccessible cliffs; sector 2 -Middle Pontão (Pontão Médio): in this sector a greater diversity of habitats can be found, from corrugated to fully vertical rock faces, where access is possible by difficult hikes or climbs with optional use of rock climbing equipment; sector 3 -Minor Pontão (Pontão Menor); and sector 4 -Higher Pontão (Pontão Maior): these two sectors are represented by large vertical cliffs over 300 m in height where access is only possible through the use of rock climbing techniques and equipment (Figure 2).The current study was conducted only in sectors 1 and 2, where access is easier and there is a larger area of exposed rocky outcrops.

Data collection
Collection of botanical specimens was conducted between 2004 and 2012.Fertile specimens were collected and subsequently herborized, according to the standard procedures used in floristic surveys (Mori et al. 1989).Vouchers  (2005) published by the Red List of Flora of ES (Simonelli & Fraga 2007).The exotic species included in the list were categorized according to Moro et al. (2012).Species were classified according to vegetative habit, as trees: woody plant with a single trunk, not branched from the base and which supports the canopy; shrubs: woody plant branched from the base, not forming a defined trunk, and usually with a height exceeding 2 m; subshrubs: low-growing shrub with a height less than to 2 m high; climbing plants: rooted plants without self-supporting capacity, relying on other plants or substrates for supporting them, and presenting different climbing mechanisms and herbaceous: nonlignified plants, which has aspect of herb or grass, opposes a woody vegetable, according to Font Quer (1977) and Gonçalves & Lorenzi (2007).
Species were categorized as having a preference for the following substrates: Holorupicolous (or "true rupicolous"): plants living directly on rocky surfaces or on a thin litholitic neosol layer existing over rock; Epiphytes: species living on existing vegetation, using haustorial structures; Hemiepiphytes: species that spend only one part in their life as epiphytes.Some species were observed occurring on more than one type of substrate (e.g., epiphytes or rupicolous vegetation) and in this case, plants were classified according to the preferred substrate, that is, the substrate over which species was more frequently found.
All species were organized according to their occupation in different rocky habitat types occurring at the site, without taking into account the microhabitats available on a smaller scale, as those observed by Porembski (2007).In this manner, rocky habitat types were classified into two major groups: islands of herbaceous vegetation (Iv; Figures 3  and 4) corresponding to groups of "bushy" plants formed by one or more vascular species distributed directly over a rocky surface, with shallow soil delimited by a rocky surface (Conceição et al. 2007); and woody thicket (Tw; Figure 5) corresponding to woody rupicolous communities with occurrence of arboreal and shrubby elements growing directly on the rocky surface, without forming stratification.
Specimens were identified by the authors using floral taxonomic monographs, comparing with previously identified specimens from MBML, RB, and VIC herbaria and through sending exsiccate to experts in each taxon.
Allocation of species to families followed guidelines set by the APG IV (2016) system for angiosperms, Smith et al. (2006) for ferns and Christenhusz et al. (2011) for lycophytes.Taxonomic names and vegetative habit, if not obtained at the time of collection, were updated according to supplementary materials in BFG (2015) for angiosperms and Prado et al. (2015) for ferns and lycophytes, and using the authors' abbreviations as suggested by Brummitt and Powell (1992) and the International Plant Names Index (2017).
The endangered species were cited according to the official list of endangered species of Brazilian Flora (MMA   represented by only a single species, and 33% by less than six species.Of these, the importance of Bromeliaceae, Velloziaceae, and Orchidaceae on the physiognomy of the area is worth mentioning, as holorupicolous species of these families establish dense single-species groupings on the inselberg (Figures 3 and 4).
The six richest families in this study (Orchidaceae, Bromeliaceae, Polypodiaceae, Araceae, Cactaceae and Piperaceae) represent 61.6% of the total number of species surveyed.The most speciose genera in this study were Peperomia (Piperaceae) with seven species, followed by Aechmea, Tillandsia (Bromeliaceae), Acianthera and Epidendrum (Orchidaceae) with six species each and Billbergia and Vriesea (Bromeliaceae) with five species each.
As for the distribution of species according to vegetative habit (Figure 16), there was a predominance of herbaceous species, with 164 species (78%), followed by subshrubs with 18 species (8%), shrubs with 12 species (5.6%), climbing plants and trees with eight species each (4% each).The occurrence of species according to their preferred substrate showed a higher prevalence of holorupicolous species with 129 species (61%), followed by epiphytes with 77 species (36%) and hemiepiphytes with five species (2%).
As for the rocky habitat types, greater richness was observed in woody thickets, with 122 exclusive species (58%) compared with the islands of herbaceous shrub vegetation, represented by 58 unique species.Of the total, 31 species occur in both habitats types.
In total, 27 species (13%) are included on official lists of endangered species (

DISCUSSION
Our study provides important contributions to the knowledge of the vascular flora of Pedra dos Pontões inselberg in Mimoso do Sul municipality and reinforces its importance as a priority area for conservation in the state of Espirito Santo.
Relevance of Orchidaceae, Bromeliaceae, Polypodiaceae, Cactaceae and Piperaceae families for species richness of the studied inselberg is mainly due to the important contribution of epiphytism in these families (Zotz 2013) that are mainly present in woody thickets.Of the most important families, only Bromeliaceae and Cactaceae are recognized as typical components of South American inselbergs, along with other smaller families represented in this study like Velloziaceae, Commelinaceae, Lentibulariaceae and Xyridaceae (Porembski 2007).
Presence of Orchidaceae as the richest family in this study is similar to observed for Serra do Brigadeiro, Minas Gerais state, in the high-montane inselbergs (campos de altitude) by Caiafa & Silva (2005).Esgario et al. (2009) also found a great richness of Orchidaceae for montane inselbergs in the midwest of ES.Orchidaceae family represents one of the principal floristic elements of inselbergs of northeastern Brazil, with high levels of endemism (Porembski et al.1998;França et al. 2006;Gomes & Alves 2010;Pessoa & Alves 2014).In both areas, the montane or cloud inselbergs, a favorable environmental factor, such as presence of continuous or intermittent clouds, responsible for horizontal precipitation, seems to be the main reason for this richness, as observed for other groups of xeric environments such as vascular epiphytes (Nieder et al. 2001).
Although they represent only a few species, typical genera of South American inselbergs were recorded in this study, like Alcantarea and Pitcairnia (Bromeliaceae), Coleocephalocereus (Cactaceae), Sinningia (Gesneriaceae) and Vellozia (Velloziaceae) (Porembski 2007), as shown in Table 1.The low representation of ferns found in the area follows a pattern of floral richness common to inselbergs world-wide (Porembski 2007).
The importance of herbs, especially monocots, to the floral composition of inselbergs is observed in other studies (Oliveira & Godoy 2007;Gomes & Sobral-Leite 2013).In this study, monocots were responsible for harboring 56% of species and 27% of families recorded for the area, indicating the importance of this group for the vegetation of inselberg, though very often neglected in restoration of areas mined for ornamental stones.
The high number of epiphytic species observed in the study area, though not common for inselbergs, is in agreement with Barthlott & Porembski (2000) observations for the tropics, where there is a strong affinity between epiphytic flora and the flora of rocky outcrops, with similar ecophysiological adaptations observed between rupicolous and epiphytic floras (e.g., stem and leaf succulence, velamen covering of aerial roots in some families, CAM metabolic pathways (crassulacean acid metabolism), presence of water and nutrient retention cisterns, thick cuticles, stomata specialized to prevent water loss, among others), mainly to cope with the xeric environment which  is very similar between the canopy and the rocky outcrops.Another important reason for epiphytes high number is presence of Pseudobombax sp.nov.tree.This phorophyte is an inselberg specialist and has been described as a nucleus of biodiversity on inselbergs in the southern portion of Espírito Santo (Couto et al. 2016).Together, this species and Guapira opposita (Vell.)Reitz (Nyctaginaceae) support a high richness of vascular epiphytes in the study area.
Extremely important is the presence of 27 endangered species, which 24 species are cited on the list of endangered flora of Espírito Santo (Simonelli & Fraga 2007) and 11 species are recognized by the Red List of Flora of Brazil (MMA 2014).
However, occurrence of Molasses Grass (Melinis minutiflora P. Beauv.), an invasive exotic species, has been documented in the area, with an alarming level of colonization in different sectors and environments, where competition with native species is severe, even with large species such as Alcantarea aff.patriae.The biological invasion process has been responsible for significant changes in the structure and composition of vegetation in diverse ecosystems around the world (D'Antonio & Vitousek 1992;McNeely et al. 2001).In particular, the African grass Melinis minutiflora is an extremely aggressive invasive, competing successfully with native flora, being found in many Brazilian protected areas, where it can disfigure the original phytophysiognomy in a few years (Martins et al. 2007(Martins et al. , 2011)).In addition, worth mentioning the large accumulation of biomass fuel, which aggravates vulnerability to fire, because it alters characteristics of the fire regime of invaded areas (D'Antonio & Vitousek 1992).The high number of endangered species occurring in the studied inselberg and presence of invasive species reinforces the need for conservation initiatives in the area.Endangered species are recognized as key priority indicators for the creation of protected areas worldwide (Brooks et al. 2006), being the most effective way to protect biodiversity (Mittermeier & Scarano 2013).
During field expeditions, two new species were recorded for the area: Pseudobombax sp.nov.(Malvaceae, Bombacoideae), which is being described by J.G. Carvalho-Sobrinho and D.R. Couto, and Bradea sp.nov.(Rubiaceae) which is being described by J.A.Oliveira.
Because of high diversity and endemism resulting from ecological peculiarities, disjunct distribution of matrix and low utility of these areas for agriculture, inselbergs are excellent sources of ecological, evolutionary, biogeographical and, in particular, comparative studies of floristic diversity.These ecosystems are important refuges for highly specialized flora, and these studies are of high scientific relevance for the proposal of measures and actions to conserve and restore these environments, keeping in mind that Espírito Santo is one of the largest exploiters of ornamental rocks in the world (Sardou Filho et al. 2013).Although located on privately owned lands, future actions should ensure the preservation of this important natural heritage, with its vegetation types and their associated biota already recognized as a priority for conservation in Espírito Santo.The state and municipal governments should encourage the creation of protected areas in the studied region, and these actions, along with environmental education programs and control of invasive exotic species, will ensure protection of the rich biodiversity found in this locality.

Figures 2- 5 .
Figures 2-5.Environments of the studied area in Pedra dos Pontões, Mimoso do Sul, Espírito Santo, Brazil.2. Inselberg Pedra dos Pontões, showing the observed sectors.3-4.Aspects of the islands of herbaceous habitat with the presence of important floristic elements in these environments such as Bromeliaceae, Orchidaceae and Velloziaceae.5. Woody thickets, demonstrating the abundant presence of woody elements and a rich vascular flora.Photos by D.R. Couto.

Table 2 )
, two are endemic species of the study area (Neoregelia dayvidiana Leme & A.P.Fontana and Pitcairnia abyssicola Leme & Kollmann) and Ditassa mucronata Mart.and Acalypha communis Müll.Arg., are new records for the flora of ES.